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McMillan 2007. Fish - Histology PDF
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Fish Histology
Fish Histology
Female Reproductive Systems
Donald B. McMillan
Department of Biology
The University of Western Ontario
London, Ontario
Canada
A C.I.P. Catalogue record for this book is available from the Library of Congress.
ISBN 978-1-4020-5415-0 (HB)
ISBN 978-1-4020-5715-1 (e-book)
Published by Springer,
P.O. Box 17, 3300 AA Dordrecht, The Netherlands.
www.springer.com
Printed on acid-free paper
All Rights Reserved
2007 Springer
No part of this work may be reproduced, stored in a retrieval system, or transmitted
in any form or by any means, electronic, mechanical, photocopying, microfilming, recording
or otherwise, without written permission from the Publisher, with the exception
of any material supplied specifically for the purpose of being entered
and executed on a computer system, for exclusive use by the purchaser of the work.
&/2 ,/.%
4!",% /& #/.4%.43
02%&!#% IX
&%-!,% '%.)4!, 3934%-3 /& &)3(
)NTRODUCTION
/RIGIN OF THE 'ENITAL 3YSTEMS
!NATOMY OF THE &EMALE 'ENITAL 3YSTEM
/VARY
/6!2)!. &/,,)#,%3
)NTRODUCTION
3TAGES OF /OCYTE $EVELOPMENT
0RIMARY 'ROWTH
#HROMATIN
NUCLEOLUS STAGE
0ERINUCLEOLUS PHASE
#ORTICAL !LVEOLUS 3TAGE
6ITELLOGENESIS
-ATURATION
4HE /OCYTE %NVELOPES
0RIMARY %NVELOPE
3ECONDARY %NVELOPES
&OLLICULAR %PITHELIUM
4HECA AND THE /VARIAN 3TROMA
/65,!4)/.
)NTRODUCTION
!TRETIC &OLLICLES 0OSTOVULATORY &OLLICLES AND #ORPORA ,UTEA
!TRETIC &OLLICLES
0OSTOVULATORY &OLLICLES
&OLLICULAR 3TEROIDOGENESIS
#HORION
-ICROPYLE
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
)NTRODUCTION
/OLEMMA AND THE #ORTICAL /OPLASM
#ORTICAL !LVEOLI
&ERTILIZATION
#ORTICAL 2EACTION
&ATE OF !LVEOLAR -EMBRANE
0ERIVITELLINE 3PACE
&ORMATION OF THE #HORION
"LOCK TO 0OLYSPERMY
VII
VIII
4ABLE OF #ONTENTS
/6)$5#43 !.$ /6)0!2)49
/VIDUCTS
/VIDUCTAL 'LAND AND %GG #APSULE
5TERUS IN %LASMOBRANCHS
6)6)0!2)49
)NTRODUCTION
6IVIPARITY IN %LASMOBRANCHS
!PLACENTAL 6IVIPARITY IN %LASMOBRANCHS
9OLK SAC 0LACENTA OF %LASMOBRANCHS
6IVIPARITY IN #OELACANTHS
6IVIPARITY IN 4ELEOSTS
&OLLICULAR 'ESTATION
,UMINAL 'ESTATION
/VARIAN ,UMINAL %PITHELIUM
%MBRYOTROPH
%MBRYONIC !BSORPTIVE %PITHELIA 4ROPHOTAENIAE
/THER %MBRYONIC !BSORPTIVE 3TRUCTURES
2%&%2%.#%3
).$%8
02%&!#%
/VER THE PAST YEARS OR SO THE TECHNIQUES OF MICROSCOPY HAVE ATTAINED A HIGH DEGREE OF EXCELLENCE RESULTING IN
THE ACCUMULATION OF MASSES OF INFORMATION ON THE HISTOLOGY OF lSHES 4HIS GOLDEN AGE OF DESCRIPTIVE MORPHOLOGY
HOWEVER IS DRAWING TO A CLOSE AND THE TIME IS RIPE TO DRAW THIS MATERIAL TOGETHER IN A FORM THAT CAN BE USED BY
RESEARCHERS WHO ARE STUDYING THE DIVERSE ASPECTS OF THE WORLDS DWINDLING STOCKS OF lSH &OR SEVERAL YEARS ) HAVE
BEEN ACCUMULATING MATERIAL ON lSH HISTOLOGY AND MORE RECENTLY HAVE BEEN COMPILING A TEXTBOOK ON THE FEMALE
REPRODUCTIVE SYSTEMS -Y AMBITION HAS BEEN TO PARALLEL THE EXCELLENT TEXTS AVAILABLE ON MAMMALIAN HISTOLOGY
AND EVENTUALLY PRODUCE SIMILAR VOLUMES ON OTHER SYSTEMS !S hlSHv ) HAVE INCLUDED !GNATHA #HONDRICHTHYES
AND /STEICHTHYES .OMENCLATURE USED FOLLOWS THAT OF THE AUTHORS BEING CITED IN OTHER CASES ) HAVE USED &ISHES OF
THE 7ORLD ND ED BY *3 .ELSON PUBLISHED BY *OHN 7ILEY 3ONS
!LTHOUGH HISTOLOGY DEALS IN VISUAL IMAGES ONE OF THE PROBLEMS THAT HAS BESET THIS DISCIPLINE IN THE PAST HAS BEEN
THE HIGH COST AND DIFlCULTY OF PUBLISHING MICROGRAPHS 4HE ADVENT OF DIGITAL TECHNOLOGY AND THE STORAGE OF IMAGES
ON COMPACT DISCS #$S HOWEVER HAS SOLVED THIS PROBLEM AND ) HAVE RESCUED MANY CLASSIC AND BEAUTIFUL IMAGES
FROM THE DUST AND OBSCURITY OF LIBRARY STACKS MAKING THEM ONCE AGAIN READILY AVAILABLE TO THE PRESENT
DAY SCIEN
TIST ) HAVE EMBRACED THIS TECHNOLOGY WITH ABANDON AND LARGE NUMBERS OF ILLUSTRATIONS ARE INCLUDED WITH THIS WORK
)T SHOULD BE NOTED THAT MAGNIlCATIONS GIVEN IN THE LEGENDS ARE TAKEN FROM THE ORIGINAL SOURCES THE ACTUAL VALUES
WILL VARY DEPENDING ON THE COMPUTER BEING USED
$R 7*2 ,ANZING FORMERLY OF THE 3CHOOL OF "IOLOGICAL 3CIENCES OF THE 5NIVERSITY OF 3YDNEY !USTRALIA
PROVIDED SUGGESTIONS AND ENCOURAGEMENT AT THE OUTSET OF THE PROJECT ) ACKNOWLEDGE WITH GRATITUDE THE PATIENT
ASSISTANCE OF MY COLLEAGUES AT THE 5NIVERSITY OF 7ESTERN /NTARIO ESPECIALLY THE $EAN OF 3CIENCE $R &* ,ONG
STAFFE AND THE #HAIR OF THE $EPARTMENT OF "IOLOGY $R -" &ENTON WHO MADE EXCELLENT FACILITIES AVAILABLE FOR MY
RESEARCH -ESSRS 2* (ARRIS AND )# #RAIG PROVIDED PATIENT AND GENEROUS TECHNICAL ASSISTANCE ) AM GRATEFUL TO
THE OBLIGING STAFF OF THE 4AYLOR 3CIENCE ,IBRARY AT THE 5NIVERSITY OF 7ESTERN /NTARIO FOR THEIR CHEERFUL ATTENTION TO
MY NEEDS 4HANKS ARE OWED TO THE MANY AUTHORS AND PUBLISHERS WHO READILY GAVE PERMISSION TO COPY THEIR MATERIAL
SPECIlC ACKNOWLEDGEMENTS ARE INCLUDED WITH THE LEGENDS
IX
#(!04%2
&%-!,% '%.)4!, 3934%-3 /& &)3(
THIS MERELY ENSURES THAT SPERMATOZOA ARE SHED NEAR THE
EGGS BUT MORE OFTEN IT INVOLVES INSEMINATION OF THE
FEMALES )NTERNAL FERTILIZATION MAY BE FOLLOWED IMME
DIATELY BY THE LAYING OF NEWLY FERTILIZED EGGS OR SOME
TIME LATER BY THE RELEASE OF EMBRYOS AT VARIOUS STAGES
OF DEVELOPMENT
6IVIPARITY IS HIGHLY SPECIALIZED IN SOME GROUPS OF
ELASMOBRANCHS AND TELEOSTS AND THE DEVELOPING YOUNG
MAY BE HOUSED WITHIN THE OVARY OR IN THE GENITAL DUCTS
6IVIPAROUS SPECIES OF ELASMOBRANCHS RANGE FROM INTER
NAL INCUBATORS THAT SIMPLY RETAIN LARGE YOLKED EGGS TO
OTHER SPECIES IN WHICH THE COMPLEXITY OF PLACENTATION
AND EGG YOLK RETENTION APPROACHES THE EUTHERIAN CON
DITION #ALLARD ET AL 4HE CARTILAGINOUS lSHES
ARE OF PARTICULAR INTEREST TO REPRODUCTIVE BIOLOGISTS BE
CAUSE OF THEIR STRUCTURAL AND FUNCTIONAL SIMILARITIES IN
PATTERNS OF REPRODUCTION AND DEVELOPMENT WITH THOSE
OF AMNIOTES 7OURMS )N THESE HIGHLY ADVANCED
ANIMALS SEVERAL PROCESSES EITHER MADE THEIR APPEAR
ANCE FOR THE lRST TIME AMONG VERTEBRATES OR BECAME
WELL ESTABLISHED INTERNAL FERTILIZATION VIVIPARITY PLA
CENTAL MECHANISMS FOR FOETAL MAINTENANCE PATTERNS OF
GENITAL TRACT DEVELOPMENT AND SEX DIFFERENTIATION AND
THE VERTEBRATE TYPE OF REPRODUCTIVE ENDOCRINOLOGY
!LTHOUGH MOST lSH ARE DIOECIOUS OR GONOCHORISTIC
(%2-!0(2/$)4)3- DOES OCCUR WHERE OVARIAN AND TESTIC
ULAR TISSUES APPEAR IN THE SAME INDIVIDUAL !TZ
'REENWOOD #HAN AND 9EUNG 'RANDI
AND #OLOMBO )T IS FOUND ESPECIALLY AMONG
CYCLOSTOMES AND TELEOSTS AND IN SOME SPECIES IS THE
NORMAL WAY OF LIFE -ALE AND FEMALE SEX CELLS RIPEN
AT THE SAME TIME IN 39.#(2/./53 (%2-!0(2/$)4%3 )N
#/.3%#54)6% (%2-!0(2/$)4%3 HOWEVER THERE IS SEX RE
VERSAL 02/4/'9./53 (%2-!0(2/$)4%3 FUNCTION lRST AS
FEMALES THEN AS MALES WHILE 02/4!.$2/53 (%2-!0(2/
$)4%3 TRANSFORM FROM MALES INTO FEMALES
2EPRODUCTION IN MOST lSHES IS CYCLIC ALTHOUGH THE
LENGTH OF THE CYCLE IS EXTREMELY VARIABLE SEE REVIEWS
BY 'REENWOOD 7OURMS "ILLARD AND
"RETON $ODD AND 3UMPTER (AMLETT AND
)NTRODUCTION
4HERE IS AN AMAZING VARIATION IN METHODS OF REPRODUC
TION IN lSHES 3OME SPECIES AT LARGE OUTLAYS OF EN
ERGY RELEASE ENORMOUS NUMBERS OF MODERATELY YOLKY
MESOLECITHAL EGGS THAT ARE SUBJECTED TO SUBSEQUENT
PARENTAL NEGLECT ! SINGLE OCEAN SUNlSH -OLA MOLA
FOR EXAMPLE BY A PRODIGIOUS FEAT OF PRODUCTIVITY IS
SAID TO SPAWN OVER EGGS .ELSON
/THER lSH MAY PRODUCE RELATIVELY SMALL NUMBERS OF
MUCH YOLKIER TELOLECITHAL EGGS OFTEN IMPROVING THEIR
CHANCES OF SURVIVAL BY PROVIDING PARENTAL SUPPORT
%LABORATE NEST
BUILDING ACTIVITIES MAY PRECEDE SEXUAL
BEHAVIOUR AND PARENTAL CARE MAY CONTINUE FOR SOME
TIME AFTER HATCHING 4HE YOUNG MAY BE SHELTERED FOR
VARYING PERIODS WITHIN THE BODY OF THE FEMALE AND
EVEN THE MALE 3OME VIVIPAROUS TELEOSTS PRODUCE ONLY
ONE TO FOUR WELL
DEVELOPED YOUNG AT A TIME 4HIBAULT
AND 3CHULTZ !N AMAZING ARRAY OF STRUCTURAL AD
APTATIONS HAS EVOLVED FOR THE PROTECTION AND NOURISH
MENT OF THESE DEVELOPING YOUNG
! REMARKABLE REPRODUCTIVE STRATEGY IS SEEN IN BIT
TERLINGS #YPRINIDAE !CHEILOGNATHINAE WHERE PAR
ENTS TRANSFER RESPONSIBILITY FOR THE CARE OF THEIR YOUNG
TO A FRESHWATER UNIONID MUSSEL !LDRIDGE
4HE FEMALE BITTERLING EXTENDS HER LONG OVIPOSITOR INTO
THE MANTLE CAVITY OF THE MUSSEL AND DEPOSITS HER EGGS
BETWEEN THE GILL lLAMENTS 4HE MALE THEN EJECTS HIS
SPERM INTO THE MUSSELS INHALENT WATER CURRENT AND
FERTILIZATION TAKES PLACE WITHIN THE GILLS OF THE HOST
%ARLY DEVELOPMENTAL STAGES ARE PROTECTED FROM THE
RISK OF PREDATION WITHIN THE BODY OF THE MUSSEL SUB
SEQUENTLY THE LARVAE SWIM AWAY FROM THE HOST TO CON
TINUE LIFE ON THEIR OWN
!LTHOUGH EXTERNAL FERTILIZATION IS USUAL AMONG lSH
ES COPULATION MAY OCCUR IN SOME SPECIES 3OMETIMES
$ETAILED IN AN EXHAUSTIVE CHART SEE "REDER AND 2OSEN
0RODUCING LIVING YOUNG INSTEAD OF EGGS
#(!04%2
+OOB 3OME LIKE THE LAMPREYS AND CERTAIN SAL
MONID AND EEL SPECIES SPAWN ONLY ONCE AND THEN DIE
OTHERS MAY BREED EVERY TWO OR THREE YEARS BUT MOST
BREED ONCE OR SEVERAL TIMES A YEAR 3OME HAGlSHES
SOME TELEOSTS AND SOME SPECIES OF OVIPAROUS SKATES
APPEAR TO BREED THROUGHOUT THE YEAR
4HE APPEARANCE OF THE OVARY OF CYCLICAL BREEDERS
VARIES GREATLY AT DIFFERENT TIMES OF THE CYCLE AND THREE
OVARIAN TYPES HAVE BEEN RECOGNIZED ON THE BASIS OF
THE PATTERN OF OOCYTE DEVELOPMENT 7ALLACE AND 3EL
MAN .AGAHAMA &ISH THAT SPAWN ONCE
AND THEN DIE AS LAMPREYS ANADROMOUS SALMON SPE
CIES /NCORHYNCHUS SPP OR CATADROMOUS EELS !N
GUILLA SPP HAVE 39.#(2/./53 /6!2)%3 IN WHICH ALL
OOCYTES ARE AT THE SAME STAGE OF DEVELOPMENT 3PE
CIES THAT GENERALLY SPAWN ONCE PER YEAR DURING A SHORT
BREEDING SEASON DISPLAY '2/50 39.#(2/./53 /6!2)%3
WITH AT LEAST TWO POPULATIONS OF OOCYTES AT DIFFERENT
DEVELOPMENTAL STAGES THIS IS THE COMMONEST SITUATION
IN TELEOSTS /VULATION OF GROUP SYNCHRONOUS OVARIES
MAY OCCUR AT INTERVALS OVER THE BREEDING SEASON SO THAT
THE OOCYTES ARE RELEASED IN hBATCHESv 4HE YELLOWTAIL
mOUNDER 0LEURONECTES FERRUGINEUS OF THE CONTINENTAL
SHELF OF THE WESTERN .ORTH !TLANTIC IS SUCH A "!4#(
30!7.%2 -ANNING AND #RIM !N !39.#(2/./53
/6!29 CONTAINS OOCYTES AT ALL STAGES OF DEVELOPMENT
AND OCCURS IN SPECIES THAT SPAWN MANY TIMES DURING A
LONG BREEDING SEASON EG MEDAKA /RYZIAS SPP KIL
LIlSH &UNDULUS HETEROCLITUS AND GOLDlSH #ARASSIUS
AURATUS
-ANY lSH IN BOTH TEMPERATE AND TROPICAL REGIONS
EXHIBIT AN ANNUAL RHYTHM OF REPRODUCTION THAT IS
CORRELATED WITH PHOTOPERIOD AND TEMPERATURE VARIA
TIONS IN THE TROPICS THE INCREASED PRODUCTIVITY OF THE
RAINY SEASON IS ALSO AN INmUENCE "ILLARD AND "RETON
4HE BREEDING SEASONS OF MARINE TELEOSTS OF THE
NORTHERN HEMISPHERE ARE CHARACTERISTICALLY SHORTER IN
NORTHERN TO MONTHS THAN IN SOUTHERN FORMS TO
MONTHS 1ASIM /OCYTES IN THE NORTHERN SPE
CIES DEVELOP SYNCHRONOUSLY AND ARE PROBABLY RELEASED
IN A SINGLE SPAWNING THERE IS A WIDE RANGE IN SIZES OF
MATURING OOCYTES IN ASYNCHRONOUS OVARIES OF SOUTHERN
SPECIES INDICATING THAT SEVERAL SPAWNINGS OCCUR IN A
SINGLE SEASON 4HE APPEARANCE OF CONTINUOUS BREED
ING HOWEVER MAY BE DECEPTIVE IN THAT INDIVIDUALS OR
POPULATIONS MAY EXHIBIT SYNCHRONIZED ANNUAL REPRO
DUCTIVE CYCLES THAT ARE SIMPLY OUT OF PHASE WITH ONE
ANOTHER 3COTT
/RIGIN OF THE 'ENITAL 3YSTEMS
/VARIES AND TESTES DEVELOP FROM PAIRED MASSES OF
MESODERMAL TISSUE ON EITHER SIDE OF THE DORSAL MESEN
TERY IN THE DORSOLATERAL LINING OF THE PERITONEAL CAVITY
&IGURE 4HESE INDIFFERENT '%.)4!, 2)$'%3 BULGE
INTO THE DEVELOPING COELOM AND ARE LATER INVADED BY
02)-/2$)!, '%2- #%,,3 THAT WILL EVENTUALLY GIVE RISE
TO OOGONIA OR SPERMATOGONIA .IEUWKOOP AND 3UTAS
URYA .AKAMURA ET AL #OVERING THE SUR
FACE OF THE OVARY IS THE SO CALLED '%2-).!, %0)4(%,)5-
WHICH IS CONTINUOUS WITH THE PERITONEUM LINING THE
COELOM &IGURE $URING EMBRYONIC DEVELOPMENT
THE GERMINAL EPITHELIUM IS THE PROLIFERATIVE LAYER THAT
GIVES RISE TO MUCH OF THE SOMATIC TISSUE OF THE RUDI
MENTARY GONAD )N THE COMMON SNOOK #ENTROPOMUS
UNDECIMALIS OOGONIA ARE DISTRIBUTED AMONG THE STRATI
lED SQUAMOUS CELLS OF THIS EPITHELIUM THEY PROLIFER
ATE BY MITOSIS AND SINK INTO THE STROMA OF THE OVARY
WHERE FURTHER DEVELOPMENT TAKES PLACE &IGURE
'RIER 0RESUMABLY THE GERM CELLS HAVE INVAD
ED THE EPITHELIUM FROM AN EXTERNAL SOURCE 3INCE IT IS
NOT KNOWN AT THIS TIME WHETHER THIS EPITHELIUM IS THE
SOURCE OF GERM CELLS IN ALL lSH SOME AUTHORS CONSIDER
IT MISLEADING TO REFER TO IT AS A hGERMINAL EPITHELIUMv
PREFERRING THE TERM h'/.!$!, %0)4(%,)5-v FOR THIS PRO
LIFERATIVE LAYER .IEUWKOOP AND 3UTASURYA
)N MOST VERTEBRATES THE SOMATIC TISSUE OF EACH
GONAD HAS A DOUBLE ORIGIN DEVELOPING FROM TWO DIS
TINCT BUT CLOSELY ASSOCIATED MESENCHYMAL SOURCES THE
#/24%8 IS DERIVED FROM PROLIFERATION OF THE COELOMIC
EPITHELIUM AND IS DESTINED TO BECOME AN OVARY THE
-%$5,,! COMES FROM A MORE MEDIAL CELLULAR PROLIF
ERATION AND PRODUCES THE TESTIS 7OURMS 7OLFF
5SUALLY ONE OF THESE PORTIONS GROWS RAPIDLY
WHILE THE OTHER FAILS TO DEVELOP AND THE SEX OF THE IN
DIVIDUAL IS DETERMINED EARLY 4HIS PATTERN OF GONADAL
DIFFERENTIATION FROM TWO COMPONENTS IS CHARACTERISTIC
OF ELASMOBRANCHS AND ALL TETRAPODS #HIEFl
)N CONTRAST BOTH MALE AND FEMALE GONADS OF CYCLO
STOMES AND TELEOSTS DEVELOP DIRECTLY FROM COELOMIC
EPITHELIUM THAT CORRESPONDS TO THE CORTEX OF OTHER
VERTEBRATES 7OLFF AND THERE APPEARS TO BE
NO CONTRIBUTION FROM MEDULLARY TISSUE $ODD AND
3UMPTER )T HAS BEEN SUGGESTED THAT THESE DIF
FERENCES MAY ACCOUNT FOR THE WIDESPREAD OCCURRENCE
4HE PHENOMENON OF SEXUAL DIFFERENTIATION HAS BEEN DISCUSSED AT
LENGTH BY ,EPORI
&%-!,% '%.)4!, 3934%-3 /& &)3(
OF INTERSEXUALITY AMONG CYCLOSTOMES AND TELEOSTS
(OAR
0RIMORDIAL GERM CELLS ARISE EARLY IN DEVELOPMENT
WITHIN EMBRYONIC ENDODERM OR MESODERM LONG BE
FORE THE RUDIMENTS OF THE GONADS ARE FORMED AND AT
A DISTANCE FROM THE SITE THEY WILL EVENTUALLY OCCUPY
&IGURE L 4HEIR SITE OF ORIGIN IS EXTRAGONADAL AND
IN SOME lSHES MAY BE EXTRAEMBRYONIC 4HEY MIGRATE
INTO THE RUDIMENTARY GONAD AND ESTABLISH RESIDENCE IN
THE OUTER MARGIN OF THE STROMA JUST BENEATH THE GONAD
AL EPITHELIUM &IGURE 7OURMS .IEUWKOOP
AND 3UTASURYA (AMAGUCHI 4IMMERMANS
AND 4AVERNE 'EVERS ET AL VAN 7INKOOP
ET AL 'RANDI AND #OLOMBO ,ATER THEY
WILL BE ENSHEATHED BY CELLS DERIVED FROM THE GONADAL
EPITHELIUM &IGURE )N CONTRAST TO OTHER SPECIES
WHERE PRIMORDIAL GERM CELLS MIGRATE TO PREVIOUSLY
FORMED GERMINAL RIDGES THE PRIMORDIAL GERM CELLS OF
THE CARP #YPRINUS CARPIO ARE PRESENT AT THE SITE OF THE
GONADAL RIDGES BEFORE A GONADAL ANLAGE APPEARS 0AR
MENTIER AND 4IMMERMANS
6ARIOUS MECHANISMS HAVE BEEN PROPOSED TO EX
PLAIN THE MIGRATION OF PRIMORDIAL GERM CELLS IN lSH
AMOEBOID MOVEMENTS OF THE GERM CELLS THEMSELVES
A PASSIVE DELIVERANCE PRODUCED BY MORPHOGENETIC
MOVEMENTS OF THE SURROUNDING TISSUES AND TRANSPORT
IN THE BLOODSTREAM -IGRATION IS SAID TO BE POWERED
BY AMOEBOID MOVEMENT IN LARGEMOUTH BLACK BASS
-ICROPTERUS SALMOIDES SALMOIDES *OHNSTON
AND THE CARP #YPRINUS CARPIO .EDELEA AND 3TEOPOE
WHILE IN THE MEDAKA /RYZIAS LATIPES (AMA
GUCHI AND BARBEL "ARBUS CONCHONIUS 4IMMER
MANS AND 4AVERNE MORPHOGENETIC MOVEMENTS
OF THE SURROUNDING TISSUES ARE THOUGHT TO PROVIDE THE
MOTIVE FORCE 3UGGESTIONS OF A VASCULAR ROUTE OF MI
GRATION HAVE RECEIVED NO RECENT SUBSTANTIATION
0RIMORDIAL GERM CELLS ARE MITOTICALLY ACTIVE AS THEY
BECOME SEGREGATED FROM SOMATIC CELLS BUT MITOSIS
CEASES DURING THE PERIOD OF MIGRATION TO THE GONADAL
PRIMORDIA (AMAGUCHI 0ARMENTIER AND 4IM
MERMANS 4IMMERMANS AND 4AVERNE
'RANDI AND #OLOMBO )N SOME SPECIES A SECOND
PROLIFERATIVE PHASE OCCURS SOON AFTER GONADAL COLONI
ZATION BUT IN OTHERS THERE MAY BE A PERIOD OF WEEKS
OR MONTHS OF INTRAGONADAL MITOTIC REST INTRAGONADAL
PRIMORDIAL GERM CELLS OF THE CARP #YPRINUS CARPIO
FOR EXAMPLE REMAIN hMITOTICALLY SILENTv FOR AN EXTEND
ED PERIOD MAKING THEM ESPECIALLY SUITABLE FOR STUDIES
BEFORE THE ONSET OF PROLIFERATION VAN 7INKOOP ET AL
0RIMORDIAL GERM CELLS ARE LARGER THAN SURROUNDING
CELLS ARE ROUNDED OVAL OR PEAR SHAPED AND SHOW A
DISTINCT CELL BOUNDARY &IGURE .EDELEA AND 3TEO
POE (OGAN .IEUWKOOP AND 3UTASURYA
(AMAGUCHI 0ARMENTIER AND 4IMMERMANS
4IMMERMANS AND 4AVERNE VAN 7INKOOP
ET AL 'RANDI AND #OLOMBO 4HE LARGE
NUCLEUS HAS A DISTINCT MEMBRANE AND IS OFTEN ECCEN
TRIC IT CONTAINS ONE OR TWO PROMINENT NUCLEOLI 4HE
CYTOPLASM IS OFTEN HOMOGENEOUS BUT DEPENDING UPON
THE STAGE OF DEVELOPMENT AND THE SPECIES BEING STUD
IED IT MAY CONTAIN YOLK GRANULES OIL DROPLETS OR PIG
MENT GRANULES 'RANULAR ENDOPLASMIC RETICULUM AND
ABUNDANT RIBOSOMES HAVE BEEN DESCRIBED IN THE CYTO
PLASM OF SOME SPECIES AND AN ACTIVE 'OLGI COMPLEX IS
FOUND IN SOME CELLS OFTEN NEAR CLUMPS OF MITOCHON
DRIA &IGURE #OATED VESICLES SUGGESTIVE OF META
BOLIC EXCHANGES WITH THE GONADAL ENVIRONMENT WERE
DESCRIBED IN THE CYTOPLASM OF PRIMORDIAL GERM CELLS OF
THE CARP #YPRINUS CARPIO OFTEN NEAR THE SURFACE MEM
BRANE &IGURE VAN 7INKOOP ET AL
4WO CYTOPLASMIC MARKERS OF UNCERTAIN SIGNIlCANCE
ARE SAID TO DISTINGUISH PRIMORIDAL GERM CELLS OF /RY
ZIAS LATIPES FROM SOMATIC CELLS 3(%%43 /& !'2!.5,!2
%.$/0,!3-)# 2%4)#5,5- AND ELECTRON DENSE -)4/#(/.
$2)!, !33/#)!4%$ '2!.5,!2 -!4%2)!, &IGURE
(OGAN 4HE FENESTRATED SHEETS OF AGRANULAR
ENDOPLASMIC RETICULUM PERHAPS PRODUCED BY BLEB
BING OF THE NUCLEAR ENVELOPE FOLLOW THE CONTOURS OF
THE NUCLEI SOMETIMES ALMOST ENCIRCLING THEM )N THE
GERM CELLS OF MANY SPECIES MITOCHONDRIAL ASSOCIATED
GRANULAR MATERIAL FORMS ONE OR TWO COMPACT MASSES
THAT HAVE BEEN DESIGNATED VARIOUSLY AS "!,")!.) "/$
)%3 0%2).5#,%!2 .5!'%3 0%2).5#,%!2 $%.3% "/$)%3
AND '%2-).!, $%.3% "/$)%3 4IMMERMANS AND 4AV
ERNE VAN 7INKOOP ET AL 'RANDI AND
#OLOMBO 4HEY ARE LOOSELY WOVEN AND STRAND
LIKE IN PREMIGRATORY GERMINAL CELLS OF /RYZIAS LATIPES
THIS APPEARANCE GRADUALLY CHANGES AS THE CELLS BEGIN
THEIR MIGRATION AND IN THE GONADAL ANLAGEN THESE BOD
IES ARE AMORPHOUS OF VARIOUS SIZES AND SHAPES AND
COMPOSED OF ELECTRON DENSE lNE lBRILS &IGURE
(AMAGUCHI )N THE CARP #YPRINUS CARPIO THEY
INCREASE IN SIZE WITH DEVELOPMENT AND PART OF THE MA
TERIAL BECOMES MORE ELECTRON DENSE THESE DARK MASSES
ADHERE TO MITOCHONDRIA AND MAY BE CENTRES FOR MITO
CHONDRIAL MULTIPLICATION &IGURE VAN 7INKOOP
ET AL
#(!04%2
!NATOMY OF THE &EMALE 'ENITAL 3YSTEM
4HE FEMALE GENITAL SYSTEM CONSISTS OF THE /6!2)%3 THAT
PRODUCE %''3 OR /6! AND IN MOST SPECIES A DUCT SYS
TEM COMMUNICATING WITH THE EXTERIOR )N ADDITION TO ITS
CYTOCRINE FUNCTION OF PRODUCING FERTILIZABLE GAMETES
THE OVARY SHARES WITH THE TESTIS THE COMPLEMENTARY
ENDOCRINE FUNCTION OF SECRETING A VARIETY OF STEROID
HORMONES THAT REGULATE DEVELOPMENT OF THE GERM CELLS
/VIDUCTS MAY BE SIMPLE PASSAGEWAYS FOR THE EGGS BUT
OFTEN THEIR LINING IS GLANDULAR AND FORMS PROTECTIVE
COVERINGS FOR THE EGGS )N SOME VIVIPAROUS SPECIES
YOUNG MAY DEVELOP WITHIN THE OVARY AND IN OTHERS
WITHIN THE OVIDUCTS
'ONADS OF VERTEBRATES ALWAYS ORIGINATE FROM BILAT
ERAL PRIMORDIA BUT MANY SPECIES POSSESS ONLY ONE GO
NAD AS ADULTS &RANCHI -ANDL AND :UCKERMAN
(ARDER )N HAGlSH THE LEFT GONAD DEGENERATES
AND ONLY THE RIGHT DEVELOPS IN LAMPREYS THE TWO PRI
MORDIA FUSE DURING DEVELOPMENT FORMING A SINGLE
MIDLINE GONAD /VARIES OF ELASMOBRANCHS DEVELOP AS
PAIRED STRUCTURES ALONG THE DORSAL WALL OF THE COELOM
ON EACH SIDE OF THE MIDLINE 7OURMS $ODD
$ODD AND 3UMPTER #ALLARD ET AL
(AMLETT AND +OOB )N SEVERAL SPECIES EITHER THE
RIGHT OR LEFT OVARY FAILS TO MATURE 4HE FUNCTIONAL OVARY
MAY BE THE RIGHT AS IN SEVERAL VIVIPAROUS SHARKS OR
THE LEFT SOME VIVIPAROUS RAYS IN SOME OVIPAROUS
SKATES HOWEVER BOTH OVARIES ARE FUNCTIONAL !TROPHY
OF THE OVIDUCT MAY OCCUR ON THE SAME SIDE AS THE NON
FUNCTIONAL OVARY 4HERE IS A RANGE IN TELEOST lSHES FROM
COMPLETE FUSION TO PARTIAL FUSION INVOLVING ONLY THE
POSTERIOR PART OF THE GONAD OR JUST THE GONODUCTS &RAN
CHI -ANDL AND :UCKERMAN (ARDER
3OMETIMES ONE OF THE GONADS IS RUDIMENTARY OR MERELY
SMALLER BUT STILL PRESENT
4HE OVARIES ARE SUSPENDED IN THE POSTERIOR BODY
CAVITY DORSAL TO THE GUT BY -%3/6!2)! THAT RUN THEIR
ENTIRE LENGTH &IGURE (ARDER 4HE OVARIES
MAY BE DISPLACED TOWARD THE INTESTINE COMING TO LIE
WITH THE INTESTINE WITHIN THE MESENTERY &IGURE
"ENEATH THE 6)3#%2!, 0%2)4/.%5- THAT ENVELOPS EACH
OVARY IS A CAPSULE OF CONNECTIVE TISSUE AND SMOOTH
MUSCLE THE 45.)#! !,"5').%! 4HE /6!2)!. !24%29 AR
RIVES BY WAY OF THE MESOVARIUM AND BRANCHES REPEAT
EDLY INTO THE TUNICA ALBUGINEA
4HE OVARIES OF CYCLOSTOMES MOST ELASMOBRANCHS
AND SOME TELEOSTS ARE SOLID AND OVA ARE SHED DIRECTLY
INTO THE BODY CAVITY .O DUCT SYSTEM IS PRESENT IN CY
CLOSTOMES AND THE EGGS ARE EXPELLED FROM THE BODY
THROUGH '%.)4!, 0/2%3 THAT DEVELOP IN THE BODY WALL
SHORTLY BEFORE SPAWNING AND LEAD INTO THE URINARY SINUS
OR URINARY DUCT AND THENCE TO THE CLOACA OR URINOGENI
TAL PAPILLA )N ELASMOBRANCHS A DUCT SYSTEM TYPICAL OF
HIGHER VERTEBRATES DEVELOPS FROM THE MESONEPHRIC OR
-LLERIAN DUCTS GATHERING UP SHED EGGS OR EMBRYOS
IN A FUNNEL SHAPED /34)5- AND PASSING THEM THROUGH
AN /6)$5#4 TO THE OUTSIDE OFTEN ADDING A SHELL OR PRO
VIDING REFUGE FOR DEVELOPING EMBRYOS ALONG THE WAY
&IGURE (OAR $ODD 4WO OVARIES
AND TWO OVIDUCTS ARE PRESENT IN THE CHIMAERA (YDROLA
GUS COLLIEI )N GENERAL THE REPRODUCTIVE SYSTEM OF THIS
HOLOCEPHALAN RESEMBLES THAT OF ELASMOBRANCHS
!LTHOUGH THE OVARIES OF MOST ELASMOBRANCHS ARE
SOLID THE VISCERAL PERITONEAL COVERING OF THE OVARY OF
LAMNID SHARKS INVAGINATES TO CREATE A HOLLOW ORGAN
-ATTHEWS 0RATT 4HE HOLLOW IS A DIRECT
EXTENSION OF THE PERITONEAL CAVITY AND FORMS A BRANCH
ING INVAGINATION FROM A POCKET ON THE RIGHT SIDE OF THE
OUTER SURFACE &IGURE 4HE CHANNELS PENETRATE ALL
PARTS OF THE OVARY AND PROVIDE A MEANS OF EXIT FOR RIPE
OOCYTES &IGURE
4ELEOSTS DISPLAY TWO TYPES OF OVARIES GYMNOVAR
IAN AND CYSTOVARIAN $ODD AND 3UMPTER +OYA
4AKANO AND 4AKAHASHI )N THE SIMPLER '9-.
/6!2)!. CONDITION THE OVARIES ARE SUSPENDED IN THE
COELOM AND OVULATION OCCURS DIRECTLY INTO THE COELOMIC
CAVITY )N #934/6!2)!. OVARIES ADHESIONS OCCUR WHICH
ISOLATE A PART OF THE COELOM THEREBY FORMING A CLOSED
SAC THE /6!2)!. #!6)49 OR ,5-%. INTO WHICH OVULA
TION OCCURS DIRECTLY &IGURE 4HIS OVARIAN CAVITY
COMMUNICATES ONLY WITH ITS DUCT AND IS LINED WITH ME
SOTHELIUM DERIVED FROM THE COELOMIC PERITONEUM &OL
LOWING OVULATION EGGS FROM BOTH TYPES OF OVARIES ARE
BATHED IN A mUID )N GYMNOVARIAN OVARIES THIS mUID IS
#/%,/-)# &,5)$ AND IS SYNTHESIZED AND SECRETED BY THE
EPITHELIUM OF THE DORSOLATERAL COELOMIC WALL AND MES
OVARIUM )N THE ENCLOSED CAVITY OF CYSTOVARIAN OVARIES
THE mUID IS DESIGNATED AS /6!2)!. &,5)$ AND ORIGINATES
IN PART FROM THE EPITHELIAL LINING 3INCE TELEOSTS DISPLAY
A WIDE SPECTRUM OF REPRODUCTIVE METHODS THESE mUIDS
HAVE MANIFOLD FUNCTIONS
4HE CAVITY OF CYSTOVARIAN OVARIES MAY BE FORMED
IN TWO WAYS !N %.$/6!2)!. #!6)49 IS DERIVED FROM
INTERNALIZED INVAGINATIONS OF THE GENITAL RIDGES WHERE
THE RIBBONLIKE OVARIES ROLL UP IN A LATERAL AND DORSAL
DIRECTION SO THAT THE SIDE AT WHICH OVULATION OCCURS IS
TURNED INWARD SURROUNDING THE CAVITY &IGURE
'OODRICH !LTERNATIVELY A 0!2/6!2)!. #!6)49
ARISES FROM A SPACE ENCLOSED BY ADHESIONS BETWEEN THE
&%-!,% '%.)4!, 3934%-3 /& &)3(
GENTIAL RIDGE AND THE PARIETAL PERITONEUM ! RANGE IS
SEEN FROM A SIMPLE OVARY WHERE OVA ARE SHED INTO THE
OVARIAN CAVITY AND SOON EXPELLED TO THE COMPLEX HOL
LOW ORGAN OF VIVIPAROUS TELEOSTS THAT PRODUCES EGGS
STORES SPERMATOZOA SERVES AS A SITE FOR FERTILIZATION
AND MAY PROVIDE NOURISHMENT FOR DEVELOPING YOUNG
FOR A PROLONGED PERIOD
3TEROID
PRODUCING CELLS ARE DESCRIBED IN THE OVARY
OF TILAPIA 3AROTHERODON NILOTICUS DURING OVARIAN DIF
FERENTIATION .AKAMURA AND .AGAHAMA !S
THE OVARIAN CAVITY IS FORMING THESE CELLS APPEAR NEAR
THE BLOOD VESSELS OF THE STROMA ON THE SIDE FACING THE
MESENTERY &IGURE 4HEY ARE PRESUMED TO ORIGI
NATE FROM STOMAL ELEMENTS AND AS THE OVARY DEVELOPS
THEIR NUMBERS INCREASE SURROUNDING THE BLOOD VESSELS
4HESE CELLS DISPLAY THE TUBULAR MITOCHONDRIAL CRISTAE
AND TUBULAR AGRANULAR ENDOPLASMIC RETICULUM WHICH
ARE CHARACTERISTIC OF STEROID PRODUCTION &IGURE
)T IS SUGGESTED THAT THE STEROIDS PRODUCED BY THESE CELLS
PLAY A ROLE IN THE FORMATION OF THE OVARIAN LUMEN &IG
URE AND IN THE DIFFERENTIATION OF GERM CELLS
)N MANY TELEOSTS THE VISCERAL PERITONEUM COVERING
THE OVARY AND THE PERITONEUM LINING ITS CAVITY OFTEN
CONTINUE POSTERIORLY BEYOND THE MASS OF OVARIAN TIS
SUE TO FORM THE UNIQUE /6)$5#4 (OAR (ARDER
&IGURE 4HIS EXTENSION OF THE OVARIAN CAV
ITY CONTINUES POSTERIORLY TO CONNECT WITH THE '%.)4!,
0/2% LEADING TO THE EXTERIOR )N SOME TELEOSTS INCLUDING
/STEOGLOSSIDAE (IODONTIDAE .OTOPTERIDAE !NGUILLI
DAE THE LOACH -ISGURNUS #OBITIDIDAE 'ALAXIIDAE
AND 3ALMONIDAE THE OVIDUCTS DEGENERATE IN WHOLE OR
IN PART SO THAT THE OVA PASS INTO THE BODY CAVITY AND
MAKE THEIR EXIT BY WAY OF FUNNELS OR PORES DEPEND
ING UPON THE DEGREE OF DEGENERATION OF THE OVIDUCTS
(OAR VAN 4IENHOVEN
/VARY
4HE VERTEBRATE OVARY IS AN AGGREGATION OF DEVELOP
ING &/,,)#,%3 ENMESHED IN A VASCULAR 342/-! OF LOOSE
CONNECTIVE TISSUE AND ENCLOSED WITHIN AN ENVELOPE OF
GONADAL EPITHELIUM &IGURE 4HE STROMA CONSISTS
OF COLLAGENOUS ELASTIC AND RETICULAR lBRES AND BE
COMES GREATLY DISTENDED AS THE FOLLICLES ENLARGE /NLY
IN A SPENT OVARY WHEN THE STROMA IS COLLAPSED IS IT
EASILY SEEN "ENEATH THE OVARIAN ENVELOPE A CONDEN
SATION OF STROMAL TISSUE FORMS THE 45.)#! !,"5').%!
A CAPSULE OF CONNECTIVE TISSUE AND SOMETIMES SMOOTH
MUSCLE &IGURE #OLLAGENOUS AND ELASTIC lBRES
ARE MOST ABUNDANT IN THE PERITONEUM LESS SO IN THE
TUNICA ALBUGINEA AND LESS AGAIN IN THE STROMA ITSELF
2ETICULAR lBRES ARE NUMEROUS IN BOTH THE CAPSULE AND
THE STROMA APPEARING AS lNE ANASTOMOSING ARGYRO
PHILIC THREADS SURROUNDING EACH EGG WITHIN A BASKET OF
lBRES &IGURE
%ARLY FOLLICLES CONSIST OF PRIMORDIAL GERM CELLS
NEWLY ARRIVED BY MIGRATION ENCLOSED WITHIN A CLUS
TER OF &/,,)#5,!2 #%,,3 DERIVED FROM DIVISIONS OF THE
GONADAL EPITHELIAL CELLS 0RIMORDIAL GERM CELLS DIVIDE
BY MITOSIS TO PRODUCE DIPLOID //'/.)! &IGURE
"Y MITOTIC DIVISION THESE OOGONIA FORM DIPLOID 02)-!
29 //#94%3 -EIOTIC DIVISION OF A PRIMARY OOCYTE RE
SULTS IN A 3%#/.$!29 //#94% AND lRST 0/,!2 "/$9 BOTH
DIPLOID &IGURE 'RANDI AND #OLOMBO
4HE FOLLICULAR EPITHELIUM EVENTUALLY COMPLETELY SUR
ROUNDS THE SECONDARY OOCYTE AND THE FOLLICLE INCREASES
GREATLY IN SIZE lRST BY THE ELABORATION OF MORE CYTO
PLASM AND LATER BY THE ACCUMULATION OF YOLK DURING
THE PROCESS OF 6)4%,,/'%.%3)3 &INALLY THE SECONDARY
OOCYTE UNDERGOES -!452!4)/. WHERE A SECOND MEI
OTIC DIVISION YIELDS AN /65- AND ANOTHER POLAR BODY
BOTH HAPLOID 4HE DEVELOPMENT AND MATURATION OF
DIPLOID OOGONIA TO PRODUCE HAPLOID OVA IS //'%.%3)3
0OLAR BODIES ARE SMALL FUNCTIONLESS HAPLOID CELLS
RESULTING FROM UNEQUAL DIVISION DURING OOGENESIS
4HEY ALLOW MOST OF THE CYTOPLASM TO PASS TO THE OVUM
WHILE PROVIDING FOR DISPOSAL OF EXCESS CHROMATIN
POLAR BODIES SUBSEQUENTLY DEGENERATE
! DETAILED DESCRIPTION OF FOLLICULOGENESIS IN TELE
OSTS HAS BEEN PROVIDED FOR ADULT FEMALES OF THE COM
MON SNOOK #ENTROPOMUS UNDECIMALIS 'RIER
/OGONIA PRESUMABLY HAVING ARISEN FROM SOME EX
TERNAL SOURCE ARE DISPERSED AMONG THE SOMATIC CELLS
OF THE GONADAL GERMINAL EPITHELIUM THAT LINES THE
OVARIAN LUMEN &IGURE 4HE OOGONIA DIVIDE BY
MITOSIS OFTEN FORMING NESTS OF CELLS !T THE OUTSET
OF FOLLICULOGENESIS SOME OOGONIA BEGIN TO DIVIDE BY
MEIOSIS TO PRODUCE OOCYTES 4HESE OOCYTES DESCEND
INTO THE DEEPER BASAL REGIONS OF THE EPITHELIUM 3OME
EPITHELIAL CELLS WHOSE PROCESSES ENVELOP MEIOTIC OO
CYTES TRANSFORM INTO PREFOLLICULAR CELLS WHICH BECOME
FOLLICULAR CELLS AT THE COMPLETION OF FOLLICULOGENESIS
&IGURE 4HE OOCYTE SURROUNDED BY ITS SIMPLE
LAYER OF PREFOLLICULAR CELLS PRESSES ON THE BASEMENT
MEMBRANE OF THE GONADAL EPITHELIUM EVAGINATING
IT AND EVENTUALLY CAUSING THE PINCHING OFF OF A DIS
CRETE FOLLICLE CONSISTING OF THE OOCYTE SURROUNDED BY
ITS LAYER OF FOLLICLAR CELLS AND ENCLOSED IN A BASEMENT
MEMBRANE #ELLS OF THE STROMA AGGREGATE AROUND THE
BASEMENT MEMBRANE OF THE FOLLICLE TO FORM THE VAS
#(!04%2
CULAR THECA INTERNA AND AVASCULAR THECA EXTERNA &OL
LICULOGENESIS IS CONSIDERED TO BE CONCLUDED WHEN
THE BASEMENT MEMBRANE COMPLETELY ENCLOSES THE FOL
LICULAR EPITHELIUM THE THECAL LAYERS MAY BE FRAGMEN
TARY AT THIS TIME %NSCONCED WITHIN THE OVARIAN STROMA
THE FOLLICLE CONTINUES ITS DEVELOPMENT
)N THE PAST IT HAS BEEN PROPOSED THAT OOGONIA AND
EARLY MEIOTIC STAGES ARE NOT PRESENT IN THE OVARIES
OF ADULT CARTILAGINOUS lSHES )T HAS BEEN SHOWN THAT
OOGENESIS OCCURS EARLY IN THE LIFE OF THE SPOTTED RAY
4ORPEDO MARMORATA AN APLACENTAL VIVIPAROUS ELAS
MOBRANCH WITH A REPRODUCTIVE CYCLE OF THREE YEARS
0RISCO 2ICCHIARI AND !NDREUCCETTI 4HE SITE
OF ORIGIN AND MIGRATORY ROUTE OF THE PRIMORDIAL GERM
CELLS WAS NOT DETERMINED #LUSTERS OF OOGONIA AND EARLY
MEIOTIC OOCYTES WERE OBSERVED IN THE GONADAL ANLAGE
OF EMBRYOS GERM CELLS IN THE CLUSTERS WERE CONNECTED
BY INTERCELLULAR BRIDGES BORDERED BY AN ELECTRON DENSE
MEMBRANE ABOUT NM THICK &IGURE )N OVARIES
OF SUBADULT AND ADULT FEMALES HOWEVER ALL THE GERM
CELLS WERE ORGANIZED INTO FOLLICLES AND NO CLUSTERS
OF OOGONIA OR EARLY MEIOTIC CELLS WERE FOUND WITH A
SINGLE EXCEPTION )N ONE ADULT FEMALE THE PERSISTENCE
OF GERM CELLS NOT ORGANIZED INTO FOLLICLES MAY SUPPORT
THE CONCEPT OF hREPRODUCTIVE PLASTICITYv AND REPRE
SENT THE VARIATION THAT IS TARGETED BY NATURAL SELEC
TION THEREBY ACCOUNTING FOR THE DIFFERENT REPRODUCTIVE
STRATEGIES ADOPTED BY CARTILAGINOUS lSHES
)N LAMPREYS PRIMARY GERM CELLS DIVIDE SLOWLY IN
THE GONADAL RIDGE BENEATH THE PERITONEUM ,EWIS AND
-C-ILLAN (ARDISTY 4HIS IS FOLLOWED BY
A PERIOD OF MORE RAPID DIVISION WHEN THE GERM CELLS
FORM '%2- #%,, .%343 OR CYSTS -EIOTIC PROPHASE BE
GINS IN BOTH ISOLATED GERM CELLS AND IN THE CELL NESTS
#ELLS FROM THE PERITONEAL EPITHELIUM GIVE RISE TO FOL
LICULAR ELEMENTS 'ERM CELLS MAY BEGIN CYTOPLASMIC
GROWTH OR UNDERGO DEGENERATION ATRESIA IN EARLY STAG
ES OF MEIOTIC PROPHASE /OGENESIS OCCURS TO SOME EX
TENT IN MOST OR ALL LAMPREY GONADS )N GONADS DESTINED
TO BECOME OVARIES OOGENESIS IS MORE SYNCHRONOUS
THAN IN TESTES AND EVENTUALLY ONLY OOCYTES ARE PRESENT
)N MALE LAMPREYS OOCYTES THAT HAVE PROCEEDED TO THE
CYTOPLASMIC GROWTH PHASE ARE ELIMINATED BY ATRESIA
SO THAT THE TESTIS BECOMES SMALLER DURING DIFFERENTIA
TION AND CONTAINS ONLY SMALL NUMBERS OF RESIDUAL GERM
CELLS AT METAMORPHOSIS THESE DEVELOP BY MITOSIS INTO
NESTS OF PRIMARY SPERMATOGONIA
$IVISION OF DEVELOPING GERM CELLS IN THE OVARIES
OF LAMPREYS CAUSES EVAGINATIONS OF THE OVARIAN WALL
TO EXPAND VENTRALLY SUBDIVIDING THE OVARY INTO LOBES
AND LOBULES THAT CONTAIN A STROMA OF VASCULAR CONNEC
TIVE TISSUE &IGURES ! TO # ,EWIS AND -C-ILLAN
4HESE mAT LEAF
LIKE EXTENSIONS OF OVARIAN TIS
SUE USUALLY TWO FOLLICLES IN THICKNESS ARE THE /6)'%2
/53 &/,$3 &IGURE $
4HE OVARY OF THE HAGlSH -YXINE GLUTINOSA IS A
DORSAL NARROW RIBBON SUSPENDED IN THE MIDLINE FROM
THE MESOVARIUM 7ALVIG 0ATZNER
)T CONSISTS OF hSERIESv OF FOLLICLES THAT DEVELOP FROM
OOGONIA CONTAINED WITHIN A BAND OF GERMINAL CELLS THAT
RUNS ALONG THE FREE EDGE OF THE OVARY &IGURE !
7HEN THE OOCYTES ENTER THE VASCULAR CONNECTIVE TIS
SUE OF THE INNER PART OF THE OVARY UNDIFFERENTIATED EPI
THELIAL CELLS FROM THE MESOTHELIUM COVERING THE OVARY
BECOME ATTACHED TO THEM GROW AND STRETCH TO ENCLOSE
THEM WITHIN A FOLLICULAR EPITHELIUM h'ENERATIONSv
OF OOCYTES DEVELOP FROM OOGONIA IN THE GERMINAL
RIDGE THEY GROW TO A DIAMETER OF TO MM WHERE
UPON THEY ENTER A RESTING PERIOD AWAITING OVULATION
OF THE PREVIOUS GENERATION OF OOCYTES 0ATZNER
4HE PRIMARY FOLLICLE CONSISTS OF AN OOCYTE SURROUNDED
BY ITS FOLLICULAR EPITHELIUM AND IS CONTAINED WITHIN A
CONNECTIVE TISSUE SHEATH THE 4(%#! &IGURE %
4WO LAYERS CAN BE DISCERNED IN THIS CONNECTIVE TIS
SUE THE THECA INTERNA AND THECA EXTERNA 4HE LARGEST
AND OLDEST OF THE IMMATURE EGGS ARE FOUND DANGLING
IN INDIVIDUAL PERITONEAL SLINGS THE &/,,)#5,!2 ,)'!
-%.43 IN A SINGLE ROW AT THE VENTRAL BOUNDARY OF THE
OVARY &IGURE & 3OME OF THESE EGGS MATURE ARE
OVULATED AND A NEW ROW OF FOLLICLES DEVELOPS TO TAKE
THEIR PLACES &IGURE ' %MPTY POSTOVULATORY FOL
LICLES REMAIN FOR A TIME HANGING FROM THE FREE SURFACE
OF THE OVARY LATER THEY WITHDRAW INTO THE STROMA AND
UNDERGO REGRESSION
4HE VISCERAL EPITHELIUM LINING THE HOLLOW CYSTOVAR
IAN OVARIES OF MANY TELEOSTS IS THROWN INTO A COMPLEX
SERIES OF OVIGEROUS FOLDS &IGURE (OAR
)N THE STICKLEBACK %UCALIA INCONSTANS THE FOLDS PROJ
ECT INTO THE CENTRE OF THE CAVITY USUALLY EXTENDING
THE ENTIRE LENGTH OF THE OVARY CROWDING THE CAVITY
INTO A VENTROLATERAL POSITION WHERE NO FOLDS ORIGINATE
"RAEKEVELT AND -C-ILLAN %ARLY GERM CELLS
ARE lRST FOUND ON THE EDGE OF THE FOLDS BORDERING THE
OVARIAN CAVITY !S THE FOLLICLES MATURE AND INCREASE IN
SIZE THEY ARE PUSHED DEEPER INTO THE STROMA 7HEN THE
FOLLICLES ARE MATURE THEY BURST THROUGH THE VISCERAL
PERITONEUM AND ARE OVULATED INTO THE OVARIAN CAVITY
WHERE THEY REMAIN UNTIL SPAWNING 4HE CAVITY WHICH
BECOMES LARGELY OBLITERATED AS THE EGGS REACH MATURITY
CONTINUES POSTERIORLY AS THE LUMEN OF THE OVIDUCT
&%-!,% '%.)4!, 3934%-3 /& &)3(
4HE OVARY OF TELEOSTS IS SUPPLIED WITH BLOOD FROM
SEVERAL ARTERIES THAT BRANCH OFF THE DORSAL AORTA ENTER
ING THE DORSAL SIDE OF THE OVARY THROUGH THE MESOVARI
UM %ACH FOLLICLE IN THE OVARY OF &UNDULUS IS SUPPLIED
BY A PRIMARY ARTERIOLE THAT REACHES IT THROUGH A STALK
OF STROMAL ELEMENTS &IGURES ! " "RUMMETT
$UMONT AND ,ARKIN "RANCHES OF THE ARTERIOLE
PENETRATE DEEPLY INTO THE INVESTING LAYERS OF THE FOL
LICLE 4HE SUPERlCIALLY LOCATED VESSELS IN THE APICAL OR
LUMINAL HEMISPHERE OF THE FOLLICLE ARE MORE READILY
APPARENT AND ARE PRESUMED TO BE VENULES THAT COLLECT
BLOOD FROM THE INTERVENING CAPILLARY BED AND TRANSPORT
IT TO A VESSEL THAT FORMS A LOOP ON THE LUMINAL SIDE OF
THE FOLLICLE &IGURES # AND ! 4HESE VESSELS TER
MINATE IN A SINGLE COLLECTING VESSEL THAT COURSES TOWARD
THE OUTER SURFACE OF THE OVARY MERGING WITH OTHERS INTO
TWO LARGE VEINS THAT UNITE IN THE DORSAL ANTERIOR REGION
OF THE OVARY TO FORM THE SINGLE OVARIAN VEIN 4HICK
BUNDLES OF NON
MYELINATED NERVES PRESUMABLY AUTO
NOMIC ACCOMPANY THE OVARIAN ARTERY AND VEIN IN THE
OVARY OF TILAPIA /REOCHROMIS NILOTICUS &IGURE
.AKAMURA 3PECKER AND .AGAHAMA 'ROUPS
OF A FEW AXONS RAMIFY FROM THESE NERVES TO TERMINATE
AMONG THE CELLS SURROUNDING THE FOLLICLES
)N THE KILLIlSH &UNDULUS HETEROCLITUS THE POSTERIOR
PORTION OF THE OVARY IS A THIN
WALLED NONGERMINAL
/6)3!# THAT IS CONTINUOUS WITH THE SHORT OVIDUCT AND
APPARENTLY SERVES AS A RECEPTACLE FOR OVULATED EGGS
PRIOR TO THEIR RELEASE TO THE EXTERNAL ENVIRONMENT
"RUMMETT $UMONT AND ,ARKIN 4HE LUMINAL
EPITHELIUM OF THIS THIN
WALLED REGION DISPLAYS A LOCAL
IZED POPULATION OF UNUSUAL CELLS WITH LONG CYTOPLAS
MIC EXTENSIONS BEARING SHORT MICROVILLI &IGURE
4HESE CELLS MAY CONTINUE TO LINE AT LEAST PART OF THE
OVIDUCT AND MAY FUNCTION IN THE TRANSPORT OF OVULATED
EGGS OR THEY MAY SECRETE A JELLY THAT FORMS A SURFACE
COAT FOR THE EXTRUDED EGGS
4HE MICROSCOPIC STRUCTURE OF THE OVARIAN LUMINAL
WALL HAS BEEN DESCRIBED IN A FEW OVIPAROUS TELEOSTS
4HE OVARIAN WALL OF VIVIPAROUS TELEOSTS IS DESCRIBED
IN THE SECTION ON 6IVIPARITY )N THE MEDAKA /RYZIAS
LATIPES ITS EPITHELIUM DISPLAYS CYCLIC CHANGES CORRE
SPONDING TO CHANGES IN THE OVARY 9AMAMOTO
!S THE OVA MATURE THE LUMINAL WALL THICKENS AND
ITS SIMPLE CUBOIDAL EPITHELIUM BECOMES SIMPLE CO
LUMNAR AS SECRETORY ACTIVITY INCREASES &IGURE
4HE UNDERLYING TUNICA ALBUGINEA THICKENS AS VASCU
LARIZATION INCREASES AND SMOOTH MUSCLE DEVELOPS )T
IS PRESUMED THAT THE mUIDS PRODUCED BY THE EPITHELIAL
CELLS FACILITATE EXTRUSION OF THE EGGS AT SPAWNING AS
WELL AS PLAYING SOME ROLE DURING EXTERNAL FERTILIZATION
!FTER SPAWNING THE EPITHELIUM AND TUNICA ALBUGINEA
UNDERGO INVOLUTION
! SIMPLE COLUMNAR EPITHELIUM OF -)#2/6),,/53
#%,,3 LINES THE OVARIAN CAVITY OF THE BLEAK !LBURNUS
ALBURNUS ,AHNSTEINER 7EISMANN AND 0ATZNER
!ROUND THE TIME OF OVULATION THESE CELLS BULGE API
CALLY INTO THE LUMEN AND A FEW SMALL CLUSTERS ARE ALSO
FOUND IN THE OVIDUCT &IGURE 4HESE CELLS HAVE
DIVERSE FUNCTIONS THEY ARE SECRETORY MAINTAINING THE
IONIC GRADIENT OF THE OVARIAN mUID BY THE SECRETION OF
GLUCOSE PROTEINS AND ENZYMES ACID PHOSPHATASE
PROTEASE AND ` $
GLUCURONIDASE THEY SYNTHESIZE
GLUCURONIDE STEROID WHICH MAY ACT AS A PHEROMONE
THAT ATTRACTS MALES AND INCREASES THE VOLUME OF MILT
AND THEY ARE PHAGOCYTIC 0ROTEIN PRODUCTION BY MICRO
VILLOUS CELLS IS INDICATED BY THE PROMINENT NUCLEOLUS
AND ABUNDANT TUBULAR GRANULAR ENDOPLASMIC RETICULUM
THAT FORMS CONCENTRIC LAYERS AROUND THE BASAL NUCLEUS
&IGURE #OATED VESICLES PINCHED OFF FROM THE
ENDOPLASMIC RETICULUM ARE ASSOCIATED WITH THE UBIQUI
TOUS 'OLGI COMPLEXES SECRETORY VESICLES ARE RELEASED
FROM THE 'OLGI CISTERNS 4HE INVOLVEMENT OF THE MI
CROVILLOUS CELLS IN IONIC REGULATION OF THE OVARIAN mUID
IS DEMONSTRATED BY THE PRESENCE OF APICAL JUNCTIONAL
COMPLEXES SEALING THE EPITHELIUM THE ABUNDANCE OF
APICAL MITOCHONDRIA AND POSITIVE TESTS FOR APICAL AD
ENOSINE TRIPHOSPHATASE ACTIVITY -AINTENANCE OF THE
INORGANIC COMPOSITION OF THE OVARIAN mUID IS ESSENTIAL
TO PREVENT EGG ACTIVATION CLOSURE OF THE MICROPYLE
SWELLING OF THE EGGS DUE TO WATER UPTAKE AND SHELL
HARDENING 4ABLE RECORDS ANALYSES OF THE COMPOSI
TION OF THE OVARIAN mUID IN THE BLEAK 4HE MICROVILLOUS
CELLS OF THE BLEAK CONTAIN HETEROPHAGIC VACUOLES AND
LAMELLAR BODIES AND ARE ACTIVE IN THE PHAGOCYTOSIS OF
DBRIS FROM THE LUMEN !UTOPHAGY OCCURS IN REGIONS
CONTAINING SECRETORY VESICLES 4HE CYTOPLASM ALSO CON
TAINS LIPID VACUOLES AND ACCUMULATIONS OF FREE RIBO
SOMES !GRANULAR ENDOPLASMIC RETICULUM IS RARE
/VARIES OF THE SYNGNATHIDS THE PIPElSH 3YNGNATHUS
SCOVELLI AND SEAHORSE (IPPOCAMPUS ERECTUS ARE UN
USUAL IN THAT THEY LACK OVIGEROUS LAMELLAE AND PRES
ENT A SEQUENTIAL ARRAY OF DEVELOPING FOLLICLES ARRANGED
WITHIN A SINGLE SHEET IN ORDER OF THEIR DEVELOPMENTAL
MATURITY "EGOVAC AND 7ALLACE 3EL
3IMILAR VALUES FOR FOUR SPECIES OF SALMONIDS ARE RECORDED IN
AN EARLIER PAPER BY THESE AUTHORS ,AHNSTEINER 7EISMANN AND
0ATZNER
#(!04%2
MAN 7ALLACE AND 0LAYER 4HIS FEATURE IS ES
PECIALLY USEFUL FOR STUDIES OF FOLLICULAR DEVELOPMENT
4HE OVARIES ARE ASYNCHRONOUS AND BECAUSE THESE lSH
ARE REPRODUCTIVELY ACTIVE THROUGHOUT THE YEAR A HET
EROGENEOUS POPULATION OF FOLLICLES IS AVAILABLE IN ALL
DEVELOPMENTAL STAGES
4HE OVARIES OF BOTH SPECIES OF SYNGNATHIDS CONSIST
OF A SHEET OF FOLLICLES WITH THEIR SUPPORTING VASCU
LAR STROMA IN THE FORM OF A TUBULAR SCROLL EXTENDING
LENGTHWISE &IGURE "EGOVAC AND 7ALLACE
3ELMAN 7ALLACE AND 0LAYER ! SINGLE '%2-)
.!, 2)$'% OF THE PIPEFISH OVARY FORMS THE INNER MARGIN
OF THE SCROLL AND EXTENDING FROM THIS IS A SEQUENTIAL
ARRAY OF FOLLICLES ARRANGED ACCORDING TO THEIR DEVEL
OPMENTAL AGE SANDWICHED BETWEEN THE OUTER OVARIAN
WALL AND THE INNER LUMINAL EPITHELIUM -ATURE OOCYTES
ARE OVULATED FROM THE OPPOSITE MARGIN OF THE SCROLL
THE -!452% %$'% INTO THE OVARIAN LUMEN "EGOVAC
AND 7ALLACE )N THE SEAHORSE THERE ARE
TWO GERMINAL RIDGES THAT RUN THE LENGTH OF THE TUBULAR
OVARY ON OPPOSITE EDGES OF THE OVARIAN SHEET 3ELMAN
7ALLACE AND 0LAYER $EVELOPING FOLLICLES ARISE
FROM EACH GERMINAL RIDGE AND GROW TOWARD A SHARED
MATURE REGION NEAR THE MIDDLE OF THE SHEET 4HESE SE
QUENCES MAY BE SEEN IN ANY CROSS SECTION OF SYGNATHID
OVARIES &IGURE )N CONTRAST TO THE RANDOM ORGA
NIZATION OF OVARIES OF OTHER lSH THIS TEMPORAL AND SPA
TIAL CORRELATION OF OOCYTE DEVELOPMENT AS SEEN IN THESE
TWO SPECIES FACILITATES THE STUDY OF SPECIlC EVENTS IN
FOLLICULAR DEVELOPMENT )N ADDITION THE EARLIEST EVENTS
OF OOGONIAL PROLIFERATION AND EARLY FOLLICLE FORMATION
BECAUSE OF THEIR SPECIlC LOCATION WITHIN THE OVARY ARE
ACCESSIBLE TO EXPERIMENTAL MANIPULATION
4HESE SYNGNATHID OVARIES ARE COVERED ON THE OUT
SIDE BY VISCERAL MESOTHELIUM OF SQUAMOUS TO LOW CU
BOIDAL CELLS THAT IS CONTINUOUS WITH THE MESOVARIUM
THESE CELLS HAVE IRREGULAR APICAL SURFACES AND NUMER
OUS PITS AND VESICLES ON BOTH THEIR APICAL AND BASAL
SURFACES &IGURE ! 4HEY CONTAIN ABUNDANT CY
TOPLASMIC lLAMENTS AND HAVE JUNCTIONAL COMPLEXES
AT THEIR APICO
LATERAL SURFACES 4HIS EPITHELIUM IS SUB
TENDED BY VARIABLE AMOUNTS OF COLLAGENOUS CONNECTIVE
TISSUE CONNECTING IT TO SEVERAL LAYERS OF SMOOTH MUSCLE
&IGURE " "LOOD AND LYMPH VESSELS ARE VISIBLE IN
THIS CONNECTIVE TISSUE WITH THE LARGER VESSELS APPARENT
AT THE CONNECTION WITH THE MESOVARIUM 3MOOTH MUS
4!",% #OMPOSITION OF THE OVARIAN mUID OF THE BLEAK !LBURNUS ALBURNUS N &ROM ,AHNSTEINER
7EISMANN AND 0ATZNER
#OMPONENT
P(
/SMOLALITY MOSMOL KGn
.A MMOL n
+ MMOL n
#A MMOL n
0ROTEIN MG X ML n
'LUCOSE MOL n
&RUCTOSE MOL n
'ALACTOSE MOL n
'LYCEROL MOL n
4RIGLYCERIDES MOL n
#HOLESTEROL MOL n
0HOSPHATIDYLCHOLINE MOL n
#HOLINE MOL n
!LKALINE PHOSPHATASE MOL MIN n n
!CID PHOSPHATASE MOL MINn n
`
$
GLUCURONIDASE MOL MINn n
0ROTEASE GELATIN SUBSTRATE MOL MINn n
0ROTEASE CASEIN SUBSTRATE MOL MIN n n
6ALUE
(
(
(
(
(
(
(
(
(
(
(
(
(
(
(
(
(
&%-!,% '%.)4!, 3934%-3 /& &)3(
CLE COMPRISES MOST OF THE THICKNESS OF THE OVARIAN WALL
THE lBRES ARE ARRANGED ROUGHLY INTO TWO LAYERS AN IN
NER CIRCULAR AND AN OUTER LONGITUDINAL &IGURE #
3MALL BLOOD VESSELS COURSE BETWEEN THE MUSCLE CELLS
AS WELL AS BUNDLES OF UNMYELINATED NERVES THAT TEND TO
RUN PARALLEL TO THE LONG AXIS OF THE OVARY 6ASCULAR CON
NECTIVE TISSUE OF VARIABLE THICKNESS OCCURS BETWEEN THE
MUSCLE CELLS AND OVARIAN FOLLICLES )T IS SUGGESTED THAT
OVULATION IS ACCOMPANIED BY A WAVE OF CONTRACTION OF
THIS SMOOTH MUSCLE COORDINATED BY NERVOUS ELEMENTS
THAT SQUEEZES EGGS FROM THE LUMEN BEGINNING CRANI
ALLY AND PROCEEDING CAUDALLY
4HE '%2-).!, 2)$'%3 EXTEND THE LENGTH OF THE OVARY
AND CONTAIN THE PROLIFERATIVE STEM CELLS FROM WHICH
THE OOCYTES ARE DERIVED AND FOLLICLES FORMED &IGURE
! 4HE RIDGES ARE COVERED BY THE LUMINAL EPITHE
LIUM OF SQUAMOUS TO CUBOIDAL CELLS AND CONTAIN RICHLY
VASCULAR CONNECTIVE TISSUE SURROUNDING EACH FOLLICLE
ESPECIALLY THE LARGEST EXTENSIVE LYMPHATIC SPACES
LINED BY ATTENUATED ENDOTHELIAL CELLS PENETRATE THIS
STROMA &IGURE " 4HE DEVELOPING FOLLICLES MI
GRATE FROM THE GERMINAL RIDGES AND CONSTITUTE THE &/,
,)#5,!2 ,!-).! OF THE OVARIAN SHEET
!S IN MANY BONY lSHES THE LUMEN OF THESE CYS
TOVARIAN OVARIES IS LINED BY AN EPITHELIUM THAT IS
DERIVED FROM THE COELOMIC MESOTHELIUM AND IS CON
TINUOUS WITH THE OVIDUCT 4HE EPITHELIAL CELLS LIE ON A
DISTINCT BASAL LAMINA AND VARY IN SHAPE FROM SQUAMOUS
OVER THE GERMINAL RIDGE TO CUBOIDAL OR COLUMNAR OVER
MORE MATURE FOLLICLES &IGURE 4HE APICAL SURFAC
ES MAY DISPLAY MICROVILLI LATERAL SURFACES ARE HIGHLY
INTERDIGITATED AND THERE MAY BE BASAL INFOLDINGS OF THE
PLASMALEMMA "LEBS FROM THE APICAL SURFACE MAY PRO
TRUDE INTO THE LUMEN &IGURE 7ITHIN THE EPITHE
LIAL CELLS ARE ABUNDANT CYTOPLASMIC lLAMENTS AND THE
CELLS ARE ATTACHED TO ONE ANOTHER LATERALLY BY DESMO
SOMES AND APICALLY BY TIGHT JUNCTIONS
! FORM OF !0/#2).% 3%#2%4)/. HAS BEEN DESCRIBED IN
SOME OF THE COLUMNAR EPITHELIAL CELLS OF THE OVARIAN LU
MEN OF TWO OTHER SPECIES OF TELEOSTS $URING APOCRINE
SECRETION PART OF THE CELL IS LOST &OLLOWING OVULATION
IN THE MEDAKA /RYZIAS LATIPES APICAL hBLEBSv BREAK OFF
FROM THE REST OF THE CELL AND CONTRIBUTE TO THE SECRETED
MATERIAL IN THE LUMEN 4AKANO 4HERE ARE NO
MICROVILLI ON THESE SPECIAL CELLS AND IRREGULAR PROCESS
ES CONTAINING VACUOLES PRESUMABLY DERIVED FROM THE
'OLGI COMPLEX FORM ON THEIR APICAL SURFACES &IGURE
! 4HE PROCESSES BREAK OFF THEREBY FORMING THE
APOCRINE SECRETION 4HIS ACTIVITY CEASES AFTER OVULATION
AND THE CYTOPLASM OF THE EPITHELIAL CELLS BECOMES MORE
ELECTRON LUCENT !S THE OVARY MATURES IN THE GOLDlSH
#ARASSIUS AURATUS THE DORSAL EPITHELIAL CELLS DEVELOP
CILIA AND LARGE CYTOPLASMIC BLEBS BREAK AWAY FROM THE
SURFACE AT THE BASES OF THE CILIA &IGURE " 4AKA
HASHI AND 4AKANO )T IS SUGGESTED THAT THE APO
CRINE SECRETIONS CONTRIBUTE TO THE MAINTENANCE OF THE
OVULATED EGGS WITHIN THE LUMEN AND THAT THE CILIA ASSIST
IN TRANSPORTING THEM TO THE OVIDUCT
!N UNUSUAL ADAPTATION IS SEEN IN SOME SPECIES OF
3CORPAENIFORMES WHERE THE LINING OF THE HOLLOW OVARY
SECRETES A BILOBED GELATINOUS MASS THAT PROVIDES PRO
TECTION FOR THE EGGS &ISHELSON %RICKSON AND
0IKITCH +OYA (AMATSU AND -ATSUBARA
+OYA AND -ATSUBARA 4HE PAIRED CYSTOVARIAN
OVARIES ARE SHEATHED WITHIN A WALL OF SMOOTH MUSCLE
AND CONNECTIVE TISSUE AND ARE ENCLOSED BY VISCERAL
PERITONEUM 4HE OVARIAN WALLS CONVERGE CAUDALLY AS
AN OVIDUCT THAT TERMINATES BETWEEN THE URINARY PORE
AND THE ANUS !NTERIORLY THE OVARIES ARE ROUNDED AND
EACH OF THEM IS SUSPENDED BY A SPONGY VESSEL
RICH HI
LUS WHOSE VESSELS PENETRATE INTO THE LUMEN TO ENTER THE
SPONGY VASCULAR /6)'%2/53 342/-! 3USPENDED BY
THE HILUS AT THE ANTERIOR END OF EACH LOBE THE OVIGER
OUS STROMA mOATS FREE WITHIN THE LUMEN 4HE OVIGEROUS
TISSUE IS COVERED BY AN OOCYTE
PRODUCING EPITHELIUM
THAT BRISTLES WITH VASCULARIZED hPEDUNCLESv THAT RADIATE
FROM THE STROMA &IGURES ! " 4HESE PEDUNCLES
ARE EXTENSIONS OF THE STROMA AND ACCOMMODATE SEC
ONDARY OOCYTE DEVELOPMENT &IGURES # $ %ACH
OOCYTE IS ENCLOSED BY ITS AMORPHOUS ZONA PELLUCIDA
A LAYER OF FOLLICULAR CELLS AND A THECA &IGURE %
4HE LUMINAL WALL IS LINED BY A SIMPLE COLUMNAR
EPITHELIUM A MORE DELICATE SIMPLE COLUMNAR EPITHE
LIUM COVERS THE OVIGEROUS TISSUE $URING THE SPAWNING
SEASON THE EPITHELIAL CELLS OF BOTH SURFACES SECRETE THE
GELATINOUS MASS THAT lLLS THE LUMEN 4HESE COLUMNAR
CELLS INCREASE IN HEIGHT FROM VITELLOGENESIS TO MATURA
TION THEY DECLINE AFTER OVULATION 4HE GELATINOUS MASS
OCCURS IN TWO LAYERS A lBROUS /54%2 ,!9%2 OF POLY
SACCHARIDE AND LIPID AND A HOMOGENEOUS )..%2 ,!9%2
OF GLYCOLIPOPROTEIN OR PROTEOGLYCAN ASSOCIATING LIPID
4HE OUTER lBROUS LAYER IS SECRETED BY THE LARGER CO
LUMNAR %0)4(%,)!, #%,,3 /& 4(% /6!2)!. 7!,, 4HESE
CELLS CONTAIN ABUNDANT AGRANULAR ENDOPLASMIC RETICU
LUM AND RELEASE APICAL BLEBS INTO THE LUMEN &IGURES
! " 4HE COLUMNAR CELLS OF THE /6)'%2/53 %0)4(%
,)5- SECRETE THE INNER LAYER AND ARE RICH IN AGRANULAR
AND GRANULAR ENDOPLASMIC RETICULUM AND 'OLGI COM
PLEXES &IGURE # 4HEY RELEASE MATERIALS BY EXO
CYTOSIS
#(!04%2
0EDUNCLE LENGTH INCREASES AS VITELLOGENESIS PRO
CEEDS 7ITHIN THE BASE OF EACH PEDUNCLE ARE PREVITEL
LOGENIC OOCYTES WHEN A MATURE OOCYTE IS RELEASED AT
OVULATION A PREVITELLOGENIC OOCYTE MOVES UP INSIDE
THE PEDUNCLE TO TAKE ITS PLACE AND UNDERGO VITELLO
GENESIS !T OVULATION THE OOCYTES EMBEDDED IN THE
GELATINOUS MASS ARE SWEPT FROM THE LUMEN &IGURE
4HE GELATINOUS MASS SECRETED BY THE EPITHELIA
OF THE TWO LOBES IS EXTRUDED AROUND THE OVIGEROUS
TISSUE OF BOTH LOBES TO FORM THE HOLLOW BILOBED EGG
MASS 4HREE FEATURES OF THESE UNUSUAL OVARIES FACILITATE
THE PRODUCTION SHAPING AND EXPULSION OF THESE EGG
MASSES THE OVIGEROUS STROMA IS ENCIRCLED BY OOCYTES
AND CONNECTED TO THE OVARIAN WALL ONLY AT THE ANTERIOR
END OF EACH LOBE THE INNER OVARIAN WALL IS LINED WITH
SECRETORY CELLS AND VITELLOGENIC OOCYTES ARE BORNE ON
PEDUNCLES THAT EXTEND INTO THE LUMEN BECOMING EM
BEDDED IN THE GELATINOUS MASS 3IMILAR ADAPTATIONS FOR
THE PRODUCTION OF GELATINOUS EGG MASSES HAVE BEEN
DESCRIBED IN THE MASKED GREENLING (EXAGRAMMOS OC
TOGRAMMUS 3CORPAENIFORMES +OYA -UNEHARA AND
4AKANO AND THE ANGLER lSH ,OPHIOMUS SETIGERUS
,OPHIIFORMES 9ONEDA ET AL
3EVERAL MARINE COTTID SPECIES 3CORPAENIFORMES
HAVE A UNIQUE REPRODUCTIVE MODE CALLED hINTERNAL GA
METIC ASSOCIATIONv WHERE SPERMATOZOA ARE INTRODUCED
INTO THE OVARIAN CAVITY BY COPULATION AND mOAT FREELY
IN THE OVARIAN mUID ALTHOUGH FERTILIZATION DOES NOT OC
CUR UNTIL THE EGGS HAVE BEEN SPAWNED INTO SEA WATER
+OYA 4AKANO AND 4AKAHASHI +OYA -UNE
HARA AND 4AKANO 4HE LUMEN OF THE OVARIAN
CAVITY IS LINED WITH A SIMPLE MICROVILLOUS EPITHELIUM
THAT SECRETES THE OVARIAN mUID BUT DOES NOT APPEAR TO
HAVE A SPECIALIZED STRUCTURE FOR SPERM STORAGE &IGURES
! " $URING THE SPAWNING PERIOD THE EPITHELIAL
CELLS OF BOTH THE OVIGEROUS LAMELLAE AND THE LUMINAL
WALL MANIFEST THE APPEARANCE OF PROTEIN PRODUCTION
WITH ABUNDANT BASAL GRANULAR ENDOPLASMIC RETICULUM
AND ACTIVE APICAL 'OLGI COMPLEXES &IGURES # TO
% .UMEROUS PINOCYTOTIC PITS AND VESICLES ARE SEEN
IN THE PERIPHERAL CYTOPLASM OF THESE CELLS INCREASING
NUMBERS OF PITS AND VESICLES ARE ALSO PRESENT IN THE
ENDOTHELIAL CELLS OF ADJACENT CAPILLARY WALLS AT THIS
TIME INDICATING THAT ACTIVE TRANSCYTOSIS IS TAKING PLACE
&IGURE & 3UBSTANCES TRANSPORTED FROM THE CAPIL
LARIES APPEAR TO BE TAKEN INTO THE EPITHELIAL CELLS BY
ENDOCYTOSIS AND SYNTHESIZED IN THE GRANULAR ENDOPLAS
MIC RETICULUM INTO MATERIALS THAT ARE ACCUMULATED IN
THE SECRETORY VESICLES BY WAY OF THE 'OLGI COMPLEXES
TO BE RELEASED INTO THE OVARIAN CAVITY BY EXOCYTOSIS
4HESE SECRETIONS MAY BE AUGMENTED BY MICROAPOCRINE
SECRETIONS WHEREIN BLEBS ARE RELEASED FROM PROJECTIONS
OF THE APICAL SURFACES OF THE EPITHELIAL CELLS &IGURES
# % 4HIS SECRETORY ACTIVITY SHOWS DISTINCT SEA
SONAL CHANGES BEING MOST ACTIVE DURING THE SPAWN
ING PERIOD DECLINING DURING THE DEGENERATION PERIOD
TO BECOME QUIESCENT DURING THE RECOVERY PERIOD !D
JACENT EPITHELIAL CELLS ARE JOINED BY JUNCTIONAL COM
PLEXES &IGURE ' AND IT IS SUGGESTED THAT THESE
TIGHT JUNCTIONS ISOLATE THE SPERMATOZOA IN THE LUMEN
FROM THE MATERNAL IMMUNE SYSTEM !FTER THE SPAWNING
PERIOD THE JUNCTIONS BREAK DOWN AND RESIDUAL SPERMA
TOZOA ARE ELIMINATED BY INVADING MATERNAL LEUCOCYTES
PLASMA CELLS POLYMORPHONUCLEAR LEUCOCYTES AND
MONOCYTESMACROPHAGES &IGURE ( ! SUMMARY
OF THE CYCLIC CHANGES IN THESE EPITHELIAL IS SHOWN IN
&IGURE )
4HE MATURE OVARIES OF #HONDRICHTHYES ARE SUR
ROUNDED BY THE GONADAL EPITHELIUM AND CONSIST OF A
CONNECTIVE TISSUE STROMA CONTAINING DEVELOPING FOL
LICLES POSTOVULATORY FOLLICLES CORPORA LUTEA AND
DEGENERATING FOLLICLES CORPORA ATRETICA 3TANLEY
7OURMS #ALLARD ET AL (AMLETT
AND +OOB "LOOD VESSELS AND NERVES COURSE
THROUGH THE STROMA 4HE STROMA ALSO CONTAINS LYMPH
SPACES OR MEMBRANOUS FOLDS THAT ARE lLLED WITH DE
VELOPING BLOOD CELLS &IGURE !LTHOUGH OVARIAN
MORPHOLOGY IS VARIABLE IN #HONDRICHTHYES DIFFERENCES
ARE SUPERlCIAL AND ATTRIBUTABLE LARGELY TO THE NUMBERS
AND SIZES OF THE YOLKY EGGS PRESENT 4E7INKEL
$ODD #ALLARD ET AL 6ARIATIONS ARE RE
LATED NOT ONLY TO THE STAGE OF THE REPRODUCTIVE CYCLE
BUT ALSO TO THE MODE OF REPRODUCTION OF THE SPECIES
WHETHER OVIPAROUS OR VIVIPAROUS 6ITELLOGENIC OOCYTES
DOMINATE THE GROSS APPEARANCE OF THE OVARY OF REPRO
DUCTIVELY ACTIVE FEMALES #ALLARD ET AL !FTER
OVULATION THE VOLUME OF THE OVARY IS GREATLY REDUCED
AND IT CONTAINS ONLY SMALLER FOLLICLES CORPORA LUTEA
AND CORPORA ATRETICA
9ELLOWISH IRREGULAR MASSES OF HAEMOPOIETIC TISSUE
THE %0)'/.!, /2'!.3 ARE ASSOCIATED WITH THE GONADS OF
ELASMOBRANCHS &IGURES AND &NGE
&NGE AND -ATTISSON :APATA &NGE AND
0ULSFORD :APATA ET AL !LTHOUGH SOME
TIMES REDUCED TO THE POINT THAT THEY ARE DETECTABLE ONLY
BY MICROSCOPIC EXAMINATION THEY HAVE BEEN FOUND IN
ALL SPECIES EXAMINED 4HEY OCCUR IN THE MESOVARIUM
AND IN YOUNG SPECIMENS OF 3CYLIORHINUS CANICULA
ARE SAID TO SURROUND THE OVARY !GGREGATIONS OF HAE
MOPOIETIC TISSUE IN THE OVARIAN STROMA OF SOME ELAS
&%-!,% '%.)4!, 3934%-3 /& &)3(
MOBRANCHS ARE PROBABLY RUDIMENTARY EPIGONAL ORGANS
&IGURE &NGE )N THE BASKING SHARK
#ETORHINUS MAXIMUS WHERE ONLY THE RIGHT OVARY PER
SISTS THE EPIGONAL ORGAN LIES POSTERIOR AND SLIGHTLY
DORSAL TO THE OVARY BEING SUSPENDED FROM THE DORSAL
ABDOMINAL WALL BY A BACKWARD EXTENSION OF THE MES
OVARIUM &IGURE -ATTHEWS 4HE LEFT EPI
GONAL ORGAN IS OF SIMILAR SIZE AND SHAPE AS THE RIGHT BUT
NO OVARY IS FUSED TO ITS ANTERIOR END AND IT IS SUSPENDED
BY ITS OWN PERITONEAL FOLD IN THE CORRESPONDING POSI
TION ON THE LEFT SIDE OF THE BODY CAVITY &IGURE
.O HAEMOPOIETIC TISSUE IS ASSOCIATED WITH THE URINO
GENITAL SYSTEM OF THE HOLOCEPHALAN (YDROLAGUS COLLIEI
3TANLEY
#(!04%2
&IGURE /VARIES AND TESTES DEVELOP FROM PAIRED MASSES OF MESODERMAL TISSUE ON EITHER SIDE OF THE DORSAL MESENTERY IN
THE DORSOLATERAL LINING OF THE PERITONEAL CAVITY 4HESE INDIFFERENT GENITAL RIDGES BULGE INTO THE DEVELOPING COELOM AND ARE LATER
INVADED BY PRIMORDIAL GERM CELLS ARROWS THAT WILL EVENTUALLY GIVE RISE TO OOGONIA OR SPERMATOGONIA 3IX STAGES OF THIS MIGRA
TION ARE SHOWN IN THESE PHOTOMICROGRAPHS OF CROSS SECTIONS OF EMBRYOS /RYZIAS LATIPES "AR M &ROM (AMAGUCHI
REPRODUCED WITH PERMISSION OF THE AUTHOR
! 0RIMORDIAL GERM CELLS 0'#S SHOWN IN THE PERIPHERAL ENDODERM
" 4HE 0'#S LIE ALONGSIDE THE NEWLY
FORMED GUT
# 4HE 0'#S COME TOGETHER BETWEEN THE LATERAL PLATE MESODERM AND ECTODERM !S THE LATERAL PLATE MESODERM DIFFERENTIATES
INTO SPLANCHNIC AND SOMATIC MESODERM THE 0'#S MIGRATE THROUGH THE SOMATIC MESODERM TO THE DORSAL MESENTERY
$ 3OME GERM CELLS HAVE REACHED THE GONADAL REGION OTHERS ARE IN THE SOMATIC MESODERM
% !LL GERM CELLS HAVE ARRIVED IN THE GONADAL ANLAGE BETWEEN THE PRONEPHRIC DUCT AND THE GUT
& /NE OF THE GERM CELLS IS UNDERGOING MITOSIS
!BBREVIATIONS N NEURAL TUBE M MESODERM ENT ENTODERM G GUT P PRONEPHRIC DUCT
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE %LECTRON MICROGRAPHS OF CROSS SECTIONS THROUGH THE DEVELOPING GONAD OF THE EEL !NGUILLA ANGUILLA CONTAINING
PRIMORDIAL GERM CELLS 0'# ENVELOPED BY SOMATIC CELLS 3# 4HE GONAD IS ENCLOSED BY PERITONEAL EPITHELIUM 0%# '0%
FORMED OF mATTENED CELLS ON THE MEDIAL SIDE -3 AND THICKER CELLS ON THE LATERAL SIDE ,3 ! CM ELVER 8 " CM
EEL 8 &ROM 'RANDI AND #OLOMBO REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
#(!04%2
&%-!,% '%.)4!, 3934%-3 /& &)3(
@
&IGURE $IAGRAMMATIC REPRESENTATION OF THE GERMINAL EPITHELIUM AND THE PROCESS OF OOGENESIS FROM A SINGLE OOGONIUM
IN THE COMMON SNOOK #ENTROPOMUS UNDECIMALIS 'ERM CELLS ARE YELLOW AND ORANGE EPITHELIAL PREFOLLICLE CELLS AND FOLLICLE CELLS
ARE BLUE CELLS WITHIN THE STROMA ARE GREEN THE BASEMENT MEMBRANE IS RED 4HE GERMINAL EPITHELIUM EXTENDS BETWEEN THE BASE
MENT MEMBRANE "- AND THE OVARIAN LUMEN /, )T IS COMPOSED OF SOMATIC CELLS EPITHELIAL CELLS % WHICH BECOME PREFOL
LICLE CELLS 0& DURING FOLLICULOGENESIS AND GERM CELLS OOGONIA /' AND PACHYTENE 0 AND DIPLOTENE OOCYTES /OGONIA MAY
DIVIDE MITOTICALLY TO MAINTAIN THEIR POPULATION WITHIN THE GERMINAL EPITHELIUM MITOSIS ARROWS 4HEY MAY ENTER INTO MEIOSIS
BECOMING OOCYTES AND MOVE AWAY FROM THE OVARIAN LUMEN !T THE INITIATION OF MEIOSIS THE PROCESS OF FOLLICULOGENESIS COM
MENCES MEIOSIS ARROWS &OLLICULOGENESIS IS COMPLETED WHEN THE BASEMENT MEMBRANE EXTENDS UP OVER THE FORMING FOLLICLE ITS
DIPLOTENE OOCYTE AND PREFOLLICLE CELLS AND PINCHES THE FOLLICLE OFF FROM THE GERMINAL EPITHELIUM 0REFOLLICULAR CELLS THEN BECOME
FOLLICULAR CELLS & 7HILE WITHIN THE GERMINAL EPITHELIUM OR ATTACHED TO A CELL NEST THE OOCYTE PRIMARY GROWTH PHASE COM
MENCES WHEN 2.!
RICH CYTOPLASM 2# BEGINS TO APPEAR DURING DIPLOTENE 2.! CONTINUES TO ACCUMULATE AS BOTH THE NUCLEAR
AND CYTOPLASMIC VOLUMES INCREASE AFTER COMPLETION OF FOLLICULOGENESIS COUPLED WITH THE APPEARANCE OF MULTIPLE NUCLEOLI .5
AND THEIR lNAL ORIENTATION AROUND THE PERIPHERY OF THE NUCLEUS . PERINUCLEOLAR STAGE &OLLICULOGENESIS IS COMPLETE BEFORE THIS
STAGE OF MATURATION IS REACHED "ESIDE AN 2.!
RICH CYTOPLASM MITOCHONDRIA - AND OTHER CELLULAR ORGANELLES BEGIN TO APPEAR
IN THE OOCYTE CYTOPLASM 4HE FOLLICLE IS COMPOSED OF THE DIPLOTENE OOCYTE AND AN ENCOMPASSING LAYER OF FOLLICULAR CELLS )T IS
SEPARATED FROM THE STROMA BY A BASEMENT MEMBRANE )N THE STROMA PRETHECAL CELLS 04 WITHIN THE EXTRAVASCULAR SPACE %63
ASSOCIATE WITH THE FOLLICLE AND FORM THE THECA INTERNA $URING PRIMARY GROWTH UNDIFFERENTIATED CELLS WITHIN THE %63 ASSOCIATE
WITH THE SURFACE OF THE THECA 4HEY DIFFERENTIATE INTO A THECA EXTERNA 4% "LOOD VESSELS "6 ALSO RESIDE WITHIN THE %63 &ROM
'RIER REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
@
&IGURE 0RIMORDIAL GERM CELLS 0'# ARISE EARLY IN DEVELOPMENT WITHIN EMBRYONIC ENDODERM END OR MESODERM MES
LONG BEFORE THE RUDIMENTS OF THE GONADS ARE FORMED AND AT A DISTANCE FROM THE SITE THEY WILL EVENTUALLY OCCUPY 0HOTOMICRO
GRAPHS OF CROSS SECTIONS AT THE LEVEL OF THE ANTERIOR SOMITES THROUGH
HOUR EMBRYOS OF "ARBUS CONCHIONUS &ROM 4IMMER
MANS AND 4AVERNE REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 8
" 8
!BBREVIATIONS CH CHORDA MESODERM ECT ECTODERM EVL ENVELOPING LAYER P PERIBLAST Y YOLK
#(!04%2
&IGURE 4HE SITE OF ORIGIN OF PRIMORDIAL GERM CELLS IS EXTRAGONADAL AND IN SOME lSHES MAY BE EXTRAEMBRYONIC
4HESE CELLS MIGRATE INTO THE RUDIMENTARY GONAD AND ESTABLISH RESIDENCE IN THE OUTER MARGIN OF THE STROMA JUST BENEATH THE
GONADAL EPITHELIUM 4HESE ARE SCHEMATIC DRAWINGS OF SECTIONS THROUGH THE CARP #YPRINUS CARPIO SHOWING MALE AND FEMALE
GONADS DURING DEVELOPMENT &ROM 0ARMENTIER AND 4IMMERMANS REPRODUCED WITH PERMISSION FROM THE #OMPANY OF
"IOLOGISTS ,TD
! )NDIFFERENT GONAD AT WEEKS
" -ALE GONAD AT WEEKS
# &EMALE GONAD AT WEEKS
!BBREVIATIONS BV BLOOD VESSEL CC CYST CELL EPO EARLY PROPHASE OOCYTES IT INTERSTITIAL TISSUE /O OOGONIA M0'# MITOTIC
PRIMORDIAL GERM CELL SG SPERMATOGONIA
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE 0RIMORDIAL GERM CELLS ARE ENSHEATHED BY CELLS DERIVED FROM THE GONADAL EPITHELIUM 3CHEMATIC DRAWINGS OF
CROSS SECTIONS THROUGH GONADAL PRIMORDIA OF THE COMMON CARP #YPRINUS CARPIO AT AND WEEKS &ROM VAN 7INKOOP ET AL
REPRODUCED WITH PERMISSION FROM 3PRINGER
6ERLAG
! )N THE lRST WEEK THE PRIMARY GERM CELL IS ENCLOSED BY EXTENSIONS OF ONE OR TWO SOMATIC CELLS THESE FORM JUNCTIONAL COM
PLEXES AT THE SIDE OF THE COELOMIC CAVITY BUT NOT AT THE DORSAL SIDE 4HE OUTLINED AREA IS SHOWN IN &IGURE $
" "Y THE THIRD WEEK THE NUMBER OF SOMATIC CELLS SURROUNDING THE PRIMARY GERM CELL HAS INCREASED 4HE OUTLINED AREA IS SHOWN
IN &IGURE %
# )N THE lFTH WEEK A CENTRAL LAYER OF LIGHTER CELLS LOCATED CLOSE TO THE PRIMARY GERM CELLS IS SURROUNDED BY A LAYER OF DARKER
PERIPHERAL CELLS 4HE UPPER OUTLINED AREA IS SHOWN IN &IGURE & AND THE LOWER AREA IS SHOWN IN &IGURE (
#(!04%2
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE #ONTINUED
&IGURES $ TO ( ARE ELECTRON MICROGRAPHS OF CROSS SECTIONS THROUGH PRIMARY GERM CELLS AND GONADAL PRIMORDIA
$ !T DAYS A PRIMARY GERM CELL IS ENVELOPED BY DORSAL EXTENSIONS OF A SOMATIC CELL SO 0ART OF THE NUCLEUS N IS SHOWN
0ERINUCLEAR DENSE BODIES 0$" LOCATED NEAR NUCLEAR PORES PO ARE ASSOCIATED WITH MITOCHONDRIA M 4HE CYTOPLASM
CONTAINS AGRANULAR ENDOPLASMIC RETICULUM %2 "AR M
% ! PRIMARY GERM CELL AT WEEKS CONTAINS LIGHT L AND DARK D MATERIAL THE LATTER ADHERES TO A MITOCHONDRION M .OTE
JUNCTIONAL COMPLEXES ARROWS BETWEEN THE EXTENSIONS OF SOMATIC CELLS SO 4HE NUCLEUS N IS AT THE LEFT "AR M
& UPPER OUTLINE IN &IGURE # 0RIMARY GERM CELL AT WEEKS $ARK CEMENT CM IS ASSOCIATED WITH MITOCHONDRIA M ,ONG
AGRANULAR CISTERNAE OF THE ENDOPLASMIC RETICULUM %2 LIE PARALLEL TO THE CELL MEMBRANE 4HE NUCLEUS N IS AT THE LEFT
"AR M
' ! PRIMARY GERM CELL 0'# ENVELOPED BY SOMATIC CELLS AT WEEKS 4HE NUCLEUS OF THE PRIMARY GERM CELL IS NOT VISIBLE
4HE LIGHTER CENTRAL SOMATIC CELLS C ARE SURROUNDED BY DARKER PERIPHERAL CELLS P "AR M
( LOWER OUTLINE IN &IGURE # %NVELOPING SOMATIC CELLS AT WEEKS "OTH THE LIGHTER CENTRAL CELLS C AND THE PERIPHERAL CELLS
P REST ON BASEMENT MEMBRANES BM WITH CONNECTIVE TISSUE BETWEEN "AR M
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF PRIMORDIAL GERM CELLS OF /RYZIAS LATIPES &ROM (AMAGUCHI REPRO
DUCED WITH PERMISSION OF THE AUTHOR
! 0RIMARY GERM CELLS G ARE LARGER THAN SURROUNDING CELLS ARE ROUNDED OVAL OR PEAR SHAPED AND SHOW A DISTINCT CELL BOUND
ARY 4HEY ARE SURROUNDED BY SOMATIC CELLS M RICH IN RIBOSOMES 0RONEPHRIC DUCT P "AR M
" -ESODERMAL CELLS SURROUND THE PRIMORDIAL GERM CELL GDB 4HE NUCLEAR MATERIAL IS HOMOGENEOUS 4HERE IS A LARGE ROUND
CONSPICUOUS NUCLEOLUS 4HE SURROUNDING SOMATIC CELLS ARE RICHER IN RIBOSOMES "AR M
&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF PRIMORDIAL GERM CELLS OF THE EEL !NGUILLA ANGUILLA &ROM 'RANDI AND #O
LOMBO REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! ! PRIMORDIAL GERM CELL HAS A NUCLEUS .' WITH IRREGULAR OUTLINE A FEW LONG CISTERNAE OF ENDOPLASMIC RETICULUM %2
hNUAGEv N A CLUSTER OF MITOCHONDRIA - IN THE CYTOPLASM COATED PITS ARROW AND MICROVILLOUS EXTENSIONS -V OF THE
BORDER !N ENVELOPING SOMATIC CELL HAS A mATTENED NUCLEUS .% AND MANY BUNDLES OF MICROlLAMENTS IN THE CYTOPLASM .OTE
THE DESMOSOME $ BETWEEN THE PRIMORDIAL GERM CELL AND THE SOMATIC CELL 8
" $ETAILS OF A PRIMORDIAL GERM CELL SHOWING A 'OLGI COMPLEX ' CENTRIOLE #T AND OTHER ORGANELLES ,ABELLING AS IN &IGURE
! 8
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE %LECTRON MICROGRAPH OF A SECTION THROUGH THE CYTOPLASM OF A PRIMORDIAL GERM CELL OF THE CARP #YPRINUS CARPIO OF
WEEKS /NE COATED VESICLES CV VESICLE HAS FUSED WITH THE PLASMA MEMBRANE AND OPENS INTO THE NARROW INTERCELLULAR SPACE AD
JACENT TO A SOMATIC CELL SO "AR M &ROM VAN 7INKOOP ET AL REPRODUCED WITH PERMISSION FROM 3PRINGER
6ERLAG
&IGURE %LECTRON MICROGRAPH OF A SECTION OF THE INDIFFERENT GONAD OF THE GENITAL RIDGE OF /RYZIAS LATIPES 4WO CYTO
PLASMIC MARKERS DISTINGUISH PRIMORDIAL GERM CELLS FROM SOMATIC CELLS 0N 4HESE ARE THIN SHEETS OF AGRANULAR ENDOPLASMIC
RETICULUM ARROWS AND ELECTRON
DENSE MITOCHONDRIAL ASSOCIATED GRANULAR MATERIAL -!'- 8 &ROM (OGAN
REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
#(!04%2
&IGURE 4HESE ELECTRON MICROGRAPHS SHOW CHANGES IN THE APPEARANCE OF MITOCHONDRIAL ASSOCIATED GRANULAR MATERIAL IN
PREMIGRATORY GERMINAL CELLS OF /RYZIAS LATIPES AS THE CELLS BEGIN THEIR MIGRATION TO THE GONADAL ANLAGEN 8 &ROM (AMA
GUCHI REPRODUCED WITH PERMISSION OF THE AUTHOR
! !S THE CELLS BEGIN THEIR MIGRATION THE MATERIAL IS LOOSELY WOVEN AND STRANDLIKE
" 4HIS APPEARANCE GRADUALLY CHANGES AS A SMALL AMORPHOUS MAT OF lNE ELECTRON DENSE lBRILS FORMS
# 4HE AMORPHOUS MAT BECOMES DOMINANT
$ 4HE MATERIAL HAS BECOME AN AMORPHOUS BODY OF lNE ELECTRON DENSE lBRILS )N THE GONADAL ANLAGEN THESE BODIES ARE AMOR
PHOUS OF VARIOUS SIZES AND SHAPES "AR M
&IGURE )N THE CARP #YPRINUS CARPIO THE MITOCHONDRIAL ASSOCIATED GRANULAR MATERIAL INCREASES IN SIZE WITH DEVELOPMENT
AND PART BECOMES MORE ELECTRON DENSE FORMING DARK MASSES THAT ADHERE TO MITOCHONDRIA AND MAY BE CENTRES FOR MITOCHONDRIAL
MULTIPLICATION "AR M &ROM VAN 7INKOOP ET AL REPRODUCED WITH PERMISSION FROM 3PRINGER
6ERLAG
! ! PRIMORDIAL GERM CELL AT DAYS SHOWING PART OF THE NUCLEUS N 4HE CYTOPLASM CONTAINS AGRANULAR ENDOPLASMIC RETICULUM
%2 ! DENSE BODY 0$" AND ASSOCIATED MITOCHONDRION M LIES NEAR A NUCLEAR PORE PO 3URFACE MEMBRANE OF PRIMORDIAL
GERM CELL PL DORSAL EXTENSION OF ENVELOPING SOMATIC CELL SO
" 4WO TYPES OF DENSE MATERIAL ARE SEEN IN PRIMORDIAL GERM CELLS AT WEEKS LIGHT L AND DARK D THE LATTER ADHERING TO A
MITOCHONDRION M !T THE RIGHT JUNCTIONAL COMPLEXES ARROWS LINK EXTENSIONS OF THE SURROUNDING SOMATIC CELLS
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE 4HE OVARIES ARE SUSPENDED IN THE POSTERIOR BODY CAVITY DORSAL TO THE GUT BY MESOVARIA THAT RUN THEIR ENTIRE
LENGTH $IAGRAMMATIC CROSS SECTIONS THROUGH THE BODY OF AN ADULT FEMALE SHARK 3CYLIORHINUS CANICULA 8 &ROM -ETTEN
REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
! 3ECTION THROUGH THE POSTERIOR END OF THE STOMACH
" 3ECTION THROUGH THE DUODENUM
&IGURE 4HE OVARIES ' MAY BE DISPLACED TOWARD THE INTESTINE COMING TO LIE WITH THE INTESTINE $ WITHIN THE MESEN
TERY &ROM (ARDER REPRODUCED WITH PERMISSION OF 3CHWEIZERBARTSCHE 6ERLAGSBUCHHANDLUNG WWWSCHWEIZERBARTDE
#(!04%2
&IGURE )N ELASMOBRANCHS A DUCT SYSTEM TYPICAL OF HIGHER VERTEBRATES DEVELOPS FROM THE MESONEPHRIC OR -LLERIAN
DUCTS GATHERING UP SHED EGGS OR EMBRYOS IN A FUNNEL
SHAPED /34)5- AND PASSING THEM THROUGH AN /6)$5#4 TO THE OUTSIDE OFTEN
ADDING A SHELL OR PROVIDING REFUGE FOR DEVELOPING EMBRYOS ALONG THE WAY &ROM (OAR REPRODUCED WITH PERMISSION FROM
%LSEVIER 3CIENCE
&IGURE !LTHOUGH THE OVARIES OF MOST ELASMOBRANCHS ARE SOLID THE VISCERAL PERITONEAL COVERING OF THE OVARY OF LAMNID
SHARKS INVAGINATES TO CREATE A HOLLOW ORGAN 4HE HOLLOW IS A DIRECT EXTENSION OF THE PERITONEAL CAVITY AND FORMS A BRANCHING
INVAGINATION FROM A POCKET ON THE RIGHT SIDE OF THE OUTER SURFACE 3HOWN IS THE RIGHT OVARY AND EPIGONAL ORGAN SEEN FROM THE
RIGHT SIDE OF THE BASKING SHARK #ETORHINUS MAXIMUS /NLY THE RIGHT OVARY PERSISTS AND THE EPIGONAL ORGAN LIES POSTERIOR AND
SLIGHTLY DORSAL TO THE OVARY BEING SUSPENDED FROM THE DORSAL ABDOMINAL WALL BY A BACKWARD EXTENSION OF THE MESOVARIUM
4HE POCKET LEADING TO THE INTERIOR IS VISIBLE ON THE RIGHT SIDE &ROM -ATTHEWS REPRODUCED WITH PERMISSION FROM THE
2OYAL 3OCIETY
&IGURE #HANNELS PENETRATE ALL PARTS OF THE OVARY AND PROVIDE A MEANS OF EXIT FOR RIPE OOCYTES 0OSTERIOR VIEW OF
THE OVARY OF A MATURE LAMNID SHARK 4HE LEFT ILLUSTRATION IS DIAGRAMMATIC THE RIGHT IS SCHEMATIC !RROWS INDICATE PATHS OF
THE OOCYTES &ROM 0RATT REPRODUCED WITH PERMISSION OF THE !MERICAN 3OCIETY OF )CHTHYOLOGISTS AND (ERPETOLOGISTS
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE 4HE CAVITY OF CYSTOVARIAN OVARIES MAY BE FORMED IN TWO WAYS &ROM 7EICHERT REPRODUCED WITH PERMIS
SION OF THE -C'RAW (ILL #OMPANIES
! !N ENDOVARIAN CAVITY IS DERIVED FROM INTERNALIZED INVAGINATIONS OF THE GENITAL RIDGES WHERE THE RIBBONLIKE OVARIES ROLL UP IN
A LATERAL AND DORSAL DIRECTION SO THAT THE SIDE AT WHICH OVULATION OCCURS IS TURNED INWARD SURROUNDING THE CAVITY
" !LTERNATIVELY A PAROVARIAN CAVITY ARISES FROM A SPACE ENCLOSED BY ADHESIONS BETWEEN THE GENITAL RIDGE AND THE PARIETAL
PERITONEUM
&IGURE 3TEROID PRODUCING CELLS ARE DESCRIBED IN THE OVARY OF TILAPIA 3AROTHERODON NILOTICUS DURING OVARIAN DIFFERENTIA
TION !S THE OVARIAN CAVITY IS FORMING THESE CELLS APPEAR NEAR THE BLOOD VESSELS OF THE STROMA ON THE SIDE FACING THE MESENTERY
4HESE PHOTOMICROGRAPHS OF CROSS SECTIONS OF THE OVARY SHOW MANY STEROID PRODUCING CELLS NEAR THE BLOOD VESSELS &ROM .AKA
MURA AND .AGAHAMA REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! DAYS AFTER HATCHING 3TERIOID PRODUCING CELLS AT CENTRE LEFT 0REMEIOTIC OOCYTE O 8
" DAYS AFTER HATCHING 3TEROID PRODUCING CELLS NEAR CENTRE /OCYTE A 8
#(!04%2
&IGURE 3TEROID PRODUCING CELLS ARE PRESUMED TO ORIGINATE FROM STROMAL ELEMENTS AND AS THE OVARY DEVELOPS THEIR NUM
BERS INCREASE SURROUNDING THE BLOOD VESSELS 4HIS ELECTRON MICROGRAPH OF A SECTION OF A STEROID PRODUCING CELL FROM THE OVARY OF
TILAPIA 3AROTHERODON NILOTICUS DAYS AFTER HATCHING SHOWS THE TUBULAR MITOCHONDRIAL CRISTAE AND TUBULAR AGRANULAR ENDOPLASMIC
RETICULUM WHICH ARE CHARACTERISTIC OF STEROID PRODUCTION 8 &ROM .AKAMURA AND .AGAHAMA REPRODUCED WITH
PERMISSION FROM "LACKWELL 0UBLISHING
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE 0HOTOMICROGRAPHS OF CROSS SECTIONS OF THE GONAD OF DEVELOPING TILAPIA 3AROTHERODON NILOTICUS )T IS SUGGESTED
THAT THE STEROIDS PRODUCED BY STEROID
PRODUCING CELLS PLAY A ROLE IN THE FORMATION OF THE OVARIAN LUMEN AND IN THE DIFFERENTIATION
OF GERM CELLS &ROM .AKAMURA AND .AGAHAMA REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! )NDIFFERENT GONAD DAYS AFTER HATCHING ! GERM CELL G IS SURROUNDED BY A FEW STROMAL CELLS 8
" /VARY DAYS AFTER HATCHING 3TEROID
PRODUCING CELLS ARE SEEN NEAR THE BLOOD VESSELS 3TROMAL AGGREGATIONS SA LARGE ARROW
IN THE PROXIMAL AND DISTAL REGION REPRESENT THE INITIAL FORMATION OF THE OVARIAN CAVITY 'ERM CELLS ARE NOT SEEN 8
# /VARY DAYS AFTER HATCHING SHOWING STROMAL AGGREGATIONS LARGE ARROWS CYSTS CONTAINING OOGONIA AND OOCYTES O AND
STEROID
PRODUCING CELLS SMALL ARROWS 8
$ /VARY DAYS AFTER HATCHING SHOWING SEVERAL OOCYTES A IN THE PERINUCLEOLUS STAGE AND NUMEROUS STEROID
PRODUCING CELLS
NEAR BLOOD VESSELS ARROWS /VARIAN CAVITY OC 8
#(!04%2
&IGURE )N MANY TELEOSTS THE VISCERAL PERITONEUM COVERING THE OVARY AND THE PERITONEUM LINING ITS CAVITY OFTEN CONTINUE
POSTERIORLY BEYOND THE MASS OF OVARIAN TISSUE TO FORM THE UNIQUE OVIDUCT 4HIS EXTENSION OF THE OVARIAN CAVITY CONTINUES POS
TERIORLY TO CONNECT WITH THE GENITAL PORE LEADING TO THE EXTERIOR !FTER 'IERSBERG AND 2IETSCHEL
!BBREVIATIONS ' GENITAL PORE / OVIDUCT 0P PARIETAL PERITONEUM LINING OVARIAN CAVITY 0V VISCERAL PERITONEUM COVERING
OVARY
&IGURE 0HOTOMICROGRAPH OF A SECTION OF THE OVARY OF A SEXUALLY MATURE GOLDlSH #ARASSIUS AURATUS 4HE VERTEBRATE
OVARY IS AN AGGREGATION OF DEVELOPING FOLLICLES ENMESHED IN A VASCULAR STROMA OF LOOSE CONNECTIVE TISSUE AND ENCLOSED WITHIN AN
ENVELOPE OF GONADAL EPITHELIUM 4HE STROMA CONSISTS OF COLLAGENOUS ELASTIC AND RETICULAR lBRES AND BECOMES GREATLY DISTENDED
AS THE FOLLICLES ENLARGE 4HE CLEAR SPACES IN THE STROMA ARE THE RESULT OF INEVITABLE SHRINKAGE 8 &ROM #OTELLI ET AL
REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
!BBREVIATIONS A PREVITELLOGENIC OOCYTES B VITELLOGENIC OOCYTE
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE "ENEATH THE OVARIAN ENVELOPE A CONDENSATION OF STROMAL TISSUE FORMS THE CAPSULE OR TUNICA ALBUGINEA 4HIS ELEC
TRON MICROGRAPH OF THE WELL DEVELOPED CAPSULE OF THE OVARY OF &UNDULUS HETEROCLITUS SHOWS ABUNDANT COLLAGEN # AND SMOOTH
MUSCLE 3- )NNER EPITHELIOID CELLS %3 OF THE STROMA LINE THE STROMAL SPACE 30 8 &ROM "RUMMETT $UMONT AND
,ARKIN REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 0HOTOMICROGRAPH OF A SECTION OF AN OVARIAN FOLLICLE OF THE BROOK STICKLEBACK %UCALIA INCONSTANS STAINED WITH
SILVER TO SHOW THE hBASKETv OF RETICULAR lBRES SURROUNDING AN EARLY OOCYTE 8 &ROM "RAEKEVELT AND -C-ILLAN
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
#(!04%2
@
&IGURE %ARLY FOLLICLES CONSIST OF PRIMORDIAL GERM
CELLS NEWLY ARRIVED BY MIGRATION ENCLOSED WITHIN A CLUS
TER OF FOLLICULAR CELLS DERIVED FROM DIVISIONS OF THE GONADAL
EPITHELIAL CELLS 0RIMORDIAL GERM CELLS IN THE OVARY OF THE EEL
!NGUILLA ANGUILLA DIVIDE BY MITOSIS TO PRODUCE DIPLOID OO
GONIA /NE GERM CELL IS IN METAPHASE M0'# ANOTHER IS
IN PROPHASE P0'# %LECTRON MICROGRAPH 8 &ROM
'RANDI AND #OLOMBO REPRODUCED WITH PERMISSION
OF *OHN 7ILEY 3ONS )NC
!BBREVIATIONS CH #HROMOSOMES CF BUNDLE OF COLLAGEN l
BRILS D0'# DEGENERATING GERM CELL '0% GONADAL PERITO
NEAL EPITHELIUM 0'#
SECONDARY PRIMORDIAL GERM CELL
@
&IGURE /OGONIA FORM DIPLOID PRIMARY OOCYTES BY
MITOTIC DIVISION -EIOTIC DIVISION OF A PRIMARY OOCYTE IN THE
OVARY RESULTS IN A SECONDARY OOCYTE AND lRST POLAR BODY BOTH
DIPLOID 4HIS SECTION OF THE OVARY OF THE EEL !NGUILLA AN
GUILLA SHOWS A CYST OF SYNCHRONIZED MEIOTIC OOCYTES IN THE
ZYGOTENE STAGE ALL CONNECTED BY CYTOPLASMIC BRIDGES )"
4HE CYST IS ENVELOPED BY mATTENED SOMATIC CELLS 3# AND IS
SEPARATED BY A BASAL LAMINA ", FROM THE STROMA 4HE OO
CYTE NUCLEI CONTAIN A NUCLEOLUS NU AND SYNAPTONEMAL COM
PLEXES 3YC WITH CHROMATIN ATTACHED TO THE LATERAL ELEMENTS
'0% GONADIC PERITONEAL EPITHELIUM %LECTRON MICROGRAPH
8 &ROM 'RANDI AND #OLOMBO REPRODUCED
WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE 3OME EPITHELIAL CELLS WHOSE PROCESSES ENVELOP MEIOTIC OOCYTES TRANSFORM INTO PREFOLLICULAR CELLS WHICH BE
COME FOLLICULAR CELLS AT THE COMPLETION OF FOLLICULOGENESIS %LECTRON MICROGRAPHS OF THE OVARY OF THE COMMON SNOOK #ENTROPO
MUS UNIDECIMALIS &ROM 'RIER REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE STRATIlED GERMINAL EPITHELIUM EXTENDS BETWEEN THE OVARIAN LUMEN /, AND THE BASEMENT MEMBRANE ARROWHEADS AND
IS COMPOSED OF EPITHELIAL CELLS % A CELL NEST OF MEIOTIC OOCYTES IN THE PACHYTENE STAGE AND A DIPLOTENE OOCYTE $/ NEAR
THE BASEMENT MEMBRANE 0ACHYTENE OOCYTES HAVE SYNAPTONEMAL COMPLEXES S NUCLEOLI NU PERHAPS MULTIPLE NUCLEOLI
ARROWS PROMINENT 'OLGI BODIES G AND NUAGE N SURROUNDED BY MITOCHONDRIA 4HE SINGLE OOCYTE IN DIPLOTENE $/ IS
BEING ENCOMPASSED BY PREFOLLICULAR CELLS 0& WITH PLEIOMORPHIC NUCLEI
.EWLY FORMED DIPLOTENE OOCYTES HAVE A PROMI
NENT NUCLEOLUS AND LACK BASOPHILIC CYTOPLASM 4HE EXTRAVASCULAR SPACE %63 IS NEARLY OCCLUDED BY PRETHECAL CELLS 04 AND
A CAPILLARY IS OBSERVED WITH A SINGLE RED BLOOD CELL 2"# ! NEST OF OOCYTES /. IS SEEN AT THE LOWER LEFT "AR M
" %PITHELIAL CELLS OF THE GERMINAL EPITHELIUM % BORDER THE OVARIAN LUMEN /, AND ENCOMPASS AN OOCYTE /% ISOLAT
ING IT FROM THE LUMEN /OCYTES WITH BASOPHILIC CYTOPLASM /" AND OOCYTES WITHOUT / ARE CONTAINED WITHIN A CELL NEST
STILL ATTACHED TO THE GERMINAL EPITHELIUM 4HE BASEMENT MEMBRANE "- IS CONTINUOUS OVER THE SURFACE OF THE NEST AND
ALSO THE BASE OF THE GERMINAL EPITHELIUM ARROWS 0RETHECAL CELLS 04 LIE WITHIN THE INTERSTITIUM .UAGE N IS PRESENT IN
THE SMALLER OOCYTES )N THE NUCLEUS OF A LARGER OOCYTE WITH BASOPHILIC CYTOPLASM GRANULAR MATERIAL DENOTING 2.! SYN
THESIS ARROWHEAD IS PRESENT BETWEEN THE NUCLEOLUS AND NUCLEAR MEMBRANE THE NUCLEUS IS RINGED BY MITOCHONDRIA M
4HESE OOCYTES ARE NOT YET ENCLOSED WITHIN A FOLLICLE ALTHOUGH PREFOLLICULAR CELLS
MAY COMPLETELY ENCOMPASS THEM
"AR M
#(!04%2
&IGURE #ONTINUED
# 5PPER LEFT ! PORTION OF AN OOCYTE NEST /NE DIPLOTENE OOCYTE WITH BASOPHILIC CYTOPLASM /" SURROUNDED BY PREFOLLICULAR
CELLS 0& IS BECOMING A FOLLICLE 0REFOLLICULAR CELLS ALSO SURROUND THE NEST WHERE OOCYTES / ARE IN CONTACT WITH EACH OTHER
4HESE OOCYTES DISPLAY PROMINENT NUCLEOLI NU VESICULAR MITOCHONDRIA M AND 'OLGI BODIES G ! PRETHECAL CELL 04 LIES
BETWEEN THE BASEMENT MEMBRANES OF THE FORMING FOLLICLE AND CELL NEST "AR M 5PPER RIGHT !N ENLARGEMENT OF THE
PRETHECAL CELL 04 4HE BASEMENT MEMBRANE EXTENDS BETWEEN THE LAYERS OF FOLLICULAR CELLS & THAT SURROUND THE OOCYTE /
AND THE PREFOLLICULAR CELLS 0& AROUND THE OOCYTE NEST 0ROCESSES FROM THE PRETHECAL CELLS DO NOT PENETRATE BETWEEN THESE
BASEMENT MEMBRANES ARROWHEADS "AR M ,OWER 0ORTIONS OF THREE FOLLICLES EACH CONTAINING A BASOPHILIC OOCYTE
/" ENCOMPASSED BY FOLLICULAR CELLS & "ASEMENT MEMBRANES ARROWS SEPARATE THE FOLLICLES FROM THE THECA INTERNA %63
EXTRAVASCULAR SPACE "AR M
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE -ICROGRAPHS OF SECTIONS OF THE OVARIAN COR
TEX OF
TO
CM EMBRYOS OF THE SPOTTED RAY 4ORPEDO MAR
MORATA &ROM 0RISCO 2ICCHIARI AND !NDREUCCETTI
REPRODUCED WITH PERMISSION
! ,IGHT MICROGRAPH OF GERM CELLS IN THE OVARIAN CORTEX
#LUSTERS OF OOGONIA ARROWS AND MEIOTIC OOCYTES AR
ROWHEAD ARE SEEN &OLLICLES ARE ABSENT 8
" %LECTRON MICROGRAPH OF AN OOGONIUM 4HE NUCLEUS IS
ROUND AND CONTAINS A CONSPICUOUS NUCLEOLUS AND SEV
ERAL PATCHES OF HETEROCHOMATIN -ITOCHONDRIA CISTERNAE
OF GRANULAR ENDOPLASMIC RETICULUM AND AN AGGREGATE
OF GERM PLASM ARROW ARE EVIDENT IN THE CYTOPLASM
8
# %LECTRON MICROGRAPH OF A LEPTOTENE OOCYTE #YTOPLASMIC
ORGANELLES ARE INITIALLY POLARIZED IN A JUXTANUCLEAR POSI
TION 3EVERAL OSMIOPHILIC VACUOLES ARROWS ARE EVIDENT
IN THE SURROUNDING THECAL CELLS 8
$ %LECTRON MICROGRAPH OF AN INTERCELLULAR BRIDGE ARROW BETWEEN TWO OOCYTES 4HE MEMBRANES BORDERING THE BRIDGE ARE ELEC
TRON DENSE AND ABOUT NM IN THICKNESS 8
% %LECTRON MICROGRAPH OF A PRIMARY FOLLICLE IN THE OVARY OF A NEONATE 4HE DIPLOTENE OOCYTE IS SURROUNDED BY A SINGLE LAYER OF
SQUAMOUS FOLLICULAR CELLS 8
!BBREVIATIONS ", BASAL LAMINA %2 GRANULAR ENDOPLASMIC RETICULUM &# FOLLICULAR CELLS , LIPOSOMES - MITOCHONDRIA
. NUCLEUS .U NUCLEOLUS 3# THECAL CELLS
#(!04%2
&IGURE $IVISION OF DEVELOPING GERM CELLS IN THE OVARIES OF LAMPREYS 0ETROMYZON MARINUS CAUSES EVAGINATIONS OF
THE OVARIAN WALL TO EXPAND VENTRALLY SUBDIVIDING THE OVARY INTO LOBES AND LOBULES THAT CONTAIN A STROMA OF VASCULAR CONNECTIVE
TISSUE &ROM ,EWIS AND -C-ILLAN REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! " # ! 4HREE CELL NESTS ARE SURROUNDED BY PERITONEUM AND PENETRATED BY A STROMA OF VASCULAR CONNECTIVE TISSUE " %ACH
OF THESE CELL NESTS GIVES RISE TO A GROUP OF CELL NESTS EACH OF WHICH CONSTITUTES A LOBE OF THE OVARY THE VASCULAR
STROMA HAS PENETRATED BETWEEN THE CELL NESTS # !S DIVISION CONTINUES THE PROGENY OF EACH CELL NESTS FORMS A
LOBULE THE LOBULE IS A DISCRETE GROUP OF OOCYTES O ROUGHLY TWO CELLS IN THICKNESS CONTAINED WITHIN PERITONEUM
#. CELL NEST 0 PERITONEUM 3 STROMA
$
0HOTOMICROGRAPH OF A SECTION OF THE OVARY OF AN AMMOCOETE IN EARLY METAMORPHOSIS SHOWING THE OVIGEROUS FOLDS
WHICH ARE mAT LEAF
LIKE EXTENSIONS OF OVARIAN TISSUE 8
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE 4HE OVARY OF THE HAGlSH -YXINE GLUTINOSA FORMS A DORSAL NARROW RIBBON SUSPENDED FROM THE MESOVARIUM IN
THE MIDLINE &IGURES ! AND ' ARE FROM 7ALVIG REPRODUCED WITH PERMISSION " TO & ARE FROM 0ATZNER AND ARE
REPRODUCED WITH PERMISSION FROM THE .ORWEGIAN *OURNAL OF :OOLOGY
! 4HE OVARY / CONSISTS OF hSERIESv OF FOLLICLES THAT DEVELOP FROM OOGONIA CONTAINED WITHIN A BAND OF GERMINAL CELLS THAT RUNS
ALONG THE FREE EDGE OF THE OVARY '% 4HE MOVEMENT OF OOCYTES AND FOLLICLES AS WELL AS FOLLICULAR INVOLUTION IS INDICATED IN
THIS IMAGINARY DIAGRAM -ATURING OOCYTES MOVE FROM THE BAND OF GERMINAL CELLS INTO THE VASCULAR CONNECTIVE TISSUE OF
THE INNER PART OF THE OVARY TO 5NDIFFERENTIATED SQUAMOUS MESOTHELIAL CELLS ATTACH TO THE OOCYTES AND STRETCH TO ENCLOSE
THEM WITHIN A FOLLICULAR EPITHELIUM &OUR hGENERATIONSv OF OOCYTES ARE SHOWN DEVELOPING FROM OOGONIA IN THE GERMINAL
BAND ) TO )6 THEY GROW TO A DIAMETER OF TO MM WHEREUPON THEY ENTER A RESTING PERIOD AWAITING OVULATION OF THE PREVI
OUS GENERATION OF OOCYTES !FTER THE MATURE EGG IS OVULATED THE EMPTY FOLLICLE FORMS A POSTOVULATORY CORPUS LUTEUM
0/ THAT REGRESSES AS IT MOVES TOWARD THE MESOVARIUM -/ TO 3OME FOLLICLES UNDERGO ATRESIA AT SOME POINT IN THEIR
DEVELOPMENT 02
# !N ENLARGED PORTION OF " SHOWING THE OOGONIA /G IN THE GERMINAL BAND AND OOCYTES /C WITHIN THE OVARY 8
#(!04%2
&IGURE #ONTINUED
" 0HOTOMICROGRAPH OF A SECTION THROUGH THE GONAD OF A
CM FEMALE 8 /OGONIA ORIGINATE IN THE BAND OF GERMINAL CELLS
+E AND MIGRATE TO THE VASCULAR CONNECTIVE TISSUE OF THE INNER PART OF THE OVARY WHERE THEY UNDER GO MEIOTIC DIVISION TO
BECOME OOCYTES /H
!BBREVIATIONS $ INTESTINAL EPITHELIUM +E GERMINAL CELLS - MESENTERY -) MESOVARIUM . NERVE /H OOCYTES 6S SUPRA
INTESTINAL VEIN
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE #ONTINUED
$ %LECTRON MICROGRAPH OF A SECTION THROUGH THE GERMINAL BAND OF A
CM FEMALE SHOWING TWO OOGONIA + AND ONE GERMINAL
CELL #OLLAGENOUS lBRES +F PROVIDE SUPPORT IN THE VASCULAR STROMA 4HE BASAL LAMINA "M IS SHOWN !RROWS INDICATE
UNDULATIONS OF THE OUTER NUCLEAR MEMBRANE OF AN OOGONIUM 8
#(!04%2
&IGURE #ONTINUED
% %LECTRON MICROGRAPH OF A PORTION OF A PRIMARY FOLLICLE SHOWING THE THIN FOLLICULAR EPITHELIUM & SURROUNDING AN OOCYTE
#Y ! THECAL CELL 4 IS SUPPORTED BY COLLAGENOUS lBRES +F ! PERITONEAL CELL 0 OF THE MESOTHELIUM ENCLOSES THE OVARY
"M BASEMENT MEMBRANE 8
&IGURE #ONTINUED
& %LECTRON MICROGRAPH OF A PORTION OF A MATURING FOLLICLE APPROXIMATELY
M IN DIAMETER !N OOCYTE #Y IS ENCLOSED BY A SQUAMOUS FOLLICULAR
CELL & RESTING ON ITS BASEMENT MEMBRANE 4HE THECA CONSISTS OF mATTENED
THECAL CELLS 4 AND STOUT COLLAGENOUS lBRES +F ! PERITONEAL CELL 0 OF
THE MESOTHELIUM RESTS ON ITS BASEMENT MEMBRANE "M 8
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE #ONTINUED
' 0HOTOGRAPH OF THE OVARY OF -YXINE GLUTINOSA .EARLY MATURE EGGS % DANGLE WITHIN INDIVIDUAL PERITONEAL SLINGS -, FROM
FOLLICULAR LIGAMENTS &, ATTACHED TO THE OVARY 4WO ATRETIC EGGS ARE SHOWN $% 4HE INTESTINE ) IS SHOWN AT THE TOP
&IGURE 4HE EPITHELIUM LINING HOLLOW CYSTOVARIAN OVARIES OF MANY TELEOSTS IS THROWN INTO A COMPLEX SERIES OF OVIGEROUS
FOLDS
! 3CHEMATIC DIAGRAM OF A CROSS SECTION OF ONE OF THE PAIRED OVARIES OF THE SCULPIN !LCICHTHYS ALCICORNIS &ROM +OYA -UNE
HARA AND 4AKANO REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
" #OMPLEX OVIGEROUS FOLDS IN THE OVARY OF THE SURFPERCH #YMATOGASTER &ROM (OAR REPRODUCED WITH PERMISSION FROM
%LSEVIER 3CIENCE
# 0HOTOMICROGRAPHS OF CROSS SECTIONS OF THE OVARY OF THE BROOK STICKLEBACK %UCALIA INCONSTANS SHOWING OVIGEROUS FOLDS
ARROWS EXTENDING INTO THE OVOCOEL /# ,EFT 8 RIGHT 8 &ROM "RAEKEVELT AND -C-ILLAN REPRODUCED
WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
#(!04%2
&IGURE 4HE OVARY OF TELEOSTS IS SUPPLIED WITH BLOOD FROM SEVERAL ARTERIES THAT BRANCH OFF THE DORSAL AORTA ENTERING THE
DORSAL SIDE OF THE OVARY THROUGH THE MESOVARIUM %ACH FOLLICLE IN THE OVARY OF THE KILLIlSH &UNDULUS IS SUPPLIED BY A PRIMARY
ARTERIOLE THAT REACHES IT THROUGH A STALK OF STROMAL ELEMENTS &ROM "RUMMETT $UMONT AND ,ARKIN REPRODUCED WITH
PERMISSION OF *OHN 7ILEY 3ONS )NC
! 3CANNING ELECTRON MICROGRAPH OF A DEVELOPING FOLLICLE 4HE FOLLICLE IS ANCHORED IN THE STROMA BY A STALKLIKE STRUCTURE 34
SURROUNDED BY STROMAL ELEMENTS "LOOD VESSELS ARROWS CAN BE SEEN IN THE APICAL HEMISPHERE OF THE FOLLICLE 8
" %LECTRON MICROGRAPH OF A CROSS SECTION THE STALKLIKE STRUCTURE ! CENTRAL ARTERIOLE !2 IS SURROUNDED BY SMOOTH MUSCLE
3- A NERVE . ABUNDANT COLLAGEN # AND STROMAL CELLS 3# !N EPITHELIOID LAYER OF STROMAL CELLS %3 ENCLOSES THE
STRUCTURE 8
# 4HE SUPERlCIALLY LOCATED VESSELS IN THE APICAL OR LUMINAL HEMISPHERE OF THE FOLLICLE ARE MORE READILY APPARENT AND ARE
PRESUMED TO BE VENULES THAT COLLECT BLOOD FROM THE INTERVENING CAPILLARY BED AND TRANSPORT IT TO A VESSEL THAT FORMS A LOOP
ARROWS SURROUNDING THE PRESUMED SITE OF FUTURE OVULATION ON THE LUMINAL SIDE OF THE FOLLICLE 4HESE VESSELS TERMINATE IN
A SINGLE COLLECTING VESSEL THAT COURSES TOWARD THE OUTER SURFACE OF THE OVARY 8
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE 4HICK BUNDLES OF NON
MYELINATED NERVES PRESUMABLY AUTONOMIC ACCOMPANY THE OVARIAN ARTERY AND VEIN IN
THE OVARY OF TILAPIA /REOCHROMIS NILOTICUS &ROM .AKAMURA 3PECKER AND .AGAHAMA REPRODUCED WITH PERMISSION FROM
THE :OOLOGICAL 3OCIETY OF *APAN
! 0HOTOMICROGRAPH OF A PART OF THE OVARY SHOWING THICK NERVE BUNDLES LARGE ARROWS NEAR THE ARTERY ! AND VEINS 6
#LUSTERS OF STEROID
PRODUCING CELLS SMALL ARROWS ARE SEEN IN THE INTERSTITIAL AREA 8
" %LECTRON MICROGRAPH OF A CROSS SECTION OF A THICK NERVE BUNDLE IN THE OVARY 4HE BUNDLE CONSISTS OF MORE THAN AXONS
AND SOME NEURILEMMA CELLS ARROWS 8
# #ROSS SECTION OF NON
MYELINATED AXONS IN A NERVE BUNDLE
!BBREVIATIONS #6 DENSE
CORED VESICLES - MITOCHONDRIA -4 MICROTUBULES .& NEUROlLAMENTS 36 SYNAPTIC VESICLES
8
$ .ERVE BUNDLE ARROWS IS DISTRIBUTED NEAR A CLUSTER OF STEROID
PRODUCING CELLS 30# SHOWING WELL
DEVELOPED AGRANULAR
ENDOPLASMIC RETICULUM AND MITOCHONDRIA WITH TUBULAR CRISTAE 8
#(!04%2
&IGURE )N THE KILLIlSH &UNDULUS HETEROCLITUS THE POSTERIOR PORTION OF THE OVARY IS A THIN WALLED NONGERMINAL OVISAC THAT
IS CONTINUOUS WITH THE SHORT OVIDUCT AND APPARENTLY SERVES AS A RECEPTACLE FOR OVULATED EGGS PRIOR TO THEIR RELEASE TO THE EXTERNAL
ENVIRONMENT 4HESE CELLS MAY FUNCTION IN THE TRANSPORT OF OVULATED EGGS OR THEY MAY SECRETE A JELLY THAT FORMS A SURFACE COAT FOR
THE EXTRUDED EGGS &ROM "RUMMETT $UMONT AND ,ARKIN REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! %LECTRON MICROGRAPH OF THE LUMINAL EPITHELIUM OF THIS THIN WALLED REGION SHOWING A LOCALIZED POPULATION OF UNUSUAL CELLS
WITH LONG APICAL CYTOPLASMIC EXTENSIONS BEARING SHORT MICROVILLI AND EXTENSIVE BASAL INTERDIGITATIONS AND DESMOSOMES
,OBATE NUCLEI AND NUMEROUS MITOCHONDRIA OCCUPY THE BASAL CYTOPLASM 8
" 5NCOATED ENDOCYTOTIC PITS AND HEMIDESMOSOMES ARROWS ARE SEEN ADJACENT TO THE BASAL LAMINA OF THESE CELLS 4HERE ARE
A FEW MICROTUBULES IN THE CYTOPLASM 8
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE OVARY
AND THE EPITHELIUM OF THE OVARIAN LUMINAL WALL THE MEDA
KA /RYZIAS LATIPES SHOWING ANNUAL CYCLIC CHANGES &ROM
9AMAMOTO REPRODUCED WITH PERMISSION FROM THE
:OOLOGICAL 3OCIETY OF *APAN
! ,UMINAL WALL DURING VITELLOGENESIS *ANUARY A
C
" !S THE OVA MATURE &EBRUARY THE LUMINAL WALL THICKENS AND ITS SIMPLE CUBOIDAL EPITHELIUM BECOMES SIMPLE COLUMNAR
AS SECRETORY ACTIVITY INCREASES 4HE UNDERLYING TUNICA ALBUGINEA THICKENS AS VASCULARIZATION INCREASES AND SMOOTH MUSCLE
DEVELOPS A
C
# 4HE LUMINAL WALL CONTINUES TO THICKEN !PRIL AND THE EPITHELIAL CELLS BECOME TALLER A
C
$ ,UMINAL WALL IN -AY SHOWING ACTIVE APOCRINE SECRETION A
C
% ,UMINAL WALL FOLLOWING OVULATION 3EPTEMBER A
C
& !FTER SPAWNING THE EPITHELIUM AND TUNICA ALBUGINEA UNDERGO INVOLUTION .OVEMBER A
C
' 2APID CHANGES OCCUR IN THE LUMINAL WALL FOLLOWING SPAWNING 8 A
C )MMEDIATELY AFTER OVULATION THE WALL BECOMES
THIN LEFT WITH A SQUAMOUS EPITHELIUM AND REDUCED TUNICA SUBMUCOSA "Y THE NEXT DAY mUID HAS ACCUMULATED IN THE EPITHE
LIAL CELLS WHICH ONCE AGAIN APPEAR COLUMNAR MIDDLE 4HE VASCULAR SUBEPITHELIAL CONNECTIVE TISSUE RECOVERS 4WO DAYS AFTER
SPAWNING RIGHT
!BBREVIATIONS BC EXTRAVASATED BLOOD CELLS BV BLOOD VESSEL LE EPITHELIUM OE OEDEMATOUS TISSUE OV OVARIAN LUMEN SS
SECRETED SUBSTANCE VO VACUOLE IN COLUMNAR EPITHELIUM
-AGNIlCATION OF lGURES ! TO & TOP 8 MIDDLE 8 BOTTOM 8
#(!04%2
&IGURE 0HOTOMICROGRAPHS OF THE SIMPLE COLUMNAR EPITHELIUM OF MICROVILLOUS CELLS LINING THE OVARIAN CAVITY OF THE BLEAK
!LBURNUS ALBURNUS !ROUND THE TIME OF OVULATION THESE CELLS BULGE APICALLY INTO THE LUMEN AND A FEW SMALL CLUSTERS ARE ALSO
FOUND IN THE OVIDUCT &ROM ,AHNSTEINER 7EISMANN AND 0ATZNER REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 'ENERAL VIEW OF THE OVARY SHOWING THE LABYRINTHINE OVARIAN CAVITY
" )N SOME REGIONS THE THECA EXTERNA OF THE FOLLICLE SURROUNDS THE OVARIAN CAVITY NOT THE EPITHELIUM OF THE OVARIAN CAVITY
# #ROSS SECTION OF THE WALL OF THE OVIDUCT 4HE ARROW INDICATES A CLUSTER OF MICROVILLOUS CELLS
$ 7ALL OF THE OVIDUCT SHOWING CLUSTERS OF MICROVILLOUS CELLS
!BBREVIATIONS CI CILIA CT CONNECTIVE TISSUE EP EPITHELIUM FO THECA EXTERNA OF FOLLICLE LU LUMEN OF OVIDUCT OC OVARIAN
CAVITY OV OVUM P PERITONEUM ST STROMA ZP ZONA PELLUCIDA
&IGURE %LECTRON MICROGRAPHS OF MICROVILLOUS CELLS FROM THE OVARIAN CAVITY OF !LBURNUS ALBURNUS &ROM ,AHNSTEINER
7EISMANN AND 0ATZNER REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
% ,IPID VACUOLES IN THE CYTOPLASM
& ! MICROVILLOUS CELL HAS RELEASED A MEMBRANE
BOUND CYTOPLASMIC BLEB THIS IS APOCRINE SECRETION
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE #ONTINUED
! 0ROTEIN PRODUCTION IS INDICATED BY THE PROMINENT NUCLEOLUS AND ABUNDANT TUBULAR GRANULAR ENDOPLASMIC RETICULUM THAT FORMS
CONCENTRIC LAYERS AROUND THE BASAL NUCLEUS
" 4HE PRESENCE OF LAMELLAR BODIES IN THE MICROVILLOUS CELLS RESULTS FROM PHAGOCYTOSIS OF DBRIS FROM THE LUMEN
# 4HE CYTOPLASM OF A MICROVILLOUS CELL DISPLAYS THE ORGANELLES OF PROTEIN PRODUCTION NUCLEOLUS AGRANULAR ENDOPLASMIC RETICU
LUM AND FREE RIBOSOMES 4HE INSET SHOWS AN AUTOPHAGIC VESICLE IN A REGION CONTAINING SECRETORY VESICLES
$ 'OLGI COMPLEX AND NEIGHBOURING SECRETORY VESICLES% ,IPID VACUOLES IN THE CYTOPLASM
& ! MICROVILLOUS CELL HAS RELEASED A MEMBRANE
BOUND CYTOPLASMIC BLEB THIS IS APOCRINE SECRETION
!BBREVIATIONS AP CYTOPLASMIC BLEB RELEASED BY APOCRINE SECRETION AV AUTOPHAGIC VESICLE BL BASAL LAMINA C COATED
VESICLES GO 'OLGI COMPLEX LB LAMELLAR BODIES LI LIPID VACUOLES LU LUMEN MI MITOCHONDRIA NL NUCLEOLUS NU NUCLEUS
R RIBOSOMES RER GRANULAR ENDOPLASMIC RETICULUM SV SECRETORY VESICLE
!BBREVIATIONS AP CYTOPLASMIC BLEB RELEASED BY APOCRINE SECRETION AV AUTOPHAGIC VESICLE BL BASAL LAMINA C COATED VESICLES
GO 'OLGI COMPLEX LB LAMELLAR BODIES LI LIPID VACUOLES LU LUMEN MI MITOCHONDRIA NL NUCLEOLUS NU NUCLEUS R RIBOSOMES
RER GRANULAR ENDOPLASMIC RETICULUM SV SECRETORY VESICLE
#(!04%2
&IGURE
4HE OVARIES OF SYNGNATHIDS
CONSIST OF A SHEET OF FOLLICLES WITH THEIR SUP
PORTING VASCULAR STROMA IN THE FORM OF A TU
BULAR SCROLL EXTENDING LENGTHWISE
! 4HE UPPER DRAWING SHOWS THE PAIRED
OVARIES OF THE PIPElSH 3YGNATHUS SCOV
ELLI WHICH OPEN INTO THE SINGLE OVIDUCT
4HE DASHED LINES INDICATE THE SEGMENT
OF THE OVARY THAT IS ENLARGED BELOW
4HE MIDDLE SECTION HAS BEEN UNFURLED
TO SHOW THE FOLLICLES AND LUMEN
! SINGLE GERMINAL RIDGE FORMS THE IN
NER MARGIN OF THE SCROLL AND EXTENDING
FROM THIS IS A SEQUENTIAL ARRAY OF FOL
LICLES ARRANGED ACCORDING TO THEIR DE
VELOPMENTAL AGE SANDWICHED BETWEEN
THE OUTER OVARIAN WALL AND THE INNER
LUMINAL EPITHELIUM -ATURE OOCYTES
ARE OVULATED FROM THE OPPOSITE MARGIN
OF THE SCROLL THE MATURE EDGE INTO THE
OVARIAN LUMEN &ROM "EGOVAC AND
7ALLACE REPRODUCED WITH PER
MISSION OF *OHN 7ILEY 3ONS )NC
" )N THE SEAHORSE (IPPOCAMPUS EREC
TUS THERE ARE TWO GERMINAL RIDGES THAT
RUN THE LENGTH OF THE TUBULAR OVARY ON
OPPOSITE EDGES OF THE OVARIAN SHEET
4HE OVARY HAS BEEN CUT ALONG ITS
DORSAL MIDLINE AND BOTH HALVES HAVE
BEEN UNROLLED $EVELOPING FOLLICLES
ARISE FROM EACH GERMINAL RIDGE AND
GROW TOWARD A SHARED MATURE REGION
NEAR THE MIDDLE OF THE SHEET &ROM
3ELMAN 7ALLACE AND 0LAYER
REPRODUCED WITH PERMISSION OF
*OHN 7ILEY 3ONS )NC
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE )N CONTRAST TO THE RANDOM ORGANIZATION OF OVARIES OF OTHER lSH THE TEMPORAL AND SPATIAL CORRELATION OF OOCYTE
DEVELOPMENT AS SEEN IN SYNGNATHIDS FACILITATES THE STUDY OF SPECIlC EVENTS IN FOLLICULAR DEVELOPMENT 4HESE SEQUENCES MAY BE
SEEN IN ANY CROSS SECTION OF THE OVARIES &IGURES ! " AND # REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 3CHEMATIC DIAGRAM INDICATING THE SEQUENTIAL STAGES OF OOCYTE DEVELOPMENT IN AN OPTIMAL SECTION OF THE OVARY OF THE PIPElSH
3YGNATHUS SCOVELLI 3TAGE DESIGNATIONS ARE INDICATED BY 2OMAN NUMERALS &ROM "EGOVAC AND 7ALLACE
#(!04%2
&IGURE #ONTINUED
" 0HOTOMICROGRAPH OF A CROSS SECTION OF THE OVARY OF THE PIPElSH ! SEQUENTIAL SPIRAL OF DEVELOPING OOCYTES IS SEEN FROM THE
EARLIEST STAGE IN THE GERMINAL RIDGE ARROWHEAD TO THE MATURE EDGE WITH THE LARGEST OOCYTE / AT THE DOTTED LINE $ DORSAL
, OVARIAN LUMEN 6 VENTRAL 8 &ROM "EGOVAC AND 7ALLACE
# 0HOTOMICROGRAPH OF A CROSS SECTION THROUGH THE OVARY OF THE SEAHORSE (IPPOCAMPUS ERECTUS 4HE FOLLICULAR LAMINA HAS
TWO GERMINAL RIDGES ARROWHEADS FROM WHICH DEVELOPING FOLLICLES MIGRATE VENTRALLY $ DORSAL , LUMEN ,% LUMINAL
EPITHELIUM / OOCYTE IN DEVELOPING FOLLICLE 6 VENTRAL 7 MUSCULAR WALL OF THE OVARY 8 &ROM 3ELMAN 7ALLACE AND
0LAYER
A
&IGURE 3YNGNATHID OVARIES ARE COVERED ON THE OUTSIDE BY VISCERAL MESOTHELIUM OF SQUAMOUS TO LOW CUBOIDAL CELLS THAT IS
CONTINUOUS WITH THE MESOVARIUM )T IS SUBTENDED BY VARIABLE AMOUNTS OF COLLAGENOUS CONNECTIVE TISSUE CONNECTING IT TO SEVERAL
LAYERS OF SMOOTH MUSCLE &IGURES ! " AND # REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 3EAHORSE (IPPOCAMPUS ERECTUS %LECTRON MICROGRAPH OF A SECTION THROUGH A TYPICAL MESOTHELIAL CELL SHOWING ITS IRREGULAR
APICAL SURFACE AS WELL AS NUMEROUS PITS AND VESICLES ARROWHEADS ON BOTH THEIR APICAL AND BASAL SURFACES 4HESE CELLS CON
TAIN ABUNDANT CYTOPLASMIC lLAMENTS ARROW 8 &ROM 3ELMAN 7ALLACE AND 0LAYER
" 3EAHORSE (IPPOCAMPUS ERECTUS 0HOTOMICROGRAPH OF A SECTION THROUGH THE JUNCTION OF THE MESOVARIUM - WITH THE
OVARIAN WALL 7 4HE OVARY IS COVERED BY VISCERAL PERITONEUM ARROWHEADS WHICH IS CONTINUOUS WITH THE EPITHELIUM OF
&%-!,% '%.)4!, 3934%-3 /& &)3(
THE MESOVARIUM "LOOD VESSELS ARE ABUNDANT WITHIN THE MESOVARIUM AND WITHIN THE OUTER LAYERS OF THE OVARIAN WALL
, OVARIAN LUMEN / OOCYTE 8 &ROM 3ELMAN 7ALLACE AND 0LAYER
# %LECTRON MICROGRAPH OF A SECTION THROUGH THE OVARIAN WALL OF THE PIPElSH 3YNGNATHUS SCOVELLI 4HE SIMPLE SQUAMOUS COE
LOMIC EPITHELIUM #% OF THE OUTER OVARIAN WALL FACES THE PERITONEAL CAVITY 0# )T OVERLIES SEVERAL LAYERS OF SMOOTH MUSCLE
3- WHICH COMPRISE MOST OF THE THICKNESS OF THE OVARIAN WALL THE lBRES ARE ARRANGED ROUGHLY INTO TWO LAYERS AN INNER
CIRCULAR AND AN OUTER LONGITUDINAL 3MALL BLOOD VESSELS COURSE BETWEEN THE MUSCLE CELLS AS WELL AS BUNDLES OF UNMYELINATED
NERVES . THAT TEND TO RUN PARALLEL TO THE LONG AXIS OF THE OVARY 6ASCULAR CONNECTIVE TISSUE OF VARIABLE THICKNESS OCCURS
WITHIN THE WALL A CONNECTIVE TISSUE CELL IS SHOWN
8 &ROM "EGOVAC AND 7ALLACE
#(!04%2
&IGURE 4HE GERMINAL RIDGES EXTEND THE LENGTH OF THE SYNGNATHID OVARY AND CONTAIN THE PROLIFERATIVE STEM CELLS FROM
WHICH THE OOCYTES ARE DERIVED AND FOLLICLES FORMED 0HOTOMICROGRAPHS OF SECTIONS THROUGH THE OVARY OF THE SEAHORSE (IPPOCAM
PUS ERECTUS &ROM 3ELMAN 7ALLACE AND 0LAYER REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4WO GERMINAL RIDGES ARROWHEADS PROJECT INTO THE OVARIAN LUMEN , 4HE RIDGES ARE COVERED BY THE LUMINAL EPITHELIUM OF
SQUAMOUS TO CUBOIDAL CELLS AND CONTAIN RICHLY VASCULAR CONNECTIVE TISSUE SURROUNDING EACH FOLLICLE 4HE GERMINAL RIDGES AND
THE FOLLICLES ARISING FROM EACH FORM SCROLLS THAT TWIST IN OPPOSITE DIRECTIONS / OOCYTE 8
" %XTENSIVE LYMPHATIC SPACES
LINED BY ATTENUATED ENDOTHELIAL CELLS PENETRATE THE STROMA OF THE OVARY ,EFT A LYMPHATIC
VESSEL LYING BETWEEN ADJACENT FOLLICLES AND THE OVERLYING LUMINAL EPITHELIUM ,% 2IGHT A LYMPHATIC VESSEL OCCUPIES MUCH
OF THE SPACE BETWEEN ADJACENT FOLLICLES AND THE OVARIAN WALL 7 6 SMALL VEIN 8
A
&IGURE !S IN MANY BONY lSHES THE LUMEN OF THE CYSTOVARIAN OVARIES OF SYNGNATHIDS IS LINED BY AN EPITHELIUM THAT IS
DERIVED FROM THE COELOMIC MESOTHELIUM AND IS CONTINUOUS WITH THE OVIDUCT 4HE EPITHELIAL CELLS LIE ON A DISTINCT BASAL LAMINA
AND VARY IN SHAPE FROM SQUAMOUS OVER THE GERMINAL RIDGE TO CUBOIDAL OR COLUMNAR OVER MORE MATURE FOLLICLES 4HESE ELECTRON
MICROGRAPHS SHOW THE LUMINAL EPITHELIUM FROM THREE REGIONS OF THE OVARY OF THE SEAHORSE (IPPOCAMPUS ERECTUS 3INGLE ARROWS
INDICATE TIGHT JUNCTIONS DOUBLE ARROWS DESMOSOMES &ROM 3ELMAN 7ALLACE AND 0LAYER REPRODUCED WITH PERMISSION
OF *OHN 7ILEY 3ONS )NC
&%-!,% '%.)4!, 3934%-3 /& &)3(
! ,UMINAL EPITHELIAL CELLS OVER THE GERMINAL RIDGE ARE RELATIVELY mAT AND ARE HIGHLY INTERDIGITATED ON THEIR LATERAL SURFACES
4HE BASAL PLASMALEMMA IS ELABORATELY INFOLDED !RROWHEADS INDICATE THE DISTINCT BASAL LAMINA 8
" #UBOIDAL LUMINAL EPITHELIAL CELLS OVERLIE SMALL FOLLICLES 4HE BASAL LAMINA ARROWHEADS OF THE LUMINAL EPITHELIAL CELLS LIES
NEXT TO THE THICK BASAL LAMINA
OF FOLLICULAR CELLS & FROM THE UNDERLYING FOLLICLE 8
# #OLUMNAR EPITHELIAL CELLS OVERLYING LARGE FOLLICLES DISPLAY LONG MICROVILLI INTERDIGITATING LATERAL MEMBRANES AND NUMEROUS
CYTOPLASMIC lLAMENTS 8 $ETAIL OF THE CYTOPLASMIC lLAMENTS IS SHOWN IN THE INSET 8
#(!04%2
&IGURE %LECTRON MICROGRAPH OF A LUMINAL EPITHELIAL CELL FROM THE OVARY OF THE PIPElSH 3YNGNATHUS SCOVELLI SHOWING
BLEBBING INTO THE OVARIAN LUMEN , 4HESE CELLS ARE HIGHLY SECRETORY )NTRACELLULAR lLAMENTS & ARE ABUNDANT 7ELL DEVELOPED
TIGHT JUNCTIONS ARE SEEN ON EACH SIDE OF THE BLEB 8 &ROM "EGOVAC AND 7ALLACE REPRODUCED WITH PERMISSION OF
*OHN 7ILEY 3ONS )NC
A
&IGURE ! FORM OF APOCRINE SECRETION HAS BEEN DESCRIBED IN THE COLUMNAR EPITHELIAL CELLS OF THE OVARIAN LUMEN OF TELE
OSTS
! %LECTRON MICROGRAPH OF THE OVARIAN WALL OF THE MEDAKA /RYZIAS LATIPES FOLLOWING OVULATION !PICAL hBLEBSv BREAK OFF FROM
THE REST OF THE CELL AND CONTRIBUTE TO THE SECRETED MATERIAL IN THE LUMEN 8 &ROM 4AKANO REPRODUCED WITH
PERMISSION OF THE 'RADUATE 3CHOOL OF &ISHERIES 3CIENCES (OKKAIDO 5NIVERSITY
!BBREVIATIONS , OVARIAN LUMEN ,3 LIQUID WITHIN INTERCELLULAR SPACES . NUCLEUS 3- SMOOTH MUSCLE OF SUBEPITHELIAL LAYER
" %LECTRON MICROGRAPH OF THE MATURING OVARY OF THE GOLDlSH #ARASSIUS AURATUS 4HE COLUMNAR EPITHELIAL CELLS LINING THE LU
MEN /, DEVELOP CILIA #I LARGE CYTOPLASMIC BLEBS !P BREAK AWAY FROM THE SURFACE AT THE BASES OF THE CILIA 8
&ROM 4AKAHASHI AND 4AKANO REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
!BBREVIATIONS - MITOCHONDRION . NUCLEUS
&%-!,% '%.)4!, 3934%-3 /& &)3(
#(!04%2
&%-!,% '%.)4!, 3934%-3 /& &)3(
@
&IGURE 4HE LINING OF THE HOLLOW OVARY IN SOME SPECIES OF 3CORPAENIFORMES SECRETES A BILOBED GELATINOUS MASS THAT
PROVIDES PROTECTION FOR THE EGGS 4HE PAIRED CYSTOVARIAN OVARIES ARE SHEATHED WITHIN A WALL OF SMOOTH MUSCLE AND CONNECTIVE
TISSUE AND ARE ENCLOSED BY VISCERAL PERITONEUM !NTERIORLY THE OVARIES ARE ROUNDED AND EACH OF THEM IS SUSPENDED BY A SPONGY
VESSEL
RICH HILUS WHOSE VESSELS PENETRATE INTO THE LUMEN TO ENTER THE SPONGY VASCULAR OVIGEROUS STROMA 3USPENDED BY THE HILUS
AT THE ANTERIOR END OF EACH LOBE THE OVIGEROUS STROMA mOATS FREE WITHIN THE LUMEN
! 3CHEMATIC DIAGRAM OF THE OVARY OF THE ROCKlSH 3EBASTOLOBUS MACROCHIR &ROM +OYA AND -ATSUBARA REPRODUCED
WITH PERMISSION OF THE 'RADUATE 3CHOOL OF &ISHERIES 3CIENCES (OKKAIDO 5NIVERSITY
" $IAGRAM OF A CROSS SECTION OF THE OVARY OF $ENDROCHIRUS BRACHYPTERUS DURING REPRODUCTION 4HE OVIGEROUS TISSUE IS COVERED
BY AN OOCYTE
PRODUCING EPITHELIUM THAT BRISTLES WITH VASCULARIZED hPEDUNCLESv THAT RADIATE FROM THE STROMA 4HESE PE
DUNCLES ARE EXTENSIONS OF THE STROMA AND ACCOMMODATE SECONDARY OOCYTE DEVELOPMENT &ROM &ISHELSON REPRODUCED
WITH PERMISSION OF THE AUTHOR
!BBREVIATIONS "6 BLOOD VESSEL %% EGG ENVELOPE %, EPITHELIAL LAYER ', GERMINATIVE LAYER -, MUSCLE LAYER /, OVARIAN
LUMEN 30 SECRETORY PROCESSES
# 0HOTOMICROGRAPH OF OOCYTE AND PEDUNCLE FROM THE OVARY OF 3EBASTOLOBUS ALASCANUS COLLECTED DURING AN EARLY PHASE OF
PRODUCTION OF GELATINOUS MATERIAL 3CALE BAR M &ROM %RICKSON AND 0IKITCH REPRODUCED WITH KIND PERMISSION
OF +LUWER !CADEMIC 0UBLISHERS
!BBREVIATIONS BV BLOOD VESSEL GM GELATINOUS MATERIAL PO PREVITELLOGENIC OOCYTE
$ 0HOTOMICROGRAPH OF AN OVARIAN FOLLICLE OF 3EBASTOLOBUS MACROCHIR IN MATURATION PHASE )T PROJECTS BY A NARROW PEDUNCLE P
FROM THE OVARIAN STROMA S O OOCYTE 3CALE BAR M &ROM +OYA AND -ATSUBARA REPRODUCED WITH PERMISSION
OF THE 'RADUATE 3CHOOL OF &ISHERIES 3CIENCES (OKKAIDO 5NIVERSITY
% %LECTRON MICROGRAPH OF A PORTION OF AN OVARIAN FOLLICLE OF 3EBASTOLOBUS MACROCHIR IN MATURATION PHASE 4HE OOCYTE O IS
ENCLOSED BY THE AMORPHOUS ZONA PELLUCIDA VE A LAYER OF FOLLICULAR CELLS G THECA T AND THE SIMPLE SQUAMOUS LUMINAL
EPITHELIUM FE 3CALE BAR M &ROM +OYA AND -ATSUBARA REPRODUCED WITH PERMISSION OF THE 'RADUATE 3CHOOL
OF &ISHERIES 3CIENCES (OKKAIDO 5NIVERSITY
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF THE EPITHELIA OF THE OVARY OF THE ROCKlSH 3EBASTOLOBUS MACROCHIR 4HE LUMINAL WALL
IS LINED BY A SIMPLE COLUMNAR EPITHELIUM ! " WHILE A MORE DELICATE SIMPLE COLUMNAR EPITHELIUM COVERS THE OVIGEROUS TISSUE
# &ROM +OYA AND -ATSUBARA REPRODUCED WITH PERMISSION OF THE 'RADUATE 3CHOOL OF &ISHERIES 3CIENCES (OKKAIDO
5NIVERSITY
! "EFORE OVULATION THERE IS A BUILDUP OF THE CELLULAR MECHANISM FOR PROTEIN PRODUCTION IN THE EPITHELIAL CELLS LINING THE OVARIAN
WALL 4HESE CELLS PRODUCE THE OUTER lBROUS LAYER OF THE GELATINOUS MASS
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE #ONTINUED
I %ACH EPITHELIAL CELL BEARS A LARGE APICAL PROJECTION CONTAINING MASSES OF ELECTRON
LUCENT MATERIAL IN THE CYTOPLASM AP
"AR M
II 4HESE ELECTRON
LUCENT MASSES
ARE SURROUNDED BY WELL
DEVELOPED AGRANULAR ENDOPLASMIC RETICULUM S%2 "AR M
III 4HE CENTRAL PART OF AN EPITHELIAL CELL CONTAINS ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM S%2 AND SPARSE GRANULAR
ENDOPLASMIC RETICULUM R%2 G GLYCOGEN M MITOCHONDRIA N NUCLEUS "AR M
IV .UMEROUS GLYCOGEN GRANULES G ARE SEEN IN THE CYTOPLASM OF THE BASAL PART OF AN EPITHELIAL CELL BM BASAL LAMINA
"AR M
" 4HE APICAL PROJECTIONS AP OF THE EPITHELIAL CELLS OF THE LUMINAL WALL HAVE DECREASED IN HEIGHT AFTER THE lRST OVULATION MV
MICROVILLI N NUCLEUS "AR M )NSET THE APICAL CYTOPLASM CONTAINS WELL
DEVELOPED AGRANULAR ENDOPLASMIC RETICULUM
S%2 M MITOCHONDRION "AR M
# 4HE MORE DELICATE COLUMNAR EPITHELIAL CELLS OF THE OVIGEOROUS LAMELLA SECRETE THE HOMOGENEOUS INNER LAYER OF THE GELATINOUS
MASS
I 4HESE CELLS LIE ON A BASEMENT LAMINA BM THAT SEPARATES THEM FROM THE CELLS OF THE THECA T M MITOCHONDRIA N NUCLEUS
R%2 GRANULAR ENDOPLASMIC RETICULUM "AR M
II 4HE PERINUCLEAR CYTOPLASM SHOWS WELL DEVELOPED AGRANULAR ENDOPLASMIC RETICULUM S%2 GRANULAR ENDOPLASMIC RETICU
LUM R%2 AND A 'OLGI COMPLEX ' N NUCLEUS "AR M
)NSET 4HE APICAL CYTOPLASM SHOWING AN EXOCYTOTIC PIT ARROW "AR M
&IGURE 3CHEMATIC DIAGRAM OF THE FORMATION OF GELATINOUS EGG MASSES IN THE ROCKFSH 3EBASTOLOBUS MACROCHIR &ROM
+OYA (AMATSU AND -ATSUBARA REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING !SIA 0TY ,TD
! !NTERIORLY THE OVARIES ARE ROUNDED AND EACH OF THEM IS SUSPENDED BY A SPONGY VESSEL
RICH HILUS WHOSE VESSELS PENETRATE
INTO THE LUMEN TO ENTER THE SPONGY VASCULAR OVIGEROUS STROMA WHICH mOATS FREE WITHIN THE LUMEN 4HE OVIGEROUS TISSUE IS
COVERED BY AN OOCYTE
PRODUCING EPITHELIUM THAT BRISTLES WITH VASCULARIZED hPEDUNCLESv THAT RADIATE FROM THE STROMA AND
BEAR DEVELOPING OOCYTES $URING THE SPAWNING SEASON EPITHELIA LINING HE LUMINAL WALL AND COVERING THE OVIGEROUS TISSUE
SECRETE A GELATINOUS MASS THAT lLLS THE LUMEN AND EMBEDS THE OOCYTES AND THEIR STALKS 0EDUNCLE LENGTH INCREASES AS VITEL
LOGENESIS PROCEEDS
" 7ITHIN THE BASE OF EACH PEDUNCLE ARE PREVITELLOGENIC OOCYTES WHEN A MATURE OOCYTE IS RELEASED AT OVULATION A PREVITELLO
GENIC OOCYTE MOVES UP INSIDE THE PEDUNCLE TO TAKE ITS PLACE AND UNDERGO VITELLOGENESIS
# $URING SPAWNING THE OOCYTES EMBEDDED IN THE GELATINOUS MASS ARE SWEPT FROM THE LUMEN 4HE GELATINOUS MASS SECRETED
BY THE EPITHELIA OF THE TWO LOBES IS EXTRUDED AROUND THE OVIGEROUS TISSUE OF BOTH LOBES
$ 4HE HOLLOW BILOBED EGG MASS IS EXTRUDED
#(!04%2
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE 3EVERAL MARINE COTTID SPECIES 3CORPAENIFORMES HAVE A UNIQUE REPRODUCTIVE MODE CALLED hINTERNAL GAMETIC AS
SOCIATIONv WHERE SPERMATOZOA ARE INTRODUCED INTO THE OVARIAN CAVITY BY COPULATION AND mOAT FREELY IN THE OVARIAN mUID ALTHOUGH
FERTILIZATION DOES NOT OCCUR UNTIL THE EGGS HAVE BEEN SPAWNED INTO SEA WATER 4HESE ELECTRON MICROGRAPHS ARE FROM THE OVARY
OF THE MARINE SCULPIN !LCICHTHYS ALCICORNIS &ROM +OYA 4AKANO AND 4AKAHASHI +OYA -UNEHARA AND 4AKANO
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE EPITHELIUM OF THE OVIGEROUS LAMELLA DURING THE RECOVERY PERIOD FOLLOWING SPAWNING
5PPER
4HE EPITHELIUM IS STRATIlED DURING EARLY RECOVERY 8
,OWER
,ATER DURING THE RECOVERY PERIOD A SIMPLE LAYER OF EPITHELIAL CELLS IS ARRANGED ON THE BASAL LAMINA BM
8
" 4HE EPITHELIUM OF THE OVARIAN WALL EARLY IN THE RECOVERY PERIOD IS CILIATED C
5PPER
4HE EPITHELIUM IS SIMPLE DURING EARLY RECOVERY 4HERE ARE FEW SHORT APICAL MICROVILLI 4HE ARROW INDICATES
SMALL APICAL PITS ON THE EPITHELIAL CELLS 8
)NSET
4HESE PITS ARE SHOWN IN GREATER DETAIL 4HE VESICLES APPEAR TO BE DISCHARGING THEIR CONTENTS INTO THE OVARIAN LUMEN
8
,OWER
-ICROVILLI ARE WELL DEVELOPED ON THE APICAL SURFACE OF THE EPITHELIAL CELLS LATER IN THE RECOVERY PERIOD 4HE
CYTOPLASM IS PACKED WITH WELL DEVELOPED GRANULAR ENDOPLASMIC RETICULUM ER 8
# %PITHELIUM FROM THE OVIGEROUS LAMELLA DURING THE SPAWNING PERIOD 4HE EPITHELIAL CELLS MANIFEST THE APPEARANCE OF PROTEIN
PRODUCTION WITH ABUNDANT BASAL GRANULAR ENDOPLASMIC RETICULUM AND ACTIVE APICAL 'OLGI COMPLEXES .UMEROUS PINOCYTOTIC
PITS AND VESICLES ARE SEEN IN THE PERIPHERAL CYTOPLASM OF THESE CELLS INCREASING NUMBERS OF PITS AND VESICLES ARE ALSO PRESENT
IN THE ENDOTHELIAL CELLS OF ADJACENT CAPILLARY WALLS AT THIS TIME INDICATING THAT ACTIVE TRANSCYTOSIS IS TAKING PLACE
5PPER
!BUNDANT MICROVILLI EXTEND FROM THE APICAL SURFACE 'RANULAR ENDOPLASMIC RETICULUM ER AND 'OLGI COM
PLEXES ' ARE WELL DEVELOPED .OTE THE APICAL DESMOSOMES BETWEEN ADJACENT EPITHELIAL CELLS 8
-ID LEFT 'RANULAR ENDOPLASMIC RETICULUM NEAR THE NUCLEUS N APPEARS TO BE FORMING A BUD LIKE EXTENSION ARROW
8
-ID RIGHT 7ELL DEVELOPED 'OLGI COMPLEX IN THE APICAL CYTOPLASM %LECTRON LUCENT VESICLES ARROW AND SLIGHTLY ELECTRON
DENSE VESICLES ARROWHEADS LIE NEAR THE 'OLGI LAMELLAE 8
,OWER LEFT 6ESICLES IN THE APICAL CYTOPLASM APPEAR TO FUSE TO FORM SECRETORY VESICLES ARROWHEADS 4HE CONTENTS OF THESE
VESICLES ARE RELEASED BY EXOCYTOSIS ARROWS 8
,OWER RIGHT "LEBBING OF THE TIPS OF MICROVILLI ARROW 3OME VESICULAR BODIES ARROWHEAD LIE FREE IN THE OVARIAN LUMEN
/# 8
$ %PITHELIUM FROM THE OVIGEROUS LAMELLA DURING THE SPAWNING PERIOD
5PPER LEFT ! PINOCYTOTIC PIT OPENS INTO THE INTERCELLULAR SPACE 8
5PPER RIGHT .UMEROUS PINOCYTOTIC PITS ARROWS AND VESICLES ARE SEEN IN THE BASAL CYTOPLASM 8
,OWER
! STRONG REACTION IS SEEN IN THE CONNECTIVE TISSUE CT AND BASAL INTERCELLULAR SPACES OF lSH TREATED WITH HORSE
RADISH PEROXIDASE 2EACTION PRODUCTS ARE ALSO OBSERVED IN THE PITS ARROWS AND VESICLES ARROWHEADS NEAR
THE OUTER SURFACES OF THE CELLS 8
#(!04%2
&IGURE #ONTINUED
% %PITHELIUM FROM THE OVARIAN WALL DURING SPAWNING
,EFT
.UMEROUS MICROVILLI BRISTLE FROM THE APICAL SURFACE OF THE EPITHELIAL CELLS THE CYTOPLASM CONTAINS WELL DEVEL
OPED GRANULAR ENDOPLASMIC RETICULUM ER AND 'OLGI COMPLEXES G 8
5PPER RIGHT 4HE APICAL SURFACE OF THE EPITHELIAL CELLS IS RIDDLED WITH EXOCYTOTIC PITS ARROW AND VESICLES ARROWHEADS
8
,OWER RIGHT !PICAL BLEBS ARROWS SEPARATE FROM THE SURFACE OF THE EPITHELIAL CELLS TO FORM A MICROAPOCRINE SECRETION
8
& $URING SPAWNING NUMEROUS VESICLES PACK THE CYTOPLASM OF ENDOTHELIAL CELLS % FROM THE CAPILLARIES OF THE OVIGEROUS LAMEL
LAE 0ITS OPEN ON BOTH THE APICAL AND BASAL SURFACES OF THE ENDOTHELIAL CELLS ARROWS 4HE CAPILLARY LUMEN , IS AT THE LEFT
8
' !DJACENT EPITHELIAL CELLS ARE JOINED BY JUNCTIONAL COMPLEXES AND IT IS SUGGESTED THAT THESE TIGHT JUNCTIONS ISOLATE THE SPERMA
TOZOA IN THE LUMEN FROM THE MATERNAL IMMUNE SYSTEM
5PPER LEFT RIGHT 4HE APICAL BORDERS OF EPITHELIAL CELLS OF AN OVIGEROUS LAMELLA ARE JOINED BY A JUNCTIONAL COMPLEX ARROW
AND DESMOSOME D 8
,OWER LEFT *UNCTIONAL COMPLEX ARROW AND DESMOSOME D SECURING THE APICAL BORDERS OF EPITHELIAL CELLS FROM THE OVARIAN
WALL 8
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE #ONTINUED
( !FTER THE SPAWNING PERIOD THE JUNCTIONS BREAK DOWN AND RESIDUAL SPERMATOZOA ARE ELIMINATED BY INVADING MATERNAL
LEUCOCYTES
5PPER LEFT 0LASMA CELL SHOWING CHARACTERISTIC WELL
DEVELOPED GRANULAR ENDOPLASMIC RETICULUM ER 8
5PPER RIGHT 0OLYMORPHONUCLEAR LEUCOCYTE SHOWING LOBED NUCLEUS AND ELECTRON
DENSE CYTOPLASMIC GRANULES 8
-ID LEFT -ONOCYTE WITH FEW CYTOPLASMIC ORGANELLES 4HE ARROW INDICATES A CYTOPLASMIC EXTENSION 8
,OWER LEFT 4HE CYTOPLASM OF A MACROPHAGE GIVES EVIDENCE OF CLEAN
UP OF CELLULAR BREAKDOWN MEMBRANOUS WHORLS
MULTILAMELLAR BODIES ARROW AND A HETEROGENEOUS COLLECTION OF VESICLES 8
,OWER RIGHT -ASSES OF MACROPHAGES CONTAINING LAMELLAR BODIES LM AND ELECTRON
DENSE GRANULES G APPEAR DURING
THE RECOVERY PERIOD 8
#(!04%2
&IGURE #ONTINUED
) 4HIS DIAGRAM SUMMARIZES THE CHANGES THAT TAKE PLACE DURING THE REPRODUCTIVE CYCLE OF THE SCULPIN !LCICHTHYS ALCICORNIS
!BBREVIATIONS BM BASAL LAMINA C CILIUM CT CONNECTIVE TISSUE D DESMOSOME $% DEGENERATING EPITHELIAL CELL ' G 'OLGI
COMPLEX LM LAMELLAR BODIES N NUCLEUS / OOGONIUM /# OVARIAN CAVITY
&%-!,% '%.)4!, 3934%-3 /& &)3(
&IGURE 0HOTOMICROGRAPHS OF CROSS SECTIONS OF THE OVARY OF 3CYLIORHINUS CANICULA 4HE OVARIES OF #HONDRICHTHYES ARE
SURROUNDED BY THE GONADAL EPITHELIUM AND CONSIST OF A CONNECTIVE TISSUE STROMA CONTAINING DEVELOPING FOLLICLES POSTOVULATORY
FOLLICLES CORPORA LUTEA AND DEGENERATING FOLLICLES CORPORA ATRETICA "LOOD VESSELS AND NERVES COURSE THROUGH THE STROMA
4HE STROMA ALSO CONTAINS LYMPH SPACES OR MEMBRANOUS FOLDS THAT ARE lLLED WITH DEVELOPING BLOOD CELLS &ROM $ODD AND
3UMPTER REPRODUCED WITH PERMISSION OF #HURCHILL ,IVINGSTONE
5PPER
/OCYTES IN THREE STAGES OF DEVELOPMENT / PRIOR TO FOLLICLE FORMATION / PREVITELLOGENIC FOLLICLE AND
/ A FOLLICLE IN EARLY VITELLOGENESIS
-IDDLE
#ROSS SECTION OF EARLY VITELLOGENIC FOLLICLE
,OWER
#ROSS SECTION OF A FOLLICLE DURING EARLY ATRESIA $ISSOLUTION OF YOLK OCCURS IN PATCHES 9$
!BBREVIATIONS "- BASEMENT MEMBRANE "6 BLOOD VESSEL BETWEEN THECA INTERNA AND FOLLICULAR BASEMENT MEMBRANE
' FOLLICULAR EPITHELIUM 4% THECA EXTERNA 4) THECA INTERNA 90 YOLK PLATELETS :2 ZONA PELLUCIDA
#(!04%2
&IGURE 0HOTOMICROGRAPH OF THE SPENT OVARY OF THE DOGlSH SHARK 3QUALUS ACANTHIAS !N UNOVULATED FOLLICLE IS SEEN AT
THE LOWER LEFT !BUNDANT HAEMOPOIETIC ACTIVITY IN SEEN IN THE LOOSE CONNECTIVE TISSUE OF THE STROMA 8
A
&IGURE 'ENERAL VIEW OF THE REPRODUCTIVE TRACT OF THE BASKING SHARK #ETORHINUS MAXIMUS ,EFT FROM THE VENTRAL SUR
FACE THE OVIDUCT ON THE RIGHT IS OPENED LONGITUDINALLY 2IGHT LATERAL VIEW FROM THE RIGHT SIDE /NLY THE RIGHT OVARY PERSISTS AND
THE EPIGONAL ORGAN LIES POSTERIOR AND SLIGHTLY DORSAL TO THE OVARY BEING SUSPENDED FROM THE DORSAL ABDOMINAL WALL BY A BACKWARD
EXTENSION OF THE MESOVARIUM 4HE LEFT EPIGONAL ORGAN IS OF SIMILAR SIZE AND SHAPE AS THE RIGHT BUT NO OVARY IS FUSED TO ITS ANTE
RIOR END AND IT IS SUSPENDED BY ITS OWN PERITONEAL FOLD IN THE CORRESPONDING POSITION ON THE LEFT SIDE OF THE BODY CAVITY &ROM
-ATTHEWS REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
!BBREVIATIONS !0 ABDOMINAL PORES #L CLOACA % EPIGONAL ORGAN ). UNPAIRED OVIDUCT )3 ISTHMUS + KIDNEY -- MESOME
TRIUM / OVARY /! OSTIUM /$ PAIRED OVIDUCT /% OESOPHAGUS 0/ POCKET IN RIGHT SIDE OF OVARY 2 RECTUM 3' OVIDUCTAL
GLAND 5 UTERUS 50 URINARY PAPILLA 52 UTERUS LINED WITH FOLDS 54 UTERUS LINED WITH TROPHONEMATA 6# COMMON VAGINA
60 PAIRED VAGINA OF THE LEFT SIDE
&%-!,% '%.)4!, 3934%-3 /& &)3(
#(!04%2
/6!2)!. &/,,)#,%3
CELLS &IGURE
0OLARITY IS LAID DOWN WITHIN THE OOCYTE OF THE ME
DAKA /RYZIAS LATIPES DURING FORMATION OF THE ZONA PEL
LUCIDA BEFORE YOLK PRODUCTION BEGINS )WAMATSU AND
.AKASHIMA 4HIS !.)-!,
6%'%4!, !8)3 CONSISTS
OF AN !.)-!, 0/,% OF THE MOST ACTIVE PROTOPLASM THAT
DEVELOPS DIAMETRICALLY OPPOSITE A 6%'%4!, 0/,% OF
YOLKY RELATIVELY INERT PROTOPLASM )T IS SUGGESTED THAT
THIS AXIS IS ESTABLISHED DURING DEVELOPMENT BY RECIPRO
CAL INTERACTIONS OF THE OOCYTE WITH THE ADJACENT FOLLICU
LAR CELLS WHERE A GROUP OF COMPACTLY CLUSTERED FOLLICULAR
CELLS DETERMINES THE POSITION OF THE VEGETAL POLE AREA
! FOLLICULAR CELL AT THE OPPOSITE SIDE OF THE OOCYTE DIF
FERENTIATES INTO A -)#2/09,!2 #%,, THEREBY DETERMINING
THE POSITION OF THE -)#2/09,% POINT OF SPERM ENTRY AT
THE ANIMAL POLE )NDEED THE MICROPYLE IS A CONVENIENT
MARKER FOR IDENTIFYING THE ANIMAL POLE
)N LAMPREYS POSSIBLY ALL ELASMOBRANCHS AND SOME
BONY lSHES OOGONIAL PROLIFERATION IS LIMITED TO THE
LARVAL OR EMBRYONIC PERIOD 4OKARZ 3UCCES
SIVE GENERATIONS OF OOCYTES APPEAR TO DEVELOP FROM
OOGONIA IN THE GERMINAL RIDGE OF ADULT HAGlSH -YXINE
GLUTINOSA THESE OOCYTES ENTER A RESTING PHASE WHILE
THEY AWAIT OVULATION OF THE PREVIOUS GENERATION OF OO
CYTES 0ATZNER )N MOST BONY lSHES OOGONIAL
PROLIFERATION IS FOUND IN THE ADULT ANIMAL 4HERE IS A
LIMITED PERIOD OF PEAK OOGONIAL DIVISION IN SPECIES
WITH CIRCUMSCRIBED ANNUAL BREEDING CYCLES IN SPECIES
WHICH DO NOT HAVE RESTRICTED BREEDING CYCLES OOGONIAL
PROLIFERATION OCCURS EITHER IN WAVES OR CONTINUOUSLY
THROUGHOUT THE YEAR
!T THE END OF OOGONIAL PROLIFERATION THE SECONDARY
OOGONIA BECOME PRIMARY OOCYTES AND ENTER A PROTRACT
ED EARLY PROPHASE ! PRIMARY OOCYTE IS SURROUNDED BY
A SINGLE LAYER OF FOLLICULAR CELLS TO FORM A 02)-/2$)!,
&/,,)#,% 4OKARZ 4HIS PROCESS IS SIMILAR IN ALL
NON
MAMMALIAN VERTEBRATES AND BEGINS AT APPROXI
MATELY THE SAME STAGE OF MEIOTIC PROPHASE ! SCHEME
OF FOLLICULAR DEVELOPMENT IN THE MEDAKA /RYZIAS
LATIPES IS SHOWN IN &IGURE
)NTRODUCTION
/OGONIA PROLIFERATE BY MITOSIS TO BECOME 02)-!29
//#94%3 )N THESE CELLS THE CHROMOSOMES ARE ARRESTED
IN THE DIPLOTENE STAGE OF THE lRST MEIOTIC PROPHASE
4HE OOCYTES THEN ENTER A PERIOD OF GROWTH THAT
VARIES FROM SPECIES TO SPECIES ENLARGING CHIEmY BY
ACCUMULATING YOLK !S THEY GROW AND MATURE VARIOUS
INTRACELLULAR AND EXTRACELLULAR CHANGES OCCUR )NITIALLY
THE FOLLICULAR CELLS FORM A SIMPLE SQUAMOUS EPITHELIUM
AROUND EACH OOCYTE BUT AS DEVELOPMENT PROCEEDS
THE CELLS ENLARGE AND MAY BECOME CUBOIDAL AND EVEN
COLUMNAR )N CYCLOSTOMES AND TELEOSTS THE &/,,)#5,!2
%0)4(%,)5- REMAINS SINGLE LAYERED BUT IN #HONDRICH
THYES IT MAY BE COMPOSED OF SEVERAL LAYERS &RANCHI
!S IS TYPICAL OF MANY EPITHELIA DESMOSOMES
CONNECT ADJACENT FOLLICULAR CELLS &OLLICULAR CELLS MAY
ALSO PRODUCE OVARIAN HORMONES 4HE FOLLICULAR EPI
THELIUM IS SURROUNDED BY ITS OWN BASAL LAMINA WHICH
SEPARATES IT FROM A SHEATH OF CONDENSED VASCULAR CON
NECTIVE TISSUE THE 4(%#! &/,,)#5,) !S THE FOLLICLE DIF
FERENTIATES THE THECA BECOMES MORE DISTINCT AND MAY
BE DIVIDED INTO A 4(%#! ).4%2.! AND 4(%#! %84%2.!
4HE THECA CONTAINS lBROBLASTS COLLAGENOUS lBRES AND
CAPILLARIES AND IN SOME SPECIES SPECIAL THECAL STEROID
PRODUCING CELLS &IGURE
$URING DEVELOPMENT A THICK TRANSLUCENT ACELLULAR
:/.! 0%,,5#)$! OR 6)4%,,).% %.6%,/0% DEVELOPS BE
TWEEN THE OOCYTE AND FOLLICULAR CELLS !FTER HATCHING
WHEN A SIMPLE PLASMA MEMBRANE WOULD BE INADEQUATE
FOR SUCH A LARGE CELL TO WITHSTAND THE RIGOURS OF INDE
PENDENT EXISTENCE THIS SHEATH SERVES AS A TOUGH EN
CLOSURE FOR THE EGG %VEN IN VIVIPAROUS FORMS WHERE
THE EMBRYOS DEVELOP WITHIN THE BODY OF THE FEMALE
THIS ENVELOPE IS FORMED DURING OOGENESIS &LEGLER
$URING GROWTH OF THE OOCYTE THE ZONA PELLU
CIDA BECOMES PERFORATED BY 0/2% #!.!,3 ENABLING AN
EXCHANGE OF MATERIALS BETWEEN THE OOCYTE AND FOLLICU
LAR CELLS THESE CHANNELS CONTAIN MICROVILLI THAT EXTEND
FROM THE SURFACES OF BOTH THE OOCYTE AND THE FOLLICULAR
#(!04%2
"ECAUSE OF THE ACCESSIBLITY OF INITIAL STAGES IN THE
SYNGNATHIDS THE PIPElSH AND THE SEAHORSE EXTEN
SIVE DESCRIPTIONS OF FOLLICULOGENESIS HAVE BEEN CARRIED
OUT ON THESE SPECIES PROVIDING MUCH OF THE INFORMA
TION USED HERE "EGOVAC AND 7ALLACE 3EL
MAN 7ALLACE AND 0LAYER 4HEIR GERMINAL RIDGE
IS WELL
DElNED AND CONTAINS //'/.)! %!2,9 02/0(!3%
) //#94%3 AND 3/-!4)# 02%&/,,)#5,!2 #%,,3 AS WELL AS
OCCASIONAL DEGENERATING CELLS &IGURE /OGONIA OF
THE GERMINAL RIDGE DIVIDE BY MITOSIS !S THE DAUGH
TER CELLS MOVE AWAY THEY ARE ENVELOPED BY &/,,)#5
,!2 #%,,3 WHICH ARE DERIVED FROM THE PROLIFERATION OF
PREFOLLICULAR CELLS THAT EXTEND PROCESSES BETWEEN CON
TIGUOUS MEIOTIC OOCYTES 4HIS RESULTS IN THE ISOLATION
OF THE GERM CELLS FROM OTHER CELLS THEREBY FORMING A
&/,,)#,% CONSISTING OF AN OOCYTE SURROUNDED BY A FOL
LICULAR EPITHELIUM ENCLOSED BY ITS OWN BASAL LAMINA
&IGURE ! 0REFOLLICULAR AND FOLLICULAR CELLS CON
TAIN CYTOPLASMIC lLAMENTS THAT DISTINGUISH THEM FROM
EARLY MEIOTIC OOCYTES WHICH CONTAIN NO lLAMENTS
.EWLY FORMED FOLLICLES ARE SURROUNDED BY A THIN 4(%#!
OF CONNECTIVE TISSUE ELEMENTS
//'/.)! OF THE PIPEFISH THE STEM CELLS OF THE
GERM CELL LINEAGE ARE OVAL TO SPHERICAL CELLS ABOUT
M IN DIAMETER WHICH OCCUR IN THE LUMINAL EPITHE
LIUM NEAR THE GERMINAL RIDGE AND WITHIN THE GERMINAL
RIDGE ITSELF "EGOVAC AND 7ALLACE &IGURE
4HEY ARE CONTIGUOUS WITH OTHER GERM CELLS AND SOMATIC
CELLS BUT ARE NOT IN CONTACT WITH THE BASAL LAMINA OF
THE LUMINAL EPITHELIUM 4HEY ARE THE ONLY GERM CELLS
WITHIN THE GERMINAL RIDGE THAT INCORPORATE ;(= THY
MIDINE INDICATING THAT THEY ARE THE ONLY GERM CELLS
CAPABLE OF NUCLEAR DIVISION SOMATIC CELLS INCLUDING
FOLLICULAR CELLS AND CONNECTIVE TISSUE CELLS INCORPORATE
THE LABEL AS WELL /OGONIA HAVE THE LARGEST NUCLEARCY
TOPLASMIC RATIO OF ANY CELLS OF THE GERM CELL LINE 4HE
OVAL NUCLEI CONTAIN ONE TO THREE NUCLEOLI $ENSE
CORED
GRANULES OF UNKNOWN COMPOSITION WITHIN THE NUCLEUS
ARE SPECIlC TO NUCLEI OF THE GERM CELL LINE AND ARE
ALSO PRESENT IN LARGER OOCYTES /OGONIAL CHROMATIN IS
MORE ELECTRON
DENSE THAN THAT OF MEIOTIC OOCYTES /O
GONIAL CYTOPLASM CONTAINS MITOCHONDRIA RIBOSOMES
AND SCANT ENDOPLASMIC RETICULUM BUT APPEARS TO LACK A
'OLGI COMPLEX !GGREGATES OF .5!'% MATERIAL ARE FRE
QUENTLY ASSOCIATED WITH MITOCHONDRIA THIS IS AN ELEC
TRON
DENSE MEMBRANELESS ORGANELLE CONSISTING OF A
SPONGELIKE AGGREGATION OF lNE GRANULAR MATERIAL 4HE
FUNCTION AND COMPOSITION OF NUAGE ARE UNCERTAIN BUT
ITS PRESENCE IS A RELIABLE MARKER OF GERM CELLS /OGO
NIA OF THE SEA LAMPREY 0ETROMYZON MARINUS APPEAR TO
BE SIMILAR TO THOSE OF TELEOSTS /KKELBERG ,EWIS
AND -C-ILLAN
3TAGES OF /OCYTE $EVELOPMENT
4HE PROCESS OF TRANSFORMATION OF OOGONIA TO OOCYTES
IS //'%.%3)3 3ELMAN AND 7ALLACE )T IS GENER
ALLY ACCEPTED THAT THE CHROMOSOMES BECOME ARRESTED
AT DIPLOTENE OF THE lRST MEIOTIC PROPHASE AND THE INITIAL
FOLLICLE IS ESTABLISHED 7ALLACE AND 3ELMAN )T
IS UNCLEAR HOW OOGONIAL DAUGHTER CELLS ARE TRANSFORMED
INTO PROPHASE ) MEIOTIC OOCYTES AND WHETHER THE OOGO
NIAL DIVISION THAT PRODUCES THE OOCYTES IS SYMMETRICAL
"EGOVAC AND 7ALLACE !LTHOUGH IT IS DIFlCULT
TO DISTINGUISH THE EARLIEST MEIOTIC OOCYTES FROM OO
GONIA SOME FEATURES ARE SAID TO CHARACTERIZE NEWLY
FORMED OOCYTES IN THE SEQUENTIALLY ARRANGED OVARIES OF
SYNGNATHIDS AN INCREASE IN SIZE ALONG WITH A DECREASE
IN NUCLEARCYTOPLASMIC RATIO LOSS OF THE PERINUCLEAR
RING OF MITOCHONDRIA PROLIFERATION OF OTHER ORGANELLES
ESPECIALLY 'OLGI COMPLEXES AND CHANGES IN NUCLEAR
MORPHOLOGY ESPECIALLY CONDENSATION OF CHROMATIN
"EGOVAC AND 7ALLACE 3ELMAN 7ALLACE AND
0LAYER &IGURES " AND ! 4HE MOST OBVI
OUS SIGN OF TRANSFORMATION OF OOGONIA TO OOCYTES IN THE
SEA LAMPREY IS THE INCREASE IN THE SIZE OF THE NUCLEUS
AND THE APPEARANCE OF A PROMINENT NUCLEOLUS ,EWIS
AND -C-ILLAN
#YTOPLASMIC BRIDGES HAVE BEEN DESCRIBED BETWEEN
OOGONIA AND OOCYTES OF SOME TELEOSTS &IGURE
"RUSL AND "RUSL 'RANDI AND #OLOMBO
THESE BRIDGES WERE NO LONGER OBSERVED WHEN FOLLICULAR
CELLS HAD ENVELOPED THE OOCYTE "RUSL /N THE
OTHER HAND INTERCELLULAR BRIDGES WERE NEVER OBSERVED
BETWEEN OOGONIA OR OOCYTES OF THE SYNGNATHIDS "EGO
VAC AND 7ALLACE 3ELMAN 7ALLACE AND 0LAYER
!N INCREASE IN SIZE IS THE MOST OBVIOUS MANIFES
TATION OF OOCYTE DEVELOPMENT &IGURE 4HE OO
CYTE GROWS BOTH BY AN ENLARGEMENT OF THE NUCLEUS
AND THE ADDITION OF CYTOPLASM ,ATER MOST GROWTH IS
DUE TO AN INCREASE IN THE AMOUNT OF CYTOPLASM AND
IN THE lNAL STAGES OF MATURATION THE OOCYTE HAS ITS
FULL COMPLEMENT OF YOLK AND IS READY TO BE OVULATED
&OUR PRINCIPAL STAGES OF OOCYTE DEVELOPMENT AS OUT
LINED BELOW HAVE BEEN DESCRIBED IN SEVERAL TELEOSTS
7ALLACE AND 3ELMAN 4HE MAJOR CELLULAR AND
PHYSIOLOGICAL PROCESSES OCCURRING AT EACH STAGE OF THE
ZEBRAlSH "RACHYDANIO RERIO ARE OUTLINED BY 3ELMAN
ET AL !VERAGE DIAMETERS OF FOLLICLES OOCYTES
/6!2)!. &/,,)#,%3
4!",% !VERAGE DIAMETERS OF OVARIAN FOLLICLES IN &UNDULUS HETEROCLITUS DURING THE STAGES OF OOCYTE DEVELOP
MENT $ATA FROM 3ELMAN AND 7ALLACE
0RIMARY GROWTH STAGE
! #HROMATIN NUCLEOLUS PHASE
" 0ERINUCLEOLUS PHASE
#ORTICAL ALVEOLUS STAGE
6ITELLOGENESIS
/OCYTE MATURATION
! %ARLY MATURATION
" ,ATE MATURATION
IN EARLY STAGES RECORDED FOR &UNDULUS HETEROCLITUS
ARE SHOWN IN 4ABLE &OUR SIMILAR STAGES HAVE BEEN
OUTLINED IN THE LAMPREY ,AMPETRA PLANERI "USSON
-ABILLOT C 3IMILAR DEVELOPMENT IN THE RED SEA
BREAM 0AGRUS MAJOR -ATSUYAMA .AGAHAMA AND
-ATSUURA THE RAINBOW TROUT 3ALMO GAIRDNERI
VAN DEN (URK AND 0EUTE AND THE SUMMER
mOUNDER 0ARALICHTHYS DENTATUS -ERSON ET AL
HAVE BEEN ASSIGNED TO SEVEN STAGES NINE STAGES IN
THE MEDAKA /RYZIAS LATIPES &IGURE )WAMATSU
ET AL AND IN THE BLENNY "LENNIUS PHOLIS ELEVEN
&IGURE 3HACKLEY AND +ING
#LASSIlCATION OF STAGES OF OVARIAN MATURITY BY MAC
ROSCOPIC OBSERVATION ARE USEFUL IN FECUNDITY STUDIES
"AGENAL AND "RAUM THESE HAVE BEEN ADAPTED
USING HISTOLOGICAL CRITERIA FOR THE PERCH 0ERCA mUVIATI
LIS AND PIKE %SOX LUCIUS &IGURE 4REASURER AND
(OLLIDAY 4REASURER AND FOR THE BASS
$ICENTRARCHUS LABRAX -AYER 3HACKLEY AND 2YLAND
02)-!29 '2/74(
3TUDIES WITH MANY TELEOSTS INDICATE THAT PRIMARY
GROWTH IS INDEPENDENT OF PITUITARY CONTROL +HOO
$URING THE PRIMARY GROWTH STAGE OOCYTES OF
MOST TELEOSTS INCREASE IN VOLUME ABOUT FOLD
GROWING IN DIAMETER FROM ABOUT n M AT LEPTO
TENE TO n M THIS IS ACCOMPANIED BY A NOTICE
ABLE DECREASE IN NUCLEARCYTOPLASMIC RATIO 3ELMAN
AND 7ALLACE !S THE OOCYTE GROWS THE DElNI
TIVE FOLLICLE FORMS /OCYTES UNDERGO THE EARLY STAGES
OF PROPHASE AND BECOME ARRESTED IN DIPLOTENE OF THE
lRST MEIOTIC DIVISION 4HE PRIMARY GROWTH STAGE MAY
BE DIVIDED INTO TWO PHASES BASED ON NUCLEOLAR MOR
PHOLOGY THE #(2/-!4). .5#,%/,53 0(!3% AND THE 0%2)
.5#,%/,53 0(!3% )N THE ZEBRAFISH "RACHYDANIO RERIO
M
M
M
M
MM
MM
MM
MM
THE FOLLICULAR CELLS DO NOT COMPLETELY ISOLATE INDIVIDUAL
OOGONIA AND SURROUND .%343 OF EARLY GERM CELLS &IG
URE 3ELMAN ET AL $URING THE PRIMARY
GROWTH PHASE THE MEIOTIC OOCYTES BECOME ENCLOSED
BY FOLLICULAR CELLS THEREBY FORMING DElNITIVE FOLLICLES
#HROMATIN
NUCLEOLUS STAGE
/OGONIA ENTERING THE EARLY STAGES OF MEIOTIC PROPHASE
WITHIN THE GERMINAL RIDGE OF SYNGNATHIDS TRANSFORM
INTO OOCYTES DURING THE CHROMATIN
NUCLEOLUS PHASE
&IGURE $.! REPLICATION PRE
LEPTOTENE OCCURS
AT THIS TIME (OMOLOGOUS CHROMOSOMES PAIR AND BE
GIN TO CONDENSE LEPTOTENE ZYGOTENE THESE PAIRS SUB
SEQUENTLY SHORTEN AND THICKEN TO FORM SYNAPTONEMAL
COMPLEXES PACHYTENE lNALLY THE CHROMOSOMES TAKE
ON THE hLAMPBRUSHv CONlGURATION DIPLOTENE 4HE NU
CLEI OF PIPElSH OOCYTES BECOME MORE SPHERICAL THAN
THOSE OF OOGONIA "EGOVAC AND 7ALLACE .UCLEI
OF LEPTOTENE OOCYTES CONTAIN DENSE
CORED GRANULES AND
THE CHROMATIN REMAINS ELECTRON
DENSE .UCLEI OF OO
CYTES IN ZYGOTENE AND PACHYTENE STAGES OF PROPHASE )
ARE LESS ELECTRON
DENSE AND CAN BE DISTINGUISHED BY THE
PRESENCE OF SYNAPTONEMAL COMPLEXES BETWEEN HOMOL
OGOUS CHROMOSOMES WITHIN THE NUCLEUS &IGURE "
"Y THE PACHYTENE STAGE THE SYNAPTONEMAL COMPLEXES
ARE LONG AND THE NUCLEOLI HAVE BECOME DISPERSED AND
FRAGMENTED $ENSE
CORED GRANULES ARE STILL PRESENT IN
THE NUCLEI /OCYTES IN ZYGOTENE AND PACHYTENE GROW
SLIGHTLY WITH AN INCREASE IN ORGANELLES USUALLY AGGRE
GATED AT ONE SIDE OF THE NUCLEUS MITOCHONDRIA 'OLGI
COMPLEX RIBOSOMES AND ENDOPLASMIC RETICULUM .U
AGE CONTINUES TO BE PRESENT
.EWLY FORMED MEIOTIC OOCYTES IN SYNGNATHIDS INI
TIALLY ARE IN CONTACT WITH OTHER OOCYTES !S THE OOCYTES
GROW WITHIN THE GERMINAL RIDGE THEY BECOME SEPARAT
ED FROM ADJACENT OOCYTES BY PROCESSES OF 02%&/,,)#5
#(!04%2
,!2 #%,,3 &IGURE 3ELMAN 7ALLACE AND 0LAYER
!S THE OOCYTE GROWS THE NUCLEUS ENLARGES TO FORM THE
'%2-).!, 6%3)#,% THE NUCLEAR MEMBRANE BECOMES
UNDULATING AND WITH FURTHER GROWTH OF THE OOCYTE IT
FORMS LARGE FOLDS AND EVAGINATIONS AND BECOMES LOBED
'URAYA 3OON AFTER THE ARREST IN PROPHASE RI
BOSOMAL GENES ARE AMPLIlED AND SEVERAL NUCLEOLI AP
PEAR IN THE OOCYTES OF MOST TELEOSTS GENERALLY ARRANGED
AT THE PERIPHERY OF THE GERMINAL VESICLE ALTHOUGH LATER
THEY MAY LIE RANDOMLY WITHIN IT &IGURE 3ELMAN
AND 7ALLACE 4HIS IS THE 0%2).5#,%/,53 34!'%
OF PRIMARY OOCYTE GROWTH 4HESE NUCLEOLI ARE PRESENT
THROUGHOUT OOCYTE GROWTH
!T THIS STAGE THE hLAMPBRUSHv APPEARANCE OF THE
CHROMOSOMES BECOMES MORE APPARENT &IGURE
4HESE CHROMOSOMES ARE FESTOONED WITH LOOPS OF $.!
THAT PRESUMABLY REPRESENT UNWINDINGS OF A SINGLE
CHROMOSOME AND ARE SITES OF ACTIVE TRANSCRIPTION OF
HETEROGENEOUS 2.! IN ADDITION TO THE RIBOSOMAL 2.!
PROVIDED BY THE MULTIPLE NUCLEOLI
5NLIKE THE SITUATION IN MOST TELEOST OOCYTES WHERE
LARGE NUMBERS OF NUCLEOLI ARE PRODUCED DURING THE
CHROMATIN NUCLEOLUS PERIOD OF PRIMARY GROWTH ONLY
ONE OR TWO NUCLEOLI ARE PRESENT AT THIS TIME IN THE VI
VIPAROUS TELEOST 8IPHOPHORUS HELLERI !ZEVEDO AND
#OIMBRA 4HESE NUCLEOLI DISPLAY A COMPACT
lBRILLAR CORE SURROUNDED BY A LOOSER GRANULAR PERIPH
ERY &IGURE &OLLOWING THE DIPLOTENE STAGE WHEN
MEIOTIC ACTIVITY IS SUSPENDED AND LAMPBRUSH CHROMO
SOMES ARE PRESENT IN THE NUCLEUS THESE NUCLEOLI EN
LARGE FROM ABOUT TO M AND BECOME INCREASINGLY
VACUOLATED INDICATING INCREASED RIBOSOMAL PRODUCTION
AS THE CELLS PREPARE FOR VITELLOGENESIS &IGURE
4HE NUCLEOLI SUDDENLY DECREASE IN SIZE DURING VITEL
LOGENESIS THEY DISAPPEAR WHEN THE lRST POLAR BODY IS
EMITTED AND THE OOCYTE )) IS READY FOR FERTILIZATION
/OCYTES INCREASE IN SIZE WITH THE CONTINUED ELABO
RATION OF CYTOPLASM MITOCHONDRIA 'OLGI COMPLEXES
RIBOSOMES ENDOPLASMIC RETICULUM AND MULTIVESICULAR
BODIES "EGOVAC AND 7ALLACE 4HIS GROWTH IS
ACCOMMODATED BY MITOTIC DIVISION OF THE FOLLICULAR
CELLS &IGURE $URING THE PRIMARY GROWTH PHASE
MOST TELEOST OOCYTES ACCUMULATE EXTENSIVE AGGREGA
TIONS OF BASOPHILIC AND ELECTRON DENSE MATERIAL IN THE
PERINUCLEAR CYTOPLASM 4HIS LOOSELY DElNED STRUCTURE
IS THE *584!.5#,%!2 #/-0,%8 /& /2'!.%,,%3 "!,
")!.)3 6)4%,,).% "/$9 &IGURE #LROT
"RUSL -AYER 3HACKLEY AND 2YLAND
3ELMAN AND 7ALLACE THERE IS ONE REPORT OF THE
JUXTANUCLEAR COMPLEX IN AN ELASMOBRANCH THE DOGlSH
3COLIODON SORRAKOWAH 'URAYA ! CONSPICUOUS
3OON AFTER THE OOCYTES ENTER THE DIPLOTENE PRE
FOLLICULAR CELLS PROLIFERATE mATTEN AND EVENTUALLY FORM
THE &/,,)#5,!2 %0)4(%,)5- THAT COMPLETELY ENVELOPS
THE GROWING OOCYTES "RUSL "EGOVAC AND 7AL
LACE %ACH OOCYTE EXTENDS NUMEROUS MICROVILLI
TOWARD THE FOLLICULAR CELLS &IGURE % AND LATER THE
FOLLICULAR CELLS RECIPROCATE BY EXTENDING MICROVILLI TO
WARD THE OOCYTE 4HE SQUAMOUS FOLLICULAR CELLS HAVE
LARGE NUCLEI WITH CYTOPLASM CONTAINING MITOCHONDRIA
GRANULAR ENDOPLASMIC RETICULUM AND SCANT 'OLGI COM
PLEXES 4HE FOLLICULAR EPITHELIUM IS ENCLOSED BY ITS
BASAL LAMINA
#HROMATIN NUCLEOLUS OOCYTES BECOME ARRESTED IN
LATE DIPLOTENE OF MEIOTIC PROPHASE ) AS THE SYNAPTONE
MAL COMPLEXES DISSOCIATE WITHIN THE OOCYTE NUCLEUS
3ELMAN AND 7ALLACE $URING THIS PHASE THE
OOCYTES BEGIN AN EXTENSIVE PERIOD OF GROWTH 4HE
OOPLASMIC MATRIX INCREASES AS WELL AS THE ORGANELLES
WHICH TEND TO REMAIN JUXTANUCLEAR .UCLEOLI REAPPEAR
ADJACENT TO THE INNER LAYER OF THE NUCLEAR ENVELOPE
4HE APPEARANCE OF MULTIPLE NUCLEOLI SEEMS TO COINCIDE
WITH THE FORMATION OF THE DElNITIVE FOLLICLE AS IT SEPA
RATES FROM THE GERMINAL RIDGE %ACH NUCLEOLUS CONSISTS
OF TWO PARTS A CORTICAL REGION OF TIGHTLY PACKED RIBO
SOMES AND A CENTRAL AREA COMPOSED LARGELY OF lNE
lLAMENTS AND SCANT AMOUNTS OF THE GRANULAR COMPO
NENT &IGURE !NDERSON 4HE $%&).)4)6%
&/,,)#,% NOW CONSISTS OF AN OOCYTE SURROUNDED BY A
SINGLE LAYER OF mATTENED FOLLICULAR CELLS WITH THE EN
TIRE COMPLEX ENCLOSED BY A BASEMENT LAMINA /UTSIDE
THE BASAL LAMINA THERE IS A SPARSE 4(%#!, ,!9%2 OF VAS
CULAR CONNECTIVE TISSUE AND A THIN SURFACE EPITHELIUM
CONSISTING OF MESOTHELIAL CELLS 4HE NUCLEUS OF THE OO
CYTE IS GENERALLY SPHERICAL WITH MULTIPLE NUCLEOLI IN
A PERINUCLEAR POSITION ADJACENT TO THE INNER LAYER OF
THE NUCLEAR ENVELOPE &IGURE $ENSE CORED GRAN
ULES CAN STILL BE OBSERVED IN THE NUCLEUS 4HE NUCLEUS
GROWS AND NUCLEOLI INCREASE IN NUMBER
0ERINUCLEOLUS PHASE
4HE GREATLY ENLARGED NUCLEUS OF AN OOCYTE DURING THE PROPHASE
OF THE lRST MEIOTIC DIVISION IS DESIGNATED A '%2-).!, 6%3)#,%
4HE REFERENCES BY 'URAYA DISCUSS "ALBIANIS VITEL
LINE BODY AT LENGTH
/6!2)!. &/,,)#,%3
hVITELLINE BODYv DESCRIBED AT THE END OF THE PRIMARY
GROWTH PERIOD IN OOCYTES OF THE BROOK LAMPREY %NTO
SPHENUS WILDERI IS PROBABLY THE SAME STRUCTURE /K
KELBERG
4HE JUXTANUCLEAR COMPLEX IS COMPOSED OF PARTICLES
OF RIBONUCLEOPROTEIN ASSOCIATED WITH A HETEROGENEOUS
POPULATION OF CYTOPLASMIC ORGANELLES GRANULAR EN
DOPLASMIC RETICULUM 'OLGI ELEMENTS MITOCHONDRIA
LYSOSOMES MULTIVESICULAR BODIES AND LIPID DROPLETS
&IGURES # $ !..5,!4% ,!-%,,!% OF UNKNOWN
FUNCTION HAVE BEEN OFTEN DESCRIBED WITHIN THE JUX
TANUCLEAR COMPLEX )WAMATSU 4HEY CONSIST
OF SEVERAL PARALLEL SMOOTH CISTERNAE EACH CONTAINING
REGULARLY ARRANGED FENESTRATIONS CORRESPONDING TO THE
NUCLEAR PORES &IGURES AND )T HAS BEEN SUG
GESTED THAT THE CISTERNAE ARISE FROM THE NUCLEAR ENVE
LOPE AND ARE A SPECIAL TYPE OF ENDOPLASMIC RETICULUM
$EPENDING UPON THE SPECIES OF lSH THE JUXTANUCLE
AR COMPLEX SHOWS DIFFERENT COMBINATIONS OF VARIOUS
ORGANELLES AND INCLUSIONS )T MAY BE A CONSEQUENCE
OF THIS VARIABILITY THAT AN EXTENSIVE ARRAY OF CONFUS
ING TERMS HAS ARISEN IN ASSOCIATION WITH IT 4HESE
TERMS INCLUDE 9/,+ .5#,%53 WHICH IS SOMETIMES USED
SYNONYMOUSLY WITH THE TERM JUXTANUCLEAR COMPLEX
.5!'% OR #%-%.4 WHICH APPEARS TO BE A MATERIAL RICH
IN RIBONUCLEOPROTEIN OCCUPYING THE OOPLASM BETWEEN
THE AGGREGATED ORGANELLES AND 0!,,)!, 35"34!.#%
A DEEPLY BASOPHILIC CLOAK ENCLOSING LESS BASOPHILIC
MATERIAL "EAMS AND +ESSEL 4HE PRESENCE OF
NUAGE HAS BEEN USED AS A CRITERION FOR IDENTIFYING PRI
MORDIAL GERM CELLS IN THE CYPRINID "ARBUS CONCHIONUS
'EVERS ET AL AND THE CENTROPOMID #ENTROPO
MUS UNDECIMALIS 'RIER
4HE SUBSTANCE OF THE JUXTANUCLEAR COMPLEX ORIGI
NATES AS A CRESCENT OR CAP ADJACENT TO THE NUCLEAR MEM
BRANE AND INCREASES IN SIZE AS THE OOCYTE GROWS &IGURE
'URAYA 4HE COMPLEX DISAPPEARS AT THE
BEGINNING OF VITELLOGENESIS 4HE #)2#5-.5#,%!2 2).'
SEEN WITH THE LIGHT MICROSCOPE IN OOCYTES OF THE COD
'ADUS MORHUA AND THE CENTROPOMID #ENTROPOMUS
UNIDECIMALIS IS THOUGHT TO BE HOMOLOGOUS TO THE JUX
TANUCLEAR COMPLEX AND IS CONSIDERED TO BE THE lRST SIGN
THAT THE lSH WILL SPAWN IN THE COMING SEASON &IGURE
+JESBU AND +RYVI 'RIER
4HE JUXTANUCLEAR COMPLEX MAY ASSUME VARIOUS
SHAPES IN DIFFERENT TELEOSTS )N OOCYTES OF SOME lSH
4HE TOPIC OF ANNULATE LAMELLAE IS REVIEWED EXTENSIVELY BY +ESSEL
A SINGLE DISCRETE STRUCTURE DEVELOPS NEAR THE NUCLEUS
EG #HANNA MARULIS $ICENTRARCHUS LABRAX 'U
RAYA -AYER 3HACKLEY AND 2YLAND IT
MAY EXPAND TO FORM A PERINUCLEAR RING EG 4ILAPIA
NILOTICA 3YNGNATHUS SCOVELLI "EGOVAC AND 7ALLACE
AND IN SOME OOCYTES A SINGLE CRESCENT THAT
LATER BECOMES OVOID AND MIGRATES TO THE PERIPHERY OF
THE OOCYTE EIGHT )NDIAN SPECIES BUT ESPECIALLY (ET
EROPNEUSTES FOSSILIS &IGURE .AYYAR
4HE COMPLEX MAY APPEAR DOUBLE IN OOCYTES OF THE
!TLANTIC MACKEREL 3COMBER SCOMBRUS #OELLO AND
'RIMM .UAGE OF THE COMMON SNOOK #ENTRO
POMUS UNDECIMALIS IS A POLYMORPHIC ORGANELLE ASSO
CIATED WITH MITOCHONDRIA 'RIER )T OCCURS AS
DENSE CYTOPLASMIC INCLUSIONS GENERALLY PERINUCLEAR IN
POSITION &IGURE "
)N THE MEDAKA /RYZIAS LATIPES THE YOLK NUCLEUS IS
AN ELECTRON DENSE THREAD LIKE STRUCTURE INHABITING THE
VEGETAL POLE SIDE OF THE OOCYTE &IGURE )WAMATSU
AND .AKASHIMA )T IS SUGGESTED THAT THE ORIENTA
TION OF THE VEGETAL POLE MAY PRIMARILY BE DETERMINED
BY THE RANDOM POSITIONING OF THE YOLK NUCLEUS WITHIN
THE OOCYTE AND ESTABLISHED BY RECIPROCAL INTERACTIONS
BETWEEN THE CYTOPLASM CONTAINING THE YOLK NUCLEUS
AND THE SURROUNDING FOLLICULAR CELLS
4HE FUNCTION OF THE JUXTANUCLEAR COMPLEX IS ENIG
MATIC )T HAS BEEN SUGGESTED THAT IT ACTS AS A CENTRE FOR
METABOLIC ACTIVITIES RELATED TO THE FORMATION MULTIPLI
CATION AND ACCUMULATION OF OTHER ORGANELLES AND INCLU
SIONS THAT ARE lNALLY DISTRIBUTED IN THE OUTER OOPLASM
BEFORE THE DEPOSITION OF YOLK REPRESENTING A MOBILIZA
TION OF THE FORCES NEEDED FOR LAYING DOWN YOLK #LROT
"RUSL 3ELMAN AND 7ALLACE
/OCYTE VOLUME INCREASES A FEW HUNDRED FOLD DURING
PRIMARY GROWTH THE NUCLEARCYTOPLASMIC RATIO DECREAS
ES AND MANY MEMBRANOUS ORGANELLES ARE ELABORATED
WITHIN THE OOPLASM &IGURES # $ !T THE END OF
THIS PHASE THE OOCYTE AND FOLLICULAR CELLS HAVE ESTAB
LISHED AN INTIMATE RELATIONSHIP 0ATCHES OF TRANSLUCENT
MATERIAL A PRECURSOR OF THE ZONA PELLUCIDA ACCUMU
LATE AROUND MICROVILLI THAT HAVE FORMED ON THE SURFACE
OF THE OOCYTE FOLLICULAR CELLS DISPLAY FEWER MICROVILLI
$URING OOCYTE GROWTH BOTH THECAL AND FOLLICULAR CELLS
THICKEN AND MULTIPLY
#/24)#!, !,6%/,53 34!'%
4HE CORTICAL ALVEOLUS STAGE IS CHARACTERIZED BY THE INI
TIAL APPEARANCE OF THREE COMPONENTS #/24)#!, !,6%/,)
THE :/.! 0%,,5#)$! AND ,)0)$ &IGURE ! "EGOVAC
#(!04%2
AND 7ALLACE 3ELMAN AND 7ALLACE
3ELMAN 7ALLACE AND 0LAYER #ORTICAL ALVEOLI
INITIALLY APPEAR CIRCUMFERENTIALLY AT VARIOUS DEPTHS IN
THE CYTOPLASM 4HEY ARE MEMBRANE BOUND HAVE A HO
MOGENEOUS APPEARANCE AND GENERALLY STAIN FOR BOTH
PROTEIN AND CARBOHYDRATE 4HEIR SIZE AND STRUCTURE ARE
VARIABLE SOME CONTAIN A SINGLE LARGE GRANULE WITHIN
A HOMOGENEOUS MATRIX WHILE OTHERS CONTAIN ONLY THE
HOMOGENEOUS MATRIX &IGURES " AND 4HEY
APPEAR TO BE FORMED BY THE GRANULAR ENDOPLASMIC RE
TICULUM AND 'OLGI COMPLEX AND CONTAIN A GLYCOPRO
TEIN SYNTHESIZED WITHIN THE OOCYTE &IGURES % &
5LRICH 4ESORIERO 'URAYA "RUSL
3ELMAN 7ALLACE AND "ARR 3ELMAN AND
7ALLACE 4HESE MEMBRANE BOUND VESI
CLES ARE CLOSELY ASSOCIATED WITH THE 'OLGI COMPLEX
!S THE OOCYTES GROW THE CORTICAL ALVEOLI INCREASE IN
NUMBER AND THEIR SIZE BECOMES MORE HETEROGENEOUS
AS THEY lLL MUCH OF THE OOPLASM 4HEY ENLARGE SOME
TIMES TO M IN DIAMETER AND BY THE END OF THE
CORTICAL ALVEOLUS STAGE ALMOST lLL THE CYTOPLASM OF THE
OOCYTE )N SUBSEQUENT STAGES THEY CONTINUE TO FORM BUT
ARE DISPLACED TO THE PERIPHERY BY YOLK PROTEIN THAT AC
CUMULATES CENTRIPETALLY 4HE CORTICAL ALVEOLI INCREASE
IN SIZE AND NUMBER AS THEY MOVE PERIPHERALLY IN THE
OOPLASM &IGURE AND ARE FOUND AT LATER STAGES IN
VARIABLE SIZES AND NUMBERS BENEATH THE OOLEMMA SEE
REVIEW BY 3ELMAN AND 7ALLACE 4HE CORTICAL
ALVEOLI WILL LATER FUSE WITH THE OOLEMMA AND AT FERTIL
IZATION RELEASE THEIR GLYCOPROTEIN INTO THE PERIVITELLINE
SPACE DURING THE hCORTICAL REACTIONv
!LSO IN THE CORTICAL ALVEOLUS STAGE THERE IS A FORMA
TION AND AGGREGATION OF SMALL LIPID DROPLETS AROUND THE
NUCLEUS &IGURE ! $ 4HE LIPID MASS CONTINUES
TO ENLARGE IN A PERINUCLEAR POSITION ,ATER THE LIPID
DROPLETS INCREASE IN SIZE ,YSOSOME LIKE BODIES OF UN
CERTAIN FUNCTION ARE PRESENT OFTEN CONTAINING ELECTRON
DENSE MATERIAL 4HEY SEEM TO DISAPPEAR WHEN YOLK
BEGINS TO ACCUMULATE
4HE PRESENCE OF hYOLK VESICLESv IS OFTEN DESCRIBED
IN SMALL OOCYTES THESE APPEAR TO BE IDENTICAL IN STRUC
TURE AND COMPOSITION WITH THE CORTICAL ALVEOLI THAT
ARE PRESENT IN EGGS 3INCE YOLK VESICLES DO NOT CON
TAIN YOLK AS A NUTRIENT SOURCE IT IS SUGGESTED THAT THIS
DESIGNATION BE DROPPED IN FAVOUR OF hNASCENT CORTICAL
ALVEOLIv OR SIMPLY hCORTICAL ALVEOLIv 3ELMAN 7ALLACE
AND "ARR
0INOCYTOTIC VESICLES APPEAR DURING THE CORTICAL AL
VEOLUS STAGE AT THE BASES OF THE MICROVILLI 3HACKLEY
AND +ING "EGOVAC AND 7ALLACE 4HE
ZONA PELLUCIDA IS lRST OBSERVED AS A THIN 0!3 POSI
TIVE BAND BETWEEN THE OOCYTE AND FOLLICULAR CELLS WITH
THE ELECTRON MICROSCOPE IT APPEARS AS HOMOGENEOUS
MATERIAL BETWEEN THE MICROVILLI OF THE OOCYTE 4HE MI
CROVILLI LENGTHEN AS THE ZONA PELLUCIDA THICKENS 4HE
FOLLICULAR CELLS ALSO FORM MICROVILLI THAT INTERDIGITATE
WITH THE OOCYTE PROCESSES )N SOME lSH THE FOLLICULAR
CELLS REMAIN SQUAMOUS BUT IN THE BLENNY THEY BECOME
CUBOIDAL TO COLUMNAR 4HEY CONTAIN MITOCHONDRIA AND
GRANULAR ENDOPLASMIC RETICULUM 'OLGI COMPLEXES
BECOME MORE ABUNDANT !T THIS STAGE ONE OF THE FOL
LICULAR CELLS ENLARGES AND IS DESIGNATED THE -)#2/09,!2
#%,, )T LATER FORMS THE -)#2/09,% A PASSAGE FOR EVEN
TUAL SPERM PENETRATION THROUGH THE ZONA PELLUCIDA
#ORTICAL ALVEOLI APPEAR TO ARISE IN OOCYTES OF THE
LAMPREY ,AMPETRA PLANERI JUST BEFORE THE BEGINNING OF
VITELLOGENESIS "USSON -ABILLOT C THEY DO NOT
FORM IN OOCYTES OF THE DOGlSH 3COLIODON SORRAKOWAH
'URAYA
6)4%,,/'%.%3)3
4HE ENLARGEMENT OF THE OOCYTE THAT TAKES PLACE DURING
VITELLOGENESIS IS DUE LARGELY TO AN ACCUMULATION OF EX
OGENOUSLY DERIVED YOLK PROTEIN PRECURSORS "EGOVAC
AND 7ALLACE 4HIS PROTEIN IS IN GENERAL CALLED
FEMALE
SPECIlC SERUM PROTEIN &UJITA 4AKEMURA AND
4AKANO )N TELEOSTS THE RELATIVE CONTRIBUTION OF
PROTEIN YOLK DEPOSITION TO OOCYTE GROWTH IS OBSCURED
TO SOME EXTENT BY THE EXTENSIVE ELABORATION OF CORTI
CAL ALVEOLI THAT WAS INITIATED PRIOR TO VITELLOGENESIS AND
BY THE HYDRATION THAT FOLLOWS VITELLOGENESIS 7ALLACE
AND 3ELMAN -OST PROTEINS APPEAR TO BE SYN
THESIZED OUTSIDE THE OOCYTE HETEROSYNTHETIC ALTHOUGH
AUTOSYNTHETIC ORIGIN OF YOLK PROTEINS MAY ALSO OCCUR
7ALLACE 4HE FEMALE SPECIlC PROTEIN 6)4%,
,/'%.). IS A LARGE LIPOGLYCOPHOSPHOPROTEIN WHICH IS
SYNTHESIZED BY THE LIVER RELEASED INTO THE BLOOD AND
TRANSPORTED TO THE OVARY )NDEED THE ASSOCIATION BE
TWEEN LIVER AND OVARY IS INDICATED BY SIMULTANEOUS
INCREASES IN THE HEPATOSOMATIC AND GONADOSOMATIC
INDEXES DURING VITELLOGENESIS IN THE CATlSH (ETERO
PNEUSTES FOSSILIS 3RIVASTAVA AND 3AXENA 4HIS
PHASE IS DEPENDENT ON PITUITARY GONADOTROPIN +HOO
WHICH STIMULATES OESTROGEN PRODUCTION BY THE
OVARY 7ALLACE /ESTROGEN ESPECIALLY OESTRADI
OL
` TRANSPORTED IN THE BLOOD TO THE LIVER REGULATES
SYNTHESIS AND SECRETION OF VITELLOGENIN .AGAHAMA
!LSO IN RESPONSE TO GONADOTROPIN VITELLOGENIN
IS SELECTIVELY SEQUESTERED FROM THE BLOODSTREAM BY
/6!2)!. &/,,)#,%3
GROWING OOCYTES 6ITELLOGENIN ITSELF IS NOT INCORPO
RATED INTO TELEOST EGG YOLK BUT RATHER IS PROTEOLYTICALLY
CLEAVED WITHIN THE OOCYTE INTO YOLK PROTEINS OF WHICH
,)0/6)4%,,). AND 0(/36)4). ARE THE MOST FAMILIAR 7AL
LACE 'REELEY #ALDER AND 7ALLACE "Y
NOW ALL TYPES OF NON MAMMALIAN VERTEBRATES FROM
HAGlSH 9U ET AL SHARKS #RAIK A AND
OTHER lSH 7IEGAND TO TURTLES AND BIRDS HAVE
BEEN SHOWN TO SYNTHESIZE AND SECRETE VITELLOGENIN AS A
RESPONSE TO OESTROGEN
-ACROMOLECULES DESTINED FOR THE PRODUCTION OF
YOLK FOLLOW AN INTERCELLULAR ROUTE FROM THE MATERNAL
CIRCULATION TO THE SURFACE OF THE OOCYTE PENETRATING
BETWEEN THE ENDOTHELIAL CELLS OF THE PERIFOLLICULAR
CAPILLARIES TO ENTER THE CONNECTIVE TISSUE SURROUNDING
THE FOLLICLE 3ELMAN AND 7ALLACE B /N REACH
ING THE FOLLICULAR EPITHELIUM THEY PASS BETWEEN RATHER
THAN THROUGH ADJACENT FOLLICULAR CELLS EN ROUTE TO THE
OOCYTE /CCASIONAL EVIDENCE HAS BEEN FOUND FOR THE IN
TERNALIZATION BY MICROPINOCYTOSIS OF ELECTRON DENSE
TRACERS WITHIN THE FOLLICULAR CELLS BUT MOST MACROMOL
ECULES APPEAR TO PASS THROUGH EXTRACELLULAR CHANNELS
OF VARYING SIZES BETWEEN THE FOLLICULAR CELLS 3ELMAN
AND 7ALLACE A 4HE MOLECULES THEN PENETRATE
THE PATENT PORE CANALS OF THE ZONA PELLUCIDA &OLLICULAR
CELLS DO NOT APPEAR TO CONTRIBUTE TO YOLK FORMATION IN
TELEOSTS 3ELMAN AND 7ALLACE
0ROTEIN YOLK PRECURSORS ARE INCORPORATED INTO THE
OOCYTE BY INTENSE MICROPINOCYTOSIS OF THE OOLEMMA
BETWEEN THE BASES OF THE MICROVILLI &IGURES AND
$ROLLER AND 2OTH !NDERSON 5L
RICH 3HACKLEY AND +ING 3ELMAN AND 7AL
LACE A !BRAHAM ET AL "RUSL
+JESBU +RYVI AND .ORBERG AND TRANSLOCATED TO
YOLK SPHERES IN LESS THAN MIN 3ELMAN AND 7ALLACE
B #OATED PITS ARE NUMEROUS ALONG THE OOLEMMA
BETWEEN THE MICROVILLI AND MICROPINOCYTOTIC VESICLES
AS WELL AS SMOOTH SURFACED TUBULES LIE TOGETHER IN THE
CORTICAL OOPLASM -ICROPINOCYTOSIS OF EXTERNAL MATE
RIALS BY THE OOCYTE IS THE MOST CHARACTERISTIC CELLULAR
EVENT OF VITELLOGENESIS 3ELMAN AND 7ALLACE A
$URING VITELLOGENESIS THE ZONA PELLUCIDA THICKENS
AND THE OOCYTE CONTINUES TO FORM CORTICAL ALVEOLI 3EL
MAN AND 7ALLACE A 4HE MOST OBVIOUS
EVENT MARKING THE INITIATION OF VITELLOGENESIS HOWEV
ER IS THE APPEARANCE OF MEMBRANE BOUND mUID lLLED
YOLK SPHERES LYING BETWEEN THE CORTICAL ALVEOLI IN THE
PERIPHERAL OOPLASM &IGURE
4WO TYPES OF YOLKY INCLUSIONS ARE FORMED DURING
VITELLOGENESIS ,)0)$ 9/,+ $2/0,%43 AND MASSES OF 02/
4%). 9/,+ 9AMAMOTO 3HACKLEY AND +ING
7ALLACE AND 3ELMAN -AYER 3HACKLEY
AND 2YLAND 3ELMAN AND 7ALLACE 3ELMAN
ET AL 4HE lRST TYPE OF YOLKY INCLUSION TO AC
CUMULATE IN MOST SPECIES IS LIPID YOLK IN THE FORM OF
DISTINCT LIPID DROPLETS IN THE BASS THESE MAKE THEIR AP
PEARANCE IN THE OUTER CORTEX BUT IN MOST TELEOSTS THEY
lRST APPEAR IN THE PERINUCLEAR CYTOPLASM GIVING RISE
TO SUGGESTIONS THAT THEY ARE PROBABLY FORMED ENDOG
ENOUSLY &IGURE 0ROTEIN YOLK ACCUMULATION IS
EXOGENOUS IN ORIGIN AND OCCURS AFTER AND CONCOMI
TANT TO LIPID YOLK ACCUMULATION )N MOST TELEOSTS YOLK
PROTEINS ACCUMULATE IN mUID lLLED YOLK SPHERES THAT
MAY EITHER MAINTAIN THEIR INTEGRITY THROUGHOUT OOCYTE
GROWTH OR FUSE CENTRIPETALLY EVENTUALLY FORMING A CON
TINUOUS MASS OF mUID YOLK A PROCESS WHICH CONFERS
ON MANY TELEOST EGGS THEIR CHARACTERISTIC TRANSPARENCY
&IGURE 4HIS COALESCENCE CAN OCCUR RELATIVELY
SOON AFTER THE INITIAL FORMATION OF YOLK SPHERES AS IN
STICKLEBACKS AND THE PIPElSH DURING THE LATER STAGES OF
VITELLOGENESIS AS IN THE SHEEPSHEAD MINNOW OR DURING
MATURATION AS IN THOSE MARINE TELEOSTS THAT PRODUCE
PELAGIC EGGS #REATION OF A CENTRAL MASS OF mUID YOLK
DISPLACES THE OOPLASM WITH ITS CORTICAL ALVEOLI AND
LIPID DROPLETS TO THE PERIPHERY OF THE OOCYTE &IGURE
! FEW YOLK SPHERES ALWAYS REMAIN IN THE PERIPH
ERAL OOPLASM BUT APPEAR TO BE REDUCED IN NUMBER AS
THE CENTRAL MASS INCREASES &IGURE 3HACKLEY AND
+ING
)N SOME SPECIES PROTEIN YOLK IS SEQUESTERED IN THE
FORM OF DISCRETE GRANULES THAT STAIN INTENSELY FOR PRO
TEINS BUT NOT FOR LIPIDS OR CARBOHYDRATES &IGURE
3ELMAN AND 7ALLACE 3ELMAN ET AL 4HE
SURFACE OF THE OOCYTE DISPLAYS CONSIDERABLE ENDOCYTO
TIC ACTIVITY DURING THIS STAGE AND ELECTRON DENSE MATE
RIAL IS VISIBLE IN SOME ENDOCYTOTIC STRUCTURES 4HE YOLK
PLATELETS OF THE ZEBRAlSH "RACHYDANIO RERIO ARE VARI
ABLE IN SIZE AND SOME MAY ATTAIN DIAMETERS OF M
4HE CONTENTS OF MOST OF THESE YOLK BODIES ARE NOT HO
MOGENEOUS AND GENERALLY DISPLAY ONE TO SEVERAL RECTI
LINEAR MASSES EMBEDDED IN A HOMOGENEOUS MATRIX )N
APPROPRIATELY ORIENTED SECTIONS THESE MASSES DISPLAY
AN ORTHORHOMBIC CRYSTALLINE STRUCTURE WITH PARALLEL
DENSE BANDS APPROXIMATELY NM APART &IGURE
4HIS GRANULAR YOLK BECOMES THE PREDOMINANT YOLK IN
CLUSION AND DENSELY PACKS THE MID AND OUTER CORTEX
5NLIKE THE mUID YOLK DROPLETS THAT COALESCE AS THEY
MIGRATE CENTRIPETALLY PROTEIN YOLK GRANULES MAINTAIN
THEIR STRUCTURAL INTEGRITY UNTIL MATURATION AFTER WHICH
THEY ACTIVELY COALESCE
#(!04%2
9/,+ '2!.5,%3 ARE CHARACTERISTIC OF FRESHWATER TE
LEOSTS ,ANGE ET AL ALTHOUGH THEY HAVE BEEN
NOTED IN EGGS OF THE COD 'ADUS MORHUA +JESBU AND
+RYVI !S DESCRIBED IN A WIDE RANGE OF lSHES
THEY CONSIST OF ONE OR MORE CRYSTALLINE MAIN BODIES
WITHIN AN AMORPHOUS SUPERlCIAL LAYER ENCLOSED BY A
MEMBRANE &IGURE 9AMAMOTO AND /OTA
7ALLACE %LEGANT CRYSTALS HAVE BEEN DESCRIBED
WITHIN THE MAIN BODY OF YOLK PLATELETS FROM A WIDE
VARIETY OF lSHES CYCLOSTOMES +ARASAKI 5LRICH
0ATZNER ,ANGE AND 2ICHTER ,ANGE
TELEOSTS ,ANGE ET AL AND THE ANCIENT
lSHES 0OLYPTERUS BICHIR !MIA CALVA AND ,EPISOSTEUS
OSSEUS ,ANGE 'RODZINSKI AND +ILARSKI 4HE
CRYSTALS OF CYCLOSTOMES APPEAR TO BE A MONOCLINIC LAT
TICE OF POSSIBLY SYMMETRIC LIPOVITELLIN
PHOSVITIN DI
MERS WHEREAS THOSE OF TELEOSTS AND THE ANCIENT lSHES
ARE AN ORTHORHOMBIC ARRAY OF LIPOVITELLIN
PHOSVITIN
COMPLEXES CONSISTING OF TWO SUBUNITS THAT ARE LIKELY
NOT IDENTICAL 4HIS CRYSTALLINE STRUCTURE IS RARE IN MA
RINE SPECIES SUGGESTING THAT THE CRYSTALS MAY STORE ES
SENTIAL NUTRIENTS UNAVAILABLE IN FRESH WATER PROVIDING
REGULARLY PACKED MICROCHAMBERS THAT SEQUESTER LOW
MOLECULAR WEIGHT PARTICLES OR IONS ,ANGE 'RODZINS
KI AND +ILARSKI 8
RAY ANALYSIS OF CRYOSECTIONS
INDICATES THE PRESENCE OF CHLORIDE AND A VARIETY OF CAT
IONS WITHIN THE PLATELETS ,ANGE ,ANGE ET
AL
%ARLY VITELLOGENESIS IN THE PIPElSH IS CHARACTER
IZED BY THE APPEARANCE OF INDIVIDUAL SMALL MEM
BRANE
BOUND YOLK SPHERES IN THE OOCYTE PERIPHERY AND
INTERIOR &IGURES ! TO # "EGOVAC AND 7ALLACE
!S VITELLOGENESIS PROGRESSES THE YOLK SPHERES
INCREASE IN SIZE WHILE THE CORTICAL ALVEOLI AND LIPID ARE
DISPLACED TO THE PERIPHERAL OOPLASM %VENTUALLY THE
YOLK SPHERES COALESCE TO FORM A CENTRAL mUID MASS THE
CORTICAL ALVEOLI AND LIPID REMAIN IN THE PERIPHERAL PART
OF THE YOLK MASS 9OLK SPHERES ARE MODERATELY ELECTRON
DENSE AND CONTAIN HIGHLY ELECTRON
DENSE INCLUSIONS
THAT OCCASIONALLY HAVE A lNELY GRANULAR APPEARANCE AND
PROVIDE A SPECIlC RELIABLE MARKER FOR FOLLOWING YOLK
FORMATION &IGURES $ % 4HERE ARE THREE TYPES OF
SMALL YOLK SPHERES PRIMARY TRANSITIONAL AND MATURE
02)-!29 9/,+ 30(%2%3 APPEAR TO CONTAIN PROTEINACEOUS
MATERIAL INTERSPERSED AMONG MULTIVESICULAR ELEMENTS
).4%2-%$)!4% 42!.3)%.4 9/,+ 30(%2%3 CONTAIN PROTEIN
ACEOUS MATERIAL VARIABLE VESICULAR ELEMENTS AND THE
YOLK
SPECIlC ELECTRON
DENSE INCLUSION -!452% 9/,+
30(%2%3 CONTAIN HOMOGENEOUS CONDENSED YOLK AND A
HETEROGENEOUS SIZE AND DISTRIBUTION OF THE YOLK
SPE
CIlC MARKER &IGURES $ & )T IS SUGGESTED THAT
THE MULTIVESICULAR BODIES REPRESENT A MODIlED LYSO
SOMAL COMPARTMENT INVOLVED IN YOLK SPHERE FORMATION
"EGOVAC AND 7ALLACE 3ECONDARY LYSOSOMES
OR MULTIVESICULAR BODIES ARE SEEN ADJACENT TO CORTICAL
ALVEOLI IN OOCYTES OF THE SEAHORSE AND PIPElSH AT ABOUT
THE TIME OF THE ONSET OF VITELLOGENESIS &IGURE
AND MAY BE REQUIRED FOR THE PROTEOLYTIC PROCESSING
INTO MATURE YOLK PROTEINS OF THE VITELLOGENIN TAKEN UP
BY ENDOCYTOSIS &IGURE ' 3ELMAN 7ALLACE AND
0LAYER -ULTIVESICULAR BODIES SEEM TO DISAP
PEAR AS VITELLOGENESIS PROGRESSES
4HE INVOLVEMENT OF LYSOSOMES OR MULTIVESICULAR
BODIES IN VITELLOGENESIS HAS BEEN DEMONSTRATED IN OO
CYTES OF THE TROUT 3ALMO TRUTTA FARIO "USSON -ABILLOT
!T AN EARLY STAGE OF DEVELOPMENT LYSOSOMES
ARISE IN THE CORTICAL OOPLASM AND MIGRATE CENTRIPETALLY
ALMOST REACHING THE NUCLEUS EVENTUALLY THEY CONSTI
TUTE THE MOST VOLUMINOUS COMPARTMENT OF THE OOCYTE
&IGURE 4HEY ARE MEMBRANE BOUND AND CONTAIN
SMALL VESICLES AND CLUMPS OF lNELY GRANULAR MATERIAL
&IGURE ! #ONTINUITIES ARE ABUNDANT BETWEEN THE
AGRANULAR ENDOPLASMIC RETICULUM AND THE MEMBRANE
ENCLOSING THE LYSOSOMES &IGURE " !T THE BEGIN
NING OF VITELLOGENESIS ENDOCYTOTIC VESICLES CONTAINING
VITELLOGENIN FUSE WITH ONE ANOTHER TO FORM LARGER VES
ICLES AND THESE THEN FUSE WITH LYSOSOMES TO FORM YOLK
BODIES THAT MAY ATTAIN DIAMETERS UP TO M &IGURE
'RANULAR MATERIAL GRADUALLY lLLS THE LYSOSOMES
AT THE ONSET OF VITELLOGENESIS AND OVER SEVERAL WEEKS
THIS TRANSFORMS INTO HOMOGENEOUS YOLK &IGURE
/THER CHANGES ARE APPARENT WITHIN THE FOLLICLE DUR
ING VITELLOGENESIS 3ELMAN AND 7ALLACE "EGO
VAC AND 7ALLACE +JESBU +RYVI AND .ORBERG
4HE GERMINAL VESICLE IS PROGRESSIVELY DISPLACED
TOWARD THE ANIMAL POLE AS YOLK ACCUMULATES CENTRIP
ETALLY WITHIN THE OOCYTE 3OME SMALL LIPID DROPLETS
REMAIN ASSOCIATED WITH THE GERMINAL VESICLE WHILE
OTHERS BEGIN TO FUSE REACHING DIAMETERS OF TO
M AND RESIDE IN THE PERIPHERAL OOPLASM )N &UNDULUS
THE ZONA PELLUCIDA CONTINUES TO ENLARGE ACQUIRING AN
ELABORATE STRUCTURE WHEREAS IN 3YNGNATHUS IT UNDER
GOES CONDENSATION 4HERE IS A CLOSE STRUCTURAL RELATION
SHIP BETWEEN BUNDLES OF MICROlLAMENTS AND ANNULATE
LAMELLAE IN VITELLOGENIC OOCYTES +ESSEL "EAMS AND
4UNG )T IS SUGGESTED THAT THERE IS A COPARTICIPA
TION OF PORES OF THE ANNULATE LAMELLAE AND POLYRIBO
SOMES IN THE DEVELOPMENT OF MICROlLAMENT BUNDLES
6ITELLOGENESIS IN THE ELASMOBRANCH 3CYLIORHINUS
CANICULA DOES NOT APPEAR TO DIFFER FUNDAMENTALLY FROM
/6!2)!. &/,,)#,%3
OTHER VERTEBRATES EITHER IN THE MECHANISM OF VITELLO
GENESIS OR IN ITS IMMEDIATE ENDOCRINE CONTROL #RAIK
A B C D E 6ITELLOGENIN IS PRESENT IN THE PLASMA
THROUGHOUT THE YEAR AND ITS UPTAKE BY GROWING OVARIAN
FOLLICLES SEEMS TO BE STIMULATED BY A HORMONE FROM THE
CRANIAL PARS DISTALIS OF THE PITUITARY
!N UNUSUAL FORM OF YOLK UPTAKE IS DESCRIBED IN
THE LAMPREY 0ETROMYZON MARINUS WHERE BOTH THE OO
CYTE AND CERTAIN ENLARGED FOLLICULAR CELLS THE hNURSE
CELLSv SIMULTANEOUSLY FORM YOLK PLATELETS ,EWIS AND
-C-ILLAN 4HESE CELLS EVENTUALLY FUSE AND THE
YOLK RICH CYTOPLASM FROM THE NURSE CELLS IS INCORPO
RATED INTO THE OOCYTE 4HE NUCLEUS OF THE NURSE CELL
DISAPPEARS
-!452!4)/.
&OLLOWING VITELLOGENESIS OOCYTES UNDERGO -!452!4)/.
WITH THE RESUMPTION OF THE MEIOTIC OR hMATURATIONv DI
VISION THAT HAS BEEN ARRESTED IN PROPHASE ) SINCE THEIR
TRANSFORMATION FROM OOGONIA !T THIS TIME THE FOLLICLES
APPEAR TO ATTAIN A CRITICAL SIZE BECOMING COMPETENT TO
RESPOND TO -!452!4)/.
).$5#).' (/2-/.%3 -)( BY
INITIATING MATURATION $IAMETERS OF TO MM HAVE
BEEN RECORDED IN SEABREAM 3PARUS AURATA 'OTHILF ET
AL TO MM IN ZEBRAlSH "RACHYDANIO
RERIO 3ELMAN ET AL TO MM IN MEDAKA
/RYZIAS LATIPES )WAMATSU ET AL TO MM
IN KILLIlSH &UNDULUS HETEROCLITUS 3ELMAN AND 7AL
LACE AND TO MM IN THE PIPElSH 3YNGNA
THUS SCOVELLI "EGOVAC AND 7ALLACE ! FURTHER
INCREASE IN SIZE OCCURS BY HYDRATION DURING MATURATION
IN MANY TELEOSTS ESPECIALLY MARINE FORMS -ATURATION
DIVISION IS FOLLOWED BY CONDENSATION OF THE CHROMO
SOMES AND EXPULSION OF THE lRST POLAR BODY
!T THE BEGINNING OF MATURATION THE OOCYTE HAS A
LARGE NUCLEUS OR '%2-).!, 6%3)#,% LOCATED CENTRALLY OR
HALFWAY BETWEEN THE CENTRE AND PERIPHERY 7ALLACE
AND 3ELMAN .AGAHAMA +JESBU
+RYVI AND .ORBERG 'OTHILF ET AL IT
IS INCONSPICUOUS IN WHOLE OOCYTES OF MANY TELEOSTS
&IGURE 4HE NUCLEUS IS IN MEIOTIC PROPHASE AND
CONTAINS LAMPBRUSH CHROMOSOMES 4HE lRST VISIBLE
EVENT ASSOCIATED WITH lNAL OOCYTE MATURATION IS THE
MIGRATION OF THE GERMINAL VESICLE TO THE ANIMAL POLE
AT WHICH TIME IT BECOMES VISIBLE UNDER THE DISSECT
ING MICROSCOPE 4HE ENVELOPE OF THE GERMINAL VESICLE
BREAKS DOWN '%2-).!, 6%3)#,% "2%!+$/7. '6"$
AND THE NUCLEAR CONTENTS BLEND WITH THE SURROUNDING
CYTOPLASM 4HIS PROVIDES A MORPHOLOGICALLY IDENTIl
ABLE EVENT THAT MAY CONVENIENTLY BE USED TO DIVIDE
MATURATION INTO TWO PHYSIOLOGICALLY DISTINCT PHASES
%!2,9 -!452!4)/. PRE '6"$ AND ,!4% -!452!4)/.
POST '6"$ 3ELMAN AND 7ALLACE 'ERMINAL
VESICLE BREAKDOWN GENERALLY OCCURS IN &UNDULUS HET
EROCLITUS WHEN THE FOLLICLE REACHES A DIAMETER OF TO
MM 7ALLACE AND 3ELMAN
%ARLY MATURATION IS CHARACTERIZED BY A RAPID INCREASE
IN FOLLICULAR VOLUME PRIMARILY DUE TO HYDRATION BUT THE
CONTINUED ACCUMULATION OF HETEROSYNTHETIC MACROMOL
ECULES BY ENDOCYTOSIS ACCOUNTS FOR ABOUT OF THIS
INCREASE 7ALLACE AND 3ELMAN 0ROTEIN INCOR
PORATION APPEARS TO STOP ABRUPTLY AT THE TIME OF GER
MINAL VESICLE BREAKDOWN 4HIS IS CONSISTENT WITH THE
OBSERVATION THAT OOCYTES IN EARLY MATURATION CONTINUE
TO DISPLAY ENDOCYTOTIC ACTIVITY AT THEIR SURFACE WHEREAS
THOSE IN LATE MATURATION DO NOT $URING HYDRATION YOLK
POLYPEPTIDES PRESENT IN EARLY MATURATIONAL OOCYTES UN
DERGO PROTEOLYSIS )N LATE MATURATION AFTER GERMINAL
VESICLE BREAKDOWN THE FOLLICLE CONTINUES TO ENLARGE BY
HYDRATION 7ITHIN THE OOCYTE LIPID DROPLETS CONTINUE
TO COALESCE LOSE THEIR PERIPHERAL ATTACHMENTS AND ARE
ABLE TO MOVE FREELY THROUGH THE OOCYTE &IGURE
)MMEDIATELY PRIOR TO OVULATION THEY COLLECT AT THE UP
PER SURFACE OF THE OOCYTE AND WILL mOAT TO THE OPPOSITE
POLE IF THE FOLLICLE IS INVERTED $URING MATURATION THE
YOLK BODIES OF THE ZEBRAlSH "RACHYDANIO RERIO LOSE
THEIR CRYSTALLINE MASSES AND DEVELOP A HOMOGENEOUS
INTERIOR &IGURE 3ELMAN ET AL
&OLLICULAR MATURATION IS CONTROLLED BY PITUITARY
GONADOTROPIN WHICH INDUCES A SHIFT IN FOLLICULAR STE
ROIDOGENESIS AWAY FROM THE PRODUCTION OF OESTRADIOL
` NECESSARY FOR VITELLOGENESIS AND OOCYTE GROWTH
TO THE PRODUCTION OF THE MATURATION INDUCING HORMONE
-)( REQUIRED FOR THE RESUMPTION OF MEIOSIS 0ATIO
AND 4HOMAS 4HOMAS AND 0ATIO .AGA
HAMA ET AL /OCYTES MUST BE PRIMED WITH GO
NADOTROPIN BEFORE MATURATION CAN BE INDUCED BY -)(
4HIS OCCURS BEFORE COALESCENCE OF THE LIPID DROPLETS
AND INCLUDES SYNTHESIS OF RECEPTORS FOR THE -)( #ON
SIDERABLE EVIDENCE HAS ACCUMULATED ESPECIALLY IN
3ALMONIFORMES *ALABERT $UFFEY AND 'OETZ
.AGAHAMA .AGAHAMA AND !DACHI
+ANAMORI !DACHI AND .AGAHAMA BUT
IN OTHER BONY lSH AS WELL *ALABERT 'OETZ AND
4HEOFAN 'REELEY ET AL ,EVAVI :ERMON
SKY AND 9ARON !SAHINA 4AGUCHI AND (IBIYA
+OBAYASHI ET AL 3CHOONEN ET AL
3UZUKI 4AN AND 4AMAOKI (AIDER ,ESS
MAN 0ETRINO ET AL &UKADA ET AL
4HE EXTENSIVE LITERATURE ON MATURATION
INDUCING HORMONES IN TELEOSTS HAS BEEN REVIEWED BY 'OETZ 3COTT AND #ANARIO
.AGAHAMA ET AL AND 0ETER AND 9U
#(!04%2
'OTHILF ET AL INDICATING THAT THE MAJOR NATU
RALLY OCCURRING -)( IS _ ` DIHYDROXY PREG
NEN ONE _ ` $0 4HIS STEROID IS SYNTHESIZED
COLLABORATIVELY BY BOTH THE THECAL AND FOLLICULAR LAY
ERS GONADOTROPIN STIMULATES THECAL CELLS TO PRODUCE
_ HYDROXYPROGESTERONE WHICH IS CONVERTED WITHIN
THE FOLLICULAR CELLS TO _ ` DIHYDROXY PREGNENE
ONE &IGURE .AGAHAMA AND !DACHI
.AGAHAMA .AGAHAMA ET AL /THER #
STEROIDS HAVE BEEN SHOWN TO BE EQUALLY POTENT IN IN
DUCING MATURATION IN A NUMBER OF SPECIES AT LEAST IN
VITRO AND ALL HAVE A AND ` HYDROXYL GROUP AND
ARE STRUCTURALLY SIMILAR TO _ ` DIHYDROXY PREG
NENE ONE 3COTT AND #ANARIO )N TWO SPECIES
OF SCIAENID lSH 0ERCIFORMES THE PREDOMINANT STE
ROID PRODUCED DURING lNAL OOCYTE MATURATION AND THE
NATURAL -)( IS _ ` TRIHYDROXY PREGNENE
ONE ` 3 4RANT 4HOMAS AND 3HACKLETON
4HOMAS AND 4RANT 4RANT AND 4HOMAS A B
"OTH HORMONES _ ` $0 AND ` 3 MAY PLAY A
ROLE IN INDUCING MATURATION IN THE STRIPED BASS -ORONE
SAXATILIS AND WHITE PERCH - AMERICANA 0ERCIFORMES
+ING ET AL +ING 4HOMAS AND 3ULLIVAN
+ING "ERLINSKY AND 3ULLIVAN -ATURATION OF
OOCYTES OF THE WINTER mOUNDER 0LEURONECTES AMERICA
NUS 0LEURONECTIFORMES APPEARS TO BE INDUCED BY THE
SYNERGISM OF SEVERAL STEROIDS DISTINCT FROM THE PROGES
TERONES WHICH PREDOMINATE IN OTHER lSH 4RUSCOTT ET
AL )T IS OF INTEREST TO NOTE THAT _ ` DIHY
DROXY PREGNENE ONE HAS BEEN DETECTED IN THE SE
RUM OF THE SEA LAMPREY 0ETROMYZON MARINUS DURING
THE EARLY SPAWNING MIGRATION SUGGESTING A ROLE IN
MATURATION AND OVULATION OF THIS CYCLOSTOME 7EISBART
ET AL
02/4%!3/-%3 APPEAR TO PLAY A ROLE IN THE MATURATION
OF lSH OOCYTES SEE REVIEW BY 4OKUMOTO 4HESE
PROTEOLYTIC COMPLEXES ARE FOUND IN EUKARYOTIC CELLS
AND ARE RESPONSIBLE FOR THE DEGRADATION OF MOST CEL
LULAR PROTEINS INCLUDING STRUCTURAL PROTEINS ENZYMES
AND PROTEINS THAT REGULATE CELL CYCLES #OUX 4ANAKA
AND 'OLDBERG 0ROTEASOMES HELP TO REGULATE THE
AMOUNT OF A PARTICULAR PROTEIN PRESENT IN A CELL AT A
GIVEN TIME 4HERE ARE TWO TYPES OF PROTEASOMES 3
K$A AND 3 K$A 4HE 3 PROTEASOME
FORMS THE CATALYTIC CORE OF THE 3 WHICH CONSISTS OF
A CENTRAL CYLINDER FORMED FROM PROTEASES WHOSE ACTIVE
SITES ARE THOUGHT TO FACE AN INNER CHAMBER %ACH END
OF THE CYLINDER IS CAPPED BY A LARGE PROTEIN COMPLEX
THESE COMPLEXES ARE THOUGHT TO BIND PROTEINS DESTINED
FOR DIGESTION AND THEN FEED THEM INTO THE INNER CHAM
BER !CTIVITY OF PROTEASOME 3 INCREASED IN OOCYTES
OF THE GOLDlSH #ARASSIUS AURATUS WITHIN ONE HOUR AF
TER EXPOSURE TO -)( AND THEN DECLINED IT ROSE AGAIN
AFTER COMPLETION OF '6"$ 4OKUMOTO ET AL
)T WAS CONCLUDED THAT PROTEASOME 3 IS INVOLVED IN
TWO STEPS IN THE MEIOTIC CYCLE OF MATURATION THE EARLY
STAGE FOLLOWING STIMULATION BY -)( BEFORE MIGRATION
OF THE GERMINAL VESICLE AND LATER AT THE TRANSITION FROM
METAPHASE ) TO ANAPHASE ) 4HE NATURE OF THE PROTEINS
BEING DEGRADED AT THESE TIMES IS STILL UNCERTAIN BUT PRO
TEINS CRITICAL TO THE REGULATION OF THE CELL CYCLE HAVE
BEEN SUGGESTED
4HE ULTRASTRUCTURE OF OOCYTES APPROACHING THE RE
SUMPTION OF MEIOSIS HAS BEEN DESCRIBED IN VITRO AND IN
VIVO IN OOCYTES OF THE MEDAKA /RYZIAS LATIPES )WAMAT
SU ET AL )MMEDIATELY BEFORE GERMINAL
VESICLE BREAKDOWN TETRAD CHROMOSOMES MAY BE DE
TECTED IN THE CENTRAL PART OF THE LARGE GERMINAL VESICLE
"EFORE MATURATION BEGINS THERE ARE MANY MITOCHON
DRIA ANNULATE LAMELLAE GRANULAR ENDOPLASMIC RETICU
LUM AND 'OLGI COMPLEXES IN THE CORTICAL CYTOPLASM
&IGURE 'ERMINAL VESICLE BREAKDOWN LEADS TO
THE FORMATION OF THE SPINDLE OF MEIOSIS AND WITHIN
THREE HOURS MEIOSIS PROGRESSES THROUGH PROMETAPHASE
) TO METAPHASE ) &OLLOWING A SHORT TIME IN ANAPHASE )
THE lRST MATURATION DIVISION IS COMPLETE BY FOUR HOURS
4HE OOCYTES REACH METAPHASE )) ABOUT lVE HOURS AFTER
GERMINAL VESICLE BREAKDOWN AND THE lRST POLAR BODY
IS EXTRUDED AT THE ANIMAL POLE !LL CYTOPLASMIC PRO
JECTIONS OF BOTH THE OOCYTE AND FOLLICULAR CELLS HAVE
WITHDRAWN FROM THE ZONA PELLUCIDA BY THE TIME OF OVU
LATION /VULATION TAKES PLACE AT THE END OF THIS STAGE
! FEW 'OLGI COMPLEXES AND NO ANNULATE LAMELLAE ARE
NOTED IN THE OVULATED EGGS OF THE MEDAKA )WAMATSU ET
AL 4HE MEIOTIC PROCESS LEADING TO THE EXPUL
SION OF THE SECOND POLAR BODY IS RESUMED AT THE TIME
OF FERTILIZATION AND SPERM PENETRATION
2EORGANIZATION OF THE MICROTUBULAR CYTOSKELETON
DURING MATURATION IN OOCYTES OF THE GOLDlSH #ARASSIUS
AURATUS HAS BEEN RECORDED BY CONFOCAL IMMUNOmUO
RESCENCE MICROSCOPY USING AN ANTI
TUBULIN ANTIBODY
*IANG ET AL )N FULLY GROWN IMMATURE OOCYTES
THE YOLK GRANULES APPEAR AS DARK MASSES SUSPENDED
WITHIN THE GLOWING MESHES OF A MICROTUBULAR NETWORK
THAT EXTENDS THROUGHOUT THE OOPLASM EXCEPT FOR THE
REGION CONTAINING THE GERMINAL VESICLE ! CONDENSED
BAND OF MICROTUBULES SURROUNDS THE GERMINAL VESICLE
&IGURE THESE MICROTUBULES PLAY A ROLE IN STABI
LIZING THE GERMINAL VESICLE AT THE CENTRE OF THE OOCYTE
7HEN THE GERMINAL VESICLE BEGINS ITS MIGRATION THE
/6!2)!. &/,,)#,%3
MICROTUBULAR NETWORK DISAPPEARS PERMITTING MOVE
MENT TOWARD THE ANIMAL POLE #YTOPLASMIC MICROTU
BULES GRADUALLY CONCENTRATE IN THE ANIMAL HEMISPHERE
!S THE GERMINAL VESICLE MIGRATES IT TRAILS A GLOWING
hPERINUCLEAR TAILv OF CONDENSED MICROTUBULES FROM ITS
VEGETAL SURFACE IT APPEARS THAT THE PERINUCLEAR TAIL PER
MITS THE ACCUMULATION OF CYTOPLASMIC MATERIALS THAT
ARE NECESSARY FOR THE SUBSEQUENT MATURATION &IGURE
)T IS PRESUMED THAT CYTOPLASMIC MICROlLAMENTS
CONTRIBUTE THE MOTIVE POWER FOR MIGRATION OF THE GER
MINAL VESICLE #OINCIDENT WITH THE BREAKDOWN OF THE
GERMINAL VESICLE '6"$ NUMEROUS MICROTUBULES
PENETRATE THE GERMINAL VESICLE FROM ITS VEGETAL SURFACE
AND A DISC SHAPED RING OF CONDENSED MICROTUBULES IS
SEEN AT THE ANIMAL POLE REGION SUGGESTING A ROLE IN
SPINDLE FORMATION OR THE ORGANIZATION OF MEIOTIC CHRO
MOSOMES &IGURES AND
4HE MARKED HYDRATION OF OOCYTES DURING MATURA
TION IS ESPECIALLY PRONOUNCED IN MARINE TELEOSTS WITH
PELAGIC OR mOATING EGGS ALTHOUGH IT OCCURS TO A LESSER
EXTENT DURING MATURATION IN MANY BRACKISH WATER AND
MARINE SPECIES WITH NON mOATING OR DEMERSAL EGGS
#RAIK AND (ARVEY 'REELEY #ALDER AND
7ALLACE 4HORSEN AND &YHN 4HE mOAT
ING EGGS OF MANY MARINE TELEOST SPECIES CONTAIN ABOUT
WATER #RAIK AND (ARVEY 4HEY OWE
THEIR BUOYANCY TO THIS HIGH WATER CONTENT RATHER THAN
FOR EXAMPLE TO LOW DENSITY LIPIDS 3UCH EGGS CONTAIN A
MORE DILUTE AQUEOUS SOLUTION THAN SEAWATER ITSELF AND
ARE CONSEQUENTLY LESS DENSE )N THESE SPECIES THERE IS A
MASSIVE AND RAPID UPTAKE OF WATER DURING MATURATION
INCREASING THE VOLUME OF THE OOCYTE BY A FACTOR OF FOUR
OR lVE THE RESULTING MATURE BUOYANT EGG IS OVULATED
SHORTLY THEREAFTER 4HIS WATER UPTAKE IS CLEARLY AN AD
APTATION LEADING TO WIDE DISPERSAL OF THE mOATING EGGS
BY WATER CURRENTS AND IS THUS RELATED TO THE HIGH FECUN
DITY OF THESE SPECIES &ULTON CITED BY 7ALLACE
4HERE IS EVIDENCE OF SECONDARY PROTEOLYSIS OF YOLK
PROTEINS DURING MATURATION BEING MOST PRONOUNCED
IN MARINE SPECIES WITH PELAGIC EGGS WHERE ITS EXTENT
IS WELL CORRELATED WITH THE EXTENT OF OOCYTE HYDRATION
'REELEY #ALDER AND 7ALLACE ! LARGE POOL OF
FREE AMINO ACIDS THAT IS PRESENT IN PELAGIC MARINE lSH
EGGS ORIGINATES MAINLY FROM THE HYDROLYSIS OF YOLK
PROTEINS DURING lNAL OOCYTE MATURATION 4HORSEN AND
&YHN 4HIS MAY ASSIST HYDRATION BY INCREASING
OSMOTIC POTENTIAL WITHIN THE OOPLASM OR BY SUPPLYING
ENERGY FOR HYDRATION TO OCCUR PERHAPS BY BREAKING
HIGH ENERGY PHOSPHORUS BONDS
4HREE FACTORS HAVE CONTRIBUTED TO THE ENLARGEMENT OF
OOCYTES EXTENSIVE ELABORATION OF CORTICAL ALVEOLI BEFORE
VITELLOGENESIS DEPOSITION OF PROTEIN YOLK AND HYDRA
TION FOLLOWING VITELLOGENESIS THE RELATIVE CONTRIBUTIONS
OF EACH ARE DIFlCULT TO ASCERTAIN &OLLICULAR GROWTH IN
&UNDULUS HETEROCLITUS FROM A DIAMETER OF
UP TO MM IS DUE TO VITELLOGENIN UPTAKE BY
THE GROWING OOCYTE WHILE lNAL ENLARGEMENT FROM
UP TO MM DURING MATURATION IS
THE RESULT OF HYDRATION 7ALLACE AND 3ELMAN
$URING MATURATION THE OOCYTE BECOMES MORE TRANS
LUCENT AS LIPID AND PROTEIN YOLK DROPLETS COALESCE
#OMPLETE FUSION OF YOLK DROPLETS DOES NOT OCCUR IN ALL
SPECIES AND IT HAS BEEN NOTED THAT THE DEGREE OF CO
ALESCENCE OF THE LIPID DROPLETS FOLLOWS A PHYLOGENETIC
PATTERN FORMING ONE MAJOR DROPLET IN HIGHER TELEOSTS
SUCH AS YELLOW PERCH 0ERCA mAVESCENS WALLEYE 3TI
ZOSTEDION VITREUM STRIPED BASS 2OCCUS SAXATILIS AND
PARADISElSH -ACROPODUS OPERCULARIS BUT SHOWING
LESS COALESCENCE IN LOWER TELEOSTS BROOK TROUT 3ALVE
LINUS FONTINALIS AND RAINBOW TROUT 3ALMO GAIRDNERI
WHERE OVULATED OOCYTES CONTAIN A LARGE NUMBER OF LIP
ID DROPLETS 'OETZ )N SOME INTERMEDIATE TELE
OSTS STICKLEBACKS 'ASTEROSTEUS ACULEATUS AND !PELTES
QUADRACUS AND THE KILLIlSH &UNDULUS HETEROCLITUS THE
DEGREE OF COALESCENCE IS INTERMEDIATE
4HE OOCYTES SOON OVULATE INTO THE OVARIAN LUMEN
AND BECOME MATURE EGGS 4HE VITELLINE ENVELOPE IS
HIGHLY COMPACTED AND POSSESSES PORE CANALS PRIOR TO
MATURATION "EGOVAC AND 7ALLACE !T SOME UN
DElNED TIME DURING MATURATION AND BEFORE OVULATION
THE PORE CANALS DISAPPEAR AS THE MICROVILLI ARE RETRACTED
OR LOST FROM THE OOCYTE AND FOLLICULAR CELL 4HE MATURE
EGG IS SURROUNDED BY THE TOUGH #(/2)/. THAT IS DERIVED
FROM REMNANTS OF THE ZONA PELLUCIDA 4HE CHORION MAY
BE DECORATED WITH A SECONDARY ENVELOPE THAT APPEARS
TO HAVE BEEN SYNTHESIZED BY THE FOLLICULAR CELLS DURING
OOCYTE GROWTH 7OURMS AND 3HELDON
-ARINE lSHES WITH PELAGIC EGGS DIFFER FROM OTHER
OVIPAROUS VERTEBRATES IN THAT A CHARACTERISTIC COMPO
NENT OF THE YOLK PROTEIN PHOSPHATE IS SYNTHESIZED AND
LAID DOWN IN THE OVARY IN THE TYPICAL VERTEBRATE MAN
NER BUT DOES NOT NOURISH THE YOUNG ANIMAL #RAIK AND
(ARVEY )NSTEAD IT IS APPARENTLY UTILIZED AT A
MUCH EARLIER STAGE IN THE LIFE CYCLE BEFORE THE EGGS
LEAVE THE OVARY TO PROVIDE THE ENERGY NECESSARY FOR
THE CONSIDERABLE TRANSPORT OF IONS BY THE POTASSIUMSO
DIUM PUMP + IN .A OUT )N SPECIES SUCH AS HERRING
#LUPEA HARENGUS WITH DEMERSAL EGGS RIPENING IS AC
COMPANIED BY A SMALLER UPTAKE OF WATER AND A SIGNIl
#(!04%2
CANT BUT CORRESPONDINGLY SMALLER DECREASE IN PROTEIN
PHOSPHATE #RAIK AND (ARVEY
)N CAPTIVE FEMALES OF THE STRIPED BASS -ORONE
SAXATILIS A CERTAIN VULNERABILITY FOLLOWING VITELLOGEN
ESIS PRESENTS A PROBLEM FOR THE ACQUACULTURE INDUSTRY
-YLONAS ET AL -YLONAS 7OODS AND :OHAR
&INAL OOCYTE MATURATION FAILS TO OCCUR DUE TO AN
ABSENCE OF A SURGE IN PLASMA GONADOTROPIN )) SO THAT
OOCYTES BECOME ATRETIC AND NO OVULATION OR SPAWNING
OCCURS !LTHOUGH CAPTIVE BROODSTOCKS WOULD PROVIDE
MORE RELIABLE EGG PRODUCTION WILD CAUGHT FEMALES
UNDERGOING lNAL OOCYTE MATURATION MUST BE USED FOR
ARTIlCIAL SPAWNING
4HE /OCYTE %NVELOPES
$EVELOPMENT OF THE FOLLICULAR ENVELOPES HAS BEEN DE
SCRIBED FOR SEVERAL SPECIES OF BONY lSH BOTH OVIPA
ROUS AND VIVIPAROUS AND IS ESSENTIALLY THE SAME FOR ALL
(URLEY AND &ISHER &LGEL A B !NDERSON
'TTING 5LRICH "USSON
-ABILLOT
!ZEVEDO 7OURMS #APORIC
CIO AND #ONNES 4ESORIERO A $UMONT AND
"RUMMETT 3TEHR AND (AWKES (OSOKAWA
"RUSL +ESSEL ET AL 3CHME
HL AND 'RAHAM )WAMATSU ET AL -AT
SUYAMA .AGAHAMA AND -ATSUURA 'IULIANINI
AND &ERRERO /OCYTES OF ALL SPECIES PRODUCE A
REFRACTILE ACELLULAR 02)-!29 %.6%,/0% AROUND THEM
SELVES 7OURMS 3EVERAL NAMES HAVE BEEN AP
PLIED TO THIS LAYER INCLUDING hZONA PELLUCIDAv hZONA
RADIATAv hCHORIONv hVITELLINE MEMBRANEv AND hVITEL
LINE ENVELOPEv 4HE TERM MOST COMMONLY USED FOR THE
HOMOLOGOUS STRUCTURE IN MAMMALS IS hZONA PELLUCIDAv
AND THIS WILL BE USED IN THIS TEXT !ROUND THE ZONA
PELLUCIDA THE FOLLICULAR CELLS MAY FORM A 3%#/.$!29
%.6%,/0% OFTEN HIGHLY ORNAMENTED 4%24)!29 %.6%
,/0%3 SUCH AS JELLY COATS OR LEATHERY EGG CASES MAY BE
FORMED BY GLANDS IN THE OVIDUCT OR ELSEWHERE AS THE
OVUM MAKES ITS WAY TO THE OUTSIDE WORLD
02)-!29 %.6%,/0%
4HE ZONA PELLUCIDA OF TELEOSTS IS SECRETED BY EXOCY
TOSIS AROUND THE BASES OF THE MICROVILLI THAT EXTEND
FROM THE SURFACE OF THE OOCYTE &IGURE 4HESE
MICROVILLI ARE ENTRAPPED IN THIS DEVELOPING ENVELOPE
ALONG WITH MICROVILLI EXTENDING FROM THE FOLLICULAR
CELLS SO THAT THE PRIMARY ENVELOPE IS PERFORATED BY
0/2% #!.!,3 CONTAINING MICROVILLI EXTENDING PERPEN
DICULAR TO ITS SURFACE &IGURE 4HESE PERFORATIONS
WITH THEIR ENCLOSED MICROVILLI ACCOUNT FOR THE STRIATED
PATTERN OF THE PRIMARY ENVELOPE AS SEEN IN SECTIONS
WITH THE LIGHT MICROSCOPE GIVING RISE TO THE TERM
hZONA RADIATAv THAT IS SOMETIMES APPLIED TO THIS LAYER
4HE MICROVILLI WITHIN THE PORE CANALS MAY BE CLOSELY
APPOSED &IGURES AND EVEN COILING AROUND
EACH OTHER +JESBU +RYVI AND .ORBERG 4HOSE
FROM THE FOLLICULAR CELLS MAY mATTEN THEIR TIPS OVER THE
OOLEMMA &IGURE WHILE THE OOCYTES MICROVILLI
RECIPROCATE BY TOUCHING THE SURFACE OF THE FOLLICULAR
CELLS )T IS ESTIMATED THAT A SINGLE OOCYTE IN THE COD
'ADUS MORHUA BRISTLES WITH ABOUT MILLION MICROVIL
LI THEREBY INCREASING ITS SURFACE AREA BY A FACTOR OF
4HE ZONA PELLUCIDA TRANSFORMS DURING EARLY OOCYTE
DEVELOPMENT &IGURES AND 'TTING
!NDERSON !ZEVEDO (OSOKAWA
#OTELLI ET AL "EGOVAC AND 7ALLACE $UR
ING PRIMARY GROWTH PRIOR TO ITS FORMATION OOCYTES
EXTEND MICROVILLI TOWARD THE INVESTING MONOLAYER OF
FOLLICULAR CELLS "EGOVAC AND 7ALLACE )NITIAL
FORMATION OF THE ZONA PELLUCIDA OCCURS AT THE EARLI
EST CORTICAL ALVEOLUS STAGE WITH THE DEPOSITION OF A
HOMOGENEOUS ELECTRON
LUCENT LAYER DESIGNATED :
BY !NDERSON BETWEEN THE MICROVILLI &IGURE
! "Y MID TO LATE CORTICAL ALVEOLUS STAGE THE
ARCHITECTURALLY COMPLEX : AND : LAYERS FORM GIV
ING THE ZONA PELLUCIDA A TRILAMINAR APPEARANCE &IG
URE " $URING VITELLOGENESIS THE ZONA PELLUCIDA
UNDERGOES COMPACTION PARTICULARLY OF THE : LAYER
&IGURE # AND SEVERAL LAYERS OF ALTERNATING ELEC
TRON
DENSE AND ELECTRON
LUCENT LAMELLAE MAY BECOME
APPARENT !CTIVE EXCHANGE OF METABOLITES TAKES PLACE
BETWEEN THE OOCYTE AND PERIFOLLICULAR SPACE BY WAY OF
THE PORE CANALS &IGURE
7HEN THE ZONA PELLUCIDA lRST APPEARS THE PERIPH
ERAL OOPLASM DISPLAYS ENHANCED APPARATUS FOR PRO
TEIN SYNTHESIS AND SECRETION FREE RIBOSOMES GRANULAR
ENDOPLASMIC RETICULUM AND WELL DEVELOPED 'OLGI
COMPLEXES !NDERSON 7OURMS %LEC
TRON
DENSE VESICLES APPARENTLY FORMED BY THE 'OLGI
COMPLEX ARISE IN THE PERIPHERAL OOPLASM PRIOR TO DE
POSITION OF THE ELECTRON
DENSE LAYER OF THE ZONA PEL
LUCIDA AND ARE APPARENT DURING ALL SUBSEQUENT STAGES
OF ITS DEPOSITION &IGURE 4ESORIERO A THIS
4HERE MAY BE CHANGES IN THE EGG ENVELOPE ON CONTACT WITH THE
EXTERNAL ENVIRONMENT FOLLOWING SPAWNING 4HE TERM hCHORIONv WILL
BE RESERVED IN THIS TEXT TO DESIGNATE THE STRUCTURAL ENVELOPE THAT
ENCLOSES THE OVULATED EGG OR DEVELOPING EMBRYO (ART 0IETRI AND
$ONOVAN
/6!2)!. &/,,)#,%3
GLYCOPROTEINACEOUS MATERIAL IS PRESUMABLY DEPOSITED
BY EXOCYTOSIS AND BECOMES THE DEVELOPING ZONA PEL
LUCIDA &IGURE 4ESORIERO B .O EVI
DENCE WAS FOUND IN #YNOLEBIAS SPP THAT THE FOLLICULAR
CELLS ARE ENGAGED IN THE PRODUCTION OF EXTRACELLULAR
MATERIAL AT THIS STAGE 7OURMS
4HE INNERMOST THICKEST LAYER OF THE PRIMARY EN
VELOPE : IN MANY TELEOSTS DEVELOPS AN ELEGANT
TRANSITORY lBRILLAR STRUCTURE WHOSE APPEARANCE IN SEC
TIONS SUGGESTS hART NOUVEAU ARABESQUESv &IGURE
7OURMS 4HE POSITIONING OF THE PORE CANALS AT
THE CENTRE OF THE ELLIPSOID CURVES OF THESE ARCHES MAY
PROVIDE mEXIBILITY TO WITHSTAND EXPANSION OF THE EGG AS
WELL AS MECHANICAL SHOCKS &IGURE #APORICCIO
AND #ONNES
4HE DIFFERENCES IN ELECTRON DENSITY OF THE LAYERS OF
THE ZONA PELLUCIDA ARE LIKELY DUE TO DIFFERENCES IN THEIR
COMPOSITION THE OUTER MORE ELECTRON
DENSE LAYER IN
/RYZIAS LATIPES IS RICH IN POLYSACCHARIDES WHILE THE IN
NER LAYER CONTAINS A HIGHER PROPORTION OF PROTEINS 4ES
ORIERO A )N THE VIVIPAROUS TELEOST 8IPHOPHORUS
HELLERI THE ZONA PELLUCIDA IS HOMOGENEOUS AND SHOWS
NO LAYERING IT ATTAINS A THICKNESS OF ABOUT M DURING
VITELLOGENESIS REGRESSES DURING MATURATION AND HAS DIS
APPEARED BEFORE SEGMENTATION BEGINS !ZEVEDO
4HE ZONA PELLUCIDA OF THE COD IS A HYDROPHOBIC PRO
TEIN AGGREGATE CONSISTING OF THREE POLYPEPTIDES DESIG
NATED _ ` AND a WITH APPARENT MOLECULAR WEIGHTS OF
AND K$A /PPEN
"ERNTSEN (ELVIK AND 7AL
THER 4WO TO FOUR MAJOR PROTEINS WITH MOLECULAR
WEIGHTS RANGING FROM TO K$A HAVE BEEN SEPA
RATED FROM THE ZONA PELLUCIDA OF OTHER TELEOSTS "RIVIO
"ASSI AND #OTELLI (YLLNER ET AL MINOR
COMPONENTS WITH MOLECULAR WEIGHTS RANGING FROM
TO K$A WERE ALSO PRESENT "RIVIO "ASSI AND #O
TELLI 4HE PRESENCE OF ENVELOPE PROTEINS IN THE
PLASMA OF FEMALES RISES DRAMATICALLY AS SEXUAL MATURA
TION PROCEEDS /PPEN
"ERNTSEN ET AL AND HAS
BEEN INDUCED IN SEVERAL SPECIES OF TELEOSTS BY OESTRA
DIOL
` (YLLNER ET AL (YLLNER .ORBERG AND
(AUX ,ARSSON (YLLNER AND (AUX (YLL
NER 3ILVERSAND AND (AUX )T HAS BEEN SUGGESTED
THAT THESE PROTEINS LIKE VITELLOGENIN ARE PRODUCED IN
THE LIVER (AMAZAKI )UCHI AND 4AMAGAMI
(AMAZAKI ET AL /PPEN
"ERNTSEN 'RAM
*EN
SEN AND 7ALTHER 4HIS SUGGESTION IS CONTRARY TO
THE CONVENTIONAL UNDERSTANDING OF THE FORMATION OF THE
TELEOSTEAN PRIMARY ENVELOPE THAT THE CONSTITUENTS OF
THE INNER LAYER ARE SYNTHESIZED BY THE OOCYTE ITSELF )T
IS NOT KNOWN WHETHER THESE PROTEINS ARE INCORPORATED
INTO THE OOCYTE AND THEN SECRETED FROM IT TO FORM THE
INNER LAYER OF THE ZONA PELLUCIDA AFTER RECEIVING SOME
MOLECULAR MODIlCATION OR WHETHER THEY GO DIRECTLY TO
THE SITE OF FORMATION OF THE EGG ENVELOPE WITHOUT PASS
ING THROUGH THE OOCYTE %VIDENCE SUPPORTIVE OF THE
CONVENTIONAL VIEW WAS FOUND IN DEVELOPING OOCYTES
OF THE PIPElSH 3YNGNATHUS SCOVELLI WHERE THE PROTEINS
OF THE ZONA PELLUCIDA COULD NOT BE TRACED TO THE LIVER
AND IT WAS CONCLUDED THAT THEY ORIGINATE WITHIN THE FOL
LICLE ITSELF &IGURE "EGOVAC AND 7ALLACE
"Y THE TIME THE OOCYTE TRANSFORMS INTO A MATURE
EGG THE MICROVILLI AND PORE CANALS ARE OFTEN LOST
&IGURE $ 4HE : LAYER IS RETAINED THROUGHOUT
OOCYTE DEVELOPMENT TO MATURITY ALTHOUGH IT BECOMES
MUCH REDUCED AS DEVELOPMENT PROGRESSES 4HE MA
TURE EGG ENVELOPE CHORION MAY RETAIN A LAMELLAR AP
PEARANCE 4HERE IS NO DEGENERATION OF THE OUTERMOST
LAYER OF THE ZONA PELLUCIDA OF THE PORGY 0AGRAS MAJOR
PRIOR TO MATURATION HOWEVER NOR ARE THE SURFACE PITS
REMAINING FROM THE PORE CANALS PLUGGED &IGURE
(OSOKAWA 4HESE PITS MAY ALSO BE OBSERVED
ON THE SURFACE OF THE ZONA PELLUCIDA OF THE mOUNDER
AND GLOBElSH BUT NOT ON THE SURFACE OF THE MEDAKA
AYU TROUT OR SALMON
! SIMPLER THINNER ENVELOPE IS DESCRIBED IN VIVIPA
ROUS POECILIIDS THAN IN OVIPAROUS SPECIES !ZEVEDO
PERHAPS PERMITTING MORE INTIMACY BETWEEN FOE
TAL AND MATERNAL CIRCULATIONS )N VIVIPAROUS 8IPHOPHO
RUS HELLERI THE ZONA PELLUCIDA DEVELOPS IN MUCH THE
SAME WAY AS IN OVIPAROUS FORMS BUT FORMS ONLY A
SINGLE LAYER )T REACHES ITS MAXIMUM THICKNESS OF M
BY THE END OF VITELLOGENESIS THEN BECOMES THINNER
AND ALMOST COMPLETELY DISAPPEARS BY THE END OF
MATURATION &IGURE -ICROVILLI FROM THE OOCYTE
PENETRATE THE PORE CANALS TO FORM A MESH AGAINST THE
FOLLICULAR CELLS 4HE FOLLICULAR CELLS OF POECILIIDS MAY
BE UNIQUE IN LACKING PROCESSES THAT PENETRATE THE PORE
CANALS 4HE ZONA PELLUCIDA DISAPPEARS DURING THE lRST
STAGES OF SEGMENTATION
&OUR DISTINCT LAYERS HAVE BEEN DESCRIBED IN THE ZONA
PELLUCIDA OF THE WHITE STURGEON !CIPENSER TRANSMON
TANUS WHERE THE INNERMOST LAYER IS CLOSELY APPOSED TO
THE OOLEMMA #HERR AND #LARK 4HE INNER TWO
LAYERS ARE lBROUS WITH lLAMENTOUS SUBSTRUCTURES AND
ARE SIMILAR TO LAYERS OF THE ZONA PELLUCIDA OF TELEOST
OOCYTES .UMEROUS lLAMENTOUS SCREWLIKE PROJECTIONS
APPEAR TO ANCHOR THE SECOND LAYER TO THE OUTER LAYERS
&IGURE %LECTROPHORETIC SEPARATION 3$3
0!'%
SHOWS A RANGE OF PROTEINS AND GLYCOPROTEINS IN THE EN
VELOPES INCLUDING THE JELLY COAT OF MOLECULAR WEIGHTS
#(!04%2
FROM TO CA K$A #HERR AND #LARK
4HE MOST PROMINENT BAND IS A K$A PROTEIN WHICH
RESIDES IN THE OUTERMOST LAYER OF THE ZONA PELLUCIDA
!FTER FRESHWATER EXPOSURE THIS LAYER CONTAINS BOTH THE
AND A K$A GLYCOPROTEIN PRESUMABLY DERIVED BY
PROTEOLYSIS OF THE K$A GLYCOPROTEIN 4HIS K$A
GLYCOPROTEIN INDUCES A SPECIES
SPECIlC ACROSOME RE
ACTION IN SPERMATOZOA OF ! TRANSMONTANUS BUT NOT OF
! FULVESCENS NO INDUCER RESIDES IN THE JELLY COAT
! ZONA PELLUCIDA HAS BEEN DESCRIBED IN THE DEVEL
OPING FOLLICLE OF A VIVIPAROUS ELASMOBRANCH THE YEL
LOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS (AMLETT
*EZIOR AND 3PIELER )T IS MORE DELICATE THAN
THE ZONA PELLUCIDA OF TELEOSTS AND NEVER BECOMES AS
STRUCTURALLY COMPLEX OR RIGID 4HERE IS NO SURFACE OR
NAMENTATION AND NO MICROPYLE )T IS MOST LIKELY A COM
POSITE LAYER BEING PRODUCED COOPERATIVELY BY BOTH THE
OOCYTE AND FOLLICULAR CELLS 0ERFORATIONS CONTAINING
PROCESSES FROM THE FOLLICULAR CELLS PRODUCE THE TYPICAL
STRIATED APPEARANCE IN SECTIONS BUT UNLIKE THE CONDI
TION IN TELEOSTS THERE ARE NO PROCESSES EXTENDING FROM
THE OVUM 4HE PROCESSES EXTENDING FROM THE FOLLICULAR
CELLS MAKE CONTACT WITH THE OOLEMMA INDENT IT AND
EVEN PENETRATE THIS MEMBRANE &IGURE
4HE PRIMARY ENVELOPE OF THE LAMPREY FOLLICLE IS
SIMILAR TO THOSE DESCRIBED FOR TELEOSTS ,EWIS AND -C
-ILLAN 4HE OOCYTE LAYS DOWN A DOUBLE TRANS
LUCENT lBROUS ZONA PELLUCIDA WHOSE OUTER LAYER IS
MORE ELECTRON
DENSE THAN THE INNER "USSON
-ABILLOT
A !FZELIUS .ICANDER AND 3JDN 4HE l
BRILS EMBEDDED WITHIN THE ZONA PELLUCIDA FORM PARALLEL
SHEETS BUT DO NOT ATTAIN THE mAMBOYANT PATTERNS SEEN
IN TELEOSTS 4HE ZONA PELLUCIDA IS PERFORATED BY RADIAL
PORE CANALS THAT CONTAIN MICROVILLI EXTENDING THROUGH
ITS ENTIRE THICKNESS FROM THE SURFACE OF THE OOCYTE AL
THOUGH SHORT MICROVILLI EXTEND TOWARD THE ZONA PEL
LUCIDA FROM THE FOLLICULAR CELLS THEY DO NOT APPEAR TO
ENTER THE PORE CANALS ! COMPLETE SHEATH OF SQUAMOUS
FOLLICULAR CELLS ENCLOSES THE OOCYTE OF 0ETROMYZON MA
RINUS 9ORKE AND -C-ILLAN BUT IN ,AMPETRA
PLANERI THEY FORM A CUP THAT ENVELOPS ONLY THE BASAL
PORTION OF THE OOCYTE "USSON
-ABILLOT B
2ESTING OOCYTES TO MM IN DIAMETER OF THE
HAGlSH -YXINE GLUTINOSA APPEAR TO SECRETE A PRIMARY
ENVELOPE RICH IN POLYSACCHARIDES SIMILAR TO THE ZONA
PELLUCIDA OF OTHER lSH 0ATZNER )T IS PEN
ETRATED BY MICROVILLI EXTENDING FROM BOTH THE OOCYTE
AND THE FOLLICULAR CELL )T ATTAINS ITS MAXIMUM THICK
NESS OF ABOUT M IN OOCYTES TO MM IN LENGTH AND
THEN BECOMES THINNER ! UNIQUE FEATURE OF THE HAGlSH
FOLLICLE IS ITS ABILITY TO SECRETE A hSHELLv AROUND THE OO
CYTE NOT MERELY A SIMPLE INVESTMENT BUT ONE WITH A
MICROPYLE FOR SPERM ENTRY AND AT EACH POLE A FAN
LIKE
ARRAY OF HOOKS $ODD AND $ODD
3%#/.$!29 %.6%,/0%3
4HE SECONDARY ENVELOPE FORMED BY THE FOLLICULAR CELLS
BEFORE OVULATION MAY CONSIST OF A SIMPLE JELLY COAT
)N THE PERCH 0ERCA mUVIATILIS THIS LAYER BECOMES lVE
TIMES THICKER THAN THE ZONA PELLUCIDA AND IS TRAVERSED
BY CYTOPLASMIC PROCESSES THAT EXTEND FROM THE FOL
LICULAR CELLS TO PENETRATE THE PORE CANALS &IGURE
&LGEL A #OLUMNAR FOLLICULAR CELLS CONTAINING
ELECTRON
DENSE DROPLETS FORM A JELLY COAT AND ATTACH
MENT DISC SURROUNDING THE ZONA PELLUCIDA AT THE ANIMAL
POLE OF MATURING FOLLICLES OF THE !FRICAN CATlSH #LAR
IAS GARIEPINUS WHILE CUBOIDAL CELLS CONTAINING MOD
ERATELY ELECTRON
DENSE DROPLETS FORM A JELLY COAT OVER
THE REST OF THE SURFACE &IGURE VAN DEN (URK AND
0EUTE !LL OF THESE FOLLICULAR CELLS CONTAIN ABUN
DANT GRANULAR ENDOPLASMIC RETICULUM AND A FEW SMALL
MITOCHONDRIA WITH LAMELLAR CRISTAE
)N MANY SPECIES OF TELEOSTS ESPECIALLY OVIPAROUS
SPECIES FOLLICULAR CELLS MAY PRODUCE A SECONDARY EN
VELOPE THAT IS OFTEN HIGHLY ORNAMENTED &IGURE
4HE FOLLICULAR CELLS MAY RETAIN AN UNSPECIALIZED AP
PEARANCE DURING THE EARLY STAGES OF PRIMARY ENVELOPE
FORMATION LACKING THE FEATURES CHARACTERISTIC OF CELLS
ENGAGED IN PROTEIN SYNTHESIS AND SECRETION BUT AS THE
OOCYTE GROWS THE NUMBER OF FOLLICULAR CELLS INCREASES
AND THEIR SHAPE TRANSFORMS FROM SQUAMOUS TO CUBOIDAL
7OURMS AND 3HELDON "USSON
-ABILLOT
4HIAW AND -ATTEI 7HEN DEPOSITION OF THE PRI
MARY ENVELOPE IS COMPLETE THE FOLLICULAR CELLS BECOME
COLUMNAR EVINCE INCREASING AMOUNTS OF GRANULAR ENDO
PLASMIC RETICULUM AND BEGIN TO LAY DOWN A SECONDARY
ENVELOPE OUTSIDE THE PRIMARY ENVELOPE &IGURE
%XTENSIVE INTERCELLULAR SPACES THAT BECOME lLLED WITH
lBRILLAR MATRIX DEVELOP BETWEEN THE FOLLICULAR CELLS
&IGURE
/RNAMENTATION OF THE SECONDARY ENVELOPE MAY TAKE
MANY FORMS AND OFTEN APPEARS TO BE SHAPED WITHIN THE
INTERCELLULAR SPACES OF THE FOLLICULAR CELLS MUCH AS A
MOULD IMPOSES ITS DESIGN ON A WAFmE 4HE ULTRASTRUC
TURE OF THE MATERIAL OF THIS ORNAMENTATION HAS BEEN
DESCRIBED IN SEVERAL SPECIES AS RESEMBLING MASSES OF
CLOSELY PACKED MICROTUBULES TO NM IN DIAMETER
OFTEN COATED WITH AN ELECTRON
DENSE GELATINOUS MATE
RIAL 4SUKAHARA 7OURMS AND 3HELDON
/6!2)!. &/,,)#,%3
"USSON -ABILLOT $UMONT AND "RUMMETT
(ART 0IETRI AND $ONOVAN 6ESICLES OF
ELECTRON DENSE MATERIAL OF A TUBULAR NATURE APPEAR IN
THE FOLLICULAR CELLS THE TUBULES RESEMBLE MICROTUBULES
BEING ABOUT NM IN DIAMETER AND HAVE BEEN TERMED
hMICROTUBULE MIMICSv 7OURMS 4HE PRESENCE
OF THESE CHARACTERISTIC TUBULES HAS BEEN USED TO ESTAB
LISH THE PROBABLE ROUTE OF THEIR INTRACELLULAR TRANSPORT
&IGURE AND IT IS CONCLUDED THAT THEY ARE SYN
THESIZED IN THE GRANULAR ENDOPLASMIC RETICULUM OF THE
FOLLICULAR CELLS AND TRANSPORTED IN VESICLES DIRECTLY TO
THE SURFACE OF THE OOCYTE THE 'OLGI COMPLEX APPEARS
TO PLAY NO PART IN THIS PROCESS 7OURMS AND 3HELDON
&IGURE
4HE 'OLGI COMPLEX OF FOLLICULAR CELLS IS INVOLVED
HOWEVER IN THE FORMATION OF THE SECONDARY ENVELOPE
OF THE CYPRINODONT !PHYOSEMION SPLENDOPLEURE 4HI
AW AND -ATTEI 4HE SECONDARY ENVELOPE IN THIS
SPECIES CONSISTS OF TWO LAYERS A THIN HOMOGENEOUS
INNER LAYER WHICH ADHERES TO THE ZONA PELLUCIDA AND
A SUPERlCIAL LAYER FORMED OF PARALLEL MICROTUBULE LIKE
ELEMENTS NM IN DIAMETER EMBEDDED IN A HOMO
GENEOUS MATRIX &IGURE 4HE SUPERlCIAL LAYER IS
STUDDED WITH LARGE SWELLINGS M HIGH INTERSPERSED
WITH GREATER NUMBERS OF SMALLER SWELLINGS &IGURE
!MORPHOUS MATERIAL FORMS IN THE CISTERNAE OF
THE ABUNDANT BASAL GRANULAR ENDOPLASMIC RETICULUM
WHOSE ELEMENTS FRAGMENT INTO VESICLES LIMITED BY A
MEMBRANE COVERED WITH RIBOSOMES &IGURE !T
THE END OF VITELLOGENESIS LARGE INTERCELLULAR SPACES
FORM BETWEEN ADJACENT COLUMNAR FOLLICULAR CELLS &IG
URE AND VESICLES ORIGINATING IN THE APICAL 'OLGI
COMPLEX RELEASE THEIR CONTENTS ONTO THE SURFACE BY
EXOCYTOSIS &IGURE 4HE RESPECTIVE CONTRIBU
TIONS OF THE GRANULAR ENDOPLASMIC RETICULUM AND APICAL
'OLGI COMPLEX TO THE VARIOUS COMPONENTS OF THE SEC
ONDARY ENVELOPE ARE NOT CLEAR PERHAPS THE AMORPHOUS
MATERIAL FROM THE GRANULAR ENDOPLASMIC RETICULUM IS
PROCESSED IN THE 'OLGI COMPLEX AND RELEASED BY EXO
CYTOSIS ONTO THE SURFACES OF THE FOLLICULAR CELLS WHERE IT
IS MOULDED BY THE INTERCELLULAR SPACES TO ORNAMENT THE
SECONDARY ENVELOPE
)N THE CICHLID #ICHLASOMA FASCIATA AND OTHER TELEOST
lSH THE ADHESIVE APPARATUS THAT lXES SPAWNED EGGS TO
THE SUBSTRATE IS COMPOSED OF TWO DISTINCT ELEMENTS AN
AMORPHOUS MUCOUS JELLY COAT THAT IS PERMEATED BY lLA
MENTS CONNECTED TO THE SURFACE OF THE ZONA PELLUCIDA
&IGURE "USSON -ABILLOT 4HE lLAMENTS
CONSIST OF BUNDLES OF MICROTUBULE MIMICS &IGURE
AND ARE THE lRST COMPONENT OF THE ADHESIVE COAT
TO BE ELABORATED FORMING OUTSIDE THE ZONA PELLUCIDA
AT THE lRST SIGNS OF SECRETORY ACTIVITY IN THE FOLLICULAR
CELLS &IGURES TO 4HE GRANULAR ENDOPLAS
MIC RETICULUM OF THE FOLLICULAR CELLS APPEARS TO BE AC
TIVE IN THE PRODUCTION OF THE lLAMENTS 4HE ADHESIVE
lLAMENTS ELONGATE AT THE BEGINNING OF VITELLOGENESIS
WHEN INTERCELLULAR SPACES OPEN BETWEEN THE FOLLICULAR
CELLS 0RODUCTION OF THE JELLY COAT IS DESCRIBED AS AN
APOCRINE SECRETION OF THE FOLLICULAR CELLS WHERE THE
MUCOUS MATERIAL PACKED WITHIN CISTERNAE OF THE GRAN
ULAR ENDOPLASMIC RETICULUM IS RELEASED BY RUPTURE OF
THE APICAL PORTION OF THE CELL /NLY A SMALL PORTION OF
THE CYTOPLASM IS RELEASED HOWEVER AND MOST ORGAN
ELLES ESPECIALLY THE EMPTY CISTERNAE OF THE ENDOPLAS
MIC RETICULUM AND MITOCHONDRIA ARE RETAINED WITHIN
THE CELL AFTER THE EXPULSION OF THE SECRETORY PRODUCTS
4HE 'OLGI COMPLEX APPEARS TO PLAY NO ROLE IN THE SE
CRETION OF EITHER COMPONENT OF THE MUCOUS COAT
4HE DEVELOPING SECONDARY ENVELOPE OF &UNDULUS
HETEROCLITUS IS SEEN AS BUNDLES OF ELECTRON DENSE lBRES
THAT WEAVE THEIR WAY OVER THE SURFACE OF THE ZONA PEL
LUCIDA COURSING THROUGH THE WIDE INTERCELLULAR SPAC
ES BETWEEN THE FOLLICULAR CELLS +UCHNOW AND 3COTT
$UMONT AND "RUMMETT )N #YNOLEBIAS
SPP THE FOLLICULAR CELLS MOULD THE MICROTUBULE MIM
ICS INTO A THISTLE LIKE SECONDARY ENVELOPE OF PROJECT
ING SPIKES &IGURE 7OURMS AND 3HELDON
4HESE CELLS SCULPT AN ELABORATE ARRANGEMENT OF POLY
GONAL COMPARTMENTS OVER THE ZONA PELLUCIDA OF EGGS OF
THE SOLE 0LEURONICHTHYS COENOSUS &IGURE 3TEHR
AND (AWKES 3INCE THE FOLLICULAR CELLS ARE PO
LYGONAL IT IS SUGGESTED THAT DEPOSITION OF ENVELOPE
MATERIAL AT THEIR LATERAL MARGINS PRODUCES THIS PATTERN
&IGURE $URING FORMATION OF THE ENVELOPE THE
CHAMBERS ENCLOSED BY THESE PARTITIONS CONTAIN MASSES
OF OOCYTE MICROVILLI EXTENDING ACROSS A LARGE SUBFOL
LICULAR SPACE TO TOUCH THE STUBBY MICROVILLI OF THE FOL
LICULAR CELLS AND EVEN THE FOLLICULAR CELLS THEMSELVES
!S THE PARTITIONS BECOME WELL DEVELOPED hmOORSv
WITH A SUBPATTERN OF HEXAGONAL RIDGES ARE LAID DOWN
BETWEEN THEM COVERING THE PRIMARY ENVELOPE &IGURE
EACH HEXAGON ENCIRCLING AN OOCYTE MICROVIL
LUS &IGURE " 4HESE HEXAGONAL PATTERNS APPEAR
SPORADICALLY ON EGGS OF OTHER SPECIES IN THE SUBFAMILY
0LEURONECTINAE (IRAI AND HAVE BEEN NOTED ON
EGGS IN SUCH DIVERSE FAMILIES AS 3YNODONTIDAE #ALLI
ONYMIDAE AND 5RANOSCOPIDAE -ITO )KEDA AND
-ITO CITED BY (IRAI 4HEIR FUNCTIONAL
SIGNIlCANCE IS OBSCURE
&OLLICULAR CELLS PRODUCE TWO TYPES OF SECONDARY EN
#(!04%2
VELOPE ON THE SURFACE OF THE LAMPREY EGG &IGURE
#OLUMNAR FOLLICULAR CELLS AT THE ANIMAL POLE MOULD A
GELATINOUS !0)#!, 45&4 ,EWIS AND -C-ILLAN
9ORKE AND -C-ILLAN THAT ATTRACTS SPERMATOZOA
DURING SPAWNING +ILLE ! RADICAL BREAKDOWN
OF FOLLICULAR CELLS OVER THE BASAL TWO
THIRDS OF THE EGG
LEAVES AN ELABORATE CUP
SHAPED !$(%3)6% #/!4 THAT
SERVES TO AFlX THE EGG TO THE SUBSTRATE IN AN APPROPRI
ATE POSITION TO PRESENT ITS APICAL TUFT FOR THE ATTENTIONS
OF PASSING SPERMATOZOA
4HE LEATHERY #!035,% OF THE EGG OF THE HAGlSH
-YXINE GLUTINOSA IS PRESUMABLY SECRETED BY THE FOL
LICULAR EPITHELIUM &ORMATION BEGINS AT THE END OF THE
GROWTH PERIOD AND THE lRST ACCUMULATIONS OCCUR AT THE
POLES 0ATZNER ,ATER THESE CAPS GROW UNTIL THEY
HAVE SURROUNDED THE ENTIRE EGG AND WHEN THE EGG IS
ENCLOSED TUFTS OF !.#(/2 &),!-%.43 BEARING HOOKS AT
THEIR ENDS &IGURE ARE SAID TO BE SECRETED AND
MOULDED BY SLEEVE
LIKE EXTENSIONS OF THE FOLLICULAR
EPITHELIUM ,YNGNES 7ALVIG +OCH ET AL
4HE ANIMAL POLE ALWAYS DISPLAYS MORE ANCHOR
lLAMENTS THAN THE VEGETAL POLE &IGURE 4HE UPPER
SIDE OF THE ANCHOR lLAMENTS APPEARS ROUGH AND GROOVED
IN SCANNING ELECTRON MICROGRAPHS WHILE THE UNDERSIDE
IS SMOOTH ! CLUSTER OF ABOUT EIGHT ANCHOR lLAMENTS
RADIATING FROM THE DISTAL RIDGE OF A -)#2/09,!2 &5..%,
SURROUNDS THE MICROPYLE OF %PTATRETUS BURGERI &IGURE
&ERNHOLM +OCH ET AL 4HE mOOR
OF THIS FUNNEL FORMS A HONEYCOMB PATTERN OF WHICH A
SINGLE hHONEYCOMB CELLv AT THE CENTRE OPENS TO THE IN
TERIOR 4HE CAPSULE OF -YXINE GLUTINOSA ATTAINS A THICK
NESS OF M AND APPEARS HOMOGENEOUS IN ELECTRON
MICROGRAPHS 7ALVIG !N INTERCELLULAR SPACE OF
ABOUT M INTERVENES BETWEEN THE CAPSULE AND THE
FOLLICULAR EPITHELIUM 4HIS EPITHELIUM IS SIMPLE SQUA
MOUS AT lRST BUT AS DEVELOPMENT CONTINUES THE CELLS
BECOME TALLER EVENTUALLY BECOMING COLUMNAR %NCIR
CLING THE EGG ABOUT ONE
lFTH OF THE DISTANCE FROM THE
ANIMAL POLE THE FOLLICULAR EPITHELIUM FORMS A RING OF
STRATIlED CELLS IN THE POSITION TO BE OCCUPIED IN THE MA
TURE EGG BY A SUTURE THE /0%2#5,!2 2).' THIS SUTURE
LATER SPLITS PROVIDING ESCAPE FOR THE YOUNG HAGlSH OF
TO CM &IGURE
&OLLICULAR %PITHELIUM
!S THE OOGONIUM BEGINS MEIOTIC DIVISION AND TRANS
FORMS INTO AN OOCYTE IT BECOMES ENVELOPED BY A THIN
EPITHELIUM OF SQUAMOUS CELLS AND A NEW FOLLICLE IS
PRODUCED 4HE EARLIEST STAGES OF THIS INVESTMENT HAVE
BEEN DEMONSTRATED IN THE GERMINAL RIDGE OF THE PIPE
lSH WHERE 02%&/,,)#5,!2 #%,,3 PRESUMABLY DERIVED
FROM THE LUMINAL EPITHELIUM EXTEND PROCESSES BE
TWEEN CONTIGUOUS MEIOTIC OOCYTES EVENTUALLY FORM
ING A SIMPLE SQUAMOUS EPITHELIUM OF &/,,)#5,!2 #%,,3
AROUND EACH OOCYTE &IGURE "EGOVAC AND 7AL
LACE 4HE FOLLICULAR CELLS ENCLOSED WITHIN THEIR
OWN BASAL LAMINAE FORM A CONTINUOUS EPITHELIUM THAT
ISOLATES THE OOCYTES FROM ONE ANOTHER $ESMOSOMES
ALREADY ESTABLISHED BETWEEN THE PROCESSES OF THE PRE
FOLLICULAR CELLS PERSIST IN THE FOLLICULAR EPITHELIUM
/OGONIA AND OOCYTES OF THE COMMON SNOOK #ENTRO
POMUS UNDECIMALIS ARE DISPERSED AMONG THE SOMATIC
CELLS OF THE GONADAL GERMINAL EPITHELIUM THAT LINES THE
OVARIAN LUMEN &IGURE 'RIER !T THE OUT
SET OF FOLLICULOGENESIS SOME OOGONIA BEGIN TO DIVIDE
BY MEIOSIS TO PRODUCE OOCYTES 4HESE OOCYTES DESCEND
INTO THE DEEPER BASAL REGIONS OF THE EPITHELIUM WHERE
THEY BECOME ENVELOPED BY PROCESSES FROM SOME OF THE
EPITHELIAL CELLS &IGURE 4HE OOCYTE SURROUNDED
BY ITS SIMPLE LAYER OF THESE PREFOLLICULAR CELLS PRESSES
ON THE BASEMENT MEMBRANE OF THE GONADAL EPITHELIUM
EVAGINATING IT AND EVENTUALLY CAUSING THE PINCHING
OFF OF A DISCRETE FOLLICLE CONSISTING OF THE OOCYTE SUR
ROUNDED BY ITS LAYER OF EPITHELIAL CELLS AND ENCLOSED
IN A BASEMENT MEMBRANE DERIVED FROM THE BASEMENT
MEMBRANE OF THE GONADAL EPITHELIUM &OLLICULOGENESIS
IS CONCLUDED WHEN THE BASEMENT MEMBRANE COMPLETE
LY ENCLOSES THE EPITHELIUM AT THIS TIME THIS IS REFERRED
TO AS THE FOLLICULAR EPITHELIUM
3EVERAL FUNCTIONS HAVE BEEN ASCRIBED TO FOLLICULAR
CELLS THESE VARY FROM SPECIES TO SPECIES REmECTING THE
SPECTRUM OF REPRODUCTIVE STRATEGIES EXPLOITED BY lSH
)T HAS BEEN SUGGESTED THAT FOLLICULAR CELLS ARE NUTRITIVE
ASSISTING IN THE UPTAKE OF MATERIALS BY THE OOCYTE THAT
THEY PRODUCE THE SECONDARY ENVELOPE THAT THEY ARE
STEROIDOGENIC AND THAT THEY ASSIST IN THE EXPULSION OF
THE EGG DURING OVULATION 3INCE THESE FUNCTIONS OCCUR
AT DIFFERENT TIMES DURING FOLLICULAR DEVELOPMENT AND
SINCE NOT ALL MAY BE REPRESENTED IN SOME SPECIES THERE
IS TEMPORAL AND INTERSPECIlC VARIATION IN THEIR ULTRA
STRUCTURAL EXPRESSION &OLLICULAR CELLS OF lSH ARE OFTEN
REFERRED TO AS hGRANULOSA CELLSv IMPLYING A HOMOLOGY
WITH THE OESTROGEN
SECRETING CELLS SURROUNDING THE OO
CYTES OF MAMMALS THIS TERM HAS BEEN AVOIDED IN THE
PRESENT WORK IN FAVOUR OF THE NON
COMMITTAL DESIGNA
TION hFOLLICULAR CELLSv
)N THE EARLIEST STAGES OF OOCYTE DEVELOPMENT IN TELE
OSTS THE FOLLICULAR EPITHELIUM IS STILL SIMPLE SQUAMOUS
&LGEL B (IROSE .ICHOLLS AND -APLE
/6!2)!. &/,,)#,%3
0ATZNER "USSON -ABILLOT #APORIC
CIO AND #ONNES 4SUNEKI AND 'ORBMAN
"RUSL .AKASHIMA AND )WAMATSU 4HE
CELLS CONTAIN A mATTENED NUCLEUS AND LITTLE CYTOPLASM
&IGURE INTERDIGITATING JUNCTIONS BETWEEN THEM
ARE REINFORCED BY DESMOSOMES ANCHORED SECURELY IN
THE CYTOPLASM BY BUNDLES OF TONOlLAMENTS &IGURE
4HE EPITHELIUM IS SURROUNDED BY ITS "!3%-%.4
-%-"2!.% WHICH SEPARATES IT FROM THE VASCULAR CON
NECTIVE TISSUE OF THE THECA &EW ORGANELLES ARE PRESENT
WITHIN THE FOLLICULAR CELLS OCCASIONAL MITOCHONDRIA A
SMALL 'OLGI COMPLEX OF TWO TO FOUR LAMELLAE POLY
RIBOSOMES AND SMALL ISOLATED CISTERNAE OF GRANULAR
ENDOPLASMIC RETICULUM
4HE FOLLICULAR EPITHELIUM OF SMALL FOLLICLES OF ELAS
MOBRANCHS IS A SINGLE SQUAMOUS OR CUBOIDAL LAYER
SURROUNDED BY ITS BASEMENT MEMBRANE &IGURES
AND #ALLARD ET AL !NDREUCCETTI ET
AL (AMLETT *EZIOR AND 3PIELER )NTER
SPERSED AMONG THE SQUAMOUS FOLLICULAR CELLS OF SOME
SPECIES ARE ENLARGED LIPID LIKE CELLS OF UNCERTAIN FUNC
TION &IGURES AND !S THE OOCYTE GROWS THE
SQUAMOUS FOLLICULAR CELLS BECOME CUBOIDAL OR COLUM
NAR MITOTIC PROLIFERATION INCREASES THEIR NUMBERS AND
THE LAYER BECOMES STRATIlED &IGURE 4HE LARGE
ROUND CELLS INCREASE GREATLY IN SIZE DURING EARLY DE
VELOPMENT OF THE FOLLICLE AND DISPLAY A ROUND NUCLEUS
AND ESSENTIALLY hEMPTYv CYTOPLASM AS FOLLICULOGEN
ESIS CONTINUES THEY DECREASE IN SIZE AND NUMBER AND
DISAPPEAR PRIOR TO OVULATION -ICROVILLI FROM THE OO
CYTE EXTEND TOWARD AND MAY TOUCH THE FOLLICULAR CELLS
ACROSS THE INTERVENING SPACE THESE INTERMINGLE WITH A
SMALLER NUMBER OF MICROVILLI FROM THE FOLLICULAR CELLS
3UBSEQUENTLY THE AMORPHOUS GEL LIKE :/.! 0%,,5#)$!
FORMS BETWEEN THE OOCYTE AND FOLLICULAR CELLS EMBED
DING THE MICROVILLI WITHIN 0/2% #!.!,3 )N THE STINGRAY
NO PROCESSES EXTEND FROM THE OOCYTE ALTHOUGH LONG
PROCESSES FROM THE FOLLICULAR CELLS PENETRATE THE ZONA
PELLUCIDA TO PRODUCE THE TYPICAL STRIATED APPEARANCE
SEEN IN SECTIONS (AMLETT *EZIOR AND 3PIELER
4HREE TYPES OF CELLS HAVE BEEN IDENTIlED IN THE
STRATIlED FOLLICULAR EPITHELIUM OF 2AYA ASTERIAS SMALL
LARGE AND PYRIFORM !NDREUCCETTI ET AL 4HE
SMALL CELLS DIVIDE RAPIDLY BY MITOSIS GIVING RISE TO
PYRIFORM CELLS BY WAY OF THE LARGE CELLS 4HE LARGE CELLS
HAVE A LARGE NUCLEUS WITH DISPERSED CHROMATIN AND A
PROMINENT NUCLEOLUS THEIR ABUNDANT CYTOPLASM CON
TAINS VESICLES MITOCHONDRIA LIPID DROPLETS AND MASS
ES OF GLYCOGEN &IGURE 4HE NUMBERS OF THESE
ORGANELLES ESPECIALLY MITOCHONDRIA INCREASE AS THE
CELLS TRANSFORM INTO PYRIFORM CELLS &IGURE 4HE
PYRIFORM CELLS SPAN THE FOLLICULAR EPITHELIUM FROM THE
BASAL LAMINA TO THE SURFACE OF THE OOCYTE %ARLY IN FOL
LICULOGENESIS SMALL SURFACE PROTRUSIONS FROM THE FOL
LICULAR CELLS FUSE WITH THE OOLEMMA AT DESMOSOME
LIKE
JUNCTIONS &IGURE " !S THE PERIVITELLINE SPACE
ENLARGES THESE JUNCTIONS PERSIST THEREBY DRAWING OUT
PROTRUSIONS FROM THE FOLLICULAR CELLS &IGURE
%VENTUALLY CYTOPLASMIC CONTINUITY IS ESTABLISHED BE
TWEEN THE FOLLICULAR CELLS AND OOCYTE AND TRUE INTERCEL
LULAR BRIDGES ARE FORMED &IGURE 4HESE BRIDGES
MAY BE M WIDE AND UP TO M LONG 4HEY CONTAIN
MITOCHONDRIA RIBOSOMES WHORLS OF MEMBRANES AND
VESICLES 4HE INTERCELLULAR BRIDGES DISAPPEAR WITH THE
THICKENING AND COMPLETION OF THE ZONA PELLUCIDA LEAV
ING A FEW SLENDER MICROVILLI WITHIN THIS ELECTRON
DENSE
LAYER !T THE ONSET OF VITEOLLOGENESIS THE CYTOPLASMIC
BRIDGES ARE LOST THE FOLLICULAR EPITHELIUM UNDERGOES
REGRESSION AND IS ONCE AGAIN COMPOSED OF A FEW LAYERS
OF SMALL CELLS AND SCATTERED LARGE CELLS
h2UDIMENTARY DESMOSOMESv ARE DESCRIBED BE
TWEEN FOLLICULAR CELLS AND THE OOCYTE OF THE SEA BASS
$ICENTRARCHUS LABRAX BEFORE THE HOMOGENEOUS ELEC
TRON
DENSE MATERIAL OF THE ZONA PELLUCIDA IS LAID DOWN
&IGURE ! #APORICCIO AND #ONNES !S
THE ZONA PELLUCIDA THICKENS THESE DESMOSOMES MAIN
TAIN THEIR CONTACT BETWEEN THE MICROVILLI WITHIN THE
PORE CANALS &IGURES AND " )N ADDITION
WELL DEVELOPED DESMOSOMES LINK ADJACENT CELLS OF THE
FOLLICULAR EPITHELIUM &IGURE # $ESMOSOMES
HAVE BEEN REPORTED BETWEEN ADJACENT FOLLICULAR CELLS
OF SOME SPECIES &LGEL B )WAMATSU ET AL
%ARLY IN VITELLOGENESIS FOLLICULAR CELLS OF THE MEDAKA
/RYZIAS LATIPES ARE JOINED BY DESMOSOMES TO WHICH
BUNDLES OF TONOlLAMENTS ARE ANCHORED &IGURE
.AKASHIMA AND )WAMATSU
/THER JUNCTIONAL TYPES HAVE ALSO BEEN REPORTED IN
THE FOLLICULAR EPITHELIUM 4IGHT JUNCTIONS BETWEEN FOL
LICULAR CELLS OF THE AYU 0LECOGLOSSUS ALTIVELUS CONSTITUTE
A MODERATELY LEAKY BLOOD
FOLLICULAR BARRIER PREVENTING
ACCESS BY MANY MATERIALS TO THE OOCYTE 4OSHIMORI AND
9ASUZUMI A 4IGHT JUNCTIONS BETWEEN FOLLICULAR
CELLS OF THE ZEBRAlSH "RACHYDANIO RERIO BECOME LESS
ELABORATE AND hLEAKIERv AS OOGENESIS PROCEEDS +ES
SEL 2OBERTS AND 4UNG 4HEY APPEAR TO BECOME
DISMANTLED DURING ACTIVE VITELLOGENESIS PERMITTING THE
PASSAGE OF YOLK PROTEINS DERIVED FROM THE BLOOD VES
SELS AND THEIR UPTAKE BY THE OOCYTE BY MICROPINOCYTO
SIS &IGURE
4HERE IS EXTENSIVE AMPLIlCATION OF CONTACTS BETWEEN
#(!04%2
OOCYTE MICROVILLI AND FOLLICULAR CELLS OF THE ZEBRA
lSH "RACHYDANIO RERIO ENHANCING CONDITIONS FOR THE
ESTABLISHMENT OF GAP JUNCTIONS +ESSEL ET AL
0ROCESSES FROM THE FOLLICULAR CELLS ARE USUALLY WIDER
AND SPARSER THAN THOSE FROM THE OOCYTE BUT OFTEN DO
NOT REACH THE SURFACE OF THE OOCYTE WHEREAS MICROVILLI
FROM THE OOCYTE MAKE AMPLE CONTACT WITH FOLLICULAR
MICROVILLI AS WELL AS WITH THE SURFACES OF THE FOLLICULAR
CELLS OFTEN mATTENING THEMSELVES AGAINST THE PLASMA
LEMMA AND GROWING FOR SOME DISTANCE ALONG THE SUR
FACE &IGURE 4HERE IS AN INTIMATE RELATIONSHIP
BETWEEN MICROVILLI FROM THE OOCYTE AND FOLLICULAR CELLS
AS THEY EXTEND IN OPPOSITE DIRECTIONS THROUGH THE PORE
CANALS OF THE ZONA PELLUCIDA &IGURE /OCYTE
MICROVILLI CONTAIN AMPLE BUNDLES OF MICROlLAMENTS
&IGURE WHICH MAY ASSIST IN THEIR ELONGATION
THROUGH THE PORE CANALS 'AP JUNCTIONS FORM BETWEEN
THE OOCYTE MICROVILLI AND THE SURFACES OF THE FOLLICU
LAR CELLS OFTEN OCCURRING NEAR THE BASES OF FOLLICULAR
CELL PROCESSES &IGURES TO 4HE OOCYTE
MICROVILLI MAY BRANCH AS THEY APPROACH THE SURFACE
OF THE FOLLICULAR CELLS THEREBY INCREASING MEMBRANE
CONTACT AND AUGMENTING THE FORMATION OF GAP JUNC
TIONS -OREOVER THE BRANCHES CONTINUE TO PARALLEL THE
PLASMA MEMBRANES OF THE FOLLICULAR CELLS FOR VARYING
DISTANCES $ISTAL ENDS OF THE MICROVILLI MAY INVAGINATE
THE SURFACE OF THE FOLLICULAR CELLS AND OFTEN INSINUATE
THEMSELVES INTO THE INTERSTICES BETWEEN THEM 3OME
GAP JUNCTIONS ALSO OCCUR BETWEEN THE TIPS OF OOCYTE
MICROVILLI AND THE BASES OF THE FOLLICULAR MICROVILLI
.O GAP JUNCTIONS WERE OBSERVED BETWEEN THE DISTAL RE
GIONS OF FOLLICULAR CELL MICROVILLI AND MORE PROXIMAL
REGIONS OF THE OOCYTE MICROVILLI
'AP JUNCTIONS BETWEEN FOLLICULAR CELLS AND MICRO
VILLI FROM THE OOCYTE HAVE ALSO BEEN REPORTED IN 0LECO
GLOSSUS ALTIVELUS THE CHUM SALMON /NCORHYNCHUS
KETA AND /RYZIAS LATIPES &IGURE 4OSHIMORI
AND 9ASUZUMI B +OBAYASHI B )WAMATSU ET
AL &LUCTUATING NUMBERS OF GAP JUNCTIONAL CON
TACTS OCCUR BETWEEN OOCYTE MICROVILLI AND FOLLICULAR
CELLS HETEROCELLULAR CONTACTS AS WELL AS BETWEEN AD
JACENT FOLLICULAR CELLS HOMOCELLULAR CONTACTS DURING
FOLLICULAR DEVELOPMENT AND MATURATION IN THE !TLANTIC
CROAKER -ICROPOGONIAS UNDULATUS 9ORK 0ATIO AND
4HOMAS 4HERE ARE HIGH LEVELS OF THESE ASSOCIA
TIONS DURING VITELLOGENESIS LOW LEVELS AFTER COMPLETION
OF VITELLOGENESIS AND A RETURN TO HIGH LEVELS DURING
EARLY MATURATION AND HYDRATION OF THE OOCYTES 4HESE
VARIATIONS SEEM TO RESULT FROM ALTERATIONS IN THE LENGTH
OF THE OOCYTE MICROVILLI AND THEIR SURFACE CONTACT WITH
FOLLICULAR CELLS RATHER THAN TO CHANGES IN THE NUMBERS
OF MICROVILLI .UMBERS OF CONTACTS DECLINE AGAIN AS
MATURATION IS COMPLETED AND OVULATION APPROACHES
)T IS SUGGESTED THAT THIS INTERCELLULAR ASSOCIATION AND
GAP JUNCTIONAL COMMUNICATION MAY FACILITATE THE TRANS
FER OF MATURATION INDUCING STEROID -)3 FROM FOLLICU
LAR CELLS TO THE OOCYTES AS WELL AS FACTORS NECESSARY FOR
NORMAL EMBRYONIC DEVELOPMENT AND OF IONS SUCH AS
POTASSIUM THAT SUPPORT OOCYTE HYDRATION
4WO TYPES OF ASSOCIATIONS ARE DESCRIBED BETWEEN
PROCESSES FROM FOLLICULAR CELLS AND THE SURFACE OF THE
OOCYTE +OBAYASHI B )N THE COMMONER TYPE
THE EXPANDED END OF A PROCESS TERMINATES IN A SLIGHT
DEPRESSION OF THE OOLEMMA &IGURE 4HE AP
POSING PLASMA MEMBRANES ARE SEPARATED BY A SPACE
OF TO NM WHICH DIMINISHES TO LESS THAN NM IN
PLACES WHERE THE OCCURRENCE OF GAP JUNCTIONS IS SUS
PECTED &IGURE " 4HE EXPANDED ENDS OF THESE
PROCESSES SHOW ENDOCYTOTIC ACTIVITY &IGURE #
4HE FORMATION OF COATED VESICLES IN THE OOLEMMA IN
THESE REGIONS &IGURE $ HINTS AT THE TRANSFER OF
MATERIALS FROM THE FOLLICULAR CELLS TO THE OOCYTE )N
RARER ASSOCIATIONS FOLLICULAR CELL PROCESSES lT DEEPLY
INTO INDENTATIONS OF THE OOLEMMA THE INTERSPACE IS
ABOUT NM AND DESMOSOMES OR DESMOSOME
LIKE
JUNCTIONS OCCUR IN SOME AREAS WHILE IN OTHERS COATED
INVAGINATIONS OF THE OOLEMMA ARE SEEN &IGURE
)N THESE JUNCTIONS NO EXOCYTOTIC ACTIVITY IS SEEN IN THE
PROCESSES FROM THE FOLLICULAR CELLS
!S THE OOCYTE ENLARGES NEW FOLLICULAR CELLS ARE PRO
DUCED AND THE FOLLICULAR EPITHELIUM THICKENS SO THAT IN
LATE VITELLOGENESIS IT MAY APPEAR CUBOIDAL OR COLUM
NAR !LTHOUGH A MULTILAYERED FOLLICULAR EPITHELIUM HAS
BEEN DESCRIBED IN THE OVARY OF THE HAGlSH -YXINE GLU
TINOSA 0ATZNER AND IN IMMATURE FOLLICLES OF THE
DOGlSH 3CYLIORHINUS CANICULA IT FORMS A SINGLE LAYER IN
MATURING FOLLICLES OF THE DOGlSH &IGURE $ODD
AND IS A SIMPLE EPITHELIUM IN LAMPREYS AND TELE
OSTS THROUGHOUT DEVELOPMENT &IGURES AND
-ITOCHONDRIA AND RIBOSOMES INCREASE IN NUMBERS AND
THE 'OLGI COMPLEX PROLIFERATES FROM A SIMPLE STACK OF
LAMELLAE INTO A COMPLEX SYSTEM OF TUBULES AND SPHERI
CAL VESICLES BOTH SMOOTH AND COATED .ICHOLLS AND
-APLE 7OURMS 7OURMS AND 3HELDON
.AGAHAMA #HAN AND (OAR .AGAHAMA
#LARKE AND (OAR /CCASIONAL CENTRIOLES APPEAR
BETWEEN THE 'OLGI COMPLEX AND THE NUCLEUS !S THE
'OLGI COMPLEX DEVELOPS THE AMOUNT OF GRANULAR ENDO
PLASMIC RETICULUM INCREASES GREATLY IN AMOUNT .EAR
/6!2)!. &/,,)#,%3
THE TIME OF OVULATION THE MICROVILLI WITHDRAW FROM THE
ZONA PELLUCIDA AND THE FOLLICULAR CELLS SHRINK
&OLLICULAR CELLS MAY ASSIST IN THE PASSAGE OF MATE
RIALS INTO THE OOCYTE 4HE QUESTION IS OFTEN ASKED AS
TO WHETHER MATERIALS PASS TO THE OOCYTE BY WAY OF
SPACES BETWEEN THE FOLLICULAR CELLS OR ARE TRANSPORTED
THROUGH THE FOLLICULAR CELLS THEMSELVES 4HIS UPTAKE
WOULD lND ITS MAXIMAL EXPRESSION DURING VITELLOGEN
ESIS WHEN MOST RAPID ENLARGEMENT OF THE OOCYTE IS OC
CURRING /CCLUDING JUNCTIONS OF lVE TO SEVEN STRANDS
DEMONSTRATED BETWEEN THE FOLLICULAR CELLS OF THE AYU
0LECOGLOSSUS ALTIVELIS IMPLY THE PRESENCE OF A BLOOD
FOLLICULAR BARRIER OF hINTERMEDIATE LEAKINESSv THAT
WOULD PREVENT EXTENSIVE INTERCELLULAR PASSAGE OF MA
TERIALS THEREBY CAUSING THEM TO PASS THROUGH THE FOL
LICULAR CELLS 4OSHIMORI AND 9ASUZUMI A &IGURE
4HE PRESENCE OF GAP JUNCTIONS BETWEEN MICRO
VILLI OF VITELLOGENIC OOCYTES AND FOLLICULAR CELLS OF THE
AYU &IGURE 4OSHIMORI AND 9ASUZUMI B
SUGGESTS THE PASSAGE OF SMALL MOLECULES THROUGH CHAN
NELS CONNECTING THESE CELLS )N RED SEABREAM 0AGRUS
MAJOR THERE IS A POSITIVE ASSOCIATION BETWEEN THE AC
QUISITION OF MATURATIONAL COMPETENCE AND INCREASED
LEVELS OF GAP JUNCTIONS NOT ONLY BETWEEN OOCYTE MI
CROVILLI AND FOLLICULAR CELLS BUT ALSO BETWEEN ADJACENT
FOLLICULAR CELLS THEMSELVES 0ATIO AND +AGAWA
#OATED INVAGINATIONS OF THE OOLEMMA ABOUT NM
IN DIAMETER MAY INDICATE THE UPTAKE OF EXOGENOUS NU
TRIENTS BY ENDOCYTOSIS IN THE PREOVULATORY OOCYTE OF
THE CHUM SALMON /NCORHYNCHUS KETA &IGURES $
AND " +OBAYASHI B
/N THE OTHER HAND EVIDENCE OF INTERCELLULAR PAS
SAGE AT VARIOUS STAGES OF FOLLICULOGENESIS WAS OBTAINED
BY INJECTING THE ELECTRON
OPAQUE TRACER HORSERADISH
PEROXIDASE INTO THE BLOODSTREAM OF SEVERAL SPECIES
OF lSH !BRAHAM ET AL 0ARMENTIER VAN DEN
"OOGAART AND 4IMMERMANS 4HE MARKER WAS
lRST DETECTED IN THE PERICAPILLARY SPACES OF THE OVARIAN
STROMA AND FROM THERE SUCCESSIVELY IN THE COLLAGEN
SPACES SURROUNDING THE FOLLICULAR EPITHELIUM BETWEEN
THE FOLLICULAR CELLS ALONGSIDE THE MICROVILLI WITHIN THE
PORE CANALS OF THE ZONA PELLUCIDA ON THE SURFACE OF THE
OOCYTE BENEATH THE ZONA PELLUCIDA AND lNALLY WITH
IN PINOCYTOTIC VESICLES IN THE OOCYTE &IGURE
!BRAHAM ET AL !LTHOUGH THE MOLECULES OF
HORSERADISH PEROXIDASE AND THE YOLK PRECURSOR VITEL
LOGENIN DIFFER IN MANY RESPECTS IT IS SUGGESTED THAT
THIS REPRESENTS THE PATHWAY OF VITELLOGENIN UPTAKE BY
OOCYTES )T ALSO APPEARS THAT MICROVILLI PENETRATING THE
ZONA PELLUCIDA DO NOT TRANSMIT THE TRACER BUT ARE BATHED
BY IT AS IT PASSES ALONGSIDE THEM THROUGH THE GLYCOCA
LYX TO THE OOCYTE SURFACE 4HE FACT THAT THE TRACER BY
PASSED THE FOLLICULAR CELLS SUGGESTS THAT VITELLOGENINS
ARE NOT TAKEN UP BY THEM BELYING THE LONG
HELD BELIEF
THAT THESE CELLS ARE NUTRITIVE )T CANNOT BE RULED OUT
HOWEVER THAT FOLLICULAR CELLS SYNTHESIZE SOME PROTEINS
THAT ARE TAKEN UP BY THE OOCYTE
$URING EARLY VITELLOGENESIS IN THE STINGRAY TRANSFER
OF MATERIALS BETWEEN FOLLICULAR CELLS AND THE OOCYTE IS
PROBABLY ENHANCED BY INCREASES IN THE SURFACE AREA PRO
VIDED BY INDENTATIONS OF THE OOLEMMA BY LARGE FOLDS OF
THE ZONA PELLUCIDA AND FOLLICULAR EPITHELIUM THAT EN
CLOSE RICHLY VASCULAR CONNECTIVE TISSUE AND THECAL CELLS
&IGURE (AMLETT *EZIOR AND 3PIELER
4HE LARGE ROUND LIPID
LIKE CELLS OF THE FOLLICULAR EPI
THELIUM ARE CARRIED IN WITH THESE FOLDS AND SINCE THEY
DISAPPEAR BEFORE OVULATION IT HAS BEEN SPECULATED THAT
THEY FULlLL A NUTRITIVE FUNCTION !S VITELLOGENESIS PRO
CEEDS THE COLUMNAR FOLLICULAR CELLS BECOME ENGORGED
WITH TRANSPORT VESICLES AND LIPID DROPLETS &IGURES
AND !T THIS TIME PROCESSES FROM THE FOLLICU
LAR CELLS EXTEND THROUGH THE ZONA PELLUCIDA INVAGINATE
THE OOLEMMA &IGURE AND BECOME PINCHED OFF
WITHIN THE OOPLASM AS DISCRETE VESICLES CALLED 42!.3/
3/-%3 &IGURE 4HE PROCESSES DEVELOP A THICK
ENED PLAQUE OF RIBOSOMAL NATURE WHERE THEY INVAGINATE
THE OOLEMMA AND THESE PLAQUES PERSIST WITHIN THE TRAN
SOSOMES 4HE PRODUCTION OF TRANSOSOMES APPEARS TO BE
RELATED TO THE ACCUMULATION OF LARGE AMOUNTS OF YOLK
IN TELOLECITHAL EGGS BUT THE MECHANISMS BY WHICH FOL
LICLES SEQUESTER YOLK ARE STILL UNCLEAR
! NUTRITIVE FUNCTION HAS BEEN ASCRIBED TO THE INTER
CELLULAR BRIDGES THAT ARE ESTABLISHED BETWEEN THE FOL
LICULAR CELLS AND OOCYTE OF PREVITELLOGENIC FOLLICLES OF
THE ELASMOBRANCH 2AYA ASTERIAS &IGURES AND
!NDREUCCETTI ET AL 4HE BRIDGES MAY
BE M WIDE AND UP TO M LONG 4HEY CONTAIN
MITOCHONDRIA RIBOSOMES WHORLS OF MEMBRANES AND
VESICLES )T IS SUGGESTED THAT THE FOLLICULAR CELLS ACT
AS hNURSE CELLSv DURING THE PREVITELLOGENIC PHASE
TRANSFERRING CYTOPLASMIC COMPONENTS SUCH AS 2.!S
AND CYTOPLASMIC ORGANELLES TO THE OOCYTE BY WAY OF
THESE BRIDGES 4HE INTERCELLULAR BRIDGES DISAPPEAR WITH
THE THICKENING AND COMPLETION OF THE ZONA PELLUCIDA
LEAVING A FEW SLENDER MICROVILLI WITHIN THIS ELECTRON
DENSE LAYER
)N THE LAMPREY 0ETROMYZON MARINUS THE FOLLICULAR
EPITHELIUM SURROUNDING THE OOCYTE FORMS A COMPLETE
AND CONTINUOUS LAYER WITHIN THE FOLLICLE &IGURE
9ORKE AND -C-ILLAN 0RIOR TO EVENTS LEADING
#(!04%2
TO OVULATION THIS IS A SIMPLE SQUAMOUS EPITHELIUM OF
STELLATE CELLS WITH WIDE GAPS BETWEEN THESE SPACES ARE
SPANNED BY CYTOPLASMIC PROCESSES FROM NEIGHBOURING
FOLLICULAR CELLS 4HE FOLLICULAR CELLS CONTAIN ABUNDANT
GRANULAR AND AGRANULAR ENDOPLASMIC RETICULUM 'OLGI
COMPLEXES AND FREE RIBOSOMES LIPIDS MAY ALSO BE
PRESENT &OLLICULAR CELLS MAKE AN UNUSUAL CONTRIBUTION
TO THE FORMATION OF YOLK IN THE LAMPREY 0ETROMYZON
MARINUS ,EWIS AND -C-ILLAN $URING VITELLO
GENESIS WHILE YOLK IS BEING FORMED WITHIN THE OOCYTE
ADDITIONAL YOLK IS ACCUMULATED WITHIN THE CYTOPLASM
OF SOME FOLLICULAR CELLS 4HESE hNURSE CELLSv ARE SUBSE
QUENTLY INCORPORATED INTO THE OOCYTE THEREBY INCREAS
ING ITS MASS AND CONTENT OF YOLK &IGURES ! "
)N THIS FUSION THE NURSE CELL LOSES ITS NUCLEUS 4HE OUT
ER PLASMALEMMA OF THE NURSE CELL BECOMES A PORTION OF
THE OOLEMMA REMNANTS OF THE INTERVENING MEMBRANES
OF THE TWO CELLS PERSIST FOR SOME TIME WITHIN THE NEWLY
CONSTITUTED OOCYTE &IGURE #
4HE ROLE OF FOLLICULAR CELLS IN THE FORMATION OF A SEC
ONDARY ENVELOPE AROUND THE ZONA PELLUCIA OF THE EGG
HAS BEEN ESTABLISHED IN SEVERAL SPECIES 7OURMS AND
3HELDON "USSON
-ABILLOT (ART 0IETRI
AND $ONOVAN !FTER VITELLOGENESIS IS COMPLETE
THE FOLLICULAR CELLS MAY GIVE EVIDENCE OF THEIR INVOLVE
MENT BY ASSUMING THE CHARACTERISTICS OF ACTIVE PROTEIN
PRODUCTION ABUNDANT GRANULAR ENDOPLASMIC RETICULUM
AND ELECTRON
DENSE SECRETORY VESICLES !S THE OOCYTE
GROWS THE NUMBER OF FOLLICULAR CELLS INCREASES AND THEY
TRANSFORM FROM SQUAMOUS TO CUBOIDAL 7HEN DEPOSI
TION OF THE PRIMARY ENVELOPE IS COMPLETE THE FOLLICU
LAR CELLS BECOME COLUMNAR AND MAY BEGIN TO SECRETE
A SECONDARY ENVELOPE OUTSIDE THE PRIMARY ENVELOPE
4HE SECONDARY ENVELOPE OF MANY SPECIES IS FORMED OF
CLOSELY PACKED MICROTUBULE
LIKE MATERIAL THE hMICRO
TUBULE MIMICSv 7OURMS THAT CAN BE EXPLOITED
AS A NATURALLY OCCURRING MARKER TO TRACE ITS ROUTE OF
TRANSPORT FROM VESICLES IN THE FOLLICULAR CELLS &IGURE
TO THE INTERCELLULAR SPACES AND TO THE SECONDARY
ENVELOPE 7OURMS AND 3HELDON )T IS CONCLUDED
THAT THE TUBULES MAKING UP THE SECONDARY ENVELOPE ARE
SYNTHESIZED AND ASSEMBLED IN THE GRANULAR ENDOPLAS
MIC RETICULUM OF THE FOLLICULAR CELLS AND EXTRUDED BY
EXOCYTOSIS &IGURE 4HE 'OLGI COMPLEX DOES NOT
APPEAR TO TAKE PART IN THIS PROCESS IN SOME SPECIES IN
THE CYPRINODONT !PHYSEMION SPLENDOPLEURE HOWEVER
LARGE VESICLES ORIGINATING IN THE APICAL 'OLGI COMPLEX
ARE RELEASED BY EXOCYTOSIS ONTO THE SURFACE OF THE ZONA
PELLUCIDA TO FORM THE SECONDARY ENVELOPE 4HIAW AND
-ATTEI 3INCE NOT ALL EGGS ARE ENCLOSED BY A SEC
ONDARY ENVELOPE AND SINCE THERE ARE GREAT VARIATIONS IN
ITS INTRICACY THERE IS A WIDE RANGE FROM SPECIES TO SPE
CIES IN THE PARTICIPATION OF FOLLICULAR CELLS IN THE PRO
DUCTION OF THE SECONDARY ENVELOPE AND A WIDE RANGE IN
THEIR MORPHOLOGICAL EXPRESSION OF PROTEIN PRODUCTION
!N UNUSUAL METHOD OF FORMATION OF THE SECONDARY
ENVELOPE IS SEEN IN THE SHEATlSH 3ILURUS GLANIS $URING
EARLY VITELLOGENESIS THE FOLLICULAR CELLS PROLIFERATE TO
FORM AN IRREGULAR MASS OF CELLS AROUND THE ZONA PEL
LUCIDA &IGURE ! !BRAHAM ET AL 4HESE
CELLS CONTAIN ABUNDANT GRANULAR ENDOPLASMIC RETICULUM
AND 'OLGI COMPLEXES AND AS DEVELOPMENT PROCEEDS
THEY SYNTHESIZE LARGE NUMBERS OF MEMBRANE
BOUND
MUCOUS DROPLETS IN THEIR INTERIOR &IGURE "
$URING VITELLOGENESIS THEIR EPITHELIAL ORGANIZATION IS
DISRUPTED THE ORGANELLES FRAGMENT AND THE CELLS ARE
TRANSFORMED INTO AN IRREGULAR MASS OF hMUCOSOMESv
WHICH ON CONTACT WITH WATER FOLLOWING OVIPOSITION
SWELLS TO FORM AN ADHESIVE COAT OF MUCOPOLYSACCHA
RIDES AND MUCOPROTEINS THAT CAUSES THE EGGS TO ADHERE
TO THE NEST WALL AND TO EACH OTHER
&OLLICULAR CELLS OF LAMPREYS PRODUCE A SECONDARY
ENVELOPE THAT CONSISTS OF TWO PARTS A mUFFY lBROUS
!0)#!, 45&4 AND EMBELLISHING THE BASAL TWO
THIRDS
OF THE OOCYTE A CUP
SHAPED !$(%3)6% #/!4 CONSIST
ING OF BROKEN
DOWN REMNANTS OF ENLARGED FOLLICULAR
CELLS &IGURE ,ARSEN 9ORKE AND -C-IL
LAN 4HESE AREAS ARE SEPARATED BY AN EXPANSE OF
NAKED CHORION ! FEW MONTHS BEFORE OVULATION THERE
IS A DRAMATIC ENLARGEMENT OF SOME OF THE FOLLICULAR
CELLS SURROUNDING THE BASAL TWO
THIRDS OF THE OOCYTE
,ARSEN 4HESE HUGE CUBOIDAL !$(%3)6% #%,,3
BECOME PACKED WITH IRREGULAR SWOLLEN INTERCONNECT
ED SACCULES CONTAINING mOCCULENT MATERIAL OF VARYING
ELECTRON DENSITY THAT MAY BE DERIVED FROM THE 'OLGI
COMPLEX OR AGRANULAR ENDOPLASMIC RETICULUM &IGURE
"USSON
-ABILLOT B 9ORKE AND -C-IL
LAN 4HE ADHESIVE CELLS ALSO CONTAIN ABUNDANT
GRANULAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA THE
NUCLEUS IS BASAL WHILE 'OLGI COMPLEXES AND SMOOTH
ENDOPLASMIC RETICULUM ARE APICAL LYING UNDER THE
PLASMALEMMA THAT IS ADJACENT TO THE ZONA PELLUCIDA
*UST BEFORE OVULATION AS VACUOLES APPEAR WITHIN THEM
THE ADHESIVE CELLS BEGIN TO BREAK DOWN THEIR DISTENDED
SACCULES HOWEVER RETAIN THEIR INTEGRITY !S THE EGG IS
EXPELLED FROM THE FOLLICLE DURING OVULATION THESE AD
HESIVE SACCULES REMAIN lRMLY AFlXED TO THE ZONA PEL
LUCIDA OF THE BASAL TWO
THIRDS OF THE EGG FORMING A
SECONDARY COAT THAT WILL ADHERE TO JUST ABOUT ANY SUR
FACE HOLDING ALOFT THE APICAL POLE FOR THE ATTENTIONS
/6!2)!. &/,,)#,%3
OF PASSING SPERMATOZOA &IGURE )T IS SUGGESTED
THAT ADHESION OF OVULATED EGGS WITHIN THE COELOM IS
INHIBITED BY THE PRESENCE OF PROTEINS IN THE COELOMIC
mUID THAT ARE RINSED OFF IMMEDIATELY AFTER OVIPOSITION
#ELLS SYNTHESIZING STEROIDS MAY BE IDENTIlED BY HIS
TOCHEMICAL TESTS FOR THE PRESENCE OF ENZYMES INVOLVED
IN STEROID BIOSYNTHESIS SUCH AS 6
`
HYDROXYSTEROID
DEHYDROGENASE `
(3$ A KEY ENZYME THAT CATALYSES
THE CONVERSION OF PREGNENOLONE TO PROGESTERONE AND
DEHYDROEPIANDROSTERONE TO ANDROSTENDIONE 3MITH AND
(ALEY !CTIVITY OF THIS ENZYME HAS BEEN SHOWN
IN FOLLICULAR CELLS OF MANY SPECIES USUALLY DURING VI
TELLOGENESIS ,AMBERT A ,IVNI 9ARON
)WASAKI "ARA 4ANG ,OFTS AND
#HAN VAN DEN (URK AND 0EUTE &OLLICU
LAR CELLS OF THE LOACH -ISGURNUS FOSSILIS REACTED WEAKLY
FROM VITELLOGENESIS TO SPAWNING BUT THE MICROPYLAR
CELLS WHICH ARE HIGHLY SPECIALIZED FOLLICULAR CELLS
DISPLAYED A STRONG REACTION THROUGHOUT THE YEAR /HTA
AND 4ERANISHI )N THE GOLDlSH #ARASSIUS AURA
TUS THE ENZYME WAS DETECTED DURING FOLLICULAR DEVEL
OPMENT BUT DISAPPEARED DURING VITELLOGENESIS +HOO
.O `
(3$ ACTIVITY WAS NOTED IN PREOVULATORY
FOLLICULAR CELLS OF SEVERAL SALMONIDS OR THE GOLDlSH
(OAR AND .AGAHAMA .AGAHAMA #LARKE AND
(OAR +AGAWA 4AKANO AND .AGAHAMA
)N ANOTHER SORT OF HISTOCHEMICAL TEST LABELLED ANTISERA
HAVE DEMONSTRATED THE PRESENCE OF `
OESTRADIOL
IN PREOVULATORY FOLLICULAR CELLS OF 3ALMO GAIRDNERI
3CHULZ
)N THE FACE OF EVIDENCE THAT FOLLICULAR CELLS ARE STE
ROIDOGENIC AT LEAST IN SOME SPECIES IT IS A PARADOX THAT
THEY REVEAL LITTLE ULTRASTRUCTURAL EVIDENCE OF THIS ACTIV
ITY SUCH AS ABUNDANT AGRANULAR ENDOPLASMIC RETICU
LUM TUBULAR MITOCHONDRIAL CRISTAE OR LIPID DROPLETS
BUT APPEAR TO BE ENGAGED IN ACTIVE PROTEIN PRODUCTION
4SUNEKI AND 'ORBMAN (OAR AND .AGAHAMA
VAN DEN (URK AND 0EUTE +AGAWA ET AL
/HTA AND 4ERANISHI .AGAHAMA +AGAWA
AND 9OUNG .AKAMURA 3PECKER AND .AGAHAMA
&OR EXAMPLE IN TWO SPECIES OF SALMON /N
CORHYNCHUS KISUTCH AND / GORBUSCHA THE FOLLICULAR
CELLS OF PREOVULATORY FOLLICLES DEMONSTRATED EXTENSIVE
GRANULAR ENDOPLASMIC RETICULUM CONTAINING AMORPHOUS
MATERIAL OF VARIABLE ELECTRON DENSITY &IGURE !
.AGAHAMA #LARKE AND (OAR (OWEVER SINCE
A SMALL AMOUNT OF TUBULAR AGRANULAR ENDOPLASMIC RE
TICULUM WAS PRESENT ESPECIALLY WITHIN THE WELL
DEVEL
OPED 'OLGI lELDS AND TUBULAR CRISTAE OCCURRED IN SOME
MITOCHONDRIA THE POSSIBLE INVOLVEMENT OF THE FOL
LICULAR CELLS IN STEROID PRODUCTION CANNOT BE EXCLUDED
$URING VITELLOGENESIS FOLLICULAR CELLS OF THE MEDAKA
/RYZIAS LATIPES CONTAIN ABUNDANT GRANULAR ENDOPLAS
MIC RETICULUM AND MITOCHONDRIA WITH LAMELLAR CRISTAE
JUST BEFORE OVULATION THE CISTERNAE OF THE ENDOPLASMIC
RETICULUM BECOME DILATED AND TUBULAR CRISTAE APPEAR
WITHIN THE MITOCHONDRIA &IGURE +AGAWA AND
4AKANO )WAMATSU ET AL .AKASHIMA AND
)WAMATSU 3IMILAR OBSERVATIONS WERE RECORDED
DURING OOCYTE MATURATION IN &UNDULUS HETEROCLITUS
WHERE THE PROLIFERATION OF ENORMOUS 'OLGI COMPLEXES
WAS ACCOMPANIED BY AN INCREASE IN AGRANULAR ENDO
PLASMIC RETICULUM AND A DECREASE IN BOTH FREE RIBO
SOMES AND GRANULAR ENDOPLASMIC RETICULUM 7ALLACE
AND 3ELMAN
&OLLICULAR CELLS OF SOME SPECIES HAVE BEEN SHOWN TO
HAVE A MECHANICAL FUNCTION DURING OVULATION APPLY
ING A GENTLE STEADY CONSTRICTION THAT EXTRUDES THE EGG
FROM THE FOLLICLE &IGURE 9ORKE AND -C-ILLAN
4HIS TOPIC WILL BE CONSIDERED MORE FULLY IN THE
SECTION ON /VULATION PAGE
4HECA AND THE /VARIAN 3TROMA
0ERITONEAL CELLS CONTINUOUS WITH THOSE LINING THE COE
LOM FORM A SIMPLE SQUAMOUS MESOTHELIUM THAT COV
ERS THE OVARY AND IN HOLLOW OVARIES LINES THE LUMEN
)N THE SALMON /NCORHYNCHUS SPP THE LATERAL PLASMA
MEMBRANES OF THESE CELLS ARE HEAVILY CONVOLUTED AND
JOINED BY TIGHT JUNCTIONS AND DESMOSOMES .AGAHAMA
#LARKE AND (OAR "OTH GRANULAR AND AGRANULAR
ENDOPLASMIC RETICULUM ARE PRESENT WITHIN THE MESO
THELIAL CELLS AS WELL AS SMALL MITOCHONDRIA MICROlLA
MENTS AND FREE RIBOSOMES -ICROPINOCYTOTIC VESICLES
OCCUR FREQUENTLY AT BOTH APICAL AND BASAL SURFACES
4IGHT JUNCTIONS AND GAP COMMUNICATING JUNCTIONS
ARE DESCRIBED BETWEEN THE MESOTHELIAL CELLS OF THE OVA
RY OF THE ZEBRAlSH "RACHYDANIO RERIO &IGURE !
+ESSEL 2OBERTS AND 4UNG 4HE TIGHT JUNCTIONS
EXHIBIT MANY DISCONTINUITIES INDICATING THAT THEY MAY
REINFORCE THE EPITHELIUM AS WELL AS SERVING THEIR OC
CLUDING FUNCTION &REEZE FRACTURE SHOWS THE PRESENCE
OF MANY MICROPINOCYTIC PITS IN THESE SQUAMOUS CELLS
&IGURES " # PERHAPS INDICATING THAT MICROPI
NOCYTOSIS OCCURS UNDER CERTAIN CONDITIONS
"ELOW THIS VISCERAL PERITONEUM THERE MAY BE A CAP
SULE THE 45.)#! !,"5').%! CONSISTING OF CONNECTIVE
TISSUE SMOOTH MUSCLE AND OCCASIONAL NON
MYELINATED
NERVE lBRES &IGURE )N THE TUBULAR OVARY OF THE
PIPElSH 3YNGNATHUS SCOVELLI SEVERAL CIRCUMFERENTIAL
#(!04%2
SMOOTH MUSCLE LAYERS SEPARATED BY LOOSE lBROUS CON
NECTIVE TISSUE LIE INTERNAL TO THE COELOMIC EPITHELIUM
PERPENDICULAR TO THE LONGITUDINAL AXIS OF THE OVARY
&IGURE # "EGOVAC AND 7ALLACE )T IS
SUGGESTED THAT EGG RELEASE MAY BE CONTROLLED BY A CON
TRACTION WAVE OF THE OVARIAN WALL COORDINATED BY LARGE
BUNDLES OF NON
MYELINATED NERVES COURSING BETWEEN
THE MUSCLE lBRES THAT BEGINS CRANIALLY AND PROCEEDS IN
A CAUDAL DIRECTION SQUEEZING THE EGGS FROM THE OVAR
IAN LUMEN
4HE CAPSULE ENCLOSES A 342/-! OF RICHLY VASCULAR
LOOSE lBROUS CONNECTIVE TISSUE THAT INVESTS THE DEVELOP
ING FOLLICLES &IGURE 3OME STROMAL lBROBLASTS
mATTEN THEMSELVES AROUND THE BASEMENT MEMBRANE OF
THE FOLLICULAR EPITHELIUM TO FORM A THIN LAYER OF CELLS
THE &/,,)#5,!2 4(%#! !S THE FOLLICLES GROW AND DIS
TEND THE SURFACE OF THE OVARY THE STROMA SEPARATING
THE THECA AND MESOTHELIUM MAY BECOME EXTREMELY
ATTENUATED &IGURE ! AND WHERE TWO FOLLICLES
ABUT THE STROMA MAY BE EXCLUDED SO THAT A SINGLE THECA
IS SHARED BETWEEN THEM &IGURE " "EGOVAC AND
7ALLACE
)N THE OVARY OF THE PIPElSH ARTERIOLES ARISING NEAR
THE OVARIAN WALL CARRY BLOOD TO CAPILLARIES AND VEINS
NEAR THE LUMINAL EPITHELIUM BATHING THE FOLLICLES WITH
BLOOD NUTRIENTS AND PLASMA PROTEINS MOST NOTABLY VI
TELLOGENIN "EGOVAC AND 7ALLACE ! SIGNIlCANT
PORTION OF THE STROMA OF THE PIPElSH OVARY CONTAINS AN
EXTENSIVE LYMPHATIC COMPARTMENT LINED BY ATTENUATED
ENDOTHELIAL CELLS LOOSELY LINKED BY DESMOSOMES &IG
URE 4HIS LYMPHATIC NETWORK IS DESCRIBED AS A
hSEAv IN WHICH DEVELOPING FOLLICLES RESIDE ITS SIGNIl
CANCE IS UNCLEAR
%ACH FOLLICLE IN THE OVARY OF &UNDULUS HETEROCLITUS
IS VASCULARIZED BY AN ARTERIOLE THAT ARRIVES WITHIN A
STALKLIKE STRUCTURE OF STROMAL ELEMENTS &IGURE
"RUMMETT $UMONT AND ,ARKIN !BUNDANT
COLLAGEN IRREGULARLY ARRANGED SMOOTH MUSCLE CELLS
AND OCCASIONAL NERVE lBRES CONSTITUTE THE REMAINDER
OF THE STALK 4HE STALK IS ENVELOPED BY AN EPITHELIOID
LAYER OF STROMAL CELLS "RANCHES OF THE ARTERIOLE PEN
ETRATE DEEPLY INTO THE INVESTING LAYERS OF THE FOLLICLE
BRINGING BLOOD TO A CAPILLARY BED THAT IS DRAINED BY
MORE SUPERlCIAL VENULES THESE mOW INTO A RING
LIKE
VESSEL SURROUNDING THE PRESUMED OVULATION SITE OF THE
FOLLICLE 4HIS SYSTEM OF VESSELS TERMINATES IN A SINGLE
COLLECTING VEIN THAT LEAVES THE FOLLICLE AND COURSES TO
WARD THE OUTER SURFACE OF THE OVARY %NDOTHELIAL CELLS
OF THE FOLLICULAR CAPILLARIES OF THE ZEBRAlSH "RACHY
DANIO RERIO ARE CONNECTED BY TIGHT JUNCTIONS AND AC
TIVE MICROPINOCYTOSIS RIDDLES THEIR SURFACES &IGURE
+ESSEL 2OBERTS AND 4UNG 4HE TIGHT
JUNCTIONS ARE NOT EXTENSIVELY DEVELOPED AND THEIR
PARTICLES ADHERE PREFERENTIALLY TO THE % FACE THEY ARE
CLOSELY ASSOCIATED WITH GAP COMMUNICATING JUNC
TIONS )T IS ASSUMED THAT THERE IS A SELECTIVE CHANNEL
ING OF MATERIALS ACROSS THE ENDOTHELIAL CELLS BY WAY
OF MICROVESICLES
4HE THECA lRST APPEARS DURING PREVITELLOGENESIS
WHEN A FEW THIN CELLS RESEMBLING lBROBLASTS SURROUND
THE BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM
&IGURE "USSON -ABILLOT B 5LRICH
#APORICCIO AND #ONNES "RUSL
"EGOVAC AND 7ALLACE 'RIER 4HE THECAL
CELLS MULTIPLY AND INCREASE IN THICKNESS DURING VITELLO
GENESIS COLLAGENOUS lBRES CONTINUOUS WITH lBRES IN
THE BASEMENT MEMBRANE COURSE BETWEEN THEM &IG
URE #APORICCIO AND #ONNES )N SOME
SPECIES A SINGLE LAYER OF SQUAMOUS CELLS MAY PERSIST
THROUGHOUT OOGENESIS BUT IN OTHERS SEVERAL LAYERS OF
CELLS APPEAR SOMETIMES FORMING TWO DISTINCT LAYERS
THE THECA INTERNA AND THECA EXTERNA
)N ADDITION TO FORMING A PROTECTIVE CAPSULE AROUND
THE FOLLICLE VARIOUS OTHER FUNCTIONS HAVE BEEN ASCRIBED
TO THE THECA )T IS THE lRST BARRIER BETWEEN THE EXTRAVAS
CULAR SPACES AND THE FOLLICULAR EPITHELIUM AND MAY EX
ERT SOME LEVEL OF SELECTIVITY ON THE MATERIALS PERMITTED
TO ENTER AND LEAVE THE FOLLICLE )N SOME SPECIES THECAL
CELLS GIVE EVIDENCE OF BEING STEROIDOGENIC ASSUM
ING AN ENDOCRINE ROLE !S WELL THE THECA MAY CONTAIN
SMOOTH MUSCLE AND IS PRESUMED TO ASSIST IN THE EXPUL
SION OF THE EGG DURING OVULATION
4HE THECA OF SMALL FOLLICLES OF -YXINE GLUTINOSA
CONSISTS OF POORLY DIFFERENTIATED CELLS PROBABLY lBRO
BLASTS IN A CONNECTIVE TISSUE MATRIX &IGURE
0ATZNER 4SUNEKI AND 'ORBMAN !T LATER
STAGES HOWEVER TWO THECAL LAYERS CAN BE DISTINGUISHED
CONSISTING OF POORLY DIFFERENTIATED lBROBLAST LIKE CELLS
AND CELLS THAT ARE POSSIBLY SECRETORY &IGURE
4HE lBROBLASTS HAVE A CONSPICUOUS GRANULAR ENDOPLAS
MIC RETICULUM AND LARGE LIPID LIKE INCLUSIONS &ERN
HOLM .O CELLS OF AN APPARENTLY STEROIDOGENIC
NATURE WERE FOUND
)N EARLY STAGES OF THECAL DEVELOPMENT IN THE LAMPREY
,AMPETRA PLANERI LOOSE lBROUS CONNECTIVE TISSUE OF
THE STROMA ENCLOSES THE FOLLICLES IT CONTAINS OCCASION
AL NERVE lBRES AND BLOOD VESSELS APPLIED TO THE BASAL
LAMINAE OF THE FOLLICULAR EPITHELIUM "USSON -ABILLOT
B $URING PREVITELLOGENESIS THIS SIMPLE CONNEC
TIVE TISSUE LAYER DIFFERENTIATES INTO A THECA EXTERNA AND
/6!2)!. &/,,)#,%3
THECA INTERNA 4HE CONNECTIVE TISSUE OF THE EARLY FOL
LICLE PERISISTS THROUGHOUT FOLLICULAR DEVELOPMENT AS THE
THECA EXTERNA 'RANULAR ENDOPLASMIC RETICULUM 'OLGI
COMPLEXES AND LARGE LIPID DROPLETS APPEAR IN THE CELLS
OF THE THECA INTERNA DURING PREVITELLOGENESIS BUT AS VI
TELLOGENESIS GAINS MOMENTUM THE THECAL CELLS ENLARGE
AND THESE ORGANELLES DIMINISH AS THE CELLS BECOME
PACKED WITH GRANULAR ENDOPLASMIC RETICULUM &IGURES
AND ,ARGE SPACES APPEAR BETWEEN THE
CELLS OF THE THECA INTERNA ACROSS WHICH THE CELLS EXTEND
SLENDER PROCESSES )T IS SUGGESTED THAT THE CELLS OF THE
THECA INTERNA SECRETE STEROIDS
)N SOME ELASMOBRANCHS EG 3CYLIORHINUS SORRA
KOWAH THE THECA EXTERNA IS MADE UP OF lBROBLASTS EM
BEDDED IN VASCULAR lBROUS CONNECTIVE TISSUE WHILE THE
THECA INTERNA CONSISTS OF POLYHEDRAL CELLS CONTAINING
LIPID DROPLETS #ALLARD ET AL 4HE REVERSE IS TRUE
IN OTHER SPECIES EG 3CYLIORHINUS CANICULA WHERE
THE THECA INTERNA IS lBROBLASTIC AND THE THECA EXTERNA
CONTAINS CUBOIDAL CELLS MANIFESTING AGRANULAR ENDO
PLASMIC RETICULUM MITOCHONDRIA WITH TUBULAR CRISTAE
AND LIPID DROPLETS $ODD AND $ODD THESE CELLS
APPEAR TO BE STEROIDOGENIC
4HE THECA OF IMMATURE FOLLICLES OF TWO CICHLIDS
#ICHLASOMA NIGROFASCIATUM AND (APLOCHROMIS MULTI
COLOR IS POORLY VASCULARIZED AS THE FOLLICLE DEVELOPS
THE VASCULARIZATION OF THE THECA INCREASES .ICHOLLS
AND -APLE %NDOTHELIAL CELLS OF THE CAPILLARIES
DEMONSTRATE ACTIVE PINOCYTOSIS INDICATING TRANSFER TO
OR FROM THE BLOOD STREAM 4HE THECAL CELLS ARE APPAR
ENTLY DERIVED FROM lBROBLASTS $URING PRIMARY OOCYTE
GROWTH THEY FORM A SIMPLE SQUAMOUS LAYER OF CELLS
AROUND THE BASEMENT MEMBRANE OF THE FOLLICULAR EPI
THELIUM 4HESE CELLS ARE EXTREMELY THIN AND CONTAIN
FEW ORGANELLES !S DEVELOPMENT PROCEEDS THEIR HEIGHT
INCREASES BUT THEIR ORGANELLES ARE LITTLE CHANGED ISO
LATED CISTERNAE OF GRANULAR ENDOPLASMIC RETICULUM
OCCASIONAL MITOCHONDRIA AND FREE POLYRIBOSOMES
$URING VITELLOGENESIS HOWEVER A FEW THECAL CELLS
USUALLY THOSE LYING CLOSE TO CAPILLARIES TRANSFORM
INTO TYPICAL STEROIDOGENIC ELEMENTS 4HE CYTOPLASM OF
THESE LARGE ROUNDED CELLS IS lLLED WITH AGRANULAR EN
DOPLASMIC RETICULUM AND THE MITOCHONDRIA APPEAR TO
HAVE TUBULAR CRISTAE
%VIDENCE OF STEROIDOGENESIS MAY APPEAR IN THECAL
CELLS OF TELEOSTS DURING DEVELOPMENT OF THE FOLLICLE OF
SOME SPECIES !CTIVITY OF THE ENZYME `
HYDROXYSTER
OID DEHYDROGENASE `
(3$ HAS OFTEN BEEN DETECTED
AND THE CELLS MAY MANIFEST THE FAMILIAR APPEARANCE
OF STEROIDOGENIC CELLS ABUNDANT AGRANULAR ENDOPLAS
MIC RETICULUM AND MITOCHONDRIA PACKED WITH TUBULAR
CRISTAE 4HESE OBSERVATIONS ARE FAR FROM CONSISTENT SO
THAT IN SOME SPECIES THE THECAL CELLS GIVE NO HINT OF
STEROIDOGENIC ACTIVITY WHILE IN OTHERS THE EVIDENCE IS
CLEAR )N A STUDY OF THREE SPECIES `
(3$ ACTIVITY WAS
NOTED IN THECAL CELLS OF MATURING OOCYTES OF THE CARP
#YPRINUS CARPIO BUT NONE IN FOLLICULAR CELLS ,IVNI
)N -UGIL CAPITO AND 4ILAPIA AUREA HOWEVER THIS
ACTIVITY WAS DEMONSTRATED IN FOLLICULAR CELLS %NZYME
ACTIVITY DISAPPEARED IN ALL SPECIES BEFORE SPAWNING
3TEROIDOGENESIS MAY BE DETECTED WITHIN ORDINARY
THECAL CELLS BUT SOMETIMES CLUMPS OF 30%#)!, 4(%#!,
#%,,3 APPEAR TO HAVE TAKEN OVER THIS FUNCTION 9AMA
MOTO AND /NOZATO .ICHOLLS AND -APLE
.AGAHAMA #HAN AND (OAR .AGAHAMA #LARKE
AND (OAR +AGAWA 4AKANO AND .AGAHAMA
"RUSL -ATSUYAMA .AGAHAMA AND
-ATSUURA .AKAMURA 3PECKER AND .AGAHAMA
3PECIAL THECAL CELLS OCCUR IN THE THECA EXTERNA
OF SOME SPECIES EG RAINBOW TROUT 3ALMO GAIRDNERI
VAN DEN (URK AND 0EUTE AND THECA INTERNA OF
OTHERS EG ZEBRAlSH "RACHYDANIO RERIO 9AMAMOTO
AND /NOZATO 4HEY ARE LARGER THAN ORDINARY THE
CAL CELLS AND ARE OFTEN FOUND NEAR BLOOD VESSELS 4HEY
REACT POSITIVELY FOR THE PRESENCE `
(3$ AND CONTAIN
ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM AS WELL
AS LARGE MITOCHONDRIA WITH DENSE MATRIX AND TUBULAR
CRISTAE GRANULAR ENDOPLASMIC RETICULUM APPEARS TO BE
ABSENT &IGURES AND 4HEY APPEAR TO ARISE
FROM INTERSTITIAL CELLS OF lBROBLASTIC ORIGIN 9AMAMOTO
AND /NOZATO VAN DEN (URK AND 0EUTE
#ELLS DISPLAYING THE ULTRASTRUCTURAL CHARACTERISTICS
OF STEROIDOGENESIS ARE ALSO FOUND IN THE INTERSTITIAL TIS
SUE BETWEEN SMALL OOCYTES FORMING CLUMPS WITH OTH
ER TYPES OF CELLS SUCH AS lBROBLASTS &IGURE #
9AMAMOTO AND /NOZATO .AKAMURA 3PECKER
AND .AGAHAMA )N TILAPIA /REOCHROMIS NILOTI
CUS IT IS CONCLUDED THAT THESE STEROID PRODUCING CELLS
ARE DERIVED FROM TISSUES NEAR THE OVARIAN ARTERY AND
VEIN &IGURES ! " AND MIGRATE TO THE INTERSTITIAL
AREAS DURING POSTHATCHING DEVELOPMENT COINCIDENT
WITH VASCULARIZATION OF THE INTERSTITIAL TISSUE 4HEY l
NALLY ENCLOSE OOCYTES DURING EARLY VITELLOGENESIS AT
A TIME WHEN PRODUCTION OF OESTRADIOL
` INCREASES
&IGURES $ TO &
)N THE RAINBOW TROUT 3ALMO GAIRDNERI THE PERIPHERAL
THECAL LAYER GRADUALLY MERGES INTO THE INTERSTITIAL TIS
SUE VAN DEN (URK AND 0EUTE )NTERSTITIAL CELLS
AND SPECIAL THECAL CELLS CONTAIN AGRANULAR ENDOPLAS
MIC RETICULUM AND MITOCHONDRIA WITH TUBULAR CRISTAE
#(!04%2
THROUGHOUT THE ANNUAL CYCLE )N ADDITION THESE CELLS
CONTAIN FREE RIBOSOMES GRANULAR ENDOPLASMIC RETICU
LUM POLYRIBOSOMES 'OLGI CISTERNAE A FEW LYSOSOME
LIKE BODIES AND LIPID DROPLETS (ISTOCHEMICAL TESTS
INDICATE THAT THE INTERSTITIAL CELLS AND SPECIAL THECAL
CELLS ARE THE SITES OF MOST INTENSE STEROIDOGENESIS ES
PECIALLY DURING THE PERIOD WHEN MATURATION OF OOCYTES
AND OVULATION TAKES PLACE !T THIS TIME THE NUMBERS
OF THESE STEROIDOGENIC CELLS INCREASE 4HE LOCALIZA
TION AND NATURE OF THE SPECIAL THECAL CELLS IN THE TROUT
OVARY INDICATE THAT THEY ARE INTERSTITIAL CELLS FOUND IN
THE OUTER PART OF THE THECA OF PRE AND POSTOVULATORY
FOLLICLES
"UNDLES OF NERVE lBRES PRESUMABLY AUTONOMIC
COURSE AMONG THE YOLKY FOLLICLES AND STEROID PRO
DUCING CELLS OF TILAPIA /REOCHROMIS NILOTICUS &IGURE
% .AKAMURA 3PECKER AND .AGAHAMA
4HICK NERVE BUNDLES ENTER THE OVARY IN ASSOCIATION
WITH THE OVARIAN ARTERY AND VEIN &IGURES ! TO #
AND SEND OUT BRANCHES THAT INVADE THE CENTRAL PARTS OF
THE OVIGEROUS LAMELLAE 'ROUPS OF AXONS RAMIFY FROM
THESE BUNDLES TO PENETRATE THE SPACES BETWEEN CLUSTERS
OF STEROID PRODUCING CELLS &IGURE $ FORMING
SLIGHTLY SWOLLEN TERMINALS NEAR THESE CELLS &IGURES
! TO $ 4HE NERVE ENDINGS CONTAIN MANY CLEAR
SYNAPTIC VESICLES TO NM IN DIAMETER A FEW
DENSE CORED VESICLES TO NM AND SOME MITO
CHONDRIA NO SYNAPTIC STRUCTURES WERE NOTED SUCH AS
A CLEFT WITH ELECTRON DENSE MATERIAL OR PRE AND POST
SYNAPTIC MEMBRANE SPECIALIZATIONS )T IS SUGGESTED
THAT THESE TERMINALS PLAY A ROLE IN THE REGULATION AND
PRODUCTION OF STEROID HORMONES IN THE OVARY BY RELEAS
ING TRANSMITTER SUBSTANCES NON SYNAPTICALLY
3MOOTH MUSCLE MAY BE INCLUDED IN THE THECA OF
SOME SPECIES 4HE THECA OF THE PREOVULATORY FOLLICLE
OF THE TROUT 3ALMO GAIRDNERI CONSISTS OF ALTERNATING
LAYERS OF mATTENED SMOOTH MUSCLE AND COLLAGENOUS l
BRES ENCLOSING THE BASEMENT MEMBRANE OF THE FOLLICLE
&IGURE 3ZLLSI *ALABERT AND "RETON
4HE MUSCLE lBRES DISPLAY THE ACTIVE PINOCYTOSIS
TYPICAL OF SMOOTH MUSCLE CELLS AND CONTAIN ABUNDANT
MICROlLAMENTS TO NM IN DIAMETER )T IS SUGGESTED
THAT CONTRACTION OF THESE lBRES ASSISTS IN THE EXPULSION
OF THE EGG AT OVULATION
/6!2)!. &/,,)#,%3
&IGURE $RAWINGS ILLUSTRATING FOLLICULAR DEVELOPMENT IN THE OVARY OF THE SURFPERCH #YMATOGASTER /OCYTES DEVELOP IN
OVIGEROUS FOLDS UPPER LEFT &ROM (OAR REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE AND *0 7IEBE
! ! NEST OF OOCYTES IN EARLY STAGES OF DEVELOPMENT
" !S THEY GROW AND MATURE VARIOUS INTRACELLULAR AND EXTRACELLULAR CHANGES OCCUR )NITIALLY FOLLICULAR CELLS FORM A SIMPLE SQUA
MOUS EPITHELIUM AROUND EACH OOCYTE
# !S DEVELOPMENT PROCEEDS THE FOLLICULAR CELLS ENLARGE AND MAY BECOME CUBOIDAL AND EVEN COLUMNAR 4HE FOLLICULAR EPITHE
LIUM IS SURROUNDED BY ITS OWN BASAL LAMINA WHICH SEPARATES IT FROM A SHEATH OF CONDENSED VASCULAR CONNECTIVE TISSUE THE
THECA FOLLICULI 4HE THECA CONTAINS lBROBLASTS COLLAGENOUS lBRES AND CAPILLARIES AND IN SOME SPECIES SPECIAL THECAL STEROID
PRODUCING CELLS
#(!04%2
&IGURE $URING OOGENESIS A THICK TRANSLUCENT ACELLULAR ZONA PELLUCIDA OR VITELLINE ENVELOPE DEVELOPS BETWEEN THE
OOCYTE AND FOLLICULAR CELLS )T IS SHOWN HERE AS TWO LAYERS ZONA PELLUCIDA AND ZONA RADIATA 4HIS DIAGRAM SHOWS A PORTION OF THE
PERIPHERAL REGION OF A TROUT OOCYTE WITH ITS ENVELOPING MEMBRANES !S THE OOCYTE GROWS THE ZONA PELLUCIDA BECOMES PERFORATED
BY PORE CANALS ENABLING AN EXCHANGE OF MATERIALS BETWEEN THE OOCYTE AND FOLLICULAR CELLS THESE CHANNELS CONTAIN MICROVILLI THAT
EXTEND FROM BOTH THE OOCYTE SURFACE AND THE FOLLICULAR CELLS 8 &ROM (URLEY AND &ISHER REPRODUCED WITH PERMIS
SION OF THE .2# 0RESS
/6!2)!. &/,,)#,%3
&IGURE $IAGRAM ILLUSTRATING GROWING OOCYTES OF THE MEDAKA /RYZIAS LATIPES AT VARIOUS STAGES OF OOGENESIS &ROM
)WAMATSU ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
!BBREVIATIONS ! ANIMAL POLE "" JUXTANUCLEAR COMPLEX YOLK NUCLEUS OR "ALBIANI BODY /7 OVARIAN WALL 0/ POSTOVULA
TORY FOLLICLE JUST AFTER OVULATION 0/ POSTOVULATORY FOLLICLE HOURS AFTER OVULATION 6 VEGETAL POLE 9 YOLK MASS 96 YOLK
VESICLE
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF THE GERMINAL RIDGE '2 AND EARLY FOLLICULAR PROGRESSION IN THE SEAHORSE (IPPOCAMPUS
ERECTUS &ROM 3ELMAN 7ALLACE AND 0LAYER REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !N OVERVIEW SHOWING THE RELATIONSHIP OF THE LUMINAL EPITHELIUM ,% GERMINAL RIDGE AND DEVELOPING FOLLICLES 4HE GERMI
NAL RIDGE CONTAINING TWO ADJACENT OOCYTES / AND SEVERAL PREFOLLICULAR CELLS 0 IS AN OUTFOLDING OF THE LUMINAL EPITHELIUM
4HE BASAL LAMINA ARROWHEADS UNDERLYING THE LUMINAL EPITHELIUM IS CONTINUOUS WITH THE BASAL LAMINA SURROUNDING THE
GERMINAL RIDGE ! PRIMORDIAL FOLLICLE 0& SURROUNDED BY mATTENED FOLLICULAR CELLS IS hPINCHINGv AWAY FROM THE GERMINAL
RIDGE SEE # 4HE AREA BETWEEN THE DASHED LINES IS MAGNIlED IN " /
OOCYTE IN A DElNITIVE FOLLICLE OF THE EARLY FOLLICULAR
PROGRESSION # CONNECTIVE TISSUE CELLS 8
" 0ART OF THE GERMINAL RIDGE AND OVERLYING LUMINAL EPITHELIUM ,% !RROWHEADS INDICATE THE BASAL LAMINA THAT UNDERLIES THE
LUMINAL EPITHELIUM AND SURROUNDS THE GERMINAL RIDGE 8
# (IGHER MAGNIlCATION OF THE PRIMORDIAL FOLLICLE 0& FROM ! THAT IS SEPARATING FROM THE GERMINAL RIDGE 4HE BASAL LAMINA
ARROWHEADS SURROUNDING THE GERMINAL RIDGE HAS NOT YET COMPLETELY SEPARATED THIS PRIMORDIAL FOLLICLE FROM THE GERMINAL
RIDGE . FOLLICULAR CELL NUCLEUS / CONTIGUOUS OOCYTES IN THE GERMINAL RIDGE 0& PREFOLLICULAR CELLS 8
$ /OCYTE / IN A DElNITIVE FOLLICLE THAT HAS SEPARATED FROM THE GERMINAL RIDGE '2 4HE BASAL LAMINA ARROWHEADS SUR
ROUNDING THE GERMINAL RIDGE IS SEPARATE FROM THE BASAL LAMINA ARROWS THAT SURROUNDS THE PRIMORDIAL FOLLICLE #YTOPLASMIC
lLAMENTS ARE VISIBLE IN THE PREFOLLICULAR CELLS . NUCLEUS OF THE FOLLICULAR CELL 8
/6!2)!. &/,,)#,%3
&IGURE $IAGRAMMATIC REPRESENTATION OF THE ELEVEN STAGES ARBITRARILY ASSIGNED TO OOGENESIS IN "LENNIUS PHOLIS &ROM
3HACKLEY AND +ING REPRODUCED WITH PERMISSION OF THE AUTHORS
! 3TAGE FOLLICLE CONSISTING OF AN OOGONIUM SURROUNDED BY SQUAMOUS FOLLICULAR CELLS 4HE FOLLICULAR CELLS CONTAIN CYTOPLASMIC
lLAMENTS
" %ARLY STAGE OOCYTE AND SQUAMOUS FOLLICULAR EPITHELIUM
# ,ATE STAGE OOCYTE AND SQUAMOUS FOLLICULAR EPITHELIUM
#(!04%2
&IGURE #ONTINUED
$ %ARLY STAGE OOCYTE WITH COLUMNAR FOLLICULAR EPITHELIUM
% ,ATE STAGE OOCYTE WITH COLUMNAR FOLLICULAR EPITHELIUM
& 3TAGE OOCYTE SURROUNDED BY A CUBOIDAL FOLLICULAR EPITHELIUM 4HE CORTEX OF THE OOCYTE IS DIVISIBLE INTO REGIONS INNER
CORTEX MID CORTEX OUTER CORTEX AND PERIPHERY
/6!2)!. &/,,)#,%3
&IGURE #ONTINUED
' 3TAGE OOCYTE WITH COLUMNAR FOLLICULAR EPITHELIUM
( 3TAGE OOCYTE WITH CUBOIDAL FOLLICULAR EPITHELIUM
&IGURE #ONTINUED
) 3TAGE OOCYTE WITH CUBOIDAL FOLLICULAR EPITHELIUM
* 3TAGE OOCYTE WITH CUBOIDAL FOLLICULAR EPITHELIUM
#(!04%2
/6!2)!. &/,,)#,%3
&IGURE #ONTINUED
+ 3TAGE OOCYTE WITH CUBOIDAL FOLLICULAR EPITHELIUM
, 3TAGES PREOVULATIONOVULATION OOCYTE 4HE OOCYTE IS RELEASED FROM THE FOLLICLE AT OVULATION
&IGURE %LECTRON MICROGRAPH OF AN OOGONIUM /' WITHIN THE GERMINAL RIDGE OF THE PIPElSH 3YNGNATHUS SCOVELLI
4HERE IS A SINGLE NUCLEOLUS WITHIN THE OVAL NUCLEUS -ITOCHONDRIA NUAGE MATERIAL ARROWS AND ENDOPLASMIC RETICULUM ARE
PRESENT WITHIN THE CYTOPLASM 3OME DENSE
CORED GRANULES ARE SEEN ABOVE THE NUCLEOLUS ARROWHEAD 8 &ROM "EGOVAC
AND 7ALLACE REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF OOCYTES / OF THE PIPElSH 3YNGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! #ELLULAR ORGANELLES OCCUR AROUND THE CENTRIOLES ARROW AT ONE SIDE OF THE NUCLEUS 'OLGI COMPLEXES ' HAVE APPEARED 4HE
SPHERICAL NUCLEUS CONTAINS DENSE CORED GRANULES ARROWHEAD ,EPTOTENE CHROMATIN IS ELECTRON DENSE 8
" #HROMATIN IS PACHYTENE ,ONG SYNAPTONEMAL COMPLEXES ARROWS ARE PRESENT IN THE NUCLEUS 4HE NUCLEUS IS LESS ELECTRON
DENSE THAN IN &IGURE ! $ENSE CORED GRANULES ARROWHEAD CAN BE SEEN IN THE NUCLEUS 8
# $ENSE CORED GRANULES SPECIlC TO GERM CELL NUCLEI 8
&IGURE %LECTRON MICROGRAPH SHOWING A CYTOPLASMIC BRIDGE )" BETWEEN TWO OOGONIA FROM THE EEL !NGUILLA ANGUILLA
%LECTRON DENSE MATERIAL OUTLINES THE CYTOPLASMIC SIDE OF THE BRIDGE WHICH APPEARS TO BE TRAVERSED BY CISTERNAE OF ENDOPLAS
MIC RETICULUM %2 AND MICROTUBULES MT ! PAIR OF CENTRIOLES #T AND VESICLES OF A 'OLGI COMPLEX ' LIE NEAR THE BRIDGE
4HE OOGONIA ARE ENVELOPED BY SOMATIC CELLS 3# THAT ARE RICH IN MICROlLAMENTS AND SEPARATED BY A BASAL LAMINA ", FROM THE
CONNECTIVE TISSUE STROMA C hCEMENTv CF COLLAGEN lBRES OF THE STROMA - MITOCHONDRIA N hNUAGEv ./ NUCLEI OF THE OOGO
NIA 8 &ROM 'RANDI AND #OLOMBO REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
/6!2)!. &/,,)#,%3
&IGURE !N INCREASE IN SIZE IS THE MOST OBVIOUS MANIFESTATION OF OOCYTE DEVELOPMENT 4HE OOCYTE GROWS BOTH BY AN
ENLARGEMENT OF THE NUCLEUS AND THE ADDITION OF CYTOPLASM ,ATER MOST GROWTH IS DUE TO AN INCREASE IN THE AMOUNT OF CYTOPLASM
AND IN THE lNAL STAGES OF MATURATION THE OOCYTE HAS ITS FULL COMPLEMENT OF YOLK AND IS READY TO BE OVULATED 3EVEN PRINCIPAL
STAGES OF OOCYTE DEVELOPMENT IN THE RAINBOW TROUT 3ALMO GAIRDNERI ARE SHOWN IN THESE PHOTOMICROGRAPHS &ROM VAN DEN (URK
AND 0EUTE REPRODUCED WITH PERMISSION OF THE AUTHOR
! 0REVITELLOGENIC FOLLICLE STAGE ' FOLLICULAR LAYER 8
" # 0REVITELLOGENIC FOLLICLES STAGE . NUCLEUS .U NUCLEOLUS 9N YOLK NUCLEUS 8 AND 8
$ 0REVITELLOGENIC FOLLICLE 3TAGE ' FOLLICULAR LAYER . NUCLEUS 4 THECA 9N YOLK NUCLEI :R ZONA PELLUCIDA 8
% 0ORTION OF AN OVARY WITH VITELLOGENIC FOLLICLES AT STAGES AND 0V PREVITELLOGENIC FOLLICLES 8
&
$ETAIL OF VITELLOGENIC FOLLICLES AT STAGES AND %N ENDOGENOUS YOLK %X EXOGENOUS YOLK ' FOLLICULAR LAYER )T INTER
STITIAL TISSUE 4 THECA :R ZONA PELLUCIDA 8
' 0ORTIONS OF TWO VITELLOGENIC FOLLICLES AT STAGE SHOWING AGGREGATED EXOGENOUS YOLK GRANULES %X ' FOLLICULAR LAYER
4 THECA :R ZONA PELLUCIDA 8
#(!04%2
&IGURE #ONTINUED
( 0ORTIONS OF MATURE FOLLICLES AT STAGE &LUID lLLS THE SPACE &S BETWEEN THE THECA 4 AND THE INTERSTITIAL TISSUE )T ' FOL
LICULAR LAYER :R ZONA PELLUCIDA 8
) 0OSTOVULATORY FOLLICLES 4HE FOLLICULAR LAYER ' IS CONTINUOUS WITH THE GERMINAL EPITHELIUM 'E 34# SPECIAL THECAL CELLS
8
/6!2)!. &/,,)#,%3
&IGURE #LASSIlCATION OF STAGES OF OVARIAN MATURITY BY MACROSCOPIC OBSERVATION ARE USEFUL IN FECUNDITY STUDIES 4HESE
HAVE BEEN ADAPTED USING HISTOLOGICAL CRITERIA FOR THE PIKE %SOX LUCIUS &ROM 4REASURER AND (OLLIDAY REPRODUCED WITH
PERMISSION FROM %LSEVIER 3CIENCE
! 3TAGE ) 0HOTOMICROGRAPH OF A TRANSVERSE SECTION OF AN IMMATURE OVARY SHOWING THREE STAGES IN OOCYTE DEVELOPMENT
" 3TAGE ))$ 4HE INTERNAL ORGANIZATION OF A LAMELLA
# 3TAGE ))) &OLLICLE AND CHORION OF DEVELOPING OVARY
$ 3TAGE )6 4HE OOCYTES ARE GREATLY ENLARGED IN THE MATURING OVARY
#(!04%2
&IGURE #ONTINUED
% 3TAGE 6 'RAVID OVARY WITH HYALINE OOCYTES
& 3TAGE 6))) 3PENT OVARY SHOWING DISORGANIZED OVIGEROUS LAMELLAE WITH EMPTY FOLLICLES
!BBREVIATIONS BV BLOOD VESSELS EF EMPTY FOLLICLE G FOLLICULAR CELLS O OOCYTE OG OOGONIUM OL OVIGEROUS LAMELLA OW WALL
OF OVIDUCT PT PRIMARY THECA TE THECA EXTERNA TP OUTER REGION OF ZONA PELLUCIDA YV YOLK VESICLE ZR ZONA PELLUCIDA
&IGURE .ESTS OF OOCYTES IN THE OVARY OF "RACHYDANIO RERIO &ROM 3ELMAN ET AL REPRODUCED WITH PERMISSION
OF *OHN 7ILEY 3ONS )NC
! %LECTRON MICROGRAPH OF A NEST OF MEIOTIC OOCYTES 0RE FOLLICULAR CELLS 0& ENVELOP THE NEST OF GERM CELLS BUT DO NOT SURROUND
INDIVIDUAL OOCYTES WHICH THEREFORE ABUT ON EACH OTHER ARROWS %ACH OOCYTE HAS A LARGE NUCLEUS . AND CONTAINS NUAGE
ARROWHEADS IN THE OOPLASM 4HE ASTERISK INDICATES THE OVARIAN LUMEN 8
" 0HOTOMICROGRAPH OF A NEST OF CHROMATIN NUCLEOLUS STAGE OOCYTES SHOWING DISTINCT CHROMOSOMES 8
/6!2)!. &/,,)#,%3
&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH THE OVARY OF THE SEAHORSE (IPPOCAMPUS ERECTUS 0REFOLLICULAR CELLS 0
AN OOGONIUM /G AND MEIOTIC OOCYTES -/ WITH VISIBLE CHROMOSOMES ARE PRESENT WITHIN THE GERMINAL RIDGE ! DEVELOPING
FOLLICLE & HAS SEPARATED FROM THE GERMINAL RIDGE % LUMINAL EPITHELIUM , OVARIAN LUMEN 8 &ROM 3ELMAN AND 7ALLACE
REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
&IGURE -ICROGRAPHS OF PERINUCLEOLAR OOCYTES / OF THE PIPElSH 3YNGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF OOCYTES IN THE PRIMARY GROWTH PHASE 4HE GERMINAL VESICLE '6 CONTAINS SEVERAL NUCLEOLI NEAR ITS
PERIPHERY *UXTANUCLEAR COMPLEXES ARE VISIBLE IN TWO OOCYTES IN THE LEFT OOCYTE IT FORMS AN OVOID MASS ARROW AND AT THE
RIGHT A MORE DIFFUSE CRESCENTIC MASS ARROWHEADS 8
" 0HOTOMICROGRAPH SHOWING THE JUXTANUCLEAR COMPLEX AS A PERINUCLEAR RING ARROWS AROUND THE GERMINAL VESICLE '6
8
#(!04%2
&IGURE #ONTINUED
# )N THIS ELECTRON MICROGRAPH THE ARROWS DESIGNATE A JUXTANUCLEAR COMPLEX OF ORGANELLES "ALBIANI VITELLINE BODY CONTAINING
MITOCHONDRIA AND AN AGGREGATE OF MULTIVESICULAR BODIES IN THE PERIPHERAL OOPLASM 4HE NUCLEUS . OF THE OOCYTE CONTAINS
A PERINUCLEAR NUCLEOLUS ARROWHEAD ", BASAL LAMINA 8
$ %LECTRON MICROGRAPH AT A HIGHER MAGNIlCATION SHOWING THE MULTIVESICULAR BODIES
OF THE JUXTANUCLEAR COMPLEX OF ORGAN
ELLES 8
% %LECTRON MICROGRAPH OF THE PERIPHERAL OOPLASM SHOWING ABUNDANT MITOCHONDRIA AND 'OLGI COMPLEXES ' ! BASAL LAMINA
ARROWHEAD OVERLIES THE SQUAMOUS FOLLICULAR CELLS &# 4HE OOCYTE HAS BEGUN TO ELABORATE NUMEROUS MICROVILLAR PROCESSES
ARROW THAT EXTEND TOWARD THE FOLLICULAR CELLS 8
&IGURE %LECTRON MICROGRAPH OF THE NUCLEOLUS OF A STAGE )) OOCYTE OF THE PIPElSH 3YNGNATHUS SCOVELLI SHOWING THE GRANU
LAR CORTICAL REGION OF TIGHTLY PACKED RIBOSOMES .' AND THE lLAMENTOUS CENTRAL AREA .& 8 &ROM !NDERSON
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
/6!2)!. &/,,)#,%3
&IGURE %LECTRON MICROGRAPHS OF PREVITELLOGENIC OOCYTES OF THE MULLET -UGIL AURATUS 4HE BARS REPRESENT M &ROM
"RUSL REPRODUCED WITH PERMISSION OF THE AUTHOR
! $EPRESSIONS IN THE UNDULATING NUCLEAR ENVELOPE ARROWHEADS NE DISPLAY SEVERAL JUXTANUCLEAR COMPLEXES CI ENCLOSED BY
AGGREGATIONS OF MITOCHONDRIA M 4HE NUCLEOPLASM . WITHOUT EVIDENT CHROMOSOMES CONTAINS A LARGE NUCLEOLUS NU
" ,ATER THE NUCLEUS . BECOMES SPHERICAL WITH AN ALMOST SMOOTH OUTLINE 3EVERAL DENSE HOMOGENEOUS NUCLEOLI NU LIE
CLOSE TO THE INNER NUCLEAR MEMBRANE -ITOCHONDRIA BECOME SCATTERED PERIPHERALLY
!BBREVIATIONS CH CHROMATIN ER ENDOPLASMIC RETICULUM &# FOLLICULAR CELL R RIBOSOMES
#(!04%2
&IGURE 0HASE CONTRAST MICROGRAPH OF A VITELLOGENIC FOLLICLE FROM #YPRINODON VARIEGATUS SHOWING YOLK SPHERES
OF
VARIOUS SIZES WITHIN THE OOPLASM 4HERE ARE SEVERAL LAMPBRUSH CHROMOSOMES WITHIN THE GERMINAL VESICLE '6 &OLLICULAR CELLS
F OVERLIE THE ZONA PELLUCIDA 8 &ROM 7ALLACE AND 3ELMAN REPRODUCED WITH KIND PERMISSION FROM THE 3OCIETY FOR
)NTEGRATIVE AND #OMPARATIVE "IOLOGY
&IGURE %LECTRON MICROGRAPH OF A PORTION OF AN OOGONIUM OF THE VIVIPAROUS TELEOST 8IPHOPHORUS HELLERI 4HE COMPACT
NUCLEOLUS HAS A lBRILLAR CORE & AND A GRANULAR PERIPHERY ' 4HERE ARE MINUTE PERIPHERAL DENSE MASSES ARROWS IN THE OO
PLASM #Y .P NUCLEOPLASM 8 &ROM !ZEVADO AND #OIMBRA "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION
/6!2)!. &/,,)#,%3
&IGURE $RAWINGS OF THE EVOLUTION OF THE NUCLEOLUS .C OF THE VIVIPAROUS TELEOST 8IPHOPHORUS HELLERI DURING OOGENESIS
&OLLOWING THE DIPLOTENE STAGE WHEN MITOTIC ACTIVITY IS SUSPENDED THE NUCLEOLI ENLARGE FROM ABOUT TO M AND BECOME
INCREASINGLY VACUOLATED .% NUCLEAR ENVELOPE &ROM !ZEVADO AND #OIMBRA "IOLOGIE #ELLULAIRE REPRODUCED WITH PER
MISSION
&IGURE %LECTRON MICROGRAPH OF AN OVARIAN FOLLICLE OF "RACHYDANIO RERIO /NE OF THE CELLS OF THE FOLLICULAR EPITHELIUM
& IS DIVIDING BY MITOSIS ARROW INDICATES CHROMATIN IN THIS CORTICAL
ALVEOLUS STAGE -ITOCHONDRIA ARE CLOSELY ASSOCIATED WITH
CISTERNAE OF GRANULAR ENDOPLASMIC RETICULUM IN THE CORTICAL OOPLASM / #! CORTICAL ALVEOLUS 6% ZONA PELLUCIDA 8
&ROM 3ELMAN ET AL REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
#(!04%2
&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH A FOLLICLE OF THE SEAHORSE (IPPOCAMPUS ERECTUS 4HE PRIMARY OOCYTE IS
IN THE PERINUCLEOLUS STAGE 4HE OOPLASM CONTAINS A DISTINCT YOLK NUCLEUS 9. OR JUXTANUCLEAR COMPLEX OF ORGANELLES 3EVERAL
NUCLEOLI LIE WITHIN THE PERIPHERY OF THE GERMINAL VESICLE ' ! DARKLY STAINED BASEMENT MEMBRANE ARROWHEADS SEPARATES
THE FOLLICULAR CELLS & FROM THE THECA , LIPID DROPLETS 8 &ROM 3ELMAN AND 7ALLACE REPRODUCED WITH PERMISSION
FROM THE :OOLOGICAL 3OCIETY OF *APAN
&IGURE %LECTRON MICROGRAPHS OF ANNULATE LAMELLAE IN THE OOPLASM OF A STAGE )) OOCYTE OF "RACHYDANIO RERIO &ROM
3ELMAN ET AL REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 8
" 4HESE ANNULATE LAMELLAE ARE CONTINUOUS WITH THE GRANULAR ENDOPLASMIC RETICULUM ARROWS NUCLEAR PORES ARE SHOWN IN SIDE
VIEW 0 ELECTRON
DENSE PORE COMPLEX 8
/6!2)!. &/,,)#,%3
&IGURE %LECTRON MICROGRAPH OF ANNULATE LAMELLAE IN A MATURING OOCYTE OF THE MEDAKA /RYZIAS LATIPES 4HE ENDS OF
THE ANNULATE LAMELLAE !, ARE CONTINUOUS WITH LAMELLAE OF THE GRANULAR ENDOPLASMIC RETICULUM %2 8 &ROM )WAMAT
SU ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
#(!04%2
&IGURE $RAWINGS OF SECTIONS OF TELEOSTEAN OOCYTES TO SHOW THE DEVELOPMENT OF THE JUXTANUCLEAR COMPLEX OF ORGANELLES
4HE DRAWINGS ARE TAKEN FROM OOCYTES OF #HANNA SP EXCEPT FOR NOS AND WHICH ARE OF (ETEROPNEUSTES SP &ROM 'URAYA
REPRODUCED WITH PERMISSION OF THE AUTHOR
9OUNG OOCYTE SHOWING DENSE BODY IN THE OOPLASM
9OUNG OOCYTE SHOWING BASOPHILIC YOLK
NUCLEUS SUBSTANCE AND DENSE BODY ADJACENT TO THE NUCLEAR MEMBRANE
9OUNG OOCYTE SHOWING YOLK
NUCLEUS SUBSTANCE ADJACENT TO THE NUCLEAR MEMBRANE
9OUNG OOCYTES SHOWING THE GROWTH OF THE YOLK NUCLEUS AND DENSE BODY
/OCYTE SHOWING THE PROLIFERATION OF BASOPHILIC MASSES FROM THE YOLK NUCLEUS
/OCYTE SHOWING HOMOGENEOUS YOLK NUCLEUS AND UNIFORMLY DISTRIBUTED BASOPHILIC SUBSTANCE PROLIFERATED FROM THE YOLK
NUCLEUS
/6!2)!. &/,,)#,%3
&IGURE #ONTINUED
/OCYTE ILLUSTRATING THE VARIOUS COMPONENTS OF THE JUXTANUCLEAR COMPLEX YOLK NUCLEUS SUBSTANCE LIPID INCLUSIONS AND
MITOCHONDRIA
/OCYTE SHOWING THE VARIOUS COMPONENTS OF THE JUXTANUCLEAR COMPLEX
&IGURE 0HOTOMICROGRAPHS OF OOCYTES OF THE COD 'ADUS MORHUA 8 &ROM +JESBU AND +RYVI REPRODUCED WITH
PERMISSION FROM %LSEVIER 3CIENCE
! /OCYTES IN VARIOUS STAGES OF DEVELOPMENT /OGONIA OG ARE SITUATED AT THE LINING OF EACH OVIGEROUS FOLD G INTERLAMELLAR
SPACE NO NUCLEOLUS
" ,ARGER OOCYTES HAVE ACQUIRED A CIRCUMNUCLEAR RING CNR IN THEIR OOPLASM
#(!04%2
&IGURE #AMERA LUCIDA DRAWINGS OF GROWING OOCYTES OF (ETEROPNEUSTES FOSSILIS &ROM .AYYAR REPRODUCED WITH
PERMISSION FROM THE #OMPANY OF "IOLOGISTS ,TD
! %ARLY OOCYTE WITH LIPID GRANULES AND MITOCHONDRIA CONCENTRATED AROUND THE NUCLEUS
" 4HE YOLK NUCLEUS HAS APPEARED BESIDE THE NUCLEUS IN THE FORM OF A MASS OF LIPID BODIES AND MITOCHONDRIA
# $ 4HE YOLK NUCLEUS HAS INCREASED IN SIZE AND FORMED A CONICAL CAP ON ONE SIDE OF THE NUCLEUS
% 4HE YOLK NUCLEUS HAS BECOME OVAL AND STILL LIES BESIDE THE NUCLEUS
&
4HE YOLK NUCLEUS IS MIGRATING TOWARD THE PERIPHERY OF THE OOCYTE
&IGURE 3ECTIONS FROM THE OVARY OF THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSU AND .AKASHIMA REPRODUCED
WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
! " 0HOTOMICROGRAPHS OF SECTIONS THROUGH THE OVARY SHOWING FOLLICLES CONTAINING OOCYTES IN VARIOUS STAGES OF OOGENESIS
4HE VEGETAL POLE AREA VPA IS LOCATED AT THE SIDE OF THE YOLK NUCLEI YN &OLLICULAR CELLS ARE THICK IN THIS AREA AND ATTACHING
lLAMENTS AF ARE PRESENT N AF NON ATTACHING lLAMENTS 4HE NUMERALS INDICATE STAGES OF OOGENESIS 8
/6!2)!. &/,,)#,%3
&IGURE #ONTINUED
# $ %LECTRON MICROGRAPHS OF YOLK NUCLEI OF PREVITELLOGENIC OOCYTES
# 4HE YOLK NUCLEUS OF A STAGE ))) OOCYTE ABOVE IS COMPOSED OF AGGREGATES OF CYTOPLASMIC ORGANELLES lLAMENTS AGRANU
LAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA 8
$ 4HE YOLK NUCLEUS OF A STAGE )6 OOCYTE ABOVE CONTAINS VESICLES 6 OF VARIOUS SIZES 'OLGI COMPLEXES AND GRANULAR
ENDOPLASMIC RETICULUM 8
#(!04%2
&IGURE -ICROGRAPHS OF OOCYTES IN THE CORTICAL ALVEOLUS STAGE FROM THE PIPElSH 3YGNATHUS SCOVELLI &ROM "EGOVAC AND
7ALLACE REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF AN OOCYTE lLLED WITH LARGE CORTICAL ALVEOLI #! 4HE ZONA PELLUCIDA 6% IS PRESENT BETWEEN THE OOCYTE
AND ITS OVERLYING FOLLICULAR CELLS ,IPID , SURROUNDS THE NUCLEUS 3EVERAL NUCLEOLI ARE PRESENT WITHIN THE GERMINAL VESICLE
8
" %LECTRON MICROGRAPH OF THE CORTEX OF AN OOCYTE IN AN EARLY CORTICAL ALVEOLUS STAGE 4HE ZONA PELLUCIDA 6% HAS APPEARED
BETWEEN THE MICROVILLAR PROCESSES AND CORTICAL ALVEOLI #! ARE PRESENT 'OLGI COMPLEXES ' INTERMINGLE WITH MITOCHON
DRIA &# FOLLICULAR CELL 8 4HE INSET SHOWS A CORTICAL ALVEOLUS WITH AN ELECTRON
DENSE INCLUSION ARROW 8
# %LECTRON MICROGRAPH OF AN OOCYTE / IN A LATER CORTICAL ALVEOLUS STAGE 4HE ZONA PELLUCIDA 6% HAS ASSUMED A TRILAMINAR
APPEARANCE &# FOLLICULAR CELL 8
$ %LECTRON MICROGRAPH OF LIPID DROPLETS , WITHIN AN OOCYTE 4HE CENTRE OF EACH DROPLET APPEARS EMPTY AS THE RESULT OF PARTIAL
EXTRACTION OF LIPID DURING PROCESSING 8
/6!2)!. &/,,)#,%3
&IGURE -ICROGRAPHS OF FOLLICLES IN THE CORTICAL ALVEOLUS STAGE FROM THE KILLIlSH &UNDULUS HETEROCLITUS &ROM 3ELMAN
AND 7ALLACE REPRODUCED WITH KIND PERMISSION FROM THE 3OCIETY FOR )NTEGRATIVE AND #OMPARATIVE "IOLOGY
! %LECTRON MICROGRAPH SHOWING MICROVILLI EXTENDING THROUGH PORE CANALS ARROWS IN THE ZONA PELLUCIDA 6% OF AN OOCYTE
/ 4HE OOPLASM CONTAINS NASCENT CORTICAL ALVEOLI #! 8
" 0HOTOMICROGRAPH OF AN OOCYTE WITH CORTICAL ALVEOLI #! AND LIPID DROPLETS ARROWS IN THE OOPLASM GV GERMINAL VESICLE
8
&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH OVIGEROUS FOLDS OF THE KILLIlSH &UNDULUS HETEROCLITUS &ROM 3ELMAN
7ALLACE AND "ARR REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! &OLLICLES ARE AT DIFFERENT STAGES OF DEVELOPMENT A PRIMARY GROWTH STAGE B YOLK VESICLE STAGE AND C VITELLOGENIC
FOLLICLE #ORTICAL ALVEOLI INCREASE IN SIZE AND NUMBER AS THE FOLLICLE DEVELOPS AND MOVE PERIPHERALLY IN THE OOPLASM
"AR MM
" #ORTEX OF AN EGG SHOWING CORTICAL ALVEOLI
IN A LAYER OF CORTICAL OOPLASM THAT SURROUNDS A CENTRAL MASS OF mUID YOLK 9
"AR MM
#(!04%2
&IGURE $IAGRAMS ILLUSTRATING THE FORMATION OF PROTEIN YOLK IN "RACHYDANIO RERIO 0INOCYTOTIC VESICLES VP FORM ON THE
SURFACE OF THE OOCYTE UPPER LEFT 4HESE FUSE TO FORM YOLK BODIES '0 WITH HOMOGENEOUS CONTENTS 4HE CONTENT OF THESE YOLK
BODIES MAY ASSUME A CRYSTALLINE STRUCTURE CR CENTRE /LDER YOLK BODIES CONTINUE TO INCREASE IN SIZE RIGHT BY INCORPORAT
ING AMORPHOUS MATERIAL MA FROM THE GRANULAR ENDOPLASMIC RETICULUM RE BY A FUSION OF MEMBRANES :2 ZONA PELLUCIDA
&ROM 5LRICH *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION
&IGURE %LECTRON MICROGRAPH SHOWING ABUNDANT MICROPINOCYTOTIC ACTIVITY AT THE SURFACE OF AN OOCYTE / FROM AN EARLY
VITELLOGENIC FOLLICLE OF THE SHEEPSHEAD MINNOW #YPRINODON VARIEGATUS #OATED PITS ARROWHEADS COATED VESICLES ARROWS
AND SMOOTH SURFACED TUBULES ARE ABUNDANT 6 ZONA PELLUCIDA 8 &ROM 3ELMAN AND 7ALLACE REPRODUCED WITH
PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
/6!2)!. &/,,)#,%3
&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH FOLLICLES OF THE KILLIlSH &UNDULUS HETEROCLITUS &ROM 3ELMAN AND
7ALLACE REPRODUCED WITH KIND PERMISSION FROM THE 3OCIETY FOR )NTEGRATIVE AND #OMPARATIVE "IOLOGY
! 6ITELLOGENIC FOLLICLE 4HE MOST OBVIOUS EVENT MARKING THE INITIATION OF VITELLOGENESIS IS THE APPEARANCE OF MEMBRANE
BOUND
mUID
lLLED YOLK SPHERES Y LYING BETWEEN CORTICAL ALVEOLI CA IN THE PERIPHERAL OOPLASM / F FOLLICULAR EPITHELIUM
V ZONA PELLUCIDA 8
" &OLLICLE IN EARLY MATURATION 4HE OOCYTE CONTAINS A CENTRAL MASS OF mUID YOLK Y SURROUNDED BY PERIPHERAL YOLK SPHERES
CORTICAL ALVEOLI CA AND A LIPID DROPLET
8
&IGURE 0HOTOMICROGRAPHS THROUGH VITELLOGENIC FOLLICLES OF THE SHEEPSHEAD MINNOW #YPRINODON VARIEGATUS 9OLK
ACCUMULATES WITHIN YOLK SPHERES THAT COALESCE TO FORM A CONTINUOUS MASS OF YOLK ' GERMINAL VESICLE &ROM 3ELMAN AND
7ALLACE REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
! &LUID
lLLED YOLK BODIES ARROWS IN THIS MID
VITELLOGENIC FOLLICLE ARE IN VARIOUS STAGES OF FUSION 8
" 4HE CENTRAL MASS OF mUID YOLK
OCCUPIES MUCH OF THE OOPLASM IN THIS LATE VITELLOGENIC FOLLICLE 8
#(!04%2
/6!2)!. &/,,)#,%3
@
&IGURE -ICROGRAPHS OF SECTIONS THROUGH FOLLICLES OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM 3ELMAN ET AL
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF AN EARLY VITELLOGENIC FOLLICLE SHOWING THE FOLLICULAR WALL AND NUMEROUS SMALL YOLK BODIES ARROWHEADS
AND CORTICAL ALVEOLI CA WITHIN THE OOCYTE 4HE MICROPYLAR CELL M WITHIN THE FOLLICULAR EPITHELIUM PROJECTS THROUGH THE
ZONA PELLUCIDA VE TOWARD THE OOCYTE 4HE DARKLY STAINED MASSES
IN THE CORTICAL OOPLASM REPRESENT AGGREGATIONS OF
MITOCHONDRIA AND ENDOPLASMIC RETICULUM 4HE PORE CANALS APPEAR AS LIGHT STRIATIONS CROSSING THE ZONA PELLUCIDA 8
" 0HOTOMICROGRAPH OF A MIDVITELLOGENIC FOLLICLE 9OLK BODIES Y WITHIN THE OOCYTE ARE OF VARIABLE SIZE AND SOME DISPLAY DARK
STAINING MASSES ARROWHEADS OR hMAIN BODIESv WITHIN THEM %RYTHROCYTES E ARE VISIBLE IN A THECAL CAPILLARY CA CORTICAL
ALVEOLUS VE ZONA PELLUCIDA 8
# %LECTRON MICROGRAPH OF THE OUTER SURFACE OF A VITELLOGENIC OOCYTE DISPLAYING ENDOCYTOTIC ACTIVITY #OATED VESICLES
ARROWHEADS AND SMOOTH
SURFACED ENDOSOMES ARE ABUNDANT E ENDOSOME CONTAINING ELECTRON
DENSE MATERIAL
BUNDLE OF
ACTIN lLAMENTS BENEATH THE OOLEMMA 8
$ %LECTRON MICROGRAPH OF MEMBRANE
LIMITED YOLK BODIES 9 IN AN EARLY VITELLOGENIC OOCYTE 4HESE SMALL YOLK BODIES REVEAL
NO INTERNAL CRYSTALLINE COMPONENT 8
% %LECTRON MICROGRAPH OF CRYSTALLINE YOLK 4HE CRYSTALLINE NATURE OF THE MAIN BODIES - IS NOT APPARENT AT THIS LOW MAGNIlCA
TION 8
& %LECTRON MICROGRAPH OF A YOLK BODY SHOWING A CRYSTALLINE COMPONENT NEXT TO THE MEMBRANE 8
&IGURE 9OLK PROTEIN MAY BE SEQUESTERED IN PLATELETS COMPRISED OF AN ORTHORHOMBIC CRYSTALLINE STRUCTURE &ROM 3ELMAN
AND 7ALLACE REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
! 0HOTOMICROGRAPH OF A SECTION THROUGH A MID
VITELLOGENIC FOLLICLE OF THE ZEBRAlSH "RACHYDANIO RERIO SHOWING NUMEROUS
YOLK PLATELETS OF VARIABLE SIZE ARROWS 8
" %LECTRON MICROGRAPH SHOWING THE CRYSTALLINE CORE OF A YOLK PLATELET FROM A MULLET -UGIL CEPHALUS / OOPLASM 8
#(!04%2
&IGURE 3CANNING TRANSMISSION ELECTRON MICROGRAPH OF AN ULTRATHIN CRYOSECTION OF A YOLK PLATELET FROM 0ELVICACHRO
MIS PULCHER #ICHLIDAE SHOWING THE COMPOSITION OF CRYSTALS #R AND THE NON
CRYSTALLINE MATRIX OR SUPERlCIAL LAYER 3,
"AR M &ROM ,ANGE ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
A
&IGURE -ICROGRAPHS OF OOCYTES OF THE PIPElSH 3YNGNATHUS SCOVELLI DURING VITELLOGENESIS &ROM "EGOVAC AND 7ALLACE
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF EARLY VITELLOGENIC OOCYTE WITH MANY SMALL YOLK SPHERES 9 WITHIN THE OOPLASM #ORTICAL ALVEOLI #!
ARE DISPLACED TO THE PERIPHERY ,IPID , IS PRESENT CENTRALLY NEAR THE GERMINAL VESICLE AND AMONG THE YOLK SPHERES 8
" 0HOTOMICROGRAPH OF AN OOCYTE IN MIDVITELLOGENESIS 4HE YOLK SPHERES 9 HAVE BECOME LARGER 0ERIPHERAL DISPLACEMENT OF
CORTICAL ALVEOLI #! AND LIPID HAS CONTINUED 8
# 0HOTOMICROGRAPH OF AN OOCYTE DURING LATE VITELLOGENESIS -OST OF THE YOLK SPHERES HAVE COALESCED TO FORM A CENTRAL mUID
MASS 9 #ORTICAL ALVEOLI #! AND LIPID DROPLETS
REMAIN IN THE PERIPHERAL PART OF THE YOLK MASS !RROWHEAD ZONA PEL
LUCIDA 8
$ %LECTRON MICROGRAPH OF AN EARLY VITELLOGENIC OOCYTE IN WHICH YOLK SPHERES ARE FORMING 4HE PRIMARY YOLK SPHERES 9
CONTAIN CONDENSED YOLK AND VESICULAR STRUCTURES &ULLY FORMED YOLK SPHERES 9 CONTAIN ELECTRON
DENSE YOLK
SPECIlC
INCLUSIONS ARROW 8
% %LECTRON MICROGRAPH OF AN EARLY VITELLOGENIC OOCYTE WITH TRANSITIONAL YOLK SPHERES 9 THAT ARE CHARACTERIZED BY CONDENS
ING YOLK MATERIAL AND VESICULAR STRUCTURES /NE OF THE YOLK SPHERES CONTAINS THE ELECTRON
DENSE YOLK
SPECIlC MARKER ARROW
IN ADDITION TO VESICULAR ELEMENTS , LIPID 8
& %LECTRON MICROGRAPH OF MIDVITELLOGENIC OOCYTE SHOWING A HETEROGENEOUS COLLECTION OF YOLK
SPECIlC INCLUSIONS ARROW
HEADS WITHIN A LARGE MATURE YOLK SPHERE 9 4HE YOLK SPHERES ARE MEMBRANE BOUND ARROWS 3MALLER YOLK SPHERES ARE
ALSO PRESENT 8
' %LECTRON MICROGRAPH SHOWING ENDOCYTOTIC ACTIVITY AT THE PERIPHERY OF A VITELLOGENIC OOCYTE 4HE ENDOCYTOTIC VESICLES ARE
CLATHRIN COATED ARROWS 6% ZONA PELLUCIDA 8
/6!2)!. &/,,)#,%3
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF LYSOSOME LIKE BODIES
WITHIN OOCYTES OF THE SEAHORSE (IPPOCAMPUS ERECTUS &ROM
3ELMAN 7ALLACE AND 0LAYER REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! ,YSOSOME BODIES LIE NEXT TO CORTICAL ALVEOLI # IN OOCYTES IN THE LATE CORTICAL ALVEOLUS STAGE 8
" 9OLK SPHERES 9 WITHIN A VITELLOGENIC OOCYTE 3OME STILL CONTAIN REMNANTS OF LYSOSOME LIKE BODIES WITHIN THEM 8
&IGURE $IAGRAMS ILLUSTRATING THE ACCUMULATION OF MULTIVESICULAR BODIES DURING PRIMARY GROWTH OF THE OOCYTE OF THE
TROUT 3ALMO TRUTTA FARIO -ULTIVESICULAR BODIES DOTS APPEAR AT THE PERIPHERY OF AN OOCYTE ABOUT M IN DIAMETER
ACCUMULATE TO FORM A CONTINUOUS LAYER SUBSEQUENTLY SPREADING TOWARD THE CENTRE AND LATER TO THE PERIPHERY OF THE OO
CYTE
4HE CIRCLES REPRESENT CORTICAL ALVEOLI . NUCLEUS ,IPID DROPLETS ARE NOT SHOWN &ROM "USSON
-ABILLOT
"IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION
/6!2)!. &/,,)#,%3
&IGURE %LECTRON MICROGRAPHS SHOWING MULTIVESICU
LAR BODIES IN OOCYTES OF THE TROUT 3ALMO TRUTTA FARIO &ROM
"USSON
-ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED
WITH PERMISSION
! -ULTIVESICULAR BODIES FROM AN OOCYTE OF M SHOW
ING LIMITING MEMBRANES INNER VESICLES AND lNELY GRAN
ULAR CLUMPS C WITHIN THE MATRIX 8
" #ONTINUITY ARROWS BETWEEN A MULTIVESICULAR BODY
-6" AND CISTERNAE OF THE AGRANULAR ENDOPLASMIC
RETICULUM
#(!04%2
&IGURE $IAGRAM SUMMARIZING THE SEQUENCE OF VITELLOGENESIS IN THE TROUT 3ALMO TRUTTA FARIO &ROM "USSON -ABILLOT
"IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION %NDOCYTOTIC VESICLES SEQUESTER VITELLOGENIN VTG 4HESE COALESCE
TO FORM LARGER VESICLES WHICH EVENTUALLY FUSE WITH PREEXISTING LYSOSOMES ,93 TO FORM YOLK BODIES 9"
&IGURE %LECTRON MICROGRAPHS OF LYSOSOMES DURING VITELLOGENESIS IN OOCYTES OF THE TROUT 3ALMO TRUTTA FARIO &ROM
"USSON
-ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION
! !T THE ONSET OF VITELLOGENESIS MOST LYSOSOMES OF THIS REGION ARE PACKED WITH A COARSE GRANULAR MATERIAL G 8
" ,ATER MOST LYSOSOMES CONTAIN HOMOGENEOUS YOLK 9 ALTHOUGH SOME GRANULAR LYSOSOMES G AND PLAIN MULTIVESICULAR
BODIES ARROWS MAY BE SEEN 8
/6!2)!. &/,,)#,%3
&IGURE 0HOTOMICROGRAPHS OF INDIVIDUAL FOLLICLES IN VITRO OF THE KILLIlSH &UNDULUS HETEROCLITUS 8 &ROM 7ALLACE
AND 3ELMAN REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
!
MM FOLLICLE CONTAINING AN OOCYTE WITH A GERMINAL VESICLE ARROW NEAR THE UPPER SURFACE
"
MM FOLLICLE CONTAINING AN OOCYTE IN WHICH THE GERMINAL VESICLE HAS MIGRATED TO THE SURFACE ARROW
#
MM FOLLICLE CONTAINING AN OOCYTE IN WHICH THERE IS NO GERMINAL VESICLE 4HE OIL DROPLETS HAVE BEGUN TO COALESCE BUT
ARE STILL PERIPHERALLY ATTACHED
$
MM FOLLICLE CONTAINING AN OOCYTE IN WHICH THE OIL DROPLETS NO LONGER PERIPHERALLY ATTACHED COLLECT AT THE UPPER
SURFACE
@
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE OVA
RY OF THE GILTHEAD SEABREAM DURING THE SPAWNING SEASON
3CALE BARS M &ROM 'OTHILF ET AL REPRODUCED
WITH PERMISSION FROM THE 3OCIETY FOR THE 3TUDY OF 2EPRODUC
TION )NC
! !N OVERVIEW SHOWING SEVERAL STAGES OF OOCYTE DEVELOP
MENT
" &OLLICLE CONTAINING POSTVITELLOGENIC OOCYTE
#(!04%2
&IGURE #ONTINUED
#
& $URING lNAL OOCYTE MATURATION LIPID DROPLETS CO
ALESCE AND THE GERMINAL VESICLE BEGINS ITS MIGRA
TION TO THE PERIPHERY
' %IGHT HOURS BEFORE SPAWNING COALESCENCE OF LIPID
DROPLETS IS COMPLETE AND THE GERMINAL VESICLE HAS
ARRIVED AT THE PERIPHERY OF THE OOCYTE
( &OUR HOURS BEFORE SPAWNING THE OOCYTE IS COM
PLETELY CLEAR AND THE GERMINAL VESICLE HAS DISAP
PEARED '6"$
!BBREVIATIONS C CORTICAL ALVEOLI '6 GERMINAL VES
ICLE L LIPID DROPLETS 0ST6 POSTVITELLOGENIC OOCYTE
06 PREVITELLOGENIC OOCYTE 6TL VITELLOGENIC OOCYTE Y YOLK
Z ZONA PELLUCIDA
/6!2)!. &/,,)#,%3
&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH THE CORTEX OF A MATURE EGG OF THE ZEBRAlSH "RACHYDANIO RERIO 9OLK BOD
IES Y HAVE SMOOTH CONTOURS HOMOGENEOUS INTERIORS AND LIE SUBJACENT TO CORTICAL ALVEOLI CA 8 &ROM 3ELMAN ET AL
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4WO
CELL MODEL FOR THE PRODUCTION OF _ `
DIHYDROXY
PREGNEN
ONE BY SALMONID POSTVITELLOGENIC
FOLLICLES &ROM .AGAHAMA ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
!BBREVIATIONS 0
SCC CHOLESTEROL SIDE
CHAIN CLEAVAGE CYTOCHROME 0
`
(3$ `
HYDROXYSTEROID DEHYDROGENASE
ISOMERASE 0
_ 0 _
HYDROXYLASE `
HYDROXYSTEROID DEHYDROGENASE
#(!04%2
&IGURE 0HOTOMICROGRAPHS SHOWING THE MICROTUBULAR NETWORK IN FULLY GROWN OOCYTES OF THE GOLDlSH #ARASSIUS AURATUS
BY CONFOCAL IMMUNOmUORESCENCE MICROSCOPY USING TUBULIN ANTIBODY 9OLK GRANULES APPEAR AS DARK MASSES SUSPENDED WITHIN
THE MESHES OF THE MICROTUBULAR NETWORK &ROM *IANG ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF
*APAN
! ! CONDENSED BAND OF MICROTUBULES SURROUNDS THE GERMINAL VESICLE '6 "AR M
" "RIGHT BAND OF MICROTUBULES SMALL ARROW SURROUNDING THE GERMINAL VESICLE "AR M
&IGURE 0HOTOMICROGRAPHS SHOWING THE REORGANIZATION OF THE MICROTUBULAR NETWORK DURING MIGRATION OF THE GERMINAL
VESICLE TO THE ANIMAL POLE IN OOCYTES OF THE GOLDlSH #ARASSIUS AURATUS CONFOCAL IMMUNOmUORESCENCE MICROSCOPY USING TUBULIN
ANTIBODY &ROM *IANG ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
! -IGRATING GERMINAL VESICLE WITH A LONG PERINUCLEAR TAIL ARROW "AR M
" 4HE PERINUCLEAR TAIL CONSISTS OF CONDENSED MICROTUBULAR ARRAYS AND SHORT MICROTUBULES IN CLEFTS ARROWS "AR M '6
GERMINAL VESICLE
&IGURE 0HOTOMICROGRAPHS SHOWING THE RELATIONSHIP OF MICROTUBULES AND THE GERMINAL VESICLE AT THE ANIMAL POLE IN OO
CYTES OF THE GOLDlSH #ARASSIUS AURATUS AT THE TIME OF GERMINAL VESICLE BREAKDOWN CONFOCAL IMMUNOmUORESCENCE MICROSCOPY
USING TUBULIN ANTIBODY &ROM *IANG ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
! .UMEROUS MICROTUBULES FORM A BRIGHT BAND AT THE VEGETAL SURFACE OF THE GERMINAL VESICLE "AR M
" -ICROTUBULES PENETRATE THE GERMINAL VESICLE '6 FROM THE BRIGHT BAND AT ITS VEGETAL SURFACE "AR M
/6!2)!. &/,,)#,%3
&IGURE 0HOTOMICROGRAPHS SHOWING THE ORGANIZATION THE MICROTUBULAR NETWORK IN THE ANIMAL POLE REGION OF OOCYTES OF
THE GOLDlSH #ARASSIUS AURATUS FOLLOWING GERMINAL VESICLE BREAKDOWN CONFOCAL IMMUNOmUORESCENCE MICROSCOPY USING TUBULIN
ANTIBODY &ROM *IANG ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
! ! DISC
SHAPED RING OF CONDENSED MICROTUBULES APPEARS IN THE ANIMAL POLE REGION "AR M
" -ICROTUBULAR ASTERS IN THE DISC
SHAPED STRUCTURE ARE SURROUNDED BY A MICROTUBULE
FREE AREA ARROWS "AR M
&IGURE $IAGRAM OF THE FOLLICULAR WALL OF THE POECILIID 8IPHOPHORUS HELLERI DURING THE INITIAL FORMATION OF THE ZONA PEL
LUCIDA :0 4HIS LAYER IS SECRETED BY EXOCYTOSIS AROUND THE BASES OF MICROVILLI MV THAT EXTEND FROM THE SURFACE OF THE OOCYTE
&ROM !ZEVEDO *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION
!BBREVIATIONS %F FOLLICULAR EPITHELIAL CELL FC COLLAGENOUS lBRES -B BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM
/C CORTICAL CYTOPLASM OF THE OOCYTE 4E THECA
#(!04%2
&IGURE $IAGRAM ILLUSTRATING THE ELEMENTS OF THE FOLLICULAR WALL IN SPAWNING !TLANTIC COD 'ADUS MORHUA 4WO SETS OF
MICROVILLI ENTWINE WITHIN THE PORE CANALS 0 THOSE FROM THE OOCYTE / EXTEND OUTWARD AND THOSE FROM THE FOLLICULAR CELL &
EXTEND INWARD 4HREE LAYERS ARE VISIBLE IN THE ZONA PELLUCIDA THE OUTER LAYER : STIPPLED A MIDDLE LAYER : %# AND THE
THICKEST LATER THE ARCHITECTURALLY COMPLEX : -# &ROM +JESBU +RYVI AND .ORBERG REPRODUCED WITH PERMISSION
FROM %LSEVIER 3CIENCE
!BBREVIATIONS ! CORTICAL ALVEOLUS 9 YOLK GRANULE
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE ZONA PELLUCIDA OF SPAWNING !TLANTIC COD 'ADUS MORHUA "AR M
&ROM +JESBU +RYVI AND .ORBERG REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! ! MICROVILLUS FROM A FOLLICULAR CELL EXTENDS INTO A PORE CANAL
" ! MICROVILLUS FROM A FOLLICULAR CELL IS CLOSELY ASSOCIATED WITHIN THE PORE CANAL WITH A MICROVILLUS FROM THE OOCYTE
# 4HIS OBLIQUE SECTION OF THE ZONA PELLUCIDA ILLUSTRATES THE RELATIONSHIP BETWEEN THE TWO MICROVILLI WITHIN PORE CANALS
/6!2)!. &/,,)#,%3
&IGURE %LECTRON MICROGRAPH OF A SECTION THROUGH THE PERIPHERY OF A FOLLICLE OF THE MARINE TELEOST 0AGRUS MAJOR /NLY
THE PERIPHERAL OOPLASM / OF A VITELLOGENIC OOCYTE IS SHOWN 4HE INTERNAL PART OF THE ZONA PELLUCIDA :) CONSISTS OF SEVEN
LAMELLAE ! SPECIAL THECAL CELL 34# IS PRESENT IN THE THECAL LAYER "AR &ROM -ATSUYAMA .AGAHAMA AND -ATSUURA
REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
!BBREVIATIONS "- BASAL LAMINA '# FOLLICULAR CELL 0# PORE CANAL :% ZONA PELLUCIDA EXTERNA
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF THE ZONA PELLUCIDA C OF SPAWNING !TLANTIC COD 'ADUS MORHUA -ICROVILLI
M EXTENDING THROUGH A PORE CANAL FROM A FOLLICULAR CELL HAVE mATTENED THEMSELVES ON THE SURFACE OF THE OOCYTE "AR M
&ROM +JESBU +RYVI AND .ORBERG REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 3CHEME ILLUSTRATING THE DEVELOPMENT OF THE ZONA PELLUCIDA IN THE POECILIID 8IPHOPHORUS HELLERI DURING OOGEN
ESIS 4HE STAGES ARE BASED PRIMARILY ON THE DIAMETER OF THE OOCYTE )N STAGES AND THE OOCYTE IS CLOSELY SURROUNDED BY THE
FOLLICULAR EPITHELIUM AND THE THECA NOT SHOWN !T STAGE MICROVILLI EXTEND FROM THE OOCYTE TOWARD THE FOLLICULAR EPITHELIUM
"Y STAGE THE BEGINNINGS OF THE ZONA PELLUCIDA ARE SEEN WHERE AN EXTRACELLULAR COAT APPEARS IN THE SPACE SEPARATING THE OOCYTE
AND FOLLICULAR CELLS )N STAGES AND THIS COAT WHICH IS PERFORATED BY MICROVILLI EXTENDING BOTH FROM THE OOCYTE AND FROM
THE FOLLICULAR CELLS THICKENS AS OOGENESIS PROCEEDS -ICROVILLI FROM THE OOCYTE ACTUALLY INVAGINATE THE FOLLICULAR CELLS 4HE FOL
LICULAR CELLS BECOME THICKER AND DEVELOP A MORE ACTIVE APPEARANCE )N STAGE OF THIS VIVIPAROUS TELEOST THE MICROVILLI REGRESS
AND THEIR CONTACT WITH THE FOLLICULAR CELLS BECOMES MORE TENUOUS THE ZONA PELLUCIDA BECOMES THINNER AND ALMOST DISAPPEARS
&ROM !ZEVEDO *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS SHOWING THE DEVELOPMENT OF THE ZONA PELLUCIDA IN THE PIPElSH 3YNGNATHUS
SCOVELLI &ROM "EGOVAC AND 7ALLACE REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !N EARLY CORTICAL ALVEOLI
STAGE OOCYTE / SHOWING THE INITIAL FORMATION OF :ONE : ARROWS OF THE ZONA PELLUCIDA &#
FOLLICULAR CELL 8
" 4HE ZONA PELLUCIDA IN AN OOCYTE / AT A LATER CORTICAL ALVEOLI
STAGE 4HE :ONES AND : : HAVE FORMED BENEATH
:ONE &# FOLLICULAR CELL 8
# :ONE IS COMPACTED AND PROMINENT IN A MID
VITELLOGENIC OOCYTE / WHILE THE :ONE APPEARS TO HAVE DISAPPEARED :ONE
ARROWS REMAINS BUT IS MUCH THINNER THAN IN PREVIOUS STAGES (ORIZONTAL LAMELLAE ARROWS ARE PROMINENT WITHIN :ONE
-ICROVILLI FROM THE OOCYTE AND A FOLLICULAR CELL ARE PRESENT WITHIN THE PORE CANALS OF THE ZONA PELLUCIDA 8
$ 4HE OUTER :ONE ARROWHEADS IS RETAINED IN THE ZONA PELLUCIDA OF A MATURE EGG :ONE IS FULLY COMPACTED THE HORIZONTAL
LAMELLAE ARE PROMINENT /NLY REMNANTS OF THE PORE CANALS ARROWS REMAIN 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A FOLLICULAR CELL AND AN OOCYTE IN EARLY VITELLOGENESIS OF A 3OUTH !MERI
CAN ANNUAL lSH #YNOLEBIAS SP -ICROVILLI EXTEND FROM THE PERIPHERY OF THE OOCYTE AND PASS THROUGH THE ZONA PELLUCIDA WITHIN
PORE CANALS 4HE PERIPHERY OF THE OOCYTE CONTAINS MANY DENSE VESICLES AND REGIONS OF CONTINUITY BETWEEN THE VESICLES AND THE
OOLEMMA 4HE DENSITY OF MATERIAL WITHIN THE VESICLES IS SIMILAR TO THAT OF :ONE : OF THE PRIMARY ENVELOPE :ONES AND
: : LIE BETWEEN THE OOCYTE AND FOLLICULAR CELL 4HE FOLLICULAR CELL EXTENDS MICROVILLI TOWARD THE OOCYTE IT CONTAINS A mAT
TENED NUCLEUS FREE RIBOSOMES AND MITOCHONDRIA 4HE BASEMENT LAMINA OF THE FOLLICULAR EPITHELIUM COLLAGENOUS lBRES AND THE
THECA INTERNA SUBTEND THE FOLLICULAR CELL 8 &ROM 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF THE PERIPHERY AND INTERIOR OF AN OOCYTE OF THE hANNUAL lSHv #YNOLEBIAS
MELATOTAENIA BEFORE THE APPEARANCE OF :ONE OF THE ZONA PELLUCIDA 4HE PERIPHERAL OOPLASM DISPLAYS ENHANCED APPARATUS FOR
PROTEIN SYNTHESIS AND SECRETION FREE RIBOSOMES GRANULAR ENDOPLASMIC RETICULUM AND WELL DEVELOPED 'OLGI COMPLEXES :ONES
AND OF THE ZONA PELLUCIDA ARE AT THE UPPER RIGHT -ICROVILLI VESICLES WITH DENSE CONTENTS AND SITES OF CONTINUITY BETWEEN THE
VESICLES AND OOLEMMA ARE SEEN 4HERE IS DENSE MATERIAL IN THE VESICLES OF THE LARGE 'OLGI COMPLEX ' AT THE LOWER LEFT #ISTERNAE
OF THE WELL
DEVELOPED GRANULAR ENDOPLASMIC RETICULUM CONTAIN lBRILLAR MATERIAL OF LOW ELECTRON DENSITY -ANY MITOCHONDRIA ARE
PRESENT 8 &ROM 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
/6!2)!. &/,,)#,%3
&IGURE 3CHEMATIC DRAWING SUMMARIZING THE PROPOSED STEPS IN THE FORMATION OF THE ZONA PELLUCIDA IN MEDAKA /RYZIAS
LATIPES 0RECURSOR IS SYNTHESIZED IN THE OOPLASM / AND APPEARS TO BE CONCENTRATED IN THE 'OLGI COMPLEXES ' )T IS RELEASED
INTO SMOOTH
SURFACED DENSE
CORED VESICLES $#6 WHICH MIGRATE TO THE OOLEMMA AND DISCHARGE THEIR CONTENTS BY EXOCYTO
SIS INTO THE SPACE BETWEEN THE OOCYTE AND THE FOLLICULAR CELL &# 4HIS MATERIAL COALESCES TO FORM THE ZONA PELLUCIDA #(
&ROM 4ESORIERO REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
!BBREVIATIONS %2 ENDOPLASMIC RETICULUM - MITOCHONDRION
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS ILLUSTRATING THE PRIMARY ENVELOPES OF OOCYTES OF TWO SPECIES OF hANNUAL lSHv
FOLLOWING THE APPEARANCE OF :ONE OF THE ZONA PELLUCIDA &ROM 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER
3CIENCE
! 3LIGHTLY TANGENTIAL SECTION OF AN OOCYTE OF #YNOLEBIAS MELANOTAENIA ! LARGE CUBOIDAL FOLLICULAR CELL DOMINATES THIS lGURE
IT CONTAINS MANY FREE RIBOSOMES AND MITOCHONDRIA BUT LITTLE GRANULAR ENDOPLASMIC RETICULUM 4HREE ZONES OF THE ZONA PEL
LUCIDA ARE PRESENT :ONE : A LOW DENSITY lBRILLAR REGION :ONE : A DENSE REGION AND :ONE : THE MAJOR
COMPONENT CONSISTING OF INTERWOVEN lBRILS 8
" 0RIMARY ENVELOPE OF A STAGE OOCYTE OF !USTROFUNDULUS TRANSILIS :ONE IS UPPERMOST AND APPEARS TO BE CONTINUOUS WITH
THE MATERIAL WITHIN THE FENESTRATIONS :ONE IS ELECTRON DENSE :ONE THE THICKEST LAYER IS ADJACENT TO THE OOCYTE AND CON
SISTS OF lNE lBRILS 0ROGRESSING OUTWARD THE lBRILS ARE COMPRESSED INTO MORE MASSIVE UNITS -ICROVILLI OF THE OOCYTE AND
FOLLICULAR CELLS ARE CONTAINED WITHIN THE PORE CANALS 8
/6!2)!. &/,,)#,%3
&IGURE $IAGRAM THROUGH THE FOLLICULAR WALL OF THE SEA BASS $ICENTRARCHUS LABRAX 4HE ARCHING ARRANGEMENT OF lBRILS
IN THE MAJOR ZONE OF THE ZONA PELLUCIDA # MAY PROVIDE mEXIBILITY ! PORTION OF A FOLLICULAR CELL #F IS SHOWN AT THE TOP THE
PERIPHERY OF AN OOCYTE /V APPEARS AT THE BOTTOM 4HE ZONA PELLUCIDA IS SHOWN IN FOUR LAYERS # # # # ! DESMOSOME
IS SHOWN CONNECTING MICROVILLI WITHIN A PORE CANAL &ROM #APORICCIO AND #ONNES REPRODUCED WITH PERMISSION -AS
SON %DITEUR
!BBREVIATIONS # SUBEPITHELIAL SPACE #AN PORE CANAL -V#F MICROVILLUS OF FOLLICULAR CELL -V/V MICROVILLUS OF OOCYTE
. NUCLEUS OF FOLLICULAR CELL
#(!04%2
&IGURE )MMUNOGOLD STAINING WAS USED TO DEMONSTRATE THAT PRINCIPAL PROTEINS OF THE ZONA PELLUCIDA ORIGINATE WITHIN THE
FOLLICLE ! MONOCLONAL ANTIBODY RAISED AGAINST PROTEINS OF THE ZONA PELLUCIDA RECOGNIZED NO OTHER COMPONENT OF THE OOCYTE
PLASMA OR LIVER )N THIS TRANSMISSION ELECTRON MICROGRAPH OF THE ZONA PELLUCIDA OF THE PIPElSH 3YNGNATHUS SCOVELLI THE LABEL
LING IS RESTRICTED TO THE :ONE : LAYER WHILE THE OUTER :ONE : AND :ONE : LAYERS ARROWS LACK IMMUNOREACTIVITY
4HE OOCYTE / FOLLICULAR CELLS &# AND MICROVILLI ARROWHEADS WITHIN THE PORE CANALS ALSO LACK IMMUNOREACTIVITY 8
&ROM "EGOVAC AND 7ALLACE REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4HERE IS NO DEGENERATION OF THE OUTERMOST LAYER OF THE ZONA PELLUCIDA IN THE PORGY 0AGRAS MAJOR PRIOR TO MATURA
TION AND THE SURFACE PITS PT OF THE PORE CANALS REMAIN OPEN 4HIS IS A SCANNING ELECTRON MICROGRAPH OF THE ANIMAL POLE REGION OF
AN OVUM WITH THE MICROPYLE MP AT THE CENTRE 8 &ROM (OSOKAWA REPRODUCED WITH PERMISSION FROM THE :OOLOGI
CAL 3OCIETY OF *APAN
/6!2)!. &/,,)#,%3
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE FRACTURED ZONA PELLUCIDA OF THE WHITE STURGEON !CIPENSER TRANSMONTANUS
4HE OUTER LAYERS ARE ANCHORED TO THE SECOND LAYER BY SCREWLIKE PROJECTIONS &ROM #HERR AND #LARK REPRODUCED WITH
PERMISSION FROM "LACKWELL 0UBLISHING
! 3CREWLIKE PROJECTIONS ARROWS CONNECT THE SECOND AND THIRD , LAYERS 8
" 3CREWLIKE PROJECTIONS ARROWS IN THE PITS OF THE THIRD LAYER 4HE PITS CONFORM TO THE SHAPE OF THE SCREWS 8
@
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS
OF THE PERIPHERAL REGION OF OVARIAN FOLLICLES OF A VI
VIPAROUS ELASMOBRANCH THE YELLOW SPOTTED STING
RAY 5ROLOPHUS JAMAICENSIS 0ORES IN THE DELICATE
ZONA PELLUCIDA
CONTAIN PROCESSES ARROWHEADS
FROM THE FOLLICULAR CELLS F 4IPS OF THE PROCESSES
INVAGINATE THE OOCYTE AS TRANSOSOMES AND BECOME
INCORPORATED IN THE CYTOPLASM 4HERE ARE NO PRO
CESSES EXTENDING FROM THE OOCYTE &ROM (AMLETT
*EZIOR AND 3PIELER REPRODUCED WITH PERMIS
SION OF 5RBAN &ISCHER 6ERLAG
! &ORMING PROCESSES FROM FOLLICULAR CELLS F
EXTEND THROUGH THE ZONA PELLUCIDA
INVAGI
NATE THE OOLEMMA AND BECOME PINCHED OFF
WITHIN THE OOPLASM AS DISCRETE VESICLES THE
TRANSOSOMES ARROWHEADS 8
" $ElNITIVE TRANSOSOMES ARROWHEADS FROM
FOLLICULAR CELLS F CROSS THE ZONA PELLUCIDA
TO IMPINGE ON AN OOCYTE O 8
#(!04%2
&IGURE 3CHEMATIC DIAGRAMS ILLUSTRATING THE INVOLVEMENT OF FOLLICULAR CELLS IN THE FORMATION OF A SECONDARY ENVELOPE
AROUND THE ZONA PELLUCIDA OF THE OOCYTE OF THE BROOK TROUT 3ALVELINUS FONTINALIS 0ROCESSES FROM THE OOCYTE EXTEND THROUGH PORE
CANALS IN THE ZONA PELLUCIDA TO INDENT THE SURFACE OF THE FOLLICULAR CELLS -EANWHILE PROCESSES FROM THE FOLLICULAR CELLS PASS
THROUGH THE PORE CANALS IN THE OPPOSITE DIRECTION 4HE FOLLICULAR CELLS ARE PUSHED FARTHER AND FARTHER AWAY FROM THE ZONA PELLU
CIDA AS THEY SECRETE THE JELLY
LIKE MATERIAL OF THE SECONDARY ENVELOPE -ICROVILLI FROM FOLLICULAR CELLS AND OOCYTE WITHDRAW FROM
THE ZONA PELLUCIDA NEAR THE TIME OF OVULATION &ROM &LGEL B REPRODUCED WITH PERMISSION OF THE AUTHOR
!BBREVIATIONS "- BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM &% FOLLICULAR EPITHELIUM /0 OOPLASM 4& THECA :% AND
:) OUTER AND INNER REGIONS OF THE ZONA PELLUCIDA
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION MICROGRAPHS OF POSTVITELLOGENIC FOLLICLES OF THE !FRICAN CATlSH #LARIAS GARIEPINUS &ROM VAN DEN
(URK AND 0EUTE REPRODUCED WITH PERMISSION OF THE AUTHORS
! ,IGHT MICROGRAPH SHOWING TWO TYPES OF FOLLICULAR CELLS THE COLUMNAR CELLS '! THAT FORM THE ATTACHMENT DISC AND CUBOIDAL
CELLS '* THAT FORM THE JELLY COAT 8
" %LECTRON MICROGRAPH OF A COLUMNAR FOLLICULAR CELL CONTAINING ELECTRON
DENSE GRANULES '2 THESE CELLS FORM THE ATTACHMENT
DISC 8
# %LECTRON MICROGRAPH OF A CUBOIDAL FOLLICULAR CELL CONTAINING ELECTRON
LUCENT GRANULES '2 4HESE CELLS FORM THE JELLY COAT
8
!BBREVIATIONS "6 BLOOD VESSEL .5 NUCLEUS 4( THECA 9' YOLK GRANULE :2 ZONA PELLUCIDA
#(!04%2
&IGURE ,IGHT MICROGRAPHS OF WHOLE FERTILIZED EGGS OF THE ANNUAL lSH #YNOLEBIUS MELANOTAENIA SHOWING THE ELABORATE
ORNAMENTATION OF THE CHORION &ROM 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 4HE SURFACE OF THE EGG IS COVERED WITH SPIKE
LIKE PROJECTIONS .OTE THE LARGE LIPID DROPLET WITHIN THE YOLK MASS 8 CA
" 0ROlLE VIEW OF THE CHORION SHOWING THREE SPIKES EXTENDING ABOVE THE ELABORATE SCULPTING OF THE SURFACE 4HE MATERIAL OF
THE SECONDARY ENVELOPE IS NEARLY TRANSPARENT 8 CA
&IGURE -ICROGRAPHS OF SECTIONS OF THE SIMPLE COLUMNAR FOLLICULAR EPITHELIUM AND OOCYTE OF THE ANNUAL lSH #YNOLEBIUS
MELANOTAENIA WHEN DEPOSITION OF THE PRIMARY ENVELOPE IS COMPLETE &ROM 7OURMS REPRODUCED WITH PERMISSION FROM
%LSEVIER 3CIENCE
! 0HOTOMICROGRAPH SHOWING THE FOLLICULAR EPITHELIUM RESTING UPON THE PRIMARY ENVELOPE THE LIGHT STRIATIONS WITHIN REPRESENT
PORE CANALS 4HE FOLLICULAR CELLS ARE PACKED WITH DARK GRANULES 8
/6!2)!. &/,,)#,%3
&IGURE #ONTINUED
" 4RANSMISSION ELECTRON MICROGRAPH OF A TANGENTIAL SECTION THROUGH THE FOLLICULAR EPITHELIUM 4HE EPITHELIAL CELLS CONTAIN
EXTENSIVE GRANULAR ENDOPLASMIC RETICULUM AND A NUMBER OF LARGE AND SMALL VESICLES lLLED WITH DENSE MATERIAL 3ECTIONS OF
FENESTRATIONS IN THE PRIMARY ENVELOPE CONTAIN MICROVILLI FROM THE OOCYTE AND FOLLICULAR CELLS %XTENSIVE INTERCELLULAR SPACES
HAVE DEVELOPED BETWEEN THE FOLLICULAR CELLS 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH
THROUGH A LARGE MEMBRANE BOUND PRESECRETION GRANULE
WITHIN A FOLLICULAR CELL OF THE ANNUAL lSH #YNOLEBIUS MELANO
TAENIA AT THE OUTSET OF FORMATION OF THE SECONDARY ENVELOPE
4HE CONTENTS OF THE VESICLE HAVE FUSED TO FORM A HOMO
GENEOUS MASS CONTAINING TUBULAR COMPONENTS IN BOTH
TRANSVERSE AND LONGITUDINAL ORIENTATION 8 &ROM
7OURMS AND 3HELDON REPRODUCED WITH PERMISSION
FROM %LSEVIER 3CIENCE
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A TANGENTIAL
SECTION OF THE SIMPLE COLUMNAR FOLLICULAR EPITHELIUM OF THE ANNUAL
lSH #YNOLEBIUS MELANOTAENIA AT THE OUTSET OF FORMATION OF THE
SECONDARY ENVELOPE ,ARGE COMPARTMENTS lLLED WITH lBRIL
LAR MATRIX HAVE DEVELOPED BETWEEN THE FOLLICULAR CELLS 8
&ROM 7OURMS AND 3HELDON REPRODUCED WITH PERMISSION
FROM %LSEVIER 3CIENCE
A
&IGURE 3CHEMATIC DIAGRAM ILLUSTRATING THE SYNTHESIS AND SECRETION OF THE TUBULAR COMPONENTS OF THE SECONDARY ENVELOPE
BY A FOLLICULAR CELL IN THE ANNUAL lSH #YNOLEBIUS MELANOTAENIA !T THE OUTSET OF FORMATION mOCCULENT MATERIAL APPEARS WITHIN
CISTERNAE OF THE GRANULAR ENDOPLASMIC RETICULUM PORTIONS OF WHICH BECOME DILATED AND SEEM TO BUD OFF TO FORM VESICLES 4HESE
VESICLES GROW BY CONTINUED SYNTHESIS AND BY FUSION WITH OTHER VESICLES THEIR MEMBRANES ARE STUDDED WITH RIBOSOMES ,ARGER
VESICLES CONTAIN PARTLY ASSEMBLED TUBULES 4HE VESICLES CONTINUE TO FUSE FORMING COMPACT PRESECRETION GRANULES CONTAINING
NM TUBULAR COMPONENTS 4HESE VESICLES TRANSPORT THE TUBULAR COMPONENTS DIRECTLY FROM THE SITE OF SYNTHESIS IN THE GRANULAR
/6!2)!. &/,,)#,%3
ENDOPLASMIC RETICULUM TO THE EXTERIOR OF THE CELL THEY APPEAR TO SHED THEIR RIBOSOMES SHORTLY BEFORE FUSING WITH THE PLASMA
MEMBRANE 4HE VESICLES DISCHARGE THEIR CONTENTS IN THE FORM OF A DISCRETE GRANULES 3EVERAL GRANULES MAY FUSE OUTSIDE THE CELL
&OLLICULAR CELLS APPEAR TO PLAY AN ACTIVE ROLE IN THE SELECTIVE DEPOSITION OF TUBULAR MATERIAL IN THE SECONDARY ENVELOPE AND IN
THE GENERATION OF ITS ELABORATE PATTERN !LTHOUGH A 'OLGI COMPLEX IS PRESENT IT DOES NOT APPEAR TO PARTICIPATE IN THE SECRETION OF
THE TUBULAR COMPONENTS &ROM 7OURMS AND 3HELDON REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EGG ENVELOPES OF THE CYPRINODONT !PHYOSEMION
SPLENDOPLEURE &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! 4HE INNER ZONE : OF THE PRIMARY ENVELOPE IS LAMELLAR 3WELLINGS OF VARIOUS SIZES ADORN THE SECONDARY ENVELOPE 3% SOME
ARE M IN HEIGHT OTHERS ARE M 8
" 4HE SECONDARY ENVELOPE COMPRISES TWO LAYERS 4HE INNER LAYER ), IS MADE UP OF MEMBRANOUS ELEMENTS LYING DIRECTLY ON
THE LAMELLAR ZONE : THE SUPERlCIAL LAYER 3, CONSISTS OF PARALLEL STRUCTURES SEPARATED BY A LUCENT MATRIX 8
# 4ANGENTIAL SECTION OF THE SUPERlCIAL LAYER OF THE SECONDARY ENVELOPE )T CONSISTS OF PARALLEL TUBULAR ELEMENTS CUT TRANS
VERSELY -OST OF THE TUBULES ARE ABOUT NM IN DIAMETER A FEW ARE LARGER ARROW 3OME OF THE TUBULES ARE JOINED BY LINKS
8
$ 3ECTION OF THE SECONDARY ENVELOPE 4HE PARALLEL TUBULAR ELEMENTS ARE OPENED AT THE BASE ARROW ), INNER LAYER 3, SUPER
lCIAL LAYER 8
/6!2)!. &/,,)#,%3
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SUPERlCIAL LAYER OF THE SECONDARY EGG ENVELOPE OF THE CYPRINODONT
!PHYOSEMION SPLENDOPLEURE &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! 3MALL SWELLINGS 33 ARE SCATTERED AMONG LARGE SWELLINGS M HIGH ,3 & lLAMENT 8
" 3WELLINGS OF THE SUPERlCIAL LAYER 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE OVARIAN FOLLICLES OF THE CYPRINODONT !PHYOSEMION
SPLENDOPLEURE DURING VITELLOGENESIS &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DI
TRICE
! /BLIQUE SECTION SHOWING THE PRIMARY ENVELOPE 0% FOLLICULAR EPITHELIUM &% AND THECA 4 4HERE IS A DIFFERENCE IN THE
ELECTRON DENSITY OF THE CYTOPLASM OF THE FOLLICULAR CELLS 4HE INTERCELLULAR SPACES CONTAIN SECTIONS OF lLAMENTS & 8
" #ISTERNAE OF THE ENDOPLASMIC RETICULUM %2 AND MITOCHONDRIA - ARE VISIBLE IN FOLLICULAR CELLS WITH ELECTRON
LUCENT CYTO
PLASM THEY ARE DIFlCULT TO IDENTIFY IN ELECTRON
DENSE CELLS $# & SECTIONS OF lLAMENTS 0% PRIMARY ENVELOPE 8
# !T THE END OF VITELLOGENESIS CISTERNAE OF THE ENDOPLASMIC RETICULUM GATHER IN THE BASAL REGION OF THE FOLLICULAR CELLS AND
PINCH OFF VESICLES 6 !RROW BASAL LAMINA . NUCLEUS 8
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE OVARIAN FOLLICLES OF THE CYPRINODONT !PHYOSEMION
SPLENDOPLEURE AT THE END OF VITELLOGENESIS &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE
%DITRICE
! !T THE END OF VITELLOGENESIS THE 'OLGI COMPLEX ARROWHEADS BECOMES ACTIVE IN THE CYTOPLASM BETWEEN THE NUCLEUS AND
THE SURFACE OF THE OOCYTE 4HE ENDOPLASMIC RETICULUM HAS FORMED VESICLES 6 IN THE OPPOSITE REGION 8
" 6ESICLES AND SECRETORY GRANULES APPEAR AT THE TRANS FACE OF THE 'OLGI COMPLEX & lLAMENTS 8
# ,ARGE INTERCELLULAR SPACES , FORM BETWEEN FOLLICULAR CELLS 4IGHT JUNCTIONS ARROWHEADS LINK THE FOLLICULAR CELLS AROUND
THE SPACES 8
$ 'RANULES ARE RELEASED ARROWHEADS FROM THE FOLLICULAR CELLS INTO THE INTERCELLULAR SPACES 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE OVARIAN FOLLICLE OF THE CYPRINODONT !PHYOSEMION
SPLENDOPLEURE AT THE END OF VITELLOGENESIS ! DENSE GRANULE ARROW IS LIBERATED ONTO THE SURFACE OF THE PRIMARY ENVELOPE 0%
8 &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
&IGURE 3ECTION THROUGH THE OVARIAN FOLLICLE OF THE CICHLID #ICHLASOMA FASCIATA SHOWING THE ADHESIVE APPARATUS
4HE ADHESIVE LAYER !A COVERS THE ZONA PELLUCIDA :0 OF THE OOCYTE /6 4HE AMORPHOUS MUCOUS JELLY COAT G IS PENETRATED
BY DENSE lLAMENTS F ATTACHED TO THE ZONA PELLUCIDA &ROM "USSON
-ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH
PERMISSION
! 3CHEMATIC DRAWING
" 4RANSMISSION ELECTRON MICROGRAPH 8
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE OVARIAN FOLLICLE OF THE CICHLID #ICHLASOMA FASCIATA
SHOWING THE ADHESIVE lLAMENTS 8 &ROM "USSON
-ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION
! ,ONGITUDINAL SECTION SHOWING THE PARALLEL ELEMENTS DOUBLE ARROW THAT CONSTITUTE A lLAMENT G GLYCOPROTEIN
" #ROSS SECTION OF A lLAMENT COMPOSED OF MICROTUBULE MIMICS ARROWS PACKED IN HEXAGONAL ARRAYS
@
&IGURE 3CHEMATIC DRAWINGS OF SECTIONS THROUGH THE
FOLLICULAR EPITHELIUM OF THE OVARIAN FOLLICLE OF THE CICHLID
#ICHLASOMA FASCIATA TO SHOW THE DEVELOPMENT OF THE ADHE
SIVE APPARATUS DURING VARIOUS STAGES IN OOGENESIS &ROM
"USSON
-ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED
WITH PERMISSION
! $URING PREVITELLOGENESIS THE OOCYTE IS IN DIRECT CONTACT
WITH THE FOLLICULAR EPITHELIUM WHICH RESTS ON ITS BASE
MENT MEMBRANE
" 4HE ZONA PELLUCIDA SURROUNDS THE OOCYTE AT THE ONSET
OF VITELLOGENESIS !DHESIVE lLAMENTS ATTACHED TO THE
ZONA PELLUCIDA APPEAR BETWEEN THE FOLLICULAR CELLS
# !T THE END OF VITELLOGENESIS THE FOLLICULAR CELLS ARE
DISTENDED WITH GLYCOPROTEINS
$A !T OVULATION THE GLYCOPROTEINS SURROUND THE OOCYTE
FORMING THE ADHESIVE LAYER
$B 4HE FOLLICULAR EPITHELIUM AND ITS BASEMENT MEMBRANE
RETRACT FOLLOWING EXPULSION OF THE OOCYTE FORMING THE
POSTOVULATORY FOLLICLE
!BBREVIATIONS C FOLLICULAR CELLS E FOLLICULAR EPITHELIUM F
ADHESIVE lLAMENTS G GLYCOPROTEINS L BASEMENT MEMBRANE
OF FOLLICULAR EPITHELIUM OV OOCYTE ZP ZONA PELLUCIDA
#(!04%2
&IGURE 3CHEMATIC DRAWINGS OF SECTIONS THROUGH THE FOLLICULAR EPITHELIUM OF THE OVARIAN FOLLICLE OF THE CICHLID #ICHLA
SOMA FASCIATA TO SHOW CHANGES IN THE FOLLICULAR EPITHELIUM DURING VARIOUS STAGES IN OOGENESIS &ROM "USSON
-ABILLOT
"IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION
! 4HE FOLLICULAR CELLS ARE SQUAMOUS DURING PREVITELLOGENESIS ORGANELLES ARE SPARSE
" &OLLICULAR CELLS ENLARGE AT THE BEGINNING OF VITELLOGENESIS AND SHOW SIGNS OF SECRETORY ACTIVITY !DHESIVE lLAMENTS APPEAR
# !T THE END OF VITELLOGENESIS THE FOLLICULAR CELLS BECOME DISTENDED WITH GLYCOPROTEINS WITHIN THE GRANULAR ENDOPLASMIC
RETICULUM
$ $URING OVULATION THE APICAL PLASMA MEMBRANE OF THE FOLLICULAR CELLS RUPTURES TO RELEASE GLYCOPROTEINS WHICH WILL CONSTITUTE
THE ADHESIVE LAYER
% )N THE RETRACTED POSTOVULATORY FOLLICLE THE FOLLICULAR CELLS EMPTIED OF THEIR GLYCOPROTEINS BECOME DISORGANIZED
!BBREVIATIONS C FOLLICULAR CELLS E FOLLICULAR EPITHELIUM F ADHESIVE lLAMENTS G GLYCOPROTEINS L BASEMENT MEMBRANE OF
FOLLICULAR EPITHELIUM OV OOCYTE ZP ZONA PELLUCIDA
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE PERIPHERY OF OVARIAN FOLLICLES OF THE CICHLID #ICHLA
SOMA FASCIATA &ROM "USSON
-ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION
! " $ISTRIBUTION OF lLAMENTS IN THE FOLLICLE AT THE BEGINNING OF VITELLOGENESIS &ILAMENTS ARROW ATTACHED TO THE ZONA
PELLUCIDA ZP PENETRATE DEEP INTO THE INTERCELLULAR SPACES OF THE FOLLICULAR EPITHELIUM EF " BASAL LAMINA OF THE FOL
LICULAR EPITHELIUM OV OOCYTE TH THECA ! 8 " 8
#
3TRUCTURE OF THE lLAMENTS F AT THE END OF VITELLOGENESIS !T THIS STAGE THE lLAMENTS BECOME FRAYED TEMPORARILY THEREBY
DISPLAYING THEIR MICROTUBULAR NATURE ARROWS EF FOLLICULAR EPITHELIUM 8
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF OVULATED EGGS OF THE SOLE 0LEURONICHTHYS COENOSUS SHOWING THE ELABORATE
ARRANGEMENT OF HEXAGONAL SURFACE COMPARTMENTS FORMED OVER THE ZONA PELLUCIDA BY THE SECONDARY ENVELOPE &ROM 3TEHR AND
(AWKES REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !N ENTIRE EGG 8
" )NSIDE EACH HEXAGONAL CHAMBER ARE REGULARLY SPACED PORE CANALS EACH OF WHICH IS SURROUNDED BY A POLYGONAL SUBPATTERN
ARROW 8
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE PERIPHERY OF OVARIAN FOLLICLES OF THE SOLE 0LEURONICHTHYS COENOSUS TO
DEMONSTRATE STAGES IN THE FORMATION OF THE COMPARTMENTALIZED SECONDARY ENVELOPE &ROM 3TEHR AND (AWKES REPRO
DUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !N OOCYTE IN THE LATE PRIMARY GROWTH STAGE (EXAGONAL PARTITIONS H ARE BEGINNING TO FORM IN THE SECONDARY ENVELOPE
&LOCCULENT MATERIAL lLLS THE SUBFOLLICULAR SPACE S -ICROVILLI M FROM THE OOCYTE EXTEND ACROSS THIS SPACE TO REACH BULBOUS
EXTENSIONS OF THE FOLLICULAR CELLS 3EVERAL ELECTRON
LUCENT VESICLES CONTAINING mOCCULENT MATERIAL ARE PRESENT IN A FOLLICU
LAR CELL SMALL ARROW AS WELL AS A VESICLE OF ELECTRON
DENSE MATERIAL G 4HE LARGE ARROW MAY INDICATE SWOLLEN GRANULAR
ENDOPLASMIC RETICULUM 8
" !N OOCYTE AT THE CORTICAL ALVEOLUS STAGE 4HE HEXAGONAL PARTITIONS H ARE LARGER AND THE SUBFOLLICULAR SPACE HAS EXPANDED
! FEW MEMBRANOUS FRAGMENTS ARROWS ARE SCATTERED IN THE SUBFOLLICULAR SPACE 8
# !N OOCYTE IN A LATE CORTICAL ALVEOLUS STAGE 7ELL DElNED HEXAGONAL PARTITIONS H EXTEND INTO THE SUBFOLLICULAR SPACE S -I
CROVILLI M FROM THE OOCYTE EXTEND TOWARD THE FOLLICULAR CELL WHILE A FEW STUBBY MICROVILLI SMALL ARROW ARE SEEN REACHING
OUT FROM THE FOLLICULAR CELL 4HE HEXAGONAL SUBPATTERN LARGE ARROW IS BEGINNING TO APPEAR IN THE mOORS OF THE COMPARTMENTS
4HE ZONA PELLUCIDA : : IS FORMING 8
4HE INSET IS OF AN EARLIER OOCYTE WHERE THE ZONA PELLUCIDA P IS JUST BEGINNING TO APPEAR $ENSE
CORED VESICLES D ARE PRES
ENT IN THE PERIPHERAL OOPLASM
$ !N OOCYTE DURING VITELLOGENESIS 4HE ZONA PELLUCIDA : : OF THE PRIMARY ENVELOPE IS WELL DElNED PARTITIONS H OF
THE SECONDARY ENVELOPE ENCLOSE THE HEXAGONAL COMPARTMENTS AND MICROVILLI M FROM THE OOCYTE SPAN THE SUBFOLLICULAR
SPACE S 8
!BBREVIATIONS B BASAL LAMINA C COLLAGENOUS lBRES F FOLLICULAR CELLS FB lBROBLASTS G GRANULAR MATERIAL H HEXAGONAL PARTI
TIONS M OOCYTE MICROVILLI O OOPLASM P PORE CANAL S SUBFOLLICULAR SPACE T THECAL CELLS : AND : ZONA PELLUCIDA
#(!04%2
&IGURE 3CHEMATIC DIAGRAM TO ILLUSTRATE THE ELEMENTS OF THE FOLLICULAR WALL IN THE SOLE 0LEURONICHTHYS COENOSUS DURING
LATE VITELLOGENESIS 4HE mOORS OF THE HEXAGONAL COMPARTMENTS DISPLAY A SUBPATTERN OF HEXAGONAL RIDGES ARROWS EACH HEXAGON
ENCIRCLING AN OOCYTE MICROVILLUS &ROM 3TEHR AND (AWKES REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
!BBREVIATIONS " BASAL LAMINA & FOLLICULAR CELLS &" lBROBLASTS ( HEXAGONAL PARTITIONS - OOCYTE MICROVILLI / OOPLASM
4 THECA : AND : ZONA PELLUCIDA
@
&IGURE -ICROGRAPHS OF THE ENVELOPE OF THE SOLE 0LEU
RONICHTHYS COENOSUS &ROM 3TEHR AND (AWKES REPRO
DUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION SHOWING
A MICROPYLAR CELL M THAT PENETRATES BOTH ENVELOPE LAYERS
AND MAKES DIRECT CONTACT WITH THE OOCYTE 4HE MICROPYLE
FORMS AROUND THE EXTENSION OF THIS CELL ARROW 8
" 3CANNING ELECTRON MICROGRAPH OF THE mOORS OF THE HEXAGONAL
COMPARTMENTS OF THE SECONDARY ENVELOPE 4HE COMPARTMENT
AT THE CENTRE OF THE lGURE ENCLOSES THE SINGLE MICROPYLE OF
THE OOCYTE 4HE mOORS OF THE HEXAGONAL COMPARTMENTS DISPLAY
A SUBPATTERN OF HEXAGONAL RIDGES EACH HEXAGON ENCIRCLING AN
OOCYTE MICROVILLUS 8
/6!2)!. &/,,)#,%3
&IGURE ! " AND $ ARE SCANNING ELECTRON MICROGRAPHS OF THE SURFACE OF A RECENTLY OVULATED EGG OF THE LAMPREY 0ET
ROMYZON MARINUS # IS A PHOTOMICROGRAPH OF A SECTION OF AN UNOVULATED LAMPREY EGG &ROM 9ORKE AND -C-ILLAN
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! %NTIRE EGG SHOWING THE ADHESIVE COAT ! APICAL TUFT 4 AND BETWEEN THESE THE EXPOSED SURFACE OF THE ZONA PELLUCIDA :0
4HE ADHESIVE COAT IS COVERED WITH CLUSTERS OF ADHESIVE SACCULES 3 8
" 4HE IRREGULAR APICAL TUFT ARROWHEADS CAPS THE APICAL POLE AND IS SURROUNDED BY THE MORE FEATURELESS EXPOSED SURFACE OF
THE ZONA PELLUCIDA :0 8
# 4HE SECTION PASSES THROUGH THE ACELLULAR APICAL TUFT 4 . NUCLEUS 4H THECA 9 YOLK 8
$ 4HE ADHESIVE COAT CONSISTS OF CLUSTERS OF ADHESIVE SACCULES ARROWS AND IS BORDERED BY THE EXPOSED SURFACE OF THE ZONA PEL
LUCIDA :0 8
#(!04%2
&IGURE 3KETCH OF THE VEGETAL POLE OF AN OVULATED
EGG OF -YXINE GLUTINOSA SHOWING lLAMENTS WITH ANCHOR LIKE
TERMINALS &ROM ,YNGNES REPRODUCED BY 7ALVIG
REPRODUCED WITH PERMISSION
&IGURE -ATURE EGG OF -YXINE GLUTINOSA LENGTH
EXCLUDING ANCHOR lLAMENTS MM !0 ANIMAL POLE
/2 OPERCULAR RING &ROM *ENSEN REPRODUCED BY
7ALVIG REPRODUCED WITH PERMISSION
@
&IGURE 0HOTOGRAPHS OF INTACT EGGS OF
THE HAGlSH %PTATRETUS BURGERI &ROM &ERN
HOLM REPRODUCED WITH KIND PERMISSION OF
"LACKWELL 0UBLISHING
!
)NSET 4HE ANIMAL POLE OF A FRESH EGG
SHOWING ANCHOR lLAMENTS 3CALE
MM
!
3CANNING ELECTRON MICROGRAPH OF THE API
CAL POLE SHOWING THE MICROPYLAR FUNNEL
SURROUNDED BY EIGHT ANCHOR lLAMENTS
4HE SQUARE IS ENLARGED IN # 3CALE
MM
"
4IP OF AN ANCHOR lLAMENT 3CALE
M
# $ 0ATTERN OF HEXAGONAL RIDGES AT THE BOT
TOM OF THE MICROPYLAR FUNNEL /NLY ONE
OF THE CELLS IS OPEN AT THE BOTTOM ARROW
IN $ 3CALE M IN # M IN $
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE GERMINAL RIDGE OF THE PIPElSH 3YNGNATHUS
SCOVELLI &OR ORIENTATION SEE &IGURE &ROM "EGOVAC AND 7ALLACE REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
! 'ROUPS OF PREFOLLICULAR CELLS 0&# AND OOCYTES / LIE IN THE RIDGE "ORDERS OF ADJACENT OOCYTES ARE CONTIGUOUS ARROWS
4HE BASAL LAMINA ARROWHEADS OF THE LUMINAL EPITHELIUM ,% DIVERGES FROM THE LUMINAL EPITHELIAL CELLS TO ENVELOP THE
GERMINAL RIDGE 8
" 4HE BASAL LAMINA SURROUNDING THE GERMINAL RIDGE COVERS THE LEFT SIDE OF THIS PREFOLLICULAR CELL 0&# -EIOTIC OOCYTES /
WITH SHARED BORDERS ARE INDICATED )NTRACELLULAR lLAMENTS ARROWS ARE APPARENT IN THE PREFOLLICULAR CELL 8
# ! PROCESS ARROWS FROM A PREFOLLICULAR CELL 0&# HAS EXTENDED BETWEEN THE BORDERS OF TWO MEIOTIC OOCYTES / AND HAS
FORMED A DESMOSOMAL CONTACT ARROWHEAD WITH AN ADJACENT PREFOLLICULAR CELL 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE FOLLICULAR EPITHELIUM OF THE MEDAKA /RYZIAS LATIPES
DURING EARLY VITELLOGENESIS &ROM .AKASHIMA AND )WAMATSU REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS
)NC
! 0ORTION OF TWO FOLLICULAR CELLS ANCHORED BY A DESMOSOME D AND TONOlLAMENTS TF 8
" 4ANGENTIAL SECTION THROUGH THE FOLLICULAR EPITHELIUM SHOWING DESMOSOMES ARROWS BETWEEN ADJACENT CELLS 4HE CELLS CON
TAIN BUNDLES OF TONOlLAMENTS TF AS WELL AS SPARSE MITOCHONDRIA AND GRANULAR ENDOPLASMIC RETICULUM 8
&IGURE 0HOTOMICROGRAPHS OF FOLLICLES OF ELASMOBRANCHS &ROM #ALLARD
ET AL REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! &OLLICLE OF 2AJA NEVUS SHOWING SMALL AND LARGE ARROWHEADS FOLLICULAR CELLS
4HERE ARE HAEMOPOIETIC CELLS ( IN THE OVARIAN TISSUE
" 3MALL FOLLICLES ABOVE AND A LARGE FOLLICLE BELOW OF A SEVEN GILL SHARK
!RROWHEADS INDICATE NUCLEI CONTAINING LAMPBRUSH CHROMOSOMES
!BBREVIATIONS G FOLLICULAR EPITHELIUM OO OOCYTE TH THECA
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF PRIMARY FOLLICLES OF THE ELASMOBRANCH 2AYA ASTERIAS &ROM !NDREUCCETTI
ET AL REPRODUCED WITH PERMISSION
! 4HE FOLLICULAR EPITHELIUM CONSISTS SIMPLE SQUAMOUS CELLS 8
" 4HE PLASMA MEMBRANES OF A FOLLICULAR CELL AND THE OOCYTE RUN PARALLEL AND ARE SEPARATED BY A SPACE OF NM ARROWHEAD
AT THE ARROW THE MEMBRANES ARE CONNECTED BY DESMOSOME
LIKE JUNCTIONS 4HE PERIVITELLINE SPACE
IS BEGINNING TO APPEAR
8
!BBREVIATIONS ", BASAL LAMINA #% COELOMIC EPITHELIUM , LIPID DROPLETS - MITOCHONDRIA . NUCLEUS /O OOCYTE 3#
SQUAMOUS CELL OF THE FOLLICULAR EPITHELIUM 4# THECAL CELL
@
&IGURE ,IGHT MICROGRAPHS OF SECTIONS THROUGH THE
FOLLICULAR EPITHELIUM IN THE OVARY OF THE YELLOW SPOTTED
STINGRAY 5ROLOPHUS JAMAICENSIS &ROM (AMLETT *EZIOR
AND 3PIELER REPRODUCED WITH PERMISSION OF 5RBAN
&ISCHER 6ERLAG
! )N A FOLLICLE OF MM DIAMETER THE OOCYTE O IS SEPA
RATED FROM THE COLUMNAR FOLLICULAR EPITHELIUM F BY THE
ZONA PELLUCIDA DARK ARROW 4HE FOLLICULAR CELLS REST ON
A BASAL LAMINA OPEN ARROW ADJACENT TO THE THECA T
2ED BLOOD CELLS
ARE VISIBLE IN THE THECAL VESSELS
E EPIGONAL GLAND 8
" ,ARGE LIPID CONTAINING CELLS
ARE INTERSPERSED AMONG
THE COLUMNAR FOLLICULAR CELLS F IN A FOLLICLE MM IN
DIAMETER &OLLICULAR CELLS CONTAIN YOLK PRECURSOR VESICLES
CIRCLES 8
#(!04%2
@
&IGURE #OMPOSITE DRAWING SHOWING THE RELA
TIONSHIP BETWEEN FOLLICULAR CELLS THE ZONA PELLUCIDA
AND THE OOCYTE IN THE FOLLICLE OF THE YELLOW SPOTTED STING
RAY 5ROLOPHUS JAMAICENSIS &ROM (AMLETT *EZIOR AND
3PIELER REPRODUCED WITH PERMISSION OF 5RBAN
&ISCHER 6ERLAG
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A FOLLICLE M IN DIAMETER OF THE ELASMOBRANCH 2AYA ASTERIAS
&OLLICULAR CELLS FORM A DOUBLE LAYER 0ROCESSES DOUBLE ARROWS EXTEND FROM THE FOLLICULAR CELLS INTO THE ZONA PELLUCIDA 8
&ROM !NDREUCCETTI ET AL REPRODUCED WITH PERMISSION
!BBREVIATIONS ", BASAL LAMINA , LIPID DROPLETS -I MICROVILLI /O OOCYTE 3# SMALL FOLLICULAR CELLS 6% ZONA PELLUCIDA
4# THECAL CELL
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF FOLLICLES OF THE ELASMOBRANCH 2AYA ASTERIAS &ROM !NDREUCCETTI ET AL
REPRODUCED WITH PERMISSION
! &OLLICLE M IN DIAMETER 3MALL AND LARGE CELLS CONSTITUTE THE FOLLICULAR EPITHELIUM 4HE SMALL CELLS ARE LOCATED BENEATH
THE BASAL LAMINA AND ALONG THE PERIVITELLINE SPACE 8
" &OLLICLE M IN DIAMETER !N INTERCELLULAR BRIDGE ARROW CONNECTS A LARGE CELL WITH THE OOCYTE 8
!BBREVIATIONS ", BASAL LAMINA 'LY GLYCOGEN , LIPID DROPLETS ,# LARGE FOLLICULAR CELL - MITOCHONDRIA /O OOCYTE
3# SMALL FOLLICULAR CELL 4# THECAL CELL 6% ZONA PELLUCIDA
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF FOL
LICLES M IN DIAMETER OF THE ELASMOBRANCH 2AYA
ASTERIAS &ROM !NDREUCCETTI ET AL REPRODUCED WITH
PERMISSION
! 4HE FOLLICULAR EPITHELIUM IS POLYMORPHIC MULTILAYERED
AND CONSISTS OF SMALL LARGE AND PYRIFORM CELLS 4HE PYR
IFORM CELLS SPAN THE FOLLICULAR EPITHELIUM FROM THE BASAL
LAMINA TO THE SURFACE OF THE OOCYTE 8
" 4HE CYTOPLASM OF THIS PYRIFORM CELL IS RICH IN MITO
CHONDRIA AND RIBOSOMES 4HE APEX OF THE PYRIFORM CELL
CONTINUES INTO AN INTERCELLULAR BRIDGE ARROWS ! LONG
PROTRUSION ARROWHEADS OF A SMALL CELL IS INTERPOSED
BETWEEN TWO PYRIFORM CELLS 8
!BBREVIATIONS ", BASAL LAMINA ,# LARGE CELL - MITO
CHONDRIA .5 NUCLEOLUS /O OOCYTE 0# PYRIFORM CELL
3# SMALL CELL 4# THECAL CELL 6% ZONA PELLUCIDA
/6!2)!. &/,,)#,%3
&IGURE ! SERIES OF TRANSMISSION ELECTRON MICROGRAPHS OF FOLLICLES OF THE ELASMOBRANCH 2AYA ASTERIAS TO ILLUSTRATE INTER
CELLULAR BRIDGES CONNECTING PYRIFORM CELLS TO THE OOCYTE 4HE BRIDGES CONTAIN ORGANELLES 4HE ARROW IN # INDICATES RIBOSOMES
AND THE ASTERISK IN $ A MEMBRANOUS WHORL &ROM !NDREUCCETTI ET AL REPRODUCED WITH PERMISSION
! 8 " 8 # 8 $ 8
!BBREVIATIONS - MITOCHONDRIA -I MICROVILLI /O OOCYTE 2% ENDOPLASMIC RETICULUM 6% ZONA PELLUCIDA
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE FOLLICULAR PERIPHERY IN THE OVARY OF THE SEA BASS $ICENTRARCHUS LABRAX
&ROM #APORICCIO AND #ONNES REPRODUCED WITH PERMISSION -ASSON %DITEUR
! $URING PREVITELLOGENESIS DESMOSOMAL CONTACTS $E LINK THE OOCYTE /V AND FOLLICULAR CELL #F BEFORE THE APPEARANCE OF
THE ZONA PELLUCIDA %I INTERCELLULAR SPACE 8
#(!04%2
&IGURE #ONTINUED
" -ICROVILLI FROM THE OOCYTE ARE CONNECTED BY DESMOSOMES ARROWS WITH MICROVILLI FROM THE FOLLICULAR CELLS WITHIN PORE
CANALS OF THE DEVELOPING ZONA PELLUCIDA # # 8
# 7ELL DEVELOPED DESMOSOMES ARROW LINK ADJACENT CELLS OF THE FOLLICULAR EPITHELIUM 8
/6!2)!. &/,,)#,%3
&IGURE %LECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS OF THE JUNCTIONS BETWEEN ADJACENT CELLS IN THE FOLLICULAR EPITHE
LIUM IN THE OVARY OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM +ESSEL 2OBERTS AND 4UNG REPRODUCED WITH PERMISSION FROM
.UOVA )MMAGINE %DITRICE
! -ULTIPLE STRANDS IN TIGHT JUNCTIONS BETWEEN FOLLICULAR CELLS OF A PREVITELLOGENIC OOCYTE !N IRREGULAR NETWORK OF STRANDS 3
IS FORMED IN PLACES BY BARS " OF DIFFERENT LENGTHS AND OCCASIONALLY BY INTERCALATED PARTICLES ARROWHEADS � PROCESS OF
A FOLLICULAR CELL 8
" 4HE JUNCTIONAL COMPLEX FROM THE FOLLICULAR EPITHELIUM OF A VITELLOGENIC OOCYTE IS NOT AS EXTENSIVE AND HAS A MORE PARTICULATE
APPEARANCE ARROWHEADS THAN THAT SHOWN ABOVE /NLY SHORT BARS " ARE PRESENT IN THIS REPLICA 8
#(!04%2
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE ZEBRAlSH "RACHY
DANIO RERIO 4HE PORE CANALS WITHIN THE ZONA PELLUCIDA 6 ARE CUT TRANSVERSELY THEREBY DEMONSTRATING THE INTIMATE RELATIONSHIP
BETWEEN MICROVILLI FROM THE OOCYTE ARROWHEADS AND PROCESSES FROM A FOLLICULAR CELL ARROWS 8 &ROM +ESSEL ET AL
REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
@
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE PERIPHERY OF OVARIAN FOLLICLES OF ZEBRAlSH "RACHYDANIO
RERIO &ROM +ESSEL ET AL REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! " 4HE ZONA PELLUCIDA IS FORMING IN THE PERIVITELLINE SPACE -ICROVILLI ARROWHEADS FROM THE OOCYTE EXTEND THROUGH THEIR
INDIVIDUAL PORE CANALS TO MAKE CONTACT WITH SQUAMOUS FOLLICULAR CELLS 3PARSER STUBBIER MICROVILLI EXTEND FROM THE FOL
LICULAR CELLS IN THE OPPOSITE DIRECTION 4HE FOLLICULAR EPITHELIUM IS SURROUNDED BY A PROMINENT BASAL LAMINA ! 8
" 8
# $ 4HERE IS CLOSE CONTACT ARROWHEADS BETWEEN PROCESSES OF FOLLICULAR CELLS AND MICROVILLI OF THE OOCYTE 8
%
!T A LATER STAGE IN ITS DEVELOPMENT THE ZONA PELLUCIDA EXHIBITS THREE LAYERS -ICROVILLI ARROWHEADS FROM THE
OOCYTE EXTEND THROUGH PORE CANALS TOWARD A FOLLICULAR CELL .OTE THE TERMINAL BRANCHING " OF ONE OF THESE MICROVILLI AS
IT PRESSES AGAINST THE PLASMALEMMA OF A FOLLICULAR CELL 8
&
!N OOCYTE MICROVILLUS ARROWHEAD HAS INVAGINATED A FOLLICULAR CELL # 8
'
! PROCESS FROM A FOLLICULAR CELL LIES PARALLEL TO AN OOCYTE MICROVILLUS ARROWHEAD WITHIN A SINGLE PORE CANAL 8
!BBREVIATIONS "- BASAL LAMINA #A CAPILLARY & FOLLICULAR CELLS - MICROVILLI / OOCYTE 0 PROCESSES 6 ZONA PELLUCIDA
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A SECTION THROUGH THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE ZEBRAlSH
"RACHYDANIO RERIO 8 &ROM +ESSEL ET AL REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! -ICROlLAMENTS -& ABOUND IN THIS LONGITUDINAL SECTION OF AN OOCYTE MICROVILLUS - AS WELL AS IN THE CORTICAL OOPLASM
/ 4HE ARROWS INDICATE TRANSVERSE CONNECTIONS BETWEEN THE MICROVILLUS AND THE ZONA PELLUCIDA 6 OF THE WALL OF THE PORE
CANAL
" -ICROlLAMENTS -& ARE ABUNDANT WITHIN THE PROCESS OF A FOLLICULAR CELL & 4HE ARROWHEADS INDICATE CROSS SECTIONS OF OO
CYTE MICROVILLI A SINGLE MICROVILLUS FROM THE OOCYTE - APPROACHES THE FOLLICULAR CELL PROCESS AT THE BOTTOM OF THE PICTURE
4HE ARROWS INDICATE TRANSVERSE CONNECTIONS BETWEEN THE MICROVILLUS AND THE ZONA PELLUCIDA 6
&IGURE ! " 4RANSMISSION ELECTRON MICROGRAPHS OF CROSS SECTIONS THROUGH OOCYTE MICROVILLI - FROM OVARIAN FOLLICLES
OF THE ZEBRAlSH "RACHYDANIO RERIO 4HE ARROWS INDICATE GAP JUNCTIONS BETWEEN THE MICROVILLI AND THE SURFACE OF FOLLICULAR CELLS
& &ROM +ESSEL ET AL REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! 8
" 8
/6!2)!. &/,,)#,%3
&IGURE %LECTRON MICROGRAPH OF FREEZE FRACTURE REPLICA THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE ZEBRAlSH "RACHYDANIO
RERIO !RROWHEADS INDICATE SEVERAL GAP JUNCTIONAL ARRAYS ON THE SURFACE OF A FOLLICULAR CELL &ROM +ESSEL ET AL REPRODUCED
WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
!BBREVIATIONS & FOLLICULAR CELL - OOCYTE MICROVILLI 0 PROCESSES FROM A FOLLICULAR CELL 6 ZONA PELLUCIDA
@
&IGURE %LECTRON MICROGRAPHS
OF FREEZE
FRACTURE REPLICAS THE PERIPH
ERY OF OVARIAN FOLLICLES OF THE ZEBRAF
ISH "RACHYDANIO RERIO TO ILLUSTRATE GAP
JUNCTIONAL ARRAYS ON MICROVILLI FROM OO
CYTES AND ON NEARBY PLASMA MEMBRANES
OF FOLLICULAR CELLS &ROM +ESSEL ET AL
REPRODUCED WITH PERMISSION FROM
.UOVA )MMAGINE %DITRICE
! 8
" 8
# 8
!BBREVIATIONS & FOLLICULAR CELL '* GAP
JUNCTIONAL ARRAY - OOCYTE MICROVILLI
/ OOCYTE 0 PROCESS FROM A FOLLICULAR
CELL 6 ZONA PELLUCIDA
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A SECTION THROUGH THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE CHUM SALMON
/NCORHYNCHUS KETA 4IPS OF OOCYTE MICROVILLI PROTRUDE BEYOND THE ZONA PELLUCIDA TO INVAGINATE A FOLLICULAR CELL ! OR ATTACH
ITSELF TO A PROCESS FROM A FOLLICULAR CELL " 4HE ARROW INDICATES A NARROW SPACE BETWEEN THE APPOSING PLASMA MEMBRANES OF THE
MICROVILLUS AND THE PROCESS &ROM +OBAYASHI B REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! 8
" 8
!BBREVIATIONS ' FOLLICULAR CELL -6 OOCYTE MICROVILLUS 0' PROCESS FROM A FOLLICULAR CELL 33 SUBFOLLICULAR SPACE : ZONA
PELLUCIDA
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A SECTION THROUGH THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE CHUM SALMON
/NCORHYNCHUS KETA SHOWING THE ASSOCIATION BETWEEN PROCESSES FROM FOLLICULAR CELLS 0' WITH THE OOLEMMA 0/ PERIPHERAL
OOPLASM &ROM +OBAYASHI B REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! 4HE EXPANDED END OF THE PROCESS TERMINATES IN A SLIGHT DEPRESSION OF THE OOLEMMA 4HERE IS A SMALL AMOUNT OF lLAMENTOUS
MATERIAL AND AGRANULAR ENDOPLASMIC RETICULUM IN THE TIP OF THE PROCESS 8
" ! TIGHT JUNCTION ARROW AND GAP JUNCTIONS ARROWHEADS SPAN THE SPACE BETWEEN THE TIP OF THE PROCESS AND THE OOLEMMA
8
/6!2)!. &/,,)#,%3
&IGURE #ONTINUED
# %NDOCYTOTIC ACTIVITY ARROW OCCURS IN THE EXPANDED END OF A PROCESS 8
$ 4HE OOLEMMA IN THESE REGIONS FORMS COATED VESICLES ARROWS 8
!BBREVIATIONS -6 OOCYTE MICROVILLUS 0' PROCESS FROM A FOLLICULAR CELL 0/ PERIPHERAL OOPLASM : ZONA PELLUCIDA
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A SECTION THROUGH THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE CHUM SALMON
/NCORHYNCHUS KETA SHOWING THE ASSOCIATION WHEREBY THE EXPANDED ENDS OF PROCESSES FROM FOLLICULAR CELLS lT DEEPLY INTO INDEN
TATIONS OF THE OOLEMMA &ROM +OBAYASHI B REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! $ESMOSOMES OR DESMOSOME
LIKE JUNCTIONS OCCUR BETWEEN THE PLASMALEMMA OF THE PROCESS AND THE OOLEMMA 8
" 4HE ARROW INDICATES A LARGE COATED VESICLE IN THE PERIPHERAL OOPLASM 8
!BBREVIATIONS #6 CORTICAL VESICLE -6 OOCYTE MICROVILLUS 0' PROCESS FROM A FOLLICULAR CELL 0/ PERIPHERAL OOPLASM
: ZONA PELLUCIDA
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF THE JUNCTIONS BETWEEN ADJACENT CELLS IN THE FOLLICULAR EPITHELIUM OF THE AYU 0LECOGLOS
SUS ALTIVELIS &ROM 4OSHIMORI AND 9ASUZUMI A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 4RANSMISSION ELECTRON MICROGRAPH SHOWING REGIONS OF CLOSE PROXIMITY ARROWS AND FOCAL FUSION ARROWHEAD OF THE OUTER
LEAmETS OF MEMBRANES OF FOLLICULAR CELLS 8
A
" %LECTRON MICROGRAPH OF A FREEZE
FRACTURED REPLICA OF THE FOLLICULAR EPITHELIUM &IVE TO SEVEN STRANDS CONSISTING OF RIDGES
AND GROOVES ON THE 0&
AND %&
FRACTURE FACES RESPECTIVELY ARE DISPLAYED ON THE SURFACE OF A FOLLICULAR CELL UPPER CENTRE
8 )NSET ! FEW STRANDS TERMINATE FREELY WITHOUT REJOINING THE NETWORK ARROWHEADS 4HE SPACES BETWEEN THE
STRANDS ARE WIDE 8
!BBREVIATIONS ! 0& PLASMATIC FRACTURE FACE " %& EXTRAPLASMATIC FRACTURE FACE ", BASAL LAMINA # ZONA PELLUCIDA
&# FOLLICULAR CELL . NUCLEUS / OOCYTE
@
&IGURE %LECTRON
MICRO
GRAPH OF A FREEZE
FRACTURED REPLICA
OF THE FOLLICULAR EPITHELIUM FROM
A VITELLOGENIC FOLLICLE OF THE AYU
0LECOGLOSSUS ALTIVELIS 'AP JUNC
TIONS CONSISTING OF CLUSTERS OF
TO INTRAMEMBRANOUS PARTICLES
ARROWS ABOUND BETWEEN MICROVIL
LI OF THE OOCYTE AND FOLLICULAR CELLS
8 &ROM 4OSHIMORI AND
9ASUZUMI B REPRODUCED WITH
PERMISSION
!BBREVIATIONS ! 0& FRACTURE FACE
# ZONA PELLUCIDA & %& FACE OF
PLASMA MEMBRANE OF FOLLICULAR
CELL - MICROVILLUS IN A PORE CANAL
0 PROCESS FROM FOLLICULAR CELL
/6!2)!. &/,,)#,%3
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE PERIPHERY OF AN OVARIAN FOLLICLE IN LATE VITELLOGENESIS
4HIS SPECIMEN WAS TAKEN FROM A CYPRINODONT !PHANIUS MENTO THAT HAD BEEN INJECTED WITH HORSERADISH PEROXIDASE 4HE ZONA PEL
LUCIDA IS SHOWN AT THE UPPER RIGHT 0EROXIDASE HAS BEEN DEPOSITED BETWEEN THE ZONA PELLUCIDA AND THE OOLEMMA CURVED ARROWS
AND IS LOCATED WITHIN PINOCYTOTIC VESICLES TRIPLE ARROWS /OCYTE MICROVILLI WITHIN PORE CANALS DOUBLE ARROWS ARE SURROUNDED
BY THE TRACER 4HE ASTERISKS INDICATE CORTICAL GRANULES 8 &ROM !BRAHAM ET AL REPRODUCED WITH PERMISSION OF
THE AUTHOR
&IGURE 0HOTOMICROGRAPH OF THE PERIPHERY OF AN VITELLOGENIC FOLLICLE OF A VIVIPAROUS ELASMOBRANCH THE YELLOW SPOTTED
STINGRAY 5ROLOPHUS JAMAICENSIS )NWARD FOLDS F OF THE FOLLICULAR WALL COVERED BY THE ZONA PELLUCIDA CURVED ARROW AND CARRY
ING THECAL CELLS T AND BLOOD VESSELS INDENT THE SURFACE OF AN OOCYTE O 4HE FOLLICULAR EPITHELIUM CONSISTS OF LARGE OPEN ARROW
AND SMALL CLOSED ARROW CELLS 4HE FOLLICLE IS SURROUNDED BY VASCULAR CONNECTIVE TISSUE B &ROM (AMLETT *EZIOR AND 3PIELER
REPRODUCED WITH PERMISSION OF 5RBAN &ISCHER 6ERLAG
/6!2)!. &/,,)#,%3
&IGURE -ICROGRAPHS OF THE PERIPHERY OF FOLLICLES
OF A VIVIPAROUS ELASMOBRANCH THE YELLOW SPOTTED STING
RAY 5ROLOPHUS JAMAICENSIS &ROM (AMLETT *EZIOR AND
3PIELER REPRODUCED WITH PERMISSION OF 5RBAN
&ISCHER 6ERLAG
!
0HOTOMICROGRAPH OF A VITELLOGENIC FOLLICLE &OL
LICULAR CELLS CONTAIN PROMINENT YOLK PRECURSOR
VESICLES CIRCLE 4HE OPEN ARROW INDICATES THE
BASAL LAMINA OF THE FOLLICULAR EPITHELIUM 4HE
THECA T CONTAINS BLOOD VESSELS
A
B 8
"
4RANSMISSION ELECTRON MICROGRAPH OF VITELLO
GENIC FOLLICULAR CELLS CONTAINING HETEROGENEOUS
TRANSPORT VESICLES CIRCLE 4HE ASTERISK INDICATES
THE ZONA PELLUCIDA B BASAL LAMINA G 'OLGI
COMPLEX 8
# $ 4RANSMISSION ELECTRON MICROGRAPHS OF ACTIVELY
VITELLOGENIC FOLLICULAR CELLS CONTAINING HETEROGE
NEOUS TRANSPORT VESICLES 8
#(!04%2
&IGURE %LECTRON MICROGRAPH OF THE FOLLICULAR EPITHELIUM OF A VITELLOGENIC FOLLICLE OF A VIVIPAROUS ELASMOBRANCH
THE YELLOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS &OLLICULAR CELLS CONTAINING YOLK PRECURSOR VESICLES CIRCLE EXTEND
PROCESSES OR TRANSOSOMES ARROWHEADS INTO THE ZONA PELLUCIDA
TO INVAGINATE THE OOLEMMA OF THE OOCYTE O B BASAL LAMINA
8 &ROM (AMLETT *EZIOR AND 3PIELER REPRODUCED WITH PERMISSION OF 5RBAN &ISCHER 6ERLAG
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS FROM A FOLLICLE OF THE ELASMOBRANCH 2AYA ASTERIAS TO ILLUSTRATE INTERCELLULAR
BRIDGES ARROWS CONNECTING A LARGE FOLLICULAR CELL TO THE OOCYTE &ROM !NDREUCCETTI ET AL REPRODUCED WITH PERMISSION
! 8
" (IGHER MAGNIlCATION OF THE SAME CELL AT THE LEVEL OF THE INTERCELLULAR BRIDGES 8
!BBREVIATIONS ,# LARGE FOLLICULAR CELL - MITOCHONDRIA -I MICROVILLI /O OOCYTE 3# SMALL FOLLICULAR CELL
/6!2)!. &/,,)#,%3
&IGURE %LECTRON MICROGRAPH OF THE MESOTHELIUM - THECA 4 AND ITS ADJACENT LAYERS AND FOLLICULAR CELLS &# OF
AN EARLY FOLLICLE OF THE LAMPREY 0ETROMYZON MARINUS &IBROCYTES &" SEND LONG CYTOPLASMIC PROCESSES ARROW THROUGHOUT
THE MATRIX TO ADJACENT lBROCYTES 4HE PROCESS FROM A CELL NOT IN THIS SECTION BORDERS ON THE CELL BODY OF THE CELL SHOWN
"LOOD VESSELS " RUN WITHIN THE THECA &ROM 9ORKE AND -C-ILLAN REPRODUCED WITH PERMISSION FROM THE 3OCIETY FOR
THE 3TUDY OF 2EPRODUCTION )NC
!BBREVIATIONS # CYTOPLASMIC PROCESS )/ INTRAOVARIAN SPACE 3 INTERCELLULAR SPACE :0 ZONA PELLUCIDA 8
&IGURE 0HOTOMICROGRAPHS OF OVARIAN FOLLICLES OF THE LAMPREY 0ETROMYZON MARINUS DURING VITELLOGENESIS SHOWING THE
MERGER OF A YOLK
LADEN hNURSE CELLv WITH A VITELLOGENIC OOCYTE &ROM ,EWIS AND -C-ILLAN REPRODUCED WITH PERMIS
SION OF *OHN 7ILEY 3ONS )NC
! .URSE CELL .# PACKED WITH YOLK GRANULES 8
" ! LARGE NURSE CELL .# HAS PARTIALLY MERGED WITH AN OOCYTE AT THE POINTS WHERE THEY ARE NOT JOINED THE CELLS HAVE BEEN
SEPARATED BY SHRINKAGE DURING PROCESSING 8
# &OLLOWING THE MERGER MEMBRANOUS REMNANTS ARROW OF THE NURSE CELL PERSIST IN THE CYTOPLASM OF THE OOCYTE 8
#(!04%2
&IGURE !N UNUSUAL METHOD OF FORMATION OF THE SECONDARY ENVELOPE SEEN IN VITELLOGENIC OOCYTES OF THE SHEATlSH 3ILURUS
GLANIS &ROM !BRAHAM ET AL REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH $URING EARLY VITELLOGENESIS THE FOLLICULAR CELLS PROLIFERATE TO FORM AN IRREGULAR MASS OF CELLS OPEN ARROWS
AROUND THE ZONA PELLUCIDA DARK ARROWS
!BBREVIATIONS #! CORTICAL ALVEOLI 90 YOLK PLATELETS
" %LECTRON MICROGRAPH OF THESE IRREGULAR CELLS OR hMUCOSOMESv MUC ADJACENT TO THE THECA ARROWS
A
&IGURE %LECTRON MICROGRAPH OF A SECTION OF THE BASAL REGION OF AN EARLY FOLLICLE OF THE LAMPREY 0ETROMYZON MARINUS
3QUAMOUS FOLLICULAR CELLS & ARE LIFTED FROM THE SURFACE OF THE ZONA PELLUCIDA :0 BY A LARGE ADHESIVE CELL -ICROVILLI -6
FROM THE LATERAL BORDERS OF THE ADHESIVE CELLS EXTEND INTO WIDE INTERCELLULAR SPACES 4HE SURFACE OF THE ZONA PELLUCIDA IS SLIGHT
LY DEPRESSED BENEATH THE ADHESIVE CELL ARROWS 4HE CYTOPLASM OF THE ADHESIVE CELL IS PACKED WITH INTERCONNECTED SACCULES
) WHICH SHOW GREAT VARIATION IN STAINING AND CONTAINS A SMALL AMOUNT OF AGRANULAR ENDOPLASMIC RETICULUM 2 4H THECA
8 &ROM 9ORKE AND -C-ILLAN REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
/6!2)!. &/,,)#,%3
#(!04%2
&IGURE -ICROGRAPHS OF THE ADHESIVE LAYER OF OOCYTES OF THE LAMPREY 0ETROMYZON MARINUS AROUND THE TIME OF OVULATION
&ROM 9ORKE AND -C-ILLAN REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF A SECTION THROUGH THE SURFACE OF A RECENTLY OVULATED EGG SHOWING THE PLEIOMORPHIC ADHESIVE SACCULES
OF THE ADHESIVE COAT 8
" 0HOTOMICROGRAPH OF A SIMILAR REGION OF AN UNOVULATED EGG JUST BEFORE SPAWNING 8
# %LECTRON MICROGRAPH OF AN EGG DURING SPAWNING $BRIS ARROWS FROM THE FOLLICULAR ADHESIVE CELLS ESPECIALLY IN THE FORM
OF ADHESIVE SACCULES ADHERES TO THE ZONA PELLUCIDA 4HE THECA PERSISTS OVER THIS PORTION OF THE EGG 8
!BBREVIATIONS !# ADHESIVE CELLS 3 ADHESIVE SACCULES 4H THECA 9 YOLK :0 ZONA PELLUCIDA
/6!2)!. &/,,)#,%3
&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF THE PREOVULATORY FOLLICLE OF A MATURE COHO /NCORHYNCHUS KISUTCH &ROM
.AGAHAMA #LARKE AND (OAR REPRODUCED WITH PERMISSION OF THE .2# 0RESS
! %XTENSIVE GRANULAR ENDOPLASMIC RETICULUM IN THE FOLLICULAR CELLS '# CONTAINS AMORPHOUS MATERIAL OF VARIABLE ELECTRON
DENSITY 3PECIAL THECAL CELLS 3# ARE SEEN IN THE THECA :2 ZONA PELLUCIDA 8
#(!04%2
&IGURE #ONTINUED
" 4HE CYTOPLASM OF A SPECIAL THECAL CELL IS PACKED WITH AGRANULAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA WITH TUBULAR
CRISTAE 8
&IGURE %LECTRON MICROGRAPH OF A SECTION OF A POSTOVULATORY FOLLICLE OF THE MEDAKA /RYZIAS LATIPES SHOWING A PORTION
OF A FOLLICULAR CELL PACKED WITH DILATED 'OLGI LAMELLAE '/ GRANULAR ENDOPLASMIC RETICULUM %2 AND MITOCHONDRIA WITH
TUBULAR CRISTAE 4HE ARROWHEADS INDICATE GAP JUNCTIONS BETWEEN THE FOLLICULAR CELL AND PROCESSES FROM THE OOCYTE 8
&ROM )WAMATSU ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
!BBREVIATIONS #), #/, INNER AND OUTER LAYERS OF THE ZONA PELLUCIDA 46 TRANSPORT VESICLES
/6!2)!. &/,,)#,%3
&IGURE $RAWINGS ILLUSTRATING THE MECHANICAL FUNCTION OF FOLLICULAR CELLS DURING OVULATION IN THE LAMPREY 0ETROMYZON
MARINUS WHERE A GENTLE STEADY CONSTRICTION EXTRUDES THE EGG FROM THE FOLLICLE 8 &ROM 9ORKE AND -C-ILLAN REPRO
DUCED WITH PERMISSION FROM THE 3OCIETY FOR THE 3TUDY OF 2EPRODUCTION )NC
! 3HORTLY AFTER THE RUPTURE OF THE FOLLICULAR AND THECAL LAYERS THE OOCYTE NUCLEUS HAS BECOME INDISTINGUISHABLE AND ADHESIVE
CELLS NEAR THE SITE OF RUPTURE ARE BREAKING DOWN IN A WAVE THAT PROGRESSES RAPIDLY AWAY FROM THIS CENTRE ! DEEPLY STAINING
AMORPHOUS MATERIAL HAS ACCUMULATED IN THE mUID OF OVULATION AND APICAL FOLLICULAR CELLS HAVE A WELL DEVELOPED SECRETORY
APPEARANCE &OLLICULAR CELLS SURROUNDING THE APICAL FOLLICULAR CELLS ARE BECOMING COLUMNAR
" 4HERE IS A CONTINUED INCREASE IN THE HEIGHT OF THE COLUMNAR FOLLICULAR CELLS DURING EARLY STAGES OF EMERGENCE OF THE EGG
!S THE EGG ENTERS THE EXTRAOVARIAN SPACE IT IS COVERED WITH THE REMNANTS OF THE ADHESIVE CELLS WHICH FORM THE ADHESIVE COAT
4HE FOLLICULAR CELLS AND THECA ARE PULLED BACK FROM THE RUPTURE ARROWS
# !T A MID STAGE IN EGG EMERGENCE FOLLICULAR CELLS NEAR THE APICAL END OF THE FOLLICLE BECOME COLUMNAR AND CREATE A CONSTRIC
TION THAT PINCHES OFF THE APICAL FOLLICULAR CELLS FORMING A SPHERE
$ 4HE WAVE OF ELONGATION CONTINUES TO TRANSFORM THE FOLLICULAR CELLS AND THEY BECOME SUCCESSIVELY MORE COLUMNAR 4HE CON
STRICTED PORTION OF THE FOLLICLE ARROW ELONGATES PUSHING THE EGG AHEAD 3TRANDS OF MATERIAL
DERIVED FROM THE mUID OF
OVULATION TRAIL FROM THE APICAL END OF THE EGG
!BBREVIATIONS !# ADHESIVE CELLS !& APICAL FOLLICULAR CELLS !- AMORPHOUS MATERIAL #& COLUMNAR FOLLICULAR CELLS % EGG
%/ EXTRAOVARIAN SPACE &/ mUID OF OVULATION )/ INTRAOVARIAN SPACE / OVARIAN WALL 3# ADHESIVE COAT 25 SITE OF RUPTURE
:0 ZONA PELLUCIDA
#(!04%2
/6!2)!. &/,,)#,%3
&IGURE %LECTRON MICROGRAPHS OF FREEZE
FRACTURE REPLICAS OF JUNCTIONS BETWEEN MESOTHELIAL CELLS FROM THE OVARY OF
THE ZEBRAlSH "RACHYDANIO RERIO &ROM +ESSEL 2OBERTS AND 4UNG REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE
%DITRICE
! ,ATTICE OF TIGHT JUNCTIONAL STRANDS 4* WITH INTERCALATED COMMUNICATING JUNCTIONS #* 8
" 4HERE IS AN ALMOST LINEAR ARRANGEMENT OF THE TIGHT JUNCTIONAL STRANDS 4* 4HE ARROWHEADS INDICATE MICROPINOCYTOTIC PITS
AND VESICLES 8
# !N ENLARGEMENT OF " TO ILLUSTRATE SHORT BARS " PARTICLES 0 AND PARTICLE FREE REGIONS ARROWHEADS 4HE BLACK ARROWS
INDICATE APPARENT FUSION OF SOME OF THE STRANDS ! SLIGHT ENLARGEMENT WHITE ARROWS OCCURS AT THE ENDS OF SOME BARS
4HE UPPER 0 AND 6 INDICATE MICROPINOCYTOTIC PITS AND VESICLES 8
#(!04%2
&IGURE 3CHEMATIC DIAGRAM OF THE FOLLICULAR WALL OF THE EASTERN BROOK TROUT 3ALVELINUS FONTINALIS %GG DIAMETER ABOUT
MM &ROM &LGEL B REPRODUCED WITH PERMISSION OF THE AUTHOR
!BBREVIATIONS "- MESOTHELIAL BASAL LAMINA "- BASAL LAMINA OF THE FOLLICULAR EPITHELIUM &% FOLLICULAR EPITHELIUM /%
OVARIAN MESOTHELIUM /0 OOPLASM 4& THECA :2% EXTERNAL REGION OF ZONA PELLUCIDA :2) INTERNAL REGION OF ZONA PELLUCIDA
/6!2)!. &/,,)#,%3
&IGURE -ICROGRAPHS OF SECTIONS OF THE OVARY OF THE PIPElSH 3YNGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF A TRANSVERSE SECTION OF AN ENTIRE OVARY DEPICTING VARIOUS STAGES OF OOCYTE DEVELOPMENT 4HE GERMINAL
RIDGE ARROWHEAD AND YOUNG DEVELOPING FOLLICLES HAVE CURLED TO PROTRUDE INTO THE OVARIAN LUMEN 4HE MATURE EDGE IS INDI
CATED BY THE DOTTED LINE OVERLYING THE LARGEST OOCYTES 4HE BOXED AREA IS ENLARGED IN " $ DORSAL 6 VENTRAL 8
" %NLARGEMENT OF BOXED REGION IN ! ! VASCULAR CONNECTIVE TISSUE STROMA lLLS THE SPACE BETWEEN ADJACENT FOLLICLES 4HE AR
ROWS INDICATE ARTERIOLES DISPERSED WITHIN THE CONNECTIVE TISSUE 8
# %LECTRON MICROGRAPH OF THE CONNECTIVE TISSUE STROMA CONSISTING OF COLLAGEN AND CONNECTIVE TISSUE CELLS
8
!BBREVIATIONS # COLLAGEN #4 CONNECTIVE TISSUE , OVARIAN LUMEN / OOCYTE /7 OVARIAN WALL
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF THE FOLLICULAR PERIPHERY IN THE OVARY OF THE PIPElSH 3YNGNATHUS SCOVELLI
&ROM "EGOVAC AND 7ALLACE REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HIS MICROGRAPH ILLUSTRATES THE LAYERS INTERPOSED BETWEEN THE OOCYTE AND THE LUMINAL EPITHELIUM 4HE THECAL LAYER CONSISTS
OF ATTENUATED lBROBLASTS AND IS WELL DEVELOPED 4HE FOLLICULAR EPITHELIUM CONSISTS OF A SIMPLE LAYER OF CUBOIDAL CELLS RESTING
ON A THICK BASAL LAMINA ARROWS 8
" 7HERE TWO FOLLICLES ABUT THE STROMA MAY BE EXTRUDED SO THAT A SINGLE THECA SANDWICHED BETWEEN TWO BASAL LAMINAE OF THE
FOLLICULAR EPITHELIA IS SHARED BETWEEN THEM 8
!BBREVIATIONS &# FOLLICULAR CELLS ,% LUMINAL EPITHELIUM / OOCYTE 4 THECA
/6!2)!. &/,,)#,%3
&IGURE -ICROGRAPHS OF THE OVARY OF THE PIPElSH 3YNGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE REPRODUCED
WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! )NDIA INK PREPARATIONS OF FRESH INTACT OVARIES DEMONSTRATING THE EXTENT OF THE LYMPHATIC NETWORK IN THE SPACES BETWEEN
FOLLICLES 4HE LYMPHATICS END ABRUPTLY AT THE EXTREME MATURE EDGES ARROWS AS EGGS % ARE VISIBLE IN THE OVARIAN LUMEN
4HE OVARY ON THE RIGHT DEMONSTRATES THE EXTENT OF LYMPHATICS AMONG EARLY FOLLICLES 8
" 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION SHOWING THE LYMPHATIC SPACE ,9 EXTENDING BETWEEN THE LATERAL BORDERS OF
ADJACENT YOUNG OOCYTES 8
# 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION SHOWING A TRIANGULAR LYMPHATIC SPACE ,9 BETWEEN ADJACENT EARLY DEVELOP
ING OOCYTES / AND THE OVARIAN WALL /7 ! DISTINCT ENDOTHELIAL CELL %# LINES THE LYMPHATIC SPACE 8
#(!04%2
&IGURE %LECTRON MICROGRAPHS FROM THE OVARY OF THE ZEBRAlSH "RACHYDANIO RERIO TO ILLUSTRATE FOLLICULAR CIRCULATION
&ROM +ESSEL 2OBERTS AND 4UNG REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! 4RANSMISSION ELECTRON MICROGRAPH OF THE FOLLICULAR ENVELOPE AND OOCYTE CORTEX EARLY IN OOGENESIS ! BLOOD VESSEL OF THE
THECA IS INTERPOSED BENEATH THE SEROSA 8
" 4RANSMISSION ELECTRON MICROGRAPH SHOWING A JUNCTION ARROWS BETWEEN TWO ENDOTHELIAL CELLS -ICROPINOCYTOTIC PITS AND
VESICLES ARE IDENTIlED BY ARROWHEADS IN BOTH SEROSAL AND ENDOTHELIAL CELLS 8
!BBREVIATIONS "6 BLOOD VESSEL #' CORTICAL GRANULE IN OOCYTE %R ERYTHROCYTE &# FOLLICULAR CELL 3E MESOTHELIAL OR SEROSAL
CELL 4H THECA 6% ZONA PELLUCIDA
# $ %LECTRON MICROGRAPHS OF FREEZE
FRACTURE REPLICAS OF MANY MICROPINOCYTOTIC PITS AND VESICLES &RACTURES THROUGH NECKS .
OF OPEN VESICLES 6 APPEAR AS CRATERS ON THE 0 FACE &RACTURE PLANES THAT INCLUDE BOTH OPEN PITS AND CONNECTED VESICLES ARE
IDENTIlED AT ARROWHEADS 4HESE lGURES MAY BE REPLICAS OF EITHER SEROSAL CELLS OR ENDOTHELIAL CELLS IT IS DIFlCULT TO DISTINGUISH
THESE CELLS IN FREEZE FRACTURE PREPARATIONS BUT PINOCYTOSIS IS SIMILARLY ACTIVE IN BOTH # 8 $ 8
/6!2)!. &/,,)#,%3
&IGURE %LECTRON MICROGRAPHS SHOWING THE DEVELOPMENT OF THE THECA DURING PREVITELLOGENESIS IN THE ZEBRAlSH "RACHY
DANIO RERIO 8 &ROM 5LRICH *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION
! 9OUNG OOCYTE M IN DIAMETER 4HECAL CELLS #4 ARE SEPARATED FROM THE SQUAMOUS FOLLICULAR EPITHELIUM #& BY A BASAL
LAMINA MB 4HE FOLLICULAR CELLS ARE CLOSELY APPLIED TO THE OOCYTE /V 4HE OOLEMMA MC SHOWS FEW INDENTATIONS
" !N OOCYTE M IN DIAMETER HAS PRODUCED MICROVILLI MV M IN LENGTH WHICH PRESS AGAINST THE FOLLICULAR CELLS /SMIO
PHILIC MATERIAL ARROWS HAS APPEARED BETWEEN THE MICROVILLI
# )N AN OOCYTE M IN DIAMETER THE MICROVILLI HAVE ELONGATED AND EXTENDED BENEATH THE FOLLICULAR EPITHELIUM 4HE FOLLICU
LAR CELLS HAVE BECOME THICKER AND THEIR CYTOPLASM IS RICH IN RIBOSOMES /SMIOPHILIC MATERIAL CONSTITUTES THE EXTERNAL LAYER
OF THE ZONA PELLUCIDA
$ -ICROVILLI CONTINUE TO ELONGATE IN AN OOCYTE M IN DIAMETER THEY FORM BUNDLES ARROWS BENEATH THE FOLLICULAR EPITHE
LIUM 4HE FOLLICULAR CELLS CONTAINING SEVERAL ORGANELLES CONTINUE TO THICKEN
!BBREVIATIONS #& FOLLICULAR EPITHELIUM #4 THECAL CELLS $ 'OLGI COMPLEX M MITOCHONDRION MB BASAL LAMINA MC OO
LEMMA MV MICROVILLI . NUCLEUS /V OOCYTE :RE EXTERNAL LAYER OF ZONA PELLUCIDA
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE SEA BASS $ICENTRARCHUS LABRAX
4HECAL CELLS #T ARE SEPARATED FROM THE FOLLICULAR EPITHELIUM #F BY A DOUBLE BASAL LAMINA ARROWS AND COLLAGENOUS lBRES
#OL 8 &ROM #APORICCIO AND #ONNES REPRODUCED WITH PERMISSION -ASSON %DITEUR
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE OVARY OF THE HAGlSH %PTATRETUS STOUTI SHOWING THE FOLLICU
LAR WALL DURING EARLY OOGENESIS 4HE OOCYTE /# IS SURROUNDED BY A DEEPLY STAINING FOLLICULAR LAYER '# 4HE THECA CONSISTS OF
POORLY DIFFERENTIATED CELLS 4# PROBABLY lBROBLASTS IN A CONNECTIVE TISSUE MATRIX #4 3QUAMOUS MESOTHELIAL CELLS %0 ABUT
THE COELOMIC CAVITY 8 &ROM 4SUNEKI AND 'ORBMAN REPRODUCED WITH KIND PERMISSION OF "LACKWELL 0UBLISHING
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE OVARY OF THE HAGlSH %PTATRETUS STOUTI SHOWING THE FOLLICU
LAR WALL DURING AN hINTERMEDIATEv STAGE OF OOGENESIS 4WO LAYERS CAN BE DISTINGUISHED IN THE THECA THE THECA EXTERNA &IGURE !
AND THE THECA INTERNA &IGURE " 8 &ROM 4SUNEKI AND 'ORBMAN REPRODUCED WITH KIND PERMISSION OF "LACKWELL
0UBLISHING
! 'RANULES ARE FORMING WITHIN THE 'OLGI COMPLEX OF A THECAL CELL
" ! lBROBLAST IN THE THECA INTERNA DISPLAYS CONSPICUOUS GRANULAR ENDOPLASMIC RETICULUM AND A LARGE LIPID
LIKE INCLUSION
!BBREVIATIONS "6 BLOOD VESSEL #$ COLLOID DROPLET #4 CONNECTIVE TISSUE %0 PERITONEAL EPITHELIUM OR MESOTHELIAL LAYER
&" lBROBLAST )3 INTERCELLULAR SPACE 2%2 GRANULAR ENDOPLASMIC RETICULUM 4# THECAL CELL
#(!04%2
&IGURE 3CHEMATIC DIAGRAMS ILLUSTRATING CHANGES IN THE THECA INTERNA DURING VITELLOGENESIS IN THE OVARY OF THE LAMPREY
,AMPETRA PLANERI &ROM "USSON
-ABILLOT B *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION
! $URING PREVITELLOGENESIS SOME lBROBLASTS BECOME mATTENED AGAINST THE BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM
" 4HESE CELLS SHORTEN AND THICKEN GRANULAR ENDOPLASMIC RETICULUM DEVELOPS WITHIN THEIR CYTOPLASM ,ARGE SPACES APPEAR
BETWEEN THE CELLS OF THE THECA INTERNA ACROSS WHICH THE CELLS EXTEND SLENDER PROCESSES !N EXTERNAL BASEMENT MEMBRANE
APPEARS
# !T THE ONSET OF VITELLOGENESIS STACKS OF GRANULAR ENDOPLASMIC RETICULUM APPEAR AT THE ENDS OF THE CELLS AND LIPID DROPLETS
APPEAR NEXT TO THE NUCLEUS
$ 4HE GRANULAR ENDOPLASMIC RETICULUM AND THE LIPID DROPLETS CONTINUE TO INCREASE DURING VITELLOGENESIS
% 4HE THECAL CELLS ONCE AGAIN BECOME mAT DURING LATE VITELLOGENESIS AND AT THE CLOSE OF VITELLOGENESIS 4HE LIPID DROPLETS BE
COME DIMINISHED AND THE ENDOPLASMIC RETICULUM ASSUMES AN AGRANULAR APPEARANCE ,ARGE APPARENTLY EMPTY INTERCELLULAR
SPACES SEPARATE THE THECAL CELLS
!BBREVIATIONS MBF BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM MBTI EXTERNAL BASEMENT MEMBRANE N NUCLEUS
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE PERIPHERAL REGIONS OF THE OVARIAN FOLLICLE OF THE LAMPREY
,AMPETRA PLANERI &ROM "USSON
-ABILLOT B *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION
! 6EGETAL POLE OF THE FOLLICLE AT THE BEGINNING OF VITELLOGENESIS 4HE ZONA PELLUCIDA CONSISTS OF A SINGLE LAYER )T IS COVERED
BY THE FOLLICULAR EPITHELIUM WHOSE CELLS ARE JOINED BY DESMOSOMES ARROW 4HE BASAL LAMINA OF THE FOLLICULAR EPITHELIUM
SEPARATES THE FOLLICLE FROM THE STROMA ! BASAL LAMINA SEPARATES THE SINGLE LAYER OF THE THECA INTERNA FROM THE VASCULAR CON
NECTIVE TISSUE OF THE THECA EXTERNA !NOTHER BASAL LAMINA SEPARATES THE THECA FROM THE COELOMIC EPITHELIUM MESOTHELIUM
COVERING THE OVARIAN LOBE 8
)NSET UPPER 4WO BASAL MEMBRANES ARROWS SEPARATE THE THECA INTERNA AND THE FOLLICULAR EPITHELIUM 8
)NSET LOWER $ETAIL OF THE PERITONEAL EPITHELIUM 4HE BORDER BETWEEN TWO EPITHELIAL CELLS IS DEEPLY INTERDIGITATED IT IS SEALED
APICALLY BY A TIGHT JUNCTION ARROW
#(!04%2
&IGURE #ONTINUED
" !T THE BEGINNING OF VITELLOGENESIS THE CYTOPLASM OF CELLS OF THE THECA INTERNA CUT PERPENDICULAR TO THEIR LONG AXIS IS VARIED
IN SOME THERE IS ONLY AGRANULAR ENDOPLASMIC RETICULUM ARROW AND 'OLGI COMPLEXES WHILE OTHERS CONTAIN LARGE LIPID DROP
LETS , NEAR PARALLEL CISTERNAE OF GRANULAR ENDOPLASMIC RETICULUM 4HE THECA INTERNA IS SEPARATED FROM THE FOLLICLE BY THE
FOLLICULAR BASAL MEMBRANE WHILE ITS OWN BASAL LAMINA BTI SEPARATES IT FROM THE THECA EXTERNA 4HIN EXTENSIONS OF FOLLICULAR
CELLS & ARE INTERPOSED BETWEEN THE ZONA PELLUCIDA AND THE FOLLICULAR BASAL LAMINA 8
/6!2)!. &/,,)#,%3
&IGURE #ONTINUED
# $URING INTENSE VITELLOGENESIS THIS FOLLICULAR CELL CONTAINS A HETEROGENEOUS COLLECTION OF SECRETION GRANULES lBROUS F
GRANULAR H AND ONE WITH DENSE GLOBULES DOUBLE ARROW 4HE BASAL MEMBRANE " OF THE FOLLICULAR CELL IS FAIRLY SMOOTH
AND IS SEPARATED FROM ITS BASAL LAMINA BY A UNIFORM SPACE -ANY MICROVILLI EXTEND FROM THE LATERAL , AND APICAL ! BOR
DERS THESE DO NOT PENETRATE THE ZONA PELLUCIDA 4HE THECA INTERNA CONSISTING OF A SINGLE LAYER OF SQUAMOUS CELLS SEPARATES
THE FOLLICLE FROM THE REST OF THE STROMA 8
!BBREVIATIONS CE PERITONEAL EPITHELIUM C COELOM #& FOLLICULAR CELL #0 ZONA PELLUCIDA $ 'OLGI COMPLEX %# COELOMIC
EPITHELIUM MESOTHELIUM %2 ENDOPLASMIC RETICULUM MBE BASAL LAMINA OF THE THECA EXTERNA MBF BASAL LAMINA OF THE FOL
LICULAR EPITHELIUM MBTI BASAL LAMINA OF THE THECA INTERNA . NUCLEUS /6 OOCYTE ST STROMA 4% THECA EXTERNA 4) THECA
INTERNA :0 ZONA PELLUCIDA
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF PREOVULATORY FOLLICLES OF THE GOLDlSH #ARASSIUS AURATUS
&ROM .AGAHAMA #HAN AND (OAR REPRODUCED WITH PERMISSION OF THE .2# 0RESS
! 4HE CONTRAST IS OBVIOUS BETWEEN A SPECIAL THECAL 3# CELL AND AN ORDINARY CELL OF THE THECA INTERNA 4I# 3QUAMOUS CELLS
OF THE THECA EXTERNA 4E# ENCLOSE THE FOLLICLE 4HE FOLLICULAR BASAL LAMINA "- SEPARATES THE THECA FROM THE FOLLICULAR
EPITHELIUM '# :2 ZONA PELLUCIDA 8
" 4HIS SECTION SHOWS A CELL OF THE THECA EXTERNA 4E# AND A SPECIAL THECAL CELL 3# CONTAINING A MODERATE AMOUNT OF AGRANU
LAR ENDOPLASMIC RETICULUM AND MANY ELECTRON
DENSE MITOCHONDRIA - WITH TUBULAR CRISTAE 8
# 4HE CYTOPLASM OF A SPECIAL THECAL CELL 3# IS CHARACTERIZED BY LARGE MITOCHONDRIA - WITH TUBULAR CRISTAE AND THE PRESENCE
OF AGRANULAR ENDOPLASMIC RETICULUM S%2 8
/6!2)!. &/,,)#,%3
&IGURE 0HOTOMICROGRAPHS ! $ AND TRANSMISSION ELECTRON MICROGRAPHS " # % & OF SECTIONS OF THE DEVELOPING FOL
LICLE DURING EARLY VITELLOGENESIS IN TILAPIA /REOCHROMIS NILOTICUS &ROM .AKAMURA 3PECKER AND .AGAHAMA REPRODUCED
WITH PERMISSION FROM 3PRINGER 6ERLAG
! #LUSTERS OF STEROID PRODUCING CELLS ARROWS ARE SEEN NEAR THE OVARIAN ARTERY AND VEIN IN THIS SECTION OF THE OVARY DAYS
AFTER HATCHING 8 "AR M
" #LUSTERS OF STEROID PRODUCING CELLS IN AN OVARY DAYS AFTER HATCHING 8 "AR M
# #LUSTERS OF STEROID PRODUCING CELLS IN THE INTERSTITIAL REGION BETWEEN OOCYTES IN AN OVARY DAYS AFTER HATCHING 8
"AR M
#(!04%2
&IGURE #ONTINUED
$ #LUSTERS OF STEROID PRODUCING CELLS ARROWS ARE DISTRIBUTED AMONG OOCYTES AT THE EARLY VITELLOGENIC AND PERINUCLEOLUS STAGES
DAYS AFTER HATCHING 8 "AR M
% ! CLUSTER OF STEROID PRODUCING CELLS ENCAPSULATES AN OOCYTE DURING EARLY VITELLOGENESIS IN AN OVARY DAYS AFTER HATCHING
8 "AR M
& 4HE FOLLICULAR EPITHELIUM AND STEROID PRODUCING CELLS IN THE THECA OF A VITELLOGENIC OOCYTE DAYS AFTER HATCHING 8
"AR M
!BBREVIATIONS ! ARTERY # CAPILLARY ' FOLLICULAR EPITHELIAL CELL .& NERVE lBRE / OOCYTE /# OVARIAN CAVITY 3 STEROID
PRODUCING CELL 6 VEIN
/6!2)!. &/,,)#,%3
&IGURE "UNDLES OF NERVE lBRES PRESUMABLY AUTONOMIC COURSE AMONG THE YOLKY FOLLICLES AND STEROID PRODUCING CELLS OF
TILAPIA /REOCHROMIS NILOTICA &ROM .AKAMURA 3PECKER AND .AGAHAMA REPRODUCED WITH PERMISSION FROM THE :OOLOGI
CAL 3OCIETY OF *APAN
! $ 4RANSMISSION ELECTRON MICROGRAPHS SHOWING THE DISTRIBUTION OF NERVE TERMINALS WITHIN THE OVARY
! !XON TERMINALS PACKED WITH SYNAPTIC VESICLES ARROW REST ON THE SURFACE OF STEROID PRODUCING CELLS 8
" !XONS INVADE THE NARROW SPACE BETWEEN STEROID PRODUCING CELLS AND TERMINATE ARROW ON THE SURFACE OF ONE OF THESE
8
# !N AXON TERMINAL ARROW IS SEEN NEAR A STEROID PRODUCING CELL IN THE THECA 8
$ $ETAIL OF THE AXON TERMINAL SHOWN AT THE ARROW IN &IGURE # )T CONTAINS MANY SYNAPTIC VESICLES AND DENSE CORED VESICLES
8
#(!04%2
&IGURE #ONTINUED
% 0HOTOMICROGRAPH OF AXON TERMINALS ARROWS STAINED WITH SILVER DISTRIBUTED WITHIN A CLUSTER OF STEROID PRODUCING CELLS
8
!BBREVIATIONS ", BASAL LAMINA "6 BLOOD VESSEL '# FOLLICULAR CELL ', FOLLICULAR EPITHELIUM 30# STEROID PRODUCING CELL
4, THECAL LAYER 9 YOLK
/6!2)!. &/,,)#,%3
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE THECAL LAYERS IN THE POSTOVULATORY OVARY OF THE TROUT
3ALMO GAIRDNERI &ROM 3ZLLSI *ALABERT AND "RETON REPRODUCED WITH PERMISSION OF ).2! 0ARIS
! ,AYERS OF SMOOTH MUSCLE
LIKE CELLS M OF THE THECA ALTERNATE WITH LAYERS OF COLLAGEN lBRES C 3MALL GROUPINGS OF OR
GANELLES CONGREGATE NEAR THE NUCLEAR POLES OF THE MUSCLE CELLS THE REST OF THE CYTOPLASM IS OCCUPIED BY THIN lLAMENTS
4HE FOLLICULAR BASAL LAMINA ", SEPARATES THE THECA FROM THE FOLLICULAR EPITHELIUM 8
" 4HE PUTATIVE MUSCLE lBRE CONTAINS lLAMENTS TO NM IN DIAMETER AND DISPLAYS ACTIVE PINOCYTOSIS TYPICAL OF SMOOTH
MUSCLE 8
#(!04%2
&IGURE #ONTINUED
# 4HE THICK BASAL LAMINA ", BETWEEN THE FOLLICULAR CELLS CENTRE AND THE THECA IS EXTENSIVELY FOLDED 8
$ 7ITHIN A FEW HOURS OF OVULATION STELLATE THECAL CELLS ISOLATE LARGE BUNDLES OF COLLAGEN lBRILS 4WO SMALL INTERNALIZED
ISOLATED PHAGOCYTIC VESICLES CONTAINING A FEW COLLAGEN lBRILS ARE SEEN 8
#(!04%2
/65,!4)/.
)NTRODUCTION
#ARASSIUS AURATUS +AGAWA AND .AGAHAMA
HYDROCORTISONE /RYZIAS LATIPES 0ENDERGRASS
AND 3CHROEDER OR THE MATURATION INDUCING STE
ROIDS ` TRIHYDROXY PREGNENE ONE ` 3
AND ` DIHYDROXY PREGNENE ONE ` 0
#YNOSCION NEBULOSUS 0INTER AND 4HOMAS TO
THE MEDIUM
3OME TIME PRIOR TO OVULATION IN &UNDULUS HETERO
CLITUS EACH FOLLICLE ESTABLISHES A CLOSE RELATIONSHIP
WITH THE LUMINAL SURFACE OF THE OVARY IN A LOCALIZED
NEARLY CIRCULAR SPOT "RUMMETT $UMONT AND ,ARKIN
! FUSION BETWEEN THE BASEMENT MEMBRANES
OF THE FOLLICULAR CELLS AND LUMINAL EPITHELIUM AP
PEARS TO OCCUR EXCLUDING BLOOD VESSELS FROM THE AREA
&IGURE 4HE SQUAMOUS LUMINAL MESOTHELIAL CELLS
COVERING THIS AREA BECOME INCREASINGLY mAT AS THE
FOLLICLE MATURES AND IT IS PRESUMED THAT OVULATION
OCCURS AT THIS SITE 4HIS AVASCULAR AREA IS SURROUNDED
BY A RAISED LIP OF CELLS CONTAINING A RING SHAPED VES
SEL THAT COLLECTS BLOOD FROM CAPILLARIES IN THE FOLLICULAR
THECA &IGURES ! # 4HE MATURE EGG OF &UNDU
LUS IS OVULATED INTO THE LUMEN OF THE OVARY AND PASSES
FROM THERE TO THE POSTERIOR NONGERMINAL PORTION OF
THE OVARY THE /6)3!#
5LTRASTRUCTURAL STUDIES HAVE REVEALED THAT MICROVILLI
FROM BOTH FOLLICULAR CELLS AND THE OOCYTE WITHDRAW
FROM THE ZONA PELLUCIDA NEAR THE TIME OF OVULATION AND
THAT A WIDE SPACE FORMS BETWEEN THE ZONA PELLUCIDA
AND THE FOLLICULAR CELLS &IGURE &LGEL B
(IROSE )WAMATSU AND /HTA 4HE MECHA
NISM DIRECTING THIS INTERRUPTION OF FOLLICLE OOCYTE COM
MUNICATION PRIOR TO OVULATION IS UNKNOWN
4HE PRESENCE OF hOVULATION INDUCING ENZYMESv HAS
BEEN POSTULATED FOR SEVERAL lSH 4HESE ARE THOUGHT TO
BREAK DOWN COLLAGEN THEREBY WEAKENING THE FOLLICULAR
WALL IN PREPARATION FOR ITS RUPTURE )SOLATED FOLLICLES OF
!FTER COMPLETION OF THE lRST MEIOTIC DIVISION A RUP
TURE THE 34)'-! DEVELOPS IN A SPECIlC AREA OF THE FOL
LICULAR WALL AND THE MATURE OOCYTES ARE RELEASED INTO
THE COELOM OR OVARIAN CAVITY BY THE PROCESS OF OVULA
TION .AGAHAMA -EIOSIS CONTINUES UP TO THE
SECOND MEIOTIC METAPHASE AND AT THIS TIME THE EGGS
ARE READY FOR FERTILIZATION 3EVERAL STEPS ARE INVOLVED
IN THIS RELEASE SEPARATION OF THE VITELLINE ENVELOPE AND
FOLLICULAR EPITHELIUM AS MICROVILLI FROM BOTH SIDES BE
COME DETACHED ENZYMATIC DEGRADATION AND RUPTURE OF
THE FOLLICLE AND EXPULSION OF THE OOCYTE 4HE MOTIVE
FORCE EXPELLING THE OOCYTE HAS BEEN ATTRIBUTED VARI
OUSLY TO THE FORMATION OF mUIDS WITHIN THE FOLLICLE TO
SWELLING OF THE OOCYTE AND TO CONTRACTIONS OF THE FOL
LICULAR WALL )N SOME VIVIPAROUS SPECIES FERTILIZATION
AND EMBRYOLOGICAL DEVELOPMENT TAKE PLACE WITHIN THE
FOLLICLE SO THAT NO OVULATION OCCURS 3UBSEQUENT RE
LEASE OF THE EMBRYOS FROM THEIR FOLLICULAR SANCTUARY IS
SOMETIMES REFERRED TO AS hOVULATIONv EG 6ENKATESH
4AN AND ,AM A B BUT THIS USAGE SEEMS INAPPRO
PRIATE AND WILL NOT BE USED IN THIS TEXT
6ARIOUS ASPECTS OF OVULATION HAVE BEEN STUDIED DUR
ING ITS NORMAL OCCURRENCE IN THE REPRODUCTIVE CYCLE OF
INTACT lSH #ARASSIUS AURATUS .AGAHAMA #HAN AND
(OAR 0ETROMYZON MARINUS 9ORKE AND -C-IL
LAN 3ALVELINUS LEUCOMAENIS +AGAWA 4AKANO
AND .AGAHAMA (OWEVER SINCE THIS EVENT OC
CURS OVER A BRIEF PERIOD OF TIME IT HAS OFTEN PROVED
CONVENIENT TO INDUCE OVULATION IN FEMALES BY MA
NIPULATIONS OF DAY LENGTH /RYZIAS LATIPES (IROSE
+AGAWA AND 4AKANO )WAMATSU AND /HTA
A OR BY INJECTIONS OF HORMONES SUCH AS HUMAN
CHORIONIC GONADOTROPIN (#' 0LECOGLOSSUS ALTIVE
LIS (IROSE AND )SHIDA ,IMANDA YOKOHOMAE
/SHIRO AND (IBIYA )N FOLLICLES ISOLATED FROM
GRAVID FEMALES OVULATION HAS BEEN INDUCED BY ADDI
TIONS OF PROSTAGLANDIN &_ 3ALMO GAIRDNERI *ALABERT
AND 3ZLLSI 3ZLLSI *ALABERT AND "RETON
0ETER AND 9U HAVE PRESENTED AN EXTENSIVE REVIEW SUMMA
RIZING THE MAJOR ENVIRONMENTAL AND HORMONAL FACTORS CONTROLLING
OVULATION IN TELEOSTS
#(!04%2
THE LOACH -ISGURNUS ANGUILLICAUDATUS PRODUCE PRO
TEASES IMMEDIATELY BEFORE INDUCED OVULATION /S
HIRO AND (IBIYA 3EVERAL LYTIC ENZYMES
CHYMOTRYPSIN AMINOPEPTIDASES ACID AND ALKALINE
PHOSPHATASES VARIOUS ESTERASES AND GLYCOSIDASES
WERE FOUND IN THE COELOMIC mUID OF THE TROUT 3ALMO
GAIRDNERI WITHIN HR OF OVULATION BUT NO COLLAGE
NASE COULD BE DETECTED 3ZLLSI *ALABERT AND "RETON
)N ADDITION COLLAGENASE WAS SOUGHT WITHOUT
SUCCESS IN EXTRACTS OF PRE AND POSTOVULATORY OVARIES
!CTINOMYCIN $ AND CYCLOHEXAMIDE INDUCED BLOCK
AGE OF STEROID INDUCED OVULATION IN ISOLATED FOLLICLES
OF YELLOW PERCH 0ERCA mAVESCENS PRESUMABLY BY IN
HIBITING PRODUCTION OF THE PROTEOLYTIC ENZYMES NEEDED
TO DETACH THE OOCYTE FROM THE FOLLICLE AND WEAKEN THE
FOLLICULAR WALL 4HEOFAN AND 'OETZ -ORE RE
CENTLY COLLAGENOLYTIC METALLO PROTEASES HAVE BEEN
DEMONSTRATED IN FOLLICULAR WALLS OF YELLOW PERCH AND
BROOK TROUT 3ALVELINUS FONTINALIS AROUND THE TIME OF
OVULATION "ERNDTSON AND 'OETZ )NCREAS
ES IN THE NUMBERS OF LYSOSOMES WITHIN FOLLICULAR CELLS
NEAR THE TIME OF OVULATION HAVE PROVIDED MORPHOLOGI
CAL EVIDENCE FOR THE PRESENCE OF HYDROLYTIC ENZYMES IN
THESE CELLS 9AMAMOTO AND 9AMAZAKI +AGAWA
AND 4AKANO +AGAWA 4AKANO AND .AGAHAMA
!N INCREASE IN LYSOSOME LIKE BODIES WAS ALSO
OBSERVED IN FOLLICULAR CELLS OF CULTURED FOLLICLES OF THE
MEDAKA JUST BEFORE OVULATION WAS EXPECTED TO OCCUR
&IGURE )WAMATSU AND /HTA A
)T HAS BEEN SUGGESTED THAT THE ACCUMULATION OF
mUID WITHIN THE FOLLICLE COULD APPLY GENTLE PRESSURE
TO EXPEL THE OOCYTE AS WELL AS LUBRICATING ITS PASSAGE
!S THE TIME OF OVULATION APPROACHES IN THE LAMPREY
0ETROMYZON MARINUS THERE IS AN ACCUMULATION OF &,5)$
/& /65,!4)/. BETWEEN THE VITELLINE ENVELOPE AND THE
FOLLICULAR EPITHELIUM IN THE APICAL REGIONS OF THE FOL
LICLE &IGURE ,EWIS AND -C-ILLAN 9ORKE
AND -C-ILLAN !CID AND NEUTRAL MUCOPLYSAC
CHARIDES PRESENT IN THE FOLLICULAR CELLS THAT DISTINT
EGRATE AT OVULATION MAY PARTICIPATE IN THIS PROCESS
AND IT IS SUGGESTED THAT ENZYMATIC BREAKDOWN OF ACID
MUCOPOLYSACCHARIDES MAY CAUSE THE OSMOTIC UPTAKE
OF WATER CAUSING SWELLING OF THE NEUTRAL MUCOPOLY
SACCHARIDES ,ARSEN 4HERE WAS A GREAT INmUX
OF WATER INTO OVARIES OF AYU 0LECOGLOSSUS ALTIVELIS
AND PLAICE ,IMANDA YOKOHOMAE JUST PRIOR TO OVU
LATION THAT WAS INDUCED BY INJECTIONS OF HORMONES
(IROSE AND )SHIDA /SHIRO AND (IBIYA
-OST OF THE WATER WAS ABSORBED BY FULLY GROWN YOLKY
OOCYTES THAT OVULATED SOON AFTER AND IT WAS SUGGESTED
THAT ABRUPT ABSORPTION OF WATER CAUSES RUPTURE OF THE
RIPENING OOCYTES
4HE EXPULSION OF THE EGG DURING OVULATION AT LEAST
IN THE LAMPREY 0ETROMYZON MARINUS APPEARS TO RESULT
FROM GENTLE CONTRACTIONS PRODUCED BY CHANGES IN
SHAPE OF THE FOLLICULAR CELLS &IGURE 9ORKE AND
-C-ILLAN !T THE lRST SIGN OF IMMINENT OVULA
TION A FEW APICAL FOLLICULAR CELLS ENLARGE AND ASSUME
A SECRETORY APPEARANCE &IGURES ! " AND !
4HESE CELLS PRODUCE THE mUID OF OVULATION THAT AC
CUMULATES BETWEEN THE ZONA PELLUCIDA AND FOLLICULAR
CELLS FORMING A HOLLOW MOUND NEAR THE APICAL POLE
,EWIS AND -C-ILLAN 9ORKE AND -C-ILLAN
-ICROVILLI FROM THE OOCYTE WITHDRAW FROM THEIR
CANALICULI AND A 0%2)6)4%,,).% 30!#% APPEARS BETWEEN
THE OOLEMMA AND THE VITELLINE ENVELOPE &IGURE !
!S OVULATION BEGINS THE FOLLICULAR CELLS CHANGE SHAPE
STARTING AT THIS mUID
lLLED END OF THE FOLLICLE FORMING
A HOLLOW SLEEVE OF COLUMNAR CELLS SURMOUNTED BY A
HOLLOW BALL OF mATTER FOLLICULAR CELLS AT ITS DISTAL END
&IGURES # $ AND 4HIS CHANGE IN SHAPE CON
STRICTS THE FOLLICLE AT ONE END THEREBY PUSHING THE OO
CYTE THROUGH AN APICAL RUPTURE WHICH APPEARS AT ABOUT
THE SAME TIME )NDICATIVE OF THE REDUCTION IN AREA OF
THE FOLLICULAR EPITHELIUM IS THE PROGRESSIVE APPEARANCE
OF CONVOLUTIONS IN ITS BASEMENT MEMBRANE WHERE THE
CELLS BECOME TALLER &IGURE " 4HE PRESENCE OF A
WELL
DEVELOPED lBROUS CYTOSKELETON WITHIN THE APICAL
FOLLICULAR CELLS AND ADHAERENS JUNCTIONS BETWEEN THEM
ENHANCES THE CONCEPT OF GENTLE PRESSURE PRODUCED BY
THESE CELLS 4HE EXPULSION OF THE EGG IS LUBRICATED BY
SLIPPERY mUIDS DERIVED FROM THE mUID OF OVULATION AND
FROM THE AUTOLYSIS OF ADHESIVE CELLS 4HE GELATINOUS mUID
OF OVULATION MOULDED BY THIS STOCKING CAP OF FOLLICULAR
CELLS PERSISTS ON THE EGG AFTER OVULATION AND CONSTITUTES
THE STICKY mUFFY !0)#!, 45&4 THAT APPEARS TO ORIENT THE
SPERMATOZOON FOR ITS PENETRATION OF THE CHORION THERE
IS NO MICROPYLE IN EGGS OF THE LAMPREY +ILLE
4HIS TUFT SHRINKS CONSIDERABLY WITH THE lXATIVES USED
FOR MICROSCOPY 9ORKE AND -C-ILLAN
4HE PREOVULATORY CHANGES IN THE FOLLICULAR EPITHE
LIUM OF THE LAMPREY ARE ACCOMPANIED BY DEGENERA
TIVE CHANGES IN THE THECA OVERLYING THE ADHESIVE CELLS
ADJACENT TO THE COELOM 9ORKE AND -C-ILLAN
!REAS OF DISRUPTION APPEAR IN THE COLLAGENOUS MATRIX
OFTEN IN ASSOCIATION WITH VACUOLATED CYTOPLASMIC EXTEN
SIONS OF A lBROBLAST 4HIS DEGENERATION IS ACCOMPANIED
BY AN INVASION OF MACROPHAGES FROM BLOOD VESSELS IN
THE AREA !UTOLYSIS OF THE THECA RESULTS IN THE RUPTURE OF
THE FOLLICLE IN AN AREA OVERLYING THE DBRIS OF THE ADHE
/65,!4)/.
SIVE CELLS AND BORDERING DIRECTLY ON THE COELOM &IGURE
! 4HUS FREED THE EGG EMERGES INTO THE COELOM
#ONTRACTIONS OF THE THECA ASSIST OVULATION IN SEVERAL
TELEOSTS 4HE THECA BEHAVES PHYSIOLOGICALLY LIKE SMOOTH
MUSCLE WHOSE CONTRACTIONS CAN BE EVOKED IN VITRO BY
THE ADDITION OF PROSTAGLANDIN &_ 3ZLLSI *ALABERT
AND "RETON 4HECAL CELLS OF SEVERAL SPECIES RE
SEMBLE SMOOTH MUSCLE CELLS DISPLAYING ABUNDANT MI
CROlLAMENTS TO NM AND PINOCYTOTIC VESICLES PRIOR
TO OVULATION &IGURES ! " 3ZLLSI AND *ALABERT
0ENDERGRASS AND 3CHROEDER .AGAHAMA
#HAN AND (OAR 3ZLLSI *ALABERT AND "RETON
)N SOME SPECIES HOWEVER THE DENSE BODIES AND
PINOCYTOTIC VESICLES CHARACTERISTIC OF SMOOTH MUSCLE
HAVE NOT BEEN SEEN 0HYSIOLOGICAL EVIDENCE FOR CON
TRACTILITY OF THE MICROlLAMENTS OF THE THECAL CELLS HAS
BEEN PROVIDED CYTOCHALASIN " WHICH BLOCKS POLYM
ERIZATION OF ACTIN lLAMENTS THEREBY PARALYSING MANY
KINDS OF CELLULAR MOVEMENT COMPLETELY AND REVERSIBLY
INHIBITS IN VITRO OVULATION OF MEDAKA AND TROUT OOCYTES
*ALABERT AND 3ZLLSI 3CHROEDER AND 0ENDER
GRASS AND AGENTS THAT BLOCK #A INmUX NE
CESSARY FOR MUSCULAR CONTRACTION INHIBIT OVULATION OF
TROUT OOCYTES IN VITRO *ALABERT AND 3ZLLSI
4HE 02/34!',!.$).3 ARE A GROUP OF
CARBON FATTY
ACIDS CONTAINING A
CARBON RING THEY ARE SHORT
LIVED
AND AFFECT A WIDE VARIETY OF PHYSIOLOGICAL PROCESSES BY
ACTING AS LOCAL HORMONES 4HEY APPEAR TO PLAY A SIGNIF
ICANT ROLE IN OVULATION IN OVIPAROUS TELEOSTS ALTHOUGH
THE EFFECTIVE PROSTAGLANDINS VARY FROM SPECIES TO SPE
CIES *ALABERT 'OETZ AND 4HEOFAN 'OETZ
ET AL "ERNDTSON 'OETZ AND $UMAN
'OETZ ET AL A B )N OVIPAROUS TELEOSTS WHERE
OVULATION IMMEDIATELY FOLLOWS OOCYTE MATURATION
FOLLICLES SYNTHESIZE LARGE AMOUNTS OF PROSTAGLANDINS
DURING OOCYTE MATURATION AND OVULATION "ERNDTSON
AND 'OETZ "ERNDTSON ET AL A 'OETZ ET
AL B "Y CONTRAST IN THE VIVIPAROUS GUPPY 0OE
CILIA RETICULATA WHERE THE FOETUS DEVELOPS WITHIN THE
FOLLICLE AND IS RELEASED A CONSIDERABLE TIME LATER PRO
DUCTION OF PROSTAGLANDINS BY FOLLICLES IS LOW DURING
OOCYTE GROWTH MATURATION AND GESTATION IT INCREASES
SIGNIlCANTLY IN MID AND LATE GESTATION 4HIS DELAY IN
SYNTHESIS MAY ARREST OVULATION THEREBY FACILITATING
INTRAFOLLICULAR FERTILIZATION AND GESTATION 6ENKATESH
4AN AND ,AM B 3EVERAL TISSUE COMPONENTS
WITHIN THE OVARY OF THE BROOK TROUT 3ALVELINUS FONTINA
LIS SYNTHESIZE PRIMARY PROSTAGLANDINS BUT DIFFER IN THEIR
CAPACITY TO PRODUCE % AND & PROSTAGLANDINS 'OETZ ET
AL B !LTHOUGH FOLLICULAR WALLS SYNTHE
SIZE SMALL AMOUNTS OF 0'% AND 0'&_ ESPECIALLY IN
POSTOVULATORY TISSUE THE GREATEST SYNTHESIS OCCURS IN
TISSUES OUTSIDE THE MATURE FOLLICLES PREDOMINANTLY OF
0'% 4HIS EXTRAFOLLICULAR TISSUE CONSISTS OF IMMATURE
FOLLICLES AND STROMAL TISSUE INCUBATED SEPARATELY THE
STROMAL TISSUE SYNTHESIZES 0'% WHILE THE IMMATURE
FOLLICLES SYNTHESIZE 0'&_
!TRETIC &OLLICLES 0OSTOVULATORY &OLLICLES
AND #ORPORA ,UTEA
%GGLESS FOLLICLES ARE OFTEN SEEN WITHIN THE OVARY OF
lSH 4HEY MAY ARISE EITHER BY ATRESIA DEGENERATION
OF A DEVELOPING FOLLICLE OR BY THE EXPULSION OF THE EGG
DURING OVULATION !42%4)# AND 0/34/65,!4/29 &/,,)
#,%3 HAVE LONG ATTRACTED THE ATTENTION OF ENDOCRINOLO
GISTS WHO HAVE SUSPECTED THEM AS A POSSIBLE SOURCE
OF HORMONES ASSOCIATED WITH REPRODUCTION "ALL
(OAR "ROWNING +OSMATH 0ATZNER AND
!DAM B 4HIS INTEREST HAS BEEN REmECTED IN THE
LITERATURE BY FREQUENT USE OF THE TERM hCORPUS LUTEUMv
IMPLYING THE PRESENCE OF AN ENDOCRINE GLAND THAT SE
CRETES STEROID HORMONES AND PLAYS A ROLE IN REPRODUC
TION )N THE PRESENT WORK THE TERM !42%4)# &/,,)#,%
WILL BE USED FOR FOLLICLES IN WHICH THE EGG IS OBVIOUSLY
UNDERGOING DEGENERATION 0/34/65,!4/29 &/,,)#,% FOR
EMPTY FOLLICLES PRODUCED BY THE EXPULSION OF AN EGG
AND #/2053 ,54%5- FOR THE RICHLY VASCULAR FOLLICULAR
REMNANT WHOSE ORIGINS WHETHER BY ATRESIA OR OVULA
TION CANNOT BE DETERMINED
!42%4)# &/,,)#,%3
!42%4)# &/,,)#,%3 OR #/20/2! !42%4)#! RESULT FROM DE
GENERATION OF AN OOCYTE AND ITS RESORPTION BY PHAGOCY
TOSIS THIS PROCESS IS !42%3)! &OLLICULAR ATRESIA OCCURS
WIDELY IN THE OVARIES OF VERTEBRATES AND MAY OCCUR AT
ANY STAGE IN FOLLICULAR DEVELOPMENT (ISAW AND (ISAW
$ODD )NDEED ATRESIA HAS BEEN DESCRIBED
IN THE PRIMORDIAL GERM CELLS OF THE INDIFFERENT GONAD
OF THE MEDAKA /RYZIAS LATIPES &IGURE (OGAN
)T IS NOT KNOWN WHY SOME FOLLICLES ARE ABLE TO
DEVELOP TO OVULATION WHILE THEIR NEIGHBOURS UNDERGO
DEGENERATION
4HE ONSET OF ATRESIA HAS BEEN SAID TO BE UNRELATED
TO AGE STAGE OF THE REPRODUCTIVE CYCLE ENVIRONMEN
TAL CONDITIONS SEASON TEMPERATURE LIGHT AVAILABILITY
OF FOOD ETC AND THE GENERAL HEALTH OF THE INDIVIDUAL
ANIMAL 3AIDAPUR ALTHOUGH EXPERIMENTS WITH
CAPTIVE !TLANTIC COD 'ADUS MORHUA SHOW AN INCREASE
#(!04%2
IN THE INCIDENCE OF ATRESIA IN VITELLOGENIC OOCYTES WITH
DECREASED FEEDING LEVELS +JESBU ET AL -ASS
ATRESIA OF MATURING OOCYTES IN WILD STOCKS OF !TLANTIC
COD HAS BEEN ATTRIBUTED TO SEVERE MALNUTRITION DURING
SOME CRITICAL PERIOD FOR OVARIAN GROWTH RESULTING IN
A FAILURE TO SPAWN OR hSKIPPED SPAWNINGv IN MOST FE
MALES DURING 2IDEOUT "URTON AND 2OSE
)T IS SUGGESTED THAT THIS FAILURE MAY HAVE CONTRIBUTED
TO THE CURRENT LACK OF RECRUITMENT IN NORTH !TLANTIC
COD STOCKS
!LTHOUGH ATRESIA MAY AFFECT THE OOCYTE AT ANY STAGE
OF DEVELOPMENT IT IS DESCRIBED MORE FREQUENTLY IN MA
TURING AND UNOVULATED MATURE OOCYTES 2ASTOGI
4HE APPARENT RARITY OF SMALL ATRETIC FOLLICLES MAY BE
DUE TO TWO FACTORS SMALL FOLLICLES TAKE A SHORTER TIME
THAN MATURE FOLLICLES TO DISAPPEAR AND BEING SMALLER
APPEAR IN FEWER MICROSCOPIC SECTIONS !TRESIA OF SMALL
FOLLICLES IS DESCRIBED IN SEVERAL SPECIES OF ELASMO
BRANCHS (ISAW AND (ISAW /VA CONTAINING
NO YOLK APPARENTLY UNDERGO SIMPLE ABSORPTION 4HE
CLEAR mUID CONTENT OF THE OVUM DECREASES THE WALLS
OF THE FOLLICLE COLLAPSE AND THE FOLLICULAR LAYER ATRO
PHIES AND DISINTEGRATES )N SLIGHTLY LARGER FOLLICLES IN
WHICH SMALL AMOUNTS OF YOLK HAVE BEEN DEPOSITED
SECRETION OF YOLK CEASES AND THE FOLLICULAR EPITHELIUM
INCREASES IN THICKNESS BY ELONGATION AND SWELLING OF
CELLS WHICH MAY REMAIN ATTACHED TO THEIR BASEMENT
MEMBRANE &OLLICULAR CELLS lLL WITH VACUOLES AND THE
VITELLINE ENVELOPE DISAPPEARS 9OLK GRANULES LIBERATED
BY DISINTEGRATION OF THE OVUM AS WELL AS DBRIS FROM
THE DEGENERATING OVUM ARE REMOVED BY FOLLICULAR CELLS
WHICH BECOME PHAGOCYTIC
4HE lRST SIGN OF ATRESIA IN SMALL YOLK
FREE OOCYTES
OF THE FRESHWATER MUD EEL !MPHIPNOUS CUCHIA IS THE
DISAPPEARANCE OF THE NUCLEAR MEMBRANE AND DISINTE
GRATION OF CHROMATIN 2ASTOGI 4HE OOLEMMA
IS THROWN INTO FOLDS INVADING THE DECOMPOSED OO
PLASM 4HE FOLLICULAR EPITHELIUM REMAINS SINGLE
LAY
ERED AND SHOWS NO HYPERPLASIA 4HE THECA THICKENS
AND BECOMES MORE VASCULAR &OLLICULAR CELLS INVADE THE
OOCYTE FUNCTIONING AS PHAGOCYTES THIS INVASION IS FOL
LOWED BY THAT OF VASCULAR THECAL TISSUE %VENTUALLY THE
OOLEMMA AND OOPLASM ARE REMOVED 4HE PHAGOCYTES
BECOME PYCNOTIC AND ARE SUSPENDED IN A MESHWORK
OF lBROUS THECAL MATERIAL 4HIS MASS SHOWS NO SIGN OF
SECRETORY ACTIVITY
)N FOLLICULAR ATRESIA OF YOLKY FOLLICLES THE SEQUENCE
OF EVENTS IS SIMILAR IN MOST lSH #9#,/3/-%3 ,EWIS
AND -C-ILLAN %,!3-/"2!.#(3 (ISAW AND (I
SAW #HIEFl ,ANCE AND #ALLARD 4E
7INKEL &ASANO 0IERANTONI AND #HIEFl
#HIEFl "ACCARI ET AL 4%,%/343 "RETSCHNEIDER
AND $UYVEN DE 7IT 2AI #HAN 7RIGHT
AND 0HILLIPS 0ANT 7IEBE 2ASTOGI
3HRIVASTAVA ,AMBERT B VAN DEN
(URK AND 0EUTE "ABU AND .AIR -IRANDA
ET AL )N EARLY STAGES THE FOLLICULAR CELLS PROLIF
ERATE AGGRESSIVELY FRAGMENT THE VITELLINE ENVELOPE AND
INVADE THE OOCYTE REMOVING ITS CONTENTS BY PHAGOCYTO
SIS &IGURE !S THE OOCYTE DISINTEGRATES THERE IS A
FOLDING AND COLLAPSE OF THE FOLLICULAR WALL &IGURE
)N SEVERAL SPECIES OF lSH THE FOLLICULAR LAYER OF LARGER
FOLLICLES BECOMES DEEPLY FOLDED DURING ATRESIA GREATLY
INCREASING THE ABSORPTIVE SURFACE EXPOSED TO THE YOLK
&IGURE (ISAW AND (ISAW 2ASTOGI
$ODD AND 3UMPTER 4HE BASEMENT MEMBRANE RE
MAINS INTACT AND CONNECTIVE TISSUE OF THE TUNICA INTIMA
IS CARRIED INTO THE FOLDS ALONG WITH BRANCHES OF BLOOD
VESSELS 5LTRASTRUCTURAL OBSERVATIONS ON THE PHAGOCYTIC
REMOVAL OF THE OOCYTE IN THE PERCH 0ERCA mUVIATILIS AND
THE ELECTRIC RAY 4ORPEDO MARMORATA INDICATE DISSOLU
TION OF THE OOCYTE NUCLEUS DISINTEGRATION OF THE YOLK
MASS BREAKDOWN OF CORTICAL ALVEOLI AND DEGENERATION
OF MITOCHONDRIA AND OTHER CYTOPLASMIC CONSTITUENTS
&IGURES ! AND ! TO $ ,ANG B #HIEFl
"ACCARI ET AL )NCREASING NUMBERS OF SMALL CY
TOPLASMIC VACUOLES APPEAR IN THE FOLLICULAR CELLS DURING
THE EARLY STAGES OF ATRESIA AND GRANULAR ENDOPLASMIC
RETICULUM INCREASES AT THE SAME TIME &IGURES "
TO ' 3EVERAL 'OLGI COMPLEXES SHED SMALL VESICLES
THAT COALESCE INTO SMOOTH SURFACED TUBULES 4HECAL
CELLS AND LEUCOCYTES WHICH INVADE THE FOLLICLE FROM
SURROUNDING CAPILLARIES APPEAR TO TAKE NO PART IN DI
GESTING OR TRANSFORMING OOCYTIC MATERIAL !GRANULAR
ENDOPLASMIC RETICULUM AS WELL AS MITOCHONDRIA WITH
TUBULAR CRISTAE ARISE IN FOLLICULAR CELLS OF THE ELECTRIC
RAY 4ORPEDO MARMORATA SUGGESTING A STEROIDOGENIC
ROLE FOR THESE CELLS &IGURES % & #HIEFl "ACCARI
ET AL )NDEED THE NUCLEI OF THESE CELLS MIGRATE
FROM THE BASAL TO APICAL POLES AT THIS TIME INDICATING
THE CHANGE IN THE ROLE OF THESE CELLS FROM PHAGOCYTOSIS
OF YOLK TO THE RELEASE OF SECRETIONS INTO THE RICHLY VAS
CULARIZED STROMA )N ADDITION THE PRESENCE OF ` (3$
ACTIVITY IN THE FOLLICULAR CELLS IMPLIES STEROIDOGENIC AC
TIVITY ,UPO $I 0RISCO CITED BY #HIEFl "ACCARI
ET AL /N THE OTHER HAND TELEOSTS HAVE REVEALED
NO EVIDENCE OF GLANDULAR FUNCTION IN THE POSTOVULATORY
CORPUS LUTEUM
!S THE AMOUNT OF YOLK IN THE FOLLICLE DECREASES
PHAGOCYTOSIS BY THE FOLLICULAR CELLS DECREASES AND
/65,!4)/.
WHEN THE YOLK IS COMPLETELY REMOVED ADJACENT FOLDS
OF THE FOLLICULAR EPITHELIUM FUSE TO PRODUCE A RICHLY
VASCULAR #/2053 ,54%5- THAT MAY ALMOST lLL THE CAV
ITY &IGURE $ 4HE THECA INCREASES IN THICKNESS
AND GRANULES APPEAR IN ITS CELLS WHICH NOW INVADE THE
FOLLICULAR TISSUE AND BECOME THE DOMINANT CELL TYPE
FOLLICULAR CELLS BECOMING RARE AND ISOLATED IN SMALL
CLUMPS &IGURE %VENTUALLY THE FOLLICULAR AND
THECAL CELLS DEGENERATE &IGURES ( TO * TO BE RE
SORBED BY THE OVARIAN STROMA AND THE FOLLICLE SHRINKS
! YELLOW
BROWN PIGMENT THE SO
CALLED AGE PIGMENT
,)0/&53#). ,ANG B "ESSEAU AND &ALIEX
IS FORMED DURING THE REGRESSION OF THE FOLLICULAR CELLS
&IGURE 4HESE SHRUNKEN FOLLICLES MAY PERSIST
FOR A LONG PERIOD 3OME FOLLICULAR CELLS STILL CONTAIN
DISCERNIBLE ELEMENTS OF THE OOCYTE BUT MOST CONTAIN
MEMBRANOUS WHORLS HETEROPHAGIC LYSOSOMES AND
ELECTRON
DENSE BODIES &IGURE ' ,ANG B
#HIEFl "ACCARI ET AL
h/PENv AND hCLOSEDv FORMS OF ATRESIA HAVE BEEN
DESCRIBED IN THE HAGlSH -YXINE GLUTINOSA 7ALVIG
+OSMATH 0ATZNER AND !DAM A B 4HE
/0%. 490% OCCURS IN EGGS LARGER THAN MM WHERE FOL
LICULAR CELLS AND YOLK PLATELETS ARE DISCHARGED INTO THE
COELOM THROUGH A PERFORATION IN THE FOLLICULAR WALL
6ASCULAR CONNECTIVE TISSUE AND WANDERING PHAGOCYTIC
CELLS FROM THE THECA THEN INVADE THE FOLLICULAR LUMEN
AND REMOVE THE DBRIS REMAINING FROM THE FOLLICULAR
CELLS .O PERFORATION OF THE FOLLICULAR WALL APPEARS IN
THE #,/3%$ 490% OF ATRESIA THAT OCCURS IN OOCYTES OF PRE
OVULATORY FOLLICLES NOT YET MM IN DIAMETER 4HESE
CEASE DEVELOPMENT AND LIPID DROPLETS OFTEN SURROUNDED
BY SMALL ELECTRON
DENSE GRANULES ACCUMULATE IN THE
PERIPHERAL OOPLASM 4HE THECAL LAYER THICKENS AND BE
COMES RICHLY VASCULAR 4SUNEKI AND 'ORBMAN
4HECAL CELLS CONTAINING LYSOSOMES BECOME PHAGO
CYTIC AND INVADE THE OOCYTE &IGURE &OLLICULAR
CELLS ARE SOMETIMES PRESENT BUT OFTEN THEY DISAPPEAR
ESPECIALLY AS ATRESIA PROGRESSES 4HE INVADING PHAGO
CYTES REMOVE RESIDUAL YOLK PLATELETS AND THE REMNANTS
OF FOLLICULAR CELLS FROM THE FOLLICULAR LUMEN 0RODUC
TION OF HORMONES WAS NOT DETECTED IN EITHER TYPE OF
ATRETIC FOLLICLE +OSMATH 0ATZNER AND !DAM B
! RARER TYPE OF ATRESIA INVOLVING NO MARKED PHAGO
CYTOSIS OR FOLLICULAR HYPERTROPHY HAS BEEN DESCRIBED
IN THE BROOK STICKLEBACK %UCALIA INCONSTANS AND IN THE
)NDIAN KNIFElSH .OTOPTERUS NOTOPTERUS "RAEKEVELT
AND -C-ILLAN 3HRIVASTAVA 4HE OOCYTE
IS REMOVED BY LIQUIFACTION AND NOTHING RESEMBLING A
CORPUS LUTEUM IS FORMED
)N SPITE OF HIGH HOPES NO ` (3$ ACTIVITY HAS
BEEN FOUND IN ATRETIC FOLLICLES OF SEVERAL SPECIES
,AMBERT AND VAN /ORDT ,ANCE AND #ALLARD
,AMBERT B 9ARON ,IVNI
,ANG B +OSMATH 0ATZNER AND !DAM B
ALTHOUGH ACTIVITY WAS NOTED IN FOLLICULAR CELLS OF
THE GOLDlSH #ARASSIUS AURATUS FOLLOWING PHAGO
CYTIC REMOVAL OF THE ATRETIC OOCYTE +HOO
.O ` (3$ REACTION WAS OBTAINED IN ATRETIC FOLLICLES
OF THE PERCH 0ERCA mUVIATILIS ALTHOUGH THE PRESENCE
OF SMOOTH SURFACED TUBULES FORMED BY THE COALES
CENCE OF SMALL VESICLES THAT AROSE FROM THE 'OLGI
COMPLEX GAVE THE APPEARANCE OF STEROIDOGENESIS
,ANG B
).4%234)4)!, ',!.$ #%,,3 HAVE BEEN DESCRIBED
IN THE OVARY OF THE DOGlSH 3COLIODON SORRAKOWAH
'URAYA AND IN A TELEOST -YSTUS CAVASIUS
3AIDAPUR AND .ADKARNI AS VASCULARIZED MASS
ES OF CELLS REMAINING FROM ATRESIA OF LARGE PREVITELLO
GENIC AND EARLY VITELLOGENIC FOLLICLES &IGURE
)N THESE SPECIES THEY ARE SAID TO ARISE FROM THE TRANS
FORMATION OF THE THECA INTERNA AND SURROUNDING STRO
MAL ELEMENTS AFTER THE OVA AND FOLLICULAR CELLS HAVE
BEEN REMOVED )N THE CARP #YPRINUS CARPIO SOME
INTERSTITIAL CELLS APPEAR TO ARISE FROM PERSISTING THE
CAL GLAND CELLS OF POSTOVULATORY FOLLICLES AND FROM
RESIDUAL FOLLICULAR EPITHELIAL CELLS 'URAYA AND +AUR
4HEY CONTAIN SUDANOPHILIC LIPID DROPLETS AND
DISPLAY ACTIVITY FOR ` (3$ AS WELL AS OTHER ENZYMES
INVOLVED IN STEROIDOGENESIS SUGGESTING THAT THEY MAY
PARTICIPATE IN THE PRODUCTION OF STEROID HORMONES
)N THE GUPPY 0OECILIA RETICULATA THESE CELLS DEMON
STRATE AGRANULAR ENDOPLASMIC RETICULUM AND MITO
CHONDRIA WITH TUBULAR CRISTAE AND HAVE BEEN SHOWN TO
PLAY A ROLE IN STEROIDOGENESIS 6ENKATESH ET AL
)T IS UNCLEAR WHAT RELATIONSHIP THESE CELLS BEAR TO THE
STEROIDOGENIC INTERSTITIAL CELLS OF TILAPIA /REOCHROMIS
NILOTICUS THAT ARISE NEAR THE OVARIAN BLOOD VESSELS AND
EVENTUALLY MIGRATE TO THE THECA AROUND VITELLOGENIC
OOCYTES .AKAMURA 3PECKER AND .AGAHAMA
0/34/65,!4/29 &/,,)#,%3
!FTER EXPULSION OF THE EGG DURING OVULATION THE FOL
LICULAR EPITHELIUM MAY HYPERTROPHY AND BECOME
PHAGOCYTIC IN MUCH THE SAME MANNER AS SEEN IN ATRET
IC FOLLICLES CLEARING AWAY ANY DBRIS REMAINING IN
THE LUMEN !S WITH ATRESIA THE FOLLICULAR EPITHE
LIUM BECOMES FOLDED AND INVADED BY RICHLY VASCULAR
THECAL TISSUE 4HE RESULTING MASS OF CELLS EVENTU
#(!04%2
ALLY BECOMES INDISTINGUISHABLE FROM THAT REMAINING
FROM AN ATRETIC FOLLICLE
0OSTOVULATORY FOLLICLES OF THE "RAZILIAN CHARACIN
!STYANAX BIMACULATUS LACUSTRIS HAVE BEEN USED AS A
MODEL FOR !0/04/3)3 OR GENETICALLY PROGRAMMED CELL
DEATH A NORMAL PHYSIOLOGICAL PROCESS OF SELF DE
STRUCTION $RUMMOND ET AL !POPTOSIS IS THE
MAJOR MECHANISM RESPONSIBLE FOR THE ELIMINATION OF
FOLLICULAR CELLS IN THE POSTOVULATORY FOLLICLES DURING
OVARIAN RECOVERY AFTER SPAWNING 0OSTOVULATORY FOL
LICLES ARE RAPIDLY REABSORBED AS THE FOLLICULAR CELLS DE
VELOP PHAGOCYTIC ACTIVITY 4HE FOLLICULAR CELLS UNDERGO
HYPERTROPHY A FEW HOURS AFTER SPAWNING SHOWING THE
WELL DEVELOPED ORGANELLES CHARACTERISTIC OF PROTEIN
SYNTHESIS BASAL GRANULAR ENDOPLASMIC RETICULUM MI
TOCHONDRIA AND 'OLGI COMPLEXES &IGURES ! "
THESE ARE REQUIREMENTS OF PROGRAMMED CELL DEATH SINCE
APOPTOSIS IS DEPENDENT ON THE EXPRESSION OF NEW GENES
BEING ENCODED IN THE $.! OF THE TARGET CELL )N SPECI
MENS lXED WITH TANNIC ACID THE PRESENCE OF DARKLY
STAINED FOLLICULAR CELLS SCATTERED AMONG CLEAR CELLS MAY
INDICATE THE PRESENCE OF DAMAGED CELLS HERALDING THEIR
EVENTUAL DISINTEGRATION &IGURE # &OLLICULAR CELLS
DESTINED FOR DESTRUCTION RELEASE LARGE ORGANELLE lLLED
BLEBS AND PROTRUSIONS THE !0/04/4)# "/$)%3 INTO THE
LUMEN OF THE FOLLICLE &IGURE $ 4HESE ARE PHAGO
CYTOSED EITHER BY ADJACENT HEALTHY FOLLICULAR CELLS OR BY
MONONUCLEAR PHAGOCYTES &IGURES % & &OUR DAYS
AFTER SPAWNING THE BULK OF POSTOVULATORY FOLLICLES ARE
REDUCED BUT NOT COMPLETELY REABSORBED
"ECAUSE OF A SUSPECTED ROLE IN HORMONAL PRODUC
TION THE FATE OF POSTOVULATORY FOLLICLES OF lSH HAS RE
CEIVED CONSIDERABLE ATTENTION #9#,/34/-%3 ,YGNES
,EWIS AND -C-ILLAN 0ATZNER +OS
MATH 0ATZNER AND !DAM A B %,!3-/"2!.#(3
(ISAW AND (ISAW ,ANCE AND #ALLARD
4E7INKEL &ASANO 0IERANTONI AND #HIEFl
4%,%/343 2AI ,EHRI 0ANT
3HRIVASTAVA .ICHOLLS AND -APLE +HOO
.AGAHAMA #HAN AND (OAR .AGAHAMA
#LARKE AND (OAR 3ZLLSI *ALABERT AND "RETON
VAN DEN (URK AND 0EUTE +AGAWA
AND 4AKANO +AGAWA 4AKANO AND .AGAHAMA
,ANG A 4HERE IS GREAT SIMILARITY IN THE DE
SCRIPTIONS )N MANY SPECIES THERE IS A PROLIFERATION OF
FOLLICULAR CELLS WHICH BECOME PHAGOCYTIC MUCH IN THE
SAME MANNER AS THOSE OF ATRETIC FOLLICLES AND REMOVE
4HE LITERATURE ON THE MORPHOLOGY OF APOPTOSIS HAS BEEN REVIEWED
BY (ACKER
DBRIS LEFT IN THE HOLLOW FOLLICLE &IGURE 4HE FOL
LICULAR WALL COLLAPSES INTO ITS EMPTY LUMEN AND FOLDS
OF THE FOLLICULAR EPITHELIUM BECOME INVADED BY RICHLY
VASCULAR THECAL ELEMENTS 0ROLIFERATION OF THE FOLLICULAR
CELLS CONTINUES AND IN A FEW SPECIES PROLIFERATION OF
THECAL CELLS IS ALSO DESCRIBED )N 3QUALUS ACANTHIAS A
CORPUS LUTEUM DEVELOPS FROM POSTOVULATORY FOLLICLES
BY HYPERTROPHY OF THE FOLLICULAR CELLS SURROUNDED BY A
SEPARATE THECAL SHEET BUT IN 3CYLIORHINUS STELLARIS AND
SEVERAL SPECIES OF 2AJA IT IS FORMED BY HYPERTROPHY
OF BOTH THECAL AND FOLLICULAR CELLS &ASANO 0IERANTONI
AND #HIEFl 3INCE THERE APPEARS TO BE CONTINU
OUS SECRETION OF YOLK BY THE FOLLICULAR EPITHELIUM LONG
AFTER THE OVUM HAS BEEN DISCHARGED AT LEAST IN SOME
ELASMBOBRANCHS CARE MUST BE EXERCISED IN DISTIN
GUISHING THE CORPORA LUTEA OF ATRESIA FROM THOSE RESULT
ING FROM OVULATION (ISAW AND (ISAW
4HECAL CELLS APPEAR TO PARTICIPATE IN THE PHAGOCYTIC
CLEANUP OF POSTOVULATORY FOLLICLES OF THE TROUT 3ALMO
GAIRDNERI 3ZLLSI *ALABERT AND "RETON 7ITH
IN TO HOURS OF OVULATION STELLATE THECAL CELLS BE
GIN PHAGOCYTOSIS OF ADJACENT COLLAGEN THEIR SLENDER
PROCESSES PENETRATING THE SURROUNDING CONNECTIVE TIS
SUE SPACE &IGURE $ 4HE NUMBER OF PHAGOCYTIC
VESICLES WITHIN THE THECAL CELLS INCREASES WITH TIME
7ITHIN A FEW HOURS OF OVULATION mATTENED SMOOTH
MUSCLE CELLS OF THE THECA TRANSFORM INTO STELLATE CELLS
WITH MANY AMOEBOID PROCESSES THAT ISOLATE AND PHAGO
CYTOSE BUNDLES OF COLLAGEN
7HEN THE DBRIS HAS BEEN REMOVED FROM THE LU
MEN THE CORPUS LUTEUM MAY BECOME ORGANIZED INTO
A COMPACT STRUCTURE OF IRREGULAR SHAPE !T THIS STAGE
IT IS IMPOSSIBLE TO DISTINGUISH POSTOVULATORY CORPORA
LUTEA FROM THOSE DERIVED FROM ATRESIA OF LARGE FOLLICLES
,UTEAL BODIES REMAINING FROM THE ATRESIA OF SMALL FOL
LICLES ALSO RESEMBLE POSTOVULATORY FOLLICLES DIFFERING
ONLY IN THEIR SMALLER SIZE %VENTUALLY THE FOLLICULAR
CELLS DEGENERATE LEAVING A SOLID COMPACT MASS THAT
lNALLY DISAPPEARS 4HE SURROUNDING THECAL ELEMENTS
AND BLOOD VESSELS ALSO DISAPPEAR 0OSTOVULATORY COR
PORA LUTEA ARE NOT FOUND IN THE MUD EEL !MPHIPNOUS
CUCHIA SINCE THE EVACUATED FOLLICLES DISAPPEAR IN THE
STROMA WITH hBEWILDERING RAPIDITYv 2ASTOGI
)N THE VIVIPAROUS GUPPY 0OECILIA RETICULATA FERTILIZA
TION AND GESTATION TAKE PLACE WITHIN THE FOLLICULAR WALL
AND POSTOVULATORY CORPORA LUTEA ARE NOT FOUND ,AM
BERT
3TEROIDOGENESIS HAS BEEN DETECTED IN POSTOVULA
TORY FOLLICLES OF SEVERAL SPECIES OF lSH BOTH OVIPAROUS
.ICHOLLS AND -APLE +HOO .AGAHAMA
/65,!4)/.
#HAN AND (OAR AND VIVIPAROUS ,ANCE AND
#ALLARD )N SOME SPECIAL THECAL CELLS REACT
POSITIVELY FOR ` (3$ AND SHOW THE ULTRASTRUCTURAL
CHARACTERISTICS OF STEROIDOGENESIS "ARA +AGA
WA 4AKANO AND .AGAHAMA IN OTHERS IT IS THE
FOLLICULAR CELLS ,AMBERT A +AGAWA AND 4AKANO
)N SOME lSH BOTH CELL TYPES APPEAR TO CONTRIB
UTE ACTIVELY TO STEROIDOGENESIS WITH THE SPECIAL THECAL
CELLS SOMETIMES APPEARING TO BE MOST ACTIVE 9ARON
.ICHOLLS AND -APLE +HOO .AGA
HAMA #HAN AND (OAR VAN DEN (URK AND 0EUTE
3MITH AND (ALEY )N THE FEW lSH IN
WHICH THE POSTOVULATORY FOLLICLES HAVE BEEN STUDIED AT
AN EXTENDED INTERVAL FOLLOWING OVULATION STEROIDOGEN
ESIS APPEARS TO SUBSIDE WITH TIME ,ANCE AND #ALLARD
.O EVIDENCE WAS FOUND FOR STEROIDOGENESIS IN
POSTOVULATORY FOLLICLES OF THE VIVIPAROUS SMOOTH DOG
lSH -USTELUS CANIS 4E7INKEL
&OUR STAGES IN THE LIFE OF A POSTOVULATORY FOLLICLE
HAVE BEEN DESCRIBED IN 0ERCA mUVIATILIS &IGURES
AND ,ANG A
34!'% 2%/2'!.):!4)/. 0(!3% &OR TWO DAYS FOL
LOWING OVULATION THERE IS A REORGANIZATION OF THE DISOR
GANIZED FOLLICULAR EPITHELIUM 3OME OF ITS CELLS BECOME
PHAGOCYTIC THEY CONTAIN LYSOSOMES AND RESORB FOL
LICULAR CELLS THAT HAVE LOST CONTACT WITH THE BASEMENT
MEMBRANE OR HAVE BEEN DAMAGED DURING OVULATION
&IGURE /THER CELLS OF THE FOLLICULAR EPITHELIUM
TRANSFORM INTO SYNTHETICALLY ACTIVE CELLS
34!'% 6!#5/,!2 0(!3% &ROM DAYS TO FOLLOW
ING OVULATION THE FOLLICLE PREPARES ITSELF FOR SECRETION
34!'% ',/"5,!2 0(!3% &ROM ABOUT TO DAYS
FOLLOWING OVULATION THE PRESENCE OF AGRANULAR ENDO
PLASMIC RETICULUM MITOCHONDRIA WITH TUBULAR CRISTAE
AND ` (3$ ACTIVITY ARE CONSISTENT WITH THE CONCEPT
THAT THE FOLLICULAR CELLS ARE STEROIDOGENIC 4HEY ENLARGE
AND FORM VACUOLES UP TO M IN DIAMETER CONTAIN
ING PROTEINACEOUS AND CHOLESTEROL RELATED MATERIAL
4HESE VACUOLES APPEAR TO BE SHED AS A HOLOCRINE SE
CRETION INTO THE FOLLICULAR LUMEN 4HE LUMEN MAY AP
PEAR AS A RED SPOT DUE TO THE PRESENCE OF ERYTHROCYTES
4HECAL CELLS DO NOT EXHIBIT ANY STRUCTURAL EVIDENCE OF
SECRETION AND SHOW NO ` (3$ ACTIVITY
34!'% 2%'2%33)/. 0(!3% 4HE FOLLICULAR CELLS RE
MAINING AFTER SECRETION DEGENERATE NO YELLOW PIG
MENTS ARE FORMED
4HE FORMATION OF A POSTOVULATORY CORPUS LUTEUM
HAS BEEN DESCRIBED IN THE CICHLID #ICHLASOMA NIGRO
FASCIATUM .ICHOLLS AND -APLE )N THIS SPECIES
THE MANIFESTATIONS OF STEROIDOGENESIS ARE APPARENT IN
BOTH THE FOLLICULAR EPITHELIUM AND THECA 4HE BASIC OR
GANIZATION OF THE PREOVULATORY FOLLICLES REMAINS AFTER
OVULATION AND THE THECAL LAYERS WITH THEIR CAPILLARIES
REMAIN INTACT FOR AT LEAST DAYS STILL SEPARATED FROM
THE FOLLICULAR EPITHELIUM BY ITS BASEMENT MEMBRANE
4HE ULTRASTRUCTURE OF PRESUMED STEROIDOGENIC CELLS
OF THE THECA REMAINS UNCHANGED DURING THIS TIME AND
PENETRATION OF THECAL ELEMENTS INTO THE FOLLICULAR LAYER
APPARENTLY DOES NOT OCCUR &OLLICULAR CELLS PROLIFERATE
RAPIDLY ATTAINING A THICKNESS OF UP TO FOUR LAYERS OF
CELLS BY ONE HOUR AFTER OVIPOSITION PRESUMABLY ONLY A
FEW HOURS AFTER OVULATION 4HE INNERMOST CELLS IN PAR
TICULAR TEND TO BECOME COLUMNAR AND TO BULGE INTO THE
REGION VACATED BY THE OOCYTE 4HIS PROLIFERATION THROWS
THE BASEMENT MEMBRANE INTO FOLDS 4HE ENDOPLASMIC
RETICULUM OF THE FOLLICULAR CELLS DISSOCIATES ITSELF FROM
RIBOSOMES AND BY HOURS AFTER OVIPOSITION THE FOL
LICULAR CELLS ARE PACKED WITH LARGE QUANTITIES OF SMOOTH
MEMBRANE LARGELY TUBULAR AGRANULAR ENDOPLASMIC RE
TICULUM -ITOCHONDRIA LIE BETWEEN THE MEMBRANES
!LSO PRESENT ARE FREE POLYRIBOSOMES OCCASIONAL LIPID
DROPLETS AND INCLUSIONS TENTATIVELY IDENTIlED AS LI
POFUSCIN 3OME CELLS CONTAIN A LARGE 'OLGI COMPLEX
CONSISTING OF SEVERAL INDIVIDUAL LAMELLAR STACKS AND
ASSOCIATED VESICLES ! FEW DAYS AFTER SPAWNING DE
GENERATIVE PROCESSES APPEAR WITHIN THESE POSTOVULA
TORY FOLLICLES ALTHOUGH COMPARABLE DEGENERATION OF
THE THECA WAS NOT OBSERVED EVEN DAYS FOLLOWING
OVIPOSITION WHEN THE PRESUMED STEROID
SECRETING THE
CAL CELLS ARE STILL CLUSTERED CLOSE TO CAPILLARIES AND MAY
CONTINUE SECRETING STEROID HORMONES DURING THIS TIME
4HE FOLLICULAR CELLS HOWEVER SEEM TO BE ACTIVELY SE
CRETORY FOR ONLY A FEW DAYS THEIR LARGE AMOUNTS OF
SMOOTH MEMBRANE THEN SEEM TO BECOME DISORGANIZED
AND GRADUALLY DISAPPEAR WHILE QUANTITIES OF DEPOSITED
LIPIDS APPARENTLY INCREASE
0OSTOVULATORY FOLLICLES OF TILAPIA /REOCHROMIS MOS
SAMBICUS ARE THE MOST PROMINENT STRUCTURES IN THE
OVARY FOR TO DAYS AFTER SPAWNING WHEN THE NEXT
CLUTCH OF EGGS BEGINS TO GROW &IGURE ! 3MITH
AND (ALEY /N THE lRST DAY AFTER SPAWNING OC
CASIONAL CAPILLARIES ARE SCATTERED THROUGHOUT THE THECA
!BOUT EIGHT PERCENT OF THE CELLS OF THE THECA INTERNA
APPEAR STEROIDOGENIC DISPLAYING AGRANULAR ENDOPLAS
MIC RETICULUM USUALLY TUBULAR AND MITOCHONDRIA WITH
TUBULAR CRISTAE &IGURES # $ AND ! !LSO
PRESENT IN THESE CELLS ARE GRANULAR ENDOPLASMIC RETICU
LUM FREE RIBOSOMES MICROlLAMENTS AND OCCASIONAL
LIPID DROPLETS 4HE CELLS OF THE THECA EXTERNA AS WELL AS
THE NON
STEROIDOGENIC CELLS CELLS OF THE THECA INTERNA
#(!04%2
ARE lBROBLASTIC WITH CYTOPLASM CONTAINING GRANULAR
ENDOPLASMIC RETICULUM FREE POLYRIBOSOMES AND MI
CROlLAMENTS #ELLS OF THE THECA EXTERNA ARE WIDELY
SEPARATED FROM ONE ANOTHER EACH IS ATTACHED TO A CELL
OF THE THECA INTERNA BY A FEW DESMOSOMES AND LARGE
INTERCELLULAR SPACES OPEN BETWEEN THE POINTS OF AT
TACHMENT &IGURE " &OLLICULAR CELLS ARE CUBOIDAL
WITH LOBED NUCLEI &IGURE " 4HE CELLS ARE PACKED
WITH ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM THAT
APPEARS VESICULAR 3OME GRANULAR ENDOPLASMIC RETICU
LUM OCCURS BASALLY AND FREE RIBOSOMES ARE SCATTERED
THROUGHOUT -ITOCHONDRIAL CRISTAE ARE LARGELY LAMEL
LAR &IGURE # 4HE APICAL SURFACE OF THESE CELLS
BULGES INTO THE LUMEN PROMINENT DESMOSOMES ATTACH
THE APICOLATERAL SURFACES 4HE APICAL SURFACE IS REGULAR
WITH FEW MICROVILLI MANY VESICLES ARE FUSED WITH ITS
INNER PLASMALEMMA /CCASIONAL BLOOD CELLS APPEAR IN
THE LUMEN "Y TO DAYS AFTER SPAWNING THE FOLLICU
LAR CELLS ARE USUALLY COLUMNAR WITH APICAL MICROVILLI
VESICLES APPEAR FUSED TO THE INNER SURFACE OF THE APICAL
PLASMALEMMA &IGURE %ACH CELL CONTAINS SEVER
AL MODERATELY DEVELOPED 'OLGI COMPLEXES AND A SMALL
AMOUNT OF TUBULAR AGRANULAR ENDOPLASMIC RETICULUM
3OME MICROTUBULES ARE FOUND AND THE NUMBER OF MI
CROlLAMENTS IS INCREASED ! FEW MULTIVESICULAR BODIES
ARE SEEN -OST MITOCHONDRIA CONTAIN LAMELLAR CRISTAE
BUT A FEW TUBULAR CRISTAE ARE OCCASIONALLY PRESENT )T IS
POSSIBLE THAT A STEROID HORMONE PRODUCED IN THE THECAL
CELLS MAY BE FURTHER CONVERTED TO OTHER STEROIDS BY EN
ZYMES IN THE AGRANULAR ENDOPLASMIC RETICULUM OF THE
FOLLICULAR CELLS 4HE PRIMARY SITE OF STEROIDOGENESIS
HOWEVER APPEARS TO BE IN THE SPECIAL THECAL CELLS
0OSTOVULATORY FOLLICLES OF VARIOUS SALMONIDS HAVE
A FOLDED FOLLICULAR EPITHELIUM THAT IS CONTINUOUS WITH
THE COELOMIC EPITHELIUM OF THE LAMELLAE &IGURES )
AND # .AGAHAMA #LARKE AND (OAR
3ZLLSI *ALABERT AND "RETON VAN DEN (URK
AND 0EUTE +AGAWA 4AKANO AND .AGAHAMA
3TRONG ` (3$ ACTIVITY IS PRESENT IN THE LARGE
NUMBERS OF SPECIAL THECAL CELLS ARRANGED AROUND THE
YOUNG POSTOVULATORY FOLICLE BUT ONLY WEAK ACTIVITY IN
THE FOLLICULAR CELLS &IGURES ! AND ! " %LEC
TRON MICROGRAPHS OF THESE SPECIAL THECAL CELLS SHOW THE
PRESENCE OF ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM
AND TUBULAR MITOCHONDRIAL CRISTAE &IGURES " #
# $ 4HESE FEATURES ALSO APPEAR TO SOME EXTENT
IN THE FOLLICULAR CELLS OF YOUNG POSTOVULATORY FOLLICLES
OF THE RAINBOW TROUT 3ALMO GAIRDNERI WHICH ALSO AP
PEAR TO BE STEROIDOGENIC &IGURES $ % VAN DEN
(URK AND 0EUTE )N ADDITION THE FOLLICULAR
CELLS EXHIBIT WELL DEVELOPED 'OLGI COMPLEXES MANY
LYSOSOME LIKE STRUCTURES COATED VESICLES AND ELEC
TRON DENSE VESICLES ,ATER THESE MANIFESTATIONS OF
STEROIDOGENESIS ARE REDUCED "OTH SPECIAL THECAL AND
FOLLICULAR CELLS OF POSTOVULATORY FOLLICLES SYNTHESIZE
STEROIDS THAT MAY BE RELATED TO THE DEVELOPMENT OF
NEW FOLLICLES 4HE SPECIAL THECAL CELLS OF TWO SPECIES
OF SALMON /NCORHYNCHUS SPP ARE DESCRIBED AS STE
ROIDOGENIC WHILE THE FOLLICULAR CELLS APPEAR DEGENERATE
.AGAHAMA #LARKE AND (OAR "Y ONE MONTH
AFTER OVULATION SPECIAL THECAL CELLS OF THE WHITE SPOT
TED CHAR 3ALVELINUS LEUCOMAENIS STILL POSSSESS THE CEL
LULAR ORGANELLES TYPICAL OF STEROIDOGENESIS BUT APPEAR
TO BE UNDERGOING DEGENERATION +AGAWA 4AKANO AND
.AGAHAMA
)N THE !FRICAN CATlSH #LARIAS GARIEPINUS WHERE
OVARIES OF UNSTRIPPED lSH MAY CONTAIN OVERRIPE EGGS
WITHIN THE OVARIAN CAVITY HYPERTROPHIED FOLLICULAR
CELLS CONTAIN HETEROPHAGIC LYSOSOMES AND ARE ACTIVELY
PHAGOCYTIC REMOVING MATERIAL OF THE DISINTEGRATING
OVULATED EGGS &IGURE VAN DEN (URK AND 0EUTE
%VENTUALLY AUTOPHAGIC LYSOSOMES TAKE PART IN
THE DEGRADATION OF THE CONTENTS OF THE FOLLICULAR CELLS
AND ARE ULTIMATELY RESPONSIBLE FOR THE DISINTEGRATION
OF THE POSTOVULATORY FOLLICLE )T IS SUGGESTED THAT DIS
INTEGRATING OVERRIPE EGGS RELEASE COMPOUNDS THAT IN
HIBIT THE PRODUCTION OF STEROIDS BY FOLLICULAR CELLS OF
THE POSTOVULATORY FOLLICLES THEREBY STOPPING THE PRO
DUCTION OF SEX PHEROMONES AND AVOIDING A POTENTIAL
SPAWNING SINCE FERTILIZATION OF OVERRIPE EGGS MIGHT
LEAD TO BIRTH OF DEFORMED FRY
4RUE CORPORA LUTEA DEVELOP IN BOTH VIVIPAROUS AND
OVIPAROUS ELASMOBRANCHS #HIEFl #HIEFl "AC
CARI ET AL 4HEY DEVELOP FROM ATRETIC FOLLICLES
IN 4ORPEDO MARMORATA AND 4 OCELLATA OVOVIVIPAROUS
AND FROM POSTOVULATORY FOLLICLES IN 3CYLIORHINUS STEL
LARIS AND 3 CANICULA OVIPAROUS !FTER PHAGOCYTOSIS
OF THE YOLK IN 4ORPEDO THE FOLLICULAR CELLS UNDERGO
HYPERTROPHY AND SHOW CLEAR SIGNS OF LIPID AND STE
ROID METABOLISM 4HUS THE ATRETIC FOLLICLE ASSUMES THE
STRUCTURE OF A TRUE EPITHELIAL GLAND WHICH PERSISTS DUR
ING SEVERAL MONTHS OF GESTATION )N 4 MARMORATA AN
INCREASE IN THE NUMBER OF FULLY DEVELOPED CORPORA LU
TEA COINCIDENT WITH THE LENGTHENING OF THE UTERINE FOLDS
DURING THE REPRODUCTIVE CYCLE SUGGESTS AN INmUENCE OF
THESE STRUCTURES ON PREGNANCY 0OSSIBLE EFFECTS OF THE
CORPORA LUTEA ON THE GENITAL TRACT OF THE OVIPAROUS 3CYL
IORHINUS IS LEFT FOR SPECULATION
4HE ORGANIZATION OF CORPORA LUTEA IS SIMILAR IN
OVIPAROUS AND VIVIPAROUS ELASMOBRANCHS AND CONSISTS
/65,!4)/.
OF LIPID
lLLED CELLS DERIVED FROM THE FOLLICULAR EPITHE
LIUM ARRANGED AROUND A CENTRAL LUMEN IN EARLY STAG
ES OF LUTEAL FORMATION HYPERTROPHY OF THE CELLS MAY
OBSCURE THE LUMEN &IGURE +OOB AND #ALLARD
4HE CELLS CONTAIN LARGE NUCLEI WITH CONSPICU
OUS NUCLEOLI AND ABUNDANT LIPID DROPLETS IN ADDITION
THEY MANIFEST THE AGRANULAR ENDOPLASMIC RETICULUM
AND MITOCHONDRIA WITH TUBULAR CRISTAE CHARACTERISTIC OF
STEROID
PRODUCING CELLS ! VASCULAR CONNECTIVE TISSUE
STROMA IS PROVIDED BY INGROWTHS FROM THE THECA 4HE
CORPORA LUTEA OF OVIPAROUS FORMS DECLINE WITHIN A FEW
WEEKS BUT IN VIVIPAROUS SPECIES THEY PERSIST THROUGH
OUT GESTATION $EGENERATION OF CORPORA LUTEA INVOLVES
A REDUCTION IN SIZE OF THE STRUCTURE INCREASED DISORGA
NIZATION OF THE LOBULES A DECREASE IN THE LIPID CONTENT
OF INDIVIDUAL CELLS DEATH OF CELLS AND AN ACCUMULATION
OF CELLULAR DBRIS IN THE LUMEN
4HERE IS NO MORPHOLOGICAL INDICATION OF STEROIDO
GENESIS IN POSTOVULATORY FOLLICLES OF -YXINE GLUTINOSA
+OSMATH 0ATZNER AND !DAM A ! PERIOD OF RE
ORGANIZATION WHERE THE CELLULAR DBRIS REMAINING AFTER
OVULATION IS REMOVED BY PHAGOCYTOSIS IS SOON FOL
LOWED BY REGRESSION AND DISAPPEARANCE OF THE FOLLICLE
IN THIS PHASE THE FOLLICULAR CELLS AND THECA DEGENERATE
AND ARE REMOVED BY BLOOD
BORNE PHAGOCYTES .O CHO
LESTEROL NOR `
(3$ ACTIVITY WAS DETECTED IN THE
CELLS OF THE POSTOVULATORY FOLLICLE +OSMATH 0ATZNER
AND !DAM B
&OLLICULAR 3TEROIDOGENESIS
4WO IMPORTANT HORMONES ARE SECRETED BY THE OVARIAN
FOLLICLES OF MANY lSH 6ITELLOGENIC FOLLICLES SECRETE
PREDOMINANTLY /%342!$)/,
` AND POSTVITELLOGENIC
FOLLICLES MAINLY _ `
$)(9$2/89
02%'.%.
/.%
_ `
$0 6ANKATESH 4AN AND ,AM A 0AN
KHURST THE PATHWAY OF THEIR BIOSYNTHESIS IS
SHOWN IN &IGURE /ESTRADIOL
` UNDER THE IN
mUENCE OF GONADOTROPIN PROMOTES VITELLOGENESIS BY
STIMULATING THE SYNTHESIS AND SECRETION OF YOLK PROTEIN
IN THE LIVER 7ALLACE AND 3ELMAN .AGAHAMA
+ANAMORI !DACHI AND .AGAHAMA 0RO
DUCTION OF THE HORMONE _ `
$0 STIMULATED BY A
GONADOTROPIN SURGE DURING POSTVITELLOGENESIS INITIATES
GERMINAL VESICLE BREAKDOWN '6"$ THE BEGINNING
OF THE PROCESSES THAT CULMINATE IN OOCYTE MATURATION
'OETZ .AGAHAMA AND !DACHI .AGA
HAMA
4HREE SOURCES OF THESE HORMONES HAVE BEEN PRO
POSED THE FOLLICULAR EPITHELIUM THE THECAL LAYERS IN
CLUDING hSPECIAL THECAL CELLSv AND INTERSTITIAL CELLS OF
THE OVARY %VIDENCE HAS BEEN GATHERED FOR A LARGE NUM
BER OF lSH USING HISTOCHEMICAL TESTS FOR THE PRESENCE
OF STEROIDOGENIC ENZYMES SUCH AS `
HYDROXYSTEROID
DEHYDROGENASE `
(3$ MORE RECENTLY IMMUNOCY
TOCHEMICAL METHODS HAVE BEEN USED !LTHOUGH ULTRA
STRUCTURAL EVIDENCE FOR STEROIDOGENESIS HAS OFTEN BEEN
RECORDED IT IS EQUIVOCAL 6ARYING PATTERNS OF STEROIDO
GENESIS THEREFORE HAVE BEEN PROPOSED FOR THE FOLLICLES
OF DIFFERENT GROUPS OF lSH "EARING IN MIND THE VAST
RANGE OF REPRODUCTIVE STRATEGIES FOUND IN lSH HOW
EVER THIS IS NOT SURPRISING
!N EXPLANATION FOR SOME OF THE DILEMMA AT LEAST
FOR SALMONIDS IS PROVIDED BY THE 47/
#%,,
490% -/$%,
THAT PROPOSES A SYNERGISM BETWEEN THE THECAL AND FOL
LICULAR CELLS WHERE THECAL CELLS SYNTHESIZE THE PRECUR
SORS TESTOSTERONE AND _
HYDROXYPROGESTERONE FOR
CONVERSION BY FOLLICULAR CELLS TO THE HORMONES OESTRA
DIOL
` AND _ `
$0 RESPECTIVELY &IGURE
+AGAWA ET AL .AGAHAMA +AGAWA AND 9OUNG
.AGAHAMA +ANAMORI !DACHI AND
.AGAHAMA )T IS SUGGESTED THAT THE TWO
CELL
TYPE MODEL AT LEAST FOR THE PRODUCTION OF OESTRADIOL
` ALSO APPLIES TO THE OVARY OF TILAPIA /REOCHROMIS
NILOTICUS .AKAMURA 3PECKER AND .AGAHAMA
!CCORDING TO THE TWO
CELL
TYPE MODEL DURING VI
TELLOGENESIS THE THECAL LAYERS PRODUCE AROMATIZABLE
ANDROGENS MAINLY TESTOSTERONE IN RESPONSE TO GO
NADOTROPIN THESE ARE CONVERTED TO OESTRADIOL
` BY
AROMATASE ENZYME SYSTEMS PRESENT IN THE FOLLICULAR
LAYER +AGAWA ET AL .AGAHAMA 9OUNG
+AGAWA AND .AGHAMA *UST PRIOR TO
OOCYTE MATURATION GONADOTROPIN STIMULATES THECAL
LAYERS TO PRODUCE _
HYDROXYPROGESTERONE THIS IS
CONVERTED TO _ `
$0 BY FOLLICULAR LAYERS WHERE
GONADOTROPIN HAS INDUCED THE ACTIVITY OF `
HY
DROXYSTEROID DEHYDROGENASE THE ENZYME INVOLVED IN
THIS CONVERSION .AGAHAMA 9OUNG !DACHI AND
.AGAHAMA ! SINGLE POPULATION OF RECEPTORS FOR
GONADOTROPIN ON BOTH THECAL AND FOLLICULAR CELLS OF THE
AMAGO SALMON /NCORHYNCHUS RHODURUS +ANAMORI
AND .AGAHAMA A STIMULATE STEROIDOGENESIS
BY MECHANISMS INVOLVING ADENYLATE CYCLASECYCLIC
!-0 C!-0 &IGURE +ANAMORI AND .AGAHA
MA B 4HE SHIFT IN STEROIDOGENIC RESPONSIVENESS
OF THESE CELLS TO GONADOTROPIN APPEARS TO RESULT FROM
A CHANGE IN CELLULAR EVENTS AT A STEPS SUBSEQUENT TO
C!-0 PRODUCTION
4HE TWO
CELL
TYPE MODEL PROVIDES AN EXPLANA
TION FOR THE SPARSE ULTRASTRUCTURAL AND HISTOCHEMICAL
#(!04%2
EVIDENCE OF STEROIDOGENESIS BY PREOVULATORY FOLLICU
LAR CELLS WHICH OFTEN MANIFEST ORGANELLES TYPICAL OF
PROTEIN SECRETING CELLS .AGAHAMA #HAN AND (OAR
(OAR AND .AGAHAMA -ATSUYAMA .AGA
HAMA AND -ATSUURA 3INCE SEVERAL BIOCHEMI
CAL STEPS ARE INVOLVED IN THE PRODUCTION OF TESTOSTERONE
BY THECAL CELLS THIS IS REmECTED IN THEIR ULTRASTRUCTURAL
APPEARANCE OF STEROIDOGENESIS &IGURE 3ELMAN
ET AL AROMATIZATION OF TESTOSTERONE TO OESTRA
DIOL ` HOWEVER INVOLVES ONLY A FEW STEPS AND THE
ORGANELLES TYPICAL OF STEROIDOGENESIS ARE MASKED BY
THOSE CARRYING OUT OTHER ACTIVITIES WITHIN THE FOLLICULAR
EPITHELIUM +AGAWA ET AL )T MAY BE NOTED IN
THIS REGARD THAT FOLLICULAR CELLS OF COHO SALMON /N
CORHYNCHUS KISUTCH CONTAIN SMALL AMOUNTS OF AGRANU
LAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA WITH
TUBULAR CRISTAE DISTRIBUTED THROUGHOUT THEIR ABUNDANT
PROTEIN PRODUCING ORGANELLES .AGAHAMA #LARKE AND
(OAR
4HE GENERALIZATION CANNOT BE MADE HOWEVER THAT
THE TWO CELL TYPE MODEL OPERATES IN THE OVARIES OF ALL
lSH &OR EXAMPLE IN THE KILLIlSH &UNDULUS HETEROCLI
TUS FOLLICULAR CELLS ARE THE PRIMARY SOURCE OF FOLLICU
LAR STEROIDS IN RESPONSE TO PITUITARY STIMULATION SO THAT
SYNTHESIS OF OESTRADIOL ` AND _ ` $0 DOES NOT
REQUIRE THE INVOLVEMENT OF THECAL CELLS 0ETRINO ET AL
4HECAL CELLS APPEAR TO BE STEROIDOGENIC HOW
EVER IN SPITE OF THEIR NONSTEROIDOGENIC APPEARANCE IT
IS SUGGESTED THAT THEY SYNTHESIZE TESTOSTERONE PROVID
ING A SECOND SOURCE OF AROMATIZABLE SUBSTRATE FOR THE
SYNTHESIS OF OESTRADIOL ` BY FOLLICULAR CELLS
4HERE IS A COMMON STEROIDOGENIC PATHWAY FOR MUCH
OF THE SYNTHESIS OF THE TWO HORMONES WHICH PLAY SUCH
AN IMPORTANT ROLE IN VITELLOGENESIS AND MATURATION OF
OVARIAN FOLLICLES IN TELEOSTS &IGURE +OBAYASHI
ET AL 0RIOR TO OOCYTE MATURATION A DISTINCT
SHIFT OCCURS FROM THE PRODUCTION OF OESTRADIOL `
TO _ ` $0 PROBABLY THE RESULT OF A DECREASE IN
THE ACTIVITY OF THE ENZYME # LYASE CYTOCHROME
0 _ HYDROXYLASE# LYASE )T IS PRESUMED
THAT THE DECREASE IN OESTRADIOL ` PRODUCTION WOULD
LEAD TO AN ACCUMULATION OF _ HYDROXY PROGESTERONE
THE IMMEDIATE PRECURSOR OF _ ` $0
4HREE STEROID HORMONES PLAY A SIGNIlCANT ROLE
IN REGULATING THE WIDE RANGE OF REPRODUCTIVE STRATE
GIES SEEN IN FEMALE ELASMOBRANCHS OESTRADIOL `
TESTOSTERONE AND PROGESTERONE 4SANG AND #ALLARD
#ALLARD ET AL +OOB AND #ALLARD
#ALLARD &ILETI AND +OOB /ES
TRADIOL ` AND TESTOSTERONE ARE ASSOCIATED WITH FOL
LICULAR DEVELOPMENT WHILE PROGESTERONE PLAYS A ROLE IN
EGG RETENTION AND PREGNANCY !S WOULD BE EXPECTED
THE AMOUNTS OF THESE STEROIDS IN THE CIRCULATION mUCTU
ATE WITH THE STAGE IN THE REPRODUCTIVE CYCLE )SOLATED
FOLLICULAR EPITHELIAL CELLS OF SEVERAL SPECIES SYNTHESIZE
SIGNIlCANT QUANTITIES OF TESTOSTERONE OESTRADIOL
`
AND PROGESTERONE WITHOUT REQUIRING THECAL ELEMENTS
4HECAL TISSUE ALONE IN THE PRESENCE OF TESTOSTERONE
IS ABLE TO SYNTHESIZE OESTRADIOL
` AND AN INTERACTION
BETWEEN FOLLICULAR AND THECAL LAYERS IN VIVO IS SUGGEST
ED 4ESTOSTERONE IS THE PREDOMINANT PRODUCT OF THECAL
CELLS AND IS ALSO PRODUCED BY THE CORPORA LUTEA 4HE
CORPORA LUTEA ARE THE PRINCIPAL SOURCE OF PROGESTERONE
IN BOTH VIVIPAROUS AND OVIPAROUS SPECIES
#ONmICTING PICTURES OF OVARIAN STEROIDOGENESIS ARE
SEEN WITHIN THE CYCLOSTOMES .O `
(3$ WAS DE
TECTED IN THE OVARY OF -YXINE GLUTINOSA NOR DID THE
CELLS OF ITS FOLLICLE REVEAL ANY ULTRASTRUCTURAL FEATURES
INDICATIVE OF STEROID PRODUCTION &ERNHOLM
4SUNEKI AND 'ORBMAN 4HE MATURE OVARY OF
%PTATRETUS BURGERI HOWEVER IS CAPABLE OF A RANGE OF
STEROID BIOCONVERSIONS WHEN INCUBATED IN VITRO WITH
VARIOUS PRECURSORS (IROSE ET AL )T IS NOT CLEAR
WHETHER THIS IS A REAL DIFFERENCE BETWEEN THE TWO SPE
CIES OR DIFFERENCE IN THE SENSITIVITIES OF THE TECHNIQUES
USED 4HE THECA INTERNA OF THE PRIMARY FOLLICLE OF
,AMPETRA PLANERI DIFFERENTIATES DURING METAMORPHO
SIS )TS CELLS MANIFEST THE CHARACTERISTIC APPEARANCE
OF STEROIDOGENESIS SOME TIME BEFORE VITELLOGENESIS
CONTAINING ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM
AND LIPID DROPLETS "USSON
-ABILLOT TENTATIVE
HISTOCHEMICAL AND SPECTROPHOTOMETRIC EVIDENCE OF HY
DROXYSTEROID DEHYDROGENASE ACTIVITY HAS BEEN NOTED IN
THESE CELLS 3EILER 3EILER AND #LAUS )N THE OVA
RY OF THE SEA LAMPREY 0ETROMYZON MARINUS HOWEVER
NO CLEARLY DElNED STEROIDOGENIC CELL TYPES WERE FOUND
AND NO `
(3$ WAS DETECTED 7EISBART 9OUSON AND
7IEBE 4HE CELLS OF THE THECA INTERNA OFTEN CON
TAINED LARGE LIPID DROPLETS IN THEIR CYTOPLASM &IGURE
BUT THESE CELLS DID NOT POSSESS OTHER CHARACTERIS
TICS OF STEROID
PRODUCING CELLS
+OOB AND #ALLARD HAVE PROVIDED AN OVERVIEW OF THE
SPECTRUM OF REPRODUCTIVE MODES TOGETHER WITH SPECULATION ON THEIR
HORMONAL REGULATION AS SEEN IN FEMALE ELASMOBRANCHS
/65,!4)/.
#HORION
!S VITELLOGENESIS ENDS AND THE OOCYTE IS READY FOR
OVULATION THE ZONA PELLUCIDA CHANGES ULTRASTRUCTUR
ALLY AND PERHAPS CHEMICALLY 4HE PRIMARY ENVELOPE
BECOMES THINNER AND THE OUTERMOST ZONE IS OFTEN LOST
THE ELABORATE lBRILLAR PATTERNS FADE INTO A HOMOGE
NEOUS TRANSLUCENT ZONE 4HE hARABESQUEv PATTERNS ARE
TRANSFORMED AT OVULATION AND THE CHORION ASSUMES THE
WOVEN APPEARANCE $UMONT AND "RUMMETT OF
A lBROUS LAMINATE THAT STRENGTHENS THE LAYER BY ACT
ING EQUALLY IN ALL DIRECTIONS TO ACCOMMODATE TENSILE
STRESSES &IGURE ! 'RIERSON AND .EVILLE
4HIS TRANSFORMED PRIMARY ENVELOPE IS SOMETIMES COV
ERED BY THE SECONDARY ENVELOPE THAT MAY BE ELABORATE
LY ORNAMENTED &IGURE " 4HE OUTER COVERING OF
THE EGG IS NOW A #(/2)/.
!LTHOUGH THE TERM hCHORIONv HAS BEEN USED IN SEV
ERAL WAYS IT MAY BE DElNED AS THE ACELLULAR HIGHLY
STRUCTURED ENVELOPE ENCLOSING AN OVULATED EGG OR
DEVELOPING EMBRYO SEPARATING IT FROM THE EXTERNAL
ENVIRONMENT (ART 0IETRI AND $ONOVAN 4HE
CHORION IS USUALLY PERFORATED BY A PASSAGE THE -)#2/
09,% THROUGH WHICH A SPERMATOZOON GAINS ACCESS TO
THE OOPLASMIC SURFACE AND EFFECTS FERTILIZATION 4HE
OUTER SURFACE IS OFTEN ADORNED WITH SPECIALIZATIONS IN
THE FORM OF THREADS lLAMENTS lBRILS OR SPIKES
4HE CHORION IS SOFT WITHIN THE OVARY BUT IT BEGINS
TO HARDEN FOLLOWING OVULATION !FTER FERTILIZATION IT
SEPARATES FROM THE SURFACE OF THE OOCYTE AND HARDEN
ING CONTINUES 0ENETRATION BY THE SPERMATOZOON BRINGS
ABOUT AN INCREASE IN CALCIUM CONTENT OF THE PERIPHERAL
OOPLASM CAUSING THE CORTICAL ALVEOLI TO FUSE WITH THE
OOLEMMA THE hCORTICAL REACTIONv BEGINNING AT THE
SITE OF SPERM ENTRY AND PROCEEDING AS A WAVE OVER THE
SURFACE OF THE EGG 5PON FUSION THE VESCLES DISCHARGE
THEIR CONTENTS INTO THE SPACE BETWEEN THE PLASMA MEM
BRANE AND THE CHORION THE 0%2)6)4%,,).% 30!#% !N
ACIDIC GLYCOSAMINOGLYCAN THAT IS TOO LARGE TO PENETRATE
THE CHORION IS RELEASED THEREBY CAUSING AN INCREASE IN
THE OSMOLARITY OF THE PERIVITELLINE mUID RELATIVE TO THE
SURROUNDINGS 3INCE THE CHORION IS PERMEABLE TO WA
TER AND SMALL ELECTROLYTES THERE IS AN INmUX OF WATER
INCREASING THE HYDROSTATIC PRESSURE IN THE PERIVITELLINE
SPACE AND FORCING THE ELASTIC CHORION TO EXPAND AWAY
FROM THE PLASMA MEMBRANE 3UBSEQUENTLY THE CHORION
LOSES ITS ELASTICITY AND BECOMES TOUGH AND RIGID IN THE
PROCESS OF HARDENING 4HE HARDENED CHORION SERVES TO
PROTECT THE EGG FROM MECHANICAL DAMAGE AND MICRO
BIAL ATTACK
)N SOME SPECIES THE MICROVILLI FROM BOTH OOCYTE
AND FOLLICULAR CELLS WITHDRAW FROM THE PORE CANALS AND
THE OUTER OPENINGS MAY BECOME BLOCKED WITH hPLUGSv
&IGURES " # &LGEL A B 3TEHR AND
(AWKES $UMONT AND "RUMMET (ART
AND $ONOVAN )N SOME SALMONIDS HOWEVER THE
MICROVILLI DO NOT WITHDRAW AND HAVE BEEN OBSERVED IN
THE PORE CANALS OF OVULATED EGGS 3CHMEHL AND 'RA
HAM )N THE ZEBRA DANIO "RACHYDANIO RERIO
MOST OF EACH PORE CANAL REMAINS OPEN EXCEPT FOR THE
PLUG PRESUMABLY DEPOSITED ON THE WITHDRAWAL OF
THE MICROVILLI BY A MECHANISM NOT UNDERSTOOD (ART
AND $ONOVAN
2EMNANTS OF THE PRIMARY ENVELOPE PERSIST AS A l
BROUS LAMELLAR COAT IN THE CHORION OF A WIDE RANGE OF
SPECIES 4HIS MAY BE SURROUNDED BY JELLY COATS lLA
MENTS AND ORNAMENTATION PROVIDED BY THE SECONDARY
ENVELOPE ! SIMPLE CHORION SAID TO BE DERIVED SOLELY
FROM THE PRIMARY ENVELOPE IS FOUND ON THE EGG OF THE
ZEBRA DANIO (ART AND $ONOVAN )T IS TO
M THICK AND CONSISTS OF THREE ZONES PORE CANALS
PENETRATE THE INNER TWO ZONES ONLY &IGURE !
4HE /54%2 ,!9%2 IS ABOUT M THICK HOMOGENEOUS
ELECTRON DENSE AND EVENLY DISPERSED OVER THE SUR
FACE IT IS ADORNED WITH PROMINENT PROJECTIONS &IGURE
# $ISTINCT PLUGS OF OSMIOPHILIC MATERIAL BLOCK
THE OUTER OPENING OF EACH PORE CANAL AT THIS LEVEL
&IGURE " 4HE -)$$,% ,!9%2 ABOUT M
THICK IS OF MEDIUM ELECTRON DENSITY AND HAS A COM
PACT lBRILLAR APPEARANCE 4HE lBRES ABOUT TO
M IN DIAMETER ARE ORGANIZED IN CRISSCROSSING
BUNDLES AROUND THE PORE CANALS 4HE )..%2 ,!9%2 COM
PRISES MOST OF THE CHORION AND CONSISTS OF HORIZONTAL
ELECTRON DENSE LAMELLAE OF ABOUT EQUAL THICKNESS AL
TERNATING WITH INTERLAMELLAR PORTIONS OF LOWER DEN
SITY 4HE CENTRE TO CENTRE SPACING OF THE PORE CANALS IS
M 4HEIR DIAMETER JUST BELOW THE PLUG IS ABOUT
M WIDENING TO OR M AT THE INSIDE
4HERE ARE ABOUT X PORE CANALS PER EGG
4HE INNER LAYERS OF THE CHORION OF THE MEDAKA
/RYZIAS LATIPES ARE SIMILAR TO THE CHORION OF THE ZE
BRA DANIO EXCEPT THAT THESE ARE ENCLOSED IN A lLAMEN
TOUS COAT DERIVED FROM THE SECONDARY ENVELOPE (ART
0IETRI AND $ONOVAN )WAMATSU 4HE CHO
RION IS ABOUT TO M THICK AND CONSISTS OF THREE
DISTINCT ZONES AN /54%2 :/.% FUZZY ELECTRON LUCENT
ABOUT M THICK A -)$$,% :/.% HOMOGENEOUS
ELECTRON DENSE ABOUT M THICK WITH AN IRREGULAR
INNER BORDER AND AN )..%2 :/.% FORMED OF TO
ELECTRON DENSE LAMELLAE ALTERNATING WITH INTERLAMELLAE
#(!04%2
OF LOWER ELECTRON DENSITY &IGURES ! " 4HE OUTER
SURFACE OF THE CHORION IS RAISED INTO A UNIFORM INTERCON
NECTING SYSTEM OF RIDGES IN A PATTERN OF HEXAGONS AND
PENTAGONS PRESUMABLY THIS PATTERN IS AN IMPRESSION OF
THE FOLLICULAR EPITHELIUM REPRESENTING AN OUTLINE OF THE
CELLS AND THEIR INTERCELLULAR SPACES &IGURES # )
4HE CHORION IS ADORNED WITH TWO TYPES OF lLAMENTS
PRODUCED BY THE FOLLICULAR EPITHELIUM !BOUT TO
!44!#().' &),!-%.43 ORIGINATE FROM THE VEGETAL
POLE AREA OF THE CHORION INTERTWINING TIGHTLY TO FORM
A ROPELIKE CORD &IGURE ) THAT JOINS WITH CORDS
FROM NEIGHBOURING EGGS TO FORM A CLUSTER SUSPENDED
WITHIN THE GONODUCT 4HE REMAINDER OF THE CHORION IS
COVERED BY ./.!44!#().' &),!-%.43 OF VARIABLE LENGTH
SOME ARE SHORT AND STUBBY WHILE OTHERS TAPER INTO LONG
THREADLIKE PROCESSES THAT INTERTWINE WITH lLAMENTS
ON ADJACENT EGGS PRODUCING A GOSSAMER NETTING THAT
SERVES TO MAINTAIN THE INTEGRITY OF THE EGG CLUSTER "OTH
TYPES OF lLAMENTS ARE FORMED OF DENSELY PACKED TU
BULES MICROTUBULES OR hMICROTUBULE MIMICSv WITH AN
AVERAGE OUTSIDE DIAMETER OF APPROXIMATELY AND
NM RESPECTIVELY &IGURES % TO ( (ART 0IE
TRI AND $ONOVAN 4HE WALL OF EACH MICROTUBULE
IS CYLINDRICAL AND IS COMPOSED OF GLOBULAR SUBUNITS AR
RAYED IN LONGITUDINAL ROWS &OURTEEN OF THESE STRUCTUR
AL SUBUNITS ARE RANGED AROUND THE WALL OF EACH TUBULE
)N MATURE OOCYTES OF THE MEDAKA /RYZIAS LATIPES THE
LONG ATTACHING lLAMENTS ARE WOUND SPIRALLY ON THE AXIS
BETWEEN THE ANIMAL AND VEGETAL POLES &IGURE
)WAMATSU 4HE SHORT NON ATTACHING lLAMENTS
DISTRIBUTED ON THE REST OF THE CHORIONIC SURFACE ARE ALSO
BENT IN A UNILATERAL DIRECTION ON THE EGG AXIS 4HIS SPI
RALING CAN BE EITHER RIGHT HANDED OR LEFT HANDED AND
IS ESTABLISHED EARLY IN OOGENESIS )T APPEARS NOT TO BE
AN INHERITED PATTERN BUT IS IMPOSED DURING OOGENESIS
BY ROTATION OF THE OOCYTE AND ITS FOLLICULAR EPITHELIUM
WITHIN THE BASEMENT MEMBRANE
#ROSS FRACTURES THROUGH THE GLUTARALDEHYDE lXED
CHORION OF /RYZIAS INDICATE THAT THE LAMELLAE ARE SHEETS
OF TIGHTLY PACKED INTERWOVEN lBRES OFTEN ENCLOSING
TEARDROP SHAPED CAVITIES MEASURING ABOUT BY
M (ART 0IETRI AND $ONOVAN 4HE LAYERING OF
THESE lBROUS SHEETS IS PRESUMABLY THE STRUCTURAL AND
PHYSICAL BASIS FOR MECHANICAL STABILITY AND TOUGHNESS
4HE lBRES APPEAR TO BE FORMED OF A HETEROGENEOUS
FAMILY OF HIGH MOLECULAR WEIGHT GLYCOPROTEINS 4HE
SMALL TEARDROP SHAPED HOLES MAY REPRESENT REMNANTS
OF THE PORE CANALS 4HE LAMELLAE OF THE INNER ZONE
OF /RYZIAS ARE CONTINUOUS AND UNINTERRUPTED BY PAT
ENT PORE CANALS 4HE INNER SURFACE OF THE CHORION IS
PEBBLED WITH REGULARLY SPACED BULGES FORMED BY THE
BULBLIKE BASES OF BOTH TYPES OF lLAMENTS WHICH ARE
lRMLY ROOTED WITHIN THE LAMELLAE OF THE INNER ZONE OF
THE CHORION &IGURE $
!NALYSES OF THE PROTEINS OF THE CHORION HAVE UTILIZED
THE (!4#().' %.:9-% A PROTEOLYTIC ENDOPROTEASE THAT
BREAKS DOWN THE CHORION DURING HATCHING 3CHOOTS ET
AL )N THE ANNUAL lSH .OTHOBRANCHIUS KORTHAU
SAE WHICH HAS A RELATIVELY THICK ENVELOPE THE INNER
ZONE OF THE CHORION IS ENTIRELY DIGESTED BUT IN THE
PIKE %SOX LUCIUS AND THE ZEBRA lSH "RACHYDANIO RERIO
WHICH HAVE THIN ENVELOPES A DECREASE IN THICKNESS OF
ONLY AND RESPECTIVELY IS OBSERVED 4HE IN
NER LAYER OF THE CHORION APPEARS TO BE THE NATURAL SUB
STRATE FOR THIS ENZYME (ISTOCHEMICAL AND BIOCHEMICAL
INVESTIGATIONS UTILIZING THIS ENZYME HAVE SHOWN THAT
THE INNER LAYER CONSISTS OF PROTEINS AND GLYCOPROTEINS
(AGENMEIER )UCHI AND 9AMAGAMI /N
THE BASIS OF BIOCHEMICAL ANALYSES OF THE PROTEOLYTIC
PRODUCTS OF THE INNER LAYER OF THE MEDAKA 9AMAGAMI
SPECULATES THAT SIX GLYCOPROTEINS RANGING IN
MOLECULAR WEIGHT FROM TO K$A WITH A REPEATING
POLYPEPTIDE UNIT OF ABOUT K$A ARE LINKED TO FORM
THE LAMELLAE WHILE THE INTERLAMELLAR PORTION MAY BE
AN INTERLINKING OF K$A PROTEINS )N ANOTHER STUDY
THE CHORION OF UNFERTILIZED MEDAKA EGGS WAS SHOWN TO
CONSIST OF TWO MAJOR PROTEINS OF TO AND K$A
AS WELL AS A MINOR K$A PROTEIN )WAMATSU 3HI
BATA AND +ANIE 5PON FERTILIZATION THE MAJOR
PROTEINS ARE POLYMERIZED TO INSOLUBLE HIGH MOLECULAR
WEIGHT PROTEINS BY THE TEMPORARY FORMATION OF SEVERAL
NEW PROTEINS AND K$A THEREBY IN
CREASING TOUGHNESS OF THE CHORION
!NALYSIS OF HOMOGENATES OF ISOLATED CHORIONS FROM
MATURE OVARIAN AND OVULATED EGGS OF #ARASSIUS AURA
TUS BY 3$3 POLYACRYLAMIDE GEL ELECTROPHORESIS SHOWS
THE PRESENCE OF AT LEAST BANDS #OTELLI ET AL
&IVE PRINCIPAL CLASSES WERE RECOGNIZED ! TO % IN OR
DER OF DECREASING SIZES /F THESE THE $ CLASS RANGING
FROM TO K$A WAS THE MOST PROMINENT AND REP
RESENTED ABOUT OF THE TOTAL CHORION COMPONENTS
4HE PRINCIPAL GLYCOPROTEINS FOUND IN THE CHORIONS OF
UNFERTILIZED EGGS OF THE WHITElSH #OREGONUS LAVARETUS
HAVE A MOLECULAR MASS RANGING FROM TO K$A
3CAPIGLIATI ET AL !NALYSIS OF PURIlED CHORION
OF /NCORHYNCHUS MYKISS SHOWED A PATTERN OF FOUR MA
JOR COMPONENTS AND K$ REPRESENT
ING ABOUT OF THE TOTAL PROTEINS "RIVIO "ASSI AND
#OTELLI 4HE AND K$ POLYPEPTIDES ARE
GLYCOSYLATED AND BELONG TO THE hASPARGINE LINKED GLY
/65,!4)/.
COPROTEIN FAMILY 4HIS hSIMPLEv PATTERN OF THE CHORION
OF / MYKISS MAY REmECT ITS APPARENT HOMOGENEITY AS
OBSERVED WITH THE ELECTRON MICROSCOPE COMPARED TO
OTHER SPECIES #OTELLI ET AL
4HE SECONDARY ENVELOPE MAY PRODUCE FANTASTIC
ORNAMENTATION /N THE PELAGIC EGGS OF THE #
/ SOLE
0LEURONICHTHYS COENOSUS IT FORMS ROUGHLY HEXAGONAL
COMPARTMENTS ABOUT M ACROSS WITH WALLS ABOUT
M HIGH AND TO M THICK &IGURE 3TEHR
AND (AWKES 4HE mOOR OF EACH COMPARTMENT
IS PERFORATED BY REMNANTS OF THE PORE CANALS EACH
PORE BEING SURROUNDED BY A SUBPATTERN OF POLYGONAL
RIDGES )T IS SUGGESTED THAT THIS COMPLEX CHORION MAY
INmUENCE BUOYANCY OF THE EGG IT MAY ALSO STRENGTHEN
THE EGG SURFACE AND ACT AS A RESILENT BUMPER 0ERHAPS
THE MOST ELABORATE SECONDARY ENVELOPE OF ANY SPECIES
SO FAR DESCRIBED IS THAT OF THE hANNUALv CYPRINODONTS
#YNOLEBIAS MELANOTAENIA AND # LADIGESI WHERE THE
EGGS MUST SURVIVE IN DAMP SOIL DURING 3OUTH !MERICAN
DRY SEASONS WHEN THEIR AQUATIC HABITAT DRIES 7OURMS
7OURMS AND 3HELDON 4HE SURFACE OF THE
EGG BRISTLES WITH UNIFORMLY SPACED HOLLOW CONICAL
PROJECTIONS ABOUT MM LONG THAT TERMINATE AS A
CROWN OF RECURVED SPIKES &IGURE 4HIS ORNAMEN
TATION OF ELABORATE CHORIONIC EXTENSIONS MAY FUNCTION
AS hGILLSv FOR THE LONG PERIODS SPENT IN DAMP SOIL 4HEY
MAY ALSO PROVIDE AN ANCHOR FOR PERIODS OF mOODING
AND BE SHOCK ABSORBERS TO PROTECT THE EGG FROM SHARP
PARTICLES IN THE SOIL
3OMETIMES THE SECONDARY ENVELOPE IS COATED WITH A
GELATINOUS MATERIAL THAT PROBABLY CONTRIBUTES TO THE AD
HESIVENESS OF THE EGG 4HE DEMERSAL EGGS OF THE BLENNY
"LENNIUS PAVO ARE ATTACHED TO THE SUBSTRATUM BY AN AD
HESIVE DISC THAT COVERS ABOUT ONE
THIRD OF ITS SURFACE
0ATZNER 4HIS DISC CONSISTS OF A TANGLED MESH
OF hANCHORING lLAMENTSv &IGURES ! " ATTACHED
TO THE REMAINDER OF THE CHORION BY BRANCHING ROOT
LIKE
STRUCTURES 4HE MICROPYLE IS LOCATED AT A NAKED AREA AT
THE CENTRE OF THIS ADHESIVE DISC &IGURES % & PRE
SUMABLY THE SPERMATOZOON MAKES ITS ENTRANCE BEFORE
ATTACHMENT OF THE EGG %LECTRON MICROGRAPHS OF CROSS
SECTIONS OF THESE lLAMENTS SHOW A PATTERN OF SUBlLA
MENTS SIMILAR TO THE hMICROTUBULE MIMICSv THAT CONSTI
TUTE THE lLAMENTS SEEN IN &UNDULUS &IGURE $
4HE THICKNESS AND COMPLEXITY OF THE CHORION OF
lSHES SHOW WIDE VARIATION 3TEHR AND (AWKES
,NNING +JRSVIK AND &ALK
0ETERSEN 'ENERAL
LY CHORIONS OF MARINE TELEOST EGGS THAT ARE PELAGIC AND
mOAT FREE IN OPEN WATER ARE THIN WITH A HOMOGENEOUS
LAMELLATED STRUCTURE &IGURE #HORIONS OF DE
MERSAL EGGS ARE USUALLY THICKER WITH A MORE COMPLEX
APPEARANCE THEREBY RESISTING THE MECHANICAL STRESSES
OF DEVELOPMENT ON THE BOTTOM OF A BODY OF WATER )N
LABRIDS VALUES RECORDED IN FRESHLY STRIPPED MATURE
EGGS RANGED FROM A THICKNESS OF M WITH lVE TO
SIX LAMELLAE IN PELAGIC EGGS OF #TENOLABRUS RUPESTRIS
TO A THICKNESS OF M WITH ABOUT LAMELLAE IN
THE DEMERSAL EGGS OF #ENTROLABRUS EXOLETUS ,NNING
)T SHOULD BE NOTED HOWEVER THAT THE CHORION OF
SEVERAL PLEURONECTIDS WITH PELAGIC EGGS RANGES FROM
M WITH SIX TO NINE LAMELLAE IN ,IMANDA LIMANDA
0LATICHTHYS mESUS AND (IPPOGLOSSOIDES PLATESSOIDES
TO M WITH lVE LAMELLAE IN 0LEURONECTES PLATES
SA 4HE CHORION OF THE PELAGIC EGGS OF THE COD 'ADUS
MORHUA HAS lVE LAMELLAE AND IS M THICK
$ISTINCTIVE FEATURES OF THE CHORION HAVE BEEN USED
TO DIFFERENTIATE THE EGGS OF SEVERAL SPECIES BY MEANS OF
TRANSMISSION AND SCANNING ELECTRON MICROSCOPY &IG
URE *OHNSON AND 7ERNER 3CHMEHL AND
'RAHAM -OOI -OOI 7INTERBOTTOM AND
"URRIDGE ,OUREIRO AND DE 3 4HIAW AND
-ATTEI 4HESE INCLUDE PATTERNS ON THE lBROUS
INNER SURFACE OF THE CHORION AS WELL AS DIFFERENCES IN
lLAMENTS HOOKS THE ADHESIVE LAYER AND PLUGS IN PORE
CANAL OPENINGS ,ITTLE RELATIONSHIP WAS OBSERVED HOW
EVER BETWEEN THE ULTRASTRUCTURE OF THE CHORIONS OF SEV
ERAL SPECIES OF TELEOSTS AND THEIR TAXONOMIC POSITION
,NNING 2ATHER THE STRUCTURE APPEARS TO BE
DETERMINED BY THE REPRODUCTIVE STRATEGY OF THE SPECIES
WITH DEMERSAL EGGS TENDING TO HAVE MORE RESISTANT CHO
RIONS 6ARIATIONS WERE ALSO FOUND IN THE CHORIONS OF THE
SAME SPECIES FROM DIFFERENT GEOGRAPHICAL AREAS THIS
MAY HAVE A GENETIC BASIS -ORIN AND !BLE OR
BE RELATED TO DIFFERENCES IN SALINITY TEMPERATURE AND
VISCOSITY OF THE SEAWATER ,NNING
4HE CHORIONS OF VIVIPAROUS lSH WHERE THE EGGS ARE
PROTECTED WITHIN THE BODY OF THE FEMALE ARE THIN AND
SIMPLE &LEGLER 4HE CHORION SEPARATES FROM
THE EGG AT OVULATION AND ENCLOSES THE EMBRYO UNTIL
HATCHING )N $ERMOGENYS PUSILLUS (EMIRAMPHIDAE
THE CHORION MAY BE PRODUCED BY THE OOCYTE ITSELF COM
PRISING ONLY A PRIMARY ENVELOPE OF TWO LAYERS PERFO
RATED BY FENESTRATIONS CONTAINING MICROVILLI FROM BOTH
THE OOCYTE AND FOLLICULAR CELLS 4HE THICKER INNER LAYER
IS lBRILLAR AND ITS STRUCTURE ALTHOUGH LESS ELABORATE
IS REMINISCENT OF THE hARABESQUESv NOTED IN THE PRIMA
RY ENVELOPE OF OVIPAROUS SPECIES !S THE EGG MATURES
THE PORE CANALS DISAPPEAR THE EXTERNAL LAYER BECOMES
THIN AND IRREGULAR AND THE THICKER INNER LAYER mATTENS
AND BECOMES ALMOST HOMOGENEOUS CONSISTING APPAR
#(!04%2
ENTLY OF lNE lBRILS THE CHORION PERSISTS DURING EM
BRYOGENESIS
4HERE ARE TWO DISTINCTIVE SECONDARY ENVELOPES ON
THE SURFACE OF THE LAMPREY EGG AN !0)#!, 45&4 ON THE
ANIMAL POLE AND AN ELABORATELY TEXTURED !$(%3)6% #/!4
THAT CUPS THE VEGETAL TWO THIRDS OF THE EGG &IGURES
! AND +ILLE 9ORKE AND -C-ILLAN
4HE APICAL TUFT CONSISTS OF TRANSPARENT NON
STICKY GELATINOUS MATERIAL THAT APPEARS TO BE SECRETED
AND MOULDED BY A CAP OF FOLLICULAR CELLS IN THE APICAL
REGION UNDER PHASE CONTRAST OR POLARIZED LIGHT IT IS
SEEN TO CONTAIN MANY lNE lBRILS &IGURES # AND
! 4HE ADHESIVE COAT IS AN UNUSUAL SECONDARY
ENVELOPE IN THAT IT CONSISTS OF REMNANTS OF SPECIALIZED
FOLLICULAR CELLS THE !$(%3)6% #%,,3 THAT BREAK DOWN
DURING OVULATION 9ORKE AND -C-ILLAN
$URING MATURATION THESE FOLLICULAR CELLS ENLARGE AND
BECOME PACKED WITH HUGE SACCULES &IGURE )N
ADDITION THEIR CYTOPLASM CONTAINS ABUNDANT GRANULAR
ENDOPLASMIC RETICULUM AND MITOCHONDRIA 'OLGI COM
PLEXES AND AGRANULAR ENDOPLASMIC RETICULUM ARE LIM
ITED TO THE CYTOPLASM ADJACENT TO THE ZONA PELLUCIDA
4HE NUCLEUS IS LOCATED IN AN EXTREME BASAL POSITION
TOWARD THE OVERLYING THECA AND THE ENTIRE SURFACE
OF THE CELL IS COVERED WITH MICROVILLI WHICH ON ONE
SIDE ARE IN CONTACT WITH THE ZONA PELLUCIDA 4HE SAC
CULES ARE FORMED BY THE COALESCENCE OF TWO TYPES OF
MEMBRANE BOUND VESICLES THAT ARE PRODUCED BY THE
'OLGI COMPLEX AND GRANULAR ENDOPLASMIC RETICULUM
RESPECTIVELY &IGURE "USSON -ABILLOT B
$URING OVULATION THE ADHESIVE CELLS BREAK DOWN
BEGINNING IN REGIONS ADJACENT TO THE ZONA PELLUCIDA
&IGURES ! " 9ORKE AND -C-ILLAN
4HE INTRACELLULAR SACCULES BECOME ATTACHED TO
THE ZONA PELLUCIDA FORMING THE ELABORATE ADHESIVE
COAT &IGURE $ ! SIMILAR SORT OF ADHESIVE COAT
IS DESCRIBED ON THE EGGS OF THE CLUPEID $OROSOMA
PETENENSE WHERE THE FOLLICULAR CELLS ARE RETAINED ON THE
SURFACE OF THE ZONA PELLUCIDA AFTER OVULATION 3HELTON
4HIS EPITHELIUM IS SAID TO TRANSFORM DIRECTLY
INTO A FUNCTIONAL STICKY EGG MEMBRANE
! BRIEF DESCRIPTION OF THE CHORION OF THE HAGlSH
%PTATRETUS STOUTI INDICATES A SIMILAR SORT OF COMPLEX
LAMELLAR CHORION IN THIS DISTANTLY RELATED SPECIES +OCH
ET AL )T IS VARIABLE IN THICKNESS BUT ABOUT
M THICK IN THE lGURE SHOWN &IGURE )T CON
SISTS OF THREE LAYERS AN OUTER COLUMNARGLOBULAR RE
GION A MIDDLE REGION OF TO HORIZONTAL LAMELLAE
AND AN INNER DENSE LAYER
-ICROPYLE
4HE TOUGH CHORION OF TELEOST EGGS IS IMPENETRABLE TO
SPERMATOZOA AND THE ONLY PASSAGEWAY FOR A SPERMATO
ZOON TO FERTILIZE THE EGG IS BY WAY OF A PORE THAT PEN
ETRATES THE CHORION AT THE ANIMAL POLE THE -)#2/09,%
3INCE TELEOSTEAN SPERMATOZOA LACK ACROSOMES AND
NEED NOT DISSOLVE THE EGG MEMBRANE TO REACH THE EGG
SURFACE THEY DO NOT REQUIRE CAPACITATION BEFORE THEY
CAN ATTACH AND FUSE WITH THE OOLEMMA )WAMATSU )SHI
JIMA AND .AKASHIMA 4HE lRST SPERMATOZOON
REACHES THE MICROPYLE WITHIN SECONDS OF INSEMINATION
AND ENTERS TO INTERACT WITH MICROVILLI OF THE 30%2- %.
429 3)4% ON THE OOLEMMA &IGURES AND /HTA
AND )WAMATSU 7OLENSKI AND (ART A "ERN
AND !VTALION 4HE MICROPYLE THEREFORE ORIENTS
THE POSITION OF SPERM ENTRY TO A REGION ON THE ANIMAL
POLE NEAR THE EGG NUCLEUS 4HE SPEED OF SPERMATO
ZOA OF THE MEDAKA /RYZIAS LATIPES DECREASES AS THEY
MOVE DOWN THE MICROPYLAR CANAL TOWARD THE OOLEMMA
&IGURE )WAMATSU )SHIJIMA AND .AKASHIMA
)SHIJIMA (AMAGUCHI AND )WAMATSU
&OLLOWING ATTACHMENT OF THE SPERMATOZOON TO THE EGG
MICROVILLI THE SPERM HEAD IS RAPIDLY ENGULFED BY FU
SION OF THE PLASMA MEMBRANES OF THE INTERACTING GAM
ETES )MMEDIATELY AFTER THIS RAPID RESPONSE THE EGG
PLASMA MEMBRANE ELEVATES TO FORM THE NIPPLE
SHAPED
&%24),):!4)/. #/.% INTO WHICH THE ENTIRE SPERM HEAD
MIDPIECE AND A PORTION OF THE mAGELLUM ARE ABSORBED
)N EGGS OF THE ZEBRA DANIO "RACHYDANIO RERIO THIS
OCCURS BETWEEN ONE AND TWO MINUTES AFTER INSEMINA
TION 7OLENSKI AND (ART A
4HE MICROPYLAR AREAS OF SALMONID AND HERRING
EGGS POSSESS SOME hSPERM GUIDANCE FACTORSv WHICH
FACILITATE ENTRY OF HOMOLOGOUS SPERMATOZOA INTO THE
MICROPYLE 9ANAGIMACHI ET AL ! SUBSTANCE IN
UNFERTILIZED EGGS OF THE MEDAKA /RYZIAS LATIPES GUIDES
SPERMATOZOA INTO THE MICROPYLE )WAMATSU )SHIJIMA
AND .AKASHIMA 4HIS GUIDANCE FACTOR MAY EXIST
IN THE MICROPYLAR APPARATUS RATHER THAN IN THE PERIVI
TELLINE SPACE OR CORTEX IT LOSES ITS ACTIVITY FOLLOWING
FERTILIZATION 'LYCOPROTEINS OCCURRING IN A hDILUTED
MUCUS AREAv IN THE OUTERMOST LAYER OF THE CHORION OF
UNFERTILIZED EGGS OF THE MEDAKA PLAY AN IMPORTANT ROLE
IN GUIDING SPERMATOZOA INTO THE MICROPYLE )WAMATSU
9OSHIZAKI AND 3HIBATA 4HE REDUCED INCIDENCE
OF SPERM ENTRY INTO MICROPYLES OF FERTILIZED EGGS SEEMS
TO RESULT FROM INACTIVATION OF THESE GLYCOPROTEINS AS
THEY ARE RENDERED INSOLUBLE BY POLYMERIZATION FOLLOW
ING FERTILIZATION
/65,!4)/.
)N THE GRASS GOBY :OSTERISESSOR OPHIOCEPHALUS FOL
LICULAR CELLS PRODUCE A FOREST OF ATTACHMENT lLAMENTS
UP TO M IN LENGTH SURROUNDING THE MICROPYLE &IG
URE 'IULIANINI AND &ERRERO 4HESE SPE
CIALIZATIONS OF THE SECONDARY ENVELOPE FORM A CROWN
ABOUT M IN DIAMETER THAT WOULD APPEAR TO PRESENT
A BARRIER TO SPERM ENTRY 'IULIANINI ET AL 4HE
SPERM HOWEVER ARE ABLE TO PASS THROUGH PERFORATIONS
BETWEEN THE lLAMENT INSERTIONS ON THE CHORION EVEN
WHEN THE EGG ADHERES STRONGLY TO ITS SUBSTRATE TO
REACH THE MICROPYLE &IGURE
3CANNING ELECTRON MICROGRAPHS SHOW THAT ENTRY
TO THE MICROPYLAR CANAL OF MANY SPECIES IS ATTAINED
THROUGH A FUNNEL
SHAPED 6%34)"5,% ON THE OUTER SUR
FACE OF THE CHORION &IGURE 3ZLLSI AND "IL
LARD 3TEHR AND (AWKES +OBAYASHI AND
9AMAMOTO )WAMATSU AND /HTA B /HTA
AND )WAMATSU (ART 0IETRI AND $ONOVAN
7OLENSKI AND (ART A )WAMATSU )SHIJIMA AND
.AKASHIMA )WAMATSU ET AL )N SOME
SPECIES THE VESTIBULE IS SURROUNDED BY SMALL PORES
ANDOR PROTRUSIONS THAT MAY PRODUCE PHEROMONES
ATTRACTING SPERMATOZOA TO THE MICROPYLE 3TEHR AND
(AWKES 3PERMATOZOA OF THE CYPRINIFORM "AR
BUS CONCHONIUS AND THE PERCIFORM ,UCIOCEPHALUS SP
MAY BE GUIDED TO THE MICROPYLE BY AN ELABORATE PAT
TERN OF SPIRAL RIDGES THAT EMBOSS THE CHORION OF THE
ANIMAL POLE ONCE SOME FORM OF SPECIES
SPECIlC CHE
MOATTRACTANT BRINGS THEM CLOSE TO THE EGG &IGURES
AND !MANZE AND )YENGAR 2IEHL AND
+OKOSCHA )N &UNDULUS HETEROCLITUS WHERE l
BRES OF THE SECONDARY ENVELOPE COULD IMPEDE ACCESS
BY SPERMATOZOA A lBRIL
FREE ZONE TO M IN DI
AMETER SURROUNDS THE MICROPYLE +UCHNOW AND 3COTT
/N THE CONTRARY THE PERIMICROPYLAR REGION OF
SEVERAL SPECIES OF CYPRINODONTS IS SURROUNDED BY AD
HESIVE lLAMENTS WHILE THE REST OF THE CHORION EXHIBITS
SIMPLE ORNAMENTATIONS OF VARYING SHAPE &IGURE
4HIAW AND -ATTEI 4HE WALLS OF THE VESTIBULE
IN &UNDULUS ARE STUDDED WITH SMALL TAPERED PROJEC
TIONS &IGURE ! $UMONT AND "RUMMETT
IN "RACHYDANIO RERIO RADIAL FOLDS ADORN THE FUNNEL
(ART AND $ONOVAN %GGS OF THE LEAFlSH .AN
DUS NANDUS .ANDIDAE 0ERCIFORMES ARE ATTACHED TO
PLANTS AND OTHER SUBSTRATES BY A DENSE CARPET OF SHORT
lLAMENTS ARRAYED IN A CIRCULAR AREA AROUND THE MICRO
PYLE &IGURE "RITZ 4HE MICROPYLE OF THE
BLENNY "LENNIUS PAVO IS AT THE CENTRE OF AN ADHESIVE
DISC THAT CONSISTS OF AN ELABORATE MESH OF ANCHORING
lLAMENTS SECONDARY ENVELOPE ATTACHED TO THE CHORION
&IGURES % & 0ATZNER )T IS A CONUNDRUM
HOW SPERMATOZOA PENETRATE THIS JUNGLE OF lLAMENTS TO
REACH THE MICROPYLE OF AN ATTACHED EGG
4HE WALLS OF THE MICROPYLAR CANAL MAY BE SCULPTED
REmECTING THE LAMINAR STRUCTURE OF THE CHORION hGIVING
THE APPEARANCE OF LEAmETS OF AN IRIS DIAPHRAGMv &IGURE
" !NNULAR OR SPIRAL RIB LIKE THICKENINGS ARE OFTEN
OBSERVED WITHIN THE CHANNEL +OBAYASHI AND 9AMA
MOTO 0ATZNER .AKASHIMA AND )WAMATSU
)N SEVERAL SPECIES THE MICROPYLAR OPENING AT
THE BOTTOM OF THE MICROPYLAR CANAL TERMINATES ON THE
INNER SURFACE OF THE CHORION AS A CRATER IN THE CENTRE OF
A BULGE THAT NESTLES SNUGLY AGAINST THE OOLEMMA 3TEHR
AND (AWKES +OBAYASHI AND 9AMAMOTO
/HTA AND )WAMATSU 9AMAMOTO AND +OBAYASHI
)N &UNDULUS THIS OPENING IS TO M IN DI
AMETER AND IS SURROUNDED BY A SMALL SMOOTH LIP $U
MONT AND "RUMMETT
$IFFERENCES IN THE APPEARANCE WITH THE SCANNING
ELECTRON MICROSCOPE OF THE MICROPYLE AND SURFACE PAT
TERNS OF THE CHORION KNOBS PITS ETC HAVE BEEN USED
TO IDENTIFY THE EGGS OF SEVERAL SPECIES OF SALMONIDS
AND A CLASSIlCATION OF THREE CATEGORIES OF MICROPYLES
HAS BEEN SUGGESTED 2IEHL 490% ) HAS A DEEP PIT
AND SHORT CANAL 490% )) A mAT PIT AND LONG CANAL AND
490% ))) A CANAL BUT NO PIT 4HE SIDES OF THE CANALS ARE
OFTEN REINFORCED BY ANNULAR OR HELICOID THICKENINGS
4HE EGGS OF SALMONIDS STUDIED lT INTO CATEGORIES
)) OR ))) )T IS INTERESTING TO NOTE HOWEVER THAT EGGS OF
SOME SPECIES OF 3ALMO ARE CLASSIlED AS 4YPE )) SALAR
ALPINUS AND OTHERS AS 4YPE ))) GAIRDNERI TRUTTA .O
PIT OR VESTIBULE IS SEEN IN THE 4YPE ))) MICROPYLE OF
THE EEL !NGUILLA JAPONICA /HTA ET AL ! SPE
CIES SPECIlC MICROPYLE MAY PRESENT THE INITIAL ISOLAT
ING MECHANISM IN SYMPATRIC SPECIATION ANDOR IS AN
IMPORTANT FEATURE OF SPERM SELECTION 2IEHL
(IRAI HAS DISTINGUISHED NINE SPECIES OF PELAGIC
EGGS BY MEANS OF A SIMPLIlED TECHNIQUE FOR SCANNING
ELECTRON MICROSCOPY
! TAXONOMIC KEY BASED ON CHARACTERISTICS OF THE
MICROPYLE OF UNFERTILIZED EGGS AS SEEN WITH THE SCAN
NING ELECTRON MICROSCOPE HAS BEEN PREPARED FOR FOUR
SPECIES OF 3PARIDAE &IGURE #HEN 3HAO AND
9ANG #LADISTIC ANALYSES OF THE STRUCTURE OF THE
MICROPYLES WERE USED TO SUGGEST GENERIC INTERRELATION
SHIPS BETWEEN THE SPECIES THE RESULTS AGREE WITH CON
CLUSIONS OBTAINED USING MORPHOLOGICAL BIOCHEMICAL
AND MOLECULAR DATA 4HIS STUDY WAS EXTENDED TO FOUR
SPECIES IN THREE OTHER FAMILIES OF 0ERCIFORMES ,I 7U
AND 9ANG ALTHOUGH THE ULTRASTRUCTURE OF THE
#(!04%2
SURFACE OF THE ZONA PELLUCIDA THE DENSITY OF DISTRIBU
TION OF PORES AND THE SIZE OF THE EGGS WERE USEFUL CHAR
ACTERS FOR DISTINGUISHING THE SPECIES THE ULTRASTRUCTURE
OF THE MICROPYLES WAS THE MOST IMPORTANT FEATURE FOR
IDENTIFYING THE EGGS -ICROPYLES IN BOTH OF THESE STUD
IES WERE OF 4YPE )))
%LABORATE SURFACE ARRAYS OF PARALLEL RIDGES ON THE
ZONA PELLUCIDA SUGGEST PHYLOGENETIC RELATIONSHIPS
AMONG CERTAIN ANABANTOID GENERA "RITZ +OKOSCHA
AND 2IEHL 4HESE RIDGES SPIRAL FROM THE 4YPE
) MICROPYLE AND ARE PRESUMED TO ASSIST IN SPERM GUID
ANCE &IGURE 4HREE OF THE GENERA #TENOPS 0ARA
SPHAERICHTHYS AND 3PHAERICHTHYS ARE CONSIDERED TO
BE MEMBERS OF THE FAMILY "ELONTIIDAE ! FOURTH GENUS
,UCIOCEPHALUS IS OFTEN GROUPED ALONE AS A SEPARATE
SUBORDER ,UCIOCEPHALOIDEI .ELSON 3IMILARI
TIES IN THE SPIRAL ARRAYS HAVE BEEN USED AS EVIDENCE
FOR INCLUSION OF ALL FOUR GENERA IN THE !NABANTOIDEI OR
PERHAPS IN A SEPARATE SUBORDER
4HE OOLEMMA BELOW THE MICROPYLE IS THE 30%2- %.
429 3)4% &IGURE "RUMMETT AND $UMONT
(ART AND $ONOVAN /HTA AND )WAMATSU
7OLENSKI AND (ART A /HTA 4HIS REGION
OF THE EGG OF "RACHYDANIO CONFORMS TO THE SHAPE OF
THE INNER SURFACE OF THE MICROPYLE RESULTING IN A DEEP
DEPRESSION OF ITS SURFACE &IGURE ! 4HE PLAS
MALEMMA OF THIS REGION DIFFERS FROM THE REST OF THE
EGG SURFACE OFTEN DISPLAYING A DISTINCT CLUSTER OF
TO MICROVILLI &IGURES " AND ! 4HE RE
MAINDER OF THE OOLEMMA SURROUNDING THIS AREA MAY BE
CONTOURED BY INTERCONNECTING SMALL FOLDS OR MICROPLI
CAE 4HE lRST POLAR BODY OR A SCAR WHICH MARKS ITS
FORMER POSITION CAN USUALLY BE FOUND ABOUT M
FROM THE CENTRE OF THE SPERM ENTRY SITE IN THE EGGS OF
&UNDULUS HETEROCLITUS "RUMMETT AND $UMONT
! BAND OF COMPACT HOMOGENEOUS ELECTRON
DENSE
MATERIAL SPREADS OUT FOR SOME DISTANCE IN THE OOPLASM
BENEATH THE SPERM ENTRY SITE &IGURE " /HTA AND
)WAMATSU 7OLENSKI AND (ART A #ORTICAL
GRANULES ARE ABSENT FROM THE CYTOPLASM IN THIS REGION
BUT MANY ELONGATE MITOCHONDRIA AND A NUMBER OF FREE
RIBOSOMES HAVE BEEN DESCRIBED &IGURES ! "
%LSEWHERE GRANULAR CORTICAL CYTOPLASM FORMS A UNI
FORMLY THICK BAND BELOW THE OOLEMMA
!LTHOUGH SPERM ENTRY SITES HAVE BEEN LESS EXTEN
SIVELY STUDIED IN NONTELEOSTEAN lSH SEVERAL INTERESTING
EXAMPLES HAVE BEEN RECORDED IN !CIPENSERIFORMES
)N !CIPENSERIDAE THE NUMBER OF MICROPYLES VARIES IN
DIFFERENT FEMALES OF A SPECIES AND ALSO IN THE EGGS OF
ONE FEMALE ,INHART AND +UDO 4HE STURGEON
!CIPENSER STELLATUS HAS FROM ONE TO THERE MAY BE
UP TO IN BELUGA (USO HUSO AND IN THE 2USSIAN
STURGEON !CIPENSER GUELDENSTAEDTI 4HERE ARE THREE TO
MICROPYLES WITHIN TWO LIGHTLY
PIGMENTED RINGS IN
AN AREA OF TO MM AT THE ANIMAL POLE OF THE EGGS
OF !CIPENSER TRANSMONTANUS &IGURE #HERR AND
#LARK 'INSBURG AND $ETTLAFF %ACH MI
CROPYLE HAS A FUNNEL
SHAPED ENTRANCE AND THEIR NUMBER
AND ARRANGEMENT SEEM TO BE CHARACTERISTIC OF A PARTICU
LAR FEMALE -ATURE EGGS OF THE CLOSELY RELATED FAMILY
0OLYODONTIDAE THE PADDLElSH 0OLYODON SPATHULA POS
SESS FROM FOUR TO MICROPYLES IN THE ANIMAL POLE RE
GION &IGURE !S IN MICROPYLES OF OTHER lSH THE
SPERM ENTRY SITE AT THE BOTTOM OF THE MICROPYLE IS ELAB
ORATED TO FORM A TUFT OF MICROVILLI !LTHOUGH THERE HAVE
BEEN DENIALS OF THE PRESENCE OF A MICROPYLE IN EGGS OF
0OLYPTERIFORMES A SINGLE MICROPYLE WAS DEMONSTRATED
AT THE ANIMAL POLE OF EGGS OF 0OLYPTERUS ORNATIPINNIS
&IGURE "ARTSCH AND "RITZ
)N MANY TELEOSTS THE MICROPYLE IS FORMED DURING
VITELLOGENESIS BY A SINGLE FOLLICULAR CELL THAT ENLARGES
AND DIFFERENTIATES TO BECOME THE HIGHLY SPECIALIZED
-)#2/09,!2 #%,, &IGURES ! AND )WAMATSU
ET AL 4HE MICROPYLAR CELL REMAINS ATTACHED BY
TIGHT JUNCTIONS TO THE OOLEMMA BY A THICK CYTOPLASMIC
EXTENSION )WAMATSU .AKASHIMA AND /NITAKE
AND AS THE ZONA PELLUCIDA IS BEING LAID DOWN AROUND
IT MOULDS THE CHANNEL OF THE MICROPYLE THROUGH THIS
LAYER SO THAT FOLDS IN THE WALL OF THE VESTIBULE AND
MICROPYLAR CANAL FORM A REPLICA OF THE SURFACE OF THE
MICROPYLAR CELL &IGURES ! AND ! " !RA
VINDAN AND 0ADMANABHAN 3TEHR AND (AWKES
+OBAYASHI AND 9AMAMOTO )N THE MEDA
KA /RYZIAS LATIPESIT IS SUGGESTED THAT THESE PATTERNS ARE
CARVED BY THE MICROPYLAR CELL DURING OOGENESIS AS A
RESULT OF MOVEMENTS OF THE FOLLICULAR CELLS )WAMATSU
.AKASHIMA AND /NITAKE 4HE FOLDS FORM LEFT
HANDED SPIRAL PATTERNS IN MOST EGGS BUT A FEW SHOW
NO SPIRALLING &IGURES # $ !FTER OVULATION THE
MICROPYLAR CELL IS LOST AND THE MICROPYLE BECOMES THE
PORE THAT ADMITS A SPERMATOZOON TO THE EGG AT THE TIME
OF FERTILIZATION
7ITH THE LIGHT MICROSCOPE THE MICROPYLAR CELL OF
THE LOACH -ISGURNUS ANGUILLICAUDATUS AND SMELT (Y
POMESUS TRANSPACIlCUS NIPPONENSIS CAN EASILY BE DIS
TINGUISHED FROM OTHER FOLLICULAR CELLS AS EARLY AS THE
YOLK VESICLE STAGE OF OOCYTE DEVELOPMENT BY ITS ENOR
MOUS SIZE AND LOW AFlNITY FOR DYES /HTA AND 4ERA
NISHI 4AKANO AND /HTA IN THE MEDAKA
/RYZIAS LATIPES HOWEVER IT STAINS MORE INTENSELY THAN
/65,!4)/.
THE OTHER FOLLICULAR CELLS .AKASHIMA AND )WAMATSU
4HE MICROPYLAR CELL IS CONICAL WITH ITS TAPERED
APEX FACING THE OOLEMMA AND WIDE BASAL SURFACE
ABUTTING PARTLY ON THE FOLLICULAR CELLS OVERLYING IT AND
PARTLY ON THE BASEMENT MEMBRANE OF THE FOLLICULAR EPI
THELIUM
4HE ULTRASTRUCTURE OF THE MICROPYLAR CELL HAS BEEN
DESCRIBED IN DETAIL IN FOLLICLES OF SEVERAL SPECIES 2IE
HL /HTA AND 4ERANISHI +OBAYASHI AND
9AMAMOTO .AKASHIMA AND )WAMATSU
! MICROPYLAR CELL IS NOT DETECTABLE IN PREVITELLOGENIC
OVARIAN FOLLICLES BUT IN THE EARLY VITELLOGENIC PHASE
IT BECOMES DIFFERENTIATED FROM NEIGHBOURING FOLLICU
LAR CELLS BY ITS SLIGHTLY LARGER SIZE AND ELECTRON DENSE
CYTOPLASM &IGURE !S VITELLOGENESIS PROCEEDS
IT ASSUMES THE SHAPE OF A MUSHROOM WITH A LARGE
CELL BODY RESTING IN AN INDENTATION OF THE ZONA PEL
LUCIDA &IGURE %VENTUALLY A THICK PROTOPLASMIC
PROCESS FROM THIS CELL PENETRATES THE ZONA PELLUCIDA
AND EXTENDS TOWARD THE OOLEMMA WITHIN THE -)#2/09
,!2 #!.!, 4HE SURFACE OF THE MICROPYLAR CELL FACING
THE OOLEMMA BEARS SEVERAL SHORT MICROVILLI WHEREAS
ITS OUTER SURFACE SURROUNDED BY POLYGONAL FOLLICULAR
CELLS IS SMOOTH +OBAYASHI AND 9AMAMOTO
7ELL DEVELOPED GRANULAR ENDOPLASMIC RETICULUM
lLLS MOST OF THE MICROPYLAR CELL BODY AND OTHER ORGAN
ELLES ARE PRESENT IN MODERATE AMOUNTS MITOCHONDRIA
'OLGI COMPLEX AGRANULAR ENDOPLASMIC RETICULUM VES
ICLES AND LYSOSOME LIKE BODIES )TS SIZE AND ELECTRON
DENSITY INCREASE WITH VITELLOGENESIS AND THE GRANULAR
ENDOPLASMIC RETICULUM AND 'OLGI COMPLEXES INCREASE
IN ABUNDANCE IN THE CYTOPLASM ADJACENT TO THE ZONA
PELLUCIDA )N SOME SPECIES CISTERNAE OF THE GRANULAR
ENDOPLASMIC RETICULUM ARE EXTREMELY DILATED AND CON
TAIN mOCCULENT MATERIAL GIVING THE CELL A VACUOLATED
APPEARANCE 4AKANO AND /HTA +OBAYASHI AND
9AMAMOTO "UNDLES OF TONOlLAMENTS OCCUPY
THE PERINUCLEAR CYTOPLASM ON THE OPPOSITE SIDE OF THE
CELL &IGURE !
"Y LATE VITELLOGENESIS THE ENLARGED MICROPYLAR CELL
EXTENDS A BROAD CYTOPLASMIC PROCESS THROUGH THE ZONA
PELLUCIDA TO REACH THE OOCYTE SURFACE &IGURE "
4HE PROCESS CONTAINS A CONSPICUOUS CENTRAL CORE OF
PARALLEL BUNDLES OF MICROTUBULES SURROUNDED BY A FEW
NM INTERMEDIATE lLAMENTS AND MICROlLAMENTS !
CONSTRICTION AROUND THE PROCESS A SHORT DISTANCE FROM
THE TIP FORMS A SPHERICAL %.$ "5," CONTAINING FEW OR
GANELLES THAT EXTENDS BEYOND THE MICROPYLAR CANAL TO
INDENT THE SURFACE OF THE OOLEMMA !DHAERENS JUNC
TIONS DEVELOP BETWEEN THE PLASMA MEMBRANES OF THE
END BULB AND OOCYTE OF THE SALMON /NCORHYNCHUS KETA
+OBAYASHI AND 9AMAMOTO &IGURES ! "
4HERE IS THE APPEARANCE OF THE TRANSFER OF MATERIALS
FROM THE END BULB TO THE SPECIALIZED CYTOPLASM OF THE
OOCYTE IN THE MICROPYLAR REGION &IGURE #
)T IS UNCLEAR WHETHER THE MICROPYLAR CANAL IS PRO
DUCED AS THE GROWING ZONA PELLUCIDA IS FORMED AROUND
THE MICROPYLAR PROCESS OR WHETHER THE PROCESS ACTUALLY
BORES ITS WAY THROUGH THIS LAYER 0RESUMABLY THE CELL
BODY AND ADJACENT STRATIlED FOLLICULAR CELLS HOLLOW OUT
THE VESTIBULE 4HE SPIRAL PATTERN OF RIDGES ON THE INSIDE
OF THE MICROPYLAR CANAL OF /RYZIAS MAY BE CARVED BY
THE MICROPYLAR PROCESS ACTING LIKE A SCREW AS IT IT EX
TENDS THROUGH THE ZONA PELLUCIDA TOWARD THE OOLEMMA
.AKASHIMA AND )WAMATSU 4HE FACT THAT THE
OUTER REACHES OF THE CHANNEL ARE LINED BY THE INTURNED
OUTERMOST LAYER OF THE ZONA PELLUCIDA ARGUES IN FAVOUR
OF THE BORING ACTION OF THE MICROPYLAR PROCESS 4HIS
EXPLANATION IS ENHANCED BY THE SCREW
LIKE APPEARANCE
OF THE CYTOPLASMIC PROCESS THAT CONTAINS A TWISTED BUN
DLE OF MICROTUBULES WITH A BUNDLE OF TONOlLAMENTS AT
ITS CORE &IGURE #
!S THE TIME OF OVULATION DRAWS NEAR THE FOLLICULAR
CELLS OVER THE ENTIRE OOCYTE SHOW SIGNS OF DEGENERATION
AS DO THE MICROPYLAR CELL AND THE STRATIlED FOLLICULAR
CELLS OF THE MICROPYLAR REGION +OBAYASHI AND 9AMA
MOTO 4HE MICROPYLAR CELL SHRINKS AND WITH
DRAWS ITS PROCESS PARTIALLY OR COMPLETELY FROM THE
MICROPYLAR CANAL ! BLUNT EXTENSION FROM THE OOCYTE
INVADES THE INNER OPENING OF THE MICROPYLAR CANAL THIS
MAY SIMPLY BE A RESPONSE TO INCREASED INTERNAL PRES
SURE OF THE OOCYTE RESULTING FROM HYDRATION
-UCH INFORMATION FOR THE ESTABLISHMENT OF THE
ANIMAL POLEVEGETAL POLE AXIS IN POSTVITELLOGENIC OO
CYTES AND THEREBY THE ULTIMATE POSITIONING OF THE
MICROPYLE HAS BEEN DERIVED FROM INVESTIGATIONS OF
THE MEDAKA /RYZIAS LATIPES )WAMATSU
)WAMATSU .AKASHIMA AND /NITAKE )WAMATSU
AND .AKASHIMA 4HE lRST INDICATION OF A FUTURE
AXIS IS THE APPARENTLY RANDOM POSITIONING OF THE ELEC
TRON
DENSE lBRILLAR YOLK NUCLEUS DURING THE LATTER PART
OF PRIMARY GROWTH &IGURES AND 0RESUM
ABLY THE YOLK NUCLEUS PRODUCES SOME DIFFUSIBLE SUB
STANCE WHICH REACHES ADJACENT FOLLICULAR CELLS CAUSING
THEM TO ELONGATE AND BECOME ANCHORED TO THE BASE
MENT MEMBRANE IN THE 6%'%4!, 0/,% !2%! %LSEWHERE
THE FOLLICULAR CELLS BECOME DISLOCATED FROM THE BASE
MENT MEMBRANE PERMITTING THE OOCYTE AND ITS JACKET
OF FOLLICULAR CELLS TO ROTATE WITHIN A CHAMBER FORMED OF
THE BASEMENT MEMBRANE SURROUNDED BY THECAL CELLS
#(!04%2
)SOLATED FOLLICLES ARE TRANSLUCENT SO THAT lLAMENTS ON
THE SURFACE OF THE CHORION PROVIDE VISUAL EVIDENCE OF
THIS MOTION &IGURE )WAMATSU ! FOREST
OF lLAMENTS EXTENDS FROM THE CHORION LONG !44!#().'
&),!-%.43 THAT FORM A TANGLED MAT IN THE VEGETAL POLE
AREA AND SHORTER ./. !44!#().' &),!-%.43 ELSEWHERE ON
THE SURFACE &IGURES AND # 4HESE lLAMENTS
EXTEND BETWEEN THE FOLLICULAR CELLS &IGURE AND
AS THE OOCYTE ROTATES THE NON ATTACHING lLAMENTS LINE
UP LIKE REEDS IN A STREAM INDICATING THAT SOME OOCYTES
ROTATE IN A CLOCKWISE DIRECTION OTHERS COUNTERCLOCK
WISE AROUND THE CENTRE OF THE VEGETAL POLE AREA )T IS
SUGGESTED THAT THE POSITION OF THE MICROPYLAR CELL AND
HENCE THE LOCATION OF THE ANIMAL POLE IS DETERMINED
BY THIS MOVEMENT 4HIS ROTATION ENABLES THE LARGE CY
TOPLASMIC EXTENSION OF THE MICROPYLAR CELL TO SCOUR ITS
SPIRAL PATTERN WITHIN THE MICROPYLAR VESTIBULE AND CA
NAL &IGURES ! " AND
4HE MICROPYLAR APPARATUS OF THE HAGlSHES -YX
INE GLUTINOSA AND %PTATRETUS BURGERI ARE SURROUNDED
BY TO ANCHORING lLAMENTS AT THE ANIMAL POLE OF
THE EGG &IGURES ! ! AND # 7ALVIG
&ERNHOLM 0ATZNER +OSMATH
0ATZNER AND !DAM +OCH ET AL $URING
DEVELOPMENT OF THE FOLICLE THE MICROPYLE IS FORMED
BY A STALK OF FOLLICULAR CELLS THAT PERFORATES THE CHO
RION CONTINUING ITS INWARD PROGRESSION TO FORM AN IN
DENTATION OF THE OOLEMMA AT THE ANIMAL POLE &IGURES
" AND ,YNGNES 4HE OUTER OPENING
IS SURROUNDED BY A HONEYCOMB PATTERN OF PARTITIONS AT
THE BASE OF THE FUNNEL &IGURES # $ AND !
7ITH A DIAMETER OF ABOUT M THE MICROPYLE OF %PTA
TRETUS IS LARGE ENOUGH TO ADMIT A SINGLE SPERMATOZOON
BUT SUFlCIENTLY RESTRICTIVE TO PREVENT POLYSPERMY +OCH
ET AL 4HE FUNCTION OF A CHAMBER HOLLOWED OUT
PARTWAY ALONG THE CANAL IS UNEXPLAINED &IGURE "
+OSMATH 0ATZNER AND !DAM
4HERE IS NO MICROPYLE IN THE EGGS OF THE LAMPREYS
,AMPETRA mUVIATILIS AND , PLANERI +ILLE
4HE ENTRY OF SPERMATOZOA IS RESTRICTED TO THE REGION
OF THE APICAL lBROUS TUFT WHICH APPEARS TO ORIENT THE
SPERM HEAD SO THAT IT STRIKES THE CHORION AT AN ANGLE OF
ABOUT 3PERMATOZOA OF LAMPREYS UNLIKE THOSE OF
OTHER lSH POSSESS AN ACROSOME AND IT IS PRESUMED THAT
ENZYMES ARE RELEASED THAT DIGEST A PATH THROUGH THE
CHORION PERHAPS BY WAY OF THE PORE CANALS !FZELIUS
.ICANDER AND 3JDN
/65,!4)/.
&IGURE -ICROGRAPHS OF SECTIONS OF THE OVARY OF THE KILLIlSH &UNDULUS HETEROCLITUS &ROM "RUMMETT $UMONT AND
,ARKIN REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF AN %PON SECTION THROUGH THE WALL AND OVIGEROUS LAMELLA OF A NONGRAVID OVARY -OST FOLLICLES ARE CLOSELY
APPOSED TO THE LAYER DElNING THE LUMEN , OF THE OVARY ! LOOSE STROMA lLLS THE SPACE BETWEEN THE FOLLICLES AND THE OUTER
MUSCULAR TUNIC 4 4HE ARROWS INDICATE ATRETIC OR DEGENERATING POSTOVULATORY FOLLICLES 8
" 0HOTOMICROGRAPH OF AN %PON SECTION THROUGH THE PRESUMED SITE OF OVULATION 4HE LUMINAL EPITHELIUM ,% IS STRETCHED mAT
AND IS CLOSELY APPLIED TO UNDERLYING CONNECTIVE TISSUE AND FOLLICULAR ELEMENTS / OOCYTE 6% ZONA PELLUCIDA 4HERE IS A
YOUNG OOCYTE AT EACH SIDE OF THE SITE 8
# 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE FUTURE OVULATION SITE AND SURROUNDING LIP "LOOD VESSELS "6
COURSE BENEATH THE ROUNDED CELLS OF THE LIP ,0 &LATTENED LUMINAL EPITHELIAL CELLS ,% OVER THE SITE ARE UNDERLAIN BY THEIR
BASAL LAMINA VASCULAR AND STROMAL ELEMENTS 3 THE FOLLICULAR BASAL LAMINA AND THE FOLLICULAR EPITHELIUM &# 8
$ 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE FUTURE OVULATION SITE 4HERE HAS BEEN A PARTIAL FUSION OF THE BASAL
LAMINAE &", OF THE mATTENED LUMINAL EPITHELIAL CELLS ,% AND FOLLICULAR EPITHELIUM &# 3OME STROMAL ELEMENTS 3 ARE
VISIBLE IN THE INTERVENING LAYER 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF THE CYTOPLASM OF A CULTURED FOLLICULAR CELL OF THE MEDAKA /RYZIAS LATIPES
SHOWING THE PRESENCE OF LYSOSOME
LIKE BODIES LY JUST BEFORE OVULATION WAS EXPECTED TO OCCUR 8 &ROM )WAMATSU AND
/HTA A REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
&IGURE h&LUID OF OVULATIONv IN THE FOLLICLE OF THE LAMPREY 0ETROMYZON MARINUS &ROM 9ORKE AND -C-ILLAN
REPRODUCED WITH PERMISSION FROM THE 3OCIETY FOR THE 3TUDY OF 2EPRODUCTION )NC
! 0HOTOMICROGRAPH OF THE APICAL AREA OF THE FOLLICLE AFTER THE FORMATION OF THE mUID OF OVULATION & AT A SITE NEAR THE POINT OF
ENTRY OF A BLOOD VESSEL " 4HE ZONA PELLUCIDA :0 IS ENCLOSED BY THE FOLLICULAR LAYERS ARROW #ORDS OF YOLK
FREE CYTO
PLASM WHITE ARROW EXTEND FROM THE ECCENTRIC NUCLEUS . TO THE SURFACE AND FORM THE POLAR PLASM 00 8
" 4RANSMISSION ELECTRON MICROGRAPH OF THE APICAL REGION OF A FOLLICLE SHOWING THE FOLLICULAR CELLS ENCLOSING THE mUID OF OVULA
TION &/ SEVERAL DAYS PRIOR TO THE EVENTS LEADING TO THE RUPTURE OF THE FOLLICLE 4HERE IS A GREATER ACCUMULATION OF LIPID IN
THIS REGION THAN IN FOLLICULAR CELLS ELSEWHERE IN THE FOLLICLE
!BBREVIATIONS " BLOOD VESSEL )/ INTRAOVARIAN SPACE ,$ LIPID :0 ZONA PELLUCIDA 9 YOLK
/65,!4)/.
&IGURE -ICROGRAPHS OF SECTIONS OF THE FOLLICLE OF THE LAMPREY 0ETROMYZON MARINUS DURING OVULATION &OLLICULAR CELLS
CHANGE SHAPE BEGINNING AT THE mUID
lLLED END OF THE FOLLICLE AS THEY BECOME COLUMNAR THEY FORM A SLEEVE
LIKE CONSTRICTION
THAT GENTLY EXTRUDES THE EGG FROM THE FOLLICLE &ROM 9ORKE AND -C-ILLAN REPRODUCED WITH PERMISSION FROM THE 3OCIETY
FOR THE 3TUDY OF 2EPRODUCTION )NC
! 4RANSMISSION ELECTRON MICROGRAPH &OLLICULAR CELLS IN THE CONSTRICTED APICAL REGION OF THE FOLLICLE ARE MUCH TALLER THAN THE
ADJACENT FOLLICULAR CELLS WHICH FORM A SPHERE CONTAINING lLAMENTOUS MATERIAL AND THE AMORPHOUS REMAINS OF THE mUID OF
OVULATION 4HE THECA IS THICKER AND MORE CONVOLUTED OVER THE COLUMNAR CELLS 8
" 3CANNING ELECTRON MICROGRAPH OF THE APICAL END OF THE FOLLICLE DURING OVULATION 4HE EGG IS EXTRUDED AHEAD OF THE LENGTHEN
ING CONSTRICTION OF THE FOLLICLE 8
!BBREVIATIONS !& APICAL FOLLICULAR CELLS !- AMORPHOUS MATERIAL ", BASAL LAMINA #& COLUMNAR FOLLICULAR CELLS & APICAL
END OF FOLLICLE &- lLAMENTOUS MATERIAL )/ INTRAOVARIAN SPACE - MESOTHELIUM 4 THECA
&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF
FOLLICLES OF THE LAMPREY 0ETROZYZON MARINUS JUST PRIOR
TO ITS RUPTURE &ROM 9ORKE AND -C-ILLAN REPRO
DUCED WITH PERMISSION FROM THE 3OCIETY FOR THE 3TUDY
OF 2EPRODUCTION )NC
! -ICROVILLI -6 FROM THE OOCYTE ARE RETRACTED FROM
CANALICULI IN THE ZONA PELLUCIDA :0 FAINT TRACES OF
THESE CANALICULI MAY BE SEEN 7ITHDRAWAL OF THE MI
CROVILLI CREATES THE PERIVITELLINE SPACE
BETWEEN
THE OOLEMMA AND THE ZONA PELLUCIDA ! CORTICAL AL
VEOLUS 8
" 4WO FOLLICULAR CELLS &# BESTRIDE THE ENTRANCE OF A
BLOOD VESSEL " 4HE mUID OF OVULATION &/ CON
TAINS AMORPHOUS MATERIAL !- 4HE FOLLICULAR LAY
ER IS FOLDED AND THROWN INTO PROJECTIONS ENCLOSING
REMNANTS OF THE INTERCELLULAR SPACES 3 ITS BASAL
LAMINA ", IS HIGHLY CONVOLUTED 4HESE FOLLICULAR
CELLS HAVE ACCUMULATED MANY LIPID DROPLETS ,$
FOLLICULAR CELLS FARTHER FROM THIS CENTRE OF ACTIVITY
DO NOT SHOW THESE CHARACTERISTICS )/ INTRAOVARIAN
SPACE 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH SHOWING AN ATRETIC GERM CELL WITHIN A CLUSTER OF INDIFFERENT GERM CELLS IN
A SECTION OF THE OVARY OF THE MEDAKA /RYZIAS LATIPES ! ANNULATE LAMELLAE 8 'OLGI COMPLEX &ROM (OGAN REPRODUCED
WITH PERMISSION FROM %LSEVIER 3CIENCE
@
&IGURE ,IGHT MICROGRAPHS OF SEC
TIONS OF THE OVARY OF THE BROOK STICKLEBACK
%UCALIA INCONSTANS SHOWING STAGES IN FOLLIC
ULAR ATRESIA &ROM "RAEKEVELT AND -C-IL
LAN REPRODUCED WITH PERMISSION OF
*OHN 7ILEY 3ONS )NC
! 4HE EDGE OF AN UNSPAWNED MATURE OO
CYTE AT AN EARLY STAGE OF ATRESIA 4HE
ZONA PELLUCIDA HAS DISAPPEARED BUT YOLK
9 IS STILL PLENTIFUL &OLLICULAR CELLS
&# ARE HYPERTROPHIED 8
" 0HAGOCYTOSIS IS WELL ADVANCED AT A LATER
STAGE OF ATRESIA LITTLE YOLK 9 REMAINS
8
# ! COLLAPSING FOLLICLE DURING ADVANCED
ATRESIA 8
$ ! BALL OF CELLS THE CORPUS LUTEUM RE
MAINS AT THE END OF THE ATRETIC PROCESS
8
/65,!4)/.
&IGURE ,IGHT MICROGRAPH OF A SECTION OF AN OVARIAN FOLLICLE OF THE SEA LAMPREY 0ETROMYZON MARINUS !TRESIA IS WELL AD
VANCED AND MUCH OF THE OOCYTE HAS BEEN REMOVED AS A RESULT OF EXTENSIVE PHAGOCYTIC INVASION 4HE ZONA PELLUCIDA IS COLLAPSED
BUT THE FOLLICULAR LAYERS REMAIN DISTENDED 0HAGOCYTES CAN BE SEEN INSIDE AND OUTSIDE THE ZONA PELLUCIDA 8 &ROM ,EWIS
AND -C-ILLAN REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE ,IGHT MICROGRAPH OF A SECTION OF THE OVARY OF THE SPINY DOGlSH 3QUALUS SUCKLEYI SHOWING EXTENSIVE FOLDING OF
THE FOLLICULAR EPITHELIUM IN A LARGE ATRETIC FOLLICLE 4HE FOLDS ENHANCE ABSORPTION OF YOLK BY THE FOLLICULAR CELLS &ROM (ISAW AND
(ISAW REPRODUCED WITH PERMISSION
#(!04%2
&IGURE -ICROGRAPHS OF SECTIONS THROUGH ATRETIC FOLLICLES OF THE PERCH 0ERCA mUVIATILIS !LL ARE ELECTRON MICROGRAPHS
EXCEPT FOR $ WHICH IS A PHOTOMICROGRAPH &ROM ,ANG B REPRODUCED WITH PERMISSION OF THE AUTHOR
! %MPTY MEMBRANE BORDERED VESICLES 29/ REMAIN IN THE OOCYTE AFTER THE RESORPTION OF PROTEINACEOUS YOLK PLATELETS 9/
4HE OOPLASM BETWEEN THESE REMNANTS IS lLLED WITH DEGENERATIVE MITOCHONDRIA 8
" 4HE CYTOPLASM OF A FOLLICULAR CELL CONTAINS NUMEROUS CARBOHYDRATE VACUOLES 6 WHOSE CONTENTS ARE BEING RESORBED LOWER
ARROWHEAD AND NUMEROUS SMOOTH
SURFACED VESICLES AND PINOCYTOTIC ELEMENTS UPPER ARROWHEAD -0& BASAL LAMINA OF THE
FOLLICULAR EPITHELIUM 8
# 4HE CYTOPLASM OF A FOLLICULAR CELL CONTAINS A 'OLGI COMPLEX ' GRANULAR ENDOPLASMIC RETICULUM '%2 AND CARBOHYDRATE
VACUOLES 6 ! TEMPORARY GELATINOUS LAYER ', FORMS BETWEEN THE ZONA PELLUCIDA AND THE FOLLICULAR CELLS -0& BASAL
LAMINA OF THE FOLLICULAR EPITHELIUM 8
/65,!4)/.
&IGURE #ONTINUED
$ 0HOTOMICROGRAPH OF THE FOLLICULAR ENVELOPE OF AN ATRETIC OOCYTE 4HE FOLLICULAR CELLS HAVE INVADED THE GELATINOUS LAYER ',
AND CONTAIN LARGE POLYSACCHARIDE GRANULES 2 ZONA PELLUCIDA 8
% 3ECTION OF THE FOLLICULAR ENVELOPE OF AN ATRETIC OOCYTE 4HE GELATINOUS LAYER ', HAS BEEN FRAGMENTED INTO ISLETS WHICH
ARE BEING PHAGOCYTOSED BY THE FOLLICULAR CELLS "OTH THE THECA AND FOLLICULAR EPITHELIUM CONTAIN LEUCOCYTES , AND WANDER
ING CELLS WHICH DISCHARGE THEIR CONTENTS INTO THE OVARIAN LUMEN ARROW -0& BASAL LAMINA OF THE FOLLICULAR EPITHELIUM 8
& !TRETIC OOCYTE SHOWING REMNANTS OF PROTEINACEOUS YOLK PLATELETS 9/ WITH LYSOSOMES 8
#(!04%2
&IGURE #ONTINUED
'
* 4HESE MICROGRAPHS ILLUSTRATE DEGENERATION OF FOLLICULAR AND THECAL CELLS AT A LATER STAGE IN ATRESIA
' ,ARGE FRAGMENTS OF THE ZONA PELLUCIDA 2) AND OTHER LYTIC VACUOLES ARE ENCLOSED WITHIN hOVAL BODIESv -0& BASAL LAMINA
OF THE FOLLICULAR EPITHELIUM 8
( 4HE INTERIOR OF THE OOCYTE HAS BEEN INVADED BY PHAGOCYTIC FOLLICULAR CELLS '# SOME LEUCOCYTES , AND THECAL CELLS 4#
8
) 4HE CONTENTS OF THE hOVAL BODIESv DISINTEGRATE INTO AN ACCUMULATION OF MEMBRANOUS WHORLS AND MYELIN lGURES CHARACTERIS
TIC OF RESIDUAL BODIES OF LYSOSOMAL BREAKDOWN ,Y 8
* ,ARGE LIPID
RICH RESIDUAL BODIES 2,Y WITHIN THE GRANULOSA CELLS ARE ENCLOSED IN DISINTEGRATING STRANDS OF THE OF THE BASAL
LAMINA OF THE FOLLICULAR EPITHELIUM -0& AND ARROWS 8
/65,!4)/.
&IGURE %LECTRON MICROGRAPHS OF SECTIONS THROUGH ATRETIC FOLLICLES OF THE ELECTRIC RAY 4ORPEDO MARMORATA &ROM #HIEFl
"ACCARI ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! )N THIS MICROGRAPH THE ZONA PELLUCIDA HAS DISAPPEARED AND SEVERAL FOLLICULAR CELLS HAVE INVADED THE OOPLASM 4HE FOLLICULAR
CELLS ARE PACKED WITH YOLK PLATELETS AND THEIR PLASMA MEMBRANES HAVE DEVELOPED NUMEROUS UNDULATING FOLDS F WHICH ARE
INDICATIVE OF THEIR PHAGOCYTIC ACTIVITY -ITOCHONDRIA MI HAVE ACCUMULATED IN THE APICAL AND BASAL REGIONS ! FOLLICULAR CELL
AT THE UPPER LEFT IS PACKED WITH LIPID DROPLETS , AND MYELIN lGURES MB THE LIPID DROPLETS ARE SURROUNDED BY ROSETTES OF
GLYCOGEN -EMBRANOUS ENVELOPES ME REMAINING FROM PHAGOCYTOSED YOLK PLATELETS ARE SCATTERED THROUGHOUT THE FOLLICULAR
CAVITY 8
" ! FOLLICULAR CELL IS PACKED WITH PHAGOCYTOSED YOLK PLATELETS Y ENCLOSED BY CONCENTRIC MEMBRANOUS LAMELLAE MI MITO
CHONDRIA 8
# ,ARGE YOLK PLATELETS ARE UNDERGOING DIGESTION 8
$ ! lNAL STAGE IN THE DIGESTION OF A YOLK DROPLET 4HE LIPID , AND CARBOHYDRATE COMPONENTS GLYCOGEN ROSETTES G HAVE
BECOME SEGREGATED 8
#(!04%2
&IGURE #ONTINUED
% ! GLANDULAR CELL FROM A LATE STAGE ATRETIC FOLLICLE CONTAINS A EUCHROMATIC NUCLEUS . AND NUMEROUS MITOCHONDRIA WITH
TUBULAR CRISTAE 8
& 4HE CYTOPLASM OF A GLANDULAR CELL FROM A LATE STAGE ATRETIC FOLLICLE IS PACKED WITH AGRANULAR ENDOPLASMIC RETICULUM G RE
SIDUAL GLYCOGEN GRANULES 8
' ! DEGENERATING GLANDULAR CELL FROM A LATE STAGE ATRETIC FOLLICLE NOTE THE THICKENING OF THE NUCLEAR MEMBRANE AND THE ACCU
MULATION OF MEMBRANOUS WHORLS AND MYELIN lGURES IN THE CYTOPLASM . NUCLEUS 8
/65,!4)/.
&IGURE 0HOTOMICROGRAPHS FROM A SECTION OF A PREOVULATORY ATRETIC FOLLICLE OF THE DOGlSH -USTELUS CANIS 7HEN YOLK HAS
BEEN REMOVED BY PHAGOCYTIC ACTIVITY OF THE FOLLICULAR CELLS ADJACENT FOLDS OF THE FOLLICULAR EPITHELIUM FUSE 4HE THECA INCREASES
IN THICKNESS AND INVADES THE FOLLICULAR TISSUE BECOMING THE DOMINANT TISSUE &ROM 4E7INKEL REPRODUCED WITH PERMIS
SION OF *OHN 7ILEY 3ONS )NC
! &USION OF THE FOLDS OF THE FOLLICULAR EPITHELIUM AND THICKENING OF THE THECA HAS OCCURRED 8
" 4HE SAME SECTION AT HIGHER MAGNIlCATION SHOWS PALE FOLLICULAR CELLS AT THE BOTTOM AND DARKER THECAL CELLS PACKED WITH
GRANULES ABOVE 8
&IGURE %LECTRON MICROGRAPHS OF LIPOFUSCIN PIGMENT IN BODIES REMAINING FROM FOLLICULAR BREAKDOWN IN THE OVARY OF
THE STRIPED BREAM ,ITHOGNATHUS MORMYRUS "ARS M &ROM "ESSEAU AND &ALIEX REPRODUCED WITH PERMISSION FROM
3PRINGER
6ERLAG
! %OSINOPHILIC GRANULOCYTES E' AND FOLLICULAR CELLS &# ARE SEEN IN THE REGION OF FOLLICULAR BREAKDOWN ,IPOFUSCIN PIGMENT
IS SEEN WITHIN A DEGENERATIVE BODY "" 8
" -YELIN lGURES MF AND DEGENERATIVE BODIES "" CONTAINING LIPOFUSCIN PIGMENT LF REMAIN AFTER FOLLICULAR BREAKDOWN
8
#(!04%2
&IGURE %LECTRON MICROGRAPH OF A SECTION OF AN ATRETIC FOLLICLE IN THE OVARY OF THE HAGlSH %PTATRETUS STOUTI 4HECAL
CELLS CONTAIN LYSOSOMES COLLOID DROPLETS GRANULAR ENDOPLASMIC RETICULUM 'OLGI COMPLEX AND MITOCHONDRIA 8
&ROM 4SUNEKI AND 'ORBMAN REPRODUCED WITH KIND PERMISSION OF "LACKWELL 0UBLISHING
!BBREVIATIONS #4 CONNECTIVE TISSUE %# ENDOTHELIAL CELL
&IGURE 0HOTOMICROGRAPH OF A CRYOSTAT SECTION OF THE OVARY OF THE CATlSH -YSTUS CAVASIUS STAINED TO SHOW ` (3$
` HYDROXYSTEROID DEHYDROGENASE ACTIVITY IN THE INTERSTITIAL GLAND CELLS )# "AR M &ROM 3AIDAPUR AND .ADKARNI
REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
/65,!4)/.
&IGURE -ICROGRAPHS OF SECTIONS OF POSTOVULATORY FOLLICLES OF THE TELEOST !STYANAX BIMACULATUS LACUSTRIS ILLUSTRATING PRO
GRAMMED CELL DEATH OR APOPTOSIS &ROM $RUMMOND ET AL REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF A SECTION TAKEN A FEW HOURS AFTER SPAWNING THE FOLLICULAR CELLS & HAVE UNDERGONE HYPERTROPHY
4HE ARROW INDICATES A MICROPYLAR CELL 8
&IGURE #ONTINUED
" %LECTRON MICROGRAPH OF A HYPERTROPHIED FOLLICULAR CELL SHOWING THE ORGANELLES CHARACTERISTIC OF PROTEIN SYNTHESIS WELL
DEVELOPED GRANULAR ENDOPLASMIC RETICULUM 2%2 'OLGI COMPLEX ' AND MITOCHONDRIA - 8
#(!04%2
&IGURE #ONTINUED
# %LECTRON MICROGRAPH OF FOLLICULAR CELLS lXED WITH TANNIC ACID $ARK CELLS WITH ELECTRON DENSE CYTOPLASM MAY BE SLATED FOR
DISINTEGRATION 8
$ %LECTRON MICROGRAPH OF A FOLLICULAR CELL DESTINED FOR DESTRUCTION 4HE CELL RELEASES LARGE ORGANELLE
lLLED BLEBS THE APOPTOPIC
BODIES !" INTO THE LUMEN OF THE FOLLICLE
% %LECTRON MICROGRAPH OF THE lNAL STAGE OF APOPTOSIS WHERE AN APOPTOPIC BODY !" IS BEING PHAGOCYTOSED BY A NORMAL FOL
LICULAR CELL 8
& %LECTRON MICROGRAPH OF A GRANULAR MACROPHAGE IN THE LUMEN OF A POSTOVULATORY FOLLICLE DURING INVOLUTION ! POSSIBLE PHAGO
CYTOSED APOPTOPIC BODY !" IS CONTAINED WITHIN THE CYTOPLASM 8
/65,!4)/.
&IGURE %LECTRON MICROGRAPH OF A PART OF A PHAGOCYTIC FOLLICULAR CELL FROM A POSTOVULATORY FOLLICLE OF THE !FRICAN CATlSH
#LARIAS GARIEPINUS 4HE CELL CONTAINS AUTOPHAGIC VACUOLES !, .5 NUCLEUS 8 &ROM VAN DEN (URK AND 0EUTE
REPRODUCED WITH PERMISSION OF THE AUTHORS
&IGURE 3CHEMATIC DRAWINGS ILLUSTRATING FOUR STAGES IN THE TRANSFORMATION OF A POSTOVULATORY FOLLICLE OF THE PERCH 0ERCA
mUVIATILIS &ROM ,ANG A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 2%/2'!.):!4)/. 0(!3% FOLLOWING OVULATION
" 6!#5/,!2 0(!3% WHERE THE FOLLICLE PREPARES ITSELF FOR SECRETION
# ',/"5,!2 0(!3% WHERE FOLLICULAR CELLS ASSUME THE APPEARANCE OF STEROIDOGENESIS
$ 2%'2%33)/. 0(!3% DEGENERATION OF THE FOLLICULAR CELLS REMAINING AFTER SECRETION
!BBREVIATIONS #4 CONNECTIVE TISSUE &, lBRILLAR LAYER '# FOLLICULAR CELL -0& BASEMENT MEMBRANE OF THE FOLLICULAR EPITHE
LIUM /% OVARIAN EPITHELIUM 4# THECAL CELL
#(!04%2
&IGURE 3CHEMATIC DRAWINGS ILLUSTRATING THE FOLLICULAR ENVELOPES AT FOUR STAGES IN THE TRANSFORMATION OF A POSTOVULATORY
FOLLICLE OF THE PERCH 0ERCA mUVIATILIS &ROM ,ANG A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 2%/2'!.):!4)/. 0(!3% 4HE FOLLICULAR CELLS CONTAIN LARGE AUTOPHAGIC VESICLES ,9
" 6!#5/,!2 0(!3% 3OME FOLLICULAR CELLS STILL CONTAIN LYSOSOMES ,9 AND DEGENERATIVE CYTOPLASM BUT MOST CELLS CONTAIN WELL
DIFFERENTIATED CYTOPLASM WITH AGRANULAR ENDOPLASMIC RETICULUM
# ',/"5,!2 0(!3% 3OME GRANULAR AND AGRANULAR ENDOPLASMIC RETICULUM IS PRESENT WITHIN THE FOLLICULAR CELLS -OST OF THESE
CELLS CONTAIN VACUOLES OF PROTEINACEOUS AND CHOLESTEROL
RELATED MATERIAL
$ 2%'2%33)/. 0(!3% 4HE REMAINING FOLLICULAR CELLS CONTAIN LARGE VACUOLES OF ACID MUCOPOLYSACCHARIDES $6 4HE FOLLICULAR
BASEMENT MEMBRANE HAS DISAPPEARED
!BBREVIATIONS !'%2 AGRANULAR ENDOPLASMIC RETICULUM $'# DEGENERATIVE FOLLICULAR CELL $4# DEGENERATIVE THECAL CELL
&, lBRILLAR LAYER &2 FREE RIBOSOMES ' 'OLGI COMPLEX '%2 GRANULAR ENDOPLASMIC RETICULUM -0& FOLLICULAR BASEMENT
MEMBRANE . NUCLEUS 3' VACUOLES OF PROTEINACEOUS AND CHOLESTEROL
RELATED MATERIAL 4# THECAL CELL 6 ACID MUCOPOLYSAC
CHARIDE VACUOLES
/65,!4)/.
&IGURE %LECTRON MICROGRAPH OF A SECTION OF A POSTOVULATORY FOLLICLE OF THE PERCH 0ERCA mUVIATILIS SHOWING TWO TYPES OF
FOLLICULAR CELLS ONE HOUR AFTER OVULATION 4HE LOWER CELL IS PHAGOCYTIC AND CONTAINS LYSOSOMES 4HE UPPER LIGHTER CELL CONTAINS
MITOCHONDRIA AND AGRANULAR ENDOPLASMIC RETICULUM -0& FOLLICULAR BASEMENT MEMBRANE 8 &ROM ,ANG A REPRO
DUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE -ICROGRAPHS OF SECTIONS OF POSTOVULATORY FOLLICLES OF TILAPIA /REOCHROMIS MOSSAMBICUS ONE DAY AFTER SPAWNING
! IS A PHOTOMICROGRAPH " # AND $ ARE ELECTRON MICROGRAPHS &ROM 3MITH AND (ALEY REPRODUCED WITH PERMISSION OF
THE AUTHORS
! 3EVERAL POSTOVULATORY FOLLICLES 0 PREVITELLOGENIC OOCYTES OF THE PERINUCLEOLAR STAGE 0. OOCYTES AT THE YOLK VESICLE STAGE
6 AND AN OOCYTE AT THE YOLK GRANULE STAGE '2 CAN BE SEEN 8 4HE INSET SHOWS A POSTOVULATORY FOLLICLE AT A HIGHER
MAGNIlCATION WITH ITS OUTER THECAL LAYER 4 AND INNER FOLLICULAR LAYER ' 8
" 7IDE SPACES EXIST BETWEEN CELLS OF THE THECA EXTERNA 4% !LTHOUGH A CELL OF THE THECA INTERNA 4) CONTAINS LIPID DROPLETS
, IT HAS A lBROBLASTIC NOT STEROIDOGENIC APPEARANCE ' FOLLICULAR CELL - MITOCHONDRIA WITH LAMELLAR CRISTAE 8
# #ELL OF THE THECA EXTERNA 4% ATTACHED BY A DESMOSOME $ TO A CELL OF THE THECA INTERNA 4) CONTAINING AGRANULAR ENDO
PLASMIC RETICULUM 3%2 '/ 'OLGI COMPLEX 2%2 GRANULAR ENDOPLASMIC RETICULUM 8
$ 4UBULAR AGRANULAR ENDOPLASMIC RETICULUM 3%2 FROM A SPECIAL THECAL CELL 8
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF POSTOVULATORY FOLLICLES OF TILAPIA /REOCHROMIS MOSSAMBICUS ONE DAY AFTER
SPAWNING &ROM 3MITH AND (ALEY REPRODUCED WITH PERMISSION OF THE AUTHORS
! -ITOCHONDRIA - WITH TUBULAR CRISTAE IN A CELL OF THE THECA INTERNA , LIPID DROPLET 8
" &OLLICULAR CELL WITH BASAL GRANULAR ENDOPLASMIC RETICULUM 2%2 AND SUBAPICAL AGRANULAR ENDOPLASMIC RETICULUM 3%2
2"# A RED BLOOD CELL IN THE FOLLICULAR LUMEN 8
# #OLLAGENOUS lBRES # COURSE BETWEEN THE THECA INTERNA 4) AND THE FOLLICULAR BASAL LAMINA "- 4HE FOLLICULAR CELLS '
CONTAIN AGRANULAR ENDOPLASMIC RETICULUM $ DESMOSOMES - MITOCHONDRIA WITH LAMELLAR CRISTAE 6 VESICLE 8
/65,!4)/.
&IGURE %LECTRON MICROGRAPHS OF A SECTION OF A FOLLICULAR CELL FROM A POSTOVULATORY FOLLICLE OF TILAPIA /REOCHROMIS MOS
SAMBICUS SIX DAYS AFTER SPAWNING 4HE CELL CONTAINS BASAL GRANULAR ENDOPLASMIC RETICULUM 2%2 TUBULAR AGRANULAR ENDOPLAS
MIC RETICULUM 3%2 AND THREE 'OLGI COMPLEXES '/ NEAR THE NUCLEUS . - MITOCHONDRION WITH TUBULAR CRISTAE 8
4HE INSET SHOWS MICROVILLI -6 AND VESICLES AT THE APICAL PLASMA MEMBRANE 8 &ROM 3MITH AND (ALEY
REPRODUCED WITH PERMISSION OF THE AUTHORS
#(!04%2
&IGURE -ICROGRAPHS OF SECTIONS OF POSTOVULATORY OVARIES OF THE RAINBOW TROUT 3ALMO GAIRDNERI &ROM VAN DEN (URK AND
0EUTE REPRODUCED WITH PERMISSION OF THE AUTHOR
! 0HOTOMICROGRAPH OF A SECTION STAINED TO SHOW `
HYDROXYSTEROID DEHYDROGENASE `
(3$ ACTIVITY 3TRONG ACTIVITY IS PRES
ENT IN LARGE NUMBERS OF SPECIAL THECAL CELLS 34# ARRANGED AROUND A YOUNG POSTOVULATORY FOLLICLE BUT ONLY WEAK ACTIVITY IN
THE FOLLICULAR CELLS ' 3T PREVITELLOGENIC FOLLICLE 4 THECA 8
&IGURES " TO % ARE TRANSMISSION ELECTRON MICROGRAPHS
" &OLLICULAR WALL OF A YOUNG POSTOVULATORY FOLLICLE ! FOLLICULAR CELL ' AT THE TOP IS SEPARATED FROM A SPECIAL THECAL CELL 34#
BY THE FOLLICULAR BASAL LAMINA "L AND lBROUS CONNECTIVE TISSUE # OF THE THECAL LAYER 8
# 4HE CYTOPLASM OF A SPECIAL THECAL CELL CONTAINS ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM 3 AND MITOCHONDRIA - WITH
TUBULAR CRISTAE 8
$ ! FOLLICULAR CELL OF A YOUNG POSTOVULATORY FOLLICLE CONTAINS 'OLGI COMPLEXES $ TRANSPORT VESICLES 4V AND LYSOSOMES ,
"L BASAL LAMINA 8
% 4HIS FOLLICULAR CELL FROM A YOUNG POSTOVULATORY FOLLICLE CONTAINS AGRANULAR ENDOPLASMIC RETICULUM 3 AND MITOCHONDRIA
- WITH TUBULAR CRISTAE AND APPEARS TO BE STEROIDOGENIC 4HE INSET SHOWS EXOCYTOTIC ACTIVITY NEXT TO THE BASAL LAMINA OF
THE FOLLICULAR CELL 4V TRANSPORT VESICLE 8
/65,!4)/.
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS FROM POSTOVULATORY FOLLICLES OF MATURE COHO /NCORHYNCHUS
KISUTCH &ROM .AGAHAMA #LARKE AND (OAR REPRODUCED WITH PERMISSION OF THE .2# 0RESS
! 3PECIAL THECAL CELLS 3# FORM A CLUSTER CLOSE TO THE SEROSAL EPITHELIUM 8
" $EGENERATE FOLLICULAR CELLS "- FOLLICULAR BASAL LAMINA , LYSOSOME 8
# 3PECIAL THECAL CELL SHOWING EXTENSIVE AGRANULAR ENDOPLASMIC RETICULUM AND LARGE MITOCHONDRIA WITH TUBULAR CRISTAE
' 'OLGI COMPLEX R%2 GRANULAR ENDOPLASMIC RETICULUM 8
$ 0ORTION OF A SPECIAL THECAL CELL CONTAINING EXTENSIVE AGRANULAR ENDOPLASMIC RETICULUM S%2 AND A LIPID DROPLET ,$
8
#(!04%2
&IGURE -ICROGRAPHS OF SECTIONS OF CORPORA LUTEA OF THE SPINY DOGlSH 3QUALUS ACANTHIAS &ROM +OOB AND #ALLARD
WITH PERMISSION 3 +ARGER !' "ASEL
!
0HOTOMICROGRAPH OF CELLS lLLED WITH LIPID DROPLETS FORMING THE BULK OF THE CORPUS LUTEUM 4HE CELLS ARE DERIVED FROM THE
FOLLICULAR EPITHELIUM AND HAVE LARGE NUCLEI WITH CONSPICUOUS NUCLEOLI 0ARTITIONS BETWEEN THESE CELLS ARE DERIVED FROM
THE FOLLICULAR BASAL LAMINA AND THECAL CONNECTIVE TISSUE "AR M
"
%LECTRON MICROGRAPH OF TWO LUTEAL CELLS FROM ! !BUNDANT LIPID DROPLETS , AND SMALL GRANULES ARROWHEADS PACK
THE CYTOPLASM ' 'OLGI COMPLEX . NUCLEUS "AR M
# $ -ITOCHONDRIA FROM CORPUS LUTEUM SHOWN IN " "AR M
/65,!4)/.
&IGURE 0ATHWAY OF STEROID BIOSYNTHESIS IN THE OVARY OF SALMONIDS ` (3$ ` HYDROXYSTEROID DEHYDROGENASE
` (3$ ` HYDROXYSTEROID DEHYDROGENASE &ROM .AGAHAMA REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL
3OCIETY OF *APAN
&IGURE ! TWO CELL MODEL FOR THE PATHWAY OF STEROID BIOSYNTHESIS IN THE OVARIAN FOLLICLE OF SALMONIDS DURING OOCYTE
GROWTH AND MATURATION SHOWING THE RELATIVE CONTRIBUTION OF THECAL AND FOLLICULAR GRANULOSA CELL LAYERS IN THE PRODUCTION OF
OESTRADIOL ` AND _ ` DIHYDROXY PREGNEN ONE _ ` $0 &ROM .AGAHAMA ET AL REPRODUCED WITH PER
MISSION FROM %LSEVIER 3CIENCE
!BBREVIATIONS 0 SCC CHOLESTEROL SIDE CHAIN CLEAVAGE CYTOCHROME 0 ` (3$ ` HYDROXYSTEROID DEHYDROGENASE
ISOMERASE 0 _ 0 _ HYDROXYLASE ` (3$ ` HYDROXYSTEROID DEHYDROGENASE 0 AROM AROMATASE CYTO
CHROME 0 ` (3$ ` HYDROXYSTEROID DEHYDROGENASE
#(!04%2
&IGURE ! DIAGRAM TO ILLUSTRATE THE RECEPTOR
ADENYLATE CYCLASE
CYCLIC !-0 MECHANISM FOR ACTIVATION OF A FOLLICULAR
GRANULOSA CELL IN THE AMAGO SALMON BY `
(3$ `
HYDROXYSTEROID DEHYDROGENASE &ROM .AGAHAMA REPRODUCED
WITH PERMISSION OF THE AUTHOR
&IGURE %LECTRON MICROGRAPH OF A SPECIAL THECAL CELL 34 WITHIN THE THECA OF A LATE CORTICAL ALVEOLUS
STAGE FOLLICLE
OF "RACHYDANIO RERIO 4HE CELL CONTAINS PROlLES OF AGRANULAR ENDOPLASMIC RETICULUM AND ABUNDANT MITOCHONDRIA 8
4HE INSET SHOWS THAT SOME MITOCHONDRIA ARE PACKED WITH TUBULAR CRISTAE IN A DENSE MATRIX 8 &ROM 3ELMAN ET AL
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
/65,!4)/.
&IGURE 3TEROIDOGENIC PATHWAYS OF OVARIAN OESTRADIOL ` AND BIOSYNTHESIS OF _ ` DIHYDROXY PREGNEN ONE IN
OVARIAN FOLLICLES OF THE MEDAKA DURING VITELLOGENESIS AND OOCYTE MATURATION &ROM +OBAYASHI ET AL REPRODUCED WITH
PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
#(!04%2
&IGURE %LECTRON MICROGRAPH OF A SECTION THROUGH THE FOLLICULAR WALL FROM THE OVARY OF THE LAMPREY 0ETEROMYZON MA
RINUS 4HE SECTION INCLUDES THE ZONA PELLUCIDA : AT THE RIGHT FOLLICULAR CELLS & THECA INTERNA ) THECA EXTERNA % AND THE
COELOMIC EPITHELIUM # ,ARGE LIPID DROPLETS , DISTEND A CELL OF THE THECA INTERNA 8 &ROM 7EISBART 9OUSON AND
7IEBE REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE %LECTRON MICROGRAPHS OF SECTIONS THROUGH THE CHORION OF AN OVULATED EGG OF &UNDULUS HETEROCLITUS &ROM
$UMONT AND "RUMMETT REPRODUCED WITH PERMISSION OF 7ILEY
,ISS )NC A SUBSIDIARY OF *OHN 7ILEY 3ONS )NC
! !S VITELLOGENESIS ENDS AND THE OOCYTE IS READY FOR OVULATION THE ZONA PELLUCIDA CHANGES TO BECOME THE CHORION 4HE ELABO
RATE lBRILLAR PATTERNS OF THIS PRIMARY ENVELOPE HAVE LARGELY DISAPPEARED AND THE PORE CANALS ARE ALMOST TOTALLY OBLITERATED
4HE ENVELOPE IS MORE COMPACT AND HAS ASSUMED A WOVEN APPEARANCE !T THE LOWER LEFT CORNER THE ENVELOPE IS LINED BY
A lLM OF LESS DENSE MATERIAL IT IS COVERED BY A THIN LAYER OF ELECTRON
DENSE JELLY #& CHORIONIC lBRILS 8
" 4HE TRANSFORMED PRIMARY ENVELOPE IS COVERED BY A SPONGY APPEARING JELLY
LIKE SECONDARY ENVELOPE * THAT IS ELABORATELY
ORNAMENTED 4HE EXTERNAL OPENING OF A PORE CANAL 0# IS PLUGGED 8
/65,!4)/.
&IGURE %LECTRON MICROGRAPHS OF THE CHORION OF THE EGG OF "RACHYDANIO RERIO &ROM (ART AND $ONOVAN REPRO
DUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CHORION OF AN UNFERTILIZED EGG SHOWING THE OUTER ELECTRON DENSE
ZONE : MIDDLE lBRILLAR ZONE : AND INNER LAMELLAR ZONE : 4HE SURFACE OF THE CHORION IS COVERED BY A THIN LAYER OF
GRANULAR MATERIAL AND DOME SHAPED ELECTRON DENSE BODIES 0 PORE CANAL 8
" 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH A PORE CANAL 0 WITH ITS PORE PLUG 00 IN THE OUTER ELECTRON DENSE
ZONE : 4HE lBRES OF THE MIDDLE LAYER ARE ARRANGED IN CRISSCROSSING BUNDLES AROUND THE OUTER PORTION OF THE PORE CANAL
8
# 3CANNING ELECTRON MICROGRAPH OF THE OUTER SURFACE OF THE CHORION SHOWING HEMISPHERICAL DOME LIKE PROJECTIONS 8
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF THE CHORION OF THE EGG OF /RYZIAS LATIPES &ROM (ART 0IETRI AND $ONOVAN
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CHORION )T IS COMPOSED OF AN OUTER ELECTRON
LUCENT ZONE :
A MIDDLE ELECTRON
DENSE ZONE : AND AN INNER ZONE : OF TEN TO TWELVE ELECTRON
DENSE LAMELLAE ALTERNATING WITH
INTERLAMELLAE OF LOWER ELECTRON DENSITY 8
" 3CANNING ELECTRON MICROGRAPH OF A FRACTURE SURFACE ACROSS THE CHORION SHOWING THE FEATHER
LIKE lBROUS APPEARANCE OF
THE INNER ZONE 8
# 3CANNING ELECTRON MICROGRAPH OF THE HONEYCOMB SURFACE OF THE CHORION WITH NONATTACHING lLAMENTS 8
$ 3CANNING ELECTRON MICROGRAPH OF A CROSS
FRACTURE OF THE CHORION THROUGH THE REGION BEARING ATTACHMENT lLAMENTS 4HE BASES
OF THE lLAMENTS ARE REmECTED AS HEMISPHERICAL PROTRUSIONS ALONG THE INNER SURFACE 4WO lLAMENTS WERE LOST IN PREPARATION
4HE ARRANGEMENT OF THE LAMELLAE INDICATES THAT THEY NORMALLY WRAP AROUND THE BASE OF THE lLAMENT 8
% 4RANSMISSION ELECTRON MICROGRAPH THROUGH A CROSS SECTION OF THE DISTAL SEGMENT OF A NONATTACHING lLAMENT 8
& 4RANSMISSION ELECTRON MICROGRAPH OF A LONGITUDINAL SECTION OF THE DISTAL SEGMENT OF A NONATTACHING lLAMENT SHOWING
THE ORDERLY ARRANGEMENT OF STRAIGHT UNBRANCHED TUBULES 8
' 4RANSMISSION ELECTRON MICROGRAPH THROUGH A CROSS SECTION OF A NONATTACHING lLAMENT SHOWING ELECTRON
DENSE TUBULES WITH
AN ELECTRON
LUCENT CORE 3OME ELECTRON
DENSE PARTICLES WERE SEEN WITHIN THE TUBULES ARROWS 8
( 4RANSMISSION ELECTRON MICROGRAPH OF THE TUBULES OF THE DISTAL SEGMENT OF A NONATTACHING lLAMENT AS SEEN IN CROSS SECTION
8
) 3CANNING ELECTRON MICROGRAPH AF AN ARRAY OF ATTACHMENT lLAMENTS ORIGINATING FROM A LOCALIZED PORTION OF THE CHORION AND
UNITING TO FORM A ROPE
LIKE CORD 8
/65,!4)/.
&IGURE $IAGRAMS ILLUSTRATING THE PATTERNS OF ATTACHING AND NONATTACHING lLAMENTS ON THE CHORION OF MATURE EGGS OF
THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSU REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
!
!NIMAL POLE 4HE ARROW INDICATES THE MICROPYLE 2IGHT HANDED PATTERN
"
,ATERAL VIEW OF EQUATOR
# # )N THESE VIEWS OF THE VEGETAL POLE THE ATTACHING lLAMENTS EXHIBIT EITHER THE LEFT
HANDED # OR RIGHT
HANDED # SPIRAL
PATTERN
!BBREVIATIONS ! ATTACHING lLAMENTS .! NONATTACHING lLAMENTS
&IGURE -ICROGRAPHS OF THE EGG OF THE BLENNY "LENNIUS PAVO &ROM 0ATZNER REPRODUCED WITH PERMISSION FROM
5RBAN &ISCHER 6ERLAG
! 3CANNING ELECTRON MICROGRAPH OF THE MICROPYLAR REGION SHOWING THE ADHESIVE DISC SURROUNDING THE ENTRANCE TO THE MICRO
PYLE ARROW "AR M
" 3CANNING ELECTRON MICROGRAPH OF THE TRANSITION ZONE BETWEEN THE ADHESIVE DISC WITH ITS ANCHORING lLAMENTS AND THE NAKED
SURFACE OF THE EGG "AR M
# 0HOTOMICROGRAPH OF A SECTION THROUGH THE ADHESIVE DISC SHOWING BRANCHED B AND UNBRANCHED ARROWS PARTS OF THE AN
CHORING lLAMENTS # CHORION "AR M
$ 4RANSMISSION ELECTRON MICROGRAPH OF CROSS SECTIONS THROUGH SEVERAL ANCHORING lLAMENTS ! PATTERN OF SUBlLAMENTS
RESEMBLES THE hMICROTUBULE MIMICSv SEEN IN &IGURE %
#(!04%2
&IGURE #ONTINUED
% & 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION "AR IN % M IN & M
&IGURE ! COMPARISON OF THE EGGS OF SEVERAL SPECIES OF lSH TO DEMONSTRATE THAT THE CHORIONS OF DEMERSAL EGGS ARE USUALLY
THICKER AND HARDER THAN THOSE OF PELAGIC SPECIES &ROM ,NNING +JRSVIK AND &ALK
0ETERSEN REPRODUCED BY PERMISSION
OF 4AYLOR &RANCIS !3
/65,!4)/.
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF THE CHORION OF THREE SPECIES OF FRESHWATER lSH &ROM *OHNSON
AND 7ERNER REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! !LOSA PSEUDOHARENGUS
" /NCORHYNCHUS KISUTCH
# /SMERUS MORDAX
!BBREVIATIONS N NODULE P PORE 0G PLUG SU SUBUNIT
&IGURE $IAGRAM OF THE EGG OF THE LAMPREY ,AMPETRA SP SHOWING THE APICAL TUFT ON THE ANIMAL POLE AND THE ADHESIVE
COAT hSTICKY JELLYv THAT CUPS THE VEGETAL TWO
THIRDS OF THE EGG &ROM +ILLE REPRODUCED WITH PERMISSION FROM %LSEVIER
3CIENCE
#(!04%2
&IGURE $IAGRAMS TO ILLUSTRATE THE ORIGIN AND DEVELOPMENT OF FOLLICULAR SECRETORY GRANULES IN THE OVARY OF THE LAMPREY
,AMPETRA PLANERI &ROM "USSON
-ABILLOT B *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION
! -EMBRANE
BOUND SECRETORY GRANULES APPEAR IN THE FOLLICULAR CELLS AT THE BEGINNING OF INTENSIVE VITELLOGENESIS 4HE GRANULES
CONTAIN A PARACRYSTALLINE lBRILLAR SUBSTANCE F OFTEN ACCOMPANIED BY A DENSE GLOBULE D 'RANULAR ENDOPLASMIC RETICULUM
R IS ABUNDANT NEAR THE GRANULES 4UBULES OF SMOOTH ENDOPLASMIC RETICULUM L APPEAR TO BE CONTINUOUS WITH THE lBRILLAR
GRANULE
" !T ABOUT THE SAME TIME SACCULES S OF THE 'OLGI COMPLEX ' ARE DISTENDED BY A HOMOGENEOUS ELECTRON
LUCENT GRANULAR
SUBSTANCE -EMBRANE
BOUND SECRETION GRANULES CONTAINING A SUBSTANCE STRUCTURALLY IDENTICAL TO THE MATERIAL IN THE 'OLGI
SACCULES GR APPEAR NEARBY
# (ETEROGENEOUS GRANULES FORM QUICKLY BY COALESCENCE OF THE GRANULES SHOWN IN &IGURES ! AND " 4HEY CONTAIN TWO OR THREE
MASSES OF lBRILLAR MATERIAL F A LARGE MASS OF THE GRANULAR SUBSTANCE GR AS WELL AS ONE OR TWO DENSE GLOBULES D
$ 4HE lBRILLAR MASSES F DIMINISH IN VOLUME DURING DEVELOPMENT OF THE HETEROGENEOUS GRANULES AND BECOME SURROUNDED BY
A MESHWORK OF SHORT lBRILS ARROW
% 4HE lBRILLAR MASSES HAVE DISAPPEARED IN THE MATURE GRANULE AND THE GRANULAR MATERIAL HAS ASSUMED A CHARACTERISTIC MARBLED
APPEARANCE MA /NLY THE DENSE GLOBULE D RETAINS ITS EARLIER APPEARANCE
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE CHORION AND OOPLASM O FROM AN OVULATED EGG OF THE HAGlSH %PTATRETUS
STOUTI FRACTURED NEAR THE MICROPYLAR CANAL NOT SEEN 4HE CHORION IS ORGANIZED INTO THREE MAIN ZONES # # AND # 8
"AR M &ROM +OCH ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
/65,!4)/.
&IGURE %LECTRON MICROGRAPHS OF SPERM ENTRY SITES ON EGGS OF THE ROSE BITTERLING 2HODEUS OCELLATUS &ROM /HTA AND
)WAMATSU REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! " 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EGG SURFACE BENEATH THE MICROPYLE -ICROVILLI -6 ARE SEEN
IN " ON THE EGG SURFACE JUST BENEATH THE MICROPYLE ! 8 " 8
# 3CANNING ELECTRON MICROGRAPH OF THE MICROPYLAR APPARATUS AND EGG SURFACE BENEATH THE MICROPYLE OF UNFERTILIZED EGGS
WITH CHORION INTACT 4HERE ARE MICROVILLI AT THE BOTTOM OF THE FUNNEL
SHAPED MICROPYLE 8
!BBREVIATIONS #! CORTICAL ALVEOLUS #( CHORION -0 MICROPYLE 9 YOLK GRANULE
#(!04%2
&IGURE -ICROGRAPHS OF SPERM ENTRY SITES ON EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM 7OLENSKI AND (ART A
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF A SECTION THROUGH THE MICROPYLAR REGION OF AN UNACTIVATED EGG 4HE MICROPYLE CONSISTING OF THE OUTER
VESTIBULE V AND THE INNER MICROPYLAR CANAL C PRODUCES A CONE SHAPED DEPRESSION IN THE EGG SURFACE ! SINGLE LAYER
OF SMALL CORTICAL GRANULES CG LIES BENEATH THE OOLEMMA EXCEPT IN THE REGION OF THE INNER MICROPYLAR APERTURE ARROW
8
" 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE SPERM ENTRY SITE SHOWING MICROVILLI PROJECTING THROUGH THE INNER
MICROPYLAR APERTURE INTO THE MICROPYLAR CANAL C !N ELECTRON DENSE LAYER ARROWS BENEATH THE SPERM ENTRY SITE SPREADS
OUTWARD FOR SOME DISTANCE BELOW THE OOLEMMA 8
# 3CANNING ELECTRON MICROGRAPH OF A CROSS FRACTURE THROUGH THE MICROPYLE lVE SECONDS AFTER INSEMINATION 4HE INNER MICRO
PYLAR APERTURE ARROWS ACCOMMODATES A SINGLE SPERMATOZOON 8
$ 3CANNING ELECTRON MICROGRAPH OF A FERTILIZING SPERM ATTACHED TO THE MICROVILLI OF THE SPERM ENTRY SITE lVE SECONDS AFTER
INSEMINATION "INDING OCCURS ARROW BETWEEN THE MICROVILLI AND THE EQUATORIAL SURFACE OF THE SPHERICAL SPERM HEAD H
8
/65,!4)/.
&IGURE $IAGRAM OF THE STRUCTURE OF THE MICROPYLE OF THE MEDAKA /RYZIAS LATIPES 4HE SPEED OF A SWIMMING SPERMATO
ZOON DECREASES AS IT MOVES DOWN THE MICROPYLAR CANAL TOWARD THE OOLEMMA 4HE INNER DIAMETER )$ AT THE VESTIBULE M
THE OUTER APERTURE M AND THE END OF THE CANAL M ARE INDICATED 4HE INNER WALL OF THE MICROPYLE CONSISTS OF THE
OUTERMOST LAYER /, OF THE CHORION IN THE OUTER TWO THIRDS INCLUDING THE VESTIBULE 6" AND THE INNER LAYERS OF THE CHORION IN
THE INNER ONE THIRD ARROW OF THE MICROPYLE &ROM )WAMATSU )SHIJIMA AND .AKASHIMA REPRODUCED WITH PERMISSION
OF *OHN 7ILEY 3ONS )NC
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR AREA OF MATURE EGGS OF THE GRASS GOBY :OSTERISESSOR OPHIO
CEPHALUS &ROM 'IULIANINI AND &ERRERO REPRODUCED WITH PERMISSION FROM 5NIONE :OOLOGICA )TALIANA
! ! FOREST OF ATTACHMENT lLAMENTS UP TO M IN LENGTH FORMS A CROWN ABOUT M IN DIAMETER AROUND THE MICROPYLE
"AR M
" 4HE MICROPYLAR PIT IS SURROUNDED BY PERFORATIONS ASTERISKS FORMED BY MERGED BASAL lLAMENTS "AR M
# ,ATERAL VIEW OF THE OOCYTE SHOWING A CRIBIFORM COLUMN OF NETTED lLAMENTS RISING FROM THE BASAL PLATE SURROUNDING THE
MICROPYLAR AREA 4HE lLAMENTS DIVIDE AND FRAY DISTALLY "AR M
!BBREVIATIONS ES EGG SURFACE F lLAMENTS FP lLAMENT PLATE M MICROPYLE PC PORE CANAL
/65,!4)/.
&IGURE %NTRY INTO THE MICROPYLAR CANAL OF MANY SPECIES IS ATTAINED THROUGH A FUNNEL
SHAPED VESTIBULE ON THE OUTER
SURFACE OF THE CHORION &ROM )WAMATSU ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
! " 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLES FROM EGGS OF MEDAKA /RYZIAS LATIPES ! AND / MELASTIGMA "
,ONGITUDINAL SECTIONS THROUGH THE MICROPYLES ARE SHOWN IN THE DIAGRAMS BELOW 6" VESTIBULE "ARS M
# $ 0HOTOMICROGRAPHS OF UNFERTILIZED EGGS OF / LATIPES SHOWING A MICROPYLE WITH A LARGE VESTIBULE # AND ONE WITH A SMALL
VESTIBULE $ "ARS M
@
&IGURE 3CANNING ELECTRON MICROGRAPHS OF ARTIlCIALLY FERTILIZED EGGS OF THE GRASS GOBY :OSTERISESSOR OPHIOCEPHALUS
&ROM 'IULIANINI ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 3IDE VIEW OF lLAMENT ADHESION APPARATUS F WITH BASAL PERFORATIONS P ADJACENT TO THE EGG SURFACE E "AR M
" "ASAL PLATE VIEWED FROM THE INNER MICROPYLAR FACE WITH HEADS OF SPERMATOZOA H INSIDE THE ADHESION APPARATUS
"AR M
# "ASAL lLAMENTS FRACTURED TO SHOW TAPERED PERFORATIONS 4HE ARROWS INDICATE THE MINIMUM WIDTH "AR M
$ 0ERFORATIONS P VIEWED FROM THE OUTER SIDE SHOWING RHOMBOID BOTTLENECK "AR M
% 3PERMATOZOON H ENTERING A PERFORATION FROM THE OUTER SIDE .OTE THE mAGELLUM m OF A SPERMATOZOON THAT HAS JUST ENTERED
"AR M
#(!04%2
&IGURE 3PERMATOZOA MAY BE GUIDED TO THE MICROPYLAR REGION OF THE EGG OF THE ROSY BARB "ARBUS CONCHIONUS BY SPI
RAL RIDGES THAT EMBOSS THE CHORION OF THE ANIMAL POLE &ROM !MANZE AND )YENGAR REPRODUCED WITH PERMISSION OF THE
#OMPANY OF "IOLOGISTS ,TD #AMBRIDGE
! $IAGRAM SHOWING THE TRAJECTORIES OF hGUIDEDv G AND hUNGUIDEDv U SPERM IN THE MICROPYLAR REGION 4HE STIPPLED REGIONS
INDICATE RIDGES MP MICROPYLAR PIT
" 3CANNING ELECTRON MICROGRAPH OF THE MICROPYLAR REGION OF AN UNFERTILIZED EGG SHOWING MICROPYLAR RIDGES AND GROOVES
"AR M
# 3CANNING ELECTRON MICROGRAPH OF A FERTILIZED EGG SHOWING MICROPYLAR PIT PLUGGED BY THREE LATE
ARRIVING SPERM ARROW
"AR M
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE EGG OF THE PERCIFORM ,UCIOCEPHALUS SP TO SHOW AN ELABORATE PATTERN OF
SPIRAL RIDGES SURROUNDING THE MICROPYLAR PIT INDICATED BY AN ARROW IN EACH MICROGRAPH &ROM 2IEHL AND +OKOSCHA
REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 6IEW OF THE ENTIRE EGG "AR M
" 3OME OF THE SPIRAL RIDGES ENTER THE MICROPYLAR PIT "AR M
# 4HE MICROPYLE CONSISTS OF THE MICROPYLAR PIT ARROW AND THE MICROPYLAR CANAL AT THE CENTRE "AR M
$ 4HE MICROPYLAR CANAL ARROW IS AT THE CENTRE OF THE MICROPYLAR PIT -0 "AR M
/65,!4)/.
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE EGG OF TWO CYPRINODONTS 4HE MICROPYLAR REGION IS SURROUNDED BY
ADHESIVE lLAMENTS WHILE THE REST OF THE CHORION EXHIBITS SIMPLE ORNAMENTATIONS OF VARYING SHAPE &ROM 4HIAW AND -ATTEI
REPRODUCED WITH PERMISSION OF THE .2# 0RESS
! &UNDULUSOMA THIERRYI 4HE MICROPYLE OPENS THROUGH A VESTIBULE ARROW 4HERE ARE MANY lLAMENTS IN THE REGION OF
THE MICROPYLE & BUT SOME ARE IMPLANTED IN OTHER REGIONS & "AR M
" 4HE MICROPYLAR APPARATUS OF THE EGG SHOWN IN ! 4HE MICROPYLAR CANAL IS BLOCKED BY A PLUG ARROW 3OME lLAMENTS & ARE
IMPLANTED IN THE VESTIBULE 6 "AR M
# %PIPLATYS FASCIOLATUS 4HE SURFACE OF THE EGG IS ORNAMENTED / lLAMENTS ARE CONCENTRATED IN A REGION WITHOUT ORNAMENTA
TION 4HE DOUBLE ARROW INDICATES A lLAMENT THAT IS IMPLANTED IN THE MEDIAN REGION OF THE EGG "AR M
$ %NLARGEMENT OF THE MICROPYLAR REGION OF THE EGG SHOWN IN # /RNAMENTATIONS O VISIBLE ON THE LEFT ARE ABSENT IN
THE MICROPYLAR REGION -2 "AR M
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION OF THE EGG OF &UNDULUS HETEROCLITUS &ROM $UMONT
AND "RUMMETT REPRODUCED WITH PERMISSION OF 7ILEY
,ISS )NC A SUBSIDIARY OF *OHN 7ILEY 3ONS )NC
! 4HE MICROPYLE - IS SITUATED AT THE BASE OF A CONICAL DEPRESSION 4HE WALLS OF THE DEPRESSION ARE ADORNED WITH SMALL
TAPERED lLAMENTS 3URROUNDING THE MICROPYLAR DEPRESSION ARE SEVERAL SHORT AND A FEW LONG ARROW CHORIONIC lLAMENTS
8
" 4HE MICROPYLE IS SURROUNDED BY A RAISED LIP 4HE WALLS OF THE MICROPYLAR CANAL APPEAR LIKE A SERIES OF IRIS DIAPHRAGMS REmECT
ING THE LAMINAR NATURE OF THE CHORION 8
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF A FRESHLY SPAWNED EGG OF THE LEAFlSH .ANDUS NANDUS 4HESE EGGS ARE ATTACHED
TO VARIOUS SUBSTRATES BY A DENSE CARPET OF SHORT lLAMENTS ARRAYED AROUND THE MICROPYLE "RITZ COURTESY OF THE !MERICAN
-USEUM OF .ATURAL (ISTORY
! %GG ATTACHED TO MOSS "AR M
" !NIMAL POLE "AR M
# -ICROPYLAR REGION "AR M
$ -ICROPYLE "AR M
/65,!4)/.
&IGURE 4HESE SCANNING ELECTRON MICROGRAPHS OF THE MICROPYLES OF UNFERTILIZED EGGS OF FOUR SPECIES OF 3PARIDAE WERE
USED AS THE BASIS OF A TAXONOMIC KEY AO ACCESSORY OPENINGS "AR M &ROM #HEN 3HAO AND 9ANG REPRODUCED WITH
PERMISSION FROM %LSEVIER 3CIENCE
! 3PARUS SARBA 8
" !CANTHOPAGRUS LATUS 8
# ! SCHLEGELI 8
$ 0AGRUS MAJOR 8
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE EGG OF ,UCIOCEPHALUS PULCHER %LABORATE ARRAYS OF PARALLEL RIDGES ON
THE ZONA PELLUCIDA SUGGEST PHYLOGENETIC RELATIONSHIPS 4HESE RIDGES SPIRAL FROM THE 4YPE ) MICROPYLE AND ARE PRESUMED TO
ASSIST IN SPERM GUIDANCE &ROM "RITZ +OKOSCHA AND 2IEHL REPRODUCED WITH PERMISSION FROM THE )CHTHYOLOGICAL
3OCIETY OF *APAN
! 6IEW OF THE ANIMAL POLE OF THE EGG 4HE ARROW INDICATES THE MICROPYLE 8
" !N IRREGULAR PATTERN OF RIDGES NEAR THE VEGETAL POLE 8
# 4HE MICROPYLE ARROW AT THE CENTRE OF THE SPIRALING RIDGES AT THE ANIMAL POLE 8
$ -ICROPYLAR PIT WITH THE MICROPYLAR CANAL ARROW 8
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE DECHORIONATED EGG OF "RACHYDANIO RERIO &ROM (ART AND $ONOVAN
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC 4HE EGG SURFACE IMMEDIATELY BENEATH THE MICROPYLAR APPARATUS
APPEARS AS A CONE SHAPED DEPRESSION ARROW 8
/65,!4)/.
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION OF EGGS OF THE ROSE BITTERLING 2HODEUS OCELLATUS
8 &ROM /HTA REPRODUCED WITH PERMISSION
! 3PERM
ENTRY SITE 33 OF AN UNFERTILIZED EGG #( CHORION
" ! FERTILIZING SPERMATOZOON APPEARS TO ATTACH TO THE MICROVILLI OF THE SPERM
ENTRY SITE
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION OF THE MATURE EGG OF THE WHITE STURGEON !CIPENSER
TRANSMONTANUS &ROM #HERR AND #LARK REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! ! GROUP OF MICROPYLES AT THE ANIMAL POLE OF THE EGG 8
" 3OME MICROPYLES ARE SUPERlCIALLY CONNECTED BY SHALLOW CHANNELS ARROW 8
# 4HE FUNNEL SHAPED ENTRANCE TO ONE OF THE MICROPYLES VIEWED FROM THE OUTSIDE 4HE LINING OF THE MICROPYLAR CANAL IS RIDGED
8
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF MATURE EGGS OF THE PADDLElSH 0OLYODON SPATHULA AN EGG WITH MULTIPLE MI
CROPYLES &ROM ,INHART AND +UDO REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! ! GROUP OF MICROPYLES AT THE ANIMAL POLE 4HE EXTERNAL APERTURES ARE LINED WITH CYLINDRICAL STRUCTURES FORMED BY DIFFER
ENTIATION OF THE OUTERMOST LAYER OF THE CHORION 8
" 4HE BROKEN SURFACE OF THE CHORION SHOWING THREE LAYERS AND 4HE OUTERMOST LAYER DIFFERENTIATES TO FORM CYLINDRICAL
STRUCTURES 8
# 4HE SURFACE OF AN EGG IN THE MICROPYLAR REGION WITH THE CHORION REMOVED 4HE ROUND IMPRESSION OF THE lRST POLAR BODY
ARROW IS LOCATED NEAR A GROUP OF SPERM ENTRY SITES ARROWHEADS 8
)NSET TUFT OF MICROVILLI OF A SPERM ENTRY SITE ON THE SURFACE OF THE OOLEMMA UNDER A MICROPYLE 8
/65,!4)/.
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE MICROPYLAR REGION OF A FERTILIZED EGG OF THE ACTINOPTERYGIAN lSH 0OLYPTERUS
ORNATIPINNIS 4HE CHORIONIC SURFACE IS COVERED WITH GLUTINOUS TUFTS EXCEPT FOR A SMALL AREA AT THE ANIMAL POLE ! NARROW RING
LIKE
WALL SURROUNDS THE MICROPYLAR AREA WITH THE MICROPYLAR CANAL AT THE CENTRE ! NUMBER OF RIDGES ORIGINATING FROM THE CIRCULAR
WALL TRANSFORM CENTRIFUGALLY INTO THE GLUTINOUS TUFTS &ROM "ARTSCH AND "RITZ REPRODUCED WITH PERMISSION OF THE #AM
BRIDGE 5NIVERSITY 0RESS
&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH A VITELLOGENIC OOCYTE OF THE WHITE BASS -ORONE CHRYSOPS SHOWING
THE ZONA PELLUCIDA Z AT THE SITE WHERE THE MICROPYLAR CELL MC PENETRATES THE MICROPYLE 4HE CYTOPLASM CY BENEATH IS
RELATIVELY FREE OF YOLK GLOBULES "AR M &ROM -YLONAS ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
#(!04%2
&IGURE 4HE MICROPYLE OF THE MEDAKA /RYZIAS LATIPES IS FORMED DURING VITELLOGENESIS BY A SINGLE MICROPYLAR CELL
)T MOULDS THE MICROPYLAR CHANNEL AS THE ZONA PELLUCIDA IS LAID DOWN AROUND IT &ROM )WAMATSU .AKASHIMA AND /NITAKE
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CYTOPLASMIC EXTENSION OF THE MICROPYLAR CELL -# AND MI
CROPYLE OF A FULLY
GROWN OOCYTE 4HE OUTER LAYER OF THE CHORION /, EXTENDS INWARD OVER THE INNER LAYER ), TO LINE
THE MICROPYLAR CANAL AS FAR AS THE LARGE ARROW 4HE CYTOPLASMIC EXTENSION CONTAINS A BUNDLE OF MICROTUBULES &OLDS IN
THE SURFACE OF THE CYTOPLASMIC EXTENSION MOULD INDENTATIONS IN THE WALL OF THE MICROPYLAR CANAL 4HE MICROPYLAR CELL IS
ATTACHED TO THE INDENTED OOLEMMA BY TIGHT JUNCTIONS ARROWHEADS /# OOCYTE 8
" 4RANSMISSION ELECTRON MICROGRAPH OF A LONGITUDINAL SECTION OF THE MICROPYLE OF A MATURE EGG 4HE OUTER LAYER /, OF
THE CHORION IS ELECTRON DENSE AND OVERLIES THE INNER LAYER ), AROUND THE OUTER TWO
THIRDS OF THE MICROPYLAR CANAL
8
/65,!4)/.
&IGURE #ONTINUED
# 3CANNING ELECTRON MICROGRAPHS OF NON
ATTACHING lLAMENTS AND MICROPYLES AT THE ANIMAL POLE MIDDLE BOTTOM AND ATTACH
ING lLAMENTS AT THE VEGETAL POLE TOP "AR M
4HE THREE PICTURES ON THE LEFT ARE FROM AN EGG WITH A LEFT
HANDED SPIRAL ARRAGEMENT OF THE ATTACHING lLAMENTS AND NON
ATTACHING
lLAMENTS "OTTOM THE SPIRAL IN THE WALL OF THE MICROPYLE IS LEFT
HANDED
4HE THREE PICTURES ON THE RIGHT ARE FROM AN EGG WITH A RIGHT
HANDED SPIRAL ARRANGEMENT OF THE ATTACHING lLAMENTS AND NON
AT
TACHING lLAMENTS "OTTOM THE SPIRAL IN THE WALL OF THE MICROPYLE IS LEFT
HANDED
#(!04%2
&IGURE #ONTINUED
$ 3CHEMATIC DIAGRAM SHOWING TWO PATTERNS OF ATTACHING AND NON
ATTACHING lLAMENTS AND MICROPYLES IN INTRAFOLLICULAR OOCYTES
OF THE MEDAKA 4HE THECAL CELL LAYER 4 AND BASEMENT MEMBRANE "- ARE IMMOBILE 4HE MICROPYLAR CELL -# ROTATES
IN A RIGHT
HANDED DIRECTION /N THE LEFT THE OOCYTE / WITH ITS FOLLICULAR LAYER ' MOVES IN A RIGHT
HANDED DIRECTION
ON THE RIGHT IT ROTATES IN A LEFT
HANDED DIRECTION
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF THE FOLLICULAR LAYER IN THE ANIMAL POLE REGION OF AN OOCYTE OF THE MEDAKA
/RYZIAS LATIPES ! MICROPYLAR CELL MC WITH ELECTRON
DENSE CYTOPLASM AND NUCLEOPLASM IS SURROUNDED BY FOLLICULAR CELL GC
AND ABUTS THE ZONA PELLUCIDA CH 8 &ROM .AKASHIMA AND )WAMATSU REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
)NSET PHOTOMICROGRAPH OF THE WHOLE FOLLICLE 8
!BBREVIATIONS B FOLLICULAR BASAL LAMINA O OOPLASM TC THECAL CELL V SHORT VILLI PENETRATING THE ZONA PELLUCIDA
/65,!4)/.
&IGURE $IAGRAM OF A MICROPYLAR CELL FROM THE CHUM SALMON /NCORHYNCHUS KETA DURING VITELLOGENESIS 4HE MAIN CELL
BODY IS ABOUT M HIGH AND M WIDE AND lTS INTO THE MICROPYLAR VESTIBULE )TS INNER SURFACE BEARS A FEW SHORT MICROVILLI
WHEREAS THE OUTER SURFACE ABUTTING POLYGONAL FOLLICULAR CELLS IS SMOOTH 4HE CENTRAL NUCLEUS CONTAINS lNELY DISPERSED CHRO
MATIN AND A PROMINENT NUCLEOLUS 'RANULAR ENDOPLASMIC RETICULUM AND OTHER ORGANELLES OCCUPY THE CYTOPLASM OF THE MAIN CELL
BODY 4HE THICK CYTOPLASMIC PROCESS EXTENDS THROUGH THE MICROPYLAR CANAL A BUNDLE OF MICROTUBULES FORMS ITS CENTRAL CORE
4HE BULBOUS END OF THE PROCESS INDENTS THE SURFACE OF THE OOCYTE FORMING DESMOSOMAL JUNCTIONS WITH THE OOLEMMA &ROM
+OBAYASHI AND 9AMAMOTO REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF MICROPYLAR CELLS OF THE MEDAKA /RYZIAS LATIPES &ROM .A
KASHIMA AND )WAMATSU REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! -ICROPYLAR CELL DURING EARLY VITELLOGENESIS 4HE CELL IS LARGE WITH A mATTENED NUCLEUS #YTOPLASMIC ORGANELLES ARE ABUNDANT
'OLGI COMPLEXES ARE WELL DEVELOPED ON THE OOCYTE SIDE OF THE CELL BUNDLES OF TONOlLAMENTS ARE APPARENT ON THE OPPOSITE
SIDE 8
)NSET 0HOTOMICROGRAPH OF THE ENTIRE FOLLICLE 8
#(!04%2
&IGURE #ONTINUED
" ,ATER IN VITELLOGENESIS THE MICROPYLAR CELL HAS ASSUMED A MUSHROOM SHAPE AND ITS CYTOPLASMIC PROCESS HAS PENETRATED
THE ZONA PELLUCIDA !RROWHEADS INDICATE STRUCTURAL DISTORTION OF THE INNER LAYER OF THE ZONA PELLUCIDA 8
)NSET 4HE RECTANGLE ON THE PROCESS HAS BEEN ENLARGED TO SHOW A BUNDLE OF MICROTUBULES BUT NO TONOlLAMENTS 8
# 4HE TIP OF THE MICROPYLAR CELL PROCESS ABUTTING THE OOLEMMA OF AN OOCYTE IN LATE VITELLOGENESIS "UNDLES OF MICROTUBULES AND
TONOlLAMENTS WITH THEIR ASSOCIATED MITOCHONDRIA BECOME SPIRALLY TWISTED AS THE PROCESS ELONGATES
!BBREVIATIONS CH ZONA PELLUCIDA ' 'OLGI COMPLEX MT MICROTUBULES N NUCLEUS O OOCYTE TF TONOlLAMENTS
/65,!4)/.
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF END BULBS OF MICROPYLAR CELLS FROM THE CHUM SALMON /NCORHYNCHUS KETA
DURING LATE VITELLOGENESIS &ROM +OBAYASHI AND 9AMAMOTO REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE BULBOUS END OF A MICROPYLAR CELL 0- HAS INVAGINATED THE SURFACE OF THE OOCYTE / !DHAERENS JUNCTIONS ARE ABUNDANT
BETWEEN THE MEMBRANES OF THE TWO CELLS 6ESICULAR BODIES AND
NM lLAMENTS ARE ABUNDANT IN THE BULB 4HERE ARE LARGE
ARROWHEADS AND SMALL ARROWS COATED VESICLES IN THE OOPLASM "AR M
" !DHAERENS JUNCTIONS HAVE DEVELOPED BETWEEN THE MEMBRANE OF THE PROCESS AND THE OOLEMMA 4HERE IS A SUGGESTION OF
EXOCYTOTIC ACTIVITY ARROWHEADS ON THE MEMBRANE OF THE MICROPYLAR CELL 0- WHERE IT LIES ADJACENT TO THE OOLEMMA
"AR M
# %LLIPSOIDAL VESICLES ARE ABUNDANT IN THE OOPLASM / ADJACENT TO THE LOBULATED END OF THE PROCESS 0- "AR M
#(!04%2
&IGURE $IAGRAMS SUMMARIZING CHANGES IN THE MORPHOLOGY AND DISTRIBUTION OF THE YOLK NUCLEUS AND THE NUCLEI OF
FOLLICULAR CELLS IN SECTIONED OOCYTES OF THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSU AND .AKASHIMA REPRODUCED WITH
PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
!BBREVIATIONS !& ATTACHING lLAMENTS &# FOLLICULAR CELL ./.
!& NON
ATTACHING lLAMENTS 9. YOLK NUCLEUS
/65,!4)/.
&IGURE 0HOTOMICROGRAPHS OF LIVING VITELLOGENIC OOCYTES OF THE MEDAKA /RYZIAS LATIPES SHOWING CHORIONIC lLAMENTS
THE lLAMENTS ASSUME EITHER A RIGHT
OR LEFT
HANDED SPIRAL PATTERN ! IS AN EARLY STAGE OF VITELLOGENESIS AND THE lLAMENTS DEMON
STRATE THE RIGHT
HANDED PATTERN " REPRESENTS A LATER STAGE AND ITS lLAMENTS SPIRAL IN A LEFT
HANDED DIRECTION ,ONG ATTACHING lLA
MENTS WIND ON THE VEGETAL HEMISPHERE THE SHORTER NON
ATTACHING lLAMENTS ADORN THE CHORION OVER THE REMAINDER OF THE OOCYTE
4HE PROXIMAL PART OF THE ATTACHING lLAMENTS BENDS IN THE DIRECTION OF THE ANIMAL POLE %ARLY PREVITELLOGENIC OOCYTES ABOUT
M IN DIAMETER ARROW ARE SHOWN IN " 4HESE DISPLAY PRIMORDIAL lLAMENTS 8 &ROM )WAMATSU REPRODUCED
WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
!BBREVIATIONS !0 ANIMAL POLE 60 VEGETAL POLE
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF PREVITELLOGENIC OOCYTES OF THE MEDAKA /RYZIAS LATIPES
SHOWING NON
ATTACHING lLAMENTS AMONG THE FOLLICULAR CELLS ' &ROM )WAMATSU REPRODUCED WITH PERMISSION FROM
THE :OOLOGICAL 3OCIETY OF *APAN
! .ON
ATTACHING lLAMENTS
BETWEEN FOLLICULAR CELLS DURING LATE PREVITELLOGENESIS 4HE FOLLICULAR EPITHELIUM ' LIES BETWEEN
ITS BASEMENT MEMBRANE " AND THE ZONA PELLUCIDA % ! THECAL CELL 4 OVERLIES THE BASEMENT MEMBRANE 8
" ! NON
ATTACHING lLAMENT AT THE CENTRE
ORIGINATES FROM THE ZONA PELLUCIDA WHICH CONSISTS OF AN OUTER LAYER % AND
AN INNER LAYER , 8
4HE INSET SHOWS THE OUTER LAYER OF THE ZONA PELLUCIDA COMPOSED OF ELECTRON
DENSE AMORPHOUS AND TUBULAR STRUCTURES 8
/65,!4)/.
&IGURE (YPOTHETICAL DIAGRAM TO ILLUSTRATE THE ROTATION OF AN OOCYTE AROUND AN AXIS IN THE FOLLICLE OF THE MEDAKA
/RYZIAS LATIPES &ROM )WAMATSU REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING 4HE OOCYTE WITH ITS FOLLICULAR
LAYER ', ROTATES WITHIN THE BASEMENT MEMBRANE "- AND THE THECAL LAYER 4, PRIOR TO THE DIFFERENTIATION OF THE MICRO
PYLAR CELL -# AT THE ANIMAL POLE !0 THE ANTIPODE OF THE VEGETAL POLE 60 AT THE CENTRE OF THE VEGETAL POLE AREA 60!
4HE DIRECTION OF ROTATION ARROWS AROUND THE OOCYTE AXIS IS OPPOSITE TO THE DIRECTION OF BENDING OF THE ATTACHING !&
AND NON
ATTACHING .!& lLAMENTS ON THE CHORION #( !N OOCYTE COULD ROTATE IN EITHER DIRECTION WITHIN THE FOLLICLE
/% OVARIAN EPITHELIUM
#(!04%2
&IGURE 3CHEMATIC DIAGRAMS FROM AN OVUM OF THE HAGlSH -YXINE GLUTINOSA &ROM +OSMATH 0ATZNER AND !DAM
REPRODUCED WITH PERMISSION FROM 5RBAN &ISCHER 6ERLAG
! 4HE MICROPYLAR AREA SHOWING ANCHORING lLAMENTS A ROOTED IN THE CHORION MICROPYLAR FUNNEL F AND THE MICROPYLAR CANAL
M
" 4HE MICROPYLAR CANAL M PENETRATES THE CHORION S PASSING THROUGH AN ENLARGED CAVITY C )T IS ENTERED BY WAY OF THE
MICROPYLAR OPENING O
/65,!4)/.
&IGURE -ICROGRAPHS ILLUSTRATING THE MICROPYLAR APPARATUS OF THE HAGlSH %PTATRETUS STOUTI &ROM +OCH ET AL
REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF THE MICROPYLAR BASE WITH POSSIBLE ENTRANCE TO THE MICROPYLAR CANAL ARROW
8
" 0HOTOMICROGRAPH OF A SECTION OF AN OOCYTE SHOWING EARLY DEVELOPMENT OF THE MICROPYLAR CANAL MCA IN THE ZONA PELLUCIDA
CH WITH ANCHOR lLAMENTS NOT YET EVIDENT ! REGION OF THE CANAL ARROWHEAD HAS PENETRATED INTO THE OOPLASM O NEAR
THE GERMINAL VESICLE GV 8 "AR M
!BBREVIATIONS BL BASAL LAMINA FE FOLLICULAR EPITHELIUM MO MESOVARIUM
# 0HOTOMICROGRAPH OF A SECTION THROUGH THE MICROPYLAR CANAL MCA OPENING FROM THE MICROPYLAR CUP MCU IN THE CHORION
CH OF AN OVULATED EGG 8 "AR M
)NSET HIGHER MAGNIlCATION OF THE HONEYCOMB BASE OF THE MICROPYLAR CUP ADJACENT TO THE CANAL 8 "AR M
#(!04%2
&IGURE 4HE MICROPYLAR APPARATUS OF AN OOCYTE OF THE HAGlSH -YXINE GLUTINOSA IMMEDIATELY BEFORE SPAWNING
&ROM ,YNGNES REPRODUCED WITH PERMISSION FROM 3PRINGER
6ERLAG
! 0HOTOMICROGRAPH OF A SECTION THROUGH THE MICROPYLAR CANAL 4HE THICK FOLLICULAR EPITHELIUM F CONSISTS OF COLUMNAR CELLS
AND IS SEPARATED FROM THE CONNECTIVE TISSUE B OF THE THECA BY THE FOLLICULAR BASEMENT MEMBRANE P 4HE ZONA PELLUCIDA S
IS PERFORATED BY THE MICROPYLAR CANAL M &OLLICULAR CELLS ALONG THE AXIS OF THE MICROPYLAR CANAL ASSUME A SPINDLE FORMA
TION AX THAT CONTINUES AS A CORD OF CELLS THROUGH THE MICROPYLAR CANAL TO FORM A CYLINDRICAL EXTENSION C THAT INVAGINATES
THE GERMINAL DISC OF THE OOCYTE 4HE YOLKY CYTOPLASM OF THE OOCYTE D IS SHOWN AT THE BOTTOM 3OME OF THE FOLLICULAR CELLS
FORMING THE MICROPYLAR CANAL APPEAR TO HAVE HOLLOWED OUT A SPACE Z ALONGSIDE 8
" 3KETCH OF THE MICROPYLAR APPARATUS BASED ON &IG ! 4HERE IS A HYALINE STREAK R IN THE GERMINAL DISC K AT THE BASE OF
THE MICROPYLAR CANAL 8
# ! SKETCH OF THE MICROPYLAR APPARATUS AT A HIGHER MAGNIlCATION !N OUTGROWTH U OF FOLLICULAR CELLS F FORMS A CYLINDER OF
CELLS C THAT INVAGINATES THE GERMINAL DISC D 8
#(!04%2
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
MICROVILLI EITHER INVADE THE LUMINA OF THE PORE CANALS
OR ARE SANDWICHED BETWEEN THE CHORION AND THE OO
LEMMA
"ENEATH THE OOLEMMA IS THE #/24)#!, ,!9%2 /& //
0,!3- +OBAYASHI A (ART AND #OLLINS
)T IS THICKEST AT THE ANIMAL POLE AND GRADUALLY BECOMES
THINNER TOWARD THE ANTIPODE 4HE ELECTRON
DENSE 0%
2)0(%2!, 2%')/. OF CORTICAL OOPLASM LACKS MOST OF
THE ORGANELLES FOUND IN THE REST OF THE CORTEX ALTHOUGH
PROlLES OF ENDOPLASMIC RETICULUM AND AN OCCASIONAL
COATED VESICLE MAY BE DETECTED 4HE OOPLASM IS LESS
COMPACT IN THE )..%2 2%')/. WHICH CONTAINS THE MOST
CONSPICUOUS ORGANELLES OF THE CORTEX THE SPHERICAL
MEMBRANE
BOUND #/24)#!, !,6%/,) &IGURES !
TO # /THER ORGANELLES OF THE INNER REGION ARE MITO
CHONDRIA CIRCULAR AND TUBULAR PROlLES OF AGRANULAR
ENDOPLASMIC RETICULUM ANNULATE LAMELLAE LYSOSOMES
AND 'OLGI COMPLEXES &IGURE " !N ELABORATE
ANASTOMOSING NETWORK OF SMOOTH CISTERNAE THROUGHOUT
THE CORTICAL CYTOPLASM CONSTITUTES THE #/24)#!, %.$/
0,!3-)# 2%4)#5,5- &IGURE ! )T CONSISTS OF ISOLATED
CIRCULAR VESICLES AND TUBULAR PROlLES AND FORMS CLOSE
ASSOCIATIONS WITH BOTH THE CORTICAL ALVEOLAR MEMBRANES
AND OOLEMMA &IGURES " TO $
%XCEPT BELOW THE MICROPYLE THE MEMBRANE
BOUND
CORTICAL ALVEOLI ARE ARRANGED WITHIN THE CORTICAL OO
PLASM ALWAYS SEPARATED FROM THE OOLEMMA BY CYTO
PLASM &IGURE 4HEY ARE VARIABLE IN SIZE ATTAINING
DIAMETERS OF TO M IN CHUM SALMON /NCORHYN
CHUS KETA +OBAYASHI A TO M IN MEDAKA
/RYZIAS LATIPES 'ILKEY ET AL AND UP TO M
IN &UNDULUS HETEROCLITUS 3ELMAN 7ALLACE AND "ARR
!N APPARENT FUSION DURING lXATION HAS ARTI
FACTUALLY PRODUCED VESICLES GREATER THAN M IN
SECTIONS OF &UNDULUS EGGS )N THESE THREE SPECIES THE
CORTICAL ALVEOLI FORM A SINGLE LAYER WITHIN THE CORTI
CAL OOPLASM BUT IN THE ROSE BITTERLING 2HODEUS OCEL
LATUS THEY OCCUR IN SEVERAL LAYERS /HTA ET AL
)N THE ZEBRA DANIO "RACHYDANIO RERIO A SINGLE LAYER
SURROUNDING THE SPERM ENTRY SITE CONTRASTS WITH MULTI
)NTRODUCTION
7ITHIN SECONDS OF FERTILIZATION IN TELEOSTS THERE IS AN
EXPLOSIVE BREAKDOWN OF THE CORTICAL VESICLES OVER THE
ENTIRE SURFACE OF THE EGG 4HE CHORION IS LIFTED AWAY
FROM THE OOLEMMA AND THE 0%2)6)4%,,).% 30!#% IS CRE
ATED !LTHOUGH THIS hCORTICAL REACTIONv IS INDUCED BY
THE PENETRATION OF THE OOLEMMA BY A SPERMATOZOON
SOME FRESHWATER EGGS MAY BE ACTIVATED hPARTHENO
GENETICALLYv BY THEIR PASSAGE FROM THE ISOTONIC BODY
mUIDS INTO FRESH WATER DURING SPAWNING (ART 9U
AND 'REENHUT (ART AND 9U +OBAYASHI
A /HTA ET AL (ART AND #OLLINS
!CTIVATION OF UNFERTILIZED MARINE EGGS OF THE LONG
ROUGH DAB (IPPOGLOSSOIDES PLATESSOIDES LIMANDOI
DES CAN BE INDUCED BY TRANSFERRING THEM TO SEA WATER
,NNING AND $AVENPORT
/OLEMMA AND THE #ORTICAL /OPLASM
"EFORE FERTILIZATION THE SURFACE OF AN EGG FROM WHICH
THE CHORION HAS BEEN REMOVED IS COBBLED WITH HEMI
SPHERICAL BULGES REVEALING THE LOCATION OF CORTICAL
ALVEOLI BELOW &IGURE "RUMMETT AND $UMONT
+OBAYASHI A /HTA ET AL (ART AND
#OLLINS 4HE OOLEMMA IS DECORATED BY NUMER
OUS MICROVILLI AND MICROPLICAE WHICH ARE SPARSER OVER
THE ELEVATIONS THAN IN THE REGIONS BETWEEN )N SEC
TIONS THE MICROPLICAE APPEAR AS ELECTRON
DENSE lN
GER
SHAPED PROJECTIONS &IGURE " 4HE APPOSITION
OF THE CORTICAL VESICLES TO THE INSIDE OF THE OOLEMMA
IS ACCOMPANIED BY AN APPARENT CLEARING OF MEMBRANE
PARTICLES FROM THE SITE OF CONTACT BETWEEN THE APPOSED
MEMBRANES A DIMPLE IN THE PARTICLE
FREE ZONE APPEARS
TO MARK THE SITE OF CONTACT (ART AND #OLLINS
&IGURES $ % 4HE OOLEMMA IS CLOSELY ASSOCI
ATED WITH THE CHORION IN INTACT EGGS AND THE FOLDS AND
(ART HAS PRESENTED AN EXHAUSIVE REVIEW OF THIS LITERATURE
,ITTLE INFORMATION IS AVAILABLE ON EGGS OF OTHER lSHES
#(!04%2
LAYERED ROWS THROUGHOUT THE REMAINDER OF THE OOPLASM
(ART AND $ONOVAN .EAR THE SPERM ENTRY SITE
OF "RACHYDANIO THE ALVEOLI ARE TO M IN DIAM
ETER AND ARE DENSELY PACKED FROM THIS REGION TO THE
VEGETAL POLE THEY PROGRESSIVELY INCREASE IN SIZE AND
BECOME SPARSER SO THAT A GRADIENT IS ESTABLISHED IN THE
STRUCTURAL ORGANIZATION OF THE EGG CORTEX FROM THE SITE
OF SPERM ENTRY TO THE VEGETAL POLE
4HERE IS INDIRECT EVIDENCE FOR THE PRESENCE OF ACTIN
AND ACTIN
CONTAINING lLAMENTS WITHIN THE CORTICAL OO
PLASM (ART AND 7OLENSKI 7OLENSKI AND (ART
B A -ICROlLAMENTS TO NM IN DIAMETER
HAVE BEEN DESCRIBED IN THE CORES OF MICROPLICAE AND IN
THE CORTICAL LAYER NEAR THE SPERM ENTRY SITE OF "RACHY
DANIO 7OLENSKI AND (ART A 4HE PRESENCE OF
ACTIN WAS DEMONSTRATED JUST BENEATH THE OOLEMMA
OF UNACTIVATED EGGS USING RHODAMINE PHALLOIDIN AND
mUORESCENCE MICROSCOPY 7OLENSKI AND (ART B
)T IS SUGGESTED THAT BUNDLES OF ACTIN lLAMENTS DISPLACE
MEMBRANOUS ORGANELLES FROM THE CORTEX AND MAY BE
IMPORTANT IN MAINTAINING THE OVERALL SHAPE OF THE EGG
AND PLICAE )N EGGS OF THE CHUM SALMON THEY MAY
ASSIST IN EXPULSION OF THE CORTICAL ALVEOLI DURING THE
CORTICAL REACTION +OBAYASHI A
#ORTICAL !LVEOLI
!N ELECTRON DENSE CORE SURROUNDED BY AN ELECTRON
LUCENT HALO HAS BEEN DESCRIBED IN CORTICAL ALVEOLI OF
SEVERAL SPECIES &IGURE " )WAMATSU AND /HTA
+UDO (ART AND 9U (ART
AND $ONOVAN +OBAYASHI A )N EGGS OF
"RACHYDANIO THE CORE CONSISTS OF TIGHTLY PACKED PAR
TICLES TO NM IN DIAMETER THESE ARE SURROUNDED BY
LESS COMPACT CIRCULAR lBRILLO GRANULAR AGGREGATES
TO NM IN DIAMETER &IGURES ! TO # (ART AND
#OLLINS 3OMETIMES CORTICAL ALVEOLI ARE OB
SERVED LACKING THE HALO IN THE ZEBRAlSH THE PERIGRANU
LAR MEMBRANE ENCLOSES A MASS OF SMALL PARTICLES OF A
SIMILAR SIZE TO THOSE OF THE CENTRAL MASS OF THE CORED
PARTICLES &IGURE $ #ORTICAL GRANULES OF 3ALMO
GAIRDNERI SHOW AN ELECTRON LUCENT CORE SURROUNDED
BY ELECTRON DENSE MATERIAL &IGURE )NOUE ET AL
4HERE ARE TWO TYPES OF CORTICAL ALVEOLI IN EGGS
OF THE ROSE BITTERLING /HTA ET AL ALVEOLI OF
THE ANIMAL POLE CONTAIN ELECTRON LUCENT DROPLETS SUS
PENDED WITHIN AN ELECTRON DENSE MATRIX &IGURE !
WHEREAS AT THE VEGETAL POLE THE CONTENTS ARE HOMO
GENEOUS AND ELECTRON DENSE &IGURE " )N ADDITION
TO CORTICAL ALVEOLI MEMBRANE BOUND GRANULES PACKED
WITH lNELY GRANULAR OR HOMOGENEOUS MATERIAL HAVE
BEEN DESCRIBED IN THE CORTICAL OOPLASM OF UNFERTILIZED
EGGS OF CARP #YPRINUS CARPIO AND GOLDlSH #ARASSIUS
AURATUS &IGURE +UDO $ESIGNATED AS #!
'2!.5,%3 THEY ARE MUCH SMALLER THAN CORTICAL ALVEOLI
AND SCATTERED AROUND THEM 4HEY ARE MORE PLENTIFUL IN
THE ANIMAL THAN THE VEGETAL HEMISPHERE
#ORTICAL ALVEOLI CONTAIN GLYCOPROTEINS 4HEY STAIN
WITH PERIODIC ACID 3CHIFF REAGENT ALCIAN BLUE AT LOW
P( COLLOIDAL IRON AND BROMPHENOL BLUE AND ARE OF
TEN METACHROMATIC WITH TOLUIDINE BLUE SUGGESTING
THAT THEY CONTAIN AN ACIDIC GLYCOCONJUGATE CONSISTING
OF A POLYSACCHARIDE AND PROTEIN THAT IS ACID MUCO
POLYSACCHARIDE ANDOR MUCOPROTEIN REVIEWED BY
(ART ! UNIQUE CLASS OF GLYCOPROTEINS SHARING
CHARACTERISTIC BIOCHEMICAL AND BIOLOGICAL FEATURES HAS
BEEN DESIGNATED (9/3/0(/2). AND IS ASSOCIATED WITH
CORTICAL ALVEOLI OF SEVERAL SPECIES +ITAJIMA )NOUE
AND )NOUE )N FACT IT HAS BEEN SUGGESTED THAT
THESE GLYCOPROTEINS NOT SULPHATED MUCOPOLYSACCHA
RIDES ARE THE MAJOR WATER SOLUBLE COMPONENTS OF COR
TICAL ALVEOLI )NOUE ET AL ( (9/3/0(/2). HAS
BEEN DElNED AS THE MAJOR GLYCOPROTEIN OF THE CORTICAL
ALVEOLI AND THEREFORE DERIVED FROM THE 'OLGI COM
PLEX WITH A HIGH CARBOHYDRATE CONTENT TO
WW WHOSE PROTEIN CORE COMPRISES TANDEM REPETI
TIONS OF IDENTICAL PROTEIN SEQUENCES IT IS COMPLETELY
CLEAVED INTO REPEATING UNITS , (9/3/0(/2). FOLLOW
ING THE CORTICAL REACTION +ITAJIMA )NOUE AND )NOUE
!LTHOUGH THE lRST HYOSOPHORINS DESCRIBED WERE
POLYSIALOGLYCOPROTEINS NOT ALL BELONG TO THIS CATEGORY
4AGUCHI ET AL $ESPITE DIFFERENCES IN SEQUENCE
HOWEVER HYOSOPHORINS FROM DIFFERENT SPECIES OF lSH
ARE CHARACTERIZED BY THE PRESENCE OF EITHER POLYANIONIC
ANDOR BULKY MULTIANTENNARY STRUCTURES &IGURE
! POLYSIALOGLYCOPROTEIN OF K$A WAS ISOLATED FROM
UNFERTILIZED EGGS OF THE RAINBOW TROUT 3ALMO GAIRDNERI
)NOUE AND )NOUE +ITAJIMA )NOUE AND )NOUE
)NOUE ET AL )T IS COMPOSED OF A SMALL
PROTEIN CORE OF K$A TO WHICH ARE COVALENTLY BOUND
MULTIPLY BRANCHED VARIABLY ELONGATED OLIGO AND
POLYSIALYLGLYCAN CHAINS 4HE CORE CONSISTS OF A COM
PLETE TANDEM REPEAT OF ABOUT TRIDECAPEPTIDE UNITS
3IMILAR POLYSIALOGLYCOPROTEINS HAVE BEEN REPORTED IN
EGGS OF OTHER SALMONIDS AND SHOW A HIGH DEGREE OF
HOMOLOGY +ITAJIMA ET AL )N THE KOKANEE
SALMON /NCORHYNCHUS NERKA HOWEVER THE HYOSOPHO
RIN OF THE UNFERTILIZED EGG IS UNIQUE IN THAT TWO POLYSI
ALYLGLYCAN CHAINS ARE CHARACTERIZED ONE CONTAINS
AMINO ACIDS THE OTHER AND IN THE OPINION OF
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
3ONG +ITAJIMA AND )NOUE THESE DIFFERENCES
ARE SUFlCIENT TO CAST DOUBT ON THE PLACEMENT OF THE KO
KANEE IN THE 'ENUS /NCORHYNCHUS 4HE HYOSOPHORIN
OF THE mOUNDER 0ARALICHTHYS OLIVACEUS DIFFERS FROM
THAT OF OTHER lSH IN POSSESSING A NOVEL PENTAANTENNARY
CARBOHYDRATE STRUCTURE WITH A lVE TINED CARBOHYDRATE
FORK ATTACHED TO THE REPEATING DECAPEPTIDE OF THE PRO
TEIN CORE &IGURE 3EKO ET AL
!TTEMPTS TO LOCATE HYOSOPHORIN WITHIN CORTICAL
ALVEOLI BY MORPHOLOGICAL METHODS HAVE BEEN DISAP
POINTING )NOUE ET AL )T IS DIFlCULT TO RAISE
ANTIBODIES TO HYOSOPHORIN PERHAPS BECAUSE OF THE
UNUSUAL CHEMICAL STRUCTURE OF BOTH THE CARBOHYDRATE
PROSTHETIC GROUPS AND THE APOPROTEIN SO THAT IMMU
NOCYTOCHEMICAL METHODS HAVE BEEN OF LITTLE HELP
)N ADDITION THE LARGE AMOUNTS OF YOLK WITHIN THE MA
TURE EGG HAVE HINDERED STUDIES OF THE CORTEX (YO
SOPHORIN HAS BEEN IDENTIlED HOWEVER IN A FRACTION
RICH IN CORTICAL ALVEOLI OBTAINED FROM HOMOGENIZED
SALMON EGGS BY LOW SPEED CENTRIFUGATION
,%#4).3 SPECIFIC CARBOHYDRATE BINDING PROTEINS
COMMONLY FOUND IN PLANTS HAVE BEEN DESCRIBED IN THE
EGGS OF VARIOUS lSH +RAJHANZL (OREJSI AND +OKOU
REK A B !LL KNOWN LECTINS CONTAIN TWO OR MORE
BINDING SITES FOR CARBOHYDRATE UNITS AND CAN AGGLU
TINATE OR CROSS LINK CELLS ,ECTINS HAVE BEEN LOCAL
IZED BY IMMUNOLOGICAL METHODS WITHIN THE CORTICAL
ALVEOLI OF PREVITELLOGENIC OOCYTES +RAJHANZL ET AL
A B .OSEK AND IN THE THIN LAYER OF COR
TICAL ALVEOLI OF MATURE EGGS THAT HAVE NOT UNDERGONE
ACTIVATION .OSEK +RAJHANZL AND +OCOUREK
,ECTINS ARE SYNTHESIZED DURING PREVITELLOGEN
ESIS IN THE 'OLGI COMPLEX .OSEK AND INCREASE
IN AMOUNT DURING LATER STAGES WHEN CORTICAL ALVEOLI lLL
THE ENTIRE OOPLASM BEFORE MOVING TO THE PERIPHERY AS
THE OOCYTE ACCUMULATES YOLK .OSEK +RAJHANZL AND
+OCOUREK 4HE LECTINS ARE DISCHARGED INTO THE
PERIVITELLINE SPACE FOLLOWING THE CORTICAL REACTION AND
IT IS SUGGESTED THAT THEY CONTRIBUTE TO THE PHYSIOLOGICAL
MECHANISMS PREVENTING POLYSPERMY BY AGGLUTINATING
SUPERNUMERARY SPERMATOZOA .OSEK +RAJHANZL AND
+OCOUREK +UDO AND )NOUE 4HEY MAY
ALSO AGGLUTINATE PATHOGENIC BACTERIA THAT PENETRATE THE
OUTER ENVELOPES OF THE EGG THEREBY PREVENTING THEM
FROM ATTACKING THE EGG
&ERTILIZATION
3PERMATOZOA OF MOST TELEOSTEAN lSHES HAVE NO ACRO
SOMAL APPARATUS AND GAIN ACCESS TO THE SURFACE OF THE
EGG THROUGH THE MICROPYLE THAT PERFORATES THE CHORION
)WAMATSU AND /HTA B +UDO B
"RUMMETT AND $UMONT 'ILKEY +OBAYAS
HI AND 9AMAMOTO /HTA AND )WAMATSU
/HTA 7OLENSKI AND (ART A "ERN
AND !VTALION /HTA /HTA AND .ASHIRO
ZAWA 4HE lRST SPERMATOZOON ARRIVING AT THE
MICROPYLE NAVIGATES THE CANAL TO REACH THE OOLEMMAL
MICROVILLI AT THE 30%2- %.429 3)4% &IGURES ! "
! " AND )T ATTACHES TO THESE MICRO
VILLI AND IN SOME SPECIES IS RAPIDLY ENGULFED BEFORE
THE OOLEMMA ELEVATES TO FORM THE &%24),):!4)/. #/.%
&IGURES TO )WAMATSU AND /HTA B
/HTA AND )WAMATSU )WAMATSU )N OTHER
SPECIES HOWEVER THE FERTILIZATION CONE MAY DEVELOP
EITHER BEFORE OR AT THE SAME TIME AS THE SPERMATOZOON
IS INCORPORATED +UDO B +UDO AND 3ATO
+OBAYASHI AND 9AMAMOTO 7OLENSKI AND
(ART A &OLLOWING PENETRATION OF THE SPERM IN
THE ROSE BITTERLING 2HODEUS OCELLATUS OCELLATUS THE
SPERM ENTRY SITE TRANSFORMS INTO A 37/,,%. -!33 THAT
PLUGS THE MICROPYLE AND PREVENTS PENETRATION OF EXCESS
SPERMATOZOA &IGURE /HTA AND .ASHIROZAWA
4HE SWOLLEN MASS MAY BE A TYPE OF FERTILIZATION
CONE IT APPEARS IDENTICAL IN FORM AND FUNCTION EXCEPT
THAT FERTILIZATION CONES RECEDE QUICKLY AFTER FUSION OF
THE MEMBRANES OF THE GAMETES BUT THE SWOLLEN MASS
PERSISTS AND APPEARS TO FUNCTION AS A MICROPYLAR PLUG
4HE EXPANDED SURFACE AREA AFFORDED BY THE CLUSTER
OF MICROVILLI AT THE SPERM ENTRY SITE MAY EXPEDITE THE
BINDING
FUSION PROCESS 7OLENSKI AND (ART A
4HERE HAVE BEEN SUGGESTIONS THAT THE INTERACTION BE
TWEEN THE SPERMATOZOON AND THE SPERM BINDING SITE
RESULTS FROM SPECIlC RECEPTORS IN THE MEMBRANE OF
THE MICROVILLI THAT RECOGNIZE ANDOR BIND WITH THE
PLASMA MEMBRANE OF THE SPERMATOZOON /HTA AND
)WAMATSU 7OLENSKI AND (ART A /HTA
(OWEVER SINCE SPERMATOZOA CAN FERTILIZE A
DECHORIONATED EGG AT ANY POINT ON ITS SURFACE 3AKAI
)WAMATSU AND /HTA RECEPTORS FOR SPER
MATOZOA IF THEY EXIST MUST BE PRESENT OVER THE ENTIRE
OOLEMMA 'ILKEY
!N EXHAUSTIVE REVIEW OF THE RECENT LITERATURE ON FERTILIZATION IN
TELEOSTS HAS BEEN PRESENTED BY )WAMATSU
#(!04%2
3PERMATOZOA OF TILAPIA /REOCHROMIS NILOTICUS
REACH THE MICROPYLE IN LESS THAN SECOND AND ATTAIN
THE SPERM BINDING SITE ON THE OOLEMMA WITHIN TO
SECONDS AFTER INSEMINATION "ERN AND !VTALION
%NGULFMENT OF THE HEAD IN THIS SPECIES IS ALWAYS FOL
LOWED BY AN INDENTATION OF THE OOLEMMA THE #,%&4 /&
0%.%42!4)/. &IGURE 4HE SPERM TAIL IS STILL VIS
IBLE PROTRUDING FROM THE OOLEMMA TO MINUTES AF
TER INSEMINATION 4HE MICROVILLI OF THE SPERM BINDING
SITE GRADUALLY DISAPPEAR FOLLOWING PENETRATION OF THE
SPERMATOZOON PERHAPS DEPRIVING OTHER SPERMATOZOA
OF RECEPTORS THEREBY PLAYING A ROLE IN THE PREVENTION
OF POLYSPERMY
&ORMATION OF A TWO TIERED FERTILIZATION CONE HAS
BEEN DESCRIBED IN SOME SPECIES )N FERTILIZED EGGS OF
THE AYU lSH 0LECOGLOSSUS ALTIVELIS THE lRST FERTILIZATION
CONE IS A CYLINDRICAL STRUCTURE ABOUT M LONG AND
TO M IN DIAMETER THAT RISES FROM THE SPERM ENTRY
SITE WITHIN TO SECONDS OF IMMERSION IN FRESH WA
TER &IGURE +UDO B !T ABOUT SECONDS A
SECOND TIER FORMS A PEDESTAL ABOUT M HIGH ELEVAT
ING THE lRST CONE FROM ITS APEX !FTER ABOUT SECONDS
THIS STRUCTURE RECEDES TO FORM A MOUND ON THE SURFACE
OF THE EGG WITH THE SPERM TAIL EXTENDING FROM IT ! LESS
ELABORATE TWO TIERED FERTILIZATION CONE APPEARS IN THE
CARP #YPRINUS CARPIO )T REACHES A HEIGHT OF MORE THAN
M AND A BREADTH OF TO M WITHIN SECONDS OF
IMMERSION OF FERTILIZED EGGS IN FRESH WATER RESULTING
IN A TRANSIENT PLUGGING OF THE MICROPYLE &IGURE
+UDO AND 3ATO 7ITHIN TO MINUTES THE
SECOND TIER APPEARS AT ITS BASE 4HE EARLIER CONE SHORT
ENS A VOLCANO LIKE STRUCTURE RISES IN THE MICROPYLAR
REGION AND EXTENDING FROM THE CENTRE OF ITS CRATER IS
THE TWO TIERED FERTILIZATION CONE BRANDISHING THE SPERM
TAIL FROM ITS APEX &IGURE
4HE ELKHORN SCULPIN !LCICHTHYS ALCICORNIS PROVIDES
A CONVENIENT MODEL FOR STUDYING THE EARLY STAGES OF
FERTILIZATION -UNEHARA 4AKANO AND +OYA
+OYA 4AKANO AND 4AKAHASHI 4HIS COTTID DEM
ONSTRATES hINTERNAL GAMETIC ASSOCIATIONv WHERE SPERM
INTRODUCED INTO THE OVARIAN CAVITY BY COPULATION ENTER
THE MICROPYLAR CANALS OF OVULATED EGGS BUT THERE IS NO
SPERMEGG FUSION UNTIL THE EGGS ARE RELEASED INTO SEA
WATER &IGURE $URING EXPERIMENTAL MANIPULA
TIONS SPERM REMAIN ATTACHED TO THE OOPLASMIC SURFACES
OF EGGS FRESHLY STRIPPED FROM COPULATED FEMALES AND
FERTILIZATION IS INITIATED WHEN THE EGGS ARE IMMERSED IN
SEA WATER "Y SECONDS AFTER IMMERSION A FERTILIZING
SPERMATOZOON PENETRATES THE OOPLASM FOR ABOUT HALF ITS
HEAD LENGTH AND SEVERAL VESICLES APPEAR IN THE AREA OF
PENETRATION &IGURE ! !S VESICULATION ADVANCES
THE PLASMA MEMBRANE OF THE SPERM DISAPPEARS THERE
BY EXPOSING THE NUCLEAR MEMBRANE OF THE SPERM TO THE
OOPLASM ! FERTILIZATION CONE FORMS AROUND THE UN
PENETRATED PORTION OF THE SPERM HEAD AND AN ELECTRON
DENSE TRIANGULAR REGION CONTAINING NO ORGANELLES OTHER
THAN RIBOSOMES APPEARS IN THE OOPLASM SURROUNDING
THE PENETRATING SPERM HEAD &IGURES " #
4HE MICROTUBULES OF THE SPERM TAIL DEGENERATE BY
SECONDS AND THERE IS A LOSS OF MOTILITY &IGURE $
4HE MITOCHONDRIA OF THE SPERM REMAIN OUTSIDE THE OO
LEMMA "Y TO MINUTES THE SPERM HAS PENETRATED
UP TO ITS MIDPIECE "Y MINUTES AFTER IMMERSION
THE NUCLEAR MEMBRANE OF THE SPERM SEPARATES FROM
THE CHROMATIN BEGINNING AT THE ANTERIOR REGION OF THE
SPERM HEAD &IGURES % & "Y MINUTES NO TRACE
OF THE SPERM CAN BE DETECTED AND A SEPARATING POLAR
BODY IS NOTICABLE ULTRASTRUCTURALLY &IGURE '
!LTHOUGH INSEMINATION TAKES PLACE IN TWO SPECIES OF
3OUTH !MERICAN CATlSHES OF THE FAMILY !UCHENIPTERI
DAE IT IS NOT CLEAR THAT FERTILIZATION IS INTERNAL -EISNER
ET AL 4HE MALE HAS A '/./0/$)5- OR INTROMIT
TENT ORGAN FORMED FROM AN ELONGATED GENITAL PAPILLA
AND MODIlED ANAL lN &IGURES ! " 4HE PRESENCE
OF SPERM WITHIN THE TORTUOUS FOLDS AND NARROW DEPRES
SIONS OF THE OVARIAN CAVITY SHOWS THAT INSEMINATION
HAS OCCURRED &IGURES # $ BUT NO FERTILIZED EGGS
OR EARLY EMBRYOS HAVE BEEN DEMONSTRATED IN EITHER
SPECIES 4HERE APPEAR TO BE NO DISTINCT STORAGE STRUC
TURES AND IN MANY CASES THE SPERM SEEM TO BE EMBED
DED WITHIN THE EPITHELIUM LINING THE CAVITY 3INCE THE
TIME AND PLACE OF FERTILIZATION ARE NOT KNOWN IT MAY
BE THAT AS IN THE CASE OF THE SCULPIN FERTILIZATION DOES
NOT OCCUR UNTIL THE EGGS REACH SEAWATER
5NLIKE THE SITUATION IN MOST lSH SPERMATOZOA OF THE
WHITE STURGEON !CIPENSER TRANSMONTANUS POSSESS AN
!#2/3/-% AT THE ANTERIOR END #HERR AND #LARK
4HIS CAPLIKE MEMBRANE
BOUND SAC CONTAINS
ENZYMES THAT ARE RELEASED DURING THE !#2/3/-!, 2%!#
4)/. AND ARE BELIEVED TO FACILITATE ENTRY OF THE SPERM
INTO THE OVUM &IGURE )T IS A MYSTERY WHY AN
ACROSOME IS NEEDED IN THE STURGEON WHEN THE SPERM
IS ABLE TO GAIN ACCESS TO THE OVUM BY WAY OF MULTIPLE
MICROPYLES !N INSOLUBLE K$A GLYCOPROTEIN FROM
LAYER , LOCATED IMMEDIATELY INSIDE THE INSOLUBLE
JELLY COAT , OF THE EGG ENVELOPE UNDERGOES PROTE
OLYSIS TO PRODUCE A SOLUBLE K$A GLYCOPROTEIN WHICH
INDUCES THE ACROSOMAL REACTION IN HOMOLOGOUS SPERM
BUT FAILS TO DO SO IN SPERM OF THE 'REAT ,AKES STURGEON
! FULVESCENS
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
4HERE IS NO MICROPYLE IN THE LAMPREYS ,AMPETRA
mUVIATILIS AND , PLANERI AND IT IS UNCLEAR HOW FERTIL
IZATION IS ACCOMPLISHED +ILLE !FZELIUS .ICA
NDER AND 3JDN .ICANDER AND 3JDN
4HE SPERMATOZOON HAS AN ACROSOME AND IS ORIENTED AT
RIGHT ANGLES TO THE ANIMAL POLE OF THE EGG BY THE APICAL
&)"2/53 45&4 &IGURE WHOSE FIBRILS APPEAR CONTIN
UOUS WITH THOSE IN THE PORE CANALS OF THE OUTER CHORION
&IGURE )T IS SUGGESTED THAT PROTEOLYTIC ENZYMES
FROM THE SPERMATOZOON DISSOLVE A PASSAGE THROUGH
THE CHORION BY WAY OF THE PORE CANALS 7ITHIN MIN
UTES OF STRIKING THE CHORION TAIL MOVEMENTS CEASE AND
THE SPERMATOZOON SLIPS PASSIVELY THROUGH THE INNER
LAYER OF THE CHORION AND CROSSES THE PERIVITELLINE SPACE
7HEN THE SPERMATOZOON EMBEDS ITSELF IN THE CHORION
A (%!$ &),!-%.4 IS THRUST FORWARD FROM ITS HEAD AND
BECOMES ATTACHED TO THE EGG CORTEX &IGURE
ACTIVATING THE EGG ! hTHIN THREADv OF OOPLASM RISES
TO MEET IT AND THE SPERMATOZOON PERHAPS DRAWN BY
ELASTICITY OF THE CORTICAL OOPLASMIC STRAND PENETRATES
THE OOLEMMA .O SUPERNUMERARY SPERMATOZOA ARE
SEEN IN THE PERIVITELLINE SPACE
#ORTICAL 2EACTION
5PON ACTIVATION OF THE EGG A WAVE OF MASSIVE EXOCY
TOSIS PASSES OVER THE SURFACE OF MANY TELEOST EGGS AND
THE CORTICAL ALVEOLI RELEASE THEIR CONTENTS BENEATH THE
CHORION INTO THE PERIVITELLINE SPACE &IGURES AND
/HTA ET AL #ORTICAL ALVEOLAR BREAKDOWN
MAY EASILY BE OBSERVED IN LIVING EGGS BY MEANS OF A
DISSECTING MICROSCOPE AS A CLEARING OF THE SOMEWHAT
OPAQUE EGG "RUMMETT AND $UMONT 4HE WAVE
BEGINS NEAR THE SITE OF SPERM PENETRATION AND PRO
CEEDS TO THE ANTIPODE OF THE EGG )WAMATSU AND /HTA
'ILKEY ET AL )WAMATSU AND +EINO
"RUMMETT AND $UMONT 'ILKEY +OBAYAS
HI A /HTA ET AL )WAMATSU ET AL
4HIS WAVE OF EXOCYTOSIS IS PRECEDED BY ABOUT SEC
ONDS BY A TRANSIENT INCREASE IN CYTOPLASMIC #A WHICH
IS RELEASED FROM CYTOPLASMIC STORES AND ALSO PASSES AS
A WAVE OVER THE SURFACE OF THE OOCYTE 2IDGWAY 'ILKEY
AND *AFFE 'ILKEY ET AL 9OSHIMOTO ET AL
)WAMATSU 9OSHIMOTO AND (IRAMOTO
4HIS WAVE HAS BEEN FOLLOWED IN EGGS OF THE MEDAKA
/RYZIAS LATIPES BY MEANS OF THE PHOTOPROTEIN !%15/
WHICH REACTS SPECIlCALLY WITH #A BY EMITTING
LIGHT &IGURE 2IDGWAY 'ILKEY AND *AFFE
'ILKEY ET AL 9OSHIMOTO ET AL )WAMATSU
ET AL &REE CYTOPLASMIC #A RISES ABOUT
FOLD FOLLOWING SPERM ENTRY AND THEN RETURNS TO ITS REST
ING LEVEL 4HIS RELEASE AND REMOVAL OF #A PASSES AS
A WAVE IN THE CORTICAL OOPLASM FROM THE POINT OF SPERM
ENTRY TO THE ANTIPODE IN TO MINUTES "OTH THE #A
WAVE AND THE CORTICAL REACTION ARE PROPAGATED AT THE
SAME CONSTANT SPEED OF ABOUT M PER SECOND WITH
ABOUT SECONDS BETWEEN THE TWO WAVES "Y CONTRAST
THE CORTICAL REACTION IS SLOW IN THE MARINE EGGS OF
THE LONG ROUGH DAB (IPPOGLOSSOIDES PLATESSOIDES LI
MANDOIDES AND A FEW INTACT CORTICAL ALVEOLI MAY BE
FOUND MINUTES AFTER INSEMINATION ,NNING AND
$AVENPORT
.O SUCH WAVE OF EXOCYTOSIS HAS BEEN OBSERVED
IN ACTIVATED EGGS OF THE ZEBRA DANIO "RACHYDANIO RE
RIO WHERE THE CORTICAL REACTION IS INITIATED RANDOMLY
SHORTLY AFTER SPERM PENETRATION AND OCCURS MORE OR
LESS SIMULTANEOUSLY OVER THE ENTIRE EGG SURFACE (ART
AND 9U (ART AND #OLLINS "REAKDOWN
IS SOMEWHAT DELAYED AROUND THE MICROPYLE PERHAPS
FACILITATING INCORPORATION OF THE SPERMATOZOON
7OLENSKI AND (ART A
! SCHEME FOR THE RELEASE OF THE CALCIUM FROM IN
TRACELLULAR STORES SUGGESTS INVOLVEMENT OF THE 0(/3
0(/)./3)4)$% #!3#!$% A COMMON PATHWAY IN MANY
TYPES OF CELLS &IGURE )WAMATSU 9OSHIMOTO
AND (IRAMOTO B )N THIS SCHEME BINDING OF A
SPERMATOZOON TO ITS RECEPTOR IN THE OOLEMMA LEADS
TO ACTIVATION OF PHOSPHOLIPASE # 0,# MEDIATED BY
GUANINE NUCLEOTIDE DEPENDENT REGULATORY PROTEIN 'P
0,# CATALYSES THE BREAKDOWN OF PHOSPHATIDYLINOSITOL
BIPHOSPHATE 0)0 INTO DIACYLGLYCEROL $' AND
INOSITOL TRIPHOSPHATE )0 )0 FUNCTIONING AS
AN INTRACELLULAR MESSENGER INTERACTS WITH A SPECIlC
RECEPTOR ON THE CYTOPLASMIC CALCIUM STORES WHICH
RELEASE #A INTO THE CYTOSOL 4HIS CYTOSOLIC #A THEN
ACTIVATES MORE 0,# THEREBY FORMING MORE )0 AND
$' AND THE CALCIUM WAVE CONTINUES OVER THE EGG
)T IS PRESUMED THAT THE ELABORATE CORTICAL ENDOPLASMIC
RETICULUM IS THE STORAGE SITE OF THIS #A &IGURE !
(ART AND #OLLINS
&ERTILIZATION ALSO TRIGGERS AN ABRUPT DEPOLARIZATION
OF THE OOLEMMA &IGURE .UCCITELLI A B
2).
#ONCENTRATIONS OF #A IN CELLS CAN BE MONITORED WITH THE mUORESCENT PROBE !%15/2). A PROTEIN PRODUCED BY THE LUMINOUS JELLYlSH !EQUOREA
FORSKALEA 4HIS BIOLUMINESCENT PROTEIN CONTAINS A mUORESCENT PHOTOPHORE THAT EMITS LIGHT ON BINDING #A THE RATE OF EMISSION DEPENDS UPON
THE CONCENTRATION OF #A
#(!04%2
4HE AVERAGE RESTING POTENTIAL OF UNFERTILIZED MEDAKA
EGGS IN 2INGERS SOLUTION IS n M6 &OLLOWING
FERTILIZATION IN DILUTE 2INGERS SOLUTION THE MEMBRANE
DEPOLARIZES OVER A PERIOD OF SEC BY A FEW MIL
LIVOLTS PRESUMABLY BY THE INmUX OF #A AND .A IONS
AND EFmUX OF + $EPOLARIZATION IS FOLLOWED BY A LONG
HYPERPOLARIZING PHASE WITH AN AVERAGE AMPLITUDE OF
M6 )T IS SUGGESTED THAT TWO CHANGES IN THE
OOLEMMA BRING ABOUT AN INCREASE IN ITS PERMEABILITY
TO + DURING HYPERPOLARIZATION AND + mOWS BACK INTO
THE OOPLASM &IRST THE RISE IN INTERNAL FREE #A MAY
CAUSE AN OPENING OF + CHANNELS AND SECONDLY NEW
+ CHANNELS MAY BE ADDED TO THE SURFACE BY THE INCOR
PORATION OF NEW MEMBRANE AS A RESULT OF THE EXOCYTOSIS
OF THE CORTICAL VESICLES 2ECOVERY FROM HYPERPOLARIZA
TION HAS A FAST PHASE LASTING SEC FOLLOWED BY
A SLOWER RATE OF CHANGE WHICH REACHES A STEADY POST
FERTILIZATION RESTING POTENTIAL OF n M6 BY
MIN AFTER FERTILIZATION
$URING THE CORTICAL REACTION THE MEMBRANES OF THE
CORTICAL VESICLES FUSE WITH THE OOLEMMA AND THERE OC
CURS A SUDDEN MASSIVE EXOCYTOSIS &IGURES * +
AND )WAMATSU AND /HTA (ART
9U AND 'REENHUT 3HACKLEY AND +ING
)WAMATSU AND +EINO (ART AND 9U "RUM
METT AND $UMONT +OBAYASHI A 3CHALKOFF
AND (ART (ART AND #OLLINS /NE OR MORE
OPENINGS APPEAR IN THE OOLEMMA AND THE CONTENTS OF
THE ALVEOLI ARE RELEASED INTO THE PERIVITELLINE SPACE
&IGURE *UST BEFORE EXPULSION A COATING OF COM
PACT OOPLASM ENVELOPS THE CORTICAL ALVEOLI OF SOME
SPECIES THIS COAT EVENTUALLY COALESCES WITH THE DENSE
PERIPHERAL OOPLASM AS EXOCYTOSIS CONTINUES &IGURES
AND )WAMATSU AND /HTA +OBAYASHI
A ! WIDE TRANSIENT #2!4%2 OR #2904 LINED WITH
MEMBRANE OF LOW PARTICLE DENSITY REMAINS ON THE SUR
FACE AT THE SITE OF THE EXPULSION &IGURE ! AND THE
DIFFERENCES IN PARTICLE DENSITY ARE MAINTAINED BETWEEN
THE DOMAINS OF THE FORMER CORTICAL VESICLE AND THE OO
LEMMA EVEN AFTER MOST EVIDENCE OF EXOCYTOSIS HAS DIS
APPEARED FROM THE SURFACE SUGGESTING THAT CONSTITUENTS
OF THE TWO MEMBRANE DOMAINS REMAIN DISTINCT AND DO
NOT READILY INTERACT &IGURE " (ART AND #OLLINS
,ARGE NUMBERS OF MICROVILLI SPROUT WITHIN THE
CRATERS OF SOME SPECIES BEGINNING AT THE OPENING AND
SPREADING THROUGHOUT EVENTUALLY THESE MICROVILLI DIS
APPEAR AS THE CRATERS SHRINK &IGURE )WAMATSU
AND /HTA )WAMATSU AND +EINO "RUM
METT AND $UMONT +OBAYASHI A
&ATE OF !LVEOLAR -EMBRANE
!S A RESULT OF CORTICAL ALVEOLAR BREAKDOWN AND EXOCY
TOSIS THE SMOOTH INNER SURFACE OF THE ALVEOLAR MEM
BRANE BECOMES PART OF THE OOLEMMA /HTA ET AL
4HIS NEW MOSAIC SURFACE CONSISTS OF TWO DOMAINS
THE ORIGINAL OOLEMMA AND THE MEMBRANE FORMERLY
DELIMITING THE CORTICAL ALVEOLI 4HE MOSAIC IS VIS
IBLE WITH THE SCANNING ELECTRON MICROSCOPE IN THE
EGGS OF SOME SPECIES (ART 9U AND 'REENHUT
(ART AND 9U +OBAYASHI A $ONOVAN AND
(ART BUT NOT IN OTHERS )WAMATSU AND +EINO
)N THE ZEBRA DANIO FOR EXAMPLE THE FORMER
ALVEOLAR MEMBRANE HAS A PEBBLED SURFACE WHILE THE
OOLEMMAL SURFACE APPEARS FOLDED &IGURE !
-ICROVILLI APPEAR IN THE CRATERS WITHIN TWO MINUTES
OF ACTIVATION IN THE CHUM SALMON /NCORHYNCHUS KETA
AND OBSCURE THE DISTINCTION BETWEEN DOMAINS +O
BAYASHI A 4HE MAGNITUDE OF THE INCORPORATION
OF MEMBRANE CAN BE APPRECIATED FROM ESTIMATES OF
THE AREAS OF THE DOMAINS IN THE ZEBRA DANIO WHOSE EGG
IS M IN DIAMETER AND CONTAINS ABOUT ALVE
OLI WITH AN AVERAGE DIAMETER OF M (ART 9U AND
'REENHUT 4HE SURFACE AREA OF THE UNFERTILIZED
EGG WOULD BE M AND THE AREA OF ALVEOLAR
MEMBRANE ADDED TO THIS SURFACE DURING THE CORTICAL
REACTION IS ESTIMATED TO BE AS GREAT AS M
(OW IS THIS EXCESS MEMBRANE ACCOMMODATED
4HE MOSAIC RESULTING FROM EXOCYTOSIS APPEARS TO
BE TEMPORARY AND THE ALVEOLAR MEMBRANES LIKELY HAVE
LIMITED EXISTENCE ON THE SURFACE OF THE EGG (ART AND
9U (ART AND #OLLINS 3EVERAL SUGGES
TIONS HAVE BEEN MADE FOR THE UPTAKE OF THE ALVEOLAR
MEMBRANE 3OME MEMBRANE IS INCORPORATED INTO NEW
MICROVILLI THAT SPROUT ON THE SURFACE ESPECIALLY WITHIN
THE CRATERS )WAMATSU AND /HTA )WAMATSU AND
+EINO "RUMMETT AND $UMONT +OBAYAS
HI A SOME IS STRUNG OUT INTO THREADS AND LOST INTO
THE PERIVITELLINE SPACE &IGURE "RUMMETT AND
$UMONT AND SOME IS TAKEN UP BY ENDOCYTOSIS
(ART AND 9U +OBAYASHI A $ONOVAN AND
(ART (ART AND #OLLINS )T APPEARS
THAT THIS ENDOCYTOSIS IS SELECTIVE WITH THE VESICULAR
MEMBRANE BEING TAKEN UP FROM THE VACATED CRATERS IN
COATED VESICLES AND PASSED TO THE LYSOSOMAL COMPART
MENT &IGURES " # AND $EGRADATION IN THE
LYSOSOMAL COMPARTMENT WOULD YIELD IMPORTANT PRO
TEIN AND LIPID PRECURSORS FOR THE CONSTRUCTION OF
THE NEW MEMBRANE THAT WILL BE REQUIRED FOR CLEAVAGE
OF THE FERTILIZED EGG ,OCALIZED FOLDS OF THE OOLEMMA
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
THEN OVERGROW AND REPLACE ANY ALVEOLAR MEMBRANE
REMAINING AT THE SURFACE .O EVIDENCE FOR MEMBRANE
UPTAKE BY ENDOCYTOSIS WAS FOUND HOWEVER IN EGGS
OF &UNDULUS HETEROCLITUS "RUMMETT AND $UMONT
0ERIVITELLINE 3PACE
3IMULTANEOUS WITH THE CORTICAL REACTION THE CHORION
SEPARATES FROM THE OOLEMMA CREATING THE 0%2)6)4%,,).%
30!#% &IGURES AND )WAMATSU AND /HTA
(ART AND 9U "RUMMETT AND $UMONT
+OBAYASHI A ! SHORT TIME AFTER FERTILIZA
TION THE CHORION IS COMPLETELY LIFTED AWAY FROM THE
OOLEMMA AND THE NARROW PERIVITELLINE SPACE IS CLEARLY
DEMARCATED !S EXOCYTOSIS CONTINUES THE SPACE CON
TINUES TO WIDEN AS THE EXTRUDED CONTENTS OF THE CORTICAL
ALVEOLI BECOME ORGANIZED AS A CONSPICUOUS LAYER OF
GELATINOUS MATERIAL UNDER THE CHORION 4HERE ARE TWO
FACTORS INVOLVED IN CREATING THE PERIVITELLINE SPACE NOT
ONLY IS THERE A DECREASE IN THE VOLUME OF OOPLASM AS
A RESULT OF THE LOSS OF THE CORTICAL ALVEOLI BUT THERE
MAY ALSO BE AN EXPANSION IN THE DIAMETER OF THE EGG
ITSELF CAUSED BY THE OSMOTIC INmUX OF WATER )WAMATSU
AND /HTA )NDEED BECAUSE OF THIS EXPANSION
THE CHORION BECOMES THINNER ! SOFT ELASTIC CHORION
IS FOUND FOR EXAMPLE IN EGGS OF THE LONG ROUGH DAB
(IPPOGLOSSOIDES PLATESSOIDES LIMANDOIDES AND A
LARGE PERIVITELLINE SPACE IS PRODUCED THAT CONSTITUTES
AS MUCH AS OF THE TOTAL VOLUME OF THE EGG ,N
NING AND $AVENPORT )N EGGS OF THE COD 'ADUS
MORHUA ON THE OTHER HAND THE CHORION IS INEXTENSIBLE
AND THE SMALL PERIVITELLINE SPACE WHICH OCCUPIES UP
TO OF THE VOLUME OF THE EGG IS CREATED MAINLY AT
THE EXPENSE OF THE OOPLASM $AVENPORT ,NNING AND
+JRSVIK
4HE CHORION ACTS AS A SEMIPERMEABLE MEMBRANE
BEING IMPERMEABLE TO MANY OF THE LARGE MOLECULES
OF THE ALVEOLAR EXUDATE BUT PERMEABLE TO WATER SMALL
ELECTROLYTES SUGARS AND DYES !LDERDICE *ENSEN AND
6ELSEN 4HEREFORE THE ALVEOLAR EXUDATE SETS UP
A CONCENTRATION GRADIENT ACROSS THE CHORION DRAWING
WATER AND SOLUTES INTO THE PERIVITELLINE SPACE FROM
THE BATHING MEDIUM THE SO CALLED hCOLLOID OSMOTIC
PRESSUREv 9AMAMOTO 0RESUMABLY THE NET IN
mUX CEASES WHEN INTERNAL HYDROSTATIC PRESSURE RESISTS
FURTHER INmOW !T EQUILIBRIUM HOWEVER THERE WOULD
STILL BE DIFFUSION IN BOTH DIRECTIONS OF WATER AND SMALL
ELECTROLYTES 0OTTS AND 2UDY 4HE HIGH AFlNITY
FOR WATER OF hHYDROPHILIC SOLSv IN THE ALVEOLAR EXUDATE
MAY ALSO CONTRIBUTE TO THE INmUX OF WATER ,NNING
AND $AVENPORT
4RANSPARENT 30(%2)#!, "/$)%3 ARE VISIBLE WITHIN
THE PERIVITELLINE SPACE SHORTLY AFTER THE CORTICAL REAC
TION BEGINS 4HESE ARE REMNANTS OF THE ELECTRON DENSE
CORES OF THE CORTICAL ALVEOLI THAT SWELL AND IN THE LIVING
EGG BECOME MORE TRANSPARENT IN THE MEDAKA /RYZIAS
LATIPES THEY ATTAIN DIAMETERS OF TO M 7ITH THE
SCANNING ELECTRON MICROSCOPE THEY APPEAR AS DENSE
SPHERULES ON THE INSIDE OF THE CHORION &IGURE
3PHERICAL BODIES REMAIN VISIBLE FOR SOME TIME DURING
DEVELOPMENT )T IS SUGGESTED THAT THE OOLEMMA AND
CHORION ARE HELD APART AT LEAST IN PART BY THE PHYSICAL
PRESENCE OF THESE BODIES )WAMATSU AND /HTA
7ITH THE RELEASE OF THE ALVEOLAR CONTENTS INTO THE
PERIVITELLINE SPACE A SPECIAL PROTEASE APPEARS THAT
CLEAVES THE LARGE ( HYOSOPHORIN MOLECULES INTO THEIR
LEAST REPEATING UNITS , HYOSOPHORIN AND THESE BECOME
A MAJOR CONSITUENT OF THE PERIVITELLINE mUID )NOUE
AND )NOUE )NOUE ET AL 4HE DEPOLYMER
IZATION APPEARS TO BE COMPLETE WITHIN MINUTES OF
FERTILIZATION 4HE ENZYME IS A UNIQUE PROTEINASE (9/
3/0(/2).!3% +ITAJIMA )NOUE AND )NOUE THAT
IS PROBABLY PRESENT IN AN INACTIVE FORM TOGETHER WITH
( HYOSOPHORIN WITHIN THE CORTICAL ALVEOLI +ITAJIMA
AND )NOUE 0RESUMBLY ITS ACTIVITY IS INHIBITED
IN THE DORMANT EGG BY THE HIGH IONIC STRENGTH WITH
IN THE ALVEOLI AND FOLLOWING EXOCYTOSIS IT BECOMES
ACTIVE IN THE LOW IONIC CONCENTRATIONS OF SALT WITHIN
THE PERIVITELLINE mUID )T HAS BEEN SUGGESTED THAT ONE
OF THE FUNCTIONS OF , HYOSOPHORIN MAY BE AS AN OSMO
REGULATOR IN THE PERIVITELLINE SPACE +ITAJIMA )NOUE
AND )NOUE , HYOSOPHORIN MOLECULES HAVE BEEN
REPORTED IN THE mUIDS SURROUNDING SALMONID EMBRYOS
UNTIL HATCHING
&ORMATION OF THE #HORION
&OLLOWING THE CORTICAL REACTION THE EGGS OF MOST SPE
CIES BECOME TURGID AS THE RESULT OF TWO PROCESSES NOT
ONLY IS THERE AN INmUX OF WATER CREATING INCREASED TUR
GOR PRESSURE ON THE CHORION THERE ARE ALSO CHEMICAL
AND STRUCTURAL CHANGES WITHIN THE CHORION ITSELF THAT
INCREASE ITS hHARDNESSv THEREBY MAKING IT TOUGHER AND
MORE RIGID 4HE ZONA PELLUCIDA IS CATALYTICALLY CON
VERTED INTO A HIGHLY CROSS
LINKED AND INSOLUBLE CHO
RION /PPEN
"ERNTSEN (ELVIK AND 7ALTHER
0EROXIDASE IN THE CHORION OF THE lSH 4RILOBON HAKO
NENSIS MAY HELP TOUGHEN THE CHORION BY CROSSLINKING
TYROSINE RESIDUES IN THE PRESENCE OF .A) AND (/
#(!04%2
IT MAY ALSO ASSIST IN THE DEFENCE OF THE EGG AGAINST BAC
TERIA FUNGI AND VIRUSES +UDO 3ATO AND )NOUE
4HIS TRANSFORMATION CONTRIBUTES TO THE PROTECTION OF
THE EMBRYO BOTH MECHANICALLY AND FUNCTIONALLY )T IS
ACHIEVED THROUGH THE ACTION OF EXUDATES RELEASED FROM
THE CORTICAL ALVEOLI THAT REACH THE PERIVITELLINE SPACE
BY WAY OF THE PORE CANALS 4HE CORTICAL ALVEOLI APPEAR
TO SUPPLY NOT ONLY THE STRUCTURAL COMPONENTS FOR THE
FORMATION OF THE CHORION BUT ALSO MAY BUILD AN ACTIVE
DEFENSE MECHANISM FOR THE PROTECTION OF THE EMBRYO
+UDO AND 9AZAWA )TS OUTER LAYER IS DIGESTED
ENZYMATICALLY AND REPLACED WITH THESE EXUDATES WHICH
COVER THE SURFACE WITH lNELY lLAMENTOUS MATERIAL AND
ENDOW IT WITH BACTERICIDAL AND FUNGICIDAL PROPERTIES
LODGED LARGELY IN THE OUTERMOST LAYERS THE ZONA PELLU
CIDA POSSESSED NO SUCH PROPERTIES +UDO
+UDO AND )NOUE +UDO 3ATO AND
)NOUE +UDO AND 4ESHIMA 4HE OUTER
LAYER GRADUALLY BECOMES lVE TIMES THICKER AND LOSES
ITS DISTINCTION INTO TWO LAYERS &IGURES AND
4HE TRANSFORMED CHORION DEVELOPS INCREASED CHEMI
CAL AND MECHANICAL RESISTANCE INCLUDING RESISTANCE
TO ENZYMATIC DEGRADATION %NZYMES PRODUCED BY THE
CHORION BUT NOT THE ZONA PELLUCIDA ARE ABLE TO DIGEST
SEVERAL SUBSTRATES AND ARE PRESUMED TO PROTECT THE EM
BRYO FROM INVADERS OR PATHOGENS PRESENT IN THE AMBIENT
WATER +UDO AND )NOUE +UDO #HORIONIC
EXTRACTS UNLIKE THOSE FROM THE ZONA PELLUCIDA HAVE
BEEN SHOWN TO AGGLUTINATE lSH SPERM THEREBY PROVID
ING A DETERRANT TO POLYSPERMY +UDO AND )NOUE
3EVERAL BIOCHEMICAL MODIlCATIONS RESULTING FROM THE
ACTIONS OF THE CORTICAL ALVEOLAR EXUDATES AT THE TIME
OF TRANSFORMATION HAVE BEEN RECORDED +UDO B
C
(ARDENING IS DEPENDENT UPON THE PRESENCE OF #A
IONS :OTIN $AVENPORT ,NNING AND +JRSVIK
+UDO AND 4ESHIMA 4HAT HARDENING IS
ACCOMPANIED BY A CHANGE IN THE PROTEINS OF THE CHO
RION WAS DEMONSTRATED BY SODIUM DODECYL SULPHATE
POLYACRYLAMIDE GEL ELECTROPHORESIS 3$3
0!'%
WHERE CHORIONS OF UNFERTILIZED EGGS OF THE MEDAKA
/RYZIAS LATIPES GAVE FOUR MAJOR PROTEIN BANDS OF
AND K$A WHEREAS AFTER HARDENING BANDS
WERE OBTAINED OF AND K$A -ASUDA )UCHI
AND 9AMAGAMI 3IMILAR CHANGES IN THE CON
STITUENT PROTEINS WERE DETECTED FOLLOWING HARDENING
OF THE CHORIONS OF RAINBOW TROUT /NCORHYNCHUS MYKISS
)UCHI -ASUDA AND 9AMAGAMI
(ARDENING OF CHORIONS DOES NOT OCCUR TO THE SAME
EXTENT IN EGGS OF ALL SPECIES $AVENPORT ,NNING AND
+JRSVIK &OR EXAMPLE CHORIONS OF THE DEMER
SAL EGGS OF THE LUMPSUCKER #YCLOPTERUS LUMPUS WHICH
MUST WITHSTAND CONTACT AND ABRASION WITH THE SUB
STRATE BECOME TEN TIMES HARDER THAN THOSE OF PELAGIC
EGGS OF THE COD 'ADUS MORHUA ,NNING +JRSVIK
AND $AVENPORT 4HERE APPEARS TO BE A STRUCTURAL
MANIFESTATION OF HARDENING IN SOME SPECIES ,NNING
+JRSVIK AND $AVENPORT $AVENPORT ,NNING
AND +JRSVIK (ARD CHORIONS HAVE A SURFACE
WITH LARGE CHARACTERISTIC PAPILLAE AND THE PORES ARE
lLLED WITH THE SAME ADHESIVE SUBSTANCE THAT COVERS THE
SURFACE OF THE EGGS AND BINDS THEM INTO MASSES SOFT
CHORIONS STILL RETAIN THE REGULAR PATTERN OF PORES OF THE
UNFERTILIZED EGG &IGURE
"LOCK TO 0OLYSPERMY
3EVERAL MECHANISMS OPERATE IN TELEOSTS TO PREVENT
PENETRATION OF THE OOLEMMA BY MORE THAN ONE SPER
MATOZOON .O RECENT LITERATURE IS AVAILABLE ON OTHER
GROUPS OF lSH BUT IT IS KNOWN THAT IN CYCLOSTOMES
ACIPENSERIDS AS WELL AS TELEOSTS A SINGLE SPERMATO
ZOON ENTERS THE EGG AT FERTILIZATION (ART )N
SHARKS AND CHIMAERAS HOWEVER MORE THAN ONE SPER
MATOZOON MAY PENETRATE THE OOLEMMA ALTHOUGH ONLY
ONE SPERMATOZOON NUCLEUS FUSES WITH THE EGG NUCLEUS
!LTHOUGH STURGEON EGGS HAVE SEVERAL MICROPYLES THESE
ARE LOCATED IN A SMALL AREA ON THE EGG SURFACE AND THE
CORTICAL REACTION PASSES OVER THEM IN SUCH A SHORT TIME
THAT POLYSPERMY SELDOM OCCURS 'INSBURG
)N MANY ANIMALS WHERE THE EGGS LACK A CHORION
THERE ARE TWO BLOCKS TO POLYSPERMY A &!34 ",/#+
BROUGHT ABOUT BY A CHANGE IN MEMBRANE POTENTIAL AND
A 3,/7 ",/#+ INDUCED BY EXOCYTOSIS OF THE CONTENTS
OF THE CORTICAL ALVEOLI *AFFE )N lSH WHERE THE
CHORION RESTRICTS SPERM ACCESS THERE IS NO NEED FOR THE
FAST ELECTRICAL BLOCK AND POLYSPERMY IS PREVENTED BY
AN ARRAY OF MECHANICAL MEANS (AGIWARA AND *AFFE
.UCCITELLI B 4HE MICROPYLE OF MANY
SPECIES IS A PASSAGE SO NARROW THAT IT RESTRICTS ACCESS
TO THE OOLEMMA TO ONLY ONE SPERMATOZOAN &IGURES
AND 'INSBURG 3AKAI "RUM
METT AND $UMONT )WAMATSU AND /HTA B
+OBAYASHI AND 9AMAMOTO (ART AND $ONO
VAN +UDO B /HTA AND )WAMATSU
)SHIJIMA (AMAGUCHI AND )WAMATSU )N ADDI
TION A NARROWING OF THE MICROPYLAR CANAL IS REPORT
ED FOLLOWING FERTILIZATION IN SOME SPECIES THEREBY
EXCLUDING SUPERNUMERARY SPERMATOZOA &IGURES
AND +OBAYASHI AND 9AMAMOTO
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
(IRAI AND 9AMAMOTO 9AMAMOTO AND +OBAYAS
HI )WAMATSU )SHIJIMA AND .AKASHIMA
)WAMATSU %XTRACTS OF THE CHORION BUT NOT OF
THE ZONA PELLUCIDA HAVE THE ABILITY NONSPECIlCALLY TO
AGGLUTINATE lSH SPERMATOZOA +UDO AND )NOUE
THIS WOULD TEND TO INHIBIT POLYSPERMY
7HEN THE HEAD OF THE lRST SPERMATOZOON PENE
TRATES THE OOLEMMA THE CORTICAL REACTION IS TRIGGERED
AND THE SUPERNUMERARY SPERMATOZOA LINED UP BEHIND
IT ARE FORCIBLY EJECTED FROM THE MICOPYLAR CANAL BY
A JET STREAM OF PERIVITELLINE mUID &IGURE AND
A FEW SECONDS AFTER ACTIVATION A PLUG OF AMORPHOUS
AND GRANULAR MATERIAL MAY BLOCK THE MICROPYLAR CANAL
&IGURES AND +OBAYASHI AND 9AMAMOTO
7OLENSKI AND (ART A )WAMATSU ET AL
)WAMATSU )SHIJIMA AND .AKASHIMA )N
ADDITION A &%24),):!4)/. #/.% MAY RISE FROM THE OO
LEMMA FORMING A PLUG AT THE INNER OPENING OF THE MI
CROPYLAR CANAL &IGURE !FTER FERTILIZATION IN THE
ROSY BARB "ARBUS CONCHIONUS THE ENTRANCE TO THE MI
CROPYLAR CANAL IS BLOCKED BY NON
FERTILIZING SPERM FOL
LOWING ELEVATION OF THE FERTILIZATION MEMBRANE &IGURE
# !MANZE AND )YENGAR !LTHOUGH THE
MICROPYLAR CANAL OF THE CARP #YPRINUS CARPIO IS BROAD
ENOUGH TO ACCOMMODATE SEVERAL SPERMATOZOA ABREAST
A CONSPICUOUS FERTILIZATION CONE FORMS A PLUG THAT PEN
ETRATES THE CANAL AND EXCLUDES SUPERNUMERARY INVADERS
&IGURE +UDO )N SOME SPECIES THE FERTIL
IZATION CONE IS FORMED BY A TUFT OF MICROVILLI THAT SUR
ROUND THE FERTILIZING SPERMATOZOON ON THE EGG SURFACE
&IGURES ! " )WAMATSU AND /HTA /HTA
AND )WAMATSU +UDO AND 3ATO /HTA
BUT IN OTHERS IT IS FORMED WITHOUT THE APPARENT
INVOLVEMENT OF MICROVILLI &IGURE +OBAYASHI
AND 9AMAMOTO "RUMMETT $UMONT AND 2ICHTER
7OLENSKI AND (ART A 4HE PLASMA MEM
BRANE SHED BY THE FERTILIZING SPERMATOZOON AS IT ENTERS
THE OOPLASM MAY BE INCORPORATED INTO THE OOLEMMA
OF THE FERTILIZATION CONE AND SINCE THIS MEMBRANE HAS
NO AFlNITY WITH THE MEMBRANE OF OTHER SPERMATOZOA
MAY DETER PENETRATION BY THEM +OBAYASHI AND 9AMA
MOTO )N SPITE OF VARIOUS MECHANICAL BLOCKS TO
POLYSPERMY HOWEVER A FEW SPERMATOZOA MAY PEN
ETRATE INTO THE PERIVITELLINE SPACE ONLY TO BE INACTIVAT
ED BY AN hAGGLUTINATING FACTORv PRESUMABLY LECTINS
RELEASED BY RUPTURE OF THE CORTICAL ALVEOLI "RUMMETT
AND $UMONT .OSEK +RAJHANZL AND +OCOUREK
+UDO AND )NOUE
7ITH AS MANY AS OR MORE MICROPYLES IN
!CIPENSERIFORMES THERE WOULD SEEM TO BE AMPLE OP
PORTUNITY FOR POLYSPERMY )T APPEARS THAT THIS IS PRE
VENTED AT LEAST IN THE PADDLElSH 0OLYODON SPATHULA
BY THE FORMATION OF CYTOPLASMIC PROCESSES PROBABLY
FERTILIZATION CONES WITHIN ONE MINUTE AFTER ACTIVATION
THAT SEAL THE MICROPYLAR CANALS &IGURE ,INHART
AND +UDO
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF UNFERTILIZED UNACTIVATED EGGS OF &UNDULUS HETEROCLITUS FROM
WHICH THE CHORION HAS BEEN REMOVED &ROM "RUMMETT AND $UMONT REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
! 4HE HEMISPHERICAL BULGES REVEAL THE LOCATIONS OF CORTICAL ALVEOLI #! BENEATH THE SURFACE OF THE EGG %3 ! DENSE MAT OF
MICROVILLI INVESTS THE SURFACE EXCEPT OVER THE CORTICAL ALVEOLI 8
" ! CORTICAL ALVEOLUS LIES IN THE OOPLASM IMMEDIATELY BENEATH THE SMOOTH BULGE ON THE SURFACE OF THE EGG MICROVILLI
ARE ABUNDANT ELSEWHERE 8
&IGURE )MAGES OF THE EGG CORTEX OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM (ART AND #OLLINS REPRODUCED WITH
PERMISSION FROM 3PRINGER 6ERLAG
! 3CANNING ELECTRON MICROGRAPH OF A CROSS FRACTURED CORTEX OF AN UNACTIVATED EGG SHOWING THE PLASMA MEMBRANE 0 DECO
RATED WITH A RETICULUM OF SMALL FOLDS AND CORTICAL GRANULES #' 8
" 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CORTEX OF AN UNACTIVATED EGG 4HE OUTER LAYER OF THE CORTICAL
CYTOPLASM SMALL ARROWHEADS IS MORE ELECTRON DENSE THAN THE DEEPER LESS COMPACT LAYER WITH CORTICAL GRANULES #'
4HE LARGE ARROWHEADS POINT TO PROlLES OF SMOOTH CISTERNAE OF THE CORTICAL ENDOPLASMIC RETICULUM 8
!BBREVIATIONS #6 COATED VESICLE , LYSOSOME - MITOCHONDRION
# &REEZE FRACTURE REPLICA OF THE CORTICAL OOPLASM OF AN UNACTIVATED EGG WITH 0 FACE 0 AND % FACE % SURFACES OF THE FRAC
TURED MEMBRANES OF CORTICAL GRANULES 4HE LARGE ARROW INDICATES THE DIRECTION OF SHADOWING 8
$ % &REEZE FRACTURE IMAGES OF AN EGG TWO MINUTES AFTER ACTIVATION 0 FACE REPLICAS OF ELEVATED CORTICAL GRANULES SHOW AN
ABSENCE OF MEMBRANE PARTICLES FROM THE SITE OF CONTACT BETWEEN THE APPOSED MEMBRANE OF THE CORTICAL ALVEOLUS AND
THE OOLEMMA 4HE INWARD DIMPLE ARROWHEAD IN % IN THE REPLICA OF THE ELEVATED CORTICAL GRANULE APPEARS TO MARK THE SITE
OF FUSION BETWEEN THE MEMBRANE OF THE CORTICAL GRANULE AND THE OOLEMMA $ 8 % 8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF THE UNACTIVATED EGG OF THE ZEBRAlSH "RACHYDANIO RERIO TO ILLUSTRATE THE CORTICAL
ENDOPLASMIC RETICULUM &ROM (ART AND #OLLINS REPRODUCED WITH PERMISSION FROM 3PRINGER
6ERLAG
! &REEZE
FRACTURE REPLICA SHOWING THE CORTICAL ENDOPLASMIC RETICULUM ARROWHEADS BRANCHING IN THE CORTICAL CYTOPLASM
8
!BBREVIATIONS ' 'OLGI COMPLEX - MITOCHONDRION
" # 2EPLICAS SHOWING THE CLOSE APPOSITION BETWEEN THE CORTICAL ENDOPLASMIC RETICULUM AND THE OOLEMMA 0 IN " AND
THE MEMBRANE OF A CORTICAL GRANULE #'- IN # " 8 # 8
$ 4RANSMISSION ELECTRON MICROGRAPH TO ILLUSTRATE THE NARROW GAP SEPARATING THE CORTICAL ENDOPLASMIC RETICULUM AND
OOLEMMA 0 8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE $IAGRAM OF AN UNFERTILIZED EGG OF THE MEDAKA /RYZIAS LATIPES MM IN DIAMETER &ROM 'ILKEY
REPRODUCED WITH KIND PERMISSION FROM THE 3OCIETY FOR )NTEGRATIVE AND #OMPARATIVE "IOLOGY ! SPERM WILL CROSS THE CHORION
#H VIA THE MICROPYLE - ENTER THE CYTOPLASM #Y AND INITIATE A WAVE OF CORTICAL VESICLE SECRETION 6ESICLES ARE INDICATED
BY SMALL CIRCLES -OST OF THE EGG IS OCCUPIED BY THE MEMBRANE
BOUND YOLK COMPARTMENT 9 4HE CYTOPLASMIC THICKNESS
MM IS EXAGGERATED AND OIL DROPLETS ARE OMITTED FOR CLARITY
&IGURE #ORTICAL GRANULES FROM UNACTIVATED EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM (ART AND #OLLINS
REPRODUCED WITH PERMISSION FROM 3PRINGER
6ERLAG
! %LECTRON MICROGRAPH OF A REPLICA OF A FREEZE
FRACTURED CORTICAL GRANULE SHOWING CENTRAL # AND PERIPHERAL 0 CONTENTS
WITHIN MEMBRANE ARROWHEADS 8
" ! HIGHER MAGNIlCATION OF THE REPLICA SHOWING CONTENTS OF THE CENTRAL REGION ON THE LEFT PERIPHERAL CONTENTS ON THE RIGHT
8
# 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF A CORTICAL GRANULE SHOWING THE lBRILLO
GRANULAR MESHWORK OF THE PERIPH
ERAL CONTENTS 8
$ 3OME CORTICAL GRANULES LACK THE PERIPHERAL HALO 4HIS ELECTRON MICROGRAPH OF A REPLICA OF A FREEZE
FRACTURED CORTICAL
GRANULE SHOWS ONLY SMALL PARTICLES WITHIN THE LIMITING MEMBRANE ARROWHEADS 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF CORTICAL GRANULES OF RAINBOW TROUT 3ALMO GAIRDNERI 4HE GRAN
ULE CONSISTS OF AN ELECTRON
LUCENT SPHERICAL CORE AND AN ELECTRON
DENSE PERIPHERAL REGION "AR M &ROM )NOUE AT AL
REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE CORTICAL CYTOPLASM OF UNACTIVATED EGGS OF THE ROSE BITTER
LING 2HODEUS OCELLATUS OCELLATUS SHOWING TWO TYPES OF CORTICAL ALVEOLI &ROM /HTA ET AL REPRODUCED WITH PERMISSION
! #ORTICAL ALVEOLI #! OF THE ANIMAL POLE AREA CONTAIN ELECTRON
LUCENT DROPLETS ARROWS WITHIN AN ELECTRON
DENSE MATRIX
8
" #ONTENTS OF CORTICAL ALVEOLI AT THE VEGETAL POLE ARE HOMOGENEOUS AND ELECTRON
DENSE 8
!BBREVIATION #( CHORION
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE CORTICAL CYTOPLASM OF A MATURE EGG OF THE COMMON CARP
#YPRINUS CARPIO $EPOSITS OF THE REACTION PRODUCT FOR CHOLINESTERASE ACTIVITY ARE LOCALIZED ON THE PLASMALEMMA IN THE CYTOPLAS
MIC MATRIX IN MITOCHONDRIA AND ON A FEW CISTERNAL MEMBRANES OF THE GRANULAR ENDOPLASMIC RETICULUM BUT NOT IN THE CORTICAL
ALVEOLI OR #!
GRANULES !' &ROM +UDO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
!BBREVIATIONS ,# LARGE CORTICAL ALVEOLUS 3# SMALL CORTICAL ALVEOLUS "AR M 8
&IGURE 4HE OVERALL STRUCTURE OF THE , HYOSOPHORIN FROM THE MEDAKA /RYZIAS MELASTIGMA &ROM 4AGUCHI ET AL
REPRODUCED WITH PERMISSION FROM THE !MERICAN 3OCIETY FOR "IOCHEMISTRY AND -OLECULAR "IOLOGY
#(!04%2
&IGURE 4HE ,
HYOSOPHORIN OF THE mOUNDER 0ARALICHTHYS OLIVACEUS DIFFERS FROM THAT OF OTHER lSH IN POSSESSING A
PENTAANTENNARY CARBOHYDRATE STRUCTURE &ROM 3EKO ET AL REPRODUCED WITH PERMISSION FROM THE !MERICAN 3OCIETY
FOR "IOCHEMISTRY AND -OLECULAR "IOLOGY
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE MICROPYLAR REGION OF AN UNFERTILIZED EGG OF
THE BITTERLING 2HODEUS OCELLATUS &ROM /HTA REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC 4HERE ARE
WELL
DEVELOPED MICROVILLI OR MICROPLICAE AT THE SPERM ENTRY SITE 33 ON THE EGG SURFACE BENEATH THE MICROPYLE #( CHORION
8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE -ICROGRAPHS OF SECTIONS OF EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO IN THE REGION OF THE MICROPYLE TAKEN
SECONDS AFTER INSEMINATION &ROM 7OLENSKI AND (ART B REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! 0HOTOMICROGRAPH OF AN EGG WHICH HAS COMPLETELY INCORPORATED THE SPERM HEAD ARROW 4HERE IS NO EVIDENCE OF A FERTILIZA
TION CONE 4HE CORTICAL GRANULES ARROWHEADS HAVE NOT BROKEN DOWN AND THE CHORION # HAS NOT RAISED FROM THE OOLEMMA
8
" 4RANSMISSION ELECTRON MICROGRAPH OF THE SAME EGG SHOWING THE SPERM NUCLEUS 3 BENEATH THE OOLEMMA 4HE CYTOPLASM
AT THE SPERM ENTRY SITE IS RAISED SLIGHTLY 8
#(!04%2
&IGURE $IAGRAMMATIC REPRESENTATION OF THE EVENTS ASSOCIATED WITH SPERM PENETRATION IN EGGS OF THE MEDAKA /RYZIAS
LATIPES AS SEEN WITH THE SCANNING ELECTRON MICROSCOPE FOLLOWING lXATION AND REMOVAL OF THE CHORION 4IMES AFTER INSEMINATION
ARE INDICATED IN SECONDS 2APID ENGULFMENT OF THE SPERM HEAD IS FOLLOWED BY FORMATION OF THE FERTILIZATION CONE 4HE FOREST OF
MICROVILLI COVERING THE SURFACE OF THE OOLEMMA IS ABSENT FROM THE FERTILIZATION CONE !FTER INCORPORATION OF THE SPERM THE CONE
RETRACTS AND DISAPPEARS &ROM )WAMATSU AND /HTA B REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE SPERM ATTACHMENT SITE IN THE EGG OF THE MEDAKA /RYZIAS LATIPES
SHORTLY AFTER INSEMINATION &ROM )WAMATSU AND /HTA REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! ! SPERMATOZOON ON THE VITELLINE SURFACE 4HE SPERM HEAD HAS BEEN CAUGHT BY MICROVILLI OF THE EGG SECONDS AFTER INSEMI
NATION 4HERE HAS BEEN NO FUSION BETWEEN THE PLASMA MEMBRANES OF THE SPERM AND EGG 8
" ! SPERMATOZOON SURROUNDED BY MICROVILLI -6 AND THE FERTILIZATION CONE &# SEE INSET OF THE EGG SECONDS AFTER INSEM
INATION 4HE SPERM TAIL 34 IS TRAPPED BY MICROVILLI 8 4HERE HAS BEEN NO FUSION BETWEEN THEIR PLASMA MEMBRANES
8
# ! HIGHER MAGNIlCATION OF THE POINT OF CONTACT BETWEEN SPERM AND EGG SHOWN IN " 4HERE HAS BEEN NO FUSION BETWEEN THEIR
PLASMA MEMBRANES 8
$ ! SPERMATOZOON ENCLOSED BY CYTOPLASMIC PROTRUSIONS OF THE EGG MINUTE AFTER INSEMINATION 4HERE HAS BEEN PARTIAL FUSION
ARROW OF THE PLASMA MEMBRANES OF THE SPERM AND EGG 8
#(!04%2
&IGURE 0HOTOMICROGRAPHS OF A LIVING EGG OF THE MEDAKA /RYZIAS LATIPES SHOWING THE EARLY RESPONSE OF THE ANIMAL
POLE REGION TO SPERM ENTRY )N THESE lGURES ABOUT lVE MINUTES HAS ELAPSED FOLLOWING ATTACHMENT OF THE SPERMATOZOON TO THE
OOLEMMA "AR M &ROM )WAMATSU REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! !N EGG WITH TWO SPERMATOZOA IN THE MICROPYLE HAS RESPONDED BY EXOCYTOSIS OF CORTICAL ALVEOLI CA AROUND THE INNER END
ARROW OF THE MICROPYLAR CANAL O OIL DROPLET
" # 4HE SECOND SPERMATOZOON WHITE ARROWHEAD HAS BEEN PUSHED TOWARD THE MICROPYLAR VESTIBULE BY THE FERTILIZATION CONE
SURROUNDING THE lRST SPERMATOZOON
$
& 3UPERNUMERARY SPERMATOZOA WHITE ARROWHEADS HAVE BEEN SQUEEZED OUT OF THE MICROPYLE
' ( 4HE LOWER THIRD BETWEEN ARROWS OF THE MICROPYLAR CANAL HAS CLOSED "LACK ARROWHEADS INDICATE THE LARGE BLISTER
LIKE
FERTILIZATION CONE
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
@
&IGURE 3CANNING ELECTRON MICROGRAPH OF AN EGG
FUSED WITH A SPERM HEAD SMALL ARROW AT THE SPERM ENTRY
SITE ON THE EGG SURFACE IMMEDIATELY UNDER THE MICROPYLE
IN EGGS OF 4RIBOLODON HAKONENSIS 4HE FERTILIZATION CONE
LARGE ARROW HAS RISEN FROM THE REGION OF THE SITE BENEATH THE
FUSED SPERM HEAD 4HE ARROWHEAD INDICATES THE SPERM TAIL
8 &ROM +UDO A REPRODUCED WITH PERMISSION
OF *OHN 7ILEY 3ONS )NC
@
&IGURE 3CANNING
ELECTRON
MICROGRAPHS SHOWING THE PROCESS OF
SPERM ENTRY THROUGH THE MICROPYLES
OF INSEMINATED EGGS OF THE ROSE BIT
TERLING 2HODEUS OCELLATUS OCELLATUS
&ROM /HTA AND .ASHIROZAWA
REPRODUCED WITH PERMISSION OF *OHN
7ILEY 3ONS )NC
! /NE MINUTE AFTER INSEMINATION
! FERTILIZING SPERMATOZOON AR
ROW IS VISIBLE AT THE SPERM ENTRY
SITE 8
" 4HREE MINUTES AFTER INSEMINATION
4HE FERTILIZING SPERMATOZOON IS NO
LONGER VISIBLE AND A SWOLLEN MASS
3- HAS FORMED AND PLUGS THE
MICROPYLE 8
# &IVE MINUTES AFTER INSEMINATION
8
$ 4WENTY MINUTES AFTER INSEMINA
TION ! SWOLLEN MASS REMAINS
PLUGGING THE MICROPYLE 8
#(!04%2
&IGURE %NGULFMENT OF THE SPERM HEAD IN EGGS OF TILAPIA /REOCHROMIS NILOTICUS IS FOLLOWED BY AN INDENTATION OF
THE OOLEMMA THE CLEFT OF PENETRATION 4HIS IS A SCANNING ELECTRON MICROGRAPH OF THE CLEFT OF PENETRATION IN A DECHORIONATED EGG
FOLLOWING PENETRATION OF THE SPERM HEAD ONE MINUTE AFTER INSEMINATION 8 4HE SPERM TAIL REMAINS OUTSIDE INSET 8
&ROM "ERN AND !VTALION REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 3CANNING ELECTRON MICROGRAPHS SHOWING THE TWO
TIERED FERTILIZATION CONE THAT IS FORMED IN THE AYU lSH
0LECOGLOSSUS ALTIVELIS 4HE CHORION WAS DISSECTED AWAY AFTER lXATION &ROM +UDO B REPRODUCED WITH PERMISSION FROM
"LACKWELL 0UBLISHING
! 4HE lRST FERTILIZATION CONE && IS A CYLINDRICAL STRUCTURE THAT RISES FROM THE SPERM ENTRY SITE WITHIN SECONDS OF IMMERSION
IN FRESH WATER 8
" !T ABOUT SECONDS A SECOND TIER FORMS A PEDESTAL 0 ELEVATING THE lRST CONE && FROM ITS APEX 4HE SPERM TAIL IS IN CLOSE
CONTACT WITH THE lRST FERTILIZATION CONE ARROWS 8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 3CANNING ELECTRON MICROGRAPHS OF FERTILIZATION CONES IN EGGS OF THE CARP #YPRINUS CARPIO )N THESE PREPARATIONS
THE EGG ENVELOPES WERE REMOVED MECHANICALLY AFTER lXATION 8 &ROM +UDO AND 3ATO REPRODUCED WITH PERMISSION
FROM "LACKWELL 0UBLISHING
! 4HE SPERM ENTRY SITE IN AN UNFERTILIZED EGG CONSISTS OF A TUFT OF MICROVILLI
" &USION OF SPERM AND EGG AT SECONDS AFTER ACTIVATION BY IMMERSION IN FRESH WATER ! FEW MICROVILLI OF THE SPERM ENTRY SITE
SURROUND THE FUSED SPERM HEAD
# &ORMATION OF AN EARLY FERTILIZATION CONE AT SECONDS 4HE CONE ARROW IS A DOME
LIKE EMINENCE ATOP THE FUSED SPERM
HEAD
$ 4HE EARLY FERTILIZATION CONE AT SECONDS
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION OF FERTILIZED EGGS OF THE CARP #YPRINUS CARPIO )N THESE
PREPARATIONS THE EGG ENVELOPES WERE REMOVED MECHANICALLY AFTER lXATION 8 &ROM +UDO AND 3ATO REPRODUCED
WITH PERMISSION FROM "LACKWELL 0UBLISHING
! 3OME LARGE PITS SURROUNDING THE MICROPYLAR REGION CONTAIN CORTICAL ALVEOLAR MATERIAL SMALL ARROW AT SECONDS AFTER
ACTIVATION BY IMMERSION IN FRESH WATER 4HE LARGE ARROW INDICATES AN EARLY FERTILIZATION CONE 8
" 4HE LATE FERTILIZATION CONE HAS FORMED IN THE MICROPYLAR REGION BY SECONDS )T CONSISTS OF AN EMINENCE RESEMBLING A WIDE
MOUTHED VOLCANO CONTAINING THE EARLY FERTILIZATION CONE WITHIN ITS CRATER ARROW 8
# ! LATE FERTILIZATION CONE AT SECONDS WITH THE SHORTENED EARLY CONE AND A SPERM TAIL AT ITS APEX 8
$ ! LATE FERTILIZATION CONE AT SECONDS 4HE EARLY FERTILIZATION CONE HAS RETRACTED AND ONLY A SPERM TAIL REMAINS ARROW
8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE EXTERNAL ORIlCE OF THE MICROPYLAR CANAL OF AN UNIMPREGNATED ! AND IM
PREGNATED " FEMALE ELKHORN SCULPIN !LCICHTHYS ALCICORNIS TO DEMONSTRATE INTERNAL GAMETIC ASSOCIATION 3PERM INTRODUCED INTO
THE OVARIAN CAVITY BY COPULATION ENTER THE MICROPYLAR CANALS OF OVULATED EGGS BUT THERE IS NO SPERMEGG FUSION UNTIL THE EGGS
ARE RELEASED INTO SEAWATER 8 &ROM -UNEHARA 4AKANO AND +OYA REPRODUCED WITH PERMISSION OF THE !MERICAN
3OCIETY OF )CHTHYOLOGISTS AND (ERPETOLOGISTS
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF EGGS OF THE ELKHORN SCULPIN !LCICHTHYS ALCICORNIS AFTER IM
MERSION IN SEAWATER &ROM +OYA 4AKANO AND 4AKAHASHI REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF
*APAN
! "Y TEN SECONDS AFTER IMMERSION IN SEAWATER A FERTILIZING SPERMATOZOON HAS PENETRATED THE OOPLASM AND FUSION OF THE MEM
BRANES OF THE SPERM AND EGG HAS BEGUN 3EVERAL VESICLES ARE SEEN NEAR THE SPERM HEAD ARROWS 8
#(!04%2
&IGURE #ONTINUED
" "Y TWO MINUTES AFTER IMMERSION IN SEA WATER THE SPERM HEAD AND MITOCHONDRIA M HAVE PENETRATED THE OOPLASM
4HE OOPLASM AROUND THE SPERM FORMS AN ELECTRON
DENSE ZONE EDL CONTAINING LYSOSOMES 8
# !T TWO MINUTES THE VESICLES ARROWS ARE ARRANGED IN A ROW NEAR THE SPERM NUCLEUS N 8
$ 4HE MICROTUBULES OF THE SPERM TAIL HAVE DEGENERATED BY SECONDS AFTER IMMERSION IN SEAWATER 4HE SPERM MITOCHONDRIA
M REMAIN OUTSIDE THE OOLEMMA 8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE #ONTINUED
% 4HE PENETRATED SPERM NUCLEUS N IN THE OOPLASM THREE MINUTES AFTER IMMERSION 4HE NUCLEAR MEMBRANE BECOMES
VESICULATED BEGINNING AT THE ANTERIOR REGION OF THE SPERM HEAD ARROWS 8
& !T THREE MINUTES CHROMATIN OF THE PENETRATED SPERM DISPERSES A FRAGMENT OF THE NUCLEAR MEMBRANE IS VISIBLE NEAR THE
CENTRIOLE ARROW 8
' "Y lVE MINUTES AFTER IMMERSION THE SECOND POLAR BODY IS UNDERGOING ITS SECOND MEIOTIC DIVISION WITHIN THE PERIVITELLINE
SPACE 8
#(!04%2
&IGURE )NTERNAL FERTILIZATION MAY TAKE PLACE IN 3OUTH !MERICAN CATlSH 4RACHELYOPTERUS SPP &ROM -EISNER ET AL
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOGRAPH NEGATIVE REVERSED OF THE UNMODIlED ANAL lN OF A MATURE FEMALE 4 LUCENAI "AR MM
" 0HOTOGRAPH NEGATIVE REVERSED OF THE MODIlED ANAL lN OF A MATURE MALE 4 LUCENAI "AR MM
# 0HOTOMICROGRAPH OF A SECTION THROUGH THE OVARY OF A MATURE FEMALE 4 LUCENAI WITH SPERMATOZOA ARROW CLOSELY ASSOCIATED
WITH THE EPITHELIUM E LINING THE OVARIAN LUMEN O OOCYTE "AR M
$ 0HOTOMICROGRAPH OF A SECTION THROUGH THE OVARY OF A MATURE FEMALE OF 4 GALEATUS SHOWING SPERMATOZOA ARROW IN THE
OVARIAN LUMEN E OVARIAN EPITHELIUM "AR M
&IGURE 3PERMATOZOA OF THE WHITE STURGEON !CIPENSER TRANSMONTANUS POSSESS A CAP
LIKE MEMBRANE
BOUND SAC
THE ACROSOME &ROM #HERR AND #LARK REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! "Y PHASE CONTRAST MICROSCOPY THE ACROSOME CAN BEEN SEEN AT THE ANTERIOR END OF THE SPERM HEAD 8
" 4HIS TRANSMISSION ELECTRON MICROGRAPH OF A LONGITUDINAL SECTION THROUGH THE BODY OF A SPERM SHOWS THE ACROSOMAL REGION
! NUCLEUS . AND MIDPIECE -0 8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CHORION AND TUFT AT THE ANIMAL POLE OF A RECENTLY
SPAWNED EGG OF A RIVER LAMPREY ,AMPETRA mUVIATILIS 4HE INNER CHORION ICH SHOWS ONLY FAINT RADIAL STRIATIONS PRODUCED BY
INDISTINCT PORE CANALS LEADING TO THE SURFACE OF THE EGG E -ANY SLIGHTLY OBLIQUE SECTIONS OF PORE CANALS PC PENETRATE THE OUTER
CHORION OCH 4HE OUTER CHORION CONTAINS LARGE NUMBERS OF ELECTRON DENSE PARTICLES DM SCATTERED AMONG lNE RADIAL lBRES AND
AN OCCASIONAL MEMBRANOUS REMNANT M /NLY THE INNERMOST LAYER OF THE TUFT T WITH SOME GRANULES G IS VISIBLE "AR M
&ROM !FZELIUS .ICANDER AND 3JDN REPRODUCED WITH PERMISSION FROM THE #OMPANY OF "IOLOGISTS ,TD
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE HEADS OF SPERM OF THE RIVER LAMPREY ,AMPETRA mUVIATILIS
&ROM .ICANDER AND 3JDN REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! " !PEX OF SPERM HEADS EMBEDDED WITHIN THE CHORION OF AN EGG FOLLOWING THE FORMATION OF THE ACROSOMAL TUBULE !T
CONTAINING ITS HEAD lLAMENT WITHIN 4HE SUBACROSOMAL RING 3!2 HAS PARTLY EMERGED FROM A DEPRESSION IN THE NUCLEAR
APEX . 4HE BASAL ACROSOMAL MEMBRANE HAS FUSED WITH THE PLASMA MEMBRANE OF THE SPERM HEAD IN ! ARROW IT RETAINS
SPOTLIKE THICKENINGS IN " ARROWS 8
# ,ONGITUDINAL SECTION OF THE ACROSOMAL TUBULE WITHIN A PORE OF THE INNER CHORION ICH )TS HEAD lLAMENT ASSUMED #F
A HELICAL FORM AND THE MEMBRANE OF THE ACROSOMAL TUBULE IS WRINKLED ARROWS 8
$ !N ACROSOMAL TUBULE !T AND HEAD lLAMENT LYING WITHIN THE NARROW PERIVITELLINE SPACE OF AN INSEMINATED EGG 0VS
BETWEEN THE INNER CHORION ICH AND PROJECTIONS OF THE EGG SURFACE EP 8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACES OF DECHORIONATED RIPE EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO
lXED AT INTERVALS AFTER ACTIVATION BY IMMERSION IN FRESH WATER &ROM (ART 9U AND 'REENHUT REPRODUCED WITH PERMIS
SION OF *OHN 7ILEY 3ONS )NC
! 4HE SURFACE OF AN EGG TWO MINUTES AFTER ACTIVATION #ORTICAL GRANULES ARE IN VARIOUS STAGES OF ELEVATION AND EXTRUSION
8
" 4HE EGG SURFACE SHOWN IN ! .OTE THE LIMITING MEMBRANE OF THE EVACUATED CORTICAL GRANULE 8
# 4HE SURFACE OF AN EGG FOUR MINUTES AFTER ACTIVATION 8
$ ! CORTICAL GRANULE WITH DENSE CORE AND SURROUNDING GRANULAR MATERIAL BEING EXTRUDED %NVELOPMENT OF THE LIMITING
MEMBRANE #- OF A CORTICAL GRANULE WITHIN SEVERAL FOLDS OF THE OOLEMMA ARROW SUGGESTS ITS RETRIEVAL BY THE EGG CELL
8
% 4HE SURFACE OF THE OOLEMMA SEVEN MINUTES AFTER ACTIVATION 8
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF MATURE EGGS OF THE ROSE BITTERLING 2HODEUS OCELLATUS OCELLATUS ACTIVATED BY
IMMERSION IN FRESH WATER &ROM /HTA ET AL REPRODUCED WITH PERMISSION 4HE MICROGRAPHS ! TO $ SHOW THAT THE BREAK
DOWN OF CORTICAL ALVEOLI PROGRESSED FROM THE VEGETAL POLE 60 TO THE ANIMAL POLE !0
! !T lVE MINUTES AFTER IMMERSION IN FRESH WATER BREAKDOWN HAS BEGUN AT THE VEGETAL POLE BUT HAS NOT YET OCCURRED AT
THE ANIMAL POLE 8
" "REAKDOWN HAS OCCURRED AT THE VEGETAL POLE 8
# "Y TEN MINUTES AFTER IMMERSION IN FRESH WATER AN AREA AROUND THE SPERM ENTRY SITE AT THE ANIMAL POLE REMAINS UNCHANGED
8
$ "Y TWENTY MINUTES AFTER ACTIVATION BREAKDOWN IS PROCEEDING AT THE ANIMAL POLE 8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE ! SERIES OF PHOTOMICROGRAPHS OF AN EGG OF THE MEDAKA /RYZIAS LATIPES AT INTERVALS FOLLOWING INSEMINATION
! WAVE OF INTRACELLULAR #A RELEASED BY FERTILIZATION PASSES DOWN THE EGG FROM THE MICROPYLE AT THE LEFT IT IS VISUALIZED BY
THE LUMINENSCENCE OF AEQUORIN MICROINJECTED INTO THE EGG "AR M &ROM 9OSHIMOTO ET AL REPRODUCED WITH
PERMISSION FROM "LACKWELL 0UBLISHING
&IGURE 4HE RELEASE OF CALCIUM FROM INTRACELLULAR STORES PRECEDES THE CORTICAL REACTION IN OOCYTES OF lSH 4HIS SCHEME
SUGGESTS THE INVOLVEMENT OF THE PHOSPHOINOSITIDE CASCADE A COMMON PATHWAY IN MANY CELLS "INDING OF A SPERMATOZOON TO
ITS RECEPTOR 2S LEADS TO THE ACTIVATION OF PHOSPHOLIPASE # 0,# MEDIATED BY A GUANINE NUCLEOTIDE
DEPENDENT REGULATORY
PROTEIN 'P 0,# CATALYSES BREAKDOWN OF PHOSPHATIDYLINOSITOL
BIPHOSPHATE 0)0 INTO DIACYLGLYCEROL $' AND INOSITOL
TRIPHOSPHATE )0 )0 INTERACTS WITH A SPECIlC RECEPTOR 2I ON CYTOPLASMIC CALCIUM STORES WHICH RELEASES #A TO
THE CYTOSOL 4HE CYTOSOLIC #A ACTIVATES 0,# IN TURN FORMING )0 AND $' &ROM )WAMATSU 9OSHIMOTO AND )WAMATSU
B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
#(!04%2
&IGURE %LECTRICAL CHANGES ACCOMPANYING FERTILIZATION AND CORTICAL VESICLE BREAKDOWN IN THE EGG OF THE MEDAKA /RY
ZIAS LATIPES 4HE AVERAGE RESTING POTENTIAL ACROSS THE OOLEMMA OF UNFERTILIZED EGGS IN 2INGERS SOLUTION IS n M6
&OLLOWING FERTILIZATION ARROW THE MEMBRANE DEPOLARIZES OVER A PERIOD OF SEC BY A FEW MILLIVOLTS 4HIS IS FOLLOWED
BY A LONGER PHASE OF HYPERPOLARIZATION ! STEADY RESTING POTENTIAL OF n M6 IS REACHED BY MIN AFTER FERTILIZATION
&ROM .UCCITELLI B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE CORTEX OF EGGS OF THE MEDAKA /RYZIAS LATIPES &ROM
)WAMATSU AND +EINO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! ! CORTICAL ALVEOLUS #! AND ITS CONTENTS INCLUDING A SPHERICAL BODY 3" BEFORE BREAKDOWN -ICROVILLI ARROWS DECORATE
THE OOLEMMA 8
" "Y SECONDS AFTER INSEMINATION ONLY EMPTY POCKETS #!0 OPENING INTO THE PERIVITELLINE SPACE 03 REMAIN FROM
THE CORTICAL ALVEOLI 8
@
&IGURE 3CANNING ! " # AND TRANSMISSION $ % & ELECTRON MICROGRAPHS ILLUSTRATING EXOCYTOSIS OF CORTICAL GRANULES
INDUCED IN EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO BY IMMERSION IN FRESH WATER &ROM 3CHALKOFF AND (ART REPRODUCED
WITH PERMISSION FROM 3PRINGER
6ERLAG
! 4HE SURFACE OF AN EGG ONE MINUTE AFTER ACTIVATION )T DISPLAYS A COMPLEX MOSAIC CONSISTING OF THE ORIGINAL OOLEMMA CORTI
CAL GRANULES IN THE PROCESS OF DISCHARGING THEIR CONTENTS ARROW AND EVACUATED CORTICAL GRANULES REPRESENTED BY PATCHES OF
PERIGRANULAR MEMBRANE 0'- 8
" "Y TWO MINUTES AFTER ACTIVATION THE SURFACE IS DOMINATED BY CRYPTS ARROW AND PATCHES OF MEMBRANE DOUBLE ARROWS
REMAINING FROM CORTICAL GRANULES 8
# 4HE SURFACE AT lVE MINUTES IS ADORNED WITH MICROPLICAE INDICATING THAT THE CORTICAL REACTION IS COMPLETE 8
$ !T ONE MINUTE AFTER ACTIVATION THE CORTEX CONTAINS INTACT MEMBRANE
BOUND CORTICAL GRANULES #' -ICROPLICAE -0
DOMINATE THE SURFACE OF THE OOLEMMA 8
% "Y TWO MINUTES AFTER ACTIVATION EVACUATION OF CORTICAL GRANULE CRYPTS ## HAS OCCURRED 8
& #ORTICAL GRANULES ARE ABSENT FROM THE CORTEX BY lVE MINUTES AFTER ACTIVATION /RGANELLES IN THE CORTICAL OOPLASM INCLUDE
MULTIVESICULAR BODIES -6" LYSOSOMES , AND SMOOTH VESICLES 36 8
#(!04%2
&IGURE $IAGRAMS ILLUSTRATING BREAKDOWN OF THE CORTICAL ALVEOLUS IN THE EGG OF THE MEDAKA /RYZIAS LATIPES "REAKDOWN
BEGINS WITH THE FORMATION OF HOLES AND GAPS B AT THE APEX OF THE CORTICAL ALVEOLUS 4HIS IS FOLLOWED BY THE FORMATION OF A LARGE
APERTURE C INTO THE PERIVITELLINE SPACE 03 AND THE RELEASE D OF COLLOIDAL MATERIAL AND A SPHERICAL BODY 3" !N ELECTRON
DENSE LAYER %$, FORMS BENEATH THE ALVEOLAR POCKET 4HE ENVELOPE SHRINKS E F G AND DISAPPEARS H -ICROVILLI ARE ABUNDANT
ON THE SURFACE OF THE OOLEMMA AND WITHIN THE ALVEOLAR POCKET &ROM )WAMATSU AND +EINO REPRODUCED WITH PERMISSION
FROM "LACKWELL 0UBLISHING
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF AN EGG OF THE MEDAKA /RYZIAS LATIPES SECONDS AFTER INSEMI
NATION *UST BEFORE ITS RELEASE A SPHERICAL BODY PEEPS THROUGH A LARGE APERTURE IN A CORTICAL ALVEOLUS 8 &ROM )WAMATSU
AND +EINO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
&IGURE 3CHEMATIC DRAWINGS SHOWING THE DISTRIBUTION OF COMPACT OOPLASM IN THE CORTICAL LAYER OF THE EGG OF THE
CHUM SALMON /NCORHYNCHUS KETA DURING THE BREAKDOWN OF CORTICAL ALVEOLI )N THE INTACT EGG A A CORTICAL ALVEOLUS #6 AP
PROACHES THE OOLEMMA !S IT APPROACHES B A SMALL AREA OF ITS MEMBRANE BECOMES DECORATED WITH COMPACT OOPLASM #/
!S THE ALVEOLUS OPENS TO THE PERIVITELLINE SPACE C THE ALVEOLAR MEMBRANE WITH THIS COMPACT OOPLASM INCREASES IN AREA
4HE COMPACT OOPLASM UNITES D WITH THE CORTICAL LAYER ARROWHEADS 4HE ALVEOLAR CONTENTS 3" ARE lNALLY DISCHARGED E
&ROM +OBAYASHI A REPRODUCED WITH PERMISSION OF THE &ACULTY OF 3CIENCE (OKKAIDO 5NIVERSITY
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CORTICAL LAYER OF THE ANIMAL POLE LAYER OF THE EGG OF
THE CHUM SALMON /NCORHYNCHUS KETA DURING THE BREAKDOWN OF A CORTICAL ALVEOLUS ! COATING OF DENSE OOPLASM #/ ENVELOPS
THE CORTICAL ALVEOLUS JUST BEFORE EXPULSION OF ITS CONTENTS #) INTO THE PERIVITELLINE SPACE 03 "AR M &ROM +OBAYASHI
A REPRODUCED WITH PERMISSION OF THE &ACULTY OF 3CIENCE (OKKAIDO 5NIVERSITY
&IGURE %LECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS OF ACTIVATED EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO TO ILLUSTRATE
LATER STAGES OF CORTICAL GRANULAR EXOCYTOSIS &ROM (ART AND #OLLINS REPRODUCED WITH PERMISSION FROM 3PRINGER
6ERLAG
! %N FACE VIEW OF A WIDE TRANSIENT CRATER LINED WITH A MEMBRANE OF LOW PARTICLE DENSITY REMAINS ON THE SURFACE OF THE
SITE OF EXPULSION 4HE DIFFERENCE IN PARTICLE DENSITY IS MAINTAINED BETWEEN THE DOMAINS OF THE FORMER CORTICAL VESICLE AND
THE OOLEMMA 8
" 0
FACE REPLICA OF THE SURFACE OF AN EGG MINUTES AFTER ACTIVATION SHOWING DISTINCT MEMBRANE DOMAINS OF HIGH ( AND
LOW , PARTICLE DENSITY 8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF EGGS OF THE MEDAKA /RYZIAS LATIPES SHOWING SHRINKAGE OF THE POCKETS
LEFT FROM THE RELEASE OF THE CONTENTS OF CORTICAL ALVEOLI ,ARGE NUMBERS OF MICROVILLI MV SPROUT WITHIN THE CRATER BEGINNING
NEAR THE APERTURE ! " !N ELECTRON
DENSE LAYER OF OOPLASM ARROWS SURROUNDS THE CRATER ! 8 " 8 # 8
&ROM )WAMATSU AND /HTA REPRODUCED WITH PERMISSION FROM 3PRINGER
6ERLAG
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF THE EGG OF THE ZEBRAlSH "RACHYDANIO RERIO FOLLOWING CORTICAL
ALVEOLAR BREAKDOWN &ROM (ART AND 9U REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !LTHOUGH MOST EVIDENCE OF EXOCYTOSIS HAS DISAPPEARED FROM THE SURFACE TWO MEMBRANE DOMAINS REMAIN DISTINCT THE hPEB
BLEDv SURFACE LEFT FROM THE PERIGRANULAR MEMBRANE IS SURROUNDED BY THE hFOLDEDv MEMBRANE DERIVED FROM THE OOLEMMA
8
" -EMBRANOUS FOLDS OF THE OOLEMMA SURROUND THE PERIGRANULAR MEMBRANE PATCH #- AS IT IS BEING ENVELOPED 8
# 4HE PERIGRANULAR MEMBRANE PATCH IS ALMOST COMPLETELY ENVELOPED BY CONVERGING RADIATING FOLDS OF THE OOLEMMA
8
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF AN EGG OF &UNDULUS HETEROCLITUS AT SECONDS AFTER INSEMINA
TION FOLLOWING THE CORTICAL REACTION 4HREADS OF EXCESS MEMBRANE ARROWS ARE EXPELLED FROM THE EMPTY CRATER OF A CORTICAL
VESICLE 8 &ROM "RUMMETT AND $UMONT REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE )MAGES OF THE EGG CORTEX OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM (ART AND #OLLINS REPRODUCED WITH
PERMISSION FROM 3PRINGER 6ERLAG
! 0ROlLE VIEW OF A FREEZE FRACTURED VACATED CRYPT OF A CORTICAL ALVEOLUS SHOWING ATTACHED COATED VESICLES ARROWHEADS
8
" 4RANSMISSION ELECTRON MICROGRAPH OF A GRAZING SECTION THROUGH A VACATED CRYPT OF A CORTICAL ALVEOLUS SHOWING SEVERAL FORM
ING COATED VESICLES 8
&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH THE CORTEX OF EGGS OF THE ZEBRA DANIO "RACHYDANIO RERIO TO SHOW THE FOR
MATION OF THE PERIVITELLINE SPACE FOLLOWING THE CORTICAL REACTION 8 &ROM (ART AND 9U REPRODUCED WITH PERMISSION
OF *OHN 7ILEY 3ONS )NC
! ! FERTILIZED EGG DURING INITIAL ELEVATION OF THE CHORION # IN THE VICINITY OF THE MICROPYLE -0
" ! FERTILIZED EGG SECONDS AFTER ACTIVATION SHOWING ELEVATION OF THE CHORION AND THE DElNITION OF A PERIVITELLINE SPACE
063 .O EXOCYTOSIS OF CORTICAL GRANULES IS VISIBLE
# ! FERTILIZED EGG SECONDS AFTER ACTIVATION -ANY CORTICAL GRANULES APPEAR AS BLISTER
LIKE ELEVATIONS AT THE SURFACE OF
THE EGG
$ % %GGS TWO TO THREE MINUTES AFTER ACTIVATION SHOWING INTENSE EXOCYTOSIS OF CORTICAL GRANULES AT THE SURFACE .EWLY RELEASED
CENTRAL CORES ARROW BECOME HYDRATED AND TRANSFORMED INTO PERIVITELLINE GLOBULES 0'
#(!04%2
&IGURE #ONTINUED
& ! FERTILIZED EGG SIX TO SEVEN MINUTES AFTER ACTIVATION 4HE DISCHARGED MATERIAL FROM THE CORTICAL GRANULES TOGETHER WITH
THE PERIVITELLINE GLOBULES 0' FORMS A COLLOID
LIKE HYALINE LAYER AROUND THE EGG
&IGURE 4HIS DIAGRAM SHOWS THE DEVELOPMENT OF THE PERIVITELLINE SPACE IN THE EGG OF THE MEDAKA /RYZIAS LATIPES
AS A RESULT OF THE CORTICAL REACTION &ROM )WAMATSU AND /HTA REPRODUCED WITH PERMISSION FROM 3PRINGER
6ERLAG
"REAKDOWN OF CORTICAL ALVEOLI #! BEGINS WITH THE FORMATION OF A LARGE APERTURE INTO THE PERIVITELLINE SPACE 03 AND THE RELEASE
OF COLLOIDAL MATERIAL AND SPHERICAL BODIES 3" 4HE ALVEOLAR ENVELOPE THEN SHRINKS AS ITS SMOOTH SURFACE BECOMES COVERED
BY MANY MICROVILLI %LEVATION OF THE CHORION IS ACCOMPANIED BY A REDUCTION IN THICKNESS OF THE CHORION #( AND THE LAYER OF
CYTOPLASM #94 BETWEEN THE YOLK AND OOLEMMA / OIL DROPLET
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE ! SCANNING ELECTRON MICROGRAPH OF THE INSIDE OF THE CHORION REMOVED FROM AN EGG OF &UNDULUS HETEROCLITUS
lXED THREE SECONDS AFTER INSEMINATION $ENSE GRANULES AND PARTICULATE MATERIAL PRESUMABLY RELEASED BY CORTICAL ALVEOLI ADHERE
TO THE INNER SURFACE 8 &ROM "RUMMETT AND $UMONT REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE CHORION OF THE CARP #YPRINUS CARPIO &ROM +UDO
REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! !T THE TIME OF FERTILIZATION THE CHORION IS PERFORATED BY PORE CANALS AND CONSISTS OF FOUR LAYERS AND 4HE PERIVITEL
LINE SPACE IS SEEN AT THE BOTTOM OF THE MICROGRAPH 8
" !T THIS TIME THE lRST LAYER OF THE CHORION CONSISTS OF AN INNER ELECTRON
DENSE REGION AND AN OUTER ELECTRON
LUCENT PORTION
THAT IS FORMED FROM MATERIAL OOZING THROUGH THE PORE CANALS ! COLUMNAR BARRIER #/ CONSTRICTS THE PORE CANAL PROVIDING
AN ANCHOR POINT FOR THE OUTER LAYER 8
# !FTER MINUTES THE lLAMENTOUS OUTER LAYER OF THE CHORION HAS INCREASED IN THICKNESS BY lVE FOLD 8
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF THE CHORION OF EGGS OF THE AYU lSH 0LECOGLOSSUS ALTIVELIS
&ROM +UDO AND )NOUE REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !T THE TIME OF FERTILIZATION THE SURFACE IS COVERED WITH A FAIRLY UNIFORM MESHWORK OF lLAMENTOUS MATERIAL EXTENDING IN ALL
DIRECTIONS 8
" 3OME TIME LATER THE lLAMENTS HAVE AGGREGATED INTO REGULARLY SPACED ROUND MASSES 8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 3CANNING ELECTRON MICROGRAPHS OF CHORIONS OF FERTILIZED EGGS &ROM $AVENPORT ,NNING AND +JRSVIK
REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 4HE HARD CHORION OF THE DEMERSAL EGG OF THE LUMPSUCKER #YCLOPTERUS LUMPUS FOUR HOURS AFTER FERTILIZATION 4HE CHORION IS
REINFORCED WHEN ITS PORES BECOME PLUGGED AFTER ACTIVATION 4HESE EGGS MUST WITHSTAND CONTACT WITH THE SEA BOTTOM
" 4HE BROKEN EDGE AND SURFACE OF THE SOFT CHORION IN THE VEGETAL REGION OF THE DEMERSAL EGG OF THE CAPELIN -ALLOTUS VILLOSUS
THREE DAYS AFTER FERTILIZATION 4HE REGULAR PATTERN OF PORE CANALS OF THE UNFERTILIZED EGG IS RETAINED !LTHOUGH THE CHORION
REMAINS SOFT AND PLIABLE DURING DEVELOPMENT IT RESISTS THE SHRINKAGE AND SWELLING CAUSED BY SEVERE CHANGES IN TEMPERATURE
OF THE INTERTIDAL REGION )T WITHSTANDS HOWEVER THE BURSTING STRESSES OF WAVE ACTION
&IGURE $IAGRAM SHOWING THE SEQUENCE OF EVENTS IN FERTILIZATION OF THE EGG OF THE MEDAKA /RYZIAS LATIPES &ROM
)WAMATSU ET AL REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING 4HE TIME FROM INSEMINATION TO SPERM ATTACH
MENT THROUGH THE MICROPYLE DEPENDS ON THE CONCENTRATION OF SPERM SURROUNDING THE EGG
!BBREVIATIONS #A CORTICAL ALVEOLUS #H CHORION
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE INNER OPENING OF THE MICROPYLE IN THE EGG OF &UNDULUS HETEROCLITUS &ROM
"RUMMETT AND $UMONT REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC 4HE DIAMETER OF THE CANAL PRECLUDES
THE ADMISSION OF MORE THAN THE SINGLE SPERM WHICH CAN BE SEEN ABOUT TO EMERGE 8
&IGURE 0HOTOMICROGRAPHS BY PHASE CONTRAST OF A LIVING EGG OF THE MEDAKA /RYZIAS LATIPES SHOWING CHANGES IN THE
MICROPYLE FOLLOWING INSEMINATION AT # !RROWS INDICATE SPERMATOZOA 8 &ROM )WAMATSU )SHIJIMA AND .AKASHIMA
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! "EFORE INSEMINATION
" SECONDS AFTER ATTACHMENT OF SPERM TO THE OOLEMMA #ONTRACTION ARROWHEADS OF THE INNER LAYER OF THE CHORION FOLLOWING
DISCHARGE OF THE ALVEOLAR CONTENTS RESULTS IN THE CLOSURE OF THE INNER THIRD OF THE MICROPYLAR CANAL
# SECONDS
$ SECONDS
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE 0HOTOMICROGRAPHS OF THE MICROPYLE IN A LIVING EGG OF THE CHUM SALMON /NCORHYNCHUS KETA "AR M
&ROM +OBAYASHI AND 9AMAMOTO REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE UNFERTILIZED EGG 4HE MICROPYLE IS INDICATED BY AN ARROW
" )MMEDIATELY AFTER INSEMINATION
# 3EVEN MINUTES AFTER INSEMINATION SHOWING THE DISCHARGE OF SUPERNUMERARY SPERMATOZOA 33 FROM THE MICROPYLAR CANAL
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR APERTURE IN EGGS OF THE MEDAKA /RYZIAS LATIPES BEFORE AND
AFTER INSEMINATION &ROM )WAMATSU ET AL REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! 4HE ARROW INDICATES THE MICROPYLE OF AN UNFERTILIZED EGG "AR M
" 4HIS MICROPYLE IS SHOWN AT A HIGHER MAGNIlCATION "AR M
# $ 6ITELLINE mUID HAS EXUDED FROM THE MICROPYLE BY SECONDS AFTER SPERM ATTACH TO THE EGG "AR M
#(!04%2
&IGURE %LECTRON MICROGRAPH OF A SECTION THROUGH THE MICROPYLAR CANAL OF AN EGG OF THE CHUM SALMON /NCORHYNCHUS
KETA SECONDS AFTER ACTIVATION 4HE LUMEN OF THE CANAL IS lLLED WITH AMORPHOUS MATERIAL BLOCKING PASSAGE OF A SUPERNUMER
ARY SPERMATOZOON 3 "AR M &ROM +OBAYASHI AND 9AMAMOTO REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE MICROPYLES OF INSEMINATED EGGS OF THE COMMON CARP
#YPRINUS CARPIO &ROM +UDO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
! 4HE FERTILIZATION CONE HAS GROWN AS FAR AS THE MICROPYLAR VESTIBULE AND PLUGS THE MICROPYLAR CANAL ! SPERM HEAD IS
EMBEDDED AT THE BASE OF THE FERTILIZATION CONE ITS TAIL LIES ALONGSIDE THE CONE 8
" 4HREE SECTIONS OF A SINGLE FERTILIZATION CONE CONTAINING THE lRST SPERM NUCLEUS 3. 3EVERAL SPERMATOZOA DENIED ACCESS BY
THE FERTILIZATION CONE ARE CLUSTERED IN THE MICROPYLAR CANAL 8
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
&IGURE %LECTRON MICROGRAPHS SHOWING THE FERTILIZATION CONES OF EGGS OF &UNDULUS HETEROCLITUS lXED THREE MINUTES AFTER
INSEMINATION 4HE CHORION WAS REMOVED FROM lXED EGGS &ROM "RUMMETT $UMONT AND 2ICHTER REPRODUCED WITH
PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE DElNITIVE FERTILIZATION CONE 3EVERAL DARK STAINING VESICLES
ARE SEEN IN THE CYTOPLASM OF THE CONE ESPECIALLY NEAR ITS SURFACE ARROWHEAD ! PORTION OF A SPERM TAIL PROTRUDES FROM
THE SURFACE OF THE CONE ARROW 8
)NSET !NOTHER SECTION OF THIS CONE SHOWING PORTION OF THE SPERM TAIL WITHIN THE OOPLASM 8
" 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF THE EGG SHOWING A SPERM TAIL PROTRUDING FROM A FERTILIZATION CONE
4HE SURFACE OF THE CONE IS RELATIVELY SMOOTH COMPARED TO THE SURFACE OF THE EGG IMMEDIATELY SURROUNDING IT 8
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF INSEMINATED EGGS OF THE PADDLElSH 0OLYODON SPATHULA ONE
MINUTE AFTER FERTILIZATION 4HE PADDLElSH PRODUCES AN EGG WITH MULTIPLE MICROPYLES &ROM ,INHART AND +UDO REPRODUCED
WITH PERMISSION FROM %LSEVIER 3CIENCE
! 4HE BALL
SHAPED END OF A FULLY DEVELOPED FERTILIZATION CONE EXTENDS FROM THE EXTERNAL APERTURE OF A MICROPYLE 8
" /NE OF THE MICROPYLAR CANALS IN THE MICROPYLAR AREA OF THE CHORION IS SEALED WITH A FULLY GROWN CONE LARGE ARROW THE OTHERS
ARROWHEADS APPEAR TO BE BLOCKED TO VARIOUS DEGREES WITH OTHER MATERIALS PROBABLY EXUDATES FROM THE CORTICAL ALVEOLI
! SPERM TAIL EXTENDS FROM A PORE OF ONE OF THE MICROPYLAR CANALS SMALL ARROW 8
#(!04%2
/6)$5#43 !.$ /6)0!2)49
/VIDUCTS
TORY NOR STEROIDOGENIC 3MALL CLUSTERS OF -)#2/6),,/53
#%,,3 SIMILAR TO THOSE LINING THE OVARIAN CAVITY SEE
PAGE ARE ALSO FOUND IN THE EPITHELIUM LINING THE
OVIDUCT OF THE BLEAK &IGURE 7ITHIN THE OVARIAN
LUMEN THEY SECRETE COMPONENTS OF THE OVARIAN mUID
WHICH MAINTAIN ITS IONIC GRADIENT THEREBY PREVENT
ING ACTIVATION OF THE EGGS CLOSURE OF THE MICROPYLE
SWELLING OF THE EGGS AND SHELL HARDENING 0RESUMABLY
THEY CONTINUE THIS FUNCTION IN THE OVIDUCT AND CONTRIB
UTE THEIR SECRETIONS TO THE OVARIAN mUID 4ABLE RE
CORDS ANALYSIS OF THE COMPOSITION OF THE OVARIAN mUID
IN THE BLEAK
4HE PERITONEAL OVIDUCTS OF VIVIPAROUS TELEOSTS ARE
INADEQUATE TO THE TASK OF SHELTERING AND NOURISHING
DEVELOPING EMBRYOS AND THESE DUTIES ARE CARRIED OUT
PERFORCE BY THE OVARY ITSELF
6IABLE SPERM ARE STORED FOR PERIODS UP TO SEVERAL
MONTHS WITHIN THE OVARY AND OVIDUCT OF THE OVIPA
ROUS POECILIID PLATYlSH 8IPHOPHORUS MACULATUS
4HE OVIDUCT OR '/./$5#4 IS A CONVOLUTED POSTERIOR
EXTENSION OF THE PERITONEUM COVERING THIS CYSTOVARIAN
OVARY IT IS LINED BY SIMPLE TO PSEUDOSTRATIlED MESO
THELIUM DERIVED FROM THE LINING OF THE LUMEN &IGURE
! 0OTTER AND +RAMER ,YING BETWEEN THE
TWO MESOTHELIAL LAYERS ARE THE TYPICAL LOOSE VASCULAR
CONNECTIVE TISSUE AND SCATTERED SMOOTH MUSCLE CELLS
THAT UNDERLIE ALL PERITONEUM &IGURE " 4HE DUCT
EXTENDS POSTERIORLY TO EXIT AT A UROGENITAL OPENING
ASSOCIATED WITH A PAPILLA JUST POSTERIOR TO THE ANUS
!N ELABORATE ARRAY OF SURFACE MODIlCATIONS DECORATE
THE MESOTHELIAL CELLS OF THE LINING SCALLOPS LOBULAR
EXTENSIONS MICROVILLI AND MICROVILLOUS APPENDAGES
AND DEEP INTRACELLULAR PITS AND POCKETS &IGURE
4HE SPERM BECOME ASSOCIATED WITH SPECIAL EPITHE
LIAL CELLS 30%2-
!33/#)!4%$ #%,,3 THAT LACK EXTENSIVE
SURFACE MICROVILLI BUT CONTAIN AN ARRAY OF DEEP SUR
/VIDUCTS OF MANY VERTEBRATES ARE DERIVED FROM THE
-LLERIAN DUCT %GGS RELEASED INTO THE COELOM AT OVU
LATION ARE GATHERED UP BY A FUNNEL AT THE END OF THE
OVIDUCT AND CONVEYED TO THE OUTSIDE %N ROUTE THE OVI
DUCT OFTEN PROVIDES A PROTECTIVE COATING AND IN SOME
VIVIPAROUS SPECIES IT BECOMES A HAVEN FOR DEVELOP
ING EMBRYOS )N THE !'.!4(! HOWEVER NO OVIDUCTS
DEVELOP AND EGGS ARE SHED DIRECTLY INTO THE COELOM
ESCAPING FROM THE BODY VIA GENTIAL PORES THAT PERFORATE
THE BODY WALL JUST BEFORE SPAWNING !NY PROTECTIVE
COATING ON THESE EGGS THEREFORE MUST BE PROVIDED BY
THE OVARY BEFORE OVULATION
4HE SO CALLED OVIDUCTS OF 4%,%/343 ARE NOT DERIVED
FROM -LLERIAN DUCTS BUT IN MOST SPECIES ARE FORMED
FROM THE PERITONEAL FOLDS THAT ENCLOSE THE OVARY (EN
DERSON 4HESE MEMBRANOUS ENVELOPES EXTEND
POSTERIORLY GUIDING THE MATURE EGGS TO A SINGLE MEDI
AN GENITAL PORE THAT OPENS AT THE TIME OF REPRODUCTION
BETWEEN THE ANUS AND URINARY PAPILLA 4HIS ARRANGE
MENT HAS AN ADVANTAGE IN ANIMALS WHERE THE ENORMOUS
NUMBERS OF EGGS PRODUCED COULD CHOKE THE COELOM
)N SALMONIDS HOWEVER THE OVA ARE DISCHARGED DIRECTLY
INTO THE COELOM AND PASS THROUGH A CONSTRICTION IN THE
POSTERIOR ABDOMINAL WALL INTO THE GENITAL CAVITY THEY
LEAVE THE BODY BY WAY OF AN ORIlCE IN THE URINOGENITAL
PAPILLA &IGURE
! SIMPLE COLUMNAR EPITHELIUM LINES BOTH THE OVAR
IAN CAVITY AND THE OVIDUCT OF THE BLEAK !LBURNUS AL
BURNUS ,AHNSTEINER 7EISMANN AND 0ATZNER
#),)!4%$ #%,,3 INTERCONNECTED BY JUNCTIONAL COM
PLEXES CONSTITUTE MOST OF THE EPITHELIUM OF THE OVI
DUCT &IGURE AND ASSIST IN THE TRANSPORT OF EGGS
"ELOW THE CILIARY ROOTLETS OF THESE EPITHELIAL CELLS THE
CYTOPLASM CONTAINS ABUNDANT TUBULAR GRANULAR ENDO
PLASMIC RETICULUM MITOCHONDRIA AND A NUCLEUS WITH
A SINGLE NUCLEOLUS 4HE CYTOPLASM ALSO CONTAINS COATED
VESICLES NUMEROUS RIBOSOMES AND SOME LIPID VACU
OLES THE ABSENCE OF A 'OLGI COMPLEX AND SECRETORY
VESICLES INDICATES THAT THESE CELLS ARE NEITHER SECRE
3IMILAR VALUES FOR FOUR SPECIES OF SALMONIDS ARE RECORDED IN
AN EARLIER PAPER BY THESE AUTHORS ,AHNSTEINER 7EISMANN AND
0ATZNER
#(!04%2
FACE PITS AND POCKETS 4HE CYTOPLASM OF THESE CELLS
IS MODERATELY ELECTRON DENSE AND CONTAINS AN ABUN
DANCE OF FREE RIBOSOMES AS WELL AS A FEW MITOCHONDRIA
AND SMALL VESICLES ENDOPLASMIC RETICULUM IS SPARSE
-ICROTUBULES INTERMEDIATE lLAMENTS AND MICROlLA
MENTS CONSTITUTE THE CYTOSKELETON OF THE SPERM ASSO
CIATED CELLS THE MICROTUBULES REINFORCE INTERCELLULAR
JUNCTIONS AND THE MICROlLAMENTS SUPPORT THE MICRO
VILLOUS EXTENSIONS OF THE SURFACE 4HE SPERM LIE EITHER
WITHIN THE INVAGINATIONS OR ARE TAKEN UP AND INCORPO
RATED WITHIN THE CYTOPLASM OF THESE CELLS &IGURES $
AND )NTACT SPERM NUCLEI NECK MITOCHONDRIA AND
mAGELLA CAN BE SEEN WITHIN THE PITS AND POCKETS WHILE
SPERM NUCLEI WITHOUT mAGELLA OR OTHER ORGANELLES OC
CUR DEEP WITHIN THE CYTOPLASM OF THE SPERM ASSOCIATED
CELLS 4HERE IS NO INDICATION OF LYSOSOMAL ACTIVITY OR
SPERM BREAKDOWN 2EJECTION OF SPERM BY THE IMMUNE
SYSTEM OF THE FEMALE IS PROBABLY AVERTED BY THE BARRIER
PROVIDED BY APICAL JUNCTIONAL COMPLEXES BETWEEN THE
EPITHELIAL CELLS &IGURE
4HE OVIDUCTS OF #(/.$2)#(4(9%3 ARE DERIVED FROM
-LLERIAN DUCTS AND DEMONSTRATE MANY HOMOLOGIES TO
THE OVIDUCTS OF OTHER VERTEBRATES &IGURE !T OVU
LATION EGGS ARE CAST INTO THE COELOM FROM THE OVARY
AND SWEPT INTO A CILIATED FUNNEL THE /34)5- AT THE UP
PER END OF THE OVIDUCT TO BEGIN THEIR JOURNEY TO THE
EXTERIOR &ERTILIZATION IS INTERNAL IN ELASMOBRANCHS
SPERM RECEIVED IN THE CLOACA DURING COPULATION MAKE
THEIR WAY TO THE UPPER REACHES OF THE OVIDUCT AND
FERTILIZE THE EGGS /FTEN THE SPERM ARE STORED WITHIN
THE OVIDUCT FOR LONG PERIODS OF TIME BEFORE FERTILIZA
TION OCCURS &IGURE 0RATT )F THE SPERM
ARE CONTAINED WITHIN A 30%2-!4/0(/2% THE OVIDUCT SE
CRETES ENZYMES THAT BREAK DOWN THIS PACKAGE TO FREE
THE SPERM CONTAINED WITHIN 4HE OVIDUCTS OF OVIPAROUS
FORMS SECRETE JELLY COATS AND TOUGH COLLAGENOUS EGG
CAPSULES THAT PROTECT DEVELOPING EGGS FROM PREDATORS
AND OTHER RIGOURS OF THE OUTSIDE WORLD !N EGG CAPSULE
USUALLY CONTAINS ONLY ONE EGG BUT IN SOME CASES THREE
OR FOUR EGGS MAY BE PRESENT )N VIVIPAROUS FORMS
THE OVIDUCTS MAY BE ENLARGED INTO UTERI WHICH PROVIDE
A HOSPITABLE ENVIRONMENT FOR GESTATION OFTEN OF SEVER
AL MONTHS DURATION OXYGEN MUST BE SUPPLIED DURING
THIS PERIOD AND WASTES MUST BE REMOVED NUTRIENTS ARE
OFTEN PROVIDED FROM THE MOTHERS CIRCULATION
4HE BASIC PLAN OF THIS REMARKABLE OVIDUCT IS SIMILAR
THROUGHOUT THE ELASMOBRANCHS )T IS LINED WITH A HIGHLY
VARIABLE 45.)#! -5#/3! WHOSE EPITHELIUM REmECTS THE
FUNCTION OF THE REGION &IGURE )N GLANDULAR RE
GIONS THE EPITHELIUM IS INVAGINATED TO FORM A THICK
LAYER OF TUBULAR GLANDS THAT POUR THEIR SECRETIONS AT
THE BASES OF BLUNT FOLDS THAT ARE COVERED WITH CILIATED
STRATIlED CUBOIDAL EPITHELIUM %LSEWHERE THE EPITHE
LIUM FORMS ROUNDED FOLDS THAT MAY BE COVERED WITH
STRATIlED SQUAMOUS TO CUBOIDAL EPITHELIUM WHICH MAY
OR MAY NOT BEAR CILIA 4HE TUNICA MUCOSA IS SUBTENDED
BY A RICHLY VASCULAR 4%,! 35"-5#/3! OF LOOSE lBROUS
CONNECTIVE TISSUE THAT MAY CONTAIN A FEW SCATTERED
SMOOTH MUSCLE lBRES 4HIS LAYER MERGES IMPERCEPTI
BLY INTO THE SMOOTH MUSCLE OF THE 45.)#! -53#5,!2)3
WHICH CONSISTS OF A LOOSE INNER LAYER OF CIRCULAR lBRES
AND A DENSER OUTER LAYER OF LONGITUDINAL lBRES 4HE
OVIDUCT IS ENCLOSED BY A 45.)#! 3%2/3! OF LOOSE lBROUS
CONNECTIVE TISSUE COVERED BY SIMPLE SQUAMOUS OR CU
BOIDAL MESOTHELIAL CELLS
4HE OVIDUCT OF #HONDRICHTHYES MAY BE DIVIDED
INTO SEVERAL FUNCTIONAL REGIONS OSTIUM OVIDUCT OVI
DUCTAL NIDAMENTAL GLAND ISTHMUS UTERUS AND CERVIX
&IGURES AND 3TANLEY +OOB
AND #ALLARD (AMLETT ET AL B (AMLETT AND
+OOB )N NEARLY ALL ELASMOBRANCHS REGARDLESS OF
REPRODUCTIVE MODE OVULATED EGGS ARE INITIALLY ENCAP
SULATED IN A SHELL PRODUCED BY A SPECIALIZED GLAND THAT
IS UNIQUE AMONG VERTEBRATES THE .)$!-%.4!, ',!.$
3(%,, ',!.$ OR /6)$5#4!, ',!.$ +OOB AND #ALLARD
)N OVIPAROUS SPECIES THE EGG IS OVIPOSITED SOON
AFTER FORMATION AND DEVELOPMENT OCCURS ENTIRELY WITH
IN THE CAPSULE AT HATCHING THE YOUNG HAVE INTERNALIZED
ALL THEIR YOLK AND ARE FULLY DEVELOPED )N MANY VIVIPA
ROUS SPECIES THE EGG CAPSULE FUNCTIONS TRANSIENTLY DUR
ING THE INITIAL STAGES OF DEVELOPMENT AND EMBRYOS MAY
EMERGE FROM IT TO COMPLETE DEVELOPMENT WITHIN THE
mUIDS OF THE UTERUS )N SOME LIVE BEARING SPECIES HOW
EVER THE EGG CAPSULE REMAINS INTACT THROUGHOUT GESTA
TION AND BECOMES INTEGRATED INTO A PLACENTA
,ITTLE HAS BEEN WRITTEN ABOUT THE OSTIUM AND UPPER
REACHES OF THE OVIDUCT OF ELASMOBRANCHS 4HESE ARE
COMMON OVIDUCTAL STRUCTURES IN MOST VERTEBRATES AND
PRESUMABLY FUNCTION SIMILARLY IN ALL ELASMOBRANCHS
TO TRANSPORT OVULATED EGGS BY MEANS OF CILIARY CUR
RENTS (AMLETT AND +OOB ,ONGIDTUDINAL FOLDS
COVERED WITH A SIMPLE COLUMNAR CILIATED EPITHELIUM
PROTRUDE INTO THE LUMEN OF THE ANTERIOR OVIDUCT OF
THE !TLANTIC GUITARlSH 2HINOBATOS LENTIGINOSUS BAS
AL BODIES OF THE CILIARY ROOTLETS FORM A DISTINCT LINE
3INCE THE GLAND DOES NOT ALWAYS PRODUCE A SHELL AND SINCE NO
hNIDUSv OR NEST IS PRODUCED IN SOME SPECIES OF ELASMOBRANCHS
(AMLETT ET AL A RECOMMEND THAT THE TERM hOVIDUCAL GLANDv
BE USED TO DESCRIBE THIS STRUCTURE
/6)$5#43 !.$ /6)0!2)49
LINE EXTENDING ACROSS THE APICAL REGIONS OF THE CELLS
&IGURE (AMLETT ET AL B 3ECRETORY CELLS
LOCATED BETWEEN ADJACENT FOLDS AND IN SMALLER NUM
BERS AMONG THE CILIATED CELLS OF THE SURFACE PROBABLY
PROVIDE A LUBRICANT THAT ASSISTS THE CILIA IN MOVING
OVULATED EGGS INTO THE OVIDUCTAL GLAND 4HE CONNECTIVE
TISSUE STROMA OF THE FOLDS IS POORLY VASCULARIZED 4HERE
IS NO SMOOTH MUSCLE IN THIS REGION
$EVELOPMENT STRUCTURE AND ACTIVITY OF THE OTHER
REGIONS OF THE FEMALE REPRODUCTIVE TRACT OF ELASMO
BRANCHS VARY WITH THE REPRODUCTIVE MODE 4HE OVI
DUCTAL GLAND IS THE PREDOMINANT ORGAN IN THE OVIDUCT
OF OVIPAROUS FORMS &IGURES AND AND THE
UTERUS IS RELATIVELY INCONSPICUOUS SIMPLY PROVIDING
A CONDUIT FOR THE LARGE EGG CAPSULE 4HE SITUATION IS
REVERSED HOWEVER IN VIVIPAROUS SPECIES AND THE OVI
DUCTAL GLAND PLAYS A RELATIVELY MINOR ROLE SOMETIMES
ENCAPSULATING THE EGGS IN DIAPHANOUS MEMBRANES
WHILE THE UTERUS OFTEN MANIFESTS VARIOUS TYPES OF STRUC
TURAL MODIlCATIONS AS IT ENVELOPS THE EMBRYOS DURING
THEIR DEVELOPMENT TO TERM )N SOME SPECIES ELABORATE
RICHLY VASCULAR EXTENSIONS OF THE UTERINE WALL THE 42/
0(/4!%.)!% SERVE TO NOURISH THE DEVELOPING YOUNG
)N AT LEAST TWO LIVE BEARING SPECIES A SHORT SEG
MENT OF THE OVIDUCT THE )34(-53 CONNECTS THE OVI
DUCTAL GLAND WITH THE UTERUS +OOB AND #ALLARD
#ALLARD AND +OOB (AMLETT AND +OOB
)N 3QUALUS ACANTHIAS THE ISTHMUS COILS BEFORE ENTER
ING THE UTERUS FORMING A STRICTURE THAT IS POSTULATED TO
BE A CLOSING MECHANISM 6ERSCHLUVORRICHTUNG THAT
PREVENTS THE BACKmOW OF URINE AND SEAWATER INTO THE
COELOM BUT BECOMES COMPLIANT AND EXTENSIBLE WHEN
EGGS ARE BEING TRANSPORTED TO THE UTERUS &IGURE
7IDAKOWICH CITED BY #ALLARD AND +OOB
(OW THE ISTHMUS FUNCTIONS IS NOT KNOWN
4HE OVIDUCTS OF BOTH EGG LAYING AND LIVE BEARING
ELASMOBRANCHS ENTER THE COMMON UROGENITAL SINUS BY
WAY OF A CONSTRICTED #%26)8 +OOB AND #ALLARD
4HE CERVIX CLOSES THE UTERUS OF OVIPAROUS SPECIES PRE
VENTING THE PREMATURE ENTRY OF THE FORMING EGG CAP
SULE INTO THE UROGENITAL SINUS )N LIVE BEARING FORMS
IT PRESENTS THE lNAL BARRIER THROUGH WHICH THE FOETUSES
EMERGE AT PARTURITION )T MUST BE CAPABLE OF CHANGING
SIZE OR PROPERTIES AT DIFFERENT TIMES DURING THE REPRO
DUCTIVE CYCLE IN ORDER TO ACCOMMODATE THE PASSAGE
OF EGGS OR TERM FOETUSES 4HE COMMON 52/'%.)4!,
3).53 IN ADULT FEMALE OVIPAROUS ELASMOBRANCHS IS AN
ENLARGED SAC INTO WHICH THE OVIDUCTS ENTER SEPARATELY
IT MAY HOUSE THE EGG CAPSULE FOR SEVERAL HOURS BEFORE
OVIPOSITION
/VIDUCTAL 'LAND AND %GG #APSULE
)N GENERAL OVIPAROUS CHONDRICHTHYES PRODUCE TWO
KINDS OF EGG CAPSULES &IGURE 4HE CAPSULE OF
THE DOGlSH 3CYLIORHINUS FOR EXAMPLE IS RECTANGULAR
WITH TENDRILS EXTENDING FROM EACH CORNER THE FAMILIAR
hMERMAIDS PURSEv OF THE SEACOAST 4HE SECOND TYPE
IS SEEN IN THE 0ORT *ACKSON SHARK (ETERODONTUS AND
IS HELICAL WITH LONG COILED lLAMENTOUS TENDRILS EX
TENDING FROM THE APEX 4HE TENDRILS ANCHOR THE EGG IN
POSITION BY COILING AROUND UPRIGHT MASSES OF SEAWEED
&IGURE ! MUCH SIMPLER CAPSULE ENCLOSES THE
EGGS OF VIVIPAROUS SPECIES &OR EXAMPLE IN THE SPINY
DOGlSH 3QUALUS ACANTHIAS A CLEAR AMBER CAPSULE
SURROUNDS SEVERAL DEVELOPING EGGS WITHIN THE UTERUS
4HIS SHELL BREAKS DOWN ABOUT THE TIME OF ABSORPTION
OF THE EXTERNAL GILLS AND THE EMBRYOS mOAT FREELY IN THE
UTERINE mUID -OST STUDIES HAVE BEEN CARRIED OUT ON
THE ELABORATE EGG CAPSULE OF AN OVIPAROUS SPECIES THE
DOGlSH 3CYLIORHINUS CANICULA
4HE OVUM OF 3CYLIORHINUS CANICULA IS ABOUT MM
IN DIAMETER WHEN SPHERICAL AND IS PROTECTED BY A TOUGH
ROUGHLY RECTANGULAR CAPSULE ABOUT X MM CON
SISTING OF TWO CONVEX WALLS lRMLY SEALED AT ALL FOUR
EDGES &IGURES AND 2USAOUN )NNOCENT
A +NIGHT AND &ENG 4WO LATERAL RIDGES THAT
FORM ALONG THE SUTURE ARE PROLONGED INTO LONG TAPER
ING TENTACLES 4HE POSTERIOR MARGIN OF THE CAPSULE THE
PART EXTRUDED lRST IS DEEPLY INCURVED AND FORMS A SEAL
SIMILAR TO A CRIMPED WELD &IGURE 4HE ANTERIOR
BORDER IS STRAIGHT AND IS JOINED BY A SOPHISTICATED SEAL
WHICH SEPARATES TO PERMIT HATCHING WHEN DEVELOPMENT
OF THE EMBRYO IS COMPLETE
4WO CAPSULES ARE PRODUCED SIMULTANEOUSLY WITHIN
THE TWO OVIDUCTAL GLANDS OF 3CYLIORHINUS CANICULA AT
A MAXIMUM RATE OF TWO EVERY HOURS DURING A PRO
TRACTED BREEDING SEASON +OOB AND #ALLARD
+NIGHT AND &ENG &ORMATION OF THE CAPSULE BE
GINS BEFORE OVULATION SO THAT THE CAPSULE IS ONE THIRD
TO ONE HALF FORMED BEFORE THE EGG ENTERS THE LUMEN OF
THE OVIDUCTAL GLAND &IGURE 4HE CAPSULE PRO
TECTS THE EMBRYO FROM PREDATION MECHANICAL INJURY
FOULING AND INFECTION THROUGHOUT AN EXTENDED PERIOD
OF DEVELOPMENT OF AT LEAST lVE MONTHS )TS WALL IS EX
TREMELY TOUGH AND RESISTANT TO CHEMICAL AND ENZYMIC
ATTACK THOUGH FREELY PERMEABLE TO SMALL MOLECULES AND
IONS +NIGHT AND &ENG A &ENG AND +NIGHT
4HIS ENVELOPE IS RESISTANT TO BURSTING AND IS
lLLED WITH A VISCOUS JELLY LIKE MATERIAL THAT FUNCTIONS
AS AN EFlCIENT SHOCK ABSORBER
#(!04%2
4HE CAPSULE WALL IS A COMPOSITE MATERIAL CONSTRUCT
ED LARGELY OF COLLAGEN lBRILS WITH A HIGHLY ORDERED
KINKED MOLECULAR ARRANGEMENT SET IN A MATRIX CONTAIN
ING SPHERICAL lLLER PARTICLES M IN DIAMETER COM
POSED OF HYDROPHOBIC PROTEINS WITH AN EXCEPTIONALLY
HIGH TYROSINE CONTENT &IGURE +NIGHT AND (UNT
2USAOUN ET AL 2USAOUN
)NNOCENT A +NIGHT AND &ENG A &ENG
AND +NIGHT +NIGHT &ENG AND 3TEWART
4HE WALL IS MADE UP OF FOUR LAYERS , ON THE OUTSIDE
THEN , AND , AND ON THE INSIDE , &IGURE
4HE OUTER LAYER , IS ABOUT M THICK IN DEHYDRAT
ED TANNED SPECIMENS IT CONSISTS OF lNE lBRILS ABOVE
DENSELY PACKED AMORPHOUS GRANULES RICH IN TYROSINE
&IGURE ,AYER , IS ABOUT M THICK AND CON
STITUTES THE BULK OF THE CAPSULE WALL IT IS SIMILAR TO
PLYWOOD AND CONSISTS OF ABOUT SHEET
LIKE ,!-%,,!%
HELD TOGETHER WITH A PHENOLIC RESIN 4HE OUTER LAMELLAE
ARE BETTER ORDERED THAN THE INNER ONES AND EACH LAMELLA
APPEARS TO CONSIST OF lVE ,!-).!% %ACH LAMINA CON
TAINS PARALLEL COLLAGEN
CONTAINING lBRILS THAT SHOW A
PERIODICITY OF ABOUT NM &IGURE +NIGHT AND
(UNT 2USAOUN
)NNOCENT B +NIGHT AND
&ENG B 4HE LAMINAE ARE STACKED WITH AN ANGLE
OF BETWEEN lBRILS IN SUCCESSIVE LAMINAE TO GIVE
AN ORTHOGONAL ARRANGEMENT &IGURE !LTHOUGH
lNELY STRIATED , APPEARS MORE HOMOGENEOUS THAN THE
OTHER LAYERS AND IS ABOUT M THICK ITS STRIATIONS ARE
ORTHOGONAL TO THE LAMINAE OF , 4HE INNER LAYER ,
IS ONLY TO M THICK AND WITH THE LIGHT MICROSCOPE
APPEARS HOMOGENEOUS
4HE LAYERS OF THE SELACHIAN CAPSULE AS WELL AS
THE TENDRILS AND JELLY ARE EXTRUDED SUCCESSIVELY BY
AN AMAZING COORDINATION OF THE SECRETIONS OF A LARGE
NUMBER OF SIMPLE TUBULAR GLANDS ARRAYED IN TRANSVERSE
ZONES OF THE OVIDUCTAL GLAND &IGURE 4HE INNER
LAYER , IS FORMED lRST BY THE MOST ANTERIOR ZONE
MORE POSTERIORLY , IS ADDED FOLLOWED BY THE THICK
EST LAYER , AND lNALLY THE OUTER LAYER , WHICH IS
PRODUCED IN THE MOST POSTERIOR ZONE &IGURE
+NIGHT AND &ENG A +NIGHT &ENG AND 3TEWART
%ACH LAMELLA IS PRODUCED FROM A SEPARATE TRANS
VERSE GROOVE IN THE LINING OF THE GLAND EACH TRANSVERSE
GROOVE IN TURN CONTAINS A SINGLE ROW OF GEOMETRICALLY
PLACED 30)..%2%43 WHICH DElNE THE ORIENTATION OF MOL
ECULES IN THE EXTRUDED MATERIAL +NIGHT ET AL
)T IS SUGGESTED THAT THESE VALUES OF THICKNESS HAVE BEEN REDUCED
BY ABOUT BY DEHYDRATION IN ADDITION TANNED SHELLS APPEAR TO
BE THINNER THAN THOSE REMOVED FROM THE OVIDUCTS
!FTER THE MATERIAL HAS mOWED FOR SOME DISTANCE FROM
THE SPINNERETS THE MOLECULES AGGREGATE INTO lBRILS
WHICH BECOME LAMINATED AT THREE HIERARCHICAL LEVELS
AND HELICALLY TWISTED AT lVE TO SIX LEVELS 4HIS LINEAR
SECRETORY PATHWAY PERMITS THE STUDY OF THE SECRETION
ORIENTATION lBRILLOGENESIS AND ASSEMBLY OF A COMPLEX
COLLAGENOUS STRUCTURE OF GREAT STRENGTH ,AYERS , ,
AND , ARE COILED AROUND EACH OTHER IN THE TENDRILS
4HE OVIDUCTAL GLAND IS A COMPOUND TUBULAR GLAND
)T IS A DILATION OF THE ANTERIOR OVIDUCT ABOUT MM
POSTERIOR TO THE OSTIUM AND IS SURROUNDED BY A THIN
TOUGH CONNECTIVE TISSUE SAC &IGURES AND
3TANLEY +NIGHT AND &ENG +NIGHT &ENG
AND 3TEWART (AMLETT ET AL A %ACH FEMALE
HAS TWO OVIDUCTAL GLANDS WHICH APPEAR TO FUNCTION IN
SYNCHRONY SO THAT EGG CAPSULES OR TENDRILS ARE AT THE
SAME STAGE OF FORMATION IN EACH OF THE TWO OVIDUCTS
3IMILAR DORSAL AND VENTRAL MIRROR
IMAGE HALVES OF THE
GLAND ENCLOSE A DORSOVENTRALLY mATTENED ,5-%. INTO
WHICH THE EGG CASE IS EXTRUDED &IGURE ! -OST
OF THE WALL CONSISTS OF LONG SIMPLE TUBULAR GLANDS
ABOUT M IN DIAMETER WHICH ARE PACKED IN A FAIRLY
HEXAGONAL PATTERN AND OPEN INTO THIS LUMEN &IGURES
" AND %ACH HALF OF THE GLAND PRODUCES ONE
OF THE TWO WALLS OF THE CAPSULE WHILE THE THICKENED
MARGINAL RIB ARISES WITHIN GROOVES AT THE LEFT AND RIGHT
LIMITS OF THE mATTENED LUMEN THE TENDRILS ARE FORMED
WITHIN TWO SHALLOW PITS LOCATED ONE ON EACH SIDE OF
THE GLAND 4HE GLAND CHANGES IN SIZE DURING THE SEXUAL
CYCLE IN SEXUALLY MATURE FEMALES OF 3CYLIORHINUS CA
NICULA IT MAY BE CM LONG AND CM IN DIAMETER BUT
IS ONLY A SLIGHT THICKENING OF THE OVIDUCT IN SEXUALLY
IMMATURE FEMALES
4HE TUBULAR GLANDS ARE ARRANGED IN SIX TRANSVERSE
:/.%3 ZONES ! TO & WHICH FORM THE CAPSULE AND ITS
JELLY AS A COEXTRUSION &IGURE &ENG AND +NIGHT
+NIGHT AND &ENG +NIGHT &ENG AND
3TEWART :ONE ! SECRETES THE JELLY ZONES " TO
% PRODUCE LAYERS , TO , RESPECTIVELY (ISTOCHEMICAL
STUDIES ON THE OVIDUCTAL GLANDS OF 3CYLIORHINUS CAN
CIULA AND OTHER SPECIES HAVE SHOWN THAT THE ZONES
HAVE DIFFERING FUNCTIONS :ONE ! THE MOST ANTERIOR
CONSTITUTES ABOUT ONE QUARTER OF THE LENGTH OF THE GLAND
AND APPEARS TO SECRETE A NEUTRAL MUCOPOLYSACCHARIDE
WITH SMALL QUANTITIES OF COLLAGEN :ONE " CONSISTS OF
A SINGLE ROW OF TUBULES SECRETING A SULPHATED MUCO
POLYSACCHARIDE AND MAY CONTRIBUTE TO A THIN LAYER ON
THE INNER SURFACE OF THE CAPSULE PROBABLY , :ONE #
HAS THREE OR FOUR ROWS OF TUBULES AND TOGETHER WITH THE
lRST FEW ROWS OF TUBULES IN ZONE $ IT APPEARS TO FORM
/6)$5#43 !.$ /6)0!2)49
LAYER , )N ADDITION IT SECRETES THE COMPONENTS OF AN
OXIDATIVE PHENOLIC TANNING SYSTEM WHICH STRONGLY STA
BILIZE THE INNER LAYER , AND THE OUTER LAYER , THESE
INCLUDE PROTEIN RICH IN TYROSINE RESIDUES FREE $/0!
AN ORTHODIHYDROXYPHENOL OXIDASE AND A PEROXIDASE
:ONE $ CONSISTS OF ABOUT ROWS OF TUBULES THAT FORM
THE BULK OF THE THICKNESS OF THE CAPSULE LAYER , SE
CRETING COLLAGEN AND POSSIBLY ACCESSORY PROTEINS THE
STORAGE GRANULES IN ZONE $ APPEAR TO CONTAIN SMALL
QUANTITIES OF PEROXIDASE :ONE % ALSO SECRETES COM
PONENTS OF A PHENOLIC TANNING SYSTEM AS WELL AS SOME
COLLAGEN :ONE & WHICH HAS BEEN SUBDIVIDED ON THE
BASIS OF HISTOCHEMICAL OBSERVATIONS CONSISTS OF SHORT
TUBULES LYING PERPENDICULAR TO THE TUBULES OF ZONE
% :ONE & SECRETES A PHENOLIC PROTEIN TOGETHER WITH
PEROXIDASE AND ORTHODIHYDROXYPHENOL OXIDASES ZONE
& SECRETES NEUTRAL MUCOPOLYSACCHARIDES AND PEROXI
DASES AND ZONES & AND & SECRETE SULPHATED MUCO
POLYSACCHARIDES AND PEROXIDASE 4UBULES OF THE & ZONE
APPEAR TO CONTRIBUTE A THIN ELECTRON
DENSE LAYER ON THE
SURFACE OF , !LTERNATIVELY A MORPHOLOGICAL BASIS HAS
BEEN USED TO DIFFERENTIATE FOUR REGIONS OF THE OVIDUCTAL
GLAND WHERE THE #,5" AND 0!0),,!29 :/.%3 CORRESPOND
TO ZONE ! THE "!&&,% :/.% TO ZONES " # $ AND % AND
THE 4%2-).!, :/.% TO ZONE & &IGURE (AMLETT ET
AL A
4HE TUBULAR GLANDS CONSIST OF A SIMPLE COLUMNAR
EPITHELIUM OF GRANULAR SECRETORY CELLS LYING BETWEEN
CILIATED COLUMNAR CELLS &IGURES ! " +NIGHT AND
&ENG +NIGHT &ENG AND 3TEWART %ACH
TUBULE IS SURROUNDED BY A BASEMENT MEMBRANE AND
RICHLY VASCULAR COLLAGENOUS CONNECTIVE TISSUE THERE
ARE NO SMOOTH MUSCLE OR MYOEPITHELIAL CELLS IN THE
WALL OF THE TUBULE 4HE TUBULES OF ZONE $ ARE SHORTEST
ABOUT MM IN THE MOST ANTERIOR ROW AND INCREASE PRO
GRESSIVELY IN LENGTH REACHING APPROXIMATELY MM IN
THE MOST POSTERIOR ROW THIS CORRELATES WITH THE THICK
NESS OF THE LAMELLAE DERIVED FROM EACH ROW
4HE SECRETORY CELLS OF ZONE $ HAVE THE CHARACTER
ISTIC APPEARANCE OF CELLS SPECIALIZED FOR PROTEIN SE
CRETION THEIR NUCLEUS CONTAINS A LARGE NUCLEOLUS AND
LITTLE HETEROCHROMATIN THERE IS EXTENSIVE GRANULAR EN
DOPLASMIC RETICULUM A LARGE 'OLGI STACK AND APICAL
MICROVILLI AND THE CYTOPLASM IS PACKED WITH NUMER
OUS APPROXIMATELY SPHERICAL SECRETORY GRANULES ABOUT
M IN DIAMETER &IGURE 2USAOUN &ENG
AND +NIGHT +NIGHT ET AL +NIGHT &ENG
AND 3TEWART 4HE MARKED JUNCTIONAL COMPLEXES
AND EXTENSIVE INTERDIGITATIONS OF THE LATERAL MEMBRANES
PROBABLY INDICATE THAT THIS EPITHELIUM IS ALSO ACTIVELY
SECRETING IONS 7ITHIN CISTERNAE OF THE ENDOPLASMIC
RETICULUM THE COLLAGEN APPEARS ANISOTROPIC BUT AS
THE GRANULES MAKE THEIR WAY TO THE APICAL BORDER OF
THE CELL IT BECOMES DEHYDRATED AND UNDERGOES A SE
RIES OF LIQUID CRYSTAL TRANSFORMATIONS THEREBY PROVID
ING A COMPACT WAY OF STORING COLLAGEN &IGURES
AND 4HE GRANULES APPEAR TO BE RELEASED INTO THE
LUMEN BY MEROCRINE SECRETION !S IT PASSES ALONG THE
TUBULES PRESUMABLY BY CILIARY ACTION THE COLLAGEN AP
PEARS TO REHYDRATE REVERTING TO THE EARLIER PHASES OF
THE LIQUID CRYSTAL #OALESCENCE OF THE SECRETED GRAN
ULES INTO A THREAD WITHIN THE LUMEN IS THOUGHT TO OCCUR
BY HYDROPHOBIC INTERACTIONS )T IS SUGGESTED THAT THE
CHANGES IN THE MOLECULAR ARRANGEMENT OF THE COLLAGEN
ARE BROUGHT ABOUT BY A DRAMATIC INCREASE IN P( EN
COUNTERED IN PASSING FROM THE SECRETORY CELL THROUGH
THE SECRETORY TUBULE AND SECRETORY DUCT INTO THE LUMEN
OF THE OVIDUCTAL GLAND &IGURE &ENG AND +NIGHT
A
:ONE $ THE LARGEST ZONE OF THE OVIDUCTAL GLAND
PRODUCES THE LAMELLAE OF THE THICKEST REGION OF THE
CAPSULE , %ACH LAMELLA ORIGINATES WITHIN A DEEP
TRANSVERSE FOLD WHICH RUNS AROUND THE CIRCUMFER
ENCE OF THE LUMEN AND RARELY BRANCHES &IGURES
AND %ACH OF THE LAMELLAE CONSTITUTING LAYER ,
IS FORMED WITHIN A TRANSVERSE GROOVE WHICH RECEIVES
SECRETION FROM A SINGLE ROW OF $ ZONE TUBULES 4HERE
IS AN EXACT NUMERICAL CORRESPONDENCE IN THE NUMBER
OF LAMELLAE OF , THE NUMBER OF $ ZONE TRANSVERSE
GROOVES AND THE NUMBER OF ROWS OF $ ZONE TUBULES
4HE DEPTH OF THE TRANSVERSE GROOVES INCREASES CONTINU
OUSLY FROM THE lRST M TO THE LAST M
$URING THE FORMATION OF THE CAPSULE WALL THE LAMEL
LAE BEND THROUGH APPROXIMATELY AS THEY LEAVE THE
TRANSVERSE GROOVE AND MOVE POSTERIORLY ADHERING TO
GETHER TO FORM A SINGLE SHEET THAT IS CLOSELY APPLIED TO
THE LUMEN OF THE GLAND &IGURE
4HE FUNCTIONAL UNIT IN ALL PARTS OF THE GLAND CONSISTS
OF A 3%#2%4/29 45"5,% COMPOSED OF COLUMNAR SECRETO
RY CELLS INTERSPERSED WITH SOME COLUMNAR CILIATED CELLS
A SHORT $5#4 LINED WITH COLUMNAR CILIATED CELLS BUT
LACKING SECRETORY CELLS AND A 30)..%2%4 &IGURE
+NIGHT AND &ENG +NIGHT &ENG AND 3TEWART
(AMLETT ET AL A B ! SINGLE ROW OF SPIN
NERETS OPENS INTO THE BASE OF EACH TRANSVERSE GROOVE
IN ZONES " TO % &IGURE 4UBULAR GLANDS IN ZONE
! SECRETE THEIR MUCOPOLYSACCHARIDES DIRECTLY INTO THE
LUMEN OF THE GLAND 4HESE GROOVES RUN AROUND THE
ENTIRE WIDTH OF THE GLAND WITH LITTLE BRANCHING %ACH
SPINNERET IS FORMED OF TWO HALF OVERLAPPING mATTENED
#(!04%2
"!&&,% 0,!4%3 WHICH PROJECT INTO THE BASE OF THE TRANS
VERSE GROOVE ON EACH SIDE OF THE OPENING OF THE SECRE
TORY DUCT &IGURE 4HE BAFmE PLATES ARE SUPPORTED
BY A THIN CORE OF LOOSE VASCULAR CONNECTIVE TISSUE AND
ARE COVERED ON BOTH SIDES BY A CILIATED LOW COLUM
NAR EPITHELIUM 4HEY ARE ARRANGED AT AN ANGLE OF AP
PROXIMATELY TO THE LONGEST AXIS OF EACH TRANSVERSE
GROOVE &IGURES ! " 4HE BAFmE PLATES DIVIDE THE
BASE OF THE GROOVE INTO THREE COMPARTMENTS THE !.
4%2)/2 AND 0/34%2)/2 #29043 BETWEEN THE BAFFLE PLATES
AND THE WALLS OF THE TRANSVERSE GROOVE AND THE OBLIQUE
SLIT #%.42!, #2904 BETWEEN EACH PAIR OF BAFmE PLATES
4HE BAFmE PLATES DIVIDE THE SECRETED MATERIAL INTO THREE
mOWS ANTERIOR CENTRALOBLIQUE AND POSTERIOR THAT JOIN
TO FORM A SINGLE SHEET &IGURE 4HE MATERIAL IS
PROBABLY STILL PLASTIC IN THE TRANSVERSE GROOVES
"OTH SURFACES OF THE TRANSVERSE GROOVE AND BOTH SUR
FACES OF EACH BAFmE PLATE ARE DENSELY CILIATED +NIGHT
AND &ENG 4HE AXIS OF CILIARY BEAT SEEMS TO BE
VERTICAL ON BOTH FACES OF THE TRANSVERSE GROOVE AND AP
PROXIMATELY
AND TO THE VERTICAL AXIS ON THE
ANTERIOR AND POSTERIOR FACES OF THE BAFmE PLATES RESPEC
TIVELY &IGURE # #ILIARY ROOTLETS ARE ORIENTED IN
LINE WITH THE DIRECTION OF BEAT /BSERVATIONS ON CAP
SULE FORMATION IN 2AJA ERINACEA INDICATE THAT MATE
RIAL WITHIN THE LUMEN OF THE TUBULAR GLAND IS ROUGHLY
CIRCULAR IN CROSS SECTION AND M IN DIAMETER AS
IT PASSES THROUGH THE SPINNERET IT DIVERGES SMOOTHLY
AND EMERGES AS A mATTENED RIBBON ABOUT X M
&IGURE ! +NIGHT ET AL %ACH SPINNERET
EXTRUDES A SINGLE mATTENED RIBBON !S THE SECRETED MA
TERIAL DIVERGES FROM THE SECRETORY TUBULE A CURVED PAT
TERN OF MOLECULAR ORIENTATIONS IS SET UP AND AFTER THE
MATERIAL HAS mOWED SOME DISTANCE FROM THE SPINNER
ETS THE MOLECULES AGGREGATE INTO lBRILS 4HIS MATERIAL
IS LARGELY COLLAGENOUS /VERLAPPING ROWS OF RIBBONS
FUSE TOGETHER TO FORM A SINGLE LAMELLA &IGURE "
4HE OVERLAPPING OF lVE RIBBONS AT EACH POINT IN THE LA
MELLA GIVES RISE TO A CONSTRUCTION THAT IS SIMILAR TO PLY
WOOD EXCEPT THAT THERE ARE CURVED lBRES IN EACH PLY
! Z
SERIES OF CONFOCAL IMAGES CUT PARALLEL TO THE PLANE
OF A SINGLE LAMELLA CONlRMS THIS PATTERN OF STEPPED
ROTATION OF THE MOLECULAR AXIS IN SUCCESSIVE RIBBONS
&IGURE # 4HIS ARRANGEMENT PROVIDES GREAT
TOUGHNESS AND RESILIENCY TO THE EGG CAPSULE
"EFORE THE OVUM ENTERS THE OVIDUCTAL GLAND THE
0/34%2)/2 4%.$2),3 ARE FORMED IN MARGINAL 4%.$2),
&/2-).' 2%')/.3 OF THE % ZONE &IGURE &ENG
AND +NIGHT B +NIGHT &ENG AND 3TEWART
4HE TENDRILS ARE MOVED ALONG THE CHANNELS BY CILIA AND
ROTATE DURING FORMATION SO THAT IN CROSS SECTION THE
LAMELLAE EXHIBIT A 3WISS ROLL CONSTRUCTION OF ALTERNAT
ING NARROW AND BROAD LAMINAE WHICH ENTRAP mUID lLLED
#!.!,)#5,) BETWEEN THEM &IGURE )N CONTRAST TO
THE ORTHOGONAL ARRANGEMENT IN ADJACENT LAMINAE OF
THE CAPSULE WALL COLLAGENOUS lBRES ARE ORIENTED AP
PROXIMATELY AT RIGHT ANGLES IN ADJACENT LAMINAE OF THE
TENDRILS CIRCUMFERENTIALLY IN THE NARROW LAMINAE AND
LONGITUDINALLY IN THE BROAD LAMINAE 7HEN THE POSTE
RIOR TENDRILS ARE FULLY FORMED ALL OF THE TUBULAR GLANDS
ARE ACTIVATED IN THE #!035,% 7!,, &/2-).' 2%')/.
BETWEEN THE TUBULAR FORMING REGIONS AND PRODUCTION
BEGINS ON THE POSTERIOR MARGIN OF THE CAPSULE THE 0/3
4%2)/2 -!2').!, 3%!, WITH ITS CRIMPED CONSTRUCTION
4HIS IS FOLLOWED BY FORMATION OF THE WALLS OF THE 0/5#(
WHOSE DORSAL AND VENTRAL HALVES ARE HELD APART BY THE
JELLY SECRETED BY THE ! ZONE &IGURE %XTRUSION
OF THE JELLY WHICH WILL COME TO SURROUND THE OVUM AP
PEARS TO PROVIDE MUCH OF THE FORCE FOR THE EXPULSION OF
THE CAPSULE 7HEN ABOUT ONE THIRD OF THE CAPSULE HAS
BEEN FORMED THE OVUM ENTERS THE LUMEN OF THE GLAND
FROM THE ANTERIOR OVIDUCT AND ASSISTS IN THE PROPUL
SION OF THE EGG CASE &IGURE 4HE OVUM BECOMES
ENVELOPED BY THE LAYERS OF THE CAPSULE WALL WHICH ARE
EXTRUDED IN SEQUENCE UNTIL lNALLY THE POUCH IS COM
PLETE AND THE !.4%2)/2 3%!, IS FORMED 4HE -!2').!,
2)"3 OF THE POUCH ARE FORMED BY THE TENDRIL FORMING
REGIONS AND THESE EXTEND BEYOND THE ANTERIOR SEAL TO
BECOME THE !.4%2)/2 4%.$2),3 )NNERVATION OF THE OVI
DUCTAL GLAND BY TWO SYMPATHETIC NERVE BRANCHES WHICH
ENTER NEAR EACH TENDRIL FORMING REGION SUGGESTS THAT
SYMPATHETIC ACTIVITY MAY ACTIVATE SECRETION OF THE POS
TERIOR TENDRILS THE lRST EVENT OF THE SECRETORY CYCLE
! CONSISTENT FEATURE OF ELASMOBRANCH OVIDUCTAL
GLANDS THAT PRODUCE AN EGG ENVELOPE IS THE BAFmE ZONE
4HE VIVIPAROUS YELLOW SPOTTED STINGRAY 5ROLOPHUS
JAMAICENSIS HOWEVER IS AN EXCEPTION IN THAT IT DOES
NOT PRODUCE AN EGG ENVELOPE A TYPICAL BAFmE ZONE IS
LACKING BUT A MODIlED hBAFmE EQUIVALENT ZONEv PER
SISTS (AMLETT ET AL B 4HE OVIDUCTAL GLANDS
ACTIVELY SYNTHESIZE AND ASSEMBLE lBRILS TO PRODUCE
A TRANSITORY EGG COVERING (AMLETT ET AL B
)N ADDITION TO THE PRODUCTION OF EGG CAPSULES THE
OVIDUCTAL GLAND OF FEMALE ELASMOBRANCHS IS A PRINCIPAL
SITE OF SPERM STORAGE THEREBY ENHANCING THE CHANCES
OF SUCCESSFUL INSEMINATION 0RATT 4HE GLAND
WITH ITS LONG NARROW TUBULES PROVIDES A FAVOURABLE
ENVIRONMENT FOR THE MAINTENANCE OF SPERM FOR PERIODS
OF MONTHS OR EVEN MORE THAN A YEAR IN SOME SPECIES
&IGURE 3OME OF THE TUBULES SEEM TO BE SPECIAL
/6)$5#43 !.$ /6)0!2)49
IZED FOR SPERM RETENTION AND IN SOME SPECIES SUCH AS
3PHYRNA LEWINI MAY CONSTITUTE A TRUE SEMINAL VESICLE
5TERUS IN %LASMOBRANCHS
)N MANY SPECIES OF ELASMOBRANCHS THE DILATED POSTE
RIOR REGION OF THE FEMALE GENITAL TRACT MAY BE MODI
lED AS A UTERUS CERVIX AND COMMON UROGENITAL SINUS
&IGURES AND ! " +OOB AND (AMLETT
(AMLETT AND (YSELL 4HE UTERUS HARBOURS THE
EGG CAPSULE OF OVIPAROUS FORMS DURING THE COMPLE
TION OF SCLEROTIZATION AND IT SECRETES MATERIALS THAT MAY
CONTRIBUTE TO THIS PROCESS )N APLACENTAL VIVIPAROUS
SPECIES THE UTERUS FUNCTIONS AS A RESPIRATORY MEM
BRANE AND REGULATOR OF THE IONIC AND OSMOTIC ENVIRON
MENT IT PROVIDES NO SUPPLEMENTAL NUTRIENTS AND THE
EMBRYOS SUBSIST ON THEIR OWN YOLK STORES OR BY FEEDING
ON OVULATED EGGS )N PLACENTAL VIVIPAROUS SPECIES THE
UTERUS PROVIDES NUTRIENTS FOR THE DEVELOPING EMBRYOS
AFTER THEIR YOLK STORES HAVE BEEN DEPLETED
4HE UTERUS IS LINED BY A 45.)#! -5#/3! CONSIST
ING OF AN EPITHELIUM WITH ITS BASAL LAMINA RESTING ON
LOOSE VASCULAR CONNECTIVE TISSUE THAT MAY BE SO RICH
LY HYDRATED THAT IT SOMETIMES APPEARS MESENCHYMAL
&IGURE (AMLETT ET AL B (AMLETT AND (Y
SELL 4HE CONNECTIVE TISSUE IS SUBTENDED BY TWO
LAYERS OF SMOOTH MUSCLE AN INNER CIRCULAR LAYER AND
OUTER LONGITUDINAL LAYER 4HE MUSCLE IS ENCLOSED BY A
45.)#! !$6%.4)4)! CONSISTING OF DELICATE FIBROUS CON
NECTIVE TISSUE AND THE SIMPLE SQUAMOUS MESOTHELIUM
OF THE PERITONEUM %ACH OF THE LAYERS OF THE UTERUS IS
MODIlED TO REmECT THE REPRODUCTIVE MODE OF THE VARI
OUS SPECIES
4HE LINING OF THE GRAVID UTERUS OF THE OVIPAROUS
LITTLE SKATE 2AJA ERINACEA IS THROWN UP INTO RICHLY
VASCULARIZED LONGITUDINAL FOLDS WITH BRANCHING TUBU
LAR GLANDS IN THE INTERVENING GROOVES &IGURE
+OOB AND (AMLETT (AMLETT AND (YSELL
4HE SIMPLE COLUMNAR EPITHELIAL CELLS ON THE SURFACES
OF THE FOLDS BRISTLE WITH CILIA AND MICROVILLI WHILE AT
THE SIDES OF THE FOLDS THE EPITHELIAL CELLS ARE LOWER AND
CONTAIN APICAL SECRETORY VESICLES 4HE LOOSE SUBEPITHE
LIAL CONNECTIVE TISSUE OF EACH RIDGE IS RICHLY VASCULAR
AND ITS CAPILLARIES PRESS AGAINST THE EPITHELIAL BASAL
LAMINA &IGURE # )N ELECTRON MICROGRAPHS THERE
IS A STRONG APPEARANCE OF A TRANSPORTING EPITHELIUM
ELABORATE INTERCELLULAR CHANNELS WITH EXTENSIVE LATERAL
CELL PROCESSES PENETRATING BETWEEN THE EPITHELIAL CELLS
AND APICAL JUNCTIONAL COMPLEXES SEALING THESE CHAN
NELS FROM THE LUMEN &IGURE 4HE CYTOPLASM
OF THE EPITHELIAL CELLS CONTAINS MITOCHONDRIA GRANU
LAR ENDOPLASMIC RETICULUM 'OLGI COMPLEXES FREE
RIBOSOMES POLYSOMES AND OCCASIONAL LYSOSOMES
4HE SECRETORY CELLS FROM THE SIDES OF THE FOLDS ARE
CUBOIDAL WITH SURFACE MICROVILLI AND ELABORATE APICAL
VESICLES CONTAINING FROTHY MODERATELY ELECTRON DENSE
SECRETORY MATERIAL &IGURE $ 4HE CYTOPLASM
CONTAINS ABUNDANT GRANULAR ENDOPLASMIC RETICULUM
AND 'OLGI COMPLEXES ,ATERAL FOLDS CREATE EXTENSIVE
INTERCELLULAR CHANNELS BETWEEN THE CELLS 4HE STRUC
TURE OF THE UTERINE WALL IS CONSISTENT WITH ITS ROLE IN
hlNISHINGv THE EGG CAPSULE #ILIARY ACTION AND SMOOTH
MUSCLE MOVE THE EGG THROUGH THE LUMEN UTERINE SE
CRETIONS ASSIST IN TANNING THE CAPSULAR MATRIX THE RICH
VASCULARIZATION PROVIDES THE OXYGEN NECESSARY FOR
TANNING TO OCCUR AND THE ELABORATE INTERCELLULAR
SPACES EVINCE A TRANSPORTING EPITHELIUM THAT REMOVES
EXCESS WATER FROM THE LUMEN
4HE EGG CAPSULE IS WHITE WHEN IT LEAVES THE OVI
DUCTAL GLAND AND CONTAINS NO CATECHOLIC SUBSTANCE
ALTHOUGH AN INACTIVE FORM OF THE ENZYME CATECHOL OXI
DASE IS INCORPORATED INTO THE MATRIX DURING SECRETION
+OOB +OOB AND #OX +OOB
AND #ALLARD 4ANNING OCCURS AS THE EGG PASSES
INTO THE UTERUS WHERE CATECHOLS BEGIN TO ACCUMULATE
IN THE CAPSULAR MATERIAL AND ARE OXIDIZED UNDER THE
INmUENCE OF CATECHOL OXIDASE TO QUINONES &IGURE
4HE OXYGEN REQUIRED FOR THIS TANNING IS TRANS
PORTED FROM THE MATERNAL CIRCULATION BY THE UTERUS
#ALCIUM AND TO A LESSER EXTENT MAGNESIUM ARE IN
CORPORATED INTO THE CAPSULE DURING ITS FORMATION IN
THE OVIDUCTAL GLAND SUBSEQUENT BINDING OF THESE MIN
ERALS IS CONCOMITANT WITH THE TANNING PROCESS IN THE
UTERUS &IGURE
4HE OVIPAROUS UTERUS OF ELASMOBRANCHS SHARES
MANY STRUCTURAL FEATURES WITH THAT OF VIVIPAROUS SPE
CIES (AMLETT AND (YSELL )NITIALLY ALL ELASMO
BRANCH EMBRYOS RELY ON THEIR YOLK RESERVES CONTAINED
WITHIN THE FOETAL YOLK SAC !S DEVELOPMENT CONTINUES
VARIOUS SOURCES OF NUTRIENTS ARE TAPPED AND VIVIPARITY
MANIFESTS ITSELF IN MANY WAYS FROM SPECIES TO SPECIES
-ODIlCATIONS IN THE UTERINE LINING PROVIDE FOR THE
PROLONGED SUPPORT OF DEVELOPING EMBRYOS )NCLUDED
ARE INCREASED VASCULARIZATION BRINGING GREATER OXY
GEN SUPPLIES TO THE LUMEN ELABORATE EXTENSIONS OF THE
TUNICA MUCOSA THAT ENHANCE ITS SURFACE AREA FOR META
BOLIC EXCHANGE AND THINNING OF THE TISSUES BETWEEN
THE CAPILLARIES AND THE SURFACE THEREBY REDUCING THE
DIFFUSION DISTANCE FOR GAS EXCHANGE &OUR TYPES OF
VIVIPARITY HAVE BEEN CATEGORIZED APLACENTAL YOLK SAC
#(!04%2
VIVIPARITY WHERE THE DEVELOPING EMBRYO RELIES SOLELY
ON ITS OWN YOLK RESERVES FOR NOURISHMENT APLACENTAL
OOPHAGOUS VIVIPARITY WHERE THE EMBRYO NOURISHES IT
SELF WITHIN THE UTERUS BY GRAZING ON ITS SIBLINGS APLA
CENTAL VIVIPARITY WITH UTERINE VILLI OR 42/0(/.%-!4!
WHERE VASCULARIZED lNGER
LIKE PROCESSES SECRETE A NU
TRIENT hUTERINE MILKv CALLED ()34/42/0( AND PLACENTAL
VIVIPARITY
4HE UTERUS OF THE SPINY DOGlSH 3QUALUS ACANTHIAS
PROVIDES NO NUTRIENTS FOR THE DEVELOPING EMBRYOS BUT
IT MAINTAINS OSMOTIC AND IONIC LEVELS THEREBY GIVING
THEM A SAFE HAVEN FOR THEIR DEVELOPMENT (AMLETT
AND (YSELL 4HIS IS AN EXAMPLE OF !0,!#%.4!,
9/,+ 3!# 6)6)0!2)49 4HE LINING OF THE GRAVID UTERUS
IS THROWN UP IN LONGITUDINAL mAPS WHOSE RIMS ARE EX
PANDED BY A LARGE ARTERY THAT SENDS CAPILLARIES INTO THE
CORE OF LOOSE CONNECTIVE TISSUE SUPPLYING NUTRIENTS
TO THE EPITHELIUM AND THE SMOOTH MUSCLE OF THE WALL
&IGURES ! TO # 4HE FOLDS ARE COVERED BY A STRATI
lED CUBOIDAL EPITHELIUM WITH A MICROVILLOUS BORDER
&IGURES $ %
4HE SANDTIGER SHARK #ARCHARIAS TAURUS EXEMPLIlES
!0,!#%.4!, //0(!'/53 6)6)0!2)49 (AMLETT AND (Y
SELL )N ADDITION TO FEEDING ON OVULATED EGGS
THE FOETUS PRACTICES INTRAUTERINE CANNIBALISM FEEDING
ON ITS HAPLESS SIBLINGS THAT HAD THE MISFORTUNE TO BE
OVULATED AT A LATER TIME 4HE SMOOTH WALL OF THE NON
GRAVID UTERUS IS LINED BY A LAYER OF CUBOIDAL EPITHE
LIAL CELLS WITH A MICROVILLOUS BORDER &IGURE !
)MMEDIATELY BELOW ARE THREE TO lVE LAYERS OF mAT
TENED CELLS CONTAINING lBRES AND LIPID DROPLETS AND
DEEPER STILL IS A THICKER LAYER OF CELLS CONTAINING FROTHY
3CHIFF
POSITIVE VESICLES ,ONGITUDINAL FOLDS DEVELOP IN
THE UTERUS OF GRAVID FEMALES THEREBY INCREASING THE
SURFACE AREA OF THE LINING &IGURE " 4HE SURFACE
EPITHELIAL CELLS HAVE BECOME CUBOIDAL AND VASCULARIZA
TION OF THE CONNECTIVE TISSUE HAS INCREASED
)N ANOTHER FORM OF !0,!#%.4!, 6)6)0!2)49 SEEN IN
THE YELLOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS
VASCULARIZED VILLI OR TROPHONEMATA INCREASE THE SUR
FACE AREA FOR THE SECRETION OF NUTRIENT hUTERINE MILKv
OR HISTOTROPH THAT IS INGESTED BY THE DEVELOPING EM
BRYO ANDOR ABSORBED BY EXTERNAL GILL lLAMENTS (AM
LETT AND (YSELL 4HE GRAVID UTERUS IS LINED BY A
DENSE MAT OF TROPHONEMATA ! LARGE BLOOD VESSEL IN THE
CORE OF EACH TROPHONEMA SENDS CAPILLARIES THROUGHOUT
THE CONNECTIVE TISSUE OF THE lNGER
LIKE ORGAN &IGURE
! 4HE SURFACE OF THE TROPHONEMA IS THROWN UP
INTO RIDGES WITH CORES OF DELICATE VASCULARIZED CONNEC
TIVE TISSUE !S THE FOETUS DEVELOPS THE CUBOIDAL EPITHE
LIUM ON THE SURFACE OF THE RIDGES BECOMES ATTENUATED
SIMPLE SQUAMOUS &IGURE " ! SINGLE BASAL LAM
INA AND SPARSE CONNECTIVE TISSUE SEPARATE THIS EPITHELI
UM FROM THE ENDOTHELIAL CELLS OF THE CAPILLARIES BELOW
!BUNDANT MICROPINOCYTOTIC VESICLES IN THE ENDOTHELIAL
CELLS INDICATE BRISK EXCHANGE OF MATERIALS 3ECRETORY
CRYPTS BETWEEN THE RIDGES ARE LINED BY SIMPLE CUBOI
DAL EPITHELIAL CELLS CONTAINING LARGE NUMBERS OF APICAL
SECRETORY VESICLES &IGURE # 4HESE CELLS CONTAIN
ABUNDANT GRANULAR ENDOPLASMIC RETICULUM NUMER
OUS 'OLGI COMPLEXES AND SEVERAL TYPES OF SECRETION
VESICLES &IGURES $ % 4HERE ARE A FEW MICRO
VILLI ON THE SURFACE OF THESE CELLS THE BORDERS BETWEEN
ADJACENT CELLS ARE STRAIGHT AND ARE JOINED APICALLY BY
TIGHT JUNCTIONS
0,!#%.4!, 6)6)0!2)49 IS SEEN IN !TLANTIC SHARPNOSED
SHARKS 2HIZOPRIONODON TERRAENOVAE (AMLETT AND
(YSELL 0LACENTAL SHARKS USUALLY DEVELOP IN
SEPARATE UTERINE COMPARTMENTS WITH EACH EMBRYO
SURROUNDED BY ITS OWN EGG ENVELOPE !FTER ITS YOLK
STORES ARE EXHAUSTED THE EMPTY YOLK SAC DEVELOPS INTO
A (!%-!42/0()# 0,!#%.4! 4HE UTERINE COMPARTMENT IS
SMOOTH BEFORE IMPLANTATION AND COMPOSED OF A SIMPLE
COLUMNAR SECRETORY EPITHELIUM OVERLYING RICHLY VAS
CULAR LOOSE CONNECTIVE TISSUE &IGURES ! TO #
4HE USUAL -%2/#2).% 3%#2%4)/. TAKES PLACE FROM THESE
EPITHELIAL CELLS WHERE DROPLETS OF SECRETION ARE RE
LEASED WITH NO LOSS OF CYTOPLASM OR MEMBRANE )N AD
DITION HOWEVER THESE CELLS RELEASE MEMBRANE
BOUND
CYTOPLASMIC MASSES OR hBLEBSv INTO THE LUMEN THIS IS
!0/#2).% 3%#2%4)/. WHERE CYTOPLASM AND MEMBRANE
ARE LOST FROM THE APEX OF A SECRETORY CELL WHILE THE
BASAL PORTION SURVIVES TO PRODUCE MORE SECRETION
4HE SURFACE OF THE UTERUS AT TERM IS A MODIlED SIMPLE
CUBOIDAL EPITHELIUM WITH FEW SECRETORY VESICLES AND
SPARSE MICROVILLI IT RESTS ON A DENSE VASCULAR BED
&IGURES # $ 4HE UTERUS IS SEPARATED FROM THE
RICHLY VASCULAR FOETAL PORTION OF THE PLACENTA THE DISTAL
PORTION OF THE FORMER YOLK SAC BY THE EGG ENVELOPE
/6)$5#43 !.$ /6)0!2)49
&IGURE 4HE URINARY AND GENITAL SYSTEM OF A FEMALE TROUT /VA ARE DISCHARGED DIRECTLY INTO THE COELOM AC AND PASS
THROUGH A CONSTRICTION C IN THE POSTERIOR ABDOMINAL WALL INTO THE GENITAL CAVITY GC 4HEY LEAVE THE BODY BY WAY OF AN ORIlCE
GO IN THE URINOGENITAL PAPILLA &ROM (ENDERSON &ISHERIES AND /CEANS #ANADA 2EPRODUCED WITH THE PERMISSION OF
THE -INISTER OF 0UBLIC 7ORKS AND 'OVERNMENT 3ERVICES
!BBREVIATIONS B BLADDER K KIDNEYS O OVARY PF PERITONEAL FOLD UD URINARY DUCT UO URINARY ORIlCE
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE OVIDUCT OF THE BLEAK !LBURNUS ALBURNUS &ROM ,AHN
STEINER 7EISMANN AND 0ATZNER REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! #ILIATED CELLS CONSTITUTE MOST OF THE EPITHELIUM LINING THE OVIDUCT THESE ARE INTERSPERSED WITH SMALL CLUSTERS OF MICROVILLOUS
CELLS CONTAINING LARGE LIPID VACUOLES
" !PICAL REGION OF A CILIATED CELL
# #ROSS SECTIONS OF CILIA FROM A CILIATED CELL
$ 3ECTIONS THROUGH CILIARY BASAL BODIES -ICROlLAMENTS INSERT ARROWHEAD AT THE TUBULE TRIPLETS OF THE BASAL BODY
% ,ONGITUDINAL SECTIONS OF BASAL BODIES AND CILIA
& 4HE MID REGION OF A CILIATED CELL CONTAINS MITOCHONDRIA AND ACCUMULATIONS OF FREE RIBOSOMES
' 4HE CYTOPLASM OF A CILIATED CELL CONTAINS ABUNDANT MITOCHONDRIA AND GRANULAR ENDOPLASMIC RETICULUM
!BBREVIATIONS B BASAL BODY C CILIATED CELL CI CILIUM CT CENTRAL MICROTUBULES OF CILIUM LI LIPID VACUOLE LU LUMEN MI MI
TOCHONDRION MV MICROVILLOUS CELL NU NUCLEUS PT PERIPHERAL MICROTUBULES OF CILIUM R RIBOSOMES RER GRANULAR ENDOPLASMIC
RETICULUM SMF STRIATED CILIARY ROOTLETS T MICROTUBULE TRIPLET
/6)$5#43 !.$ /6)0!2)49
&IGURE -ICROGRAPHS OF SECTIONS FROM THE BLEAK !LBURNUS ALBURNUS &ROM ,AHNSTEINER 7EISMANN AND 0ATZNER
REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 0HOTOMICROGRAPH OF AN OVIDUCT SHOWING THE LOCATION OF A CLUSTER OF MICROVILLOUS CELLS ARROW IN THE CREVICE BETWEEN
MUCOSAL FOLDS COVERED WITH CILIATED CELLS
" 4RANSMISSION ELECTRON MICROGRAPH OF MICROVILLOUS EPITHELIAL CELLS OF THE OVARIAN CAVITY
!BBREVIATIONS BL BASAL LAMINA CI CILIA CTL SUBMUCOSAL CONNECTIVE TISSUE EP EPITHELIUM LU LUMEN MI MITOCHONDRIA
NL NUCLEOLUS NU NUCLEUS P PERITONEUM RER GRANULAR ENDOPLASMIC RETICULUM
#(!04%2
&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH THE OVARY AND OVARIAN DUCTS OF THE PLATYlSH 8IPHOPHORUS MACULATUS
&ROM 0OTTER AND +RAMER REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! #ROSS SECTION THROUGH THE MATURE OVARY SHOWING OOCYTES AT DIFFERENT STAGES OF DEVELOPMENT SURROUNDING THE OVARIAN DUCT
AND LUMEN /$, 8
" 3ECTION THROUGH THE OVARIAN DUCT OF AN INSEMINATED lSH SHOWING SPERM HEADS ARROWHEADS INCORPORATED WITHIN THE CYTO
PLASM OF EPITHELIAL CELLS LINING THE LUMEN OF THE OVARIAN DUCT /$, 8
/6)$5#43 !.$ /6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EPITHELIUM OF OVARIAN DUCTS OF THE PLATYlSH
8IPHOPHORUS MACULATUS &ROM 0OTTER AND +RAMER REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 3OME EPITHELIAL CELLS EXHIBIT A UNIFORMLY SCALLOPED APICAL MEMBRANE 8
" 4HE SURFACE MEMBRANES OF SOME EPITHELIAL CELLS EXHIBIT BROAD LOBULAR EXTENSIONS !PICAL JUNCTIONAL COMPLEXES ARROWHEADS
ARE APPARENT 8
#(!04%2
&IGURE #ONTINUED
# )N SOME REGIONS THE SURFACE EPITHELIUM CONTAINS EXTENSIVE MICROVILLI AND BRANCHED MICROVILLUS
LIKE APPENDAGES PROJECTING
INTO THE LUMEN /$, *UNCTIONAL COMPLEXES ARROWHEADS ARE CONSPICUOUS 8
$ ! SPERM NUCLEUS ARROWHEAD IS INCORPORATED WITHIN A SPECIALIZED EPITHELIAL CELL OF THE DUCT THE SPERM
ASSOCIATED CELL
4HIS EPITHELIUM HAS DEEP SURFACE FOLDS AND POCKETS 8
/6)$5#43 !.$ /6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EPITHELIUM OF OVARIAN DUCTS OF THE PLATYlSH
8IPHOPHORUS MACULATUS &ROM 0OTTER AND +RAMER REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! #OMPLEX INFOLDINGS ARROWHEADS PENETRATE DEEP BETWEEN THESE EPITHELIAL CELLS OF THE OVARIAN DUCT !PICAL TIGHT JUNCTIONS
ARROWS AND DESMOSOMES CURVED ARROWS ARE APPARENT ! SPERM NUCLEUS 3. IS INCORPORATED WITHIN A SPERM
ASSOCIATED
CELL 8
" 4HESE SPERM
ASSOCIATED CELLS EXHIBIT DEEP SURFACE PITS AND POCKETS )NTACT SPERM NUCLEI 3. WITH MIDPIECE MITOCHONDRIA
- AND mAGELLA ARROWHEADS ARE SEEN WITHIN THE POCKETS /$, LUMEN OF THE OVARIAN DUCT 8
#(!04%2
&IGURE #ONTINUED
# .UMEROUS SPERM ARROWHEADS ARE CONTAINED WITHIN THE SURFACE POCKETS AND PITS OF SPERM
ASSOCIATED CELLS 3PERM NUCLEI
3. ARE ALSO SEEN WITHIN THE LUMEN OF THE OVARIAN DUCT /$, AND DEEP WITHIN THE CYTOPLASM OF A SPERM
ASSOCIATED CELL
4HE OPEN ARROWS INDICATE SPERM TAILS AT THE SURFACE WITHIN PITS AND INCORPORATED WITHIN THE CYTOPLASM 8
$ 3PERM
ASSOCIATED CELLS CONTAIN SPERM NUCLEI ARROWHEADS IN THEIR BASAL REGIONS -ANY SPERM TAILS ARROWS ARE EMBEDDED
WITHIN THE CYTOPLASM 8
/6)$5#43 !.$ /6)0!2)49
&IGURE #ONTINUED
% 3EVERAL SPERM NUCLEI ARROWHEADS AND mAGELLA ARROWS ARE INCORPORATED WITHIN THE SPERM
ASSOCIATED CELLS /$, LUMEN OF
OVARIAN DUCT 8
#(!04%2
@
&IGURE $RAWING OF A VENTRAL VIEW OF THE UROGENITAL
ORGANS OF A MATURE PREGNANT FEMALE DOGlSH /NE OVARY IS
SHOWN ONLY IN OUTLINE AND PART OF ONE UTERUS HAS BEEN RE
MOVED IN ORDER TO EXPOSE STRUCTURES LYING DORSAL TO THEM
&ROM 7EICHERT REPRODUCED WITH PERMISSION OF
THE -C'RAW
(ILL #OMPANIES
/6)$5#43 !.$ /6)0!2)49
&IGURE 0HOTOMICROGRAPH OF A CROSS SECTION OF THE OVIDUCT OF A DOGlSH 3QUALUS ACANTHIAS 8 4HE WALL IS THROWN UP
INTO ROUNDED FOLDS COVERED BY A TUNICA MUCOSA OF STRATIlED CUBOIDAL EPITHELIUM 4HE TUNICA SUBMUSOSA FORMING THE CORE OF
THE FOLDS AND SUBTENDING THEM IS MADE UP OF LOOSE lBROUS CONNECTIVE TISSUE CONTAINING SEVERAL BLOOD VESSELS AND SCATTERED
SMOOTH MUSCLE CELLS 4HIS LAYER MERGES IMPERCEPTIBLY INTO THE SMOOTH MUSCLE OF THE TUNICA MUCULARIS CONSISTING OF A LOOSE INNER
LAYER OF CIRCULAR lBRES AND A DENSER OUTER LAYER OF LONGITUDINAL lBRES 4HE OVIDUCT IS ENCLOSED BY A TUNICA SEROSA OF LOOSE lBROUS
CONNECTIVE TISSUE COVERED BY SIMPLE CUBOIDAL TO LOW COLUMNAR CELLS
@
&IGURE 0HOTOMICROGRAPHS TO ILLUSTRATE SPERM STORAGE IN THE OVIDUCTAL GLAND OF A RECENTLY INSEMINATED BLUE SHARK
0RIONACE GLAUCA &ROM 0RATT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
! #ROSS SECTION OF THE OVIDUCTAL GLAND 3PERM APPEAR AS DARK MASSES IN THE SHELL SECRETING TUBULES SURROUNDING THE 3
SHAPED
CENTRAL LUMEN 3: SPERM STORAGE ZONE
" 3ECTIONS OF OVIDUCTAL TUBULES SHOWING SPERM 3 STORAGE WITHIN THE LUMINA ARROW
#(!04%2
&IGURE $IAGRAM OF THE ADULT FEMALE REPRODUCTIVE TRACT OF THE CHIMAEROID (YDROLAGUS COLLIEI !BOUT LIFE SIZE 4HE LOWER
REGION IS SPLIT ALONG ONE SIDE AND LAID OPEN SO THAT THE DORSAL HALF LIES TO THE RIGHT &ROM 3TANLEY REPRODUCED WITH
PERMISSION OF *OHN 7ILEY 3ONS )NC
!BBREVIATIONS !' ACCESSORY GENITAL GLAND $' DORSAL MEDIAN GROOVE OF THE UTERUS ,! LAMELLAE /! OSTIUM /# OVIDUCTAL
CONE /6 OVIDUCT 3' SHELL GLAND 30 UTERO
VAGINAL SPHINCTER 5 UTERUS 6 VAGINA
/6)$5#43 !.$ /6)0!2)49
&IGURE &EMALE REPRODUCTIVE TRACTS OF 2AJA ERINACEA OVIPAROUS AND 3QUALUS ACANTHIAS VIVIPAROUS TO SHOW THE RELA
TIVE SIZES OF OVULATED AND ENCAPSULATED EGGS AND EMBRYOS &OLLICULAR CIRCUMFERENCE AT OVULATION IS INDICATED &ROM #ALLARD
AND +OOB REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
!BBREVIATIONS OV OVARY SG SHELL GLAND
&IGURE 0HOTOMICROGRAPH OF A SECTION OF THE SIMPLE CILIATED COLUMNAR EPITHELIUM C OF THE OVIDUCT OF THE !TLANTIC
GUITARlSH 2HINOBATOS LENTIGINOSUS !RROWS INDICATE SECRETORY CELLS IN THE CRYPT REGION "ASAL BODIES OF THE CILIARY ROOTLETS FORM
A DISTINCT LINE EXTENDING ACROSS THE APICAL REGIONS OF THE CELLS 8 &ROM (AMLETT ET AL B REPRODUCED WITH PERMISSION
OF THE .ORTH #AROLINA !CADEMY OF 3CIENCE
#(!04%2
&IGURE $RAWING OF A VERTICAL SECTION THROUGH A NON SECRETING OVIDUCTAL GLAND OF 3CYLLIORHINUS CANICULA 8 &ROM
-ETTEN REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
&IGURE $RAWINGS TO ILLUSTRATE THE ISTHMUS 6ERSCHLUVORRICHTUNG A SHORT CONSTRICTED SECTION OF THE OVIDUCT CONNECTING
THE OVIDUCTAL GLAND WITH THE UTERUS IN 3QUALUS ACANTHIAS &ROM 7IDAKOWICH REPRODUCED WITH PERMISSION FROM 5RBAN
&ISCHER 6ERLAG
!BBREVIATIONS ! UTERINE ARTERY AL- OUTER LONGITUDINAL MUSCLE OF THE OVIDUCT - MESENTERY O OVIDUCT 3 SEROSA 6 VENOUS
SPACE 5 UTERUS 6V ISTHMUS
/6)$5#43 !.$ /6)0!2)49
&IGURE %LASMOBRANCH EGG CASES &ROM 7EICHERT REPRODUCED WITH PERMISSION OF THE -C'RAW (ILL #OMPANIES
! 4HE DOGlSH 3CYLLIUM
" 4HE BULLHEAD SHARK (ETERDONTUS GALEATUS
&IGURE 2EPRESENTATIVE EGG CAPSULES OF OVIPAROUS SHARKS AND SKATES &ROM (AMLETT AND +OOB REPRODUCED
WITH PERMISSION OF THE *OHNS (OPKINS 5NIVERSITY 0RESS
! #EPHALOSCYLLIUM VENTRIOSUM
" (ETERODONTUS MEXICANUS
# "ATHYRAJA INTERRUPTA
#(!04%2
&IGURE 0HOTOGRAPH OF THE VENTRAL SURFACE OF A WHOLE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA !NTERIOR TENDRILS
FORM TWO HOOK
LIKE STRUCTURES WHERE THEY JOIN THE EGG CAPSULE BLACK ARROWS THE POSTERIOR TENDRILS CROSS AT APPROXIMATELY
WHITE ARROW 3CALE IN MILLIMETRES &ROM &ENG AND +NIGHT B REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
&IGURE 0HOTOGRAPH OF WHOLE EGG CAPSULES OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM +NIGHT &ENG AND 3TEWART
REPRODUCED WITH PERMISSION OF #AMBRIDGE 5NIVERSITY 0RESS ! RARE DOUBLE
YOLKER IS SHOWN AT THE LEFT ! SINGLE
YOLKED
CAPSULE IS SHOWN AT THE CENTRE AND A RARE ANOVULAR CAPSULE AT THE RIGHT
/6)$5#43 !.$ /6)0!2)49
&IGURE 0HOTOMICROGRAPHS OF ADJACENT CRYOSTAT SECTIONS SHOWING THE FOLDED STRUCTURE OF THE POSTERIOR MARGINAL SEAL
OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA ! 0EROXIDASE REACTION " $/0!
OXIDASE 4HE CAPSULE FROM WHICH
THESE SECTIONS WERE TAKEN WAS APPROXIMATELY HALF FORMED WITHIN THE OVIDUCTAL GLAND 4HE SEAL HAS A SIMILAR STRUCTURE AND
FUNCTION TO A CRIMPED WELD AND IS PROBABLY EXTENSIVELY CROSS
LINKED &ROM &ENG AND +NIGHT REPRODUCED WITH
PERMISSION FROM %LSEVIER 3CIENCE
#(!04%2
&IGURE 3EMIDIAGRAMMATIC DRAWINGS OF HALVED ACTIVELY SECRETING OVIDUCTAL GLANDS SHOWING STAGES IN THE FORMATION
OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM &ENG AND +NIGHT B REPRODUCED WITH PERMISSION FROM
THE 2OYAL 3OCIETY
! 2ESTING GLAND ! AND $ INDICATE ZONES OF GLANDULAR TUBULES
" &ORMATION OF THE POSTERIOR THIRD OF THE CAPSULAR WALL 4HE OVUM HAS YET TO ENTER THE LUMEN OF THE GLAND
# 0RESSURE OF THE OVUM ON THE OPENINGS OF THE !
ZONE TUBULES IS THOUGHT TO PREVENT SECRETION OF THE JELLY ALLOWING THE OVUM
TO BE ENCAPSULATED WHILE MOVING POSTERIORLY RELATIVE TO THE GLAND
$ 3ECRETION OF THE JELLY RESTARTS AFTER THE OVUM HAS PASSED THE !
ZONE OPENINGS BUT GRADUALLY REDUCES TO PRODUCE THE TAPERING
POSTERIOR TWO THIRDS OF THE CAPSULAR WALL 3CALE BAR MM
/6)$5#43 !.$ /6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE WALL OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS
CANICULA 4HE WALL IS A COMPOSITE MATERIAL CONSTRUCTED LARGELY OF COLLAGEN lBRES WITH A HIGHLY ORDERED KINKED MOLECULAR
ARRAGEMENT SET IN A MATRIX CONTAINING HYDROPHOBIC SPHERICAL lLLER PARTICLES M IN DIAMETER 8 &ROM +NIGHT AND
&ENG A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 4HE OUTERMOST LAYER , OF THE EGG CAPSULE SHOWING HYDROPHOBIC GRANULES $ 3OME REPEATS OF THE AXIAL PERIOD OF
THE lNE lBRILLAR PHASE OF THE COLLAGEN CAN BE SEEN BETWEEN THE TWO GRANULES
" !S IN ! ! HYDROPHOBIC GRANULE APPEARS TO LIE BETWEEN TWO SEGMENTS OF THE lNAL lBRILLAR PHASE 4HE BROAD LUCENT BAND
OF THE BANDING PATTERN APPEARS TO RUN ALL THE WAY AROUND THE GRANULE SUGGESTING THAT IT IS COATED WITH A COMPLETE LAYER OF
COLLAGEN MOLECULES
#(!04%2
&IGURE $IAGRAM OF A LONGITUDINAL SECTION OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA INDICATING
THE SOURCE OF THE VARIOUS SUBSTANCES INVOLVED IN TANNING OF THE EGG CAPSULE 4HE LAYERS OF THE CAPSULE ARE SHOWN ON THE RIGHT
FROM THE EXTERIOR , TO THE INTERIOR , 4HE ZONES OF THE GLAND FROM ! TO & ARE INDICATED &ROM 2USAOUN
)NNOCENT A
REPRODUCED WITH PERMISSION OF THE .2# 0RESS
!BBREVIATIONS #O CATECHOL OXIDASE $O $/0!
OXIDASE 0 POLYPHENOL 0O PEROXIDASE 4 TYROSINE
@
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE EGG
CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM 2US
AOUN
)NNOCENT A REPRODUCED WITH PERMISSION OF
THE .2# 0RESS 4HE OUTER LAYER , IS ABOUT M THICK
IN DEHYDRATED TANNED SPECIMENS IT CONSISTS OF lNE lBRILS
ABOVE DENSELY PACKED AMORPHOUS GRANULES RICH IN TYRO
SINE ,AYER , CONSTITUTES THE BULK OF THE WALL AND IS ABOUT
M THICK IT IS SIMILAR TO PLYWOOD AND CONSISTS OF ABOUT
LAMELLAE !LTHOUGH lNELY STRIATED , APPEARS MORE HO
MOGENEOUS THAN THE OTHER LAYERS AND IS ABOUT M THICK
4HE INNER LAYER , IS ONLY TO M THICK AND APPEARS
HOMOGENEOUS
! ,AYER , AND A PORTION OF , STAINED TO SHOW TYROSINE G
GRANULES 8
" ,AYERS , AND , STAINED TO SHOW TYROSINE 8
/6)$5#43 !.$ /6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH LAYER , OF THE NEWLY FORMED EGG CAPSULE OF THE DOGlSH
3CYLIORHINUS CANICULA 4HE LONGITUDINALLY SECTIONED SPINDLE
SHAPED COLLAGEN
CONTAINING lBRILS SHOW A PERIODICITY OF ABOUT
NM &ROM +NIGHT AND &ENG B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE $IAGRAMS ILLUSTRATING STRUCTURAL HIERARCHIES IN LAYER , OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA
&ROM +NIGHT AND &ENG B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 4HE COILED COLLAGEN MOLECULE IS FORMED OF THREE HELICAL PEPTIDE CHAINS TWISTED TOGETHER
" )T IS SUGGESTED THAT THE COLLAGEN MOLECULE IS NM LONG WITH A RELATIVELY LARGE hHEADv FORMED FROM HYDROPHOBIC NON
HELICAL PEPTIDES AND A SMALLER hTAILv FORMED IN THE SAME WAY 4HE CHAINS MAY BE ASSOCIATED HEAD
TO
TAIL TO FORM A TETRAMER
WITH A DUMBBELL SHAPE
# 4HE DUMBBELL SHAPED UNITS ARE CROSS
LINKED AND ALIGNED IN SUCH A WAY AS TO FORM CROSS STRIATIONS
$ &IBRILS TWIST TOGETHER TO FORM A lBRE
% 4HE lBRES ARE ARRANGED AT IN ADJACENT LAMINAE TO FORM A STRUCTURE SIMILAR TO PLYWOOD
#(!04%2
&IGURE $IAGRAM OF A VERTICAL LONGITUDINAL SECTION OF PART OF THE ACTIVELY SECRETING OVIDUCTAL GLAND OF THE DOGlSH
3CYLIORHINUS CANICULA &ROM +NIGHT &ENG AND 3TEWART REPRODUCED WITH PERMISSION OF #AMBRIDGE 5NIVERSITY
0RESS *ELLY * IS SECRETED FROM THE ! ZONE LAYERS , TO , OF THE CAPSULAR WALL ARE SECRETED FROM ZONES " TO % RESPECTIVELY
4HE OUTERMOST LAYER OF THE CAPSULE , IS LOWEST IN THE DRAWING :ONE & CONTRIBUTES LITTLE TO THE OUTER SURFACE OF THE EGG CAPSULE
&OR THE SAKE OF CLARITY ONLY THE EPITHELIUM SURROUNDING THE TUBULAR GLANDS LOWEST PARTS OF THE DRAWING HAS BEEN DRAWN
#4 CONNECTIVE TISSUE 3CALE BAR M
/6)$5#43 !.$ /6)0!2)49
&IGURE 3EMIDIAGRAMMATIC VIEW OF A QUARTER OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA 4HE LONGI
TUDINAL SURFACE AT THE LEFT IS SHADED AND SHOWS THE DISTRIBUTION OF GLANDS ! TO % 4HE LUMEN OF THE GLAND IS SHOWN TO THE RIGHT
WITH THE MORE SUPERlCIAL ZONES OF GLANDS & TO & $ ZONE GROOVES LIE BETWEEN THE $ FOLDS WHICH ENCIRCLE THE ENTIRE GLAND
3CALE BAR MM &ROM +NIGHT ET AL REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
#(!04%2
&IGURE
! 0HOTOGRAPH OF A lXED ACTIVELY SECRETING OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA 4HE GLAND HAS BEEN CUT IN
HALF AND THE JELLY AND OVUM HAVE BEEN REMOVED 4HE POSITION OF THE OVUM / CAN BE SEEN AS AN OVAL DILATION OF THE LUMEN
OF THE ANTERIOR OVIDUCT AND ANTERIOR PART OF THE OVIDUCTAL GLAND :ONES ! AND $ OF THE TUBULAR GLANDS ARE LABELLED ,ESS THAN
ONE
THIRD OF THE CAPSULE WALL # HAS BEEN FORMED 4HE LIMITS OF THE $
ZONE FOLDS DOWNWARD POINTING ARROWS AND !
ZONE
GLAND OPENINGS UPWARD POINTING ARROW CAN BE DISTINGUISHED IN THE LUMEN OF THE GLAND A ANTERIOR AXIS V VERTICAL AXIS
3CALE SHORT GRADATIONS MM
" 3CANNING ELECTRON MICROGRAPH OF A TRANSVERSE FRACTURE OF $
ZONE TUBULES 3ECRETION NARROW ARROW IS SEEN IN THE LUMINA
OF THE TUBULES 3PHERICAL SECRETORY GRANULES BROAD ARROW THOUGHT TO CONTAIN COLLAGEN ARE SEEN IN THE COLUMNAR EPITHELIAL
CELLS "AR M
&ROM +NIGHT AND &ENG REPRODUCED WITH PERMISSION FROM +LUWER !CADEMIC0LENUM 0UBLISHER
/6)$5#43 !.$ /6)0!2)49
&IGURE ! MORPHOLOGICAL BASIS HAS BEEN USED TO DIFFERENTIATE FOUR REGIONS OF THE OVIDUCTAL GLAND OF ELASMOBRANCHS
!T THE TOP IS A COMPOSITE LINE DIAGRAM OF A hGENERICv OVIDUCTAL GLAND CONSISTING OF FOUR ZONES CLUB PAPILLARY BAFmE AND
TERMINAL 4HE LOWER ILLUSTRATION SHOWS A UNIT OF THE BAFmE ZONE COMPRISING A GLANDULAR TUBULE SECRETORY DUCT SPINNERET WITH
BAFmE PLATES AND A TRANSVERSE GROOVE BETWEEN PLATEAU PROJECTIONS &ROM (AMLETT ET AL A REPRODUCED WITH PERMISSION
OF *OHN 7ILEY 3ONS )NC
#(!04%2
&IGURE -ICROGRAPHS OF SECTIONS THROUGH THE TUBULAR GLANDS OF :ONE $ IN THE OVIDUCTAL GLAND OF A DOGlSH &ROM
2USAOUN REPRODUCED WITH PERMISSION OF -ASSON 0ARIS
! 0HOTOMICROGRAPH 'RANULAR SECRETORY CELLS INTERSPERSED WITH COLUMNAR CILIATED CELLS ARE ABUNDANT 8
" 4RANSMISSION ELECTRON MICROGRAPH 4HE APICAL REGIONS OF THE SECRETORY CELLS #ILIATED COLUMNAR CELLS CL LIE BETWEEN
SECRETORY CELLS WITH LARGE MICROVILLI MVL 8
!BBREVIATIONS MT MITOCHONDRIA . NUCLEUS
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH A SECRETORY CELL IN :ONE $ OF THE OVIDUCTAL GLAND OF
THE DOGlSH 3CYLIORHINUS CANICULA 4HIS CELL DISPLAYS THE CHARACTERISTIC SPECIALIZATIONS FOR PROTEIN SECRETION EXTENSIVE GRANULAR
ENDOPLASMIC RETICULUM WELL DEVELOPED 'OLGI COMPLEX AND NUMEROUS SECRETORY GRANULES ARROWS 3MALL GRANULES NEAR THE
MATURING FACE ARROWS OF THE 'OLGI COMPLEX REACT TO THE PEROXIDASE REAGENT 4HE LETTERS ! " AND # INDICATE A TRANSITION IN
THE GRANULES AS THEY MOVE AWAY FROM THE 'OLGI COMPLEX 8 &ROM &ENG AND +NIGHT REPRODUCED WITH PERMISSION
FROM %LSEVIER 3CIENCE
/6)$5#43 !.$ /6)0!2)49
&IGURE $IAGRAM SHOWING A PART OF A SECRETORY CELL IN THE PROXIMAL PART OF A $ ZONE SECRETORY TUBULE OF THE OVIDUCTAL
GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA ! TENTATIVE SCHEME IS ILLUSTRATED FOR THE SEQUENCE OF CHANGES THOUGHT TO OCCUR DUR
ING STORAGE AND SECRETION OF PRO COLLAGEN 7ITHIN THE CISTERNAE OF THE ENDOPLASMIC RETICULUM THE COLLAGEN APPEARS ANISOTROPIC
BUT AS THE GRANULES MAKE THEIR WAY TO THE APICAL BORDER OF THE CELL IT BECOMES DEHYDRATED AND UNDERGOES A SERIES OF LIQUID
CRYSTAL TRANSFORMATIONS TO THEREBY PROVIDING A COMPACT WAY OF STORING COLLAGEN 4HE GRANULES APPEAR TO BE RELEASED INTO
THE TUBULE BY MEROCRINE SECRETION 4HE JUNCTIONAL COMPLEX UPPER RIGHT AND EXTENSIVE INTERDIGITATIONS OF THE LATERAL
MEMBRANES PROBABLY INDICATE THAT THIS EPITHELIUM IS ALSO ACTIVELY SECRETING IONS &ROM +NIGHT ET AL REPRODUCED WITH
PERMISSION FROM THE 2OYAL 3OCIETY
!BBREVIATIONS - SECRETED MATERIAL THAT FORMS A COALESCED STRAND . NUCLEUS
#(!04%2
&IGURE %LECTRON MICROGRAPHS FROM SECRETORY CELLS IN THE PROXIMAL PART OF A $ ZONE TUBULE OF THE OVIDUCTAL GLAND OF
THE DOGlSH 3CYLIORHINUS CANICULA 4HESE MICROGRAPHS ARE ARRANGED FROM LEAST ! TO MOST MATURE & TO ILLUSTRATE A TENTATIVE
SCHEME FOR THE SEQUENCE OF CHANGES IN GRANULES THOUGHT TO OCCUR DURING STORAGE AND SECRETION OF PRO COLLAGEN $URING THIS
TRANSFORMATION THE MATERIAL IN THE GRANULES BECOMES ARRANGED TO GIVE RISE TO A CONCENTRIC OR SPIRAL PATTERN #OMPARE THESE
lGURES WITH &IGURE &ROM +NIGHT ET AL REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
! " % & "AR M # $ "AR NM
/6)$5#43 !.$ /6)0!2)49
&IGURE $IAGRAM ILLUSTRATING THE SUGGESTED P( VALUES IN DIFFERENT PARTS OF THE OVIDUCTAL GLAND AND FORMING EGG CAPSULE
OF THE DOGlSH 3CYLIORHINUS CANICULA " REPRESENTS AN ENLARGEMENT OF THE RECTANGULAR BOX IN ! ARROW 4HE SECRETED MATERIAL IS
SHADED &INAL lBRILS lRST APPEAR & AFTER THE SECRETED MATERIAL HAS MOVED APPROXIMATELY M IN A POSTERIOR DIRECTION FROM
THE TRANSVERSE GROOVE OF ORIGIN &ROM &ENG AND +NIGHT A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
!BBREVIATIONS $ LUMEN OF SECRETORY DUCT ' TRANSVERSE GROOVE 4 LUMEN OF SECRETORY TUBULE
&IGURE 3CANNING ELECTRON MICROGRAPH OF $
ZONE FOLDS IN A FRACTURED SURFACE OF THE OVIDUCTAL GLAND OF THE DOGlSH
3CYLIORHINUS CANICULA ,AMELLAE WHICH GIVE RISE TO PART OF LAYER , OF THE CAPSULAR WALL ARE BEING EXTRUDED FROM THE TRANSVERSE
GROOVES OF THE $
ZONE ! LAMELLA CAN BE SEEN TO ARISE FROM THE CONmUENCE OF THREE mOWS ANTERIOR ! CENTRAL # AND POS
TERIOR 0 SEPARATED BY TWO BAFmE PLATES ! ANTERIOR AXIS 6 VERTICAL AXIS 3CALE BAR M &ROM +NIGHT AND &ENG
REPRODUCED WITH PERMISSION FROM +LUWER !CADEMIC0LENUM 0UBLISHER
#(!04%2
&IGURE 4HE FUNCTIONAL UNIT IN ALL PARTS OF THE OVI
DUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA CONSISTS OF
A SECRETORY TUBULE OF COLUMNAR SECRETORY CELLS INTERSPERSED
WITH SOME COLUMNAR CILIATED CELLS A SHORT DUCT LINED WITH
COLUMNAR CILIATED CELLS BUT LACKING SECRETORY CELLS AND A
SPINNERET ! SINGLE ROW OF SPINNERETS OPENS INTO THE BASE OF
EACH TRANSVERSE GROOVE IN ZONES " TO % &ROM +NIGHT &ENG
AND 3TEWART REPRODUCED WITH PERMISSION OF #AM
BRIDGE 5NIVERSITY 0RESS
! ! SIMPLIlED DRAWING OF AN INTERNAL CAST OF PART OF A SIN
GLE $
ZONE TRANSVERSE GROOVE VIEWED FROM THE POSTERIOR
SIDE TO SHOW THE STRUCTURE OF THE SPINNERETS WHICH SECRETE
THE BULK OF THE THICKNESS OF THE CAPSULAR WALL 4HE SECRE
TORY TUBULE 4 OPENS VIA A SHORT SECRETORY DUCT $ INTO
THE SPACE BETWEEN TWO OBLIQUE BAFmE PLATES " SHOWN
DOTTED
" ! DIAGRAMMATIC SECTION OF THE PLANE OUTLINED IN !
4WO BAFmE PLATES WHICH SEPARATE THE SECRETORY MATERIAL
INTO THREE mOWS ARE SHOWN 4HESE mOWS COALESCE IN THE
TRANSVERSE GROOVE 4HE SECRETED MATERIAL IN THE LUMEN OF
THE GLAND TUBULE 4 SECRETORY DUCT $ SPINNERET 3
AND THE TRANSVERSE GROOVE ' IS STIPPLED
&IGURE $IAGRAM ILLUSTRATING THE FUNCTIONAL UNIT
OF THE $ ZONE GLAND OF THE OVIDUCTAL GLAND OF THE DOGlSH
3CYLIORHINUS CANICULA ! LONG NONCOILED GLANDULAR TUBULE
'4 PASSES ITS SECRETION TO A SECRETORY DUCT 3$ &ROM THIS
THE SECRETION PASSES BETWEEN TWO BAFmE PLATES "0 WHICH
LIE AT AN ANGLE TO FORM THE SPINNERET 3 &ROM HERE THE SE
CRETION PASSES APICALLY THROUGH THE TRANSVERSE GROOVE 4'
TO GIVE RISE TO A SINGLE LAMELLA OF THE WHITE EGG CASE 7
4HE GLANDULAR TUBULE IS APPROXIMATELY M IN DIAMETER
&ROM +NIGHT ET AL REPRODUCED WITH PERMISSION FROM
THE 2OYAL 3OCIETY
/6)$5#43 !.$ /6)0!2)49
&IGURE -ICROGRAPHS OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM +NIGHT AND &ENG
REPRODUCED WITH PERMISSION FROM +LUWER !CADEMIC0LENUM 0UBLISHER
! 3CANNING ELECTRON MICROGRAPH LOOKING DOWN INTO TWO %
ZONE TRANSVERSE GROOVES WHICH RUN VERTICALLY UP THIS lGURE
4HE SPINNERETS IN THE BOTTOM OF THE GROOVE CONSIST OF A REGULAR ARRANGEMENT OF BAFmE PLATES 4HE SMALL ARROW INDICATES
THE OBLIQUE SPACE BETWEEN TWO BAFmE PLATES THE LARGE ARROW POINTS TO THE SPACE BETWEEN THE POSTERIOR SURFACE OF THE BAFmE
PLATE AND THE WALL OF THE TRANSVERSE GROOVE 3CALE BAR M
" 0HOTOMICROGRAPH OF A SECTION OF THE OVIDUCTAL GLAND SHOWING THE $
ZONE GROOVES BROAD ARROW BAFmE PLATES NARROW
ARROW SECRETORY DUCTS AND GLAND TUBULES WHITE ARROW 3CALE BAR M
#(!04%2
&IGURE #ONTINUED
# 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF THE APICAL PARTS OF THE BAFmE PLATES 6ISCOUS SECRETION IS THOUGHT TO mOW
VERTICALLY VERTICAL ARROW FROM THE APEX OF THE SPINNERETS AND OBLIQUELY ACROSS THE ANTERIOR AND POSTERIOR SURFACES
OBLIQUE ARROW #ILIA ARE ORIENTED IN THESE DIRECTIONS AND MAY HELP TO DIRECT THE mOWS 3CALE BAR M
A
&IGURE -ICROGRAPHS FROM THE OVIDUCTAL GLAND OF THE RAY 2AJA ERINACEA &ROM +NIGHT ET AL REPRODUCED WITH
PERMISSION FROM +LUWER !CADEMIC0LENUM 0UBLISHER
! 3CANNING ELECTRON MICROGRAPH OF A NATURAL CAST OF THREE $
ZONE SPINNERETS 4HE ARROWHEAD INDICATES THE DIRECTION OF mOW OF
MATERIAL -ATERIAL WITHIN THE LUMEN OF THE TUBULAR GLAND IS ROUGHLY CIRCULAR IN CROSS SECTION AS IT PASSES THROUGH THE SPIN
NERET IT DIVERGES SMOOTHLY AND EMERGES AS A mATTENED RIBBON 3CALE BAR M
" .OMARSKI MICROGRAPH OF A SINGLE ROW OF $
ZONE SPINNERETS !N OVERLAPPING ROW OF RIBBONS FUSED TOGETHER TO FORM A SINGLE
LAMELLA 4HE OVERLAPPING OF lVE RIBBONS AT EACH POINT OF THE LAMELLA GIVES RISE TO A PLYWOOD
LIKE CONSTRUCTION 2IBBONS FUSE
ALONG CURVED LINES TO FORM A LAMELLA ARROWS 4HE ARROWHEAD INDICATES THE DIRECTION OF mOW OF MATERIAL THROUGH THE SPIN
NERETS 3CALE BAR M
/6)$5#43 !.$ /6)0!2)49
#(!04%2
&IGURE #ONTINUED
# 3ELECTED IMAGES FROM A CONFOCAL Z
SERIES OF OPTICAL SECTIONS CUT PARALLEL TO THE PLANE OF A SINGLE LAMELLA IN AN AREA SIMILAR
TO THAT BOXED IN " 4HE lBRE AXIS AT ANY POINT EG THE TIP OF THE ARROW CAN BE SEEN TO PASS THROUGH lVE STEPPED ANTI
CLOCKWISE ROTATIONS FROM THE INNER LAMELLA A TO THE OUTER E CONlRMING THE PLYWOOD
LIKE CONSTRUCTION INFERRED FROM "
4HE CURVATURE OF THE lBRES CAN BE SEEN IN C AND E ARROWS
/6)$5#43 !.$ /6)0!2)49
&IGURE 0HOTOGRAPHS TO ILLUSTRATE FORMATION OF POSTERIOR TENDRILS IN THE MARGINAL TRENDRIL FORMING REGIONS OF THE % ZONE
OF THE NIDAMENTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM &ENG AND +NIGHT B REPRODUCED WITH PERMISSION FROM
THE 2OYAL 3OCIETY
! 3CANNING ELECTRON MICROGRAPH OF A TENDRIL FORMING IN AN ACTIVE RIGHT TENDRIL FORMING REGION ! SEPARATE DUCT JOINS THE MAIN
LUMEN AT THE POINT INDICATED BY THE BLACK ARROW AND CONTINUES AS THE MARGINAL CHANNEL WHITE ARROW WHICH RECEIVES OPENING
OF THE GLANDS OF THE & ZONE 3CALE BAR M
" 0ARAFlN SECTION OF AN ACTIVE RIGHT TENDRIL FORMING REGION FORMING THE PROXIMAL PART OF AN ANTERIOR TENDRIL 4 /NLY THE
POSTERIOR OR SO TRANSVERSE GROOVES ON THE DORSAL SIDE OF THE MARGINAL CHANNEL ARE ACTIVE AT THIS STAGE .O SECRETION IS SEEN
IN THE ANTERIOR GROOVES OR THE GROOVES ON THE VENTRAL SIDE 3CALE BAR M
# 0HOTOGRAPH OF A WHOLE OVIDUCTAL GLAND AND THE ANTERIOR PART OF THE POSTERIOR OVIDUCT OPENED WITH A VENTRAL MIDLINE
INCISION 4HE FORMING TENDRILS EMERGE FROM THE TENDRIL FORMING REGIONS BROAD ARROWS AND REMAIN UNCOILED UNTIL THEY REACH
THE POSTERIOR OVIDUCT 4HE TENDRIL APPEARS TO HANG RANDOMLY IN THE POSTERIOR OVIDUCT 4HE SMALL ARROWS INDICATE THE lRST
AND LAST TRANSVERSE GROOVES OF THE $
ZONE OF THE CAPSULAR WALL FORMING REGION 3CALE IN MILLIMETRES
!BBREVIATIONS ! ANTERIOR $ DORSAL 6 VENTRAL
#(!04%2
&IGURE $IAGRAMS ILLUSTRATING THE FORMATION AND STRUCTURE OF TENDRILS OF THE EGG CASE OF THE DOGlSH 3CYLIORHINUS
CANICULA &ROM &ENG AND +NIGHT B REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
! 4RANSVERSE SECTION OF A PORTION OF A TENDRIL SHOWING ITS LAMELLAR NATURE 4HE lBRIL ORIENTATION IS LONGITUDINAL IN THE BROAD
LAMINA " AND CIRCUMFERENTIAL IN THE NARROW LAMINA . 4HE SLIGHT PROGRESSIVE CHANGE OF ORIENTATION OF THE lBRILS WITHIN
THE BROAD LAMINA IS INDICATED DOTTED LINES &LUID
lLLED CANALICULI # AND LINES OF SMALL VOIDS ARROW ARE ENTRAPPED
BETWEEN THE LAMINAE 3CALE BAR M
" 4RANSVERSE SECTION OF A PART OF A FORMING TENDRIL SUGGESTING THAT CANALICULI # ARE FORMED BY THE INCOMPLETE ADHESION
OF A PLEATED LAMELLA , SECRETED FROM A TRANSVERSE GROOVE OF THE $
ZONE " IS A BROAD LAMINA . IS A NARROW LAMINA
3CALE BAR M
A
&IGURE 4HE GRAVID UTERUS OF THE SPINY DOGlSH 3QUALUS ACANTHIAS &ROM (AMLETT AND (YSELL REPRODUCED WITH
PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOGRAPH OF THE UTERUS OPENED TO SHOW LONGITUDINAL ROWS OF mAP
LIKE APPENDAGES ARROWS 4HE OVIDUCT O IS SHOWN AT
THE RIGHT %MBRYO SACS hCANDLESv CM IN TOTAL LENGTH HAVE BEEN REMOVED 3CALE IN CM
" 3CANNING ELECTRON MICROGRAPH OF A UTERINE mAP CONSISTING OF A THIN FOLD F AND A ROUNDED FREE EDGE
ON THE INNER SURFACE
OF THE UTERUS SHOWN ABOVE 8
/6)$5#43 !.$ /6)0!2)49
#(!04%2
&IGURE #ONTINUED
# 0HOTOMICROGRAPH OF A SECTION THROUGH A UTERINE mAP 4HE mAP CONTAINS A CORE OF CONNECTIVE TISSUE ARROW AND ITS ROUNDED
EDGE IS CREATED BY AN ARTERY
4HE EPITHELIA OF THE FOLD ITS ROUNDED EDGE A AND THE UTERINE LINING B ARE IDENTICAL
3MOOTH MUSCLE M OF THE UTERINE WALL IS SEEN AT THE LOWER RIGHT 8
$ %QUIVALENT SECTION TO hAv IN lGURE # 4HE EPITHELIUM HAS MICROVILLI ARROW IS VASCULARIZED
AND RESTS ON A CORE OF
COLLAGENOUS CONNECTIVE TISSUE PREDOMINANTLY COMPOSED OF COLLAGEN C 8
% %QUIVALENT SECTION TO hBv IN lGURE # 4HE EPITHELIUM IS VASCULARIZED
RESTS ON A LAYER OF COLLAGENOUS CONNECTIVE TISSUE
C AND IS SURROUNDED BY SMOOTH MUSCLE M 8
/6)$5#43 !.$ /6)0!2)49
&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH THE WALL OF THE GRAVID UTERUS OF THE SKATE 2AJA ERINACEA 4HE FOLDS OF
THE LINING ARE COVERED WITH A SIMPLE COLUMNAR CILIATED EPITHELIUM E AND HAVE A CORE OF RICHLY VASCULAR LOOSE CONNECTIVE TISSUE
4HE ARROWHEAD POINTS TO A FEW CILIA ON THE EPITHELIAL CELLS !STERISKS INDICATE ABUNDANT BLOOD VESSELS IN THE SUBMUCOUS CONNEC
TIVE TISSUE 8 &ROM (AMLETT AND (YSELL REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
!BBREVIATIONS C SECRETORY CRYPTS BETWEEN THE FOLDS P SUBMUCOUS CONNECTIVE TISSUE
&IGURE -ICROGRAPHS OF THE UTERINE LINING OF THE LITTLE SKATE 2AJA ERINACEA &ROM +OOB AND (AMLETT REPRO
DUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! " 3CANNING ELECTRON MICROGRAPHS SHOWING THE RICHLY VASCULAR BRANCHING LONGITUDINAL FOLDS
IN THE LINING OF THE UTERUS
'LANDS G OPEN INTO THE UTERINE SLITS 4HE ARROWHEAD INDICATES SECRETORY GLAND CELLS
#(!04%2
&IGURE #ONTINUED
# ,IGHT MICROGRAPH OF A SECTION THROUGH THE RICHLY VASCULAR
UTERINE WALL 4HE DENSE COVERING OF CILIA ARROW SUBTENDS
WELL DElNED BASAL BODIES BENEATH UNDULATING ARROW 8
$ 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH SECRETORY CELLS IN THE EPITHELIUM LINING THE UTERUS
4HE CHARACTERISTICS OF ACTIVE SECRETION ARE EVIDENT IN THESE CELLS MICROVILLI V SECRETORY VESICLES
MITOCHONDRIA M
GRANULAR ENDOPLASMIC RETICULUM ER 'OLGI COMPLEX G AND LATERAL MEMBRANE FOLDS F ENCLOSING INTERCELLULAR CHANNELS
! CAPILLARY LINED BY ENDOTHELIAL CELLS E AND ENCLOSED BY ITS BASAL LAMINA B COURSES THROUGH THE BOTTOM OF THE MI
CROGRAPH 4HE CAPILLARY IS SEPARATED FROM THE EPITHELIUM BY A DELICATE LAYER OF LOOSE CONNECTIVE TISSUE AND THE EPITHELIAL
BASAL LAMINA B 4HE ARROWHEAD INDICATES A CROSS SECTION OF A COLLAGEN BUNDLE 8
/6)$5#43 !.$ /6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EPITHELIUM OF THE UTERINE LINING OF THE LITTLE SKATE
2AJA ERINACEA &ROM +OOB AND (AMLETT REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 3ECTION THROUGH COLUMNAR SURFACE CELLS SHOWING CILIA C BASAL BODIES ARROWHEAD STRIATED ROOTLET lBRES ARROW
AND ELABORATE INTERCELLULAR FOLDS
4HE BASAL LAMINA OF THE EPITHELIUM B AND THE BASAL LAMINA OF THE ENDOTHELIUM B
ENCLOSE A DELICATE LAYER OF LOOSE CONNECTIVE TISSUE E ENDOTHELIUM M MITOCHONDRIA 8
#(!04%2
&IGURE #ONTINUED
" 4HIS SECTION SHOWS WELL DEVELOPED JUNCTIONAL COMPLEXES SEALING THE INTERCELLULAR CHANNELS IN THE UTERINE EPITHELIUM FROM
THE LUMEN 4HE JUNCTIONS COMPRISE A ZONULA OCCLUDENS O ZONULA ADHAERENS A AND A MACULA ADHAERENS OR DESMOSOME
D !LSO SHOWN ARE MICROVILLI M AND CILIA C WITH THEIR BASAL BODIES ARROWHEAD 8
&IGURE $IAGRAM TO ILLUSTRATE THE MECHANISM OF TANNING IN THE EGG CAPSULE OF THE LITTLE SKATE 2AJA ERINACEA 4HE EGG
CAPSULE IS WHITE WHEN IT LEAVES THE OVIDUCTAL GLAND AND CONTAINS NO CATECHOLIC SUBSTANCE ALTHOUGH AN INACTIVE FORM OF THE EN
ZYME CATECHOL OXIDASE IS INCORPORATED INTO THE MATRIX DURING SECRETION 4ANNING OCCURS AS THE EGG PASSES INTO THE UTERUS WHERE
CATECHOLS BEGIN TO ACCUMULATE IN THE CAPSULAR MATERIAL AND ARE OXIDIZED UNDER THE INmUENCE OF CATECHOL OXIDASE TO QUINONES
4HE OXYGEN REQUIRED FOR THIS TANNING IS TRANSPORTED FROM THE MATERNAL CIRCULATION BY THE UTERUS &ROM +OOB AND #OX
REPRODUCED WITH PERMISSION OF THE #AMBRIDGE 5NIVERSITY 0RESS
/6)$5#43 !.$ /6)0!2)49
&IGURE $IAGRAM TO ILLUSTRATE THE SEQUENCE OF DEPOSITION AND BINDING OF CALCIUM AND MAGNESIUM DURING FORMATION AND
TANNING IN THE EGG CAPSULE OF THE LITTLE SKATE 2AJA ERINACEA &ROM +OOB REPRODUCED WITH PERMISSION OF THE !MERICAN
3OCIETY OF )CHTHYOLOGISTS AND (ERPETOLOGISTS
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE UTERINE WALL OF THE SANDTIGER SHARK #ARCHARIAS TAURUS &ROM (AMLETT AND
(YSELL REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! .ONGRAVID UTERUS 4HE SURFACE EPITHELIUM HAS MICROVILLI M AND IS SUPPORTED BY SEVERAL LAYERS OF mATTENED CELLS CONTAINING
PROMINENT CYTOPLASMIC lLAMENTS ARROWS "ELOW THIS LAYER IS A ZONE OF ROUNDED CELLS CONTAINING FROTHY VESICLES V AND
A BLOOD VESSEL
8
" 'RAVID UTERUS 4HIS FOLD IS FROM A UTERUS THAT CONTAINED EGGS AND EMBRYOS 4HE DEVELOPMENT OF LONGITUDINAL FOLDS HAS
INCREASED THE EPITHELIAL SURFACE AREA OVER THAT SHOWN IN ! "LOOD VESSELS
HAVE ENLARGED 8
#(!04%2
&IGURE -ICROGRAPHS OF SECTIONS THROUGH THE UTERINE WALL OF GRAVID YELLOW SPOTTED STINGRAYS 5ROLOPHUS JAMAICENSIS
&ROM (AMLETT AND (YSELL REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF A LONGITUDINAL SECTION OF A TROPHONEMA FROM A GRAVID FEMALE 3ECRETORY CRYPTS C ALTERNATE WITH EPI
THELIAL RIDGES R ! THIN LAMINA PROPRIA MUCOSAE P SEPARATES THE EPITHELIUM FROM THE CORE BLOOD VESSEL
8
" 4RANSMISSION ELECTRON MICROGRAPH OF AN EPITHELIAL RIDGE OF A TROPHONEMA 4HE SIMPLE SQUAMOUS EPITHELIAL CELLS SE DISPLAY
A FEW MICROVILLI M AND REST ON A THIN BASAL LAMINA B WHICH IS SEPARATED FROM A BLOOD VESSEL
BY A LAMINA PROPRIA
MUCOSAE OF DELICATE LOOSE CONNECTIVE TISSUE P 0INOCYTOTIC VESICLES ARROWHEAD ARE ABUNDANT WITHIN THE ENDOTHELIAL CELL
!N ERYTHROCYTE RBC IS INDICATED IN THE BLOOD VESSEL 8
# 0HOTOMICROGRAPH OF A LONGITUDINAL SECTION OF A TROPHONEMA FROM A GRAVID FEMALE %ACH SURFACE RIDGE CONTAINS A VASCULAR
BRANCH
BELOW A SIMPLE SQUAMOUS EPITHELIUM ARROWHEADS 4HE SIMPLE COLUMNAR EPITHELIAL CELLS OF THE CRYPTS C CON
TAIN APICAL SECRETORY VESICLES S AND ARE SEPARATED FROM THE SUBJACENT BLOOD SUPPLY
BY THE DELICATE CONNECTIVE TISSUE OF
THE LAMINA PROPRIA MUCOSAE P 8
$ 4RANSMISSION ELECTRON MICROGRAPH OF A TROPHONEMA FROM A GRAVID FEMALE 3ECRETORY CELLS CONTAIN GRANULAR ENDOPLASMIC
RETICULUM ER 'OLGI COMPLEXES G AND SECRETORY VESICLES S ! BLOOD VESSEL
IS SHOWN AT THE LOWER LEFT 8
/6)$5#43 !.$ /6)0!2)49
#(!04%2
&IGURE #ONTINUED
% 4RANSMISSION ELECTRON MICROGRAPH OF EPITHELIAL CELLS FROM THE SURFACE OF A TROPHONEMA 4HE CELLS ARE JOINED APICALLY BY
TIGHT JUNCTIONS CIRCLE AND DISPLAY MICROVILLI M 4HEY CONTAIN THE ORGANELLES INDICATIVE OF ACTIVE SECRETION GRANULAR ENDO
PLASMIC RETICULUM ER AND 'OLGI COMPLEXES G 4WO TYPES OF SECRETORY VESICLES ARE PRESENT LARGE VESICLES WITH mOCCULENT
CONTENTS V AND SMALLER VESICLES WITH ELECTRON
DENSE CONTENTS V 8
/6)$5#43 !.$ /6)0!2)49
&IGURE -ICROGRAPHS OF SECTIONS OF THE UTERINE WALL OF THE !TLANTIC SHARPNOSED SHARK 2HIZOPRIONODON TERRAENOVAE
&ROM (AMLETT AND (YSELL REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! "EFORE IMPLANTATION AN EMBRYO RESIDES IN ITS OWN UTERINE COMPARTMENT UC )T IS NOURISHED BY THE CONTENTS OF ITS YOLK SAC
Y THAT ARE CONVEYED TO THE EMBRYO BY WAY OF THE YOLK STALK ARROWHEAD
" 0HOTOMICROGRAPH OF A SECTION THROUGH THE WALL OF THE UTERINE COMPARTMENT SHOWING ITS SMOOTH LINING OF SIMPLE COLUMNAR
EPITHELIUM E RESTING ON A RICH VASCULAR BED
.OTE THE SECRETORY BLEBS ARROWHEAD ON THE EPITHELIAL CELLS 8
# 4HIS TRANSMISSION ELECTRON MICROGRAPH THROUGH THE EPITHELIUM OF A UTERINE COMPARTMENT ILLUSTRATES MICROVILLI M
MEROCRINE SECRETORY VESICLES V MEROCRINE SECRETION ARROWHEAD AND APOCRINE SECRETORY BLEBS A 8
#(!04%2
&IGURE #ONTINUED
$ 0HOTOMICROGRAPH OF A TERM UTERUS AND FOETAL PORTION OF THE PLACENTA 4HE FOETAL PLACENTA P HAS A DENSE VASCULAR BED
AND IS SEPARATED BY THE EGG ENVELOPE EE FROM THE UTERUS U WHICH ALSO HAS A DENSE VASCULAR BED
8
% 4RANSMISSION ELECTRON MICROGRAPH SHOWING THE FOETAL PORTION OF THE PLACENTA P WITH ITS PLACENTAL VASCULAR BED
P
ABUTTING THE EGG ENVELOPE EE AND THE UTERUS U WITH ITS VASCULAR BED
U SEPARATED FROM THE EGG ENVELOPE 8
#(!04%2
6)6)0!2)49
HAS THE MOTHER LAID DOWN YOLK DURING VITELLOGENESIS
BUT SHE SUPPLIES ADDITIONAL NUTRIENTS DURING EMBRYONIC
DEVELOPMENT 7ITH THE ESTABLISHMENT OF MATROTROPHY
VARIOUS ELABORATE STRUCTURES HAVE EVOLVED ALWAYS FROM
PREEXISTING STRUCTURES THAT FACILITATE NUTRIENT TRANSFER
DURING GESTATION 'ROVE AND 7OURMS
4HIS TRANSFER OF NUTRIENTS IS ACHIEVED IN SEVERAL
WAYS 7OURMS 'ROVE AND ,OMBARDI )N THE
SIMPLEST TERMED EITHER //0(!'9 OR !$%,0(/0(!'9
SOME EMBRYOS OF THE BROOD PREY ON THEIR SIBLINGS EI
THER AS EGGS OR AS EMBRYOS -ORE ADVANCED TRANSFER
IS BY WAY OF 42/0(/$%2-9 WHERE RICHLY VASCULARIZED
ELABORATIONS OF MATERNAL AND EMBRYONIC EPITHELIA AL
THOUGH NOT IN INTIMATE ASSOCIATION FACILITATE EXCHANGE
ACROSS INTERTISSUE SPACES )N A THIRD TYPE OF MATROP
ROPHIC ADAPTATION 0,!#%.4/42/0(9 MATERNAL NUTRIENTS
ARE TRANSFERRED TO THE EMBRYO BY WAY OF A 0,!#%.4!
WHICH MAY BE DElNED AS THE INTIMATE APPOSITION OR
FUSION OF MATERNAL AND FOETAL ORGANS FOR PHYSIOLOGICAL
EXCHANGE /NE TYPE OF PLACENTOTROPHY IS FOUND ONLY
IN SHARKS THE 9/,+ 3!# 0,!#%.4! WHICH CONSISTS OF A
MODIlED YOLK SAC CLOSELY APPOSED TO THE UTERINE EPI
THELIUM 4HIS STRUCTURE FUNCTIONS IN THE ABSORPTION OF
YOLK DURING EARLY GESTATION LATER IT BECOMES MODIlED
AS THE FOETAL PORTION OF THE PLACENTA /THER PLACENTAL
RELATIONSHIPS HAVE BEEN CITED INCLUDING THE &/,,)#5
,!2 0,!#%.4! AN INTIMATE ASSOCIATION BETWEEN THE
FOLLICULAR WALL AND EMBRYONIC SURFACES "5##!, !.$
"2!.#()!, 0,!#%.4!3 WHERE RICHLY VASCULAR EXTENSIONS
OF MATERNAL TISSUE GROW INTO THE FOREGUT OF THE FOETUS
AND THE 42/0(/4!%.)!, 0,!#%.4! WHERE ELABORATE OUT
GROWTHS OF THE HINDGUT OF THE FOETUS THE 42/0(/4!%
.)!% ABSORB NUTRIENTS PROVIDED BY THE OVARIAN LUMINAL
EPITHELIUM
)T IS OFTEN DIFlCULT NOT TO OVERSTEP THE LINE SEPARAT
ING THE REALMS OF HISTOLOGY AND EMBRYOLOGY THIS DIS
TINCTION BECOMES ESPECIALLY TENUOUS IN A DISCUSSION OF
VIVIPARITY &OR THE MOST PART DEVELOPMENTAL CONSIDER
ATIONS HAVE BEEN OMITTED FROM THE PRESENT WORK EXCEPT
WHERE THEY MAY CAST LIGHT ON THE NATURE OF A MATURE
)NTRODUCTION
6IVIPARITY IS A PROCESS IN WHICH EGGS ARE FERTILIZED IN
TERNALLY AND UNDERGO DEVELOPMENT WITHIN THE MATERNAL
REPRODUCTIVE SYSTEM 7OURMS 'ROVE AND ,OMBAR
DI !LTHOUGH MOST lSHES ARE OVIPAROUS
FAMILIES OF LIVING lSHES HAVE SPECIES THAT BEAR LIVING
YOUNG THESE INCLUDE FAMILIES OF CHONDRICHTHYANS
THE SINGLE COELACANTH ,ATIMERIA CHALUMNAE AND
FAMILIES OF TELEOSTS 7HILE AS MANY AS OF TO
SPECIES OF CHONDRICHTHYANS PRACTICE VIVIPARITY
ONLY OF AN ESTIMATED SPECIES OF TELEOSTS
DO SO /NE EXPLANATION FOR THIS DISPARITY MAY BE THAT
TELEOSTS LACK -LLERIAN DUCTS WHICH ARE USED AS BROOD
CHAMBERS IN OTHER VIVIPAROUS VERTEBRATES 7AKE
3CHINDLER AND (AMLETT 4HE TELEOSTS HOWEVER
HAVE SHOWN GREAT RESOURCEFULNESS IN MAKING OTHER AR
RANGEMENTS FOR THE INTERNAL CARE OF THEIR YOUNG AND
GESTATION OCCURS WITHIN THE OVARY ITSELF
)N THE EVOLUTION OF VIVIPARITY THERE HAS BEEN A TEN
DENCY AWAY FROM A DEPENDENCY OF THE EMBRYO ON ITS
OWN YOLK RESERVES TO A GREATER RELIANCE ON NUTRIENTS
SUPPLIED BY THE MOTHER THEREBY ESTABLISHING THE DIS
TINCTION BETWEEN ,%#)4(/42/0(9 AND -!42/42/0(9 )N
LECITHOTROPHY LITTLE OR NO NUTRIENT MATERIAL CROSSES TO
THE EMBRYO FROM THE MATERNAL CIRCULATION AND ALL OR
NEARLY ALL OF THE SUBSTRATES FOR GROWTH AND METABO
LISM ARE OBTAINED FROM YOLK RESERVES STORED IN THE EGG
PRIOR TO FERTILIZATION 'ROVE AND 7OURMS
(OLLENBERG AND 7OURMS $URING GESTATION
LECITHOTROPHIC EMBRYOS UNDERGO A LOSS IN WEIGHT OF OR
GANIC MATERIAL SIMILAR TO THAT WHICH TAKES PLACE DURING
THE DEVELOPMENT OF OVIPAROUS lSHES )N MATROTROPHY
HOWEVER YOLK RESERVES ARE SUPPLEMENTED DURING GES
TATION BY MATERIALS PROVIDED BY THE MOTHER NOT ONLY
! CLASSIC SERIES OF PAPERS ON VIVIPARITY IN lSHES WAS PUBLISHED
BETWEEN AND BY #, 4URNER AND IS LISTED IN THE ,ITERATURE
#ITED THIS WORK FORMED A SOLID BASIS FOR THE LATER RESEARCH THAT IS
CITED IN THIS SECTION
#(!04%2
ORGAN &OETAL STRUCTURES SUCH AS GILLS THE GUT AND
SKIN HAVE BEEN INCLUDED ONLY WHERE THEY COMBINE
WITH MATERNAL TISSUES TO FORM A MORE OR LESS DISCRETE
ORGAN THE 0,!#%.4!
6IVIPARITY IN %LASMOBRANCHS
6IVIPARITY IS THE DOMINANT FORM OF REPRODUCTION AMONG
ELASMOBRANCHS ESPECIALLY THE SHARKS AND RAYS WHERE AN
EVOLUTIONARY TRANSITION SHOWS INCREASING DEPENDENCE
ON THE MOTHER DURING DEVELOPMENT 7OURMS
(AMLETT 7OURMS 'ROVE AND ,OMBARDI
(AMLETT AND +OOB /VIPAROUS SPECIES DEVELOP
INDEPENDENTLY OF THE MOTHER THEY ARE LECITHOTROPHIC
AND ARE COMPLETELY DEPENDENT ON THE YOLK RESERVES
CONTAINED WITHIN THEIR YOLK SACS 3OME VIVIPAROUS SPE
CIES ARE ALSO LECITHOTROPHIC AND ALTHOUGH THEY DEVELOP
WITHIN THE UTERUS THEY ALSO DEPEND ON THEIR OWN YOLK
RESERVES THE MOTHER SIMPLY PROVIDES PHYSICAL PROTEC
TION FOR HER BROOD AND PERMITS THE NECESSARY RESPIRA
TORY EXCHANGES &IGURE 4HE MOST EFlCIENT ROUTE
FOR NUTRIENT TRANSFER OCCURS IN FOETAL SHARKS AND RAYS
BY WAY OF ()34/42/0( A NUTRIENT mUID PROVIDED BY THE
TISSUES OF THE MOTHER 7OURMS 7ITH THE ESTAB
LISHMENT OF THE YOLK SAC PLACENTA IN #ARCHARHINIDAE
AND 3PHYRNIDAE HAEMATROPHIC EXCHANGE PROVIDES NU
TRIENTS DIRECTLY FROM THE MATERNAL TO FOETAL CIRCULATION
6IVIPAROUS DEVELOPMENT IN ELASMOBRANCHS IS EITHER
!0,!#%.4!, WHERE NO MORPHOLOGICALLY DEFINITIVE VAS
CULAR EXCHANGE ORGAN IS FORMED OR 0,!#%.4!, WHERE
A MATERNAL
FOETAL EXCHANGE ORGAN IS FORMED (AMLETT
AND (YSELL
!LTHOUGH THE OVARIES AND OVIDUCTS BEGIN DEVELOP
MENT AS PAIRED STRUCTURES THEY OFTEN BECOME ASYM
METRICAL IN ADULTS AND IN SOME VIVIPAROUS SHARKS THE
RIGHT OVARY IS FUNCTIONAL AND THE LEFT ATROPHIES 7OUR
MS .EVERTHELESS BOTH OVIDUCTS ARE PRESENT
!MONG VIVIPAROUS RAYS THE RIGHT OVARY AND OVIDUCT
UNDERGO VARYING DEGREES OF REDUCTION OR LOSS 4HE OVI
DUCT OF ELASMOBRANCHS ORIGINATES AS A SIMPLE TUBULAR
-LLERIAN DUCT WHICH THEN UNDERGOES REGIONAL DIFFER
ENTIATION
$URING OVULATION AN OVUM IS EXPELLED FROM THE
OVARY INTO THE COELOM DRAWN INTO THE /34)5- 45"!%
AND TRANSMITTED DOWN ONE OF THE TWO OVIDUCTS &IGURE
!S IT PASSES THE /6)$5#4!, OR 3(%,, ',!.$ IT IS
FERTILIZED AND ENVELOPED IN AN OVERSIZED AMBER
CO
LOURED %'' #!035,% THAT IT WILL EVENTUALLY hGROW INTOv
AS IT DEVELOPS 4HE EGG CAPSULE IS A TERTIARY MEMBRANE
OF STOUT CONSTRUCTION IN OVIPAROUS FORMS ABLE TO WITH
STAND THE RIGOURS OF LIFE OUTSIDE THE MOTHER 7OURMS
'ROVE AND ,OMBARDI (AMLETT ! MORE
DELICATE EGG CAPSULE SURROUNDS VIVIPAROUS EMBRYOS
AND APPEARS TO CONTAIN A UNIQUE FORM OF COLLAGEN OR
A COLLAGEN
LIKE PROTEIN WHERE THE BANDING PATTERN
CHARACTERISTIC OF COLLAGEN MAY BE ABSENT 4HE CAP
SULE ESTABLISHES TWO SUBCOMPARTMENTS THE 54%2).%
#/-0!24-%.4 AND 0%2)&/%4!, #/-0!24-%.4 &IGURES
AND AND MAY BE RETAINED THROUGHOUT GESTA
TION EVEN BEING INCORPORATED INTO THE PLACENTA ALTER
NATIVELY THE EMBRYO MAY EMERGE FROM IT TO COMPLETE
DEVELOPMENT UNCONlNED WITHIN THE UTERINE LUMEN
)N ONLY ONE SPECIES 0RIONACE GLAUCA HAS THE AB
SENCE OF AN EGG CAPSULE BEEN NOTED /TAKE AND -IZUE
4HE VIVIPAROUS EMBRYO ENCLOSED IN ITS OVERSIZED
EGG CAPSULE PASSES INTO THE ENLARGED LOWER REGION
OF THE OVIDUCT THAT IS MODIlED TO FORM A 54%253
&IGURE (AMLETT #ASTRO AND 7OURMS
(AMLETT AND (YSELL %XCESS EGG CAPSULE
IS FOLDED INTO A NEAT PACKAGE AND STORED IN A DIVER
TICULUM OF THE UTERINE WALL THE -%-"2!.% 2%3%26/)2
&IGURES AND 4ESHIMA AND -IZUE
(AMLETT 7OURMS AND (UDSON C ,OMBARDI AND
&ILES !S THE FOETUS GROWS ITS INCREASING SIZE IS
ACCOMMODATED BY MEMBRANE PAID OUT FROM THE RES
ERVOIR !T TERM ALL OF THE MEMBRANE WILL HAVE BEEN
WITHDRAWN TO ENCLOSE THE FULL
SIZED FOETUS AND THE LU
MEN OF THE RESERVOIR BECOMES CONmUENT WITH THAT OF
THE UTERUS
3EVERAL EMBRYOS MAY BE ACCOMMODATED WITHIN
THE UTERI OF SOME SHARKS $URING THE INITIAL MONTHS OF
GESTATION EACH EMBRYO ENCLOSED IN ITS OWN EGG CAP
SULE MAY BE SURROUNDED BY DORSOLATERAL AND VENTRO
MEDIAL FOLDS OF THE UTERINE WALL THAT SPAN THE LUMEN TO
FORM 54%2).% #/-0!24-%.43 EACH OF WHICH CONTAINS
ONE EMBRYO WITHIN ITS SURROUNDING EGG CAPSULE &IG
URES AND 3CHLERNITZAUER AND 'ILBERT
(AMLETT 7OURMS 'ROVE AND ,OMBARDI
#ASTRO AND 7OURMS (AMLETT ET AL A
/NLY A FEW APLACENTAL SHARKS DEVELOP UTERINE COMPART
MENTS EG 'ALEUS CANIS -USTELUS VULGARIS
!0,!#%.4!, 6)6)0!2)49 ).
%,!3-/"2!.#(3
$EPENDING UPON THE AMOUNT OF YOLK CONTAINED WITH
IN THE OVA OF VIVIPAROUS EMBRYOS THERE IS A VARIABLE
PERIOD OF DEPENDENCE ON THE MOTHER FOR SUSTENANCE
7OURMS 7OURMS 'ROVE AND ,OMBARDI
6)6)0!2)49
(AMLETT AND (YSELL 4HE FOETUS MAY BE
WHOLLY ,%#)4(/42/0()# AND RETAIN ITS INDEPENDENCE
BY UTILIZING ITS OWN YOLK RESOURCES THROUGHOUT GESTA
TION UNDERGOING CONSIDERABLE NET LOSS IN DRY WEIGHT
DURING DEVELOPMENT !LTERNATIVELY EMBRYOS MAY
OBTAIN NUTRIENTS BY PREYING ON THEIR SIBLINGS WITHIN
THE UTERUS EITHER CONSUMING OVULATED EGGS //0(!'9
OR CANNIBALIZING DEVELOPING EMBRYOS !$%,0(/0(!'9
)N CONTRAST TO OTHER VIVIPAROUS SHARKS OVULATION CON
TINUES THROUGHOUT GESTATION IN MOST OOPHAGOUS SPE
CIES PROVIDING A STEADY FOOD SUPPLY FOR THE DEVELOPING
FOETUSES 7OURMS 'ROVE AND ,OMBARDI
)N APLACENTAL YOLK SAC VIVIPARITY THE MOTHER PRO
VIDES FOR RESPIRATORY EXCHANGE AND THE REGULATION
OF WATER AND ELECTROLYTES SHE DOES NOT NECESSARILY
PROVIDE NUTRIENTS DIRECTLY BUT MAY SIMPLY CREATE A
FELICITOUS ENVIRONMENT FOR GESTATION (YPERTROPHY
OF SMOOTH MUSCLE OF THE WALL AS WELL AS INCREASES IN
ITS CONNECTIVE TISSUE LAYERS ADAPT THE UTERUS FOR ITS
BURDEN OF A LONG GESTATION 2ESPIRATORY EXCHANGE IS
ACCOMMODATED BY AN INCREASE IN VASCULARIZATION OF
THE UTERUS AND A REDUCTION IN THE TISSUE BARRIERS
BETWEEN THE MATERNAL BLOOD AND THE UTERINE LUMEN
)N THE SPINY DOGlSH 3QUALUS ACANTHIAS WHERE DE
VELOPMENT IS LECITHOTROPHIC THE EGGS AND THEIR JELLY
ARE ENCAPSULATED WITHIN A THIN MEMBRANE THE #!.$,%
WHICH IS CLOSELY APPOSED TO THE UTERINE WALL 4HE
CANDLE RUPTURES ABOUT HALFWAY THROUGH GESTATION AND
THE EMBRYOS COMPLETE DEVELOPMENT IN THE UTERINE
mUIDS 4HE AREA OF THE UTERINE RESPIRATORY SURFACE IS
INCREASED BOTH BY THE DILATION NECESSARY TO ACCOM
MODATE THE EMBRYOS AND ALSO BY THE DEVELOPMENT OF
LONGITUDINAL FOLDS OR 25'!% &IGURES ! " *OLLIE
AND *OLLIE B (AMLETT AND (YSELL 4HESE
HAVE A CORE OF LOOSE RICHLY VASCULAR CONNECTIVE TIS
SUE WHOSE CAPILLARIES RADIATE FROM A CENTRAL ARTERIOLE
&IGURES # TO % AND ! # 4HE CAPILLARIES
INSINUATE THEMSELVES BETWEEN THE BASES OF THE EPI
THELIAL CELLS THEREBY REDUCING THE BARRIER TO GASEOUS
EXCHANGE !LTHOUGH THEY APPEAR TO BE INTRAEPITHELIAL
THE CAPILLARIES ARE SEPARATED FROM THE EPITHELIAL CELLS
BY A DELICATE BASAL LAMINA PRESUMABLY DERIVED FROM
BOTH THE ENDOTHELIUM AND EPITHELIUM NO OTHER STRO
MAL ELEMENTS INTERVENE &IGURES " $ 4HE LUMI
NAL EPITHELIUM SIMPLE COLUMNAR IN THE NON PREGNANT
UTERUS BECOMES STRATIlED CUBOIDAL ITS MICROVILLOUS
BORDER SUGGESTS AN OSMOREGULATORY FUNCTION #ONSPIC
UOUS EXTRACELLULAR COMPARTMENTS SEPARATING THE LAYERS
AND JUNCTIONAL COMPLEXES BETWEEN THE APICAL BORDERS
OF ADJACENT JUXTALUMINAL EPITHELIAL CELLS MAY INDICATE
ACTIVE TRANSPORT &IGURES # & ' ( 4HE APICAL
CYTOPLASM OF THE JUXTALUMINAL CELLS IS PACKED WITH
SMOOTH SURFACED ELECTRON LUCENT VACUOLES &IGURE
( 3INCE THESE ARE CONlNED TO THE APICAL REGIONS
OF THE EPITHELIUM THEY DO NOT APPEAR TO BE INVOLVED
IN TRANSPORT ACROSS THE BARRIER 2ESPIRATORY EXCHANGE
OCCURS ACROSS THE ECTODERM OF THE YOLK SAC FOR ONLY A
BRIEF PERIOD IN EARLY DEVELOPMENT BEFORE THE DEVELOP
MENT OF EXTERNAL GILLS *OLLIE AND *OLLIE A /NLY
A THIN LAYER OF ONE OR TWO NON KERATINIZED SQUAMOUS
ECTODERMAL CELLS SPARSE UNDERLYING CONNECTIVE TISSUE
AND THIN ENDOTHELIAL CELLS RESIST RESPIRATORY EXCHANGE
BETWEEN THE UTERINE LUMEN AND THE VITELLINE CAPILLAR
IES BOTH THE EPITHELIAL AND ENDOTHELIAL CELLS DISPLAY AC
TIVE PINOCYTOSIS &IGURE 7HEN THE GILLS ASSUME
THEIR FUNCTION OF RESPIRATORY EXCHANGE THE OUTER LAYERS
OF THE YOLK SAC TAKE ON THE APPEARANCE OF A PROTECTIVE
EPIDERMIS AND THE SQUAMOUS EPITHELIAL CELLS BECOME
KERATINIZED AND CONJOINED BY DESMOSOMES #OLLAG
ENOUS lBRES lBROBLASTS AND SCATTERED SMOOTH MUSCLE
lBRES THICKEN AND STRENGTHEN THE SUBEPITHELIAL CONNEC
TIVE TISSUE
%MBRYOS OF MANY SHARKS AND RAYS ARE NOURISHED
BY A VISCOUS NUTRIENT mUID THE ()34/42/0( SECRETED
BY THE UTERINE EPITHELIUM 7OURMS 7OURMS
'ROVE AND ,OMBARDI 4HIS mUID PROVIDES
BOTH A SOURCE OF ENERGY AS WELL AS THE MOLECULAR
CONSTITUENTS REQUIRED FOR SYNTHESIS DURING CELL REPLI
CATION AND TISSUE GROWTH AND IN SOME SPECIES EG
-USTELUS LAEVIS $ASYATIS VIOLACEA ITS ORGANIC CON
TENT EXCEEDS THAT OF COWS MILK 4HE PRESENCE OF
MATERNAL BLOOD SERUM PROTEINS ESPECIALLY IMMU
NOGLOBULIN - )G- SUGGESTS THAT HISTOTROPH PLAYS
AN IMMUNOLOGICAL ROLE IN ADDITION TO ITS SPECIALIZED
NUTRIENT FUNCTIONS (ISTOTROPH OF PLACENTAL SHARKS
MAY CONTAIN OESTROGENS INDICATING THAT IT MAY ALSO
HAVE AN ENDOCRINE FUNCTION
)N MANY ELASMOBRANCHS MOST OF THE UTERINE LINING
SECRETES HISTOTROPH BUT IN MORE ADVANCED SPECIES THIS
PRODUCTION IS ENHANCED BY SPECIALIZED PROJECTIONS OF
THE UTERINE WALL THE 42/0(/.%-!4! WHICH MAY CLOSELY
ENVELOP THE EMBRYO IN SOME RAYS THE ENTIRE LINING OF
THE UTERUS UNDERGOES HYPERTROPHY &IGURE (AM
LETT 7OURMS AND 3MITH 7OURMS 'ROVE AND
,OMBARDI (AMLETT ET AL A $URING
EARLY GESTATION TROPHONEMATA FORM FROM THE LUMINAL
EPITHELIUM AS BEDS OF RICHLY VASCULAR CONNECTIVE TIS
SUE COVERED BY A SIMPLE EPITHELIUM 4ROPHONEMATA
ARE SPATULATE VILLIFORM PROCESSES EMBOSSED WITH A PAT
TERN OF ANASTOMOSING CABLE LIKE RIDGES &IGURE
#(!04%2
! SIMPLE SQUAMOUS EPITHELIUM INVESTS A MASSIVE CAP
ILLARY NETWORK THAT EXTENDS BETWEEN TWO ARTERIES THAT
RUN ALONG THE INTERNAL MARGIN OF THE TROPHONEMA AND A
LARGE CENTRAL AXIAL VEIN &IGURES AND 4HE
CAPILLARIES WITH THEIR INVESTING EPITHELIUM ARE PROB
ABLY THE SITE OF TRANSPORT OF AMINO ACIDS LIPIDS AND
PROTEINS FROM THE MATERNAL BLOOD TO THE HISTOTROPH )N
ADDITION THE CAPILLARY BED LIKELY FUNCTIONS IN GAS EX
CHANGE AND WASTE ABSORPTION ! DENSE STROMA OF RETIC
ULAR CONNECTIVE TISSUE SUPPORTS EACH TROPHONEMA 4HE
EFlCIENCY OF TROPHONEMATA MAY BE ENHANCED IN SOME
SPECIES WHERE THEY ARE SAID TO ENTER THE FOETUS BY WAY
OF THE SPIRACLES PASS INTO THE OESOPHAGUS AND SECRETE
HISTOTROPH DIRECTLY INTO THE GUT
$URING MID TO LATE GESTATION TROPHONEMATA ENTER
THEIR SECOND DIFFERENTIATIVE PHASE WHEN SOME OF THE
EPITHELIAL CELLS FORM ACINI AMONG THE EXTENSIVE CAPIL
LARY BEDS THESE SYNTHESIZE AND SECRETE PROTEINS INTO
THE HISTOTROPH BY WAY OF PITS LYING BETWEEN THE SURFACE
RIDGES 4HUS THE COMPONENTS OF HISTOTROPH HAVE TWO
ORIGINS TRANSPORT DIRECTLY FROM THE MATERNAL BLOOD AND
SYNTHESIS AND SECRETION BY TROPHONEMAL CELLS 3IMPLE
CUBOIDAL TO LOW COLUMNAR EPITHELIAL CELLS COVER THE
CABLE
LIKE RIDGES AND EXTEND INTO THE CRYPTS &IGURES
AND ! (AMLETT 7OURMS AND 3MITH
(AMLETT ET AL A A (UGE LIPID DROPLETS
DISTEND THESE CELLS BUT LESS CONSPICUOUS PROTEIN SE
CRETORY GRANULES AND MUCOUS DROPLETS ARE ALSO PRES
ENT &IGURES " # .UCLEI ARE ROUND TO OVAL AND
CONTAIN A DISPERSED PATTERN OF HETEROCHROMATIN 3CANT
APICAL MICROVILLI ARE PRESENT 4HE EPITHELIUM IS RE
INFORCED BY AN APICAL TERMINAL WEB ASSOCIATED WITH
JUNCTIONAL COMPLEXES BETWEEN ADJACENT CELLS &IG
URE $ AND # 4HE ORGANELLES INDICATIVE OF
PROTEIN PRODUCTION ARE PRESENT WELL DEVELOPED GRANU
LAR ENDOPLASMIC RETICULUM POLYRIBOSOMES AND AN EX
TENSIVE SUPRANUCLEAR 'OLGI COMPLEX &IGURE %
5NCOATED VESICLES ARE GIVEN OFF BY THE 'OLGI COMPLEX
AND THERE IS A PROGRESSIVE INCREASE APICALLY IN THE ELEC
TRON DENSITY OF MATERIAL CONTAINED WITHIN VACUOLES AND
PRESECRETORY GRANULES
)T IS ASSUMED THAT TRANSPORT GAS EXCHANGE AND WASTE
REMOVAL CONTINUE DURING MID TO LATE GESTATION !S TERM
APPROACHES THE TROPHONEMATA BECOME INCREASINGLY EF
lCIENT FOR RESPIRATORY EXCHANGE (AMLETT ET AL A
A 4HE SURFACE EPITHELIUM AT THE mATTENED EDGES
OF THE TROPHONEMATA BECOMES ATTENUATED AND THE UN
DERLYING CAPILLARIES BECOME DILATED FORMING IRREGULAR
SINUSOIDS THAT BULGE CLOSE BENEATH THE SURFACE &IGURES
! " ! TO $ 4HE ENDOTHELIAL CELLS CONTAIN
MICROPINOCYTOTIC VESICLES AND MITOCHONDRIA ! FEW
RETICULAR lBRES SEPARATE THE BASAL LAMINAE OF THE EN
DOTHELIUM AND EPITHELIUM OFFERING SCANT RESISTANCE TO
THE EXCHANGE OF GASES 3TELLATE PERICYTES COMMON TO
THE MICROCIRCULATION OF MANY PARTS OF THE BODY EM
BRACE THE SINUSOIDS &IGURES $ AND IT HAS
BEEN VARIOUSLY SUGGESTED THAT PERICYTES ARE CONTRACTILE
AND CONTROL THE mOW OF BLOOD THROUGH SMALL VESSELS OR
THAT THEY CONSTITUTE A MESENCHYMAL RESERVE OF UNDIF
FERENTIATED CELLS
9/,+ 3!# 0,!#%.4! /&
%,!3-/"2!.#(3
4HE MOST ADVANCED FORM OF VIVIPARITY IN ELASMO
BRANCHS IS SEEN IN #ARCHARHINIDAE AND 3PHYRNIDAE
WHERE THERE IS HAEMOTROPHIC EXCHANGE OF MATERIALS
BETWEEN THE UTERINE WALL AND THE 9/,+ 3!# 0,!#%.4!
OF THE FOETUS 7OURMS 'ROVE AND ,OMBARDI
!MONG lSHES WITH THE POSSIBLE EXCEPTION OF THE COEL
ACANTH ,ATIMERIA THE YOLK SAC PLACENTA OCCURS ONLY
IN SHARKS OF SPECIES OF VIVIPAROUS SHARKS ABOUT
ARE KNOWN TO BE PLACENTAL 4HE YOLK SAC FORMS
A VASCULAR PAD THAT mATTENS ITSELF AGAINST THE UTERINE
WALL AND NUTRIENTS ARE PASSED FROM THE MATERNAL BLOOD
INTO THE BLOOD OF THE FOETUS &IGURE )N MOST OF
THESE SHARKS THE EMBRYO IS LECITHOTROPHIC FOR THE lRST
FEW MONTHS OF GESTATION 7HEN YOLK RESERVES ARE EX
HAUSTED USUALLY IN MID GESTATION THE YOLK SAC PLACEN
TA BECOMES FUNCTIONAL (AMLETT AND 7OURMS
(AMLETT 7OURMS AND (UDSON A 7OURMS
'ROVE AND ,OMBARDI (AMLETT #ASTRO
AND 7OURMS (AEMATROPHIC EXCHANGE IS AUG
MENTED IN SOME PLACENTAL SPECIES BY NUTRIENTS PRO
VIDED BY HISTOTROPH SECRETED BY THE UTERINE WALL AND
ABSORBED BY THE FOETUS EITHER BY WAY OF THE GUT OR
OTHER ROUTES
$URING GESTATION DORSAL AND VENTRAL FOLDS OF THE
UTERINE WALL MAY FORM CREATING INDIVIDUAL COMPART
MENTS FOR EACH DEVELOPING FOETUS 3CHLERNITZAUER AND
'ILBERT 4HEY CONSIST OF A SIMPLE COLUMNAR EPI
THELIUM ENCLOSING A CORE OF VASCULAR CONNECTIVE TISSUE
AND A FEW SMOOTH MUSCLE CELLS &USION OF THE FOLDS
TAKES PLACE IN THE BONNETHEAD SHARK 3PHYRNA TIBURO
JUST AFTER THE PLACENTAS ARE ESTABLISHED 4HE ORIENTATION
OF THE PARTITIONS GRADUALLY CHANGES TO ACCOMMODATE
THE GROWING FOETUSES BECOMING PROGRESSIVELY MORE
LONGITUDINALLY PLACED &IGURE 4HE COMPART
MENTS INCREASE THE SURFACE AREA OF THE UTERINE LINING
BOTH FOR THE SECRETION OF HISTOTROPH AND ALSO FOR META
6)6)0!2)49
BOLIC EXCHANGE BETWEEN MOTHER AND FOETUS (AMLETT
4HE PARTITIONS ISOLATE EACH FOETUS FROM ITS SIB
LINGS THEREBY PREVENTING ENTANGLEMENT OF THE UMBILI
CAL STALKS AND ABRASION FROM DEVELOPING SCALES WHEN
THE EGG CAPSULES RUPTURE
)N BOTH APLACENTAL AND PLACENTAL SHARKS THE YOLK
SAC ARISES AS A VENTRAL OUTPOUCHING OF THE EMBRYONIC
GUT AND CONTAINS THE YOLK MASS ENCLOSED WITHIN EN
DODERMAL EPITHELIUM (AMLETT AND 7OURMS
7OURMS 'ROVE AND ,OMBARDI !S THIS ENDO
DERMAL EVAGINATION DISTENDS IT REMAINS ENCLOSED BY
THE MESODERM AND ECTODERM OF THE BODY WALL AND IS AT
TACHED TO THE EMBRYO BY THE 9/,+ 34!,+ &IGURE
! SPLIT SUBSEQUENTLY FORMS WITHIN THE MESODERM CRE
ATING THE %842!%-"29/.)# #/%,/- A SPACE ENCLOSED
BY 3/-!4)# -%3/$%2- ON THE OUTSIDE AND 30,!.#(.)#
-%3/$%2- INSIDE
4HE WALL OF THE YOLK SAC CONSISTS OF SIX CONCENTRIC
REGIONS ECTODERM SOMATIC MESODERM EXTRAEMBRYON
IC COELOM SPLANCHNIC MESODERM ENDODERM AND YOLK
SYNCYTIUM &IGURE (AMLETT AND 7OURMS
4HE EXTRAEMBRYONIC COELOM IS LINED BY -%3/4(%,)5-
A SIMPLE SQUAMOUS EPITHELIUM WHOSE mATTENED CELLS
ARE PINOCYTOTICALLY ACTIVE WITH NUMEROUS SMOOTH
WALLED VESICLES ASSOCIATED WITH THEIR UPPER AND LOWER
CELL SURFACES &IGURE DENSE MEMBRANE
BOUND
HOMOGENEOUS GRANULES AND LONGITUDINALLY ORIENTED l
BRILS OCCUPY THE CYTOPLASM 4HE MESODERM IS INVADED
BY ABUNDANT BLOOD VESSELS THAT EXTEND FROM THE VITEL
LINE ARTERY AND VITELLINE VEIN OF THE EMBRYO 6ITELLINE
CAPILLARIES DELIMITED BY A BASAL LAMINA ARE CLOSELY AP
POSED TO THE BASAL SURFACE OF THE SPLANCHNIC MESODERM
3MOOTH
WALLED PINOCYTOTIC VESICLES OCCUR IN BOTH THE
INNER AND OUTER SURFACES OF THE CONTINUOUS CAPILLARY
ENDOTHELIUM AND THE CYTOPLASM CONTAINS DENSE MEM
BRANE
BOUND GRANULES AND TRANSPORT VESICLES
4HE YOLK SAC IS COVERED WITH ECTODERMAL EPITHE
LIUM THAT IS CONTINUOUS BY WAY OF THE YOLK STALK WITH
THE ECTODERM THAT ENCLOSES THE EMBRYO ITSELF &IGURE
(AMLETT AND 7OURMS 7OURMS 'ROVE
AND ,OMBARDI 4HE CAVITY CONTAINING THE YOLK
IS SURROUNDED BY THE 9/,+ 39.#94)5- AND %.$/$%2
-!, %0)4(%,)5- &IGURES AND ! AND IS CON
TINUOUS WITH THE LUMEN OF THE GUT BY WAY OF A PASSAGE
WITHIN THE YOLK STALK THE $5#453 6)4%,,/
).4%34).!,)3
$URING THE PERIOD OF VITELLOGENIC DEVELOPMENT YOLK
PLATELETS FROM THE YOLK MASS ARE PASSED UP THE DUCTUS
BY CILIARY ACTION OF ITS EPITHELIAL CELLS AND ARE DIGESTED
AND ABSORBED IN THE INTESTINE &IGURE (AMLETT
(AMLETT 3CHWARTZ AND $I$IO )N ADDI
TION SOME ENZYMATIC BREAKDOWN OF YOLK OCCURS WITH
IN THE YOLK SYNCYTIUM AND NUTRIENT MACROMOLECULES
ARE TRANSPORTED TO THE EMBRYO BY THE ABUNDANT BLOOD
VESSELS OF THE YOLK SAC &IGURE 4HE PRESENCE
OF MICROVILLI ON SOME OF THE SIMPLE COLUMNAR EPITHE
LIAL CELLS OF THE DUCTUS RAISES THE POSSIBILITY THAT YOLK
METABOLITES ARE ALSO ABSORBED WITHIN THE DUCTUS ITSELF
&IGURES AND 3CATTERED BETWEEN THE EPITHE
LIAL CELLS OF THE DUCTUS ARE GRANULAR %.4%2/%.$/#2).%
#%,,3 WHICH DO NOT ATTAIN THE SURFACE AND WHOSE SECRE
TIONS APPEAR TO BE DIRECTED BASALLY INTO THE SURROUND
ING CONNECTIVE TISSUE %NTEROENDOCRINE CELLS CONSTITUTE
PART OF THE 0!2!#2).% 3934%- THEIR SECRETIONS MAY HAVE
A REGULATORY EFFECT ON ADJACENT CELLS
0REIMPLANTATION EMBRYOS POSSESS TRANSITORY %84%2
.!, '),, &),!-%.43 THAT ORIGINATE ON THE POSTERIOR SUR
FACE OF THE GILL ARCH AND EMERGE THROUGH THE GILL SLITS
&IGURE (AMLETT ET AL (AMLETT
4HESE AID IN RESPIRATION BUT MAY ALSO ABSORB NUTRIENTS
FROM THE HISTOTROPH BEFORE THE ESTABLISHMENT OF THE
YOLK SAC PLACENTA %ACH lLAMENT CONTAINS A SINGLE CAP
ILLARY LOOP CONNECTING AFFERENT AND EFFERENT BRANCHIAL
ARTERIES $URING LATER EMBRYONIC LIFE THE lLAMENTS ARE
RETRACTED AND RESORBED WHEN DElNITIVE GILL LAMELLAE
DEVELOP AT THE BASE OF THE lLAMENTS !T THIS TIME THE
YOLK SAC PLACENTA ASSUMES THE FUNCTIONS OF BOTH RESPI
RATION AND HAEMATROPHIC NUTRITION
"EFORE IMPLANTATION IN PLACENTAL SHARKS THE ECTO
DERM COVERING THE YOLK SAC IS A SIMPLE LOW CUBOIDAL
EPITHELIUM AND ALTHOUGH IT APPEARS TO BE IMPERVIOUS
TO MACROMOLECULES IT MAY ACCOMMODATE SOME RESPI
RATORY AND EXCRETORY EXCHANGE (AMLETT AND 7OURMS
7OURMS 'ROVE AND ,OMBARDI )NTER
LOCKING MICROPLICAE EXTEND OVER THE EPITHELIAL SUR
FACE EXCEPT AT THE PERIPHERY WHERE THERE ARE RIDGE LIKE
BOUNDARIES BETWEEN ADJACENT CELLS &IGURE !
4HE CYTOPLASM OF THIS EPITHELIUM IS CHARACTERISTIC OF
CELLS THAT ARE SYNTHESIZING AND SECRETING PROTEINS AND
CONTAINS GRANULAR ENDOPLASMIC RETICULUM WITH DILATED
VESICULAR CISTERNAE MANY POLYSOMES MITOCHONDRIA
! 39.#94)5- IS A MULTINUCLEATE MASS OF PROTOPLASM
3ECRETORY CELLS OCCURRING SINGLY IN EPITHELIA OF MANY PARTS OF THE BODY MAY RELEASE PEPTIDES WHICH REGULATE THE ACTIVITY OF NEIGHBOURING
CELLS !S A RULE THESE CELLS DO NOT EXTEND TO THE SURFACE OF THE EPITHELIUM 4HEY CONSTITUTE THE 0!2!#2).% 3934%- AND MAY BE CONTRASTED WITH
THE MORE FAMILIAR ENDOCRINE SYSTEM WHICH RELEASES HORMONES THAT ACT ON A TARGET TISSUE USUALLY AT SOME DISTANCE FROM THE POINT OF RELEASE
#(!04%2
A 'OLGI COMPLEX WITH ASSOCIATED POPULATIONS OF COAT
ED AND UNCOATED VESICLES AND CONSPICUOUS LIPID
LIKE
INCLUSIONS &IGURES " # 4HERE IS NO EVIDENCE OF
PINOCYTOTIC ACTIVITY 4HIS EPITHELIUM RESTS ON A BASAL
LAMINA BELOW WHICH IS A COLLAGENOUS STROMA CONTAIN
ING DENSE SPHERICAL INCLUSIONS &IGURE $
4HE INNER REGIONS OF THE YOLK SAC COMPRISE THE SO
MATIC MESODERM AN INTERVENING NARROW EXTRAEMBRY
ONIC COELOM AND THE SPLANCHNIC MESODERM
VITELLINE
CAPILLARY REGION &IGURE 7OURMS 'ROVE AND
,OMBARDI 4HE STRUCTURE OF THE SOMATIC AND
SPLANCHNIC MESODERM IS SIMILAR TO THAT OF CLASSIC ME
SOTHELIUM CONSISTING OF A SINGLE LAYER OF SQUAMOUS
CELLS LYING ON VASCULAR AREOLAR CONNECTIVE TISSUE -E
SOTHELIAL CELLS HAVE mATTENED NUCLEI LONGITUDINAL CY
TOPLASMIC lBRILS SMOOTH
WALLED AND COATED VESICLES
AND DENSE MEMBRANE
BOUND GRANULES 3URFACES OF
ADJACENT CELLS INTERDIGITATE BUT SHOW FEW DESMOSOMES
9OLK
SAC CAPILLARIES LINED BY CONTINUOUS ENDOTHE
LIUM ARE ADJACENT TO THE INNER SURFACE OF THE SPLANCH
NIC MESODERMAL LAYER !BUNDANT ENDOCYTOTIC ACTIVITY
IN MESOTHELIAL AND ENDOTHELIAL EPITHELIA INDICATES THE
OCCURRENCE OF VESICULAR TRANSPORT PRESUMABLY OF MA
TERIALS DERIVED FROM YOLK BREAKDOWN 4HE ENDODERM
IS IN CLOSE CONTACT WITH THE BASAL LAMINA OF THE CAPIL
LARY ENDOTHELIUM )TS CELLS CONTAIN MANY MITOCHONDRIA
AND POLYRIBOSOMES HETEROGENEOUS SMOOTH
WALLED
VESICLES AND MANY YOLK DEGRADATION VESICLES &IGURE
! 4HE INNERMOST LAYER THE YOLK SYNCYTIAL LAYER
CONTAINS MANY HETEROGENEOUS YOLK GRANULES IN VARIOUS
STAGES OF DEGENERATION &IGURES " #
!S YOLK RESERVES ARE DEPLETED THE UTERINE EPITHELIUM
SECRETES HISTOTROPH THAT BATHES THE EMBRYO (AMLETT
)N MOST SHARKS THE EMBRYO IS STILL CONTAINED
WITHIN ITS EGG CAPSULE &IGURE 4HE CAPSULE IS
M THICK IN THE SHARK -USTELUS CANIS AND CONSISTS
OF FOUR OR MORE ORTHOGONALLY
ARRANGED LAMINAE OF l
BROUS MATERIAL &IGURE ,OMBARDI AND &ILES
4HE OUTER LAMINA IS TIGHTLY CONSTRUCTED WITH
NO VISIBLE PORES GREATER THAN NM IN DIAMETER
4HE CAPSULE IS PERMEABLE TO MATERIALS BELOW A MO
LECULAR WEIGHT OF K$A SO THAT UREA AND GLUCOSE CROSS
READILY )T IS SUGGESTED THAT THE EGG CAPSULE ASSISTS IN
THE ESTABLISHMENT AND MAINTENANCE OF THE PLACENTAL
ATTACHMENT BY ACTING AS A SEMIPERMEABLE MEMBRANE
BETWEEN THE INTRACAPSULAR AND EXTRACAPSULAR COM
PARTMENTS )N THIS SCHEME THE FOETUS RELEASES SOL
UTES OF HIGH MOLECULAR WEIGHT DRAWING WATER FROM
THE EXTRACAPSULAR mUIDS ACROSS THE EGG CAPSULE INTO
THE CAPSULAR COMPARTMENT &IGURE 4HE RESULTING
DISTENTION OF THE EGG CAPSULE EVENTUALLY OBLITERATES THE
EXTRACAPSULAR SPACE APPOSING THE YOLK SACEGG CAPSULE
COMPLEX AGAINST THE UTERINE LINING THEREBY PERMITTING
THE SUBSEQUENT INTERDIGITATION OF MATERNAL AND EMBRY
ONIC TISSUES IN THE FORMATION OF THE YOLK SAC PLACENTA
&IGURE
!ROUND THE TIME OF IMPLANTATION WHEN THE YOLK IS
CONSUMED THE YOLK SAC ESPECIALLY THE PROXIMAL POR
TION BECOMES A HOLLOW SPHERICAL BAG SUPPORTED BY
RICHLY VASCULAR CONNECTIVE TISSUE LINKED TO THE VITELLINE
ARTERY AND VEIN 7OURMS 'ROVE AND ,OMBARDI
#ASTRO AND 7OURMS )NCREASED RAMIlCATION OF
THESE VESSELS IN THE DISTAL RUGOSE PLACENTA COMBINED
WITH SURFACE FOLDING AND CONNECTIVE TISSUE HYPERPLA
SIA GIVE THIS REGION ITS SPONGY TEXTURE )NITIALLY THE
MATERNAL PORTION OF THE PLACENTA CONTAINS ALL OF THE
CELL LAYERS THAT ARE PRESENT AT NONATTACHMENT SITES
!LTHOUGH VARYING DEGREES OF INTERDIGITATION AND FUSION
OF MATERNAL AND FOETAL TISSUES ENHANCE THE EXCHANGE
OF MATERIALS THE SELACHIAN PLACENTA IS CONSIDERED TO
BE ./.
).6!3)6% AND ./.
$%#)$5!4% SO THAT MATERNAL
AND FOETAL TISSUES CAN BE SEPARATED WITHOUT DETACHING
UTERINE TISSUE (AMLETT 7OURMS AND (UDSON C
(AMLETT 4HERE IS NO BLEEDING NOR SHEDDING OF
MATERNAL TISSUE AT PARTURITION
!S THE FOETUS IMPLANTS THE YOLK STALK ELONGATES
'ILBERT AND 3CHLERNITZAUER (AMLETT 7OURMS
AND (UDSON A 7OURMS 'ROVE AND ,OMBARDI
(AMLETT (AMLETT -IGLINO AND $IDIO
7HEN THE YOLK SAC mATTENS ITSELF AGAINST THE
UTERINE WALL TO FORM THE FOETAL PORTION OF THE PLACEN
TA THE YOLK STALK IS DESIGNATED THE 5-"),)#!, 34!,+
IT CONTAINS THE MUSCULAR UMBILICAL ARTERY UMBILICAL
VEIN THE DUCTUS VITELLO
INTESTINALIS AND IN MOST SPE
CIES A REMNANT OF THE EXTRAEMBRYONIC COELOM &IGURE
4HE YOLK SAC BECOMES REGIONALLY MODIlED INTO
TWO DISTINCT REGIONS THE DIAPHANOUS 02/8)-!, 3-//4(
3%'-%.4 IS CONFLUENT WITH THE UMBILICAL STALK AND
DRAPES OVER THE RICHLY VASCULAR $)34!, 25'/3% 0/24)/.
THAT ABUTS THE UTERINE ATTACHMENT SITE &IGURES
AND )NCREASED VASCULARIZATION OF THE YOLK SAC
IS REmECTED AT THE POINT OF CONTACT BY ENHANCED VAS
CULARIZATION OF THE UTERINE WALL !DJACENT REGIONS OF
THE UTERUS DIFFERENTIATE INTO 0!2!0,!#%.4!, 3)4%3 THAT
PRODUCE MUCUS &IGURE 4HE JUNCTION OF THE VAS
CULARIZED YOLK SAC AND UTERINE WALL IS THE SITE AT WHICH
THE EMBRYO WILL IMPLANT AND THE 0,!#%.4! WILL BE
FORMED 4HE PLACENTA CONSISTS OF THE !44!#(-%.4 3)4%
ON THE UTERINE WALL THE EGG CAPSULE IN MOST SPECIES
AND THE mATTENED VASCULAR PAD OF THE FOETAL YOLK SAC
6)6)0!2)49
4HE FOETAL PORTION OF THE PLACENTA INCLUDES THE UMBILI
CAL CORD THE SMOOTH PROXIMAL PORTION THE RICHLY VASCU
LAR RUGOSE DISTAL PORTION AND THE EGG CAPSULE &IGURES
AND 4HERE ARE NO NOTICEABLE DIFFERENCES
IN THE STRUCTURE FROM REGION TO REGION OF THE YOLK SAC
PLACENTA PRIOR TO IMPLANTATION (AMLETT AND 7OURMS
(AMLETT (AMLETT ET AL A
)N THE (!%-!42/0()# NUTRITION OF PLACENTAL SHARKS
MATERIALS ARE TRANSFERRED FROM THE BLOOD IN MATERNAL
CAPILLARIES OF THE UTERINE WALL TO FOETAL CAPILLARIES IN THE
RUGOSE DISTAL PORTION OF THE PLACENTA 3CHLERNITZAUER
AND 'ILBERT 4ESHIMA (AMLETT 7OURMS
AND (UDSON A C 7OURMS 'ROVE AND ,OM
BARDI (AMLETT ET AL A &OETAL CAPILLARIES
ARE BETTER DEVELOPED THAN MATERNAL ONES IN -USTELUS
GRISEUS THEREBY FACILITATING THE EXCHANGE OF MATERI
ALS 4ESHIMA )N ADDITION FOETAL HAEMOGLOBIN
OF 3QUALUS SUCKLEYI HAS A GREATER AFlNITY FOR OXYGEN
THAN ADULT HAEMOGLOBIN THEREBY OPTIMIZING THE TRANS
FER OF OXYGEN FROM MATERNAL TO FOETAL CIRCULATION
-ANWELL
4HE BARRIERS TO THE EXCHANGE OF MATERIALS ARE MA
TERNAL ENDOTHELIUM MATERNAL EPITHELIUM EGG CAPSULE
FOETAL EPITHELIUM AND FOETAL ENDOTHELIUM &IGURE
)N DIFFERENT CLASSES OF PLACENTAS THERE MAY BE A
REDUCTION IN THESE BARRIERS AND AN INCREASE IN THE AREA
OF TISSUE CONTACT BY MEANS OF INTERDIGITATION &IGURE
)N SOME SHARKS THE NUMBER AND THICKNESS OF
LAYERS OF CELLS AND EXTRACELLULAR MATRIX MAY BE DIMIN
ISHED 4HE MATERNAL AND FOETAL EPITHELIA MAY DEGENER
ATE PERMITTING EACH OF THE CAPILLARY NETWORKS TO ABUT
ITS OWN SIDE OF THE EGG CAPSULE AT THE MATERNAL
FOETAL
PLACENTAL JUNCTION 4HE EMBRYONIC COELOM WITHIN THE
PLACENTA MAY BE OBLITERATED BY FUSION 4HE ROLE OF THE
EGG CAPSULE AS A POSSIBLE BARRIER TO PLACENTAL TRANSPORT
IS ENIGMATIC SINCE LITTLE IS KNOWN OF ITS PERMEABIL
ITY 7OURMS 'ROVE AND ,OMBARDI ,OMBARDI
AND &ILES )T IS PRESUMED THAT ITS PERMEABILITY
IN VIVIPAROUS SPECIES IS ENHANCED BY A REDUCTION IN
THICKNESS AND THE POSSIBLE LOSS OR MACROMOLECULAR
REARRANGEMENT OF COLLAGEN !LTHOUGH IT IS A POTENTIAL
PERMEABILITY BARRIER THE EGG CAPSULE APPEARS TO PERMIT
THE READY PASSAGE OF SMALL MOLECULES BUT MAY HINDER
PASSAGE OF MACROMOLECULES )N SOME SPECIES THERE
MAY BE NO EGG CAPSULE
$URING EARLY GESTATION IN THE !TLANTIC SHARPNOSE
SHARK 2HIZOPRIONODON TERRAENOVAE THE UTERINE WALL
CONSISTS OF A SIMPLE CUBOIDAL EPITHELIUM RESTING ON
A LAYER OF VASCULAR LOOSE AREOLAR TISSUE CONTAINING
STRANDS OF LONGITUDINAL SMOOTH MUSCLE &IGURE
#ASTRO AND 7OURMS (AMLETT -IGLINO AND $I
DIO "ELOW IS A CONTINUOUS LAYER OF INNER CIR
CULAR AND OUTER LONGITUDINAL SMOOTH MUSCLE COVERED
BY A CLOSELY APPLIED TUNICA SEROSA !S GESTATION CON
TINUES VASCULARIZATION INCREASES IN THE DISTAL YOLK SAC
AS WELL AS IN ADJACENT REGIONS OF THE UTERINE WALL 4HE
UTERINE WALL INCREASES IN THICKNESS AND BECOMES SOFT
AND SPONGY )TS EPITHELIAL CELLS PROLIFERATE AND BECOME
CLOSELY PACKED 7HEN THE YOLK SUPPLY IS EXHAUSTED
THE DISTAL YOLK SAC IMPLANTS AND BECOMES ENVELOPED BY
THE UTERINE WALL !T THIS TIME THERE ARE TWO SOURCES OF
NUTRIENTS FOR THE FOETUS HAEMATROPHIC EXCHANGE TAKES
PLACE BY WAY OF THE YOLK SAC PLACENTA WHILE APLACEN
TAL REGIONS OF THE UTERINE WALL PRODUCE HISTOTROPH
!T THE IMPLANTATION SITE THE UTERINE WALL BEARS NUMER
OUS RIDGES FOLDS AND PROTRUBERANCES &IGURE
COVERED WITH EITHER A PSEUDOSTRATIlED EPITHELIUM OR A
LAYER OF SHORT COLUMNAR EPITHELIAL CELLS TWO CELLS THICK
4HESE PROJECTIONS INTERDIGITATE WITH RIDGES OF THE YOLK
SAC INCORPORATING PLEATS OF THE EGG CAPSULE BETWEEN
THEM &IGURE %XTENSIVE CAPILLARY BEDS ARE EM
BEDDED IN LOOSE AREOLAR CONNECTIVE TISSUE BENEATH BOTH
THE MATERNAL AND FOETAL EPITHELIA THE CAPILLARIES MAY
BE FENESTRATED &IGURE 4HE PARAPLACENTAL REGION
OF THE LUMINAL LINING OF THE UTERUS IS ALSO THROWN UP
INTO ELABORATE FOLDS WHOSE SIMPLE COLUMNAR EPITHELIAL
CELLS ELABORATE MUCUS &IGURE 4HESE FOLDS AP
PEAR SHORTLY AFTER IMPLANTATION WHEN THE UTERINE WALL
BEGINS TO PRODUCE HISTOTROPH lLLING THE COMPARTMENT
4HE EPITHELIAL CELLS OF THE UTERINE ATTACHMENT SITE ARE
CUBOIDAL TO SQUAMOUS (AMLETT 4HEIR CYTO
PLASM HAS A RICH ARRAY OF ENDOPLASMIC RETICULUM AND
PROMINENT SECRETION VESICLES lLLED WITH mOCCULENT MA
TERIAL THAT RESEMBLES THE SUBSTANCE SEEN IN THE SPACE
BETWEEN THE UTERINE EPITHELIUM AND THE EGG CAPSULE
&IGURES AND 4HE APPEARANCE OF STEROID
PRODUCTION IN THESE CELLS MAY BE INDICATIVE OF AN EN
DOCRINE FUNCTION IN THE SHARK PLACENTA 4HE APLACENTAL
FOLDS CONTINUE TO GROW AND INCREASE IN COMPLEXITY UN
TIL PARTURITION
!44!#(-%.4 3)4%3 IN THE UTERINE LINING INCORPO
RATE HIGHLY VASCULAR FOLDS THAT INTERDIGITATE WITH DEEP
GROOVES IN THE RUGOSE DISTAL PORTION OF THE FOETAL YOLK
SAC &IGURE " (AMLETT 7OURMS AND (UDSON
C (AMLETT 4HE EGG CAPSULE LIES BETWEEN
THE MATERNAL AND FOETAL EPITHELIA AND IS CLOSELY APPOSED
TO BOTH &IGURE !TTACHMENT SITES IN THE SANDBAR
SHARK #ARCHARHINUS PLUMBEUS CONSIST OF A SIMPLE
LOW COLUMNAR EPITHELIUM UNDERLAIN BY AN EXTENSIVE
VASCULAR NETWORK &IGURES ! % 4HE ULTRASTRUC
#(!04%2
TURE OF THE UTERINE EPITHELIUM INDICATES GREAT ACTIVITY
IN THE TRANSPORT OF MATERIALS BETWEEN THE RICH BLOOD
SUPPLY AND LUMINAL SURFACE INCLUDING FEATURES SUCH AS
THE TIGHT JUNCTIONS SEALING THE LUMINAL BORDERS ELABO
RATE FOLDING AND INTERDIGITATION OF LATERAL CELL BOUND
ARIES BRANCHED MICROVILLI AND SACCULAR INVAGINATIONS
OF THE APICAL SURFACE THE PRESENCE OF APICAL COATED
PITS AND NUMEROUS COATED VESICLES PROBABLY INDICATES
THE TRANSFER OF SERUM PROTEINS TO THE EMBRYO &IGURES
# $ 4HE UTERINE EPITHELIAL CELLS ALSO CONTAIN
LIPID
LIKE INCLUSIONS A PROMINENT GRANULAR ENDOPLAS
MIC RETICULUM AND MANY FREE RIBOSOMES 4HE ENDOTHE
LIUM OF THE UTERINE CAPILLARIES IS PINOCYTOTICALLY ACTIVE
AND THERE IS LITTLE DISTANCE TO IMPEDE mOW BETWEEN
THE EPITHELIAL CELLS AND THE CAPILLARIES NOR IS A SIGNIl
CANT BARRIER PRESENTED BY THEIR THIN BASAL LAMINAS AND
SPARSE INTERVENING CONNECTIVE TISSUE )N ADDITION TO THE
TRANSPORT OF MATERNAL SERUM PROTEINS GASES WASTES
AND POSSIBLY IMMUNOGLOBULINS THE ATTACHMENT SITES
PROBABLY REGULATE WATER ELECTROLYTES AND OSMOREGULA
TORY FACTORS
4HE 25'/3% $)34!, 0/24)/. OF THE PLACENTA OF
# PLUMBEUS CONSISTS OF A SIMPLE COLUMNAR 352&!#%
%0)4(%,)5- OF PEG
LIKE CELLS DERIVED FROM THE ECTODERM
&IGURES ! " A COLLAGENOUS 342/-! CONTAINING
VITELLINE CAPILLARIES AND AN INNERMOST "/5.$!29 #%,,
,!9%2 &IGURE + (AMLETT 7OURMS AND (UDSON
A 4HE EGG CAPSULE lTS CLOSELY AROUND THE SURFACE
EPITHELIUM &IGURE # 4HE ULTRASTRUCTURE OF THIS
REGION BEARS WITNESS TO ITS HAEMOTROPHIC FUNCTION THE
SURFACE EPITHELIAL CELLS ARE CLOSELY APPOSED TO THE ABUN
DANT CAPILLARIES OF THE VITELLINE CIRCULATION AND GIVE THE
APPEARANCE OF ACTIVE ABSORPTION WITH THEIR EXTENSIVE
APICAL SYSTEM OF SMOOTH
WALLED MEMBRANOUS ANAS
TOMOSING CANALICULI AND TUBULES &IGURES $ %
!CTIVE ENDOCYTOTIC UPTAKE OF THE TRACER HORSERADISH
PEROXIDASE HAS BEEN DEMONSTRATED IN THE EPITHELIAL
CELLS OF THE DISTAL PLACENTA BUT NOT BY THE EPITHELIUM OF
THE SMOOTH PORTION NOR BY THE UMBILICAL CORD 7HORL
LIKE INCLUSIONS IN THE BASAL CYTOPLASM OF THE SURFACE
EPITHELIAL CELLS LIE ADJACENT TO THE PINOCYTOTICALLY AC
TIVE ENDOTHELIUM OF THE CAPILLARIES AND ARE ASSUMED
TO BE YOLK PROTEINS BEING TRANSFERRED FROM THE MOTHER
TO THE EMBRYO THROUGHOUT GESTATION &IGURES & TO
) PRESUMABLY THE SAME YOLK PROTEIN PRECURSORS THAT
ARE INVOLVED IN OOCYTE GROWTH CONTINUE TO BE PRODUCED
BY THE MATERNAL LIVER AND ARE USED AS NUTRIENTS FOR THE
DEVELOPING EMBRYO AFTER IT HAS EXHAUSTED ITS ORIGINAL
SUPPLY OF YOLK !LL ABSORPTIVE ACTIVITY OF THE YOLK SAC
APPEARS TO HAVE BEEN ASSUMED BY THE EPITHELIAL CELLS
OF THE ECTODERMAL SURFACE WHILE THE FORMERLY ACTIVE
ENDODERMAL CELLS FORM A SUPPORTIVE "/5.$!29 ,!9%2
WITH SCANT MICROVILLI AND SPARSE ORGANELLES EXCEPT FOR
A FEW MITOCHONDRIA &IGURE * ! WELL DEVELOPED
COLLAGENOUS STROMA SEPARATES THE TWO EPITHELIA
4HE 3-//4( 02/8)-!, 3%'-%.4 OF THE SHARK PLACENTA
DOES NOT COME INTO CONTACT WITH THE UTERINE LINING BUT
ISOLATES THE ATTACHMENT SITE BY DRAPING OVER THE DISTAL
PORTION OF THE PLACENTA SO THAT LITTLE OF IT IS EXPOSED
TO THE PERIFOETAL COMPARTMENT CONTAINED WITHIN THE
EGG CAPSULE (AMLETT 7OURMS AND (UDSON B
4HE PROXIMAL SEGMENT OF # PLUMBEUS CONSISTS OF
OUTER %#4/$%2-!, %0)4(%,)5- AN INTERVENING COL
LAGENOUS 342/-! AND THE INNER -%3/4(%,)5- &IGURE
* 0RESUMABLY WITH THE DISAPPEARANCE OF THE
YOLK THE ENDODERMAL EPITHELIUM HAS WITHDRAWN FROM
THE YOLK SAC #APILLARIES ARE SPARSE IN THE STROMA
4HE SURFACE EPITHELIUM BEARS A PROMINENT GLYCOCA
LYX )T MAY BE ONE TO THREE CELLS THICK AND CONTAINS
TWO CELL TYPES &IGURES ! " # $ & 'OLGI COM
PLEXES AND ELEMENTS OF ENDOPLASMIC RETICULUM ARE RARE
IN BOTH EPITHELIAL CELL TYPES AND THERE ARE FEW OF THE
ORGANELLES CHARACTERISTIC OF CELLS ENGAGED IN SYNTHET
IC ACTIVITY #UBOIDAL CELLS PREDOMINATE THESE HAVE A
DOME LIKE APICAL SURFACE COVERED WITH MICROVILLI AND
AN OVOID NUCLEUS 4HE SECOND TYPE HAS A CONVOLUTED
NUCLEUS AND A mATTENED APEX WITH MICROVILL AND CILIA
&IGURES # $ ' -ICROPLICAE OCCUR ON THE SUR
FACES OF A FEW CELLS "OTH TYPES CONTAIN LIPID INCLU
SIONS MANY CYTOPLASMIC lLAMENTS AND ARE JOINED BY
DESMOSOMES &IGURE % %PITHELIAL CELLS OF THE
MIDDLE LAYER ARE JOINED BY DESMOSOMES AND ARE SIMI
LAR TO THOSE OF THE SURFACE EXCEPT THAT THEY LACK MICRO
VILLI AND CILIA 4HE INNERMOST EPITHELIAL CELLS POSSESS
AN UNDULATING BASAL CONTOUR AND REST ON A CONSPICUOUS
BASAL LAMINA -ESOTHELIAL CELLS ARE SQUAMOUS WITH A
FUSIFORM NUCLEUS MANY SMOOTH WALLED PINOCYTOTIC
PITS TRANSPORT VESICLES MITOCHONDRIA FREE RIBOSOMES
AND A LARGE NUMBER OF CYTOPLASMIC lLAMENTS &IG
URES ( ) 4HE ENDOPLASMIC RETICULUM EXCEPT FOR
A FEW PATCHES OF THE GRANULAR TYPE AND 'OLGI COM
PLEXES ARE POORLY DEVELOPED 4HE MESOTHELIAL CELLS
REST ON A PROMINENT BASAL LAMINA THAT SEPARATES THEM
FROM THE CONNECTIVE TISSUE STROMA 4HE FUNCTION OF THE
PROXIMAL PORTION OF THE PLACENTA IS ENIGMATIC BUT THE
PRESENCE OF WELL DEVELOPED COLLAGENOUS TISSUE AS WELL
AS ABUNDANT DESMOSOMES AND CYTOPLASMIC lLAMENTS
WITHIN THE EPITHELIAL AND MESOTHELIAL CELLS SUGGESTS THAT
IT MAY RESIST MECHANICAL STRESS 4HE NUMEROUS PINO
CYTOTIC PITS AND VESICLES IN THE MESOTHELIAL CELLS MAY
6)6)0!2)49
INDICATE mUID EXCHANGE BETWEEN THE CAVITY OF THE PLA
CENTA AND THE PERIFOETAL COMPARTMENT WITHIN THE EGG
CAPSULE 3TRUCTURES CHARACTERISTIC OF STEROID SECRETION
HAVE BEEN DESCRIBED IN THE SIMPLE CUBOIDAL EPITHELIUM
OF THE SMOOTH PROXIMAL SEGMENT OF THE YOLK SAC OF
2HIZOPRIONODON TERRAENOVAE MITOCHONDRIA WITH TU
BULAR CRISTAE AGRANULAR ENDOPLASMIC RETICULUM AND
EXTENSIVE LAMELLAR BODIES &IGURE (AMLETT
)T IS SUGGESTED THAT THESE CELLS MAY BE A SOURCE
OF OESTRADIOL AND TESTOSTERONE
5MBILICAL STALKS OF MOST SPECIES OF #ARCHARHINUS
ARE SMOOTH AND THEIR SQUAMOUS EPITHELIUM APPEARS
NOT TO BE PERMEABLE TO THE mUIDS WITHIN THE UTERUS
)N MANY SELACHIANS HOWEVER THE STALK IS FESTOONED
WITH ARBORESCENT RICHLY VASCULAR ABSORPTIVE PROCESSES
CALLED !00%.$)#5,!% &IGURES TO (AMLETT
7OURMS 'ROVE AND ,OM
BARDI #ASTRO AND 7OURMS (AMLETT ET AL
A 4HESE OUTGROWTHS MAY BE OF VARIOUS SHAPES
mATTENED OR CYLINDRICAL lNGER
LIKE OR CLUB
SHAPED
SOMETIMES BRANCHING !FTER PLACENTATION HAS OC
CURRED IT HAS BEEN SUGGESTED THAT THE PLACENTAL UTERINE
WALL CONTINUES TO SECRETE HISTOTROPH UNTIL PARTURITION
ALTHOUGH PERHAPS ONLY IN SPECIES THAT POSSESS APPEN
DICULAE (AMLETT
!PPENDICULAE OF 2 TERRAENOVAE FORM VASCULAR
LOBED PROTRUSIONS FROM THE UMBILICAL CORD (AMLETT
(AMLETT ET AL A B &IGURE ! 4HEY
ARE COVERED WITH CONTINUATIONS OF THE SURFACE EPITHE
LIUM OF THE STALK AND ENCLOSE A CORE OF RICHLY VASCULAR
AREOLAR CONNECTIVE TISSUE 4HE EPITHELIUM CONSISTS OF
-)#2/6),,!2 AND '2!.5,!2 #%,,3 SUBTENDED BY FLAT
TENED "!3!, #%,,3 &IGURES # $ ' -ICROVILLAR
CELLS BRISTLING WITH LONG MICROVILLI FORM PYRIFORM
PROCESSES THAT ARE INSINUATED BETWEEN ADJACENT CELLS
THEIR CYTOPLASM CONTAINS LIPID AND MICROPINOCYTOTIC
VESICLES AT THE APEX $ILATED INTERCELLULAR SPACES OF
TEN OCCUR BETWEEN ADJACENT CELLS AND MAY REPRESENT
FUNCTIONAL TRANSPORT CHANNELS -ICROVILLAR CELLS ABSORB
NUTRIENTS PRODUCED BY THE UTERUS AS WELL AS EXOGENOUS
MATERIAL OF THE SIZE OF PROTEINS 'RANULATED CELLS UN
DERGO CYCLES OF SYNTHESIS SO THAT DIFFERENT SECRETORY
PHASES MAY BE OBSERVED WITHIN A SINGLE TISSUE SECTION
&IGURES $ TO & #ELLS SEEMINGLY DEVOID OF MOST
ORGANELLES HAVE JUST UNDERGONE EXOCYTOSIS GRANULAR
ENDOPLASMIC RETICULUM IS ACTIVE IN OTHER CELLS AND THE
SUPRANUCLEAR 'OLGI COMPLEX IS PROMINENT !S SYNTHE
SIS PROCEEDS THE APICAL CYTOPLASM BECOMES ENGORGED
WITH SECRETORY DROPLETS DISPLACING THE MITOCHONDRIA
TO THE BASE OF THE CELL FOLLOWING EXOCYTOSIS THE SYN
THESIS
SECRETION CYCLE REPEATS 4HE NATURE OF THE SECRE
TORY MATERIAL IS UNKNOWN )N ADDITION TO ABSORPTION
OF NUTRIENTS FROM THE HISTOTROPH APPENDICULAE ARE
PROBABLY ENGAGED IN RESPIRATION AND ION REGULATION OF
THE PERIEMBRYONIC mUID )T IS DIFlCULT TO SPECULATE ON
OTHER FUNCTIONS UNTIL THE NATURE OF THE SECRETORY DROP
LETS IS KNOWN "ENEATH THE SURFACE LAYER IS A LAYER OF
BASAL CELLS THAT REST ON THE BASAL LAMINA &IGURE $
)T IS BELIEVED THAT THESE CELLS ARE GENERATIVE AND PRO
VIDE REPLACEMENTS FOR THE SURFACE EPITHELIAL CELLS
4HE CORE OF THE UMBILICAL CORD CONTAINS AN ARTERY
VEIN AND THE DUCTUS VITELLO
INTESTINALIS &IGURE
4HESE STRUCTURES ARE INVESTED BY VASCULAR lBROUS CON
NECTIVE TISSUE CONTAINING OCCASIONAL SMOOTH MUSCLE
lBRES &IGURE ! 4HE DUCTUS VITELLO
INTESTINALIS IS
LINED BY A SIMPLE COLUMNAR EPITHELIUM OF INTERSPERSED
CILIATED AND MICROVILLOUS CELLS &IGURES " # 4HE
APICAL BORDERS OF THESE CELLS ARE SEALED BY TIGHT JUNC
TIONS WHILE DESMOSOMES REINFORCE THEIR LATERAL MEM
BRANES -ITOCHONDRIA ARE ABUNDANT APICALLY A MODEST
'OLGI COMPLEX SCANT GRANULAR ENDOPLASMIC RETICULUM
LIPID DROPLETS AND MODERATE GLYCOGEN DEPOSITS lLL OUT
THE CYTOPLASM ! LITTLE AGRANULAR ENDOPLASMIC RETICU
LUM IS OBSERVED $EEPLY WEDGED BETWEEN THE BASES
OF THESE SURFACE EPITHELIAL CELLS ARE SCATTERED FUSIFORM
ENTEROENDOCRINE CELLS lLLED WITH MEMBRANE
BOUND
ELECTRON
DENSE GRANULES &IGURES $ % !S IS USUAL
WITH THESE CELLS THE NUCLEUS IS APICAL AND THE GRANULES
ARE IN THE BASAL CYTOPLASM 4HE APPARENT INVERSION OF
THESE CELLS INDICATES THAT THEY DO NOT DEPOSIT THEIR SE
CRETIONS INTO THE LUMEN BUT RATHER INTO CONNECTIVE TISSUE
NEAR CAPILLARIES 4HEIR CYTOPLASM IS RICH IN GRANULAR EN
DOPLASMIC RETICULUM AND FREE RIBOSOMES 0RESUMABLY
THESE CELLS HAVE A PARACRINE FUNCTION MODULATING THE
ACTIVITY OF LOCAL AREAS OF THE PLACENTA
.O EGG CAPSULE INTERVENES IN THE PLACENTA OF THE
BLUE SHARK 0RIONACE GLAUCA /TAKE AND -IZUE
#ELLS OF THE SIMPLE COLUMNAR UTERINE EPITHELIUM PRESENT
THE CLASSIC APPEARANCE OF PROTEIN SECRETION ABUNDANT
BASAL GRANULAR ENDOPLASMIC RETICULUM SUPRANUCLEAR
'OLGI COMPLEXES AND APICAL SECRETORY VESICLES THEY
APPEAR TO SECRETE AN ELECTRON
DENSE MATERIAL THAT AC
CUMULATES IN THE SPACE BETWEEN MATERNAL AND FOETAL
TISSUES &IGURES ! TO & !BUNDANT CAPILLARIES ARE
CLOSELY APPLIED TO THE EPITHELIUM AND JUNCTIONAL COM
PLEXES SEAL THE APICAL BORDERS BETWEEN ADJACENT CELLS
4WO LAYERS OF CELLS CONSTITUTE THE EPITHELIUM OF THE
DISTAL PORTION OF THE FOETAL YOLK SAC &IGURES ' TO
+ (UGE SUPERlCIAL CELLS BRISTLING WITH MICROVILLI
APPEAR ACTIVE IN THE VESICULAR UPTAKE OF MACROMOLEC
#(!04%2
ULAR MATERIAL 4HEIR APICAL CYTOPLASM IS PACKED WITH
TUBULAR STRUCTURES AND COATED VESICLES WHILE MOST OF
THE CYTOPLASM CONTAINS SCATTERED GRANULAR AND AGRANU
LAR ENDOPLASMIC RETICULUM $ESMOSOMES CONNECT THE
CELLS LATERALLY 4HE mATTENED BASAL CELLS CONTAIN MITO
CHONDRIA AND ENDOPLASMIC RETICULUM 4HEIR INDENTED
BASAL SURFACE IS SEPARATED BY TWO THIN BASAL LAMINAS
FROM THE EXTREMELY THIN FENESTRATED ENDOTHELIAL CELLS
OF THE UNDERLYING CAPILLARIES 4HIS DESCRIPTION PRES
ENTS A PICTURE OF READY UPTAKE BY VITELLINE CAPILLARIES
OF MACROMOLECULAR MATERIAL PRODUCED BY THE UTERINE
EPITHELIUM 3INCE BOTH MATERNAL AND FOETAL EPITHELIA
WITHIN THE PLACENTA ARE THICK HOWEVER THEY DO NOT
SEEM TO BE CONDUCIVE TO GASEOUS EXCHANGE BETWEEN
MATERNAL BLOOD AND THE UTERINE mUID AND THIS EXCHANGE
APPEARS TO TAKE PLACE IN APLACENTAL REGIONS OF THE INTRA
UTERINE LINING WHERE THE EPITHELIUM IS THIN AND CLOSELY
APPLIED TO ABUNDANT UNDERLYING CAPILLARIES WHICH MAY
BE FENESTRATED &IGURE ! /TAKE AND -IZUE
)N ADDITION THE UTERINE EPITHELIUM DISPLAYS
THE CHARACTERISTICS OF HIGHLY ACTIVE mUID TRANSPORT
SUGGESTING ITS INVOLVEMENT IN OSMOREGULATION OF THE
UTERINE mUID ITS CELLS SHOW ABUNDANT BRANCHING MI
CROVILLI ELABORATE INTERCELLULAR SPACES SEALED BY APICAL
TIGHT JUNCTIONS AND ELABORATIONS OF THE BASAL PLASMA
LEMMA 4HERE IS SOME EVIDENCE OF SECRETION ALTHOUGH
SCANT ENDOPLASMIC RETICULUM OR 'OLGI COMPLEXES ARE
SEEN &IGURES " TO % A FEW GOBLET CELLS ARE SCAT
TERED HERE AND THERE &OETAL INVOLVEMENT IN GASEOUS
EXCHANGE AND WATER SOLUTE TRANSPORT PROBABLY TAKES
PLACE IN THE PROXIMAL REGION OF THE PLACENTA
!N EXTREME EXAMPLE OF PLACENTAL EFlCIENCY IS SEEN
IN 3COLIODON LATICAUDUS SORRAKOWAH WHERE THERE IS
VIRTUALLY NO LECITHOTROPHIC PHASE AND THE EMBRYO IM
PLANTS IMMEDIATELY AFTER OVULATION THIS IS PROBABLY THE
MOST HIGHLY EVOLVED EXAMPLE OF VIVIPARITY IN SHARKS
4ESHIMA !HMAD AND -IZUE 7OURMS
4HE OOCYTE IS PROBABLY THE SMALLEST OF ALL SHARKS
ABOUT MM IN DIAMETER AND NUTRITION OF THE EMBRYO
IS ALMOST COMPLETELY MATROTROPHIC 0LACENTATION COM
MENCES SOON AFTER IMPLANTATION AND THE FOETUS IS DE
PENDENT UPON ITS MOTHER UNTIL PARTURITION 4HE UTERINE
WALL FORMS STALKED RICHLY VASCULAR GOBLET SHAPED
42/0(/.%-!4/53 #503 INTO WHICH THE FOETAL PORTION
OF EACH PLACENTA lTS &IGURE 4HIS PLACENTA IS
HIGHLY VASCULAR AND THE BARRIERS TO THE EXCHANGE OF NU
TRIENTS ARE GREATLY REDUCED BY THE ELIMINATION OF THE
EGG CAPSULE AND POSSIBLE DEGENERATION OF THE UTERINE
EPITHELIUM DURING LATE DEVELOPMENT )T IS ASSUMED THAT
MATERNAL NUTRIENTS ARE CONVEYED TO THE EMBRYO BOTH
BY HAEMATROPHIC TRANSFER ACROSS THE PLACENTA AND BY
IMBIBITION OF UTERINE mUID INTO THE GUT IN THE ABSENCE
OF PHYSIOLOGICAL STUDIES IT IS NOT POSSIBLE TO DETERMINE
THE RELATIVE CONTRIBUTION FROM EACH SOURCE !S MIGHT
BE EXPECTED IN THE VIRTUAL ABSENCE OF YOLK THERE IS
NO DUCTUS VITELLO INTESTINALIS OR ELSE IT IS OBLITERATED
EARLY IN DEVELOPMENT &IGURES " # 4HE UM
BILICAL STALK BECOMES EXTREMELY LONG AND IS ADORNED
BY ABUNDANT LONG APPENDICULAE WHOSE DENSE CAPIL
LARY BEDS CLOSELY UNDERLYING THE THIN EPITHELIUM IM
POSE THEIR EMBOSSED CABLE LIKE PATTERN ON THE SURFACE
&IGURES ! $ )T SEEMS LIKELY THAT THE MAJOR FUNC
TION OF THE APPENDICULAE IS GAS EXCHANGE BUT THEY MAY
ALSO PARTICIPATE IN OTHER ACTIVITIES SUCH AS EXCRETION
6IVIPARITY IN #OELACANTHS
,ATIMERIA CHALUMNAE IS VIVIPAROUS 7OURMS !TZ AND
3TRIBLING 4HE EGGS ARE REMARKABLY LARGE AND
CONTAIN MASSIVE AMOUNTS OF YOLK %ACH FOETUS IS CON
TAINED WITHIN ITS OWN WELL VASCULARIZED COMPARTMENT
WITHIN THE UTERINE REGION OF THE RIGHT OVIDUCT &IGURE
%MBRYOS ARE LECITHOTROPHIC DURING THE EARLY AND
MIDDLE STAGES OF DEVELOPMENT WITH OOPHAGY THE IN
GESTION OF SUPERNUMERARY EGGS BY DEVELOPING YOUNG
AS A PROBABLE SOURCE OF ADDITIONAL NUTRIENTS 4HE YOLK
SAC OF LATE TERM FOETUSES IS LARGE mACCID HEAVILY VAS
CULARIZED AND NEARLY DEVOID OF YOLK &IGURE
! MASSIVE VASCULAR PLEXUS DEVELOPS IN THE WALL OF THE
UTERINE COMPARTMENT AT ITS SITE OF CONTACT WITH THE YOLK
SAC AND TOGETHER THESE RICHLY VASCULARIZED TISSUES FORM
A YOLK SAC PLACENTA 3INCE THERE IS NO INTERDIGITATION OF
MATERNAL AND FOETAL TISSUE THE YOLK SAC IS FREE TO MOVE
AND THE PLACENTA IS SAID TO BE NON ADHERENT OR TRANS
POSABLE 2EGIONS OF THE UTERINE WALL THAT ARE ADJACENT
TO OTHER PARTS OF THE FOETUS DO NOT DEVELOP THIS RICH
VASCULARIZATION NOR IS IT SEEN IN THE NON GRAVID UTERUS
4HE PLACENTAL REGIONS OF THE UTERINE LINING ARE EM
BOSSED BY AN ANASTOMOSING NETWORK OF CAPILLARIES
COVERED BY A THIN SIMPLE SQUAMOUS EPITHELIUM WHOSE
SURFACE MAY BE AMPLIlED EITHER BY PLEATS RIDGES
OR BRANCHING PROCESSES &IGURE ! "ENEATH THE
CAPILLARY NETWORK LIES A SUBCORTICAL SINUS THAT APPEARS
TO BE LINED BY ENDOTHELIUM 3URROUNDING THIS ARE A
WELL VASCULARIZED CONNECTIVE TISSUE STROMA ALTERNATING
LAYERS OF TRANSVERSE AND LONGITUDINAL SMOOTH MUSCLE
AND A SIMPLE SQUAMOUS SEROSAL EPITHELIUM &IGURE
"
-OST OF THE WALL OF THE YOLK SAC CONSISTS OF A DENSE
STROMA OF lBROUS CONNECTIVE TISSUE &IGURE #
6)6)0!2)49
)TS EXTERNAL SURFACE IS CONVOLUTED AND FOLDED &IGURES
$ % AND CONSISTS A SIMPLE SQUAMOUS EPITHELIUM
ADHERING CLOSELY TO AN INTERCOMMUNICATING BED OF COR
TICAL SINUSES PRESUMABLY DERIVED FROM THE VITELLINE
CIRCULATION 4HE INTERNAL SURFACE IS LACED WITH BLOOD
VESSELS FROM THE VITELLINE CIRCULATION AND IS LINED BY A
LAYER OF YOLK
DIGESTING ENDODERM AND SYNCYTIAL CELLS
4HE PRIMARY FUNCTION OF THE YOLK SAC PLACENTA IS
PRESUMED TO BE GAS EXCHANGE AND THE EXCHANGE OF MA
TERIALS OF LOW MOLECULAR WEIGHT SUCH AS METABOLITES
AND METABOLIC WASTES 4HERE IS LITTLE EVIDENCE THAT
UTERINE HISTOTROPH PLAYS A SIGNIlCANT ROLE IN NUTRITION
OF THE EMBRYOS AND OOPHAGY MAY WELL BE THE MAJOR
SOURCE OF SUPPLEMENTAL NUTRITION
6IVIPARITY IN 4ELEOSTS
6IVIPARITY HAS EVOLVED INDEPENDENTLY IN SEVERAL GROUPS
FROM TWO ORDERS OF TELEOSTS #YPRINODONTIFORMES AND
0ERCIFORMES (OAR 7AKE )N THE ABSENCE
OF -LLERIAN DUCTS THERE ARE NO UTERI OR TRUE OVIDUCTS
AND A CHANNEL TO THE EXTERIOR IS FORMED EITHER FROM A
SHEATH OF PERITONEAL FOLDS OUTLYING THE OVARY OR FROM
THE TISSUE OF THE OVARY ITSELF 3INCE THESE STRUCTURES
CONDUCT GENITAL PRODUCTS TO THE OUTSIDE IT IS APPROPRIATE
TO DESIGNATE THEM hOVIDUCTSv ALTHOUGH THEY ARE NOT HO
MOLOGOUS WITH OVIDUCTS OF OTHER VERTEBRATES "ECAUSE
OF THEIR ORIGINS HOWEVER THEY LACK THE COMPETENCY FOR
HYPERVASCULARIZATION AND SECRETION THAT IS REQUIRED OF
A NUTRITIVE CHAMBER AND INSTEAD THE CYSTOVARIAN OVARY
OF ALL VIVIPAROUS TELEOSTS PROVIDES THE HOSPITABLE EN
VIRONMENT REQUIRED FOR GESTATION THE LUMEN IS LINED
WITH PERITONEUM AND THE DEVELOPING EMBRYOS ARE SHED
INTO THIS SANCTUARY INSTEAD OF BEING RELEASED INTO THE
COELOM AS IN OTHER VERTEBRATES &IGURE
&ERTILIZATION IS INTERNAL IN VIVIPAROUS ANIMALS !S
FAR AS IS KNOWN IN ALL TELEOSTS WITH THE EXCEPTION OF
:OARCES IT OCCURS WITHIN THE OVARIAN FOLLICLES 3PERM
ARE DEPOSITED IN THE OVIDUCTS AND OVARIAN LUMEN WHERE
THEY MAY BE STORED FOR LONG PERIODS BEING NOURISHED
BY CELLS OF THE LUMINAL EPITHELIUM &IGURES AND
*ALABERT AND "ILLARD .AGAHAMA
0USEY AND 3TEWART "URNS ET AL -U
OZ #ASADEVALL AND "ONET ! DIVERTICULUM
OF THE LUMEN MAY FORM A 3%-).!, 2%#%04!#,% LINED
BY A SIMPLE EPITHELIUM RESTING ON A PROMINENT BASAL
LAMINA SPERM HEADS APPEAR TO BE EMBEDDED WITHIN
THE EPITHELIAL CELLS &IGURES AND &OR THE
SEVERAL MONTHS BETWEEN COPULATION AND FERTILIZATION
IN #YMATOGASTER AGGREGATA SPERM ARE HELD WITHIN
SPERM POCKETS IN THE LUMINAL EPITHELIUM UNDERGOING
NO MORPHOLOGICAL CHANGES DETECTABLE WITH THE ELECTRON
MICROSCOPE 'ARDINER 4HE SPERM HEADS MAIN
TAIN A CLOSE ASSOCIATION WITH THE UNSPECIALIZED CELLS
LINING THE POCKETS BUT THE PLASMA MEMBRANES OF EACH
SPERM AND EPITHELIAL CELL REMAIN INTACT SEPARATED BY A
SPACE OF SEVERAL NANOMETERS &IGURE !BOUT ONE
MONTH AFTER FERTILIZATION RESIDUAL SPERM ARE NO LONGER
HOUSED WITHIN THE POCKETS AND HAVE EITHER BEEN TAKEN
UP BY GRANULOCYTES OR CONSUMED BY THE DEVELOPING
EMBRYOS
3IMILAR RETENTION OF SPERM OCCURS IN THE OVIDUCT
OF THE OVIPAROUS POECILIID PLATYlSH 8IPHOPHORUS
MACULATUS 0OTTER AND +RAMER 4HE OVIDUCT
OR '/./$5#4 IS LINED BY SIMPLE TO PSEUDOSTRATIlED
MESOTHELIUM DERIVED FROM THE LINING OF THE OVAR
IAN LUMEN &IGURE !N ELABORATE ARRAY OF SURFACE
MODIlCATIONS FESTOONS THE CELLS OF THE LINING SCALLOPS
LOBULAR EXTENSIONS MICROVILLI MICROVILLOUS APPEND
AGES AND DEEP INTRACELLULAR INVAGINATIONS &IGURE
4HE SPERM BECOME ASSOCIATED WITH SPECIAL EPITHELIAL
CELLS 30%2-
!33/#)!4%$ #%,,3 THAT LACK EXTENSIVE SUR
FACE MICROVILLI BUT CONTAIN AN ARRAY OF DEEP SURFACE
PITS AND POCKETS 4HE SPERM LIE EITHER WITHIN THE IN
VAGINATIONS OR ARE TAKEN UP AND INCORPORATED WITHIN
THE CYTOPLASM OF THESE CELLS &IGURE )NTACT SPERM
NUCLEI NECK MITOCHONDRIA AND mAGELLA CAN BE SEEN
WITHIN THE PITS AND POCKETS WHILE SPERM NUCLEI WITH
OUT mAGELLA OR OTHER ORGANELLES OCCUR DEEP WITHIN THE
CYTOPLASM OF THE SPERM
ASSOCIATED CELLS 4HERE IS NO
INDICATION OF LYSOSOMAL ACTIVITY OR SPERM BREAKDOWN
2EJECTION OF SPERM BY THE IMMUNE SYSTEM OF THE FE
MALE IS PROBABLY AVERTED BY THE BARRIER PROVIDED BY
APICAL JUNCTIONAL COMPLEXES BETWEEN THE EPITHELIAL
CELLS &IGURE !
!T THE TIME OF FERTILIZATION OVARIAN FOLLICLES AP
PROACH THE INSIDE OF THE LUMINAL EPITHELIUM AND A
SMALL DEPRESSION OR $%,,% MAY FORM IN THE EPITHELIUM
&IGURE CREATING A THIN MEMBRANE BETWEEN
SPERM AND EGG .AGAHAMA 0RESUMABLY A
SPERM PENETRATES THIS THIN BARRIER AND FERTILIZATION IS
EFFECTED IN THE ABSENCE OF A MICROPYLE 3MALL POCKETS
OF THE LUMINAL EPITHELIUM EXTEND TOWARD THE MATURE
FOLLICLES IN (ETERANDRIA FORMOSA FORMING A THIN EPI
THELIAL DISC PRESSED AGAINST THE FOLLICULAR EPITHELIUM
&IGURE ! &RASER AND 2ENTON 7HEN THE
OVUM IS READY FOR FERTILIZATION IT EXTENDS A SPHERI
CAL PROTRUBERANCE TOWARD THE LUMINAL POCKET &IGURE
" ,ARGE NUMBERS OF SPERM SWARM TOWARD THE
THIN MEMBRANE SEPARATING THEM FROM THE OVUM AND
#(!04%2
ONE OF THEM MUST PENETRATE TO EFFECT FERTILIZATION !FTER
ENTRANCE OF THE SPERM THE PROTRUBERANCE IS WITHDRAWN
AND THE EPITHELIUM OF THE FOLLICLE AND THAT OF THE POCKET
FORM A PLUG OF CELLS THAT PROJECTS INTO THE OVARIAN LU
MEN &IGURE #
#LEAVAGE COMMENCES AND DEVELOPMENT BEGINS
WITHIN THE FOLLICLE !T SOME POINT THE EGG IS EXPELLED
INTO THE OVARIAN LUMEN AND DEVELOPMENT IS COMPLETED
7OURMS )N SOME SPECIES MOST DEVELOPMENT
OCCURS WITHIN THE FOLLICLE SO THAT GESTATION IS &/,,)#5
,!2 AND A HIGHLY ADVANCED EMBRYO IS RELEASED INTO THE
LUMEN )N ,5-).!, GESTATION THE EMBRYO IS RELEASED
INTO THE LUMEN AT AN EARLY STAGE AND MOST DEVELOPMENT
OCCURS WITHIN THE OVARIAN LUMEN *ENYNSIA IS AN INTER
MEDIATE FORM WHERE THE lRST HALF OF DEVELOPMENT OC
CURS WITHIN THE FOLLICLE AND THE LATTER HALF WITHIN THE
OVARIAN LUMEN )N ALL SITUATIONS THE EMBRYO IS ENVEL
OPED BY A RICHLY VASCULARIZED NUTRITIVE EPITHELIUM THAT
HAS BEEN PROVIDED BY THE OVARY $EPENDING ON WHETHER
GESTATION IS FOLLICULAR OR LUMINAL THE EMBRYOS UNDERGO
A LONGER OR SHORTER SOJOURN IN THE OVARIAN LUMEN BEFORE
BEING RELEASED TO THE EXTERIOR IN THE PROCESS OF PARTURI
TION 3INCE THERE IS NO DIRECT CONTACT BETWEEN MATERNAL
AND FOETAL MEMBRANES THE TRANSFER OF NUTRIENTS GASES
ELECTROLYTES AND WASTES IN MATROTROPHIC SPECIES IS
MEDIATED THROUGH A VISCOUS SECRETION OF THE FOLLICULAR
OR LUMINAL EPITHELIA THE %-"29/42/0( 3CHINDLER AND
(AMLETT )NDEED RICHLY VASCULAR POSTOVULATORY
FOLLICLES MAY CONTINUE TO BE ACTIVE AND CONTRIBUTE TO
THE EMBRYOTROPH DURING LUMINAL GESTATION +ORSGAARD
6IVIPARITY IN SEVERAL SPECIES OF TWO GENERA OF
HALFBEAKS (EMIRAMPHIDAE HAS BEEN DIVIDED INTO lVE
CATEGORIES DEPENDING ON WHETHER DEVELOPMENT IS FOL
LICULAR OR LARGELY LUMINAL AS WELL AS UPON THE DEGREE
OF LECITHOTROPHYMATROTROPHY PRESENT -EISNER AND
"URNS
&/,,)#5,!2 '%34!4)/.
&OLLICULAR GESTATION WHERE THE EMBRYO DEVELOPS WITHIN
THE OVARIAN FOLLICLE IS KNOWN TO OCCUR IN TWO FAMILIES
OF 0ERCIFORMES ,ABRISOMIDAE AND #LINIDAE AND THREE
FAMILIES OF #YPRINODONTIFORMES 0OECILIIDAE (EMIR
AMPHIDAE AND !NABLEPIDAE 3CHINDLER AND (AM
LETT 4HE EVOLUTION OF FOLLICULAR GESTATION HAS
REQUIRED THE SOLUTION OF SEVERAL FUNCTIONAL PROBLEMS
'ROVE AND 7OURMS SPERMATOZOA MUST CROSS
THE FOLLICULAR WALL FOR FERTILIZATION TO OCCUR THE SITE
OF GESTATION MUST BE COMPARTMENTALIZED FROM OTHER
MATERNAL TISSUES IN ORDER TO MAINTAIN THE APPROPRIATE
ENVIRONMENT FOR EMBRYONIC DEVELOPMENT AND TO PRO
TECT THE EMBRYO FROM THE MATERNAL IMMUNE SYSTEM
AND THERE MUST BE METABOLIC EXCHANGE BETWEEN THE
MOTHER AND THE EMBRYO )N ADDITION IN THOSE SPECIES
WHERE EMBRYONIC NUTRITION IS MATROTROPHIC NUTRIENTS
MUST CROSS THE FOLLICULAR EPITHELIUM
)N SOME SPECIES THE FOLLICLE IS LITTLE MORE THAN A
PASSIVE HOLDING CHAMBER FOR THE EMBRYO WHILE IN
OTHERS ITS WALL BECOMES SECRETORY AND RICHLY VASCU
LAR PROVIDING NUTRIENTS AND CARRYING AWAY WASTES
/FTEN THE SECRETIONS OF THE FOLLICULAR EPITHELIUM ARE
ENHANCED BY INCREASES IN ITS SURFACE AREA PROVIDED BY
ELABORATIONS SUCH AS VILLI OR RIDGES 4HESE STRUCTURES
CONSTITUTE THE MATERNAL CONTRIBUTION TO THE hFOLLICULAR
PLACENTAv THE FOETAL COMPONENT IS A CLOSELY APPOSED
RICHLY VASCULAR AND EXPANDED PERICARDIAL SAC AND
YOLK SAC 7OURMS 'ROVE AND 7OURMS
4HIS MATERNAL EMBRYONIC ASSOCIATION VARIES WITH THE
QUANTITY OF YOLK IN THE EGG (OAR )F YOLK
IS ABUNDANT THE FOLLICULAR WALL MERELY BECOMES l
BROUS AND VASCULAR AND INTIMATELY ASSOCIATED WITH THE
EXPANDED PERICARDIAL SAC OF THE EMBRYO 0OECILIIDAE
)F THE YOLK MASS IS SMALL BOTH THE FOLLICULAR WALL AND
THE EMBRYO ARE MODIlED TO FORM A VASCULAR LOOSE PLA
CENTAL TYPE OF INTERCONNECTION !NABLEPIDAE
!LTHOUGH THERE SEEMS TO BE LITTLE MATERNAL EMBRY
ONIC TRANSFER OF NUTRIENTS IN THE GUPPY ,EBISTES RETICU
LATUS 0OECILIIDAE THERE ARE STRUCTURAL RESPONSES TO
THE PRESENCE OF AN EMBRYO *OLLIE AND *OLLIE A B
PERHAPS THE FOLLICULAR PLACENTA PROVIDES FOR RESPIRA
TORY AND OSMOREGULATORY DEMANDS DURING GESTATION
3CHINDLER AND (AMLETT !S THE EMBRYO DE
VELOPS VASCULARITY OF THE FOLLICLE INCREASES AND TONO
lLAMENTS APPARENTLY ASSOCIATED WITH DESMOSOMES
ACCUMULATE WITHIN CELLS OF THE THECAL LAYERS STRENGTH
ENING THE FOLLICLE THERE APPEARS TO BE NO INCREASE IN
THE NUMBER OF COLLAGENOUS lBRES *OLLIE AND *OLLIE
B 4HE MATERNAL PORTION OF THE 0,!#%.4! IS THE
RICHLY VASCULAR PORTION OF THE FOLLICULAR WALL WHERE MA
TERNAL CAPILLARIES APPROXIMATE EMBRYONIC CAPILLARIES
OF THE YOLK SAC &IGURE )N THIS REGION THE ZONA
PELLUCIDA DISAPPEARS ABOUT THREE TO FOUR WEEKS AFTER
FERTILIZATION 4HE FOLLICULAR EPITHELIUM IS COMPOSED
OF ACTIVELY PINOCYTOTIC SQUAMOUS CELLS THAT RESEMBLE
4HE WORD hOVULATIONv IS SOMETIMES USED FOR THE RELEASE OF A FERTILIZED EMBRYO OF VIVIPAROUS SPECIES FROM THE FOLLICLE INTO THE OVARIAN LU
MEN 4HIS USAGE SEEMS INAPPROPRIATE AND THE TERM hHATCHINGv IS PREFERRED
6)6)0!2)49
ENDOTHELIAL CELLS .O EMBRYONIC VASCULARITY IS EVIDENT
IN REGIONS WHERE THE ZONA PELLUCIDA IS STILL PRESENT IN
THE SPACE BETWEEN THE FOLLICULAR WALL AND EMBRYONIC
SURFACE AND THE FOLLICULAR WALL IS LARGELY AVASCULAR AND
THINNER 4HE 0,!#%.4!, "!22)%2 AT THE TIME OF CLOSEST
APPROXIMATION OF MATERNAL AND FOETAL BLOOD CONSISTS
OF SIX OR SEVEN LAYERS MATERNAL CAPILLARY ENDOTHELIUM
MATERNAL CAPILLARY BASEMENT MEMBRANE INNER FOL
LICULAR EPITHELIUM FERTILIZATION MEMBRANE IF PRESENT
FOETAL YOLK SAC EPITHELIUM FOETAL CAPILLARY BASEMENT
MEMBRANE AND FOETAL CAPILLARY ENDOTHELIUM -ICROPI
NOCYTOSIS APPEARS TO BE THE ONLY MECHANISM BY WHICH
TRANSPLACENTAL EXCHANGE IS EFFECTED AND MICROPINOCY
TOTIC VESICLES ARE ABUNDANT IN ALL CELLULAR LAYERS OF THE
BARRIER !LTHOUGH THERE ARE DISTINCT CHANGES IN THE STE
ROIDOGENIC POTENTIAL OF THE FOLLICLES DURING THE REPRO
DUCTIVE CYCLE OF THE GUPPY NO PARTICULAR STEROID SEEMS
TO BE INVOLVED IN MAINTAINING GESTATION 6ENKATESH ET
AL
'ROVE AND 7OURMS DESCRIBE GESTATION IN
(ETERANDRIA FORMOSA A MATROTROPHIC SPECIES WHERE
EMBRYOS INCREASE IN DRY WEIGHT ABOUT FOLD DUR
ING DEVELOPMENT WITHIN THE OVARIAN FOLLICLE .UTRI
ENT TRANSFER IS PRESUMED TO OCCUR ACROSS A FOLLICULAR
PLACENTA THAT IS FORMED BY THE CLOSE APPOSITION OF THE
EMBRYONIC SURFACE TO THE FOLLICULAR EPITHELIUM h%M
BRYONIC SURFACEv INCLUDES THE ENTIRE BODY SURFACE DUR
ING EARLY GESTATION AND THE PERICARDIAL AMNION
SEROSA
DURING MID AND LATE GESTATION 4HE SINGLE HOLLOW OVA
RY OCCUPIES MOST OF THE BODY CAVITY IN GRAVID FEMALES
&IGURE "ECAUSE ( FORMOSA DISPLAYS SUPERFOE
TATION EMBRYOS AT ABOUT lVE STAGES OF DEVELOPMENT
MAY BE OBTAINED FROM THE SAME OVARY %MBRYOS AT
THREE STAGES OF DEVELOPMENT ARE VISIBLE IN THE lGURE
4HE OVARY CONSISTS OF AN OUTER SIMPLE EPITHELIUM AN
OVIGEROUS STROMA OF CONNECTIVE TISSUE AND AN INNER
SIMPLE EPITHELIUM THAT LINES THE LUMEN 4HE LUMEN IS
CONNECTED TO THE EXTERIOR BY A SHORT DUCT JUST POSTERIOR
TO THE ANUS 0OCKETS OF THE LUMEN PENETRATE THE STROMA
AND EXTEND BETWEEN THE FOLLICLES %ACH FOLLICLE IS SUP
PLIED WITH BLOOD FROM A MEDIAN DORSAL BLOOD VESSEL
THAT BRANCHES EXTENSIVELY ALONG THE LENGTH OF THE OVARY
4HE BLOOD SUPPLY TO INDIVIDUAL FOLLICLES INCREASES AFTER
FERTILIZATION BY DEVELOPMENT OF AN EXTENSIVE CAPILLARY
NETWORK AT THE BASE OF THE FOLLICULAR EPITHELIUM
$URING VITELLOGENESIS THE ZONA PELLUCIDA AND FOL
LICULAR EPITHELUM ARE TYPICAL OF THOSE OF OTHER TELEOSTS
&IGURE 4HE ZONA PELLUCIDA IS A DENSE MATRIX
PENETRATED BY MICROVILLI FROM THE OOCYTE 4HE SIMPLE
CUBOIDAL EPITHELIUM OF THE FOLLICLE LACKS THE MEMBRANE
SPECIALIZATIONS TYPICAL OF TRANSPORTING CELLS APICAL
MICROVILLI JUNCTIONAL COMPLEXES AND BASAL SURFACE
SPECIALIZATIONS 4HE NUMEROUS MICROVILLI THAT EXTEND
THROUGH THE EGG ENVELOPE FROM THE OOCYTE ARE CLOSELY
ASSOCIATED WITH THE FOLLICULAR CELLS AND EXTEND INTO SUR
FACE INVAGINATIONS !PICAL LATERAL AND BASAL COATED
PITS AND COATED VESICLES ARE PROMINENT &OLLICULAR CELLS
ARE CLOSELY APPLIED TO EACH OTHER ALONG THEIR LATERAL
SURFACES BUT NO JUNCTIONAL COMPLEXES DESMOSOMES OR
LATERAL INFOLDINGS ARE PRESENT 4HE FOLLICULAR EPITHELI
UM RESTS ON A WELL DEVELOPED BASAL LAMINA /NLY A FEW
CAPILLARIES ARE ASSOCIATED WITH THE FOLLICLE !S IN OTHER
TELEOSTS YOLK PROTEINS AND OTHER METABOLITES DESTINED
FOR THE OOCYTE LIKELY CROSS THE FOLLICULAR EPITHELIUM BY
AN INTRACELLULAR ROUTE 4HE PRESENCE OF COATED PITS AND
VESICLES AS WELL AS OTHER VESICULAR STRUCTURES INDICATES
THAT FOLLICULAR CELLS MAY ALSO ABSORB AND PROCESS EXOG
ENOUS PROTEINS
&OLLICULAR CELLS UNDERGO A DRAMATIC CHANGE IN MOR
PHOLOGY AFTER FERTILIZATION AND ACQUIRE THE ULTRASTRUC
TURAL FEATURES TYPICAL OF TRANSPORTING CELLS *UNCTIONAL
COMPLEXES ARE SEEN AT AN EARLY STAGE &IGURE
APICAL MICROVILLI AND SURFACE INVAGINATIONS APPEAR LAT
ER 4HE ZONA PELLUCIDA NOW CALLED THE EGG ENVELOPE IS
MUCH THICKER THAN THAT OF VITELLOGENIC OOCYTES AND IS
NOT PERFORATED BY MICROVILLI $ENSE EXTRACELLULAR MA
TERIAL LIES BETWEEN THE EGG ENVELOPE AND THE FOLLICULAR
CELLS #APILLARIES OF THE FOLLICULAR CIRCULATION LIE BE
NEATH THE WELL DEVELOPED BASAL LAMINA &IGURE
"Y THE TIME EMBRYOS REACH THE EARLY TAILBUD STAGE
THE FOLLICULAR PLACENTA IS FULLY DIFFERENTIATED AND THE
ULTRASTRUCTURE OF THE FOLLICULAR CELLS INDICATES BY DIS
PLAYING APICAL MICROVILLI APICAL JUNCTIONAL COMPLEXES
SURFACE INVAGINATIONS AND AN EXTENSIVELY FOLDED BASAL
SURFACE THAT THE FOLLICULAR EPITHELIUM IS SPECIALIZED FOR
MATERNAL EMBRYONIC TRANSPORT &IGURES AND
!PICAL AND BASAL COATED PITS ARE PRESENT 4HE CYTO
PLASM CONTAINS GRANULAR ENDOPLASMIC RETICULUM 'OLGI
COMPLEXES AND ELECTRON DENSE VESICLES THAT MAY BE
LYSOSOMES .UMEROUS APICAL ELECTRON LUCENT VESICLES
APPEAR TO BE DERIVED FROM THE APICAL SURFACE AND MAY
INDICATE THAT THESE FOLLICULAR CELLS ABSORB AND PROCESS
FOLLICULAR mUID 4HE WELL DEVELOPED JUNCTIONAL COM
PLEXES BETWEEN THE FOLLICULAR CELLS FORM A BARRIER TO
THE FREE MOVEMENT OF LARGE MOLECULES AND IONS AND EF
FECTIVELY ISOLATE THE EMBRYO FROM THE MOTHER THIS BAR
RIER MAY BE IMPORTANT FOR IMMUNOLOGICAL PROTECTION
OF THE EMBRYO PREVENTING ITS REJECTION BY THE MOTHER
4HE EGG ENVELOPE WHICH LACKS PERFORATIONS AND RE
MAINS INTACT THROUGHOUT GESTATION BECOMES PROGRES
#(!04%2
SIVELY THINNER AND LESS DENSE AS GESTATION PROCEEDS
0RESUMABLY NUTRIENT MOLECULES IN THE MATERNAL CIRCU
LATION CROSS THE CAPILLARY ENDOTHELIUM EITHER BY DIFFU
SION OR TRANSCYTOSIS CROSS THE BASAL LAMINAE SEPARATING
THE CAPILLARIES AND FOLLICULAR EPITHELIUM AND THEN
CROSS THE FOLLICULAR EPITHELIUM BY A TRANSCELLULAR ROUTE
.UTRIENT MOLECULES ENTERING THE INTRAFOLLICULAR SPACE
THEN CROSS THE EGG ENVELOPE TO BE ABSORBED BY SURFACE
CELLS OF THE EMBRYO %XTENSIVE FOLDING OF THE BASAL
SURFACE OF THE FOLLICULAR CELLS AND THE POSSIBILITY THAT
THE EGG ENVELOPE MAY ACT AS A MOLECULAR lLTER SUGGEST
THAT MOLECULES OF LOW MOLECULAR WEIGHT MAY CONSTI
TUTE A SIGNIlCANT PART OF THE NUTRIENT TRAFlC ACROSS THE
FOLLICULAR PLACENTA -ORPHOLOGICAL EVIDENCE OF MAC
ROMOLECULAR UPTAKE BY FOLLICULAR CELLS AND THE EMBRY
ONIC SURFACE IS PROVIDED BY THE ENDOCYTOTIC PITS AND
VESICLES AT THE BASE OF THE FOLLICULAR EPITHELIUM AND ON
THE SURFACE OF ABSORPTIVE CELLS ON THE EMBRYO
!N EXTREME OF MATROTROPHIC NUTRITION IS SEEN IN THE
FOUR EYED lSH !NABLEPS SPP WHERE EMBRYOS INCREASE
IN DRY WEIGHT BY AS MUCH AS TIMES DURING GES
TATION 4URNER A +NIGHT ET AL .UTRIENT
TRANSFER IS FACILITATED WITHIN THE FOLLICULAR PLACENTA BY
INCREASES IN SURFACE AREA PROVIDED BY RICHLY VASCULAR
HEMISPHERICAL PROJECTIONS THE 6!3#5,!2 "5,"3 ON THE
PERICARDIAL SAC IN ADDITION MICROPLICAE ON THE SURFACE
OF THE BULBS FURTHER AMPLIFY THEIR SURFACE AREA FOR EX
CHANGE &IGURE $URING MID TO LATE GESTATION
THE JUXTAEMBRYONIC FOLLICULAR EPITHELIUM DIFFERENTIATES
INTO TWO REGIONS A REGION OF SHALLOW PITS WHERE THE
VASCULAR BULBS COME TO INTERDIGITATE IN A BALL AND SOCK
ET FASHION WITH THE FOLLICULAR WALL &IGURES ! TO
& AND A REGION WHERE THE FOLLICULAR EPITHELIUM FORMS
LONG VASCULAR VILLOUS EXTENSIONS &IGURES ' (
4HE FOLLICULAR CELLS OF BOTH REGIONS APPEAR TO CONSTI
TUTE A TRANSPORTING RATHER THAN A SECRETORY EPITHELIUM
.O EGG MEMBRANE INHIBITS THE EXCHANGE OF MATERIALS
BY INTERVENING IN THE mUID lLLED SPACE BETWEEN THE
MATERNAL AND EMBRYONIC EPITHELIA &IGURE 0L
)N TERMS OF PERCENTAGE WEIGHT INCREASE THE FOLLICULAR
PLACENTA OF !NABLEPS APPEARS TO BE THE MOST EFlCIENT
ADAPTATION FOR MATERNAL EMBRYONIC NUTRIENT TRANSFER IN
TELEOST lSHES AND CLOSELY APPROXIMATES THE EFlCIENCY
OF OOPHAGY AND EMBRYONIC CANNIBALISM OF LAMNOID
SHARKS
#LINUS SUPERCILIOSIS IS A MATROTROPHIC CLINID /RDER
0ERCIFORMES THAT BREEDS ALL YEAR ROUND AND EXHIBITS
EXTREME SUPERFOETATION AS MANY AS BROODS MAY
BE FOUND WITHIN THE OVARY OF A SINGLE FEMALE 6EITH
B !UTORADIOGRAPHIC STUDIES REVEAL THAT NUTRIENTS
IN THE FORM OF AMINO ACIDS ARE SECRETED BY THE FOLLICU
LAR EPITHELIUM AND ABSORBED BY EMBRYOS OF # SUPER
CILIOSUS AND # DORSALIS WITHIN THE FOLLICLE ESPECIALLY
BY THE EPIDERMIS INCLUDING THAT OF THE lNS AND THE
GUT 6EITH #ORNISH
,5-).!, '%34!4)/.
4HE OVARIAN EPITHELIUM PLAYS THE DOMINANT ROLE IN THE
TRANSFER OF NUTRIENTS FROM THE MOTHER TO THE EMBRYO
DURING LUMINAL GESTATION IN MATROTROPHIC SPECIES (OAR
3CHINDLER )N EARLY STAGES OF GESTATION THE
EPITHELIAL CELLS OF THE OVIGERIOUS FOLDS BECOME HYPER
TROPHIED AND THERE IS INCREASED VASCULARIZATION OF THE
SUPPORTING CONNECTIVE TISSUE 3INCE THERE IS NO ATTACH
MENT BETWEEN MATERNAL AND FOETAL TISSUES THE PASSAGE
OF ALL SUBSTANCES IS MEDIATED BY WAY OF %-"29/42/0(
3CHINDLER AND (AMLETT /VIGEROUS FOLDS MAY
FORM COMPARTMENTS AROUND THE EMBRYOS INCREASING
SURFACE AREA OF CONTACT AND ENHANCING EFlCIENT NUTRI
ENT TRANSFER &IGURES AND 6ARIOUS ORGANS
HAVE EVOLVED INTO A RANGE OF STRUCTURES FOR THE TRANSFER
OF NUTRIENTS 4ABLE 7OURMS 7AKE
7OURMS 'ROVE AND ,OMBARDI 3CHINDLER AND
(AMLETT ,EAF
LIKE EXTENSIONS FROM THE LUMINAL
WALL OF THE OVARY MAY PARTLY lLL THE GILL CAVITIES AND
MOUTH OF THE EMBRYO &IGURE TO PROVIDE A SPE
CIALIZED ORGAN FOR TRANSFER OF MATERIALS BETWEEN ADULT
AND EMBRYO 4HE YOLK SAC PERICARDIAL SAC AND COELO
MIC SAC PLAY A MAJOR ROLE IN NUTRIENT UPTAKE IN SEVERAL
SPECIES &IGURE mAT VASCULAR EXTENSIONS OF SOFT
ABSORPTIVE TISSUE GROW BETWEEN THE RAYS OF THE VERTICAL
lNS OF %MBIOTOCIDAE IN A FEW TELEOSTS lNGER
SHAPED
OR RIBBON
LIKE EXTENSIONS OF THE PROCTODAEUM THE 42/
0(/4!%.)!% TAKE UP MATERIALS FROM THE EMBRYOTROPH
&IGURE /THER NUTRITIVE DEVICES HAVE ALSO BEEN
DESCRIBED BUT BY FAR THE GREATEST AMOUNT OF MORPHO
LOGICAL AND PHYSIOLOGICAL STUDY HAS BEEN DIRECTED TO
THE TROPHOTAENIAE OF GOODEIDS
/VARIAN ,UMINAL %PITHELIUM
4HE WALL OF THE CYSTOVARIAN OVARY OF VIVIPAROUS TELE
OSTS CONSISTS OF FOUR LAYERS THE LUMINAL EPITHELIUM
CONNECTIVE TISSUE STROMA A LAYER OF SMOOTH MUSCLE
AND PERITONEUM 4HE LUMEN MAY BE PARTITIONED BY
OVIGEROUS FOLDS WHOSE EPITHELIUM AND CONNECTIVE
TISSUE CORE ARE CONTINUOUS WITH THOSE OF THE OVARIAN
WALL SOME OF THE OVIGEROUS FOLDS ENCLOSE DEVELOPING
FOLLICLES &IGURES AND 4HE CONNECTIVE TISSUE
6)6)0!2)49
4!",% 4ROPHIC PATTERNS IN VIVIPAROUS lSHES &ROM 7OURMS
) &ACULTATIVE VIVIPARITY
)) /BLIGATE VIVIPARITY
! ,ECITROPHY
" -ATROTROPHY
/OPHAGY AND ADELPHOPHAGY
0LACENTAL ANALOGUES
A %PIDERMIS AND lN EPITHELIUM
B 'ILL EPITHELIUM
C 4ROPHONEMATA
D "RANCHIAL PLACENTA
E 9OLK SAC
F 0ERICARDIAL AMNION AND CHORION
G &OLLICULAR PSEUDOPLACENTA
H (YPERTROPHIED GUT
I 4ROPHOTAENIAE
9OLK SAC PLACENTA
STROMA CONTAINS NUMEROUS STELLATE lBROBLASTS BUNDLES
OF COLLAGENOUS lBRES TO M IN DIAMETER AND LARGE
BLOOD VESSELS A WELL
DEVELOPED CAPILLARY BED IS AP
POSED TO THE BASAL LAMINA OF THE EPITHELIUM &IGURES
! AND # 4HE MUSCLE CONSISTS OF A THIN
OUTER SHEET OF LONGITUDINAL lBRES AND AN INNER CIRCULAR
LAYER &IGURE ! ,OMBARDI AND 7OURMS A
4HE LUMINAL EPITHELIUM OF GOODEIDS IS SIMPLE SQUA
MOUS TO CUBOIDAL AND IS DERIVED FROM THE PERITONEAL
EPITHELIUM ,OMBARDI AND 7OURMS A 3CHINDLER
+UJAT AND DE 6RIES 3CHINDLER (OLLEN
BERG AND 7OURMS )T LINES THE LUMEN COVERING
THE RICHLY VASCULAR OVIGEROUS FOLDS 4HE EPITHLIAL CELLS
ARE OFTEN DOMED REMINISCENT OF A TRANSITIONAL EPITHELI
UM &IGURE &ISSURES SEPARATE THE EPITHELIAL CELLS
GIVING THE SURFACE A COBBLESTONE APPEARANCE IN SCAN
NING ELECTRON MICROGRAPHS &IGURES " # THESE
-!2').!, #,%&43 MAY BECOME DEEP AND MAY CONTAIN
LEUCOCYTES &IGURE (OLLENBERG AND 7OURMS
4HE SURFACE CELLS BECOME mATTENED IN A GRAVID
OVARY AS THE EPITHELIUM STRETCHES TO ACCOMMODATE THE
DEVELOPING EMBRYOS THE SUBEPITHELIAL CONNECTIVE TIS
SUE SWELLS FORCING THE CAPILLARIES CLOSER TO THE SURFACE
THEREBY REDUCING THE BLOOD
EMBRYOTROPH PATHWAY
&IGURES ! " 3CHINDLER +UJAT AND DE 6RIES
4HE LATERAL MEMBRANES OF THE EPITHELIAL CELLS INTER
DIGITATE AND THE CELLS ARE CONNECTED BY LARGE DESMO
SOMES WITH THICK ATTACHMENT PLAQUES INTERMEDIATE
lLAMENTS RADIATE INTO THE CYTOPLASM FROM THE PLAQUES
&IGURES " AND 4IGHT JUNCTIONS ARE NOT CON
SPICUOUS BETWEEN THE EPITHELIAL CELLS AND THE INTERCEL
LULAR DISTANCES ARE THE SAME IN THE ADLUMINAL POSITION
AS ELSEWHERE ALONG THE LATERAL MEMBRANES /FTEN DES
MOSOMES OCCUR IN POSITIONS WHERE TIGHT JUNCTIONS
WOULD BE EXPECTED -ANY TONOlLAMENTS INTERMEDI
ATE lLAMENTS PERMEATE THE EPITHELIAL CELLS MANY ARE
CONTINUOUS WITH THE lLAMENTS ASSOCIATED WITH THE AT
TACHMENT PLAQUES OF THE DESMOSOMES &IGURE
4HE RESEMBLANCE OF THE LUMINAL EPITHELIUM TO A TRAN
SITIONAL EPITHELIUM AND THE REINFORCEMENT PROVIDED BY
DESMOSOMES AND INTRACELLULAR TONOlLAMENTS WOULD
BE EXPECTED IN A MEMBRANE SUBJECTED TO THE DISTEN
SION BROUGHT ABOUT BY ITS BURDEN OF GROWING EMBRYOS
4HE WELL DEVELOPED COLLAGENOUS LAYER BELOW THE EPI
THELIUM EVIDENT IN SEVERAL OF THE lGURES IS CONSISTENT
WITH THIS EXPLANATION
4HE APICAL SURFACE OF THE EPITHELIAL CELLS IS WITHOUT
EXTENSIONS EXCEPT FOR OCCASIONAL CILIA %NDOCYTOTIC
ACTIVITY MAY BE OBSERVED ON ALL SURFACES OF THE CELLS
INCREASING GREATLY IN GRAVID OVARIES &IGURES # $
AND 4HE CYTOPLASM IS CRISS CROSSED BY ORGA
NIZED BUNDLES OF INTERMEDIATE lLAMENTS AND CONTAINS
SCANT GRANULAR ENDOPLASMIC RETICULUM SEVERAL MITO
CHONDRIA 'OLGI STACKS AND A DIVERSIlED VACUOLAR AP
PARATUS COMPOSED OF NUMEROUS SMALL VESICLES SOME
#(!04%2
LYSOSOME LIKE VESICLES AND MULTIVESICULAR BODIES AND
A FEW SHORT TUBULES &IGURE $ 4HE EPITHELIAL CELLS
EXHIBIT MORPHOLOGICAL FEATURES ASSOCIATED WITH THE VE
SICULAR TRANSPORT OF MACROMOLECULES AND APPEAR INAD
EQUATE FOR THE SYNTHESIS OF PROTEINACEOUS SECRETIONS
IT IS SUGGESTED THAT THEY PASS ALONG MACROMOLECULES
DERIVED FROM THE SERUM 3CHINDLER +UJAT AND DE 6R
IES 3CHINDLER 3CHINDLER AND +UJAT
(OLLENBERG AND 7OURMS 4HE ONLY RECENT DIS
SENTING VOICE IN THIS GENERAL ACCEPTANCE OF VESICULAR
TRANSPORT BY THE LUMINAL EPITHELIUM IS THAT OF ,OM
BARDI AND 7OURMS A WHO DESCRIBE THE PRESENCE
OF GRANULAR ENDOPLASMIC RETICULUM A 'OLGI COMPLEX
AND SPHERICAL VESICLES WITHIN THE APICAL CYTOPLASM IN
THE GOODEID !MECA SPLENDENS SUGGESTING A SECRETORY
PROCESS SIMILAR TO THAT OF OTHER PROTEIN SECRETING CELLS
! FORM OF APOCRINE SECRETION BY THE LUMINAL EPITHELIUM
HAS BEEN SUGGESTED IN SOME SPECIES WHERE APICAL BLEBS
APPEAR TO BE RELEASED INTO THE LUMINAL CAVITY POSSI
BLY CONTRIBUTING TO THE EMBRYOTROPH &IGURE
(OLLENBERG AND 7OURMS
4HE THIN LAYER OF EPITHELIAL CELLS IS SEPARATED FROM
THE ATTENUATED ENDOTHELIAL CELLS OF THE CAPILLARIES BY
A DELICATE WEB OF COLLAGENOUS CONNECTIVE TISSUE AND
THE THIN BASAL LAMINAE OF BOTH EPITHELIA SO THAT THERE
IS SLIGHT BARRIER TO THE PASSAGE OF MATERIALS FROM THE
LUMEN OF THE CAPILLARIES TO THE LUMEN OF THE OVARY
&IGURES ! # ,OMBARDI AND 7OURMS A
3CHINDLER 3CHINDLER AND +UJAT )NDEED
THE LARGE NUCLEI OF THE EPITHELIAL CELLS BECOME RECESSED
BETWEEN THE MESHES OF THE CAPILLARY NETWORK THEREBY
REDUCING THE BLOOD EMBRYOTROPH PATHWAY IN SOME
PLACES TO LESS THAN M &IGURE
)N THE JENYNSIID *ENYNSIA LINEATA WHERE NO PLA
CENTA FORMS AND THE EMBRYOS SUCKLE ON hNIPPLESv
FORMED FROM THE LUMINAL WALL THE STRUCTURE OF THE
NUTRITIVE EPITHELIUM IS REMARKABLY SIMILAR TO THAT OF
GOODEIDS 3CHINDLER AND DE 6RIES B )N *ENYN
SIA LONG RICHLY VASCULAR BRANCHING FOLDS OF THE LU
MINAL WALL FORM 6),,) /6!2)!,%3 THAT GROW INTO ONE
OPERCULAR CLEFT OF EACH EMBRYO ESTABLISHING CONTACT
BETWEEN THE MATERNAL NUTRITIVE TISSUE AND THE EMBRY
ONIC DIGESTIVE TRACT &IGURES AND 4URNER
D !S IN THE GOODEIDS THE LUMINAL EPITHELIAL CELLS
SHOW EVIDENCE BOTH APICALLY AND BASALLY OF VESICU
LAR TRANSPORT OF MACROMOLECULES APPEARING TO SERVE
FOR THE TRANSCELLULAR PASSAGE OF MATERNALLY DERIVED
SUBSTANCES &IGURE ! 3INCE THERE IS LITTLE UL
TRASTRUCTURAL EVIDENCE OF PROTEIN PRODUCTION IT IS AS
SUMED THAT THE EPITHELIUM IS NOT A SOURCE OF SECRETORY
PRODUCTS 4HE EPITHELIUM OF BOTH THE LUMEN AND VILLI
IS SIMPLE SQUAMOUS :ONULAE OCCLUDENTES ARE ABUN
DANT BETWEEN THE APICAL BORDERS OF ADJACENT CELLS AND
THE EPITHELIUM IS CONTINUOUS EXCEPT FOR A FEW GAPS AT
THE TIPS OF THE VILLI THAT ALLOW PARACELLULAR PASSAGE OF
PARTICULATE MATTER &IGURE " -OST ADJACENT
CELLS INTERDIGITATE &IGURE # PRESUMABLY PRO
VIDING PLASMALEMMAL RESERVES THAT ACCOMMODATE
VARIATIONS IN HEIGHT OF THE EPITHELIUM 4HE LUMINAL
EPITHELIUM RESTS ON A THIN BASAL LAMINA 4HE EPITHE
LIAL CELLS CONTAIN ABUNDANT lLAMENTS ELECTRON
DENSE
GRANULES MITOCHONDRIA POLYSOMES A 'OLGI COMPLEX
AND A VARIETY OF VACUOLES &IGURE ! GRANULAR
ENDOPLASMIC RETICULUM IS SPARSE
%MBRYOTROPH
%MBRYOTROPH CONTAINS LIPIDS AMINO ACIDS GLUCOSE
AND OTHER SUGARS ITS CONTENT OF PROTEINS IS LOW 4HE
MEAN OSMOLARITY OF EMBRYOTROPH HAS BEEN SHOWN TO
BE HIGHER THAN THAT OF THE PLASMA SO THAT THERE TENDS
TO BE AN INmUX OF mUID INTO THE GESTATIONAL CHAMBER
6EITH A +ORSGAARD #ORNISH AND 6EITH
%LECTROPHORETIC COMPARISONS OF MATERNAL BLOOD
SERUM AND THE EMBRYOTROPH INDICATE MANY SIMILARI
TIES IN THE COMPOSITION OF THESE mUIDS +RISTOFFERSON
"ROBERG AND 0EKKARINEN +ORSGAARD
DE 6LAMING ET AL 3CHINDLER AND DE 6RIES A
3CHINDLER AND +UJAT 3CHINDLER AND (AMLETT
(OLLENBERG AND 7OURMS 3INCE MOST UL
TRASTRUCTURAL STUDIES OF THE MATERNAL EPITHELIA PRESENT
LITTLE EVIDENCE OF PROTEIN PRODUCTION IT IS SUGGESTED
THAT EMBRYOTROPH IS ELABORATED BY TRANSCYTOSIS WHERE
MATERIALS ARE TAKEN UP BY ENDOCYTOSIS AT ONE SURFACE
OF AN EPITHELIAL CELL PASS ACROSS THE CELL UNCHANGED
WITHIN PINOCYTOTIC VESICLES AND ARE RELEASED AT THE
OTHER SURFACE BY EXOCYTOSIS 3CHINDLER AND DE 6RIES
A 3CHINDLER )N ADDITION SIBLING EMBRYOS
WHOSE DEVELOPMENT HAS BEEN ARRESTED ATRETIC OVA AND
SLOUGHINGS FROM THE LUMINAL EPITHELIUM MAY PROVIDE
ANOTHER SOURCE OF EMBRYOTROPHIC PROTEINS (OLLENBERG
AND 7OURMS
!LTHOUGH UREA WAS ABSENT FROM THE MATERNAL SERUM
OF SURFPERCHES %MBIOTOCIDAE LARGE AMOUNTS WERE
DETECTED IN THE EMBRYOTROPH SUGGESTING THAT EMBRYOS
BUT NOT ADULTS PRODUCE UREA AS A NITROGENOUS WASTE
AND THAT THE OVARIAN MEMBRANES ARE RELATIVELY IMPER
MEABLE TO IT DE 6LAMING ET AL
6)6)0!2)49
%MBRYONIC !BSORPTIVE %PITHELIA 4ROPHOTAENIAE
3OME EMBRYOS DEVELOP ABSORPTIVE EXTENSIONS OF THE
PROCTODAEUM THE 42/0(/4!%.)!% WHICH ASSIST IN THE
UPTAKE OF MATERIALS FROM THE EMBRYOTROPH &IGURE
!LTHOUGH MOST DESCRIPTIONS HAVE BEEN FROM
GOODEIDS OF THE /RDER #YPRINODONTIFORMES THE PRES
ENCE OF TROPHOTAENIAE HAS ALSO BEEN NOTED IN MEMBERS
OF TWO OTHER ORDERS THE ZOARCID 0ARABROTULA DENTIENS
0ERCIFORMES &IGURE 4URNER AND IN
THE BYTHITID /LIGOPUS LONGHURSTI /PHIDIIFORMES
7OURMS AND #OHEN 4ROPHOTAENIAE ARE CLOSELY
APPLIED TO THE WALL OF THE OVARIAN LUMEN AND TOGETHER
THESE TWO COMPONENTS CONSTITUTE THE 42/0(/4!%.)!,
0,!#%.4! ,OMBARDI AND 7OURMS B 3CHINDLER
AND +UJAT &ACILITATING THE EXCHANGE OF MATE
RIALS ARE DENSE CAPILLARY BEDS LYING BENEATH BOTH THE
LUMINAL AND TROPHOTAENIAL EPITHELIA
4ROPHOTAENIAE ARE ROSETTE
OR RIBBON
LIKE EXTRAEM
BRYONIC PROCESSES EXTENDING FROM THE PERIANAL REGION
OF MOST GOODEID EMBRYOS &IGURES ! " DURING
GESTATION THEY ARE BATHED IN THE EMBRYOTROPH SECRETED
BY THE INTERNAL LUMINAL EPITHELIUM BUT DO NOT APPEAR TO
ESTABLISH PERMANENT RELATIONSHIPS WITH THIS EPITHELIUM
&IGURES & AND ,OMBARDI AND 7OURMS
B (OLLENBERG AND 7OURMS )NDIVIDUAL
TROPHOTAENIAE COMMONLY CONTAIN TWO TO THREE MAJOR
BLOOD VESSELS DEEPLY EMBEDDED IN A CORE OF LOOSE
CONNECTIVE TISSUE THAT IS SURROUNDED BY THE CLOSELY AP
POSED TROPHOTAENIAL EPITHELIUM &IGURES # $ %
)N THE CONNECTIVE TISSUE WAVY COLLAGENOUS lBRES AND
STELLATE lBROBLASTS WITH LONG CYTOPLASMIC PROCESSES
ARE COMMONLY ORIENTED IN SUCCESSIVE TRANSVERSE LA
MELLAE ABOUT TO M APART "LOOD IS SUPPLIED
THROUGH A VENTRAL RAMIlCATION OF THE DORSAL MESENTERIC
ARTERY 7ITHIN EACH TROPHOTAENIA THE ARTERIES BRANCH
EXTENSIVELY GIVING RISE TO A CAPILLARY BED THAT EXTENDS
THROUGHOUT IMMEDIATELY BENEATH THE BASAL LAMINA
OF THE EPITHELIUM "LOOD IS DRAINED BY TROPHOTAENIAL
VEINS SITUATED ON EITHER SIDE OF THE POSTERIOR HINDGUT
THESE JOIN THE SUBINTESTINAL VEIN WHICH CARRIES BLOOD
TO THE HEPATIC PORTAL VEIN
!T THE BASE OF EACH TROPHOTAENIA THERE IS A CONmUENCE
OF THE ENDODERMAL EPITHELIUM LINING OF THE GUT AND THE
ECTODERMAL EPITHELIUM OF THE INTEGUMENT 4HESE EPI
THELIA MERGE AS THE TROPHOTAENIA ELONGATES FORMING A
MOSAIC OF !"3/204)6% #%,,3 DERIVED FROM ENTEROCYTES
SURROUNDING SMALL ISLANDS OF STRATIlED SQUAMOUS 0!6%
-%.4 #%,,3 FROM THE INTEGUMENT 4HESE REGIONS MAY
BE DISTINGUISHED IN SCANNING ELECTRON MICROGRAPHS BY
THE FORESTS OF MICROVILLI ON THE SURFACE OF THE ABSORP
TIVE CELLS AND THE lNGERPRINT PATTERNS OF MICRORIDGES
ON THE PAVEMENT CELLS &IGURE 3CHINDLER AND
DE 6RIES A B B #APILLARIES THAT ARE FE
NESTRATED IN SOME SPECIES NESTLE AGAINST THE BASAL
LAMINA OF THE EPITHELIUM &IGURES AND !
AND CARRY ABSORBED MATERIALS TO THE SINUS
LIKE BLOOD
VESSELS IN THE MESENCHYMATOUS CORE OF THE TROPHOTAE
NIA FROM WHENCE THEY ARE DRAINED INTO THE FOETAL HE
PATIC PORTAL SYSTEM
4ROPHOTAENIAL ABSORPTIVE CELLS RESEMBLE INTESTI
NAL ABSORPTIVE CELLS AND SHOW AN APICAL MICROVILLOUS
BORDER APICOLATERAL JUNCTIONAL COMPLEXES AND DESMO
SOMES BETWEEN ADJACENT CELLS A CISTERNAL COMPLEX MAY
PARALLEL THE LATERAL PLASMA MEMBRANES AND PINOCYTOTIC
INVAGINATIONS OF THE BASOLATERAL PLASMA MEMBRANES
ARE COMMON &IGURES AND -ENDOZA
,OMBARDI AND 7OURMS B 3CHINDLER AND
DE 6RIES A A B A 3CHINDLER AND +UJAT
3CHINDLER AND (AMLETT (OLLENBERG AND
7OURMS +OKKALA AND 7OURMS 4HE CY
TOPLASM MAY BE HORIZONTALLY TRAVERSED BY BUNDLES OF
INTERMEDIATE lLAMENTS AND CONTAINS NUMEROUS MITO
CHONDRIA SOME GRANULAR ENDOPLASMIC RETICULUM POLY
SOMES A 'OLGI COMPLEX MICROTUBULES IRREGULAR DENSE
BODIES AND A FEW MEMBRANE
BOUND BODIES THE NUCLE
US IS BASAL 4HE EPITHELIUM IS SEPARATED BY A SPACE
OF ABOUT NM FROM A DELICATE BASAL LAMINA ABOUT
NM THICK -ACROMOLECULES FROM THE EMBRYOTROPH
CANNOT PENETRATE THE EXPOSED CELL MEMBRANES OF THIS
EPITHELIUM BY WAY OF INTRAMEMBRANOUS PROTEIN CHAN
NELS OR PUMPS BUT MUST BE TAKEN UP BY MICROPINOCYTO
SIS 3CHINDLER AND DE 6RIES A
4HERE ARE TWO MORPHOLOGICALLY DISTINCT SPECIES
SPECIlC LINES OF TROPHOTAENIAL ABSORPTIVE CELLS BASED
ON THE PRESENCE OR ABSENCE OF A TYPICAL ENDOCYTOTIC
APPARATUS &IGURE 3CHINDLER AND DE 6RIES
A (OLLENBERG AND 7OURMS +OKKALA AND
7OURMS 4HE ENDOCYTOTIC APPARATUS IS WELL
DEVELOPED IN MOST GOODEIDS AND INGESTION OF PROTEINS
IS COMPARABLE TO THAT OF OTHER ABSORPTIVE EPITHELIA
4HE CORTICAL ZONE OF THE EPITHELIAL CELLS IS CROWDED
WITH MEMBRANOUS INVAGINATIONS VESICLES VACUOLES
AND DENSE APICAL TUBULES MITOCHONDRIA ARE LOCATED
BETWEEN THIS ENDOCYTOTIC APPARATUS AND THE NUCLEUS
&IGURES ! ! AND ,OM
BARDI AND 7OURMS B C 'ROE 7ICHTRUP
3CHINDLER AND DE 6RIES B A
)NTERNALIZED SOLUTES ACCUMULATE IN LARGE APICAL STOR
AGE VACUOLES AND AFTER SEVERAL HOURS MAKE THEIR WAY
#(!04%2
TO A LAMELLAR MEMBRANOUS COMPLEX THAT UNDERLIES THE
PERIPHERAL PLASMA MEMBRANES AND COMMUNICATES
WITH THE INTERCELLULAR SPACE VESICLES CARRY MATERIALS
TO THE BASOLATERAL OR BASAL CELL SURFACE WHERE THEIR
CONTENTS ARE RELEASED BY EXOCYTOSIS &IGURE
&IGURE IS A SUMMARY OF THE PROPOSED PATHWAY
BY WHICH PROTEINS ARE TRANSFERRED ACROSS THE TROPHO
TAENIAL PLACENTA
)N SPECIES WHERE THERE IS A WELL
DEVELOPED ENDO
CYTOTIC APPARATUS IN THE TROPHOTAENIAL ABSORPTIVE CELLS
IT IS SUGGESTED THAT THERE IS BOTH OPPORTUNISTIC AND
SELECTIVE UPTAKE OF PROTEINS FROM THE HETEROGENEOUS
MIXTURE IN THE EMBRYOTROPH (OLLENBERG AND 7OUR
MS 4HE SYSTEM OF APICAL CYTOPLASMIC TUBULES
SEEMS TO PROVIDE FOR THE NON RECEPTOR
MEDIATED UPTAKE
OF PROTEINS TARGETTING THEM TO LYSOSOMES FOR DEGRADA
TION TO AMINO ACIDS #OATED PITS ON THE OTHER HAND
ARE ASSOCIATED WITH RECEPTOR
MEDIATED ENDOCYTOSIS
AND THE TARGETTING OF ENDOCYTOSED PROTEINS TO BOTH
LYSOSOMAL AND NON LYSOSOMAL COMPARTMENTS
!N ENDOCYTOTIC APPARATUS IS LACKING IN TWO GENERA OF
GOODEIDS 'IRARDINICHTHYS AND 'OODEA AND THE SUPRA
NUCLEAR CYTOPLASM IS DOMINATED BY A LARGE NUMBER OF
MITOCHONDRIA THAT ARE SEPARATED FROM THE MICROVILLOUS
BORDER BY A NARROW RIM CONTAINING THE TERMINAL WEB
INVAGINATIONS OF THE APICAL PLASMA MEMBRANE ARE RARE
AND FEW MULTIVESICULAR BODIES ARE PRESENT 3CHINDLER
AND DE 6RIES A (OLLENBERG AND 7OURMS
+OKKALA AND 7OURMS &IGURES " AND
" 4HE BRUSH BORDER ABUNDANT MITOCHONDRIA
AND BASAL COATED VESICLES SUGGEST A TRANSPORTING EPI
THELIUM IN WHICH NUTRIENTS ARE ABSORBED PACKAGED AND
EXPORTED WITHOUT DEGRADATION 0RESUMABLY A HYPERPRO
TEINACEOUS ENVIRONMENT AT THE FREE SURFACE STIMULATES
MICROPINOCYTOTIC ACTIVITY GIVING RISE TO AN INTERNAL
APICAL CANALICULAR SYSTEM WHICH SUBSEQUENTLY DEVEL
OPS INTO MULTIVESICULAR BODIES 4HIS AMPLIlCATION OF
MEMBRANOUS MATERIAL IS LIKELY MORE TIME
CONSUMING
THAN SIMPLY STEPPING UP THE ACTIVITY OF A PRE
EXISTING
ENDOCYTOTIC APPARATUS SO THAT PROTEIN UPTAKE IS SLOW
3OME MATERIAL IS TRANSFERRED TO THE BASAL AND BASOLAT
ERAL PLASMA MEMBRANES WHERE IT IS RELEASED BY EXOCY
TOSIS &IGURE ! .O MECHANISM HAS DEVELOPED
WHEREBY THE INTERNALIZED MEMBRANES ARE RECYCLED
4HE STRATIlED SQUAMOUS PAVEMENT EPITHELIUM
FORMS IRREGULAR ISLANDS OF RIDGED CELLS BETWEEN THE AB
SORPTIVE CELLS &IGURE )T PROCLAIMS ITS INTEGU
MENTARY ORIGINS BY ITS STRATIlCATION IN UP TO SIX LAYERS
THE MUCOPOLYSACCHARIDE
COATED MICRORIDGES ON THE
FREE SURFACES AND THE LARGE NUMBERS OF DESMOSOMES
STRENGTHENING THE INTERDIGITATING BORDERS OF ADJACENT
CELLS 4ONOlLAMENTS CONVERGE ON THE DESMOSOMES AND
JUNCTIONAL COMPLEXES SEAL THE SUPERlCIAL LAYER OF CELLS
4HERE IS A WELL DEVELOPED 'OLGI COMPLEX AND BOTH
GRANULAR AND AGRANULAR ENDOPLASMIC RETICULUM EVIDENT
IN SOME PLACES &IGURE # /FTEN THE SQUAMOUS
CELLS SLIDE BENEATH THE ABSORPTIVE EPITHELIUM FORMING
A "!3!, ,!9%2 &IGURES " AND
4HE TWO STRAINS OF TROPHOTAENIAL EPITHELIAL CELLS
APPEAR TO PROVIDE FOR THE TWO BASIC NECESSITIES OF LIFE
OF THE YOUNG A SUPPLY OF NUTRIENTS AND RESPIRATORY
EXCHANGE 3CHINDLER AND DE 6RIES A 4HE AB
SORPTIVE EPITHELIUM DERIVED FROM THE ENDODERMAL
LINING OF THE GUT RESEMBLES INTESTINAL ABSORPTIVE CELLS
AND MAY BE REGARDED AS FULlLLING THE ABSORPTIVE FUNC
TION 4HE RIDGED STATIlED SQUAMOUS EPITHELIUM IS SIM
ILAR TO THE EPITHELIUM COVERING THE SECONDARY LAMELLAE
OF lSH GILLS AND IS PRESUMED TO BE ACTIVE IN GASEOUS
EXCHANGE
! SYSTEM OF ).4%2#%,,5,!2 30!#%3 CONTINUOUS WITH
THE INFOLDINGS OF THE BASOLATERAL MEMBRANES OF THE
ABSORPTIVE CELLS EXTENDS BETWEEN THE ABSORPTIVE AND
BASAL CELLS &IGURES AND !S DEVELOPMENT
PROCEEDS INCREASING DISTENSION OF THE INTERCELLULAR
SPACES MAY CAUSE PROGRESSIVE DISTORTION OF THE ABSORP
TIVE EPITHELIUM &IGURE -ENDOZA 4HESE
SPACES MAY HAVE AN EXCRETORY ROLE BY STORING WASTES
A SUGGESTION THAT IS REINFORCED BY THE APPEARANCE OF
LAMELLAR STRUCTURES AND MEMBRANOUS BLEBS RELEASED
INTO THESE CAVITIES &IGURE ! 4HE PRESENCE OF
LEUCOCYTES WITHIN THE INTERCELLULAR SPACES AND CROWDED
INTO THE CONNECTIVE TISSUE MAY INDICATE THE ACQUISITION
OF PASSIVE IMMUNITY &IGURES " #
/THER %MBRYONIC !BSORPTIVE 3TRUCTURES
/F ALL THE EMBRYONIC STRUCTURES THAT CONTRIBUTE TO THE
PLACENTAS OF VIVIPAROUS TELEOSTS THE TROPHOTAENIAE
HAVE RECEIVED MOST ATTENTION /THER STRUCTURES INCLUDE
THE PERICARDIAL YOLK AND COELOMIC SACS THE SKIN OF THE
BODY lNS AND lN FOLDS AND THE GILLS AND BUCCOPHA
RYNGEAL TISSUES $PCHE $OBBS 'ROVE
AND 7OURMS 3CHINDLER AND (AMLETT
4HESE ABSORPTIVE STRUCTURES ARE OFTEN COVERED WITH A
THIN SQUAMOUS EPITHELIUM CLOSELY APPLIED TO RICHLY
VASCULAR LOOSE CONNECTIVE TISSUE -OST OF THE EPITHELIAL
CELLS SHOW PATTERNS OF MICRORIDGES THAT ENHANCE THEIR
SURFACE AREA PRESUMABLY FACILITATING THE EXCHANGE OF
MATERIALS &OSCARINI )NDEED IN #LINUS SUPER
CILOSUS THE SURFACE EPIDERMIS ESPECIALLY THAT OF THE
6)6)0!2)49
PERICARDIAL AND YOLK SACS GRADUALLY LOSES ITS MICROR
IDGES AS THE GUT ASSUMES MORE AND MORE OF THE DUTIES
OF NUTRIENT UPTAKE 6EITH )N ADDITION TO THESE
PLACENTAL ABSORPTIVE STRUCTURES EMBRYOTROPH MAY BE
TAKEN IN BY THE MOUTH AND ITS NUTRIENTS ABSORBED BY
A PRECOCIOUSLY DEVELOPED GUT $OBBS 6EITH
4HE 0%2)#!2$)!, 9/,+ !.$ #/%,/-)# 3!#3 PLAY A
MAJOR ROLE IN MATERNAL
EMBRYONIC EXCHANGE IN MANY
VIVIPAROUS TELEOSTS ESPECIALLY DURING EARLY STAGES OF
GESTATION $PCHE 'ROVE AND 7OURMS
3CHINDLER AND (AMLETT ,ATER AS IN GOODEIDS
AND JENYNSIIDS THESE ORGANS MAY REGRESS AS THEIR FUNC
TIONS ARE TAKEN OVER BY OTHER STRUCTURES )N LECITHOTRO
PHIC SPECIES SUCH AS THE GUPPY 0OECILIA RETICULATA
WHICH RELY ON NUTRIENTS STORED IN THE EGG THE FUNCTIONS
OF THESE SACS ARE RESTRICTED TO GAS EXCHANGE AND OSMO
REGULATION CHLORIDE CELLS HAVE BEEN DESCRIBED AMONG
THE MICRORIDGES AND ARE PRESUMED TO CONTRIBUTE TO OS
MOREGULATION $PCHE
)N MATROTROPHIC SPECIES HOWEVER THESE SACS BE
COME GREATLY EXPANDED AND PARTICIPATE IN NUTRIENT
ABSORPTION IN ADDITION TO RESPIRATION AND OSMOREGULA
TION 6EITH 'ROVE AND 7OURMS )N THE
FOLLICULAR PLACENTA OF (ETERANDRIA FORMOSA THE PERI
CARDIAL SAC EXPANDS TO FORM A HOOD COVERING THE HEAD
AND TOGETHER WITH THE YOLK SAC IS EXTENSIVELY VASCU
LARIZED BY A PORTAL PLEXUS DERIVED FROM THE VITELLINE
CIRCULATION &IGURE 'ROVE AND 7OURMS
$URING EARLY DEVELOPMENT IN ADDITION TO THE ABSORP
TIVE EPITHELIUM THAT COVERS THE SURFACES OF THE PERI
CARDIAL AND YOLK SACS THE SURFACE EPITHELIUM ON OTHER
REGIONS OF THE BODY ALSO PARTICIPATES IN THE EXCHANGE
OF MATERIALS 4HIS EPIDERMAL EPITHELIUM IS A PATCHWORK
OF BOTH ABSORPTIVE CELLS AND CELLS THAT DO NOT APPEAR
TO BE ABSORPTIVE &IGURE DURING SUBSEQUENT
DEVELOPMENT THE AREAS COVERED BY NON
ABSORPTIVE
CELLS INCREASE SO THAT EVENTUALLY THERE IS LITTLE ABSORP
TION THROUGH THE SKIN AND THE PERICARDIAL AND YOLK SACS
BECOME THE PRIMARY SITES OF UPTAKE OF EXOGENOUS NUTRI
ENTS 4HE ABSORPTIVE EPITHELIA ARE BILAMINAR CONSISTING
OF A LAYER OF SPECIALIZED SUPERlCIAL CELLS AND A LAYER OF
EXTREMELY THIN BASAL CELLS &IGURE "ASAL CELLS
ARE CONNECTED TO EACH OTHER AND TO THE SUPERlCIAL CELLS
BY DESMOSOMES
4HE THICKER 350%2&)#)!, ,!9%2 OF THE ABSORPTIVE EPI
THELIUM RANGES FROM TO M IN THICKNESS AND IS
MORE CONSPICUOUS AND COMPLEX THAN THE BASAL LAYER
'ROVE AND 7OURMS 3PECIALIZATIONS BETWEEN
THE SUPERlCIAL CELLS INCLUDE THE INTERDIGITATION OF LATER
AL PLASMA MEMBRANES DESMOSOMES AND APICAL JUNC
TIONAL COMPLEXES &IGURE .UMEROUS ELONGATE
BRANCHING MICROVILLI PROJECT FROM THE APICAL SURFACE
3UPERlCIAL CELLS CONTAIN SEVERAL 'OLGI COMPLEXES AND
EXTENSIVE GRANULAR ENDOPLASMIC RETICULUM #OATED PITS
OFTEN OCCUR BETWEEN THE BASES OF THE MICROVILLI AND
THERE ARE COATED VESICLES IN THE APICAL CYTOPLASM ,ARGE
ELECTRON LUCENT VESICLES TO M IN DIAMETER
WITHIN THE APICAL CYTOPLASM CONTAIN mOCCULENT MATE
RIAL AND ARE OFTEN ASSOCIATED WITH THE 'OLGI COMPLEX
4HEY APPEAR TO BE ENDOSOMES ACIDIC PRELYSOSOMAL
COMPARTMENTS ASSOCIATED WITH RECEPTOR MEDIATED
ENDOCYTOSIS -YELIN lGURES ARE ALSO OFTEN PRESENT
! HETEROGENEOUS GROUP OF DENSE STAINING VESICLES AND
MULTIVESICULAR BODIES ARE SCATTERED THROUGHOUT THE CY
TOPLASM AND MAY BE LYSOSOMES "ECAUSE MICROVILLI
INCREASE SURFACE AREA FOR TRANSMEMBRANE ABSORPTION
UPTAKE OF LOW MOLECULAR WEIGHT MOLECULES INCLUDING
NUTRIENTS SUCH AS MONOSACCHARIDES AND AMINO ACIDS
MAY PLAY AN IMPORTANT ROLE 4HE PRESENCE OF THE COAT
ED PITS AND VESICLES INDICATES THAT SPECIlC PROTEINS ARE
ABSORBED THROUGH RECEPTOR MEDIATED ENDOCYTOSIS
"!3!, #%,,3 ARE TO M THICK AND CONTAIN FEW
ORGANELLES ALTHOUGH SOME MITOCHONDRIA A LIMITED
AMOUNT OF GRANULAR ENDOPLASMIC RETICULUM AN OCCA
SIONAL 'OLGI COMPLEX AND SOME COATED PITS AND VES
ICLES ARE PRESENT &IGURE 'ROVE AND 7OURMS
%.$/4(%,)!, #%,,3 OF THE PORTAL PLEXUS ARE SO
CLOSELY APPLIED TO THE BASAL CELLS THAT AT SOME POINTS
THEIR RESPECTIVE BASAL LAMINAE CANNOT BE DISTINGUISHED
&IGURES # $ 4HE ENDOTHELIAL CELLS POSSESS FEW
ORGANELLES BUT SMALL SMOOTH SURFACED PITS ARE PROMI
NENT ON THEIR INNER AND OUTER SURFACES 0RESUMABLY MA
TERNAL NUTRIENTS FROM THE EMBRYOTROPH ARE PASSED INTO
THE FOETAL CAPILLARIES BY TRANSCYTOSIS
#ELLS RESEMBLING #(,/2)$% #%,,3 OCCUR SINGLY OR IN
PAIRS IN THE SURFACE EPITHELIUM INDICATING ITS PROBABLE
ROLE IN OSMOREGULATION 'ROVE AND 7OURMS
4HEY REST ON THE BASAL LAMINA AND CONTAIN A BASAL NU
CLEUS NUMEROUS MITOCHONDRIA AND AN EXTENSIVE SYS
TEM OF TUBULAR MEMBRANE BOUND CHANNELS &IGURES
! " 4HE CHANNELS APPEAR SWOLLEN IN PLACES AND
COMMUNICATE LATERALLY AND BASALLY WITH THE INTERCEL
LULAR SPACES #OATED VESICLES 'OLGI COMPLEXES NU
MEROUS MICROTUBULES AND TO A LESSER EXTENT GRANULAR
ENDOPLASMIC RETICULUM ARE PRESENT AS WELL !PICAL
JUNCTIONAL COMPLEXES ARE PRESENT BETWEEN THE CHLORIDE
CELLS AND ADJACENT SUPERlCIAL EPITHELIAL CELLS
4HE ABSORPTIVE EPITHELIUM CONTINUES TO COVER THE
PERICARDIAL AND YOLK SACS AS DEVELOPMENT PROGRESSES
#(!04%2
BUT ./. -)#2/6),,/53 350%2&)#)!, #%,,3 APPEAR IN IN
CREASING NUMBERS IN OTHER REGIONS OF THE SURFACE EPI
THELIUM 'ROVE AND 7OURMS 4HESE CELLS ARE
MORE SQUAMOUS TO M THICK AND LESS COMPLEX
IN ULTRASTRUCTURAL ORGANIZATION THAN THE MICROVILLOUS
CELLS &IGURES # $ 4HEY ARE COVERED WITH A
GLYCOCALYX AND BEAR MICROPLICAE AND LATERAL RIDGES
THAT BECOME MORE APPARENT AS PARTURITION APPROACHES
0RESUMABLY THESE CELLS REPRESENT THE INITIAL STAGES OF
EPIDERMAL DIFFERENTIATION AND PLAY LITTLE ROLE IN NUTRI
ENT UPTAKE
!N ESPECIALLY INTIMATE PLACENTAL ASSOCIATION BE
TWEEN MATERNAL AND EMBRYONIC TISSUES IS DESCRIBED IN
THE EXTREME MATROTROPH !NABLEPS WHERE AS THE EM
BRYO DEVELOPS hVASCULAR BULBSv FORM ON THE RICHLY
VASCULAR PERICARDIAL TROPHODERM AND ASSOCIATE WITH
PITS IN THE FOLLICULAR WALL IN A BALL AND SOCKET FASH
ION &IGURES AND " % +NIGHT ET AL
4HE SURFACE CELLS OF THE VASCULAR BULBS ARE RIDGED BY
MICROPLICAE %ACH VASCULAR BULB CONTAINS A BLOOD SINUS
AND THE SINUSES OF ADJACENT BULBS ARE CONTINUOUS &IG
URE $ 4HESE SINUSES DRAIN INTO THE PORTAL SYSTEM
THAT DRAINS INTO THE SINUS VENOSUS !DJACENT REGIONS
OF THE FOLLICULAR WALL FORM ROWS OF VILLI WHICH COME
IN CONTACT WITH THE LATERAL AND DORSAL SURFACES OF THE
EMBRYO &IGURES ' ( 4HE SURFACE OF THE VILLI IS
COVERED WITH SHORT STUMPY MICROVILLI A WELL DElNED
BRUSH BORDER IS ABSENT 4HE VILLI EMBRACE THE VASCU
LAR BULBS AND MAY INITIATE THE FORMATION OF PITS IN THE
FOLLICULAR WALL )N TERMS OF PERCENTAGE WEIGHT INCREASE
OF THE DEVELOPING EMBRYO THE FOLLICULAR PLACENTA OF
!NABLEPS APPEARS TO BE THE MOST EFlCIENT ADAPTATION
FOR MATERNAL
EMBRYONIC NUTRIENT TRANSFER IN TELEOST
lSHES
%XCHANGE WITH THE EMBRYOTROPH ALSO MAY OCCUR
THROUGH THE 3+). COVERING THE BODY THE lN
FOLDS AND
lNS 2ICHLY VASCULAR &). &/,$3 ARE WELL DEVELOPED
IN 'OODEA LUITPOLDII AND TO A LESSER EXTENT IN OTHER
GENERA OF GOODEIDS -ENDOZA 'ERAUDIE AND
#HILMONCZYK 4HESE FOLDS OF RICHLY VASCULAR
LOOSE CONNECTIVE TISSUE ARE COVERED WITH A THIN SQUA
MOUS EPITHELIUM AND PROBABLY AUGMENT THE EXCHANGE
OCCURRING IN THE TROPHOTAENIAE AND BODY SURFACE
&IGURE 6ASCULARIZED SPATULATE EXPANSIONS OF
THE INTERRADIAL lN WEB ON THE DORSAL lN OF SOME EM
BIOTOCIDS ARE ALSO PRESUMED TO FUNCTION IN MATERNAL
FOETAL EXCHANGE &IGURES AND 7EBB AND
"RETT $OBBS )N SCANNING ELECTRON MI
CROGRAPHS THE EPIDERMAL CELLS OF THESE lN mAPS APPEAR
AS mATTENED SHEETS PATTERNED WITH NUMEROUS MICROR
IDGES OCCASIONAL MUCOUS CELLS ARE INTERSPERSED AMONG
THE SQUAMOUS EPITHELIAL CELLS 4HE VILLOUS HINDGUT OF
THIS SPECIES PROBABLY FUNCTIONS PRIMARILY IN THE AB
SORPTION OF NUTRIENTS FROM THE EMBRYOTROPH WHILE THE
VASCULAR lN mAPS FACILITATE THE RESPIRATORY EXCHANGE
OF GASES
6)6)0!2)49
&IGURE ! SCHEME TO ILLUSTRATE THE EVOLUTION OF
PLACENTATION IN SHARKS &ROM (AMLETT REPRODUCED
WITH PERMISSION OF THE AUTHOR
! 5TERINE RETENTION OF LECITHOTROPHIC EMBRYO
" 5TERINE COMPARTMENTS FORM EGG ENVELOPE THINS AND BE
COMES PLIABLE
# 9OLK SAC PLACENTA ESTABLISHED
$ 0URELY MATROTROPHIC DEVELOPMENT WITH FUNCTIONAL
PLACENTA ESTABLISHED AT IMPLANTATION &OR SIMPLICITY
THE PRESENCE OF ADDITIONAL COMPARTMENTALIZED EMBRYOS
IS NOT INDICATED IN # AND $
&IGURE 3KETCH OF THE FEMALE REPRODUCTIVE ORGANS
OF THE SUMITSUKI SHARK #ARCHARHINUS DUSSUMIERI &ROM
4ESHIMA AND -IZUE REPRODUCED WITH PERMISSION OF
THE AUTHORS
#(!04%2
&IGURE )NTERPRETIVE DRAWING OF AN !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE DURING AN EARLY STAGE OF
GESTATION 4HE OVARY CONTAINS SMALL DEVELOPING OOCYTES WHILE THE UTERUS HARBOURS YOLK
DEPENDENT EARLY
TERM EMBRYOS
! DELICATE EGG CAPSULE THAT SURROUNDS THE EMBRYO ESTABLISHES TWO SUBCOMPARTMENTS THE UTERINE COMPARTMENT AND THE PERI
FOETAL COMPARTMENT &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE 0HOTOGRAPH OF AN ISOLATED EGG CAPSULE OF AN EARLY TERM EMBRYO OF THE SMOOTH DOGlSH -USTELUS CANIS
4HE ASTERISK INDICATES THE FORMER LOCATION OF THE EMBRYO WHICH HAS BEEN REMOVED 'ATHERED REGIONS OF THE EGG CAPSULE G LIE
BOTH ANTERIOR AND POSTERIOR TO THE EMBRYOS POSITION $ARKENED LATERAL BANDS ARROWHEADS REPRESENT PLEATING OF THE EGG CAPSULE
3CALE BAR CM &ROM ,OMBARDI AND &ILES REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
6)6)0!2)49
&IGURE 0HOTOGRAPH OF A RECENTLY FERTILIZED EGG OF THE SHARPNOSE SHARK 2HIZOPRIONON TERRAENOVAE -OST OF THE EGG
ENVELOPE E IS GATHERED TOGETHER AT ONE END OF THE EGG 8 &ROM #ASTRO AND 7OURMS REPRODUCED WITH PERMISSION
OF *OHN 7ILEY 3ONS )NC
&IGURE 3KETCHES OF THE FEMALE REPRODUCTIVE ORGANS OF THE SUMITSUKI SHARK #ARCHARHINUS DUSSUMIERI &ROM 4ESHIMA
AND -IZUE REPRODUCED WITH PERMISSION OF THE AUTHORS
! 5TERUS WITH THE MEMBRANE RESERVOIR EMBRYONIC MEMBRANE
STORE CHAMBER IN THE ANTERIOR REGION 4HE PLACENTA HAS NOT YET
BEEN ESTABLISHED
" 4HE PLACENTA HAS BEEN ESTABLISHED WITHIN THE GRAVID UTERUS
#(!04%2
&IGURE $IAGRAM OF A PREIMPLANTATION STAGE OF A CARCHARHINID EMBRYO EARLY IN GESTATION &ROM (AMLETT REPRO
DUCED WITH PERMISSION OF THE AUTHOR 4HE EXTERNAL GILL lLAMENTS ARE CONSPICUOUS 4HE YOLK SAC CONTAINS YOLK AND IS NOT ATTACHED
TO MATERNAL TISSUES %XCESS EGG CAPSULE IS FOLDED INTO A NEAT PACKAGE AND STORED IN THE MEMBRANE RESERVOIR
6)6)0!2)49
&IGURE 3EVERAL EMBRYOS MAY BE ACCOMMODATED WITHIN COMPARTMENTS IN THE UTERI OF SOME PLACENTAL SHARKS TWO COM
PARTMENTS ARE SHOWN IN THESE DIAGRAMS OF LONGITUDINAL SECTIONS OF THE REPRODUCTIVE SYSTEM OF A PLACENTAL SHARK )MMATURE
SHARKS POSSESS AN OVARY O WITH DEVELOPING EGGS AND A SMALL OVIDUCT OV 9OLKED EGGS Y ARE SHED FERTILIZED AND ENTER THE
SHELL GLAND SG &ERTILIZED EGGS E RESIDE IN UTERINE COMPARTMENTS UC AND THE EXCESS EGG ENVELOPE IS SEQUESTERED IN A MEM
BRANE RESERVOIR
4HE YOLK SAC DIFFERENTIATES INTO AN UMBILICAL CORD UC AND THE YOLK SAC BECOMES A FUNCTIONAL PLACENTA P
&ROM (AMLETT ET AL A REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
#(!04%2
&IGURE 0HOTOGRAPH OF THE GRAVID UTERUS OF THE SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE 4HE UTERUS U HAS BEEN DIS
SECTED TO REVEAL THREE UTERINE COMPARTMENTS CP THAT CONTAIN EGGS E WITH SMALL EMBRYOS 4HE ANTERIOR END A IS TO THE LEFT
8 &ROM #ASTRO AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE -ICROGRAPHS OF SECTIONS THROUGH THE UTERUS OF THE SPINY DOGlSH 3QUALUS ACANTHIAS &ROM *OLLIE AND *OLLIE
B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 0HOTOMICROGRAPH OF A CROSS SECTION OF THE NONPREGNANT UTERUS 4HE VASCULAR UTERINE hMESENTERYv IS SHOWN AT THE TOP
4HE LINING OF THE UTERINE LUMEN IS SMOOTH AND THE CONNECTIVE TISSUE OF THE WALL IS THIN BUT DENSE AND LARGELY AVASCULAR
3ECTIONS OF THE MAJOR BLOOD VESSELS ARE SEEN IN THE MESENTERY AND BETWEEN THE LAYERS OF SMOOTH MUSCLE 8
" 0HOTOMICROGRAPH OF A SECTION OF THE SIMPLE COLUMNAR EPITHELIUM THAT LINES THE NONPREGNANT UTERUS !PICALLY SOME OF THESE
CELLS BEAR CILIA OTHERS APPEAR TO HAVE A BRUSH BORDER 4HE SUBEPITHELIAL CONNECTIVE TISSUE IS DENSE ! CAPILLARY LIES IMMEDI
ATELY BENEATH THE EPITHELIUM 8
6)6)0!2)49
&IGURE #ONTINUED
# %LECTRON MICROGRAPH OF A SECTION THROUGH THE EPITHELIUM OF THE NONPREGNANT UTERUS *UNCTIONAL COMPLEXES ARE WELL DEVEL
OPED BETWEEN THE APICAL BORDERS OF THE EPITHELIAL CELLS AND LATERAL PLASMA MEMBRANES ARE CLOSELY INTERDIGITATED /NE CELL IS
CILIATED 8
$ 0HOTOMICROGRAPH OF A CROSS SECTION OF A PORTION OF THE WALL OF A PREGNANT UTERUS -UCOSAL FOLDS OR RUGAE ARE LONGITUDINALLY
ORIENTED !RTERIOLES ARE PRESENT IN THE CORES OF THE RUGAE ,AYERS OF SMOOTH MUSCLE OF THE TUNICA MUSCULARIS ARE LOCATED AT
THE LEFT 8 #OMPARE WITH !
% 0HOTOMICROGRAPH OF A SECTION OF PREGNANT UTERUS 4HE EPITHELIUM OF THE TUNICA MUCOSA IS RICHLY SUPPLIED WITH CAPILLARIES
#, CONNECTIVE TISSUE IS SPARSE 5, UTERINE LUMEN 8 #OMPARE WITH "
#(!04%2
&IGURE #ONTINUED
& %LECTRON MICROGRAPH OF A SECTION OF THE PREGNANT UTERUS TO DEMONSTRATE THE hRESPIRATORY BARRIERv 4HE EPITHELIUM CONSISTS OF
TWO LAYERS OF LOW CUBOIDAL OR SQUAMOUS CELLS 4HE APICAL CYTOPLASM OF THE JUXTALUMINAL EPITHELIAL CELLS IS HIGHLY VACUOLATED
AND THE INTERCELLULAR SPACES EXTENSIVELY DILATED ! LAYER OF CONNECTIVE TISSUE SEPARATES THIS EPITHELIUM FROM THE ENDOTHELIUM
OF A UTERINE CAPILLARY 8
' !N ELECTRON MICROGRAPH OF THE SECTION SHOWN IN & AT A GREATER MAGNIlCATION !PICAL VESICLES ABOUND IN THE SURFACE EPITHELIAL
CELLS AND DISTENTION OF THE INTERCELLULAR SPACES IS APPARENT ! THIN LAYER OF CONNECTIVE TISSUE IS INTERPOSED BETWEEN THE EPITHE
LIUM AND THE ENDOTHELIAL CELL AT THE LOWER RIGHT 8 4HE INSET SHOWS THIS CONNECTIVE TISSUE !BUNDANT MICROPINOCYTOTIC
VESICLES LINE THE BASAL PLASMALEMMA OF THE JUXTACAPILLARY EPITHELIAL CELLS 8
6)6)0!2)49
&IGURE #ONTINUED
( %LECTRON MICROGRAPH OF A SECTION OF ADJOINING JUXTANUCLEAR EPITHELIAL CELLS JLE FROM A PREGNANT UTERUS 4HE OCCLUDING ZON
ULE OF A JUNCTIONAL COMPLEX SEALS THE INTERCELLULAR SPACES FROM THE LUMEN 5, 4HE APICAL CYTOPLASM OF THE JUXTALUMINAL
CELLS IS PACKED WITH SMOOTH
SURFACED ELECTRON
LUCENT VACUOLES !T SEVERAL POINTS ARROWS THE VACUOLES APPEAR TO COMMU
NICATE WITH THE APICAL PLASMALEMMA AND WITH EACH OTHER 8
#(!04%2
&IGURE %LECTRON MICROGRAPHS OF SECTIONS THROUGH THE RESPIRATORY BARRIER OF THE YOLK SAC OF THE SPINY DOGlSH 3QUALUS
ACANTHIAS &ROM *OLLIE AND *OLLIE A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 4HE RESPIRATORY BARRIER CONSISTS OF NON
KERATINIZED SQUAMOUS ECTODERMAL CELLS %CT A LAYER OF lNE RETICULAR lBRES 2&,
AND THE ENDOTHELIUM OF THE VITELLINE CAPILLARY 6#% 8
" 4HE ECTODERMAL EPITHELIUM OF THE FUNCTIONING RESPIRATORY BARRIER IS NON
KERATINIZED ! FEW PINOCYTOTIC VESICLES ARE SEEN
.OTE THE LARGE 'OLGI COMPLEXES AND ABUNDANT ENDOPLASMIC RETICULUM 4HE BASAL LAMINA OF THE ECTODERMAL EPITHELIUM IS
SEEN AT THE BOTTOM OF THE MICROGRAPH 8
6)6)0!2)49
&IGURE 4ROPHONEMATA ENHANCE THE PRODUCTION OF HISTOTROPH IN THE UTERUS OF THE SOUTHERN STINGRAY $ASYATIS AMERICANA
&ROM (AMLETT ET AL A REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !N EMBRYO WITH ITS YOLK STALK ST AND YOLK SAC YS STILL ATTACHED RESIDES IN THE UTERUS UT ADORNED WITH TROPHONEMATA
T
" 3CANNING ELECTRON MICROGRAPH OF A SINGLE TROPHONEMA SHOWING ITS CENTRAL VESSEL mATTENED NATURE AND CABLED SURFACE
8
#(!04%2
&IGURE 4ROPHONEMATA OF THE COWNOSE RAY 2HINOPTERA BONASUS ARE RICHLY VASCULARIZED SPATULATE VILLIFORM PROCESSES
EMBOSSED WITH A PATTERN OF ANASTOMOSING CABLE LIKE RIDGES ! " AND # ARE SCANNING ELECTRON MICROGRAPHS OF THE SURFACE OF
A TROPHONEMA &ROM (AMLETT 7OURMS AND 3MITH REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! !STERISKS MARK THE EDGES OF THE TROPHONEMA 4HE SURFACE IS RIDGED ARROWS 8
" 4HE SURFACE IS EMBOSSED WITH A SERIES OF INTERLOCKING RIDGES 2 4HE BORDERS OF ADJACENT CELLS ARE VISIBLE ARROWS 8
# 4HE SURFACE EPITHELIAL CELLS ARE ROUGHLY POLYHEDRAL WITH SHARPLY DElNED BOUNDARIES BETWEEN ADJACENT CELLS AND A RELATIVELY
SMOOTH AND CONVEX CONTOUR # 8
$ 0HOTOMICROGRAPH OF A SECTION THROUGH A TROPHONEMA SHOWING THE RICH VASCULARIZATION 6 OF THE RIDGES 2 ,OOSE CONNEC
TIVE TISSUE
FORMS THE CORE OF THE TROPHONEMA 8
6)6)0!2)49
&IGURE 3CANNING ELECTRON MICROGRAPHS OF TROPHONEMATA IN THE UTERINE WALL OF THE BUTTERmY RAY 'YMNURA MICRURA DURING
EARLY GESTATION &ROM 7OURMS 'ROVE AND ,OMBARDI REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 4ROPHONEMATA ARE SPATULATE VILLIFORM PROCESSES
" 4HE SURFACE OF THE TROPHONEMA IS EMBOSSED WITH A CONVOLUTED NETWORK OF hCABLESv THAT ENCLOSE A CAPILLARY NETWORK
!N ARTERY IS CONTAINED WITHIN THE DISTENDED LATERAL MARGIN ON THE LEFT
# 4HE BASIC ORGANIZATION OF AN ANASTOMOSING CAPILLARY BED PREDOMINATES AT THE SPATULATE TIP OF A TROPHONEMA !CINAR GLANDS
LOWER RIGHT ARE OCCASIONALLY OBSERVED
$ 3ECTIONS OF THE CAPILLARY BED COVERED BY THE SURFACE EPITHELIUM ARE SEEN IN THIS FREEZE
FRACTURE PREPARATION OF A TROPHO
NEMA
#(!04%2
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF AN EARLY TROPHONEMA OF THE SOUTHERN STINGRAY $ASYATIS AMERICANA &ROM
(AMLETT ET AL REPRODUCED WITH PERMISSION OF THE .2# 0RESS
! 4HIS CROSS SECTION THROUGH AN ENTIRE TROPHONEMA SHOWS THE CENTRAL BLOOD VESSEL V SMALLER PERIPHERAL VESSELS P AND MANY
CRYPTS ARROWHEADS 8
" 4HE SURFACE IS COVERED WITH A SIMPLE CUBOIDAL EPITHELIUM E OVERLYING PERIPHERAL BLOOD VESSELS BV !T THIS MAGNIlCATION
THE CELLS OF THE CRYPTS ARE SEEN TO BE lLLED WITH SMALL DARK SECRETION VESICLES ARROWS AND LARGE LIPID DROPLETS
8
A
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EPITHELIAL SURFACE OF TROPHONEMATA OF THE COW
NOSE RAY 2HINOPTERA BONASUS &ROM (AMLETT 7OURMS AND 3MITH REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE
%DITRICE
! 4HE CYTOPLASM OF AN EPITHELIAL CELL DISPLAYS THE CHARACTERISTIC ARRAY OF ORGANELLES INVOLVED IN PROTEIN SYNTHESIS AND SECRE
TION GRANULAR ENDOPLASMIC RETICULUM 2 'OLGI COMPLEXES ' AND SECRETION GRANULES 3 IN VARYING STAGES OF MATURATION
4HE NUCLEUS . IS AT THE LOWER LEFT ITS NUCLEAR ENVELOPE IS CONTINUOUS WITH THE DILATED CISTERNAE OF THE GRANULAR ENDOPLASMIC
RETICULUM ARROW ! MULTIVESICULAR BODY - AND COATED VESICLES CIRCLE ARE ALSO PRESENT 8
" *UNCTION OF TWO EPITHELIAL CELLS 4HE LATERAL BOUNDARIES ARE STRAIGHT ARROWS 4HE CYTOPLASM IS DOMINATED BY GRANULAR
ENDOPLASMIC RETICULUM 2 WHOSE CISTERNAE MAY BECOME GREATLY DISTENDED
0RESECRETORY GRANULES 0 ARE MORE ELEC
TRON
DENSE THAN THE MATERIAL WITHIN THE CISTERNAE OF THE GRANULAR ENDOPLASMIC RETICULUM -ITOCHONDRIA - ARE ABUNDANT
8
6)6)0!2)49
#(!04%2
&IGURE #ONTINUED
# 4HE CYTOPLASM OF A TROPHONEMAL EPITHELIAL CELL #OATED VESICLES ARROWS OCCUR IN THE REGION OF THE 'OLGI COMPLEX ' BUT
ARE NOT SEEN TO BE DIRECTLY ASSOCIATED WITH IT 4HE NUCLEUS . POLYRIBOSOMES 0 PRESECRETION GRANULES 3 AND GRANULAR
ENDOPLASMIC RETICULUM 2 ALSO OCCUPY THE CYTOPLASM 8
$ 4HIS MICROGRAPH IS A TANGENTIAL SECTION THROUGH THE APICES OF SEVERAL TROPHONEMAL CELLS 4HE ARROWS INDICATE AN EXTENSIVE
ARRAY OF JUNCTIONAL COMPLEXES BETWEEN ADJACENT CELLS 0RESECRETORY GRANULES 0 ARE LESS ELECTRON
DENSE THAN MATURE MEM
BRANE
LIMITED SECRETORY GRANULES - 8
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH TROPHONEMAL EPITHELIAL CELLS OF THE SOUTHERN STINGRAY
$ASYATIS AMERICANA &ROM (AMLETT ET AL REPRODUCED WITH PERMISSION OF THE .2# 0RESS
! #ELLS COVERING THE hCABLESv ON THE SURFACE OF A TROPHONEMA DISPLAY APICAL MICROVILLI ARROWS WHICH ALSO EXTEND INTO
THE CRYPTS BETWEEN THE EPITHELIAL CELLS 4HE CELLS CONTAIN SECRETORY GRANULES CIRCLES AND ARE PACKED WITH LARGE LIPID
DROPLETS
8
" 4ROPHONEMAL EPITHELIAL CELLS MAY CONTAIN PROTEIN SECRETORY GRANULES G LIPID
AND MUCUS M AT THE SAME TIME
4HE 'OLGI COMPLEX GC AND NUCLEUS N ARE SHOWN 8
#(!04%2
&IGURE #ONTINUED
# 4ROPHONEMATAL EPITHELIAL CELLS CONTAINING LAGE LIPID DROPLETS
!RROWS INDICATE THE TERMINAL WEB N NUCLEUS 8
$ #ELLS FROM A SECRETORY CRYPT CONTAIN PROTEINACEOUS SECRETORY VESICLES S %LECTRON
DENSE E AND mOCCULENT F SECRETORY
MATERIAL ARE PRESENT IN THE LUMEN 8
% 4HIS SURFACE SECRETORY CELL CONTAINS LIPID
GRANULAR ENDOPLASMIC RETICULUM RER 'OLGI COMPLEXES GO PROTEINACEOUS
SECRETORY GRANULES G AND MUCUS M 8
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH A TROPHONEMA OF THE SOUTHERN STINGRAY $ASYATIS AMERI
CANA AS TERM APPROACHES )NCREASED EFlCIENCY FOR RESPIRATORY EXCHANGE IS APPARENT &ROM (AMLETT ET AL A REPRODUCED
WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE SURFACE EPITHELIUM BECOMES ATTENUATED HALF CIRCLES AND UNDERLYING CAPILLARIES BV BECOME DILATED FORMING IRREGULAR
SINUSOIDS THAT BULGE CLOSE BENEATH THE SURFACE 4HE ARROW INDICATES LIPID DROPLETS 8
" ,ITTLE RESISTANCE TO RESPIRATORY EXCHANGE IS PRESENTED BY THE SQUAMOUS EPITHELIAL CELL OF THE TROPHONEMA SQ AND
THE ATTENUATED ENDOTHELIAL CELL E OF THE CAPILLARY 4HESE CELLS ARE SEPARATED BY A THIN LAYER OF LOOSE CONNECTIVE TISSUE AND
A BASAL LAMINA BL 8
#(!04%2
&IGURE -ICROGRAPHS OF SECTIONS THROUGH TRO
PHONEMATA OF THE SOUTHERN STINGRAY $ASYATIS AMERI
CANA AT TERM &ROM (AMLETT ET AL REPRODUCED
WITH PERMISSION OF THE .2# 0RESS
! 0HOTOMICROGRAPH OF A CROSS SECTION THROUGH AN
ENTIRE TROPHONEMA SHOWING ITS LARGE CENTRAL BLOOD
VESSEL V AND DILATED PERIPHERAL VESSELS P AT THE
mATTENED TERMINALS 4HE EPITHELIUM OVER THE PE
RIPHERAL VESSELS HAS BECOME SQUAMOUS CIRCLES
)NTERSTITIAL VESSELS HAVE DILATED TO FORM SINUSOIDS
ARROWS 8
" 3IMPLE SQUAMOUS EPITHELIUM CIRCLE COVERS THE
PERIPHERAL VESSEL AT THE CENTRE OF THIS PHOTOMI
CROGRAPH )NTERSTITIAL VESSELS HAVE DILATED TO FORM
SINUSOIDS ARROWS 8
# 4RANSMISSION ELECTRON MICROGRAPH OF A TROPHO
NEMA FROM A UTERUS CONTAINING NEAR TERM FOE
TUSES %NDOTHELIAL CELLS OF THE DILATED PERIPHERAL
VESSEL AT THE CENTRE ARE SEPARATED FROM THE THIN
SQUAMOUS EPITHELIAL CELLS ARROWHEADS BY SPARSE
LOOSE CONNECTIVE TISSUE BETWEEN THE ENDOTHELIAL
BASAL LAMINA B AND EPITHELIAL BASAL LAMINA B
4ROPHONEMAL SECRETORY CELLS T ARE SEEN ON EACH
SIDE OF THE VESSEL 8
$ ! PERICYTE P LYING IN LOOSE CONNECTIVE TISSUE
CLASPS A PERIPHERAL BLOOD VESSEL IN THIS TROPHONE
MA 4HE PERICYTE IS SEPARATED FROM THE ENDOTHELIAL
CELL E BY THE THIN ENDOTHELIAL BASAL LAMINA B
AND FROM THE EXTREMELY THIN SURFACE EPITHELIUM
ARROWHEAD BY THE EPITHELIAL BASAL LAMINA B
8
6)6)0!2)49
&IGURE #OMPOSITE LINE DRAWING DERIVED FROM TRANSMISSION ELECTRON MICROGRAPHS OF THE UTERUS OF THE SOUTHERN STINGRAY
$ASYATIS AMERICANA 4HE SITUATION IN A UTERUS CONTAINING FERTILIZED EGGS IS SHOWN AT THE LEFT THAT OF A UTERUS CONTAINING TERM
FOETUSES ON THE RIGHT 3MALL VESSELS LIE UNDER A CUBOIDAL EPITHELIUM IN EARLY GESTATION )N LATER GESTATIONAL STAGES THE PERIPHERAL
VASCULATURE INCREASES IN SIZE TO FORM SINUSOIDS AND THE EPITHELIUM OVER THESE IS THINNER 4HE REMAINDER OF THE SURFACE AND CRYPT
CELLS CONTINUE TO FUNCTION IN SECRETION &ROM (AMLETT ET AL REPRODUCED WITH PERMISSION OF THE .2# 0RESS
#(!04%2
&IGURE $IAGRAM OF A NEAR TERM CARCHARHINID EMBRYO WITHIN THE MATERNAL UTERUS 4HE NOW EMPTY YOLK SAC HAS BECOME
IMPLANTED IN THE MATERNAL UTERINE WALL 4HE EGG ENVELOPE INTERVENES BETWEEN EMBRYONIC AND MATERNAL TISSUES #ONCOMITANT
WITH GROWTH AND ELONGATION OF THE EMBRYO THE MEMBRANE RESERVOIR HAS BEEN OBLITERATED AND THE EMBRYO HAS ENLARGED TO lLL
THE ENVELOPE &ROM (AMLETT REPRODUCED WITH PERMISSION OF THE AUTHOR
&IGURE $IAGRAMS SHOWING THE ORIENTATION OF THE UTERINE COMPARTMENTS IN THE BONNETHEAD SHARK 3PHYRNA TIBURO DUR
ING EARLY AND LATE GESTATION 4HE CHANGE IN THE ORIENTATION OF THESE COMPARTMENTS OCCURS GRADUALLY AS THE EMBRYOS GROW
&ROM 3CHLERNITZAUER AND 'ILBERT REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
6)6)0!2)49
&IGURE $IAGRAM OF AN IDEALIZED TRANSVERSE SECTION OF A PREIMPLANTATION SHARK EMBRYO AT A LEVEL JUST ANTERIOR TO
THE JUNCTIONS OF THE DUCTUS VITELLO
INTESTINALIS AND THE GUT )N BOTH APLACENTAL AND PLACENTAL SHARKS THE YOLK SAC ARISES AS
A VENTRAL OUTPOUCHING OF THE EMBRYONIC GUT AND CONTAINS THE YOLK MASS ENCLOSED WITHIN ENDODERMAL EPITHELIUM !S THIS
ENDODERMAL EVAGINATION DISTENDS THE YOLK SAC REMAINS ENCLOSED BY THE MESODERM AND ECTODERM OF THE BODY WALL AND IS ATTACHED
TO THE EMBRYO BY THE YOLK STALK ! SPLIT SUBSEQUENTLY FORMS WITHIN THE MESODERM CREATING THE EXTRAEMBRYONIC COELOM A SPACE
ENCLOSED BY SOMATIC MESODERM ON THE OUTSIDE AND SPLANCHNIC MESODERM INSIDE 4HE CAVITY CONTAINING THE YOLK IS CONTINUOUS
WITH THE LUMEN OF THE GUT BY THE DUCTUS VITELLO
INTESTINALIS &ROM (AMLETT AND 7OURMS REPRODUCED WITH PERMISSION
FROM %LSEVIER 3CIENCE
@
&IGURE 4HE WALL OF THE PREIMPLANTATION YOLK SAC CON
SISTS OF SIX CONCENTRIC REGIONS ECTODERM EC SOMATIC MESODERM
EXTRAEMBRYONIC COELOM SPLANCHNIC MESODERM ENDODERM EN
AND YOLK SYNCYTIUM YS 4HE MESODERMAL LAYERS AND EXTRAEM
BRYONIC COELOM LIE BETWEEN THE BASAL LAMINAE B OF THE ECTODERM
AND ENDODERM IN THIS STYLIZED DRAWING ! BLOOD VESSEL BV LIES IN
THE LOOSE CONNECTIVE TISSUE OF THE MESODERM 0ARTIALLY SOLUBILIZED
YOLK IS MODULATED THROUGH THE 'OLGI COMPLEX G OF THE YOLK SYN
CYTIUM AND IS TRANSFERRED TO THE ENDODERM IN MEMBRANE
LIMITED
VESICLES ARROWHEADS &ROM (AMLETT REPRODUCED WITH KIND
PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE WALL OF THE YOLK SAC OF A PREIMPLANTATION EMBRYO
OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE 4HE EXTRAEMBRYONIC COELOM # LIES BETWEEN THE SOMATIC ME
SODERM 3 AND SPLANCHNIC MESODERM 3P 4HE ENDOTHELIAL BASAL LAMINA ARROWS SEPARATES THE SPLANCHNIC MESODERM FROM
THE ENDOTHELIUM OF A YOLK SAC CAPILLARY CONTAINING AN ERYTHROCYTE 8 &ROM (AMLETT AND 7OURMS REPRODUCED
WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 4HE YOLK SAC OF A PREIMAPLANTATION STAGE OF A CARCHARHINID EMBRYO IS COVERED WITH ECTODERMAL EPITHELIUM THAT IS
CONTINUOUS BY WAY OF THE YOLK STALK WITH THE ECTODERM THAT ENCLOSES THE EMBRYO ITSELF 4HE YOLK STALK CONTAINS A VITELLINE ARTERY
VEIN AND CILIATED DUCTUS VITELLO
INTESTINALIS CONmUENT WITH THE FOETAL GUT &ROM (AMLETT REPRODUCED WITH PERMISSION OF
THE AUTHOR
6)6)0!2)49
&IGURE $RAWING OF A SECTION OF THE YOLK SYNCYTIAL
ENDODERMAL COMPLEX IN THE YOLK SAC OF A PREIMPLANTATION SHARK
EMBRYO 9OLK PLATELETS ARE PARTIALLY DIGESTED WITHIN THE YOLK SYNCYTIUM 4HE PRODUCTS ARE MODIlED WITHIN THE SYNCYTIAL
'OLGI COMPLEX AND TRANSPORTED TO THE ENDODERM IN MEMBRANE
LIMITED PACKETS -ETABOLITES ARE THEN PASSED TO THE ENDOTHELIUM
&ROM (AMLETT REPRODUCED WITH PERMISSION OF THE AUTHOR
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE PREIMPLANTATION YOLK SAC OF THE SHARK 2HIZOPRIONODON
TERRAENOVAE &ROM (AMLETT 3CHWARTZ AND $I$IO REPRODUCED WITH PERMISSION OF THE AUTHORS
! 4HE YOLK SYNCYTIAL
ENDODERMAL COMPLEX IS COMPOSED OF THE CENTRAL YOLK SYNCYTIUM S THE ENDODERM E A CONNECTIVE
TISSUE SPACE
CONTAINING MESENCHYMAL CELLS M AND THE ENDOTHELIUM OF THE VITELLINE VESSELS V 4HE ENDODERM IS A
SIMPLE CUBOIDAL LAYER ABUTTING THE YOLK SYNCYTIUM AND IS INTENSELY AMPLIlED BY FOLDS THAT INTERDIGITATE WITH THE MEMBRANE
DELIMITING THE YOLK SYNCYTIUM 8
" )N THIS SECTION THROUGH THE YOLK SYNCYTIUM VESICLES CONTAINING YOLK DROPLETS FUSE WITH THE FORMING FACE OF THE 'OLGI
COMPLEX OPEN ARROWS 9OLK DROPLETS BUD OFF THE ENDS OF THE DILATED 'OLGI CISTERNAE AS WELL AS FROM THE MATURING FACE IN
MEMBRANE
BOUND PACKETS SOLID ARROWS 4HE ENDODERM E IS VISIBLE AT THE TOP 8 4HE INSET SHOWS SEVERAL YOLK
DROPLETS BEING MODIlED WITHIN THE 'OLGI COMPLEX 8
6)6)0!2)49
&IGURE #ONTINUED
# -EMBRANE
BOUND PACKETS OPEN ARROWS CONTAINING YOLK DROPLETS ARE VISIBLE WITHIN THE YOLK SYNCYTIUM 4HE MEMBRANES
OF THE YOLK SYNCYTIUM ARROWHEADS AND THE ADJACENT ENDODERMAL CELL SOLID ARROWS ARE CLOSELY APPOSED AND ENCLOSE AN IN
TERSPACE
CONTAINING YOLK DROPLETS 9OLK DROPLETS ARE SUBSEQUENTLY ENDOCYTOSED BY THE ENDODERMAL CELLS AND ARE INITIALLY
SURROUNDED BY A MEMBRANE CIRCLES 8
#(!04%2
&IGURE #ONTINUED
$ 4HE MEMBRANES OF THE YOLK SYNCYTIUM AND THE ENDODERMAL CELLS ARE CLOSELY APPOSED ELABORATELY INTERDIGITATED AND JOINED
BY DESMOSOMES SOLID ARROWS 9OLK DROPLETS ARE SEEN IN THE INTERSPACE OPEN ARROWS 8
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE INTERIOR OF THE DUCTUS VITELLO INTESTINALIS FROM THE YOLK STALK OF AN ELAS
MOBRANCH EMBRYO ,INEAR ROWS OF CILIATED # AND MICROVILLAR - CELLS LINE THE WALL $URING VITELLOGENIC DEVELOPMENT
YOLK PLATELETS FROM THE YOLK MASS ARE PASSED UP THE DUCTUS BY CILIARY ACTION OF THE EPITHELIAL CELLS &ROM (AMLETT ET AL A
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
6)6)0!2)49
&IGURE 4HIS DRAWING DEPICTS THE THREE CELL TYPES THAT MAKE UP THE EPITHELIAL LINING OF THE DUCTUS VITELLO INTESTINALIS FROM
THE YOLK STALK OF AN ELASMOBRANCH EMBRYO 4HESE INCLUDE CILIATED COLUMNAR CELLS C MICROVILLAR CELLS MV WITH PROMINENT
LIPID INCLUSIONS LP AND GLYCOGEN CIRCLE AND ENTEROENDOCRINE CELLS EE .OTE THAT THE ENTEROENDOCRINE CELL DOES NOT ATTAIN THE
SURFACE ITS SECRETION GRANULES APPEAR TO BE DIRECTED BASALLY INTO THE VASCULAR CONNECTIVE TISSUE LYING BELOW ! BASAL LAMINA B
SEPARATES THE EPITHELIUM FROM THE CONNECTIVE TISSUE BV BLOOD VESSEL &ROM (AMLETT REPRODUCED WITH KIND PERMISSION
OF +LUWER !CADEMIC 0UBLISHERS
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE EPITHELIAL LINING OF THE DUCTUS VITELLO INTESTINALIS FROM
THE UMBILICAL CORD OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE 4HREE DISTINCT CELL TYPES MAKE UP THE EPI
THELIUM #OLUMNAR CELLS WITH CILIA AND MICROVILLI # ALTERNATE WITH STRICTLY MICROVILLAR CELLS - RICH IN LIPID AND GLYCOGEN
%NTEROENDOCRINE CELLS % DO NOT ATTAIN THE SURFACE 8 &ROM (AMLETT REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
#(!04%2
&IGURE 0HOTOGRAPH OF A CM EMBRYO OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE 'ILL lLAMENTS
ARROWHEAD ARE PROMINENT 4HE CONTENTS OF THE YOLK SAC YS ARE REDUCED AND THE YOLK STALK IS COVERED BY BUSHY APPENDICULAE
ARROW &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE -ICROGRAPHS OF THE ECTODERM OF THE YOLK SAC FROM AN EMBRYO OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON
TERRAENOVAE &ROM (AMLETT AND 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 4HIS SCANNING ELECTRON MICROGRAPH SHOWS THE LABYRINTHINE PATTERN OF MICROPLICAE EXTENDING OVER THE EPITHELIAL SURFACE
EXCEPT AT THE PERIPHERY WHERE RIDGE
LIKE BOUNDARIES DELINEATE ADJACENT CELLS ARROWS 8
" 4RANSMISSION ELECTRON MICROGRAPH OF DILATED CISTERNAE OF GRANULAR ENDOPLASMIC RETICULUM 2 LIPID
LIKE INCLUSIONS ,
COATED VESICLES LARGE ARROWS UNCOATED VESICLES SMALL ARROWS AND 'OLGI COMPLEXES ' IN THE CYTOPLASM OF A SOMATIC
ECTODERMAL CELL 8
# 4HE NUCLEUS . AND PARALLEL ARRAYS OF GRANULAR ENDOPLASMIC RETICULUM 2 IN A SOMATIC ECTODERMAL CELL #ISTERNAE OF
THE ENDOPLASMIC RETICULUM ARE NOT DILATED 8
$ ! COLLAGENOUS STROMA # LIES BETWEEN THE SOMATIC ECTODERM % AND THE MESODERM OF THE YOLK SAC ! BASAL LAMINA ,
SUBTENDS THE ECTODERMAL CELL #IRCULAR PROlLES OF INCLUSION BODIES ARROWS OCCUR WITHIN THE STROMA 8
6)6)0!2)49
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE YOLK SAC FROM AN EMBRYO OF THE !TLANTIC SHARPNOSE SHARK
2HIZOPRIONODON TERRAENOVAE &ROM (AMLETT AND 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 4HE CYTOPLASM OF ENDODERMAL CELLS CONTAINS MITOCHONDRIA - SCATTERED ELEMENTS OF GRANULAR ENDOPLASMIC RETICULUM 2
AND YOLK DEGRADATION BODIES 9 8
" ! HETEROGENEOUS COLLECTION OF YOLK GRANULES 9 MITOCHONDRIA - AND MEMBRANOUS LAMELLAE ARROWS ARE SEEN IN THE YOLK
SYNCYTIUM 8
6)6)0!2)49
&IGURE #ONTINUED
# .UMEROUS SMALL YOLK DEGRADATION VESICLES 6 AND LARGER YOLK DEGRADATION BODIES $" ARE ASSOCIATED WITH THE PERIPHERY
OF YOLK PLATELETS 9 WITHIN THE YOLK SYNCYTIUM 8
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE CUT SURFACE OF AN EGG CAPSULE OF THE VIVIPAROUS SHARK -USTELUS CANIS
REVEALING MULTIPLE LAMINAE WHITE ARROWHEADS "LACK ARROWHEADS INDICATE THE EDGE OF THE INCOMPLETE OUTER LAMINA 'RANULAR
CALCIUM DEPOSITS ARE PRESENT ON THE CAPSULAR SURFACE
8 &ROM ,OMBARDI AND &ILES REPRODUCED WITH PERMIS
SION OF *OHN 7ILEY 3ONS )NC
#(!04%2
&IGURE $IAGRAMS TO ILLUSTRATE A HYPOTHETICAL MECHANISM OF PLACENTATION IN -USTELUS CANIS &ROM ,OMBARDI AND &ILES
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! %ARLY TERM EMBRYO ENCLOSED WITHIN THE EGG CAPSULE
" (YPERTROPHY OF THE SURFACE OF THE YOLK SAC AND FORMATION OF THE YOLK SACEGG CAPSULE COMPLEX
# 2ELEASE BY THE EMBRYO OF SOLUTE PARTICLES OF HIGH MOLECULAR WEIGHT CAUSES MOVEMENT OF WATER INTO THE INTRACAPSULAR SPACE
FROM EXTRACAPSULAR AND MATERNAL TISSUE mUIDS WHITE ARROW THEREBY CAUSING DISTENTION OF THE EGG CAPSULE BLACK ARROWS
$ $ISTENTION OF THE EGG CAPSULE OBLITERATES THE EXTRACAPSULAR SPACE RESULTING IN THE APPOSITION OF THE YOLK SACEGG CAPSULE
COMPLEX AGAINST THE UTERINE LINING
% 4HE YOLK SAC PLACENTA IS FORMED BY THE INTERDIGITATION OF MATERNAL AND EMBRYONIC TISSUES
6)6)0!2)49
&IGURE 3CHEMATIC DRAWING OF A FEMALE OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE AT TERM 4HE YOLK
STALK IS TRANSFORMED INTO AN UMBILICAL CORD WITH APPENDICULAE THE YOLK SAC CONTRIBUTES TO A FUNCTIONAL PLACENTA 3PECIALIZED
ATTACHMENT SITES FOR THE DISTAL PORTION OF THE PLACENTA MODULATE METABOLIC EXCHANGE &ROM (AMLETT REPRODUCED WITH KIND
PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE 3KETCH OF A CROSS SECTION OF A MATURE UMBILICAL CORD OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAE
NOVAE 3HOWN ARE SECTIONS OF THE MUSCULAR UMBILICAL ARTERY A UMBILICAL VEIN V DUCTUS VITELLOINTESTINALIS D WITH ROWS OF
CILIA
AND THE EXTRAEMBRYONIC COELOM C 3MALL BLOOD VESSELS ARROWHEADS OCCUPY THE CONNECTIVE TISSUE STROMA OF THE
APPENDICULAE A AS WELL AS THE BODY OF THE CORD &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC
0UBLISHERS
#(!04%2
&IGURE 3KETCH OF THE YOLK SAC OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE 4HE YOLK SAC BECOMES
REGIONALLY MODIlED INTO TWO REGIONS 4HE DIAPHANOUS PROXIMAL SMOOTH SEGMENT SP IS CONmUENT WITH THE UMBILICAL CORD UC
AND DRAPES OVER THE RICHLY VASCULAR DISTAL RUGOSE PORTION RP THAT ABUTS THE UTERINE ATTACHMENT SITE !PPENDICULAE ARROWHEADS
EMERGE FROM THE UMBILICAL CORD &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE 0HOTOGRAPH OF THE PLACENTA OF THE BLACKNOSE SHARK #ARCHARHINUS PLUMBEUS 4HE PLACENTA IS DIFFERENTIATED INTO
A PROXIMAL SMOOTH PORTION P THAT IS CONmUENT WITH THE UMBILICAL CORD UC AND A DISTAL RUGOSE PORTION D &ROM (AMLETT
ET AL A REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
6)6)0!2)49
&IGURE 2EPRESENTATIONS OF SECTIONS OF THE PARAPLACENTAL AREA OF THE TERM UTERUS OF THE !TLANTIC SHARPNOSE SHARK 2HIZO
PRIONODON TERRAENOVAE
! )N THIS SKETCH THE COLUMNAR EPITHELIAL CELLS HAVE PROMINENT 'OLGI COMPLEXES G AND APICAL MUCOUS VESICLES
-UCUS
MU IS RELEASED BY EXOCYTOSIS ARROWS ! MACROPHAGE MC IS WANDERING BETWEEN THE EPITHELIAL CELLS &ROM (AMLETT
REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
" 4RANSMISSION ELECTRON MICROGRAPH OF A SIMILAR SECTION AS THAT SHOWN ABOVE 4HE ASTERISKS INDICATE MUCOUS VESICLES IN
THE COLUMNAR EPITHELIAL CELLS 8 &ROM (AMLETT -IGLINO AND $I$IO REPRODUCED WITH PERMISSION FROM
.UOVA )MMAGINE %DITRICE
#(!04%2
&IGURE !SPECTS OF THE INTACT UMBILICAL CORD AND PLACENTA OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE
&ROM (AMLETT -IGLINO AND $I$IO REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! 0HOTOGRAPH OF A TERM FOETUS CONNECTED TO THE FOETAL YOLK SAC PORTION OF THE PLACENTA P BY THE UMBILICAL CORD U
" 4HIS CLOSE
UP VIEW SHOWS APPENDICULAE A EXTENDING FROM THE UMBILICAL CORD U 6ASCULAR CHANNELS ARROWS ARE VISIBLE
IN THE PROXIMAL PORTION P OF THE YOLK SAC 4HE DISTAL PORTION OF THE YOLK SAC D HAS A LOBULATED RUGOSE SURFACE ARROW
HEADS
6)6)0!2)49
&IGURE 3TEREODIAGRAM OF THE GERM LAYER CONTRIBUTIONS TO THE SHARK YOLK SAC PLACENTA 4HE APPENDICULAE ARE VASCULARIZED
OUTPOCKETINGS OF ECTODERM THAT ARE lLLED WITH LOOSE CONNECTIVE TISSUE 4HE SMOOTH PLACENTA HAS CONTRIBUTIONS FROM ECTODERM
AND SOMATIC MESODERM 4HE RUGOSE ROUGH PLACENTA IS RICHLY SUPPLIED BY MESODERMALLY DERIVED VASCULATURE %NDODERMAL CELLS
COAT THE BLOOD VESSELS AND THE INNER ASPECT OF THE ECTODERM &ROM (AMLETT REPRODUCED WITH PERMISSION OF THE AUTHOR
#(!04%2
&IGURE 4HE SITE OF PLACENTAL UTERINE EXCHANGE IN THE SHARK
! " %LECTRON MICROGRAPHS OF SECTIONS OF THE UTERUS OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE &ROM (AM
LETT -IGLINO AND $I$IO REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! 4HE PLACENTAL EPITHELIUM P IS SEPARATED FROM THE UTERINE EPITHELIUM U BY THE EGG ENVELOPE E AND AN INTERSPACE
4HE UTERINE EPITHELIAL CELLS OF THE ATTACHMENT SITE CONTAIN SECRETORY VESICLES
AND LIPID INCLUSIONS L 3ECRETORY MATE
RIAL BLACK ARROWS IS PRESENT IN THE INTERSPACE ! BASAL LAMINA ARROWHEADS SEPARATES THE UTERINE EPITHELIUM FROM THE
CONTINUOUS ENDOTHELIUM OF THE VASCULAR BED V 4HE PLACENTAL EPITHELIUM IS SEPARATED FROM ITS SUBJACENT BLOOD SUPPLY
V BY A PROMINENT BASAL LAMINA OPEN ARROWS 8
" 4HE UTERINE EPITHELIUM IS A SINGLE LAYER OF LOW CUBOIDAL CELLS BEARING A FEW MICROVILLI ARROWHEADS 4HE PLASMALEM
MAS OF ADJACENT CELLS ARE ELABORATELY INFOLDED OPEN ARROW AND THE INTERCELLULAR SPACES ARE SEALED APICALLY BY JUNCTIONAL
COMPLEXES CIRCLE 4HE CYTOPLASM OF THE EPITHELIAL CELLS CONTAINS 'OLGI COMPLEXES G POLYSOMES AND FREE RIBOSOMES
R ! BASAL LAMINA BLACK ARROW SEPARATES THE EPITHELIUM FROM THE CONTINUOUS ENDOTHELIUM E OF A VESSEL CONTAINING
ERYTHROCYTES AND WHITE BLOOD CELLS W 8
# 4HE UTERINEPLACENTAL ASSOCIATION IN THE BLACKNOSE SHARK #ARCHARHINUS PLUMBEUS IS SHOWN IN THIS DRAWING 4HE EGG
ENVELOPE EE IS BORNE ALOFT BY ABUNDANT MICROVILLI OF THE EPITHELIAL CELLS OF THE TERM PLACENTA UPPER PORTION OF ILLUSTRA
TION 4HIS EPITHELIUM IS SEPARATED FROM THE FENESTRATED ENDOTHELIUM OF ITS BLOOD SUPPLY BY A COMMON BASAL LAMINA
/N THE UTERINE SIDE THE FENESTRATED ENDOTHELIUM OF THE BLOOD VESSELS IS SEPARATED BY A BASAL LAMINA FROM THE SIMPLE
CUBOIDAL EPITHELIUM LOWER PORTION OF ILLUSTRATION 4HESE EPITHELIAL CELLS DISPLAY EXTENSIVE GRANULAR ENDOPLASMIC
RETICULUM AND BOTH COATED AND UNCOATED VESICLES &ROM (AMLETT ET AL A REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
6)6)0!2)49
#(!04%2
&IGURE 4HERE MAY BE A REDUCTION IN THE BARRIERS TO THE EXCHANGE OF MATERIALS IN THE SHARK PLACENTA AND AN INCREASE IN
THE AREA OF TISSUE CONTACT BY MEANS OF INTERDIGITATION 4HIS IS A SIMPLIlED DRAWING OF THE PLACENTA OF A
MM EMBRYO OF
-USTELUS GRISEUS 4HE PLACENTA CONSISTS OF A MATERNAL SOLID BLACK AND FOETAL PORTION DOTTED AREA "LOOD VESSELS ARE CROSS
HATCHED &ROM 4ESHIMA REPRODUCED WITH PERMISSION FROM THE )CHTHYOLOGICAL 3OCIETY OF *APAN
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE UTERINE WALL OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE
DURING EARLY GESTATION &ROM #ASTRO AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! /UTER REGION OF THE UTERINE WALL SHOWING SEROSAL EPITHELIUM Z LONGITUDINAL AND CIRCULAR MUSCLE LAYERS M AND A CONNEC
TIVE TISSUE LAYER CT 8
" )NNER REGION OF THE UTERINE WALL SHOWING THE LUMEN THE EGG ENVELOPE E OVERLYING THE LUMINAL EPITHELIUM W AND
CONNECTIVE TISSUE CT 8
6)6)0!2)49
&IGURE #ONTINUED
# 3ECTION OF THE INNER PART OF THE UTERUS SHOWING THE EPITHELIUM W ! SHALLOW LUMINAL PIT CONTAINING PUTATIVE SECRETORY
PRODUCTS S LIES ON THE ON THE EPITHELIAL SIDE OF THE EGG ENVELOPE E YOLK PLATELETS P ARE SEEN ON THE LUMINAL SIDE 8
$ 4HE EGG ENVELOPE IS CLOSELY APPLIED TO THE LUMINAL EPITHELIUM EXCEPT IN THE REGION OF THE LUMINAL PIT 8
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE UTERINE WALL OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE
AT THE TIME OF IMPLANTATION &ROM #ASTRO AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !T THE IMPLANTATION SITE THE UTERINE WALL BEARS NUMEROUS RIDGES FOLDS AND PROTRUBERANCES COVERED WITH EITHER
A PSEUDOSTRATIlED EPITHELIUM OR A LAYER OF SHORT COLUMNAR EPITHELIAL CELLS TWO CELLS THICK 0LACENTAL VILLI V ARE COVERED
BY THE EGG ENVELOPE E 8
" 4HIS PLACENTAL VILLUS IS COVERED BY THE MUCH
FOLDED EGG ENVELOPE 8
#(!04%2
&IGURE #ONTINUED
# 4HE YOLK SAC Y AND A VILLUS V AT THE IMPLANTATION SITE ARE SEPARATED BY THE EGG ENVELOPE E 8
$ 4HE YOLK SAC IS COMPOSED TO THREE LAYERS ECTODERM EC MESODERM M AND ENDODERM EN 8
% 4HE EPITHELIUM W OF THIS PLACENTAL VILLUS IS TWO CELLS THICK AND RESTS ON LOOSE CONNECTIVE TISSUE CONTAINING CAPILLARIES B
8
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE UTERINE WALL OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE
DURING GESTATION &ROM #ASTRO AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0LACENTAL VILLI V INTERDIGITATE WITH THE YOLK SAC Y THE EGG ENVELOPE E SEPARATES THEM 8
" %XTENSIONS OF THE YOLK SAC Y ARE CLOSELY INTERDIGITATED WITH A PLACENTAL VILLUS V 4HE EGG ENVELOPE E ADHERES TIGHTLY TO
THE YOLK SAC
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE PLACENTA OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRION
ODON TERRAENOVAE ! LARGE SURFACE CELL OF THE UTERINE EPITHELIUM CONTAINS LYSOSOMES
THE EGG ENVELOPE E IS CLOSELY APPLIED
TO ITS APICAL SURFACE %LECTRON
DENSE MATERIAL BLACK ARROWS PRESUMABLY OF UTERINE ORIGIN IS PRESENT IN THE INTERSPACE BETWEEN
THE EGG ENVELOPE AND THE PLASMALEMMA 3LITS OR DELAMINATIONS OCCUR IN THE EGG ENVELOPE ARROWHEADS $EEPER EPITHELIAL
CELLS HAVE SMOOTH
WALLED CAVEOLAE ON BOTH THEIR ABLUMINAL AND ADLUMINAL SURFACES OPEN ARROWS ! BASAL LAMINA B SEPA
RATES THE EPITHELIUM FROM THE UNDERLYING FENESTRATED ENDOTHELIUM EN OF A CAPILLARY #IRCLES INDICATE FENESTRATIONS 8
&ROM (AMLETT -IGLINO AND $I$IO REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE EPITHELIUM OF THE PARAPLACENTAL REGION OF THE SHARK UTERUS
AT TERM 4HE SIMPLE COLUMNAR EPITHELIAL CELLS ARE PACKED WITH MUCOUS DROPLETS M &ROM (AMLETT ET AL A REPRODUCED
WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
A
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE UTERUS OF THE TERM !TLANTIC SHARPNOSE SHARK 2HIZOPRION
ODON TERRAENOVAE &ROM (AMLETT REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE UTERUS - AND DISTAL PLACENTA 0 ARE SEPARATED BY THE EGG ENVELOPE % ,EUCOCYTES , OCCUPY A BLOOD VESSEL IM
MEDIATELY BENEATH THE EPITHELIUM 8
" ! BASAL LAMINA ARROWHEADS SEPARATES THE VASCULAR ENDOTHELIUM 6 FROM THE UTERINE EPITHELIUM - 3ECRETORY VESICLES
6 OCCUPY THE CYTOPLASM OF THE EPITHELIAL CELLS AND SECRETORY PRODUCT
LIES IN THE SPACE BENEATH THE EGG ENVELOPE %
8
# 4HERE IS LITTLE SEPARATION BETWEEN THE BLOOD CHANNELS OF THE UTERUS "# AND PLACENTA "# 5TERINE SECRETORY VESICLES 6
AND EXTRACELLULAR SECRETORY PRODUCT 0 ARE EVIDENT 4HE EGG ENVELOPE % IS CLOSELY APPLIED TO THE PLACENTAL EPITHELIAL CELLS
0, 8
$ /N THE UTERINE SIDE THE EGG ENVELOPE SHOWS DELAMINATIONS ARROWHEADS THAT MAY REPRESENT TRANSVERSE OR TANGENTIAL SECTIONS
OF LAMINATED MATERIAL ADJACENT TO LAMELLAE SECTIONED LONGITUDINALLY
4HE PLACENTAL PLASMALEMMA ARROWS IS IN CLOSE
CONTACT WITH THE EGG ENVELOPE AND MAY ENDOCYTOSE UTERINE SECRETIONS 3 8
6)6)0!2)49
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE YOLK SAC OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON
TERRAENOVAE &ROM (AMLETT -IGLINO AND $I$IO REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
! 4WO ADJACENT EPITHELIAL CELLS FROM THE PROXIMAL PORTION OF THE YOLK SAC ARE PACKED WITH MASSES OF AGRANULAR ENDOPLASMIC
RETICULUM SER 4HESE CELLS HAVE A BORDER OF STUBBY MICROVILLI MV THEY CONTAIN 'OLGI COMPLEXES G AND IRREGULAR INCLU
SIONS
8
" 4HE CYTOPLASM OF AN EPITHELIAL CELL FROM THE PROXIMAL PORTION OF THE YOLK SAC IS PACKED WITH AGRANULAR ENDOPLASMIC RETICU
LUM SER AND CONTAINS LAMELLAR WHORLS OF MEMBRANE
8
&IGURE 2EPRESENTATIONS OF ATTACH
MENT SITES IN THE GRAVID TERM UTERUS OF THE
SANDBAR SHARK #ARCHARHINUS PLUMBEUS
&ROM (AMLETT 7OURMS AND (UDSON C
REPRODUCED WITH PERMISSION FROM %LSEVIER
3CIENCE
! 0HOTOMICROGRAPH OF A SECTION OF THE UTER
US SHOWING ITS SIMPLE CUBOIDAL TO LOW CO
LUMNAR EPITHELIUM % BLOOD VESSELS "
AND SUBEPITHELIAL CONNECTIVE TISSUE #
8
" 3CANNING ELECTRON MICROGRAPH OF A TRANS
VERSE SECTION OF THE PLACENTAL ATTACHMENT
SITE -ATERNAL BLOOD VESSELS
LIE BE
NEATH THE FOLDED EPITHELIUM 8
6)6)0!2)49
&IGURE #ONTINUED
# 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE UTERINE WALL 4HE EPITHELIAL CELLS HAVE BRANCHING APICAL MICROVILLI
- HIGHLY FOLDED AND INTERDIGITATED LATERAL BOUNDARIES
AND ELEMENTS OF GRANULAR ENDOPLASMIC RETICULUM 2 ! BASAL
LAMINA " SEPARATES THE EPITHELIUM FROM THE THIN CAPILLARY ENDOTHELIUM ARROW BELOW LITTLE CONNECTIVE TISSUE INTERVENES
ARROWHEAD 8
#(!04%2
&IGURE #ONTINUED
$ 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF A UTERINE EPITHELIAL CELL 4HE CELL HAS BRANCHED MICROVILLI ARROWHEADS AND
CONTAINS ELEMENTS OF GRANULAR ENDOPLASMIC RETICULUM 2 WITH DILATED CISTERNAE COATED PITS ARROWS MITOCHONDRIA -
LIPID
LIKE INCLUSIONS , AND PROMINENT FREE RIBOSOMES CIRCLE 4HE LARGE NUCLEUS . IS INDICATED 8
6)6)0!2)49
&IGURE #ONTINUED
% 3CHEMATIC DRAWING OF THE CELLULAR ORGANIZATION OF THE UTERINE ATTACHMENT SITE AS SEEN WITH THE TRANSMISSION ELECTRON MI
CROSCOPE ,ITTLE BARRIER INTERVENES BETWEEN THE SIMPLE MATERNAL EPITHELIUM - FROM THE ENDOTHELIUM % OF A SUBJACENT
CAPILLARY
#(!04%2
&IGURE 3CHEMATIC DRAWING OF A SECTION OF THE TERM PLACENTA OF THE !TLANTIC SHARPNOSE 2HIZOPRIONODON TERRAENOVAE
4HE EGG ENVELOPE EE SEPARATES THE FOETAL ABOVE AND MATERNAL BELOW PORTIONS OF THE PLACENTA 4HE SQUAMOUS UTERINE
EPITHELIUM UT HAS BASAL PINOCYTOTIC VESICLES LARGE CIRCLES LIPID INCLUSIONS LP AND SECRETORY VESICLES THAT RELEASE THEIR
CONTENTS INTO THE UTERINE LUMEN
3UBJACENT CAPILLARIES BV ARE CONTINUOUS %LECTRON
DENSE VESICLES ARROWS OF UTERINE
ORIGIN ARE ENDOCYTOSED BY THE DISTAL PORTION OF THE FOETAL PLACENTA PL 4HE PLACENTAL EPITHELIUM HAS BASAL PINOCYTOTIC VESICLES
LARGE CIRCLES AND CRYSTALLINE INCLUSIONS C THAT ARE INTERPRETED AS YOLK PRECURSORS 3UBJACENT CAPILLARIES BV ARE FENESTRATED
SMALL CIRCLES "ASAL LAMINAE OF THE EPITHELIA AND ENDOTHELIA ARE INDICATED B &ROM (AMLETT REPRODUCED WITH KIND
PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
A
&IGURE 2EPRESENTATIONS OF THE RUGOSE DISTAL PORTION OF THE PLACENTA IN THE GRAVID TERM UTERUS OF THE SANDBAR SHARK
#ARCHARHINUS PLUMBEUS 5NLESS OTHERWISE INDICATED THE lGURES ARE TRANSMISSION ELECTRON MICROGRAPHS OF SECTIONS %XCEPT
FOR ) ALL lGURES ARE FROM (AMLETT 7OURMS AND (UDSON A AND ARE REPRODUCED WITH PERMISSION OF %LSEVIER 3CIENCE
! 3CANNING ELECTRON MICROGRAPH OF THE ELONGATE PEG
SHAPED SURFACE EPITHELIAL CELLS ARROWS 8
" 0HOTOMICROGRAPH OF A SECTION REVEALS THE EGG ENVELOPE ARROW ABOVE THE SURFACE EPITHELIUM % #APILLARIES # AND
BOUNDARY PAVEMENT CELLS 0 LIE BELOW 8
# 4HE TRANSVERSELY SECTIONED EGG ENVELOPE % ABUTS THE APICAL CANALICULAR SYSTEM # IN THE EPITHELIAL CELLS OF THE DISTAL
PLACENTA 8
$ 2UTHENIUM RED 2 COATS THE UTERINE SURFACE OF THE EGG ENVELOPE % AND ITS INTERSTICES ARROWS 8
6)6)0!2)49
#(!04%2
&IGURE #ONTINUED
% ! CELL FROM THE DISTAL PORTION OF THE PLACENTA INCUBATED FOR MINUTES IN HORSERADISH PEROXIDASE 2EACTION PRODUCT (20
CAN BE SEEN WITHIN THE CANALICULAR SYSTEM # 4HE BASE OF THE EPITHELIAL CELL IS CLOSELY APPOSED TO THE CAPILLARY ENDOTHELIUM
% ! COMMON BASAL LAMINA ARROW SEPARATES THE TWO CELL TYPES 8 )NSET 3MOOTH WALLED VESICLES CONTAIN (20
REACTION PRODUCT ARROWS THAT HAS BUDDED OFF FROM THE CANALICULI 8
6)6)0!2)49
&IGURE #ONTINUED
& "OTH COATED # AND UNCOATED 3 VESICLES ARE CLOSELY ASSOCIATED WITH CYTOPLASMIC MICROTUBULES ARROWS IN AN EPITHE
LIAL CELL FROM THE BASAL REGION OF THE DISTAL PORTION OF THE PLACENTA ! BASAL LAMINA " SEPARATES THE EPITHELIAL CELL FROM
THE ENDOTHELIUM % OF A CAPILLARY CONTAINING A RED BLOOD CELL 2 8
#(!04%2
&IGURE #ONTINUED
' ! SURFACE EPITHELIAL CELL # OF THE DISTAL PORTION OF THE PLACENTA IS CLOSELY APPOSED TO THE ENDOTHELIUM % OF ONE OF THE
ABUNDANT CAPILLARIES OF THE VITELLINE CIRCULATION 7HORL
LIKE INCLUSIONS ARROWS OCCUPY THE BASAL CYTOPLASM OF THE EPITHELIAL
CELL 8
( 4HE WHORL
LIKE INCLUSIONS IN AN EPITHELIAL CELL ARE MADE UP LAMELLAR SUBUNITS ARROW IN VARIOUS STAGES OF AGGREGATION
8
) 0ARACRYSTALLINE WHORL
LIKE INCLUSIONS 0 WITHIN THE EPITHELIAL CELLS MAY REPRESENT VITELLOGENIN OR ITS PRECURSORS PRODUCED
BY THE MATERNAL LIVER AND TRANSFERRED ACROSS THE UTEROPLACENTAL COMPLEX 8 &ROM (AMLETT REPRODUCED WITH
PERMISSION OF *OHN 7ILEY 3ONS )NC
6)6)0!2)49
&IGURE #ONTINUED
* &ORMERLY ACTIVE ENDODERMAL CELLS FORM A SUPPORTIVE BOUNDARY LAYER WITH SCANT MICROVILLI - AND SPARSE ORGANELLES EXCEPT
FOR A FEW MITOCHONDRIA 4HE BOUNDARY PAVEMENT CELLS REST ON A DISTINCT BASAL LAMINA "
+ 3CHEMATIC DRAWING SHOWING THE CELLULAR ORGANIZATION IN THE RUGOSE DISTAL PORTION OF THE YOLK SAC PLACENTA 2UTHENIUM RED
2 ADHERES TO THE MATERNAL SURFACE OF THE EGG ENVELOPE % 4HE CYTOPLASM OF THE EPITHELIAL CELL CONTAINS AN APICAL CANALICU
LAR SYSTEM 3 AND WHORL
LIKE INCLUSIONS ARROWS ! CAPILLARY
PART OF THE VITELLINE CIRCULATION IS CLOSELY ASSOCIATED WITH
THE BASAL
LATERAL SURFACE OF THE EPITHELIAL CELL ITS ENDOTHELIAL CELLS SHOW ACTIVE PINOCYTOSIS ! WELL DEVELOPED COLLAGENOUS
STROMA # SEPARATES THE SURFACE EPITHELIUM FROM THE INNER BOUNDARY LAYER ,
#(!04%2
&IGURE 2EPRESENTATIONS OF THE SMOOTH PROXIMAL PORTION OF THE PLACENTA IN THE GRAVID TERM UTERUS OF THE SANDBAR SHARK
#ARCHARHINUS PLUMBEUS &IGURES ! TO % ARE SCANNING ELECTRON MICROGRAPHS WHILE & TO ) ARE TRANSMISSION ELECTRON MICROGRAPHS
OF SECTIONS &ROM (AMLETT 7OURMS AND (UDSON B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! 0ERIPHERIES OF THE CELLS ON THE SURFACE OF THE SMOOTH PORTION ARE MARKED BY PROMINENT ELEVATIONS ARROW -ANY MICROVILLI
- AND MICROPLICAE
COVER THE BULGING APICAL SURFACES ! OF THE EPITHELIAL CELLS 8
" 4HE BROKEN EDGE OF A CROSS SECTION OF THE PLACENTA SHOWS THE EPITHELIAL CELLS % SEPARATED FROM THE INNER LAYER ) BY A COL
LAGENOUS STROMA 3 CONTAINING A BLOOD VESSEL 6 8
6)6)0!2)49
&IGURE #ONTINUED
# &IVE ADJACENT CELLS ON THE SURFACE OF THE SMOOTH PORTION FORM A ROSETTE AROUND A CENTRAL CELL 4HE PERIPHERAL CELLS POSSESS
MICROVILLI - THAT ARE MOST DENSE AT THE CELL BORDERS
4HE SURFACE OF THE CENTRAL CELL SHOWS MICROVILLI ARROW CILIA #
AND VESICULATIONS 6 8
$ 3OME EPITHELIAL CELLS HAVE MICROVILLI - OTHERS HAVE MICROPLICAE ARROW WHILE STILL OTHERS POSSESS A SMOOTHER SURFACE
CONTOUR 3 AND BULGING CELL APICES " 8
#(!04%2
&IGURE #ONTINUED
% %PITHELIAL CELLS CONTAIN LARGE LIPID
LIKE INCLUSIONS , AND MANY CYTOPLASMIC lLAMENTS $ESMOSOMES ARROWS JOIN CELLS
AND THE DEEPEST CELL LAYER POSSESSES AN UNDULATING BASAL CONTOUR
AND A PROMINENT BASAL LAMINA ARROWHEAD ADJACENT TO
A COLLAGENOUS STROMA # 8
& ! PROMINENT GLYCOCALYX ARROWS COATS THE SURFACE OF THE MICROPLICAE
&IBROUS ELEMENTS & OF THE TERMINAL WEB OCCUR
JUST BENEATH THE APICAL PLASMALEMMA 8
6)6)0!2)49
&IGURE #ONTINUED
' 4HIS EPITHELIAL CELL HAS A LOBATE NUCLEUS . mAT APICAL BORDER
CILIA # WITH ASSOCIATED ROOTLETS MICROVILLI ARROWHEAD
AND LIPID
LIKE INCLUSIONS , 8
( 4HE INNER CELL LAYER IS MUCH LIKE A MESOTHELIUM 4HE mATTENED CELLS HAVE A FUSIFORM NUCLEUS . A BASAL LAMINA " ADJA
CENT TO A COLLAGENOUS STROMA # AN ABUNDANCE OF CYTOPLASMIC lBRILS & AND MANY PINOCYTOTIC PITS AND VESICLES ARROWS
ON BOTH THE ABLUMINAL AND ADLUMINAL SURFACES 4HE INNER SURFACE OF THE CELLS IS BOUNDED BY THE CAVITY OF THE PLACENTA
8
#(!04%2
6)6)0!2)49
&IGURE 3CHEMATIC DRAWING OF CUBOIDAL EPITHELIAL CELLS FROM THE SMOOTH PROXIMAL PORTION OF THE TERM PLACENTA OF
THE SANDBAR SHARK #ARCHARHINUS PLUMBEUS 0ROMINENT 'OLGI COMPLEXES G AND ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM
SER WHICH MAY ASSUME LAMELLAR CONlGURATIONS
ARE CHARACTERISTIC OF STEROID PRODUCTION &ROM (AMLETT REPRODUCED
WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
@
&IGURE #ONTINUED
) 0INOCYTOTIC VESICLES 6 FORM A NEARLY CONTINUOUS ZONE ON THE CELL SURFACE ADJACENT TO THE BASAL LAMINA " .UMEROUS
TRANSPORT VESICLES
OCCUR IN THE CYTOPLASM AS DO FREE RIBOSOMES 2 AND lLAMENTOUS ELEMENTS & 8
* 3CHEMATIC DRAWING SHOWING THE CELLULAR ORGANIZATION IN THE SMOOTH PROXIMAL PORTION OF THE YOLK SAC PLACENTA 4HE SURFACE
EPITHELIAL CELLS % MAY POSSESS MICROVILLI
OR CILIA ARROW $ESMOSOMES ARROWHEADS JOIN ADJACENT CELLS AND LIPID ,
INCLUSIONS OCCUR IN THE CYTOPLASM 4HE BASAL LAMINAS " OF BOTH THE SURFACE EPITHELIAL CELLS AND THE DEEPER MESOTHELIAL
CELLS - ARE SEPARATED BY A COLLAGENOUS STROMA # -ESOTHELIAL CELLS ARE CHARACTERIZED BY AN ABUNDANCE OF CYTOPLASMIC
lLAMENTS & AND NUMEROUS PINOCYTOTIC PITS AND VESICLES CURVED ARROWS
#(!04%2
&IGURE 3CHEMATIC DRAWINGS TO ILLUSTRATE THE STRUCTURE OF THE YOLK SAC PLACENTA OF THE SHARK &ROM (AMLETT REPRO
DUCED WITH PERMISSION OF THE AUTHOR
! 3TEREOGRAM OF THE UMBILICAL CORD AND PLACENTA !PPENDICULAE ARE VASCULARIZED OUTPOCKETINGS OF ECTODERM THAT ARE lLLED
WITH LOOSE CONNECTIVE TISSUE 4HE SMOOTH PROXIMAL PORTION OF THE PLACENTA HAS CONTRIBUTIONS FROM ECTODERM AND SOMATIC
MESODERM 4HE RUGOSE OR ROUGH DISTAL PORTION IS RICHLY SUPPLIED BY MESODERMALLY DERIVED BLOOD VESSELS %NDODERMAL CELLS
COAT THE BLOOD VESSELS AND THE INNER ASPECT OF THE ECTODERM
6)6)0!2)49
&IGURE #ONTINUED
" $RAWING OF A CROSS SECTION OF THE UMBILICAL CORD ILLUSTRATING THE UMBILICAL ARTERY AND VEIN CILIATED DUCTUS VITELLOINTESTINA
LIS EXTRAEMBRYONIC COELOM AND APPENDICULAE 4HE ENLARGEMENT DEMONSTRATES THE HISTOLOGICAL FEATURES OF AN APPENDICULA
4HE EPITHELIUM WITH MICROVILLAR AND GRANULATED CELLS REST ON A BASAL LAMINA 4HE CONNECTIVE TISSUE ELEMENTS AND ENDOTHE
LIUM WITH ITS BASAL LAMINA ARE MESODERMALLY DERIVED
#(!04%2
&IGURE 0HOTOGRAPH OF A MM EMBRYO OF THE SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE AT MIDTERM 4HE APPEN
DICULAE COVERING THE UMBILICAL CORD HAVE REACHED THEIR MAXIMUM DEVELOPMENT AND THE YOLK SAC IS REDUCED 8 &ROM #ASTRO
AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 0HOTOMICROGRAPH OF A CROSS SECTION OF THE UMBILICAL CORD OF THE SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE
SHOWING THE UMBILICAL ARTERY ! UMBILICAL VEIN 6 DUCTUS VITELLOINTESTINALIS $ EXTRAEMBRYONIC COELOM % AND APPENDICU
LAE ARROWHEADS &ROM (AMLETT ET AL B REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
6)6)0!2)49
&IGURE 2EPRESENTATIONS DEMONSTRATING APPENDICULAE ON THE UMBILICAL CORD OF THE SHARPNOSE SHARK 2HIZOPRIONODON
TERRAENOVAE ! TO & ARE FROM (AMLETT REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOGRAPH OF THE UMBILICAL CORD # FESTOONED WITH PROMINENT APPENDICULAE !
" 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF AN APPENDICULA REVEALS TWO CELL TYPES -ICROVILLAR EPITHELIAL CELLS -
OUTNUMBER THE DEEPER GRANULATED CELLS
8 ;=
#(!04%2
&IGURE #ONTINUED
&IGURES # TO & ARE TRANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF APPENDICULAE
# #ROSS SECTION 4HE SURFACE IS COVERED WITH MICROVILLAR CELLS - BRISTLING WITH LONG MICROVILLI 4HE SURFACE CELLS ARE SEPA
RATED BY DILATED INTERCELLULAR SPACES FROM THE BASAL CELLS " ,OOSE CONNECTIVE TISSUE WITH lBROBLASTS & AND BLOOD VESSELS
" FORM THE CORE OF THE APPENDICULA 8
6)6)0!2)49
&IGURE #ONTINUED
$ #ROSS SECTION 'RANULAR CELLS ' ARE INTERPOSED BETWEEN MICROVILLAR CELLS - ON THE SURFACE OF THIS APPENDICULA %XCEP
TIONALLY LONG AND DENSE MICROVILLI ARISE FROM THE APICAL SURFACE OF THE MICROVILLAR CELLS )NTERCELLULAR SPACES ARE CONSPICUOUS
! LAYER OF BASAL CELLS " ABUTS THE CORE OF VASCULAR CONNECTIVE TISSUE 8
#(!04%2
&IGURE #ONTINUED
% 4HE SUPRANUCLEAR 'OLGI COMPLEX ' IN AN APPENDICULAR GRANULATED CELL IS ACTIVELY MODULATING PRESECRETORY MATERIAL
8
& 4HIS APPENDICULAR GRANULATED CELL CONTAINS A PROFUSION OF SECRETORY VESICLES 6 AND PROMINENT 'OLGI COMPLEXES '
8
6)6)0!2)49
&IGURE #ONTINUED
' 3UMMARY DIAGRAM ILLUSTRATING THE STRUCTURE OF THE APPENDICULAR SURFACE -ICROVILLI MV ABOUND ON THE COLUMNAR MICRO
VILLAR CELLS THESE CELLS CONTAIN LIPID INCLUSIONS LP 7EDGED BETWEEN THE MICROVILLAR CELLS ARE GRANULAR CELLS CONTAINING
'OLGI COMPLEXES G MITOCHONDRIA M AND SECRETORY GRANULES SG )NTERCELLULAR SPACES
BETWEEN ADJACENT SURFACE
CELLS AND THE UNDERLYING EPITHELIAL LAYER E ARE OFTEN DILATED !PICAL TIGHT JUNCTIONS OCCUR BETWEEN ADJACENT SURFACE CELLS
&ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS FROM SECTIONS OF THE DUCTUS VITELLO
INTESTINALIS IN THE UMBILICAL CORD OF
THE SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE &ROM (AMLETT B REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE
%DITRICE
! 4HE CONNECTIVE TISSUE INVESTMENT OF THE DUCTUS CONTAINS BLOOD VESSELS "6 COLLAGEN # AND SMOOTH MUSCLE CELLS 3
8
" #ILIATED CELLS # ARE INTERSPERSED WITH MICROVILLAR CELLS - CONTAINING PROMINENT LIPID INCLUSIONS
AND GLYCOGEN
! BASAL LAMINA ARROWHEADS SEPARATES THE EPITHELIUM FROM THE SURROUNDING CONNECTIVE TISSUE ELEMENTS 8
6)6)0!2)49
&IGURE #ONTINUED
# ! PROFUSION OF CILIA
EMERGES FROM A ROW OF BASAL BODIES " ANCHORED BY STRIATED ROOTLET lBRES ARROWHEADS WITHIN CILI
ATED CELLS # -ICROVILLI OPEN ARROWS ALSO OCCUR ON THE CILIATED CELLS -ICROVILLAR CELLS - HAVE UNBRANCHED MICROVILLI
ARROWS PROMINENT LIPID INCLUSIONS , AND GLYCOGEN STORES CIRCLE 8
$ %NTEROENDOCRINE CELLS % WITH SECRETION GRANULES ' ARE WEDGED BETWEEN ADJACENT EPITHELIAL CELLS OF THE DUCTUS
8
% 'RANULES OF THE ENTEROENDOCRINE CELLS ' ARE MEMBRANE BOUND AND OF VARIABLE SHAPE AND ELECTRON DENSITY 8
#(!04%2
6)6)0!2)49
&IGURE -ICROGRAPHS OF SECTIONS OF THE PLACENTA OF THE BLUE SHARK 0RIONACE GLAUCA .O EGG CAPSULE INTERVENES BETWEEN
MATERNAL AND FOETAL TISSUES IN THIS SPECIES !LL lGURES ARE TRANSMISSION ELECTRON MICROGRAPHS EXCEPT FOR ! AND ) WHICH ARE
PHOTOMICROGRAPHS &ROM /TAKE AND -IZUE REPRODUCED WITH PERMISSION FROM THE )CHTHYOLOGICAL 3OCIETY OF *APAN
! 0HOTOMICROGRAPH OF THE DISTAL RUGOSE PORTION OF THE PLACENTA 8
!BBREVIATIONS # CAPILLARY %%# EXTRA
EMBRYONIC COELOM &% FOETAL EPITHELIUM '# GIANT CELL -% MATERNAL EPITHELIUM
" %LECTRON MICROGRAPH FROM THE RUGOSE DISTAL PORTION OF THE PLACENTA SHOWING THE FOETAL EPITHELIUM &% CLOSELY APPOSED
ARROWHEADS TO THE MATERNAL EPITHELIUM -% 4HERE ARE NUMEROUS MITOCHONDRIA - IN THE BASAL CYTOPLASM OF THE MATER
NAL EPITHELIAL CELL 4HE FOETAL EPITHELIUM IS COVERED BY MICROVILLI -6 -# MATERNAL CONNECTIVE TISSUE 8
# ! 'OLGI COMPLEX IN THE CYTOPLASM OF AN EPITHELIAL CELL OF THE MATERNAL PLACENTA 8
$ 4HE BASAL PORTION OF A MATERNAL EPITHELIAL CELL -% IS PACKED WITH MITOCHONDRIA - !N ENDOTHELIAL CELL %# OF A CAPILLARY
IS NEARBY 8
% 0ACKED MICROVILLI FROM FOETAL EPITHELIAL CELLS &% PRESS AGAINST MATERNAL EPITHELIAL CELLS -% NO EGG CAPSULE INTERVENES
4HE ARROWHEAD INDICATES A TUBULAR STRUCTURE IN THE FOETAL EPITHELIAL CELL 8
& 4HE ARROWHEADS INDICATE ELECTRON
DENSE MATERIAL IN THE REGION WHERE MATERNAL -% AND FOETAL &% EPITHELIA COME IN CLOSE
CONTACT 8
' $ESMOSOMES $% CONNECT ADJACENT CELLS IN THE APICAL PORTION OF THE FOETAL EPITHELIUM 4HE INTERCELLULAR SPACE CONTAINS
MATERIAL OF HIGH ELECTRON
DENSITY 8
( 4HE BASAL PORTION OF A FOETAL EPITHELIAL CELL &% IS SEPARATED BY TWO THIN BASAL LAMINAS FROM THE THIN FENESTRATED ENDOTHELIAL
CELL %# OF AN UNDERLYING CAPILLARY !N UNDERLYING DEGENERATE BASAL CELL 5%# AND A GIANT SUPERlCIAL CELL '# CROWD INTO
THIS REGION 4HE EXTRAEMBRYONIC COELOM %%# IS SEEN AT THE TOP 8
#(!04%2
&IGURE #ONTINUED
) 0HOTOMICROGRAPH OF THE SMOOTH PROXIMAL PORTION OF THE PLACENTA ABUTTING ON THE UTERINE CAVITY 5# 'IANT SUPERlCIAL CELLS
'# AND UNDERLYING BASAL CELLS 5%# CONSTITUTE THE FOETAL EPITHELIUM &% 8
* 4RANSMISSION ELECTRON MICROGRAPH SHOWING MICROVILLI -6 ON THE FREE SURFACE OF A GIANT EPITHELIAL CELL FROM THE FOETAL YOLK
SAC 4HERE ARE COATED VESICLES #6 IN THE APICAL CYTOPLASM 8
+ 'IANT SUPERlCIAL CELL '# AND mATTENED BASAL CELL 5%# FROM SMOOTH PROXIMAL PORTION OF THE PLACENTA 8
6)6)0!2)49
&IGURE -ICROGRAPHS OF SECTIONS OF THE INTRAUTERINE EPITHELIUM OF THE BLUE SHARK 0RIONACE GLAUCA DURING LATE GESTATION
! IS A PHOTOMICROGRAPH THE OTHER lGURES ARE TRANSMISSION ELECTRON MICROGRAPHS &ROM /TAKE AND -IZUE REPRODUCED
WITH PERMISSION FROM THE )CHTHYOLOGICAL 3OCIETY OF *APAN
! 4HE INTRAUTERINE EPITHELIUM PRESENTS A THIN BARRIER BETWEEN THE UTERINE CAVITY AND THE ENDOTHELIUM OF CAPILLARIES 8
" 4HE INTRAUTERINE EPITHELIUM RESTS ON LOOSE VASCULAR CONNECTIVE TISSUE )NTERCELLULAR SPACES ARE ABUNDANT BETWEEN THE EPITHE
LIAL CELLS !BUNDANT MITOCHONDRIA ARE DISTRIBUTED IN THE BASAL AND LATERAL PORTIONS OF THE SUPERlCIAL EPITHELIAL CELL 8
# 4HE FREE SURFACE OF A SUPERlCIAL EPITHELIAL CELL WITH BRANCHED MICROVILLI )NVAGINATIONS ARROWHEADS ARE SEEN BETWEEN
THE BASES OF THE MICROVILLI 8
#(!04%2
&IGURE #ONTINUED
$ 4HE BASAL PLASMALEMMAS OF SUPERlCIAL AND BASAL EPITHELIAL CELLS ARE ELABORATELY FOLDED 4HESE CELLS REST ON A DISTINCT BASAL
LAMINA 8
% ! SUPERlCIAL EPITHELIAL CELL CONTAINS ABUNDANT MITOCHONDRIA ! WANDERING PHAGOCYTE CONTAINS LARGE LYSOSOME
LIKE GRANULES
8
!BBREVIATIONS #6 COATED VESICLE %. ENDOTHELIAL CELL %2 ERYTHROCYTE )3 INTERCELLULAR SPACES , LYSOSOME
LIKE GRANULES
- MITOCHONDRIA -6 MICROVILLI O%0 SUPERlCIAL CELL OF THE UTERINE EPITHELIUM 0# PHAGOCYTE 5# UTERINE CAVITY U%0 BASAL
CELL OF THE UTERINE EPITHELIUM
6)6)0!2)49
&IGURE !N EXTREME EXAMPLE OF PLACENTAL EFlCIENCY IS SEEN IN 3COLIODON LATICAUDUS SORRAKOWAH WHERE THERE IS VIRTU
ALLY NO LECITHOTROPHIC PHASE AND THE EMBRYO IMPLANTS IMMEDIATELY AFTER OVULATION $ISTINCTIVE FEATURES OF THIS DEVELOPMENT ARE
SUMMARIZED IN THIS DIAGRAM &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
! 4HE MINUTE MM NEARLY YOLK FREE EGG UNDERGOES A MODIlED FORM OF SELACHIAN DEVELOPMENT WHERE THE BLASTODERM
APPEARS TO UNDERGO COMPLETE EPIBOLY OVER THE YOLK MASS
" ! MM EMBRYO SHORTLY AFTER HATCHING FROM THE EGG ENVELOPE 4HE HEAD IS TO THE LEFT AND THERE ARE ABOUT EIGHT TO NINE
SOMITES $EVELOPMENT OF THE CAUDAL REGION IS INCOMPLETE 4HE EMBRYO IS CONNECTED TO THE YOLK SAC BY AN UMBILICAL STALK
9OLK RESERVES ARE RAPIDLY DEPLETED
# "Y THE MM STAGE ALTHOUGH THE EMBRYO HAS DEVELOPED ONLY TO A MID SOMITE CONDITION THE YOLK HAS DISAPPEARED 4HE YOLK
SAC IS UNDERGOING GROWTH AND DIFFERENTIATION THE UMBILICAL STALK HAS ELONGATED AND APPENDICULAE ARE BEGINNING TO DEVELOP
)MPLANTATION TAKES PLACE SHORTLY AFTER THIS STAGE
$ !T MM THE IMPLANTED EMBRYO IS STILL AT A RUDIMENTARY STAGE OF DEVELOPMENT AND ORGANOGENESIS &IN FOLDS AND lNS EYES
BUCCAL OPENING GILL ARCHES LIVER HEART AND INTESTINE ARE FORMING 4HE UMBILICAL STALK HAS LENGTHENED AND ITS APPENDICU
LAE HAVE BEGUN DO ELONGATE 4HE YOLK SAC HAS DIFFERENTIATED INTO THE EMBRYONIC PORTION OF THE YOLK SAC PLACENTA AND HAS
IMPLANTED INTO THE TROPHONEMATOUS CUP A SPECIALIZED OUTGROWTH OF THE UTERINE WALL 4HE MATERNAL PORTION OF THE PLACENTA
CONSISTS OF THE TROPHONEMATOUS CUP THE TROPHONEMATOUS CORD THE TROPHONEMATOUS BULB AND THE TROPHONEMATOUS STALK
!BBREVIATIONS AP APPENDICULAE BD BLASTODERM H HEAD MY SOMITES T BB TROPHONEMATOUS BULB T CD TROPHONEMATOUS CORD
T CP TROPHONEMATOUS CUP T ST TROPHONEMATOUS STALK U UMBILICAL STALK YK YOLK MASS YS YOLK SAC YSP YOLK SAC PLACENTA
#(!04%2
6)6)0!2)49
&IGURE 3KETCH OF THE REPRODUCTIVE TRACT OF A GRAVID FEMALE COELACANTH ,ATIMERIA CHALUMNAE %ACH FOETUS NUMBERED
TO IS CONTAINED WITHIN ITS OWN WELL
VASCULARIZED COMPARTMENT IN EXPANDED PORTIONS OF THE RIGHT OVIDUCT &ROM 3MITH
ET AL REPRODUCED WITH PERMISSION FROM THE !MERICAN !SSOCIATION FOR THE !DVANCEMENT OF 3CIENCE
!BBREVIATIONS ) INFUNDIBULUM OF THE OVIDUCT / OVARY /6 DISTAL PART OF THE OVIDUCT 2 RECTUM
@
&IGURE &EATURES OF THE PLACENTAL APPARATUS OF 3COLIODON LATICAUDUS SORRAKOWAH &ROM 7OURMS REPRODUCED
WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
! )N THIS PHOTOGRAPH OF A MID LATE TERM PUP ABOUT MM LONG THE VASCULARIZED UMBILICAL STALK U EXTENDS FROM THE VENTRAL
REGION TO AN OPAQUE SPHERICAL YOLK SAC PLACENTA YP ABOUT MM IN DIAMETER ,ONG THIN mATTENED APPENDICULAE A EXTEND
FROM THE UMBILICAL STALK 3CALE BAR MM
" 0HOTOGRAPH OF A PART OF THE UMBILICAL STALK U WITH APPENDICULAE A 4HE ARROW INDICATES THE ORIGIN OF ONE APPENDICULA
"ECAUSE OF THEIR LENGTH AND FRAGILITY ONLY THE BASAL REGIONS OF THE APPENDICULAE ARE PRESENT 3CALE MM
# 4HIS SCANNING ELECTRON MICROGRAPH OF A CRYOFRACTURED SECTION THROUGH THE UMBILICAL STALK REVEALS A VEIN AND AN ARTERY
! VASCULAR BRANCH ARROW TO AN APPENDICULA LIES IN THE MIDDLE OF THE LOWER WALL 7HAT APPEARS TO BE A THIRD VESSEL IN
THE UPPER MIDDLE PORTION OF THE SECTION IS ACTUALLY THE LEFT HAND VESSEL FOLDED ON ITSELF 3MALL PITS P OCCUR ON THE LEFT UPPER
SURFACE ! VITELLO
INTESTINAL DUCT COMMON TO MOST PLACENTAL AND NON
PLACENTAL SHARKS IS ABSENT 3CALE M
$ /VERVIEW OF AN APPENDICULA BY SCANNING ELECTRON MICROSCOPE 4HE SURFACE IS A SYSTEM OF BRANCHING AND ANASTOMOSING
CAPILLARIES C 4HE TRANSVERSE SECTION IN THE FOREGROUND REVEALS TWO MAJOR VESSELS LYING PARALLEL TO EACH OTHER WITH AN INTER
VENING CENTRAL LUMEN 3CALE M
#(!04%2
&IGURE #OELACANTH ,ATIMERIA CHALUMNAE 0HOTOGRAPH OF A PUP LYING ON ITS RIGHT SIDE AFTER REMOVAL FROM ITS UTERINE
COMPARTMENT 4HE YOLK SAC IS mACCID WITH A LONG JUNCTION BETWEEN THE VENTRAL SURFACE AND THE PUP &ROM 7OURMS !TZ AND
3TRIBLING REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE WALLS OF THE UTERUS AND YOLK SAC OF THE COELACANTH ,ATIMERIA CHALUMNAE
&ROM 7OURMS !TZ AND 3TRIBLING REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
! 0LACENTAL REGIONS OF THE UTERINE LINING ARE EMBOSSED BY AN ANASTOMOSING NETWORK OF CAPILLARIES CN COVERED BY A SIMPLE
SQUAMOUS EPITHELIUM UE WHOSE SURFACE IS AMPLIlED BY PLEATS AND RIDGES 5NDERLYING CAPILLARIES C WERE EXPOSED BY
CUTTING THROUGH THE WALL 4HE ARROW INDICATES THE CUT SURFACE
" )N THIS SECTION OF THE UTERINE WALL THE LUMINAL SURFACE OF THE UTERINE EPITHELIUM UE IS AT THE TOP #IRCULAR PROlLES CN
OF THE CAPILLARY NETWORK ARE EXPOSED ALONG THE CUT SURFACE "LOOD VESSELS BV LIE WITHIN THE CONNECTIVE TISSUE STROMA CTS
AND SMOOTH MUSCLE SM OF THE WALL 4HE WALL IS ENCLOSED WITHIN SEROSAL EPITHELIUM ESU
6)6)0!2)49
&IGURE #ONTINUED
# 4HIS TRANSVERSE SECTION OF THE WALL OF THE YOLK SAC SHOWS THAT IT IS CONSTITUTED LARGELY OF A DENSE STROMA OF lBROUS CONNEC
TIVE TISSUE CTS ! THIN EPITHELIAL LAYER ARROWS COVERS THE EXTERNAL SURFACE 9OLK Y AND BLOOD VESSELS BV OF THE VITELLINE
CIRCULATION LIE BENEATH THE CORTEX
$ 4HE EXTERNAL SURFACE OF THE YOLK SAC IS CONVOLUTED AND FOLDED AND CONSISTS OF A SIMPLE SQUAMOUS EPITHELIUM YSE ADHERING
TO AN INTERCOMMUNICATING BED OF CORTICAL SINUSES
% 4RANSVERSE SECTION OF THE CORTEX OF THE YOLK SAC 4HE SQUAMOUS EPITHELIUM YSE OF THE YOLK SAC ENCLOSES A WELL DEVEL
OPED SYSTEM OF CORTICAL SINUSES CS #OLUMNAR TRABECULAE TR EXTEND FROM THE UNDERSURFACE OF THE EPITHELIUM TO A LOOSELY
ORGANIZED BOUNDARY AT THE UPPER SURFACE OF THE CONNECTIVE TISSUE STROMA CTS
#(!04%2
&IGURE 3CHEMATIC REPRESENTATION OF A TRANSVERSE SECTION OF THE OVARY OF THE GUPPY 0OECILIA RETICULATA 4HE OVARY IS
A SINGULAR SACCULAR ORGAN $EVELOPMENT OF OOCYTES AND EMBRYOS TAKES PLACE WITHIN ITS WALL 6ARIOUS STAGES OF FOLLICULAR
GROWTH AND FOLLICULAR ATRESIA HAVE BEEN COMBINED INTO ONE PICTURE ACTUALLY THESE STAGES DO NOT OCCUR SIMULTANEOUSLY
/ TO / ARE OOCYTES IN VARIOUS STAGES OF DEVELOPMENT % INDICATES EMBRYOS WHILE _ ` AND a ARE STAGES OF FOLLICULAR ATRESIA
&ROM ,AMBERT A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF THE OVIDUCT OF ,EPIDOGALAXIAS SALAMANDROIDES A SMALL FRESHWATER lSH
&AMILY ,EPIDOGALAXIIDAE /RDER 3ALMONIFORMES ENDEMIC TO THE SOUTHWEST OF 7ESTERN !USTRALIA &ROM 0USEY AND 3TEWART
REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! &REE SPERMATOZOA IN THE OVIDUCT 3CALE BAR M
" 4HE CRYPT REGION OF THE OVIDUCT SHOWING EMBEDDED SPERMATOZOA 3CALE BAR M
!BBREVIATIONS C CILIA DE DUCT EPITHELIUM S SPERMATOZOA
6)6)0!2)49
&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH MATURE OVARIES OF SEVERAL SPECIES FROM THE 3UBFAMILY 'LANDULOCAUDINAE
OF THE &AMILY #HARACIDAE !RROWS INDICATE SPERMATOZOA &ROM "URNS ET AL REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
! 0LANALTINA MYERSI 8
" 'EPHRYOCHARAX ATRICAUDATUS 8
# 8ENUROBRYCON POLYANCISTRUS 8
$ 4YTTOCHARAX SP 8
% 0SEUDOCORNYOPOMA HETERANDRIA 8
& 0SEUDOCORNYOPOMA DORIAE 8
' -IMAGONIATES SYLVICOLA 8
( -IMAGONIATES MICROLEPIS 8
#(!04%2
&IGURE 3PERM STORAGE IN THE GUPPY 0OECILIA RETICULATA &ROM .AGAHAMA REPRODUCED WITH PERMISSION FROM
%LSEVIER 3CIENCE AND + 4AKANO
! $IAGRAMMATIC REPRESENTATION OF THE OVARY SHOWING FOLLICLES AT VARIOUS STAGES OF DEVELOPMENT TO AND THE LOCATION OF
THE SPECIALIZED STRUCTURES OF INTERNAL FERTILIZATION THE DELLE AND SEMINAL RECEPTACLE
" %LECTRON MICROGRAPH OF A SECTION OF THE SEMINAL VESICLE WITHIN THE OVARY 3PERMATOZOA ARE DEEPLY EMBEDDED IN THE APICAL
CYTOPLASM OF THE EPITHELIAL CELLS
6)6)0!2)49
&IGURE 4HE SEMINAL RECEPTACLE OF THE GUPPY 0OECILIA RETICULATA &ROM *ALABERT AND "ILLARD REPRODUCED WITH
PERMISSION OF ).2! 0ARIS
! 3CHEMATIC DIAGRAM OF A SAGITTAL SECTION OF AN OVARY SHOWING THE SEMINAL RECEPTACLE AT THE TOP 4HE OVARY IS SURROUNDED BY
VISCERAL PERITONEUM /OCYTES AT VARIOUS STAGES OF DEVELOPMENT ARE INDICATED BY NUMBERED CIRCLES 4HE SEMINAL RECEPTACLE
IS INCOMPLETELY DIVIDED INTO CHAMBERS
" !N ENLARGEMENT OF THE RECTANGLE SHOWN IN ! SHOWING A PORTION OF AN ALVEOLAR CHAMBER OF THE SEMINAL RECEPTACLE 4HE SEC
TION SHOWN IN THE ELECTRON MICROGRAPH BELOW &IGURE # WAS CUT ALONG THE LINE B B &OR SIMPLICITY SPERMATOZOA
HAVE BEEN SHOWN WITHIN ONLY ONE CELL
#(!04%2
&IGURE #ONTINUED
# %LECTRON MICROGRAPH OF A TANGENTIAL SECTION OF THE SEMINAL RECEPTACLE B B ABOVE SHOWING SPERMATOZOA AT VARIOUS
LEVELS WITHIN HOST CELLS .UMEROUS DESMOSOMES CONNECT THE CELLS AND LATERAL BORDERS ARE MARKEDLY INTERDIGITATED 4HE LOBES
OF THE NUCLEUS AT THE CENTRE ARE SEPARATED BY A CYTOPLASMIC BRIDGE
!BBREVIATIONS " BASAL LAMINA #S BLOOD CAPILLARY CY CYTOPLASM OF HOST CELL D DESMOSOME & mAGELLUM G 'OLGI COMPLEX
- CELL MEMBRANE M MITOCHONDRIA . NUCLEUS 0I MITOCHONDRIAL MIDPIECE OF SPERM 3 SPERM HEAD 3TR CONNECTIVE TISSUE
STROMA OF THE OVARY TF TONOlLAMENTS 8
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE OVARY OF #YMATOGASTER AGGREGATA SHOWING SPERMATOZOA
WITHIN POCKETS IN THE LUMINAL EPITHELIUM &ROM 'ARDINER REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE SPERMATOZOA ARE ORIENTED WITH THEIR HEADS TOWARD THE EPITHELIAL CELLS AND ARE SECTIONED TRANSVERSELY AT VARIOUS LEVELS OF
THE HEAD AND MITOCHONDRIAL MIDPIECE 8
" 3PERM HEADS LODGED WITHIN INDENTATIONS OF THE OVARIAN EPITHELIUM 4HE MEMBRANES OF THE SPERM AND EPITHELIA ARE SEPARATED
BY A SPACE OF SEVERAL NANOMETERS AND REMAIN INTACT 8
#(!04%2
6)6)0!2)49
&IGURE )LLUSTRATIONS SHOWING SPERM STORAGE IN THE OVARY OF (ETERANDRIA FORMOSA &ROM &RASER AND 2ENTON
REPRODUCED WITH PERMISSION FROM THE #OMPANY OF "IOLOGISTS ,TD
! $RAWING OF A SECTION THROUGH A POCKET OF THE OVARIAN CAVITY THE EXPANDED DISTAL WALL OF WHICH IS PRESSED AGAINST THE FOL
LICULAR EPITHELIUM -ASSES OF SPERMATOZOA ARE SEEN BOTH IN THE POCKET AND IN THE OVARIAN CAVITY 8
" 0HOTOMICROGRAPH OF A SECTION THROUGH A SPECIAL PROTRUBERANCE FROM AN EGG INTO THE OVARIAN CAVITY AT THE TIME OF FERTILIZA
TION #ROWDS OF SPERMATOZOA ARE GATHERED OVER THE THIN MEMBRANE OF THE PROTRUBERANCE 4HE ZONA PELLUCIDA AND FOLLICULAR
EPITHELIUM ARE ABSENT BENEATH THE PROTRUBERANCE 8
# $RAWING OF A SECTION THROUGH THE SOLID PLUG FORMED AFTER FERTILIZATION FROM THE UNION OF THE FOLLICULAR EPITHELIUM AND THAT
OF THE OVARIAN POCKET 4HE ZONA PELLUCIDA HAS SEPARATED FROM THE FOLLICLE DURING lXATION 0ART OF THE WALL OF ANOTHER OVUM
FEP IS ALSO SEEN 8
!BBREVIATIONS CT CONNECTIVE TISSUE SHEATH OF THE OVARY FEP FOLLICULAR EPITHELIUM MIT CELL UNDERGOING MITOSIS OVC OVARIAN
CAVITY OVP POCKET OF THE OVARIAN CAVITY PL PLUG SP SPERMATOZOA UNILECT UNILAMINAR ECTODERM YG YOLK GRANULES Z ZONA
PELLUCIDA
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE OVARY OF THE GUPPY ,EBISTES RETICULATUS SHOWING THE FOETAL
MATERNAL BARRIER AT FOUR WEEKS OF GESTATION 3EVERAL LAYERS ARE INTERPOSED BETWEEN THE LUMINA OF A MATERNAL CAPILLARY -#, AND
A FOETAL CAPILLARY &#, 4HESE INCLUDE BOTH MATERNAL AND FOETAL ENDOTHELIAL CELLS E THEIR BASAL LAMINAS THE INNER FOLLICULAR
EPITHELIUM )% AND THE YOLK SAC EPITHELIUM 93% 4HERE IS EXTENSIVE MICROPINOCYTOSIS IN ALL CELLULAR LAYERS OF THE BARRIER
8 &ROM *OLLIE AND *OLLIE B REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE $IAGRAM OF A SECTION THROUGH THE OVARY OF THE POECILIID (ETERANDRIA FORMOSA TO ILLUSTRATE THE RELATIONSHIP
OF THE EMBRYOS TO THE OVARIAN TISSUES /NE FOLLICLE HAS BEEN ENLARGED TO ILLUSTRATE THE PRESENCE OF THE EGG ENVELOPE BETWEEN
THE ABSORPTIVE SURFACE OF THE EMBRYO AND THE FOLLICULAR EPITHELIUM 4HIS DIAGRAM DEMONSTRATES SUPERFOETATION WHERE EMBRYOS
AT THREE STAGES OF DEVELOPMENT ARE PRESENT IN THE SAME OVARY &ROM 'ROVE AND 7OURMS REPRODUCED WITH PERMISSION
OF *OHN 7ILEY 3ONS )NC
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE FOLLICULAR EPITHELIUM OF AN EARLY VITELLOGENIC OOCYTE OF THE
POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! &OLLICULAR EPITHELIUM .OTE THE IRREGULAR ELECTRON
LUCENT VESICLE ELV AND ASSOCIATED TUBULAR EXTENSIONS ARROWHEADS
"AR M
" !PICAL REGION OF A FOLLICULAR CELL AND OOCYTE -ITOCHONDRIA MITO SOME GRANULAR ENDOPLASMIC RETICULUM 2%2 VESICLES
CONTAINING mOCCULENT MATERIAL
COATED VESICLES CIRCLE IRREGULAR ELECTRON
LUCENT VESICLES ELV AND CROSS
SECTIONAL
PROlLES OF THEIR TUBULAR EXTENSIONS ARROWHEADS OCCUR IN THE CYTOPLASM "AR NM
# ! COATED VESICLE FROM THE CELL SHOWN IN " "AR NM
$ % #OATED PITS ON THE LATERAL SURFACES OF FOLLICULAR CELLS "AR NM
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE FOLLICULAR EPITHELIUM SOON AFTER FERTILIZATION IN THE POECI
LIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE FOLLICULAR CELLS HAVE ACQUIRED THE ULTRASTRUCTURAL FEATURES OF TRANSPORTING CELLS "AR M
" 4HE APICAL CYTOPLASM OF THE CELL SHOWN IN ! CONTAINS GRANULAR ENDOPLASMIC RETICULUM 2%2 COATED VESICLES ARROWHEADS
AND OTHER VESICLES
"AR M
6)6)0!2)49
&IGURE #ONTINUED
# !N APICAL JUNCTIONAL COMPLEX FROM THE CELL SHOWN IN ! "AR NM
$ *UNCTIONAL COMPLEX ILLUSTRATING A REGION WITH THE CHARACTERISTICS OF A TIGHT JUNCTION "AR NM
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A SECTION THROUGH THE BASAL REGION OF THE FOLLICULAR EPITHELIUM SOON AFTER
FERTILIZATION IN THE POECILIID (ETERANDRIA FORMOSA "ARS NM &ROM 'ROVE AND 7OURMS REPRODUCED WITH PERMIS
SION OF *OHN 7ILEY 3ONS )NC
! ! CAPILLARY IS CLOSELY APPOSED TO THE FOLLICULAR BASAL LAMINA )TS ENDOTHELIAL CELL CONTAINS SMALL VESICLES
" #OATED PITS ARE SEEN IN THE BASAL PLASMALEMMA OF THE FOLLICULAR CELL
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE FOLLICULAR EPITHELIUM INVESTING A MIDTERM EMBRYO OF THE
POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE FOLLICULAR CELLS FORM A LOW CUBOIDAL EPITHELIUM THE EGG ENVELOPE ZONA PELLUCIDA IS INTACT AND CAPILLARIES ARE CLOSELY
APPLIED TO ITS BASAL LAMINA "AR M
" -ICROVILLI COVER THE APICAL SURFACE OF A FOLLICULAR CELL "AR M
# 4HE ARROWHEAD INDICATES A COATED ENDOCYTOTIC PIT AT THE BASE OF A MICROVILLUS ON THE APICAL SURFACE OF A FOLLICULAR CELL
"AR NM
$ !N APICAL MICROVILLUS IS SURROUNDED BY A COATED PIT ARROWHEAD "AR NM
% 4HE APICAL SUPRANUCLEAR CYTOPLASM OF A FOLLICULAR EPITHELIAL CELL CONTAINS ELECTRON
LUCENT VESICLES ELV MITOCHONDRIA
GRANULAR ENDOPLASMIC RETICULUM 2%2 'OLGI COMPLEXES AND ELECTRON
DENSE VESICLES DSV "AR M
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE FOLLICULAR EPITHELIUM INVESTING A MIDTERM EMBRYO OF THE
POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! ,ATERAL MEMBRANES OF ADJACENT CELLS INTERDIGITATE EXTENSIVELY WITH EACH OTHER "AR M 4HE INSET SHOWS APICAL JUNCTIONAL
COMPLEXES "AR NM
" 4HE BASAL SURFACE OF A FOLLICULAR CELL SHOWS COATED PITS CIRCLES "AR NM
# 3MOOTH SURFACED PITS ARE ALSO SEEN IN THE BASAL MEMBRANE "AR NM
$ 4HE BASAL SURFACE OF THIS FOLLICULAR CELL IS EXTENSIVELY FOLDED ! CAPILLARY IS CLOSELY APPOSED TO ITS BASAL LAMINA "AR M
#(!04%2
&IGURE $RAWINGS DEMONSTRATING ADAPTATIONS FOR VIVIPARITY IN EMBRYOS AND THE OVARY OF !NABLEPS ANABLEPS &ROM
4URNER A REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
0LATE /VARY
/VARY CONTAINING SEVEN
MM EMBRYOS ! INDICATES A FOLLICLE WITH THE OVARIAN WALL DISSECTED AWAY AND A mAP OF
THE FOLLICULAR WALL LAID BACK TO SHOW THE RELATION OF THE YOLK SAC AND YOLK SAC BULBS TO THE FOLLICULAR WALL AND FOLLICULAR
VILLI " IS A SPACE FROM WHICH AN EMBRYO AND THE FOLLICLE HAVE BEEN REMOVED # $ % AND & REPRESENT EMBRYOS ENCLOSED
WITHIN INTACT FOLLICLES AND THE OVARIAN WALL
!N ENLARGEMENT OF THE INTERNAL SURFACE OF THE FOLLICLE FROM THE WINDOW DEPICTED IN 3HOWN ARE FOLLICULAR VILLI AND THE
DEPRESSIONS CAUSED BY CONTACT WITH YOLK SAC BULBS
6)6)0!2)49
&IGURE #ONTINUED
0LATE %MBRYONIC STAGES
"LASTULA SHOWING YOLK OIL DROPLETS BLASTODISC AND VITELLINE MEMBRANE
%MBRYO MM WITH EXPANDED YOLK SAC "LOOD VESSELS ARE INDICATED BY LIGHT LINES 4HE YOLK SAC IS TRANSPARENT AND CONTAINS
NO YOLK
%MBRYO MM WITH EXPANDED YOLK SAC AND EARLY STAGES OF YOLK SAC BULBS
%MBRYO MM WITH MORE ADVANCED YOLK SAC BULBS
%MBRYO MM WITH YOLK SAC AT MAXIMAL STAGE OF EXPANSION
%MBRYO MM 9OLK SAC BULBS HAVE REACHED THEIR MAXIMAL SIZE
%MBRYO MM 9OLK SAC IS BEING ABSORBED AND YOLK SAC BULBS ARE DISAPPEARING
%MBRYO MM 9OLK SAC HAS BEEN WITHDRAWN INTO THE BODY CAVITY AND VENTRAL BODY WALL IS CLOSING
#(!04%2
&IGURE #ONTINUED
0LATE 3ECTIONS OF THE FOLLICULAR WALL
4HE CAPSULE SURROUNDING A BLASTULA AS WELL AS THE UNDERLYING SPONGY CONNECTIVE TISSUE STROMA 8
4HE WALL OF A FOLLICLE CONTAINING A
MM EMBRYO 4HE YOLK SAC OF THE EMBRYO IS COVERED WITH A CUBOIDAL EPITHELIUM SUP
PORTED BY A THIN LAYER OF CONNECTIVE TISSUE "ENEATH THIS EPITHELIUM BLOOD VESSELS AND BULBS HAVE THIN WALLS COMPOSED OF
ENDOTHELIUM LYING UPON DELICATE CONNECTIVE TISSUE -ANY RICHLY VASCULAR FOLLICULAR VILLI HANG FREE IN THE FOLLICULAR SPACE
8
!BBREVIATIONS #!0 CAPILLARY %-"%#4 EMBRYONIC ECTODERM %-"'47 EMBRYONIC GUT WALL &/,#!03 FOLLICULAR CAP
SULE &/,%0)4( OLD FOLLICULAR EPITHELIUM &/,30 FOLLICULAR SPACE &/,6), FOLLICULAR VILLUS &/,7 FOLLICULAR WALL
/634 OVARIAN STROMA /67 OVARIAN WALL 4330 TISSUE SPACE 93 YOLK SAC 9+3"," YOLK SAC BULB 9+330 YOLK SAC
SPACE
6)6)0!2)49
&IGURE 4HE FOUR EYED lSH !NABLEPS DOWI DEMONSTRATES AN EXTREME OF MATROTROPHIC NUTRITION WHERE EMBRYOS INCREASE
IN DRY WEIGHT AS MUCH AS TIMES DURING GESTATION AND NUTRIENT TRANSFER IS FACILITATED IN THE FOLLICULAR PLACENTA BY INCREASES IN
SURFACE AREA FOR EXCHANGE &IGURES " TO ( ARE SCANNING ELECTRON MICROGRAPHS +NIGHT ET AL REPRODUCED WITH PERMIS
SION OF *OHN 7ILEY 3ONS )NC
! 0HOTOGRAPH OF A MM EMBRYO REMOVED FROM ITS FOLLICLE 4HE LARGE PROMINENT PERICARDIAL TROPHODERM BEARS VASCULAR
BULBS ON ITS SURFACE AND OCCUPIES THE SAME POSITION IN WHICH THE YOLK SAC IS FOUND IN MOST EMBRYOS 8
" 6ASCULAR BUDS STUDDING THE SURFACE OF THE PERICARDIAL TROPHODERM INCREASE THE SURFACE AREA FOR EXCHANGE 8
# 3EVERAL VASCULAR BULBS FROM THE REGION SHOWN IN " )NDIVIDUAL EPITHELIAL CELLS ON THEIR SURFACES ARE DELINEATED BY INTERCEL
LULAR CLEFTS 8 4HE INSET SHOWS THE MICROPLICAE THAT FURTHER AMPLIFY THE SURFACE FOR EXCHANGE 8
$ 6ASCULAR BULBS ARE HOLLOW DOMELIKE CHAMBERS ! PORTION OF THE WALL OF THIS VASCULAR BULB HAS BEEN BROKEN AWAY TO REVEAL AN
EMPTY BLOOD SINUS WITHIN 4HE BLOOD SINUSES ARE CONTINUOUS FROM ONE VASCULAR BULB TO ANOTHER 8 ! FRACTURED VASCULAR
BULB CONTAINING ERYTHROCYTES IS SHOWN IN THE INSET 8
% 2EGIONS OF THE INNER SURFACE OF THE FOLLICULAR WALL ARE RIDDLED WITH SHALLOW PITS THAT INTERDIGITATE WITH THE VASCULAR BULBS OF
THE PERICARDIAL TROPHODERM 8
& !N ADJACENT REGION OF THE SAME FOLLICULAR WALL SHOWN IN % IS COVERED WITH VILLOUS PROCESSES SOME OF WHICH HAVE BEEN DE
FORMED TO ACCOMMODATE VASCULAR BULBS 8
#(!04%2
&IGURE #ONTINUED
' )N LATE GESTATION THE HYPERTROPHIED EPITHELIUM LINING THE FOLLICULAR WALL IS COMPRISED ENTIRELY OF FREE VILLI 8
( /N THE SURFACE OF A FOLLICULAR VILLUS THE EPITHELIAL CELLS POSSESS SHORT STUBBY MICROVILLI AND IRREGULAR MICROPLICAE 8
&IGURE 3CHEMATIC DIAGRAM OF THE NEAR
TERM OVARY OF THE GOODEID !MECA SPLENDENS ILLUSTRATING THE RELATIONSHIPS OF
EMBRYOS TO THE INTERNAL STRUCTURES OF THE OVARY 4HE ANTERIOR THIRD OF THE OVARY HAS BEEN REMOVED TO ILLUSTRATE THE INTERNAL
OVARIAN ANATOMY 2IBBON
LIKE ABSORPTIVE TROPHOTAENIAE EXTENDING FROM THE HINDGUT OF THE EMBRYOS ARE BATHED IN THE NUTRITIVE
EMBRYOTROPHE OF THE OVARIAN LUMEN "AR CM &ROM 7OURMS 'ROVE AND ,OMBARDI REPRODUCED WITH PERMISSION FROM
%LSEVIER 3CIENCE
!BBREVIATIONS OF OOCYTE OM MESOVARIUM OS OVARIAN SEPTUM OW OVARIAN WALL
6)6)0!2)49
&IGURE 0HOTOMICROGRAPH OF A CROSS SECTION THROUGH THE OVARY CONTAINING SIX EMBRYOS % OF THE GOODEID 8ENO
TOCA EISENI &ROM 3CHINDLER REPRODUCED WITH PERMISSION 4HE OVARY IS SUSPENDED BY TWO MESOVARIA OPEN ARROWS
4HE OVARIAN CAVITY IS INCOMPLETELY ARROWHEADS DIVIDED BY A FOLDED MEDIAN SEPTUM ARROWS 4HE INTERNAL OVARIAN EPITHELIUM
COVERS THE INNER LINING OF THE OVARIAN WALL AS WELL AS BOTH SIDES OF THE SEPTUM 4HE ASTERISKS INDICATE SECTIONS THROUGH EMBRYONIC
TROPHOTAENIAE 8
&IGURE $RAWINGS OF THE ANTERIOR END OF AN UNBORN MM EMBRYO OF THE EMBIOTOCID lSH #YMATOGASTER AGGREGATA TO
SHOW THE RELATIONSHIP OF A FOLD OF OVARIAN TISSUE /64 TO THE OPERCULUM /0 OF THE EMBRYO &ROM 4URNER REPRODUCED
WITH PERMISSION OF THE !MERICAN 3OCIETY OF )CHTHYOLOGISTS AND (ERPETOLOGISTS
! )NTACT EMBRYO WITH A FOLD OF MATERNAL OVARIAN TISSUE INSERTED UNDER THE RIGHT OPERCULUM
" 6ENTRAL VIEW OF THE SAME EMBRYO
#(!04%2
&IGURE 4HE YOLK SAC PERICARDIAL SAC AND COELOMIC SAC PLAY A MAJOR ROLE IN THE UPTAKE OF NUTRIENTS IN SEVERAL SPECIES
&ROM 4URNER A C REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! )N THIS DRAWING OF AN EARLY STAGE OF THE GOODEID !TAENOBIUS TOWERI THE PERICARDIAL SAC AND YOLK SAC ARE COVERED BY A PORTAL
VASCULAR NETWORK
" 4HIS EARLY STAGE OF THE GOODEID 'OODEA LUITPOLDII ILLUSTRATES THE PORTAL NETWORK IN A RELATIVELY SMALL YOLK SAC AND AN
EXPANDED PERICARDIAL SAC
# 4HE YOLK SAC HAS BEEN ALMOST COMPLETELY ABSORBED IN THIS EMBRYO OF THE POECILIID 0OECILIOPSIS SP 4HE hBELLY SACv IS
COVERED BY A PORTAL NETWORK AND CONSISTS OF THE PERICARDIAL SAC ANTERIORLY AND AN EXPANDED COELOM POSTERIORLY
!BBREVIATIONS "3 hBELLY SACv (4 HEART 0#3AC PERICARDIAL SAC 36 SINUS VENOSUS 9K3 YOLK SAC
6)6)0!2)49
&IGURE )N A FEW TELEOSTS lNGER SHAPED OR RIBBON LIKE EXTENSIONS OF THE PROCTODAEUM THE TROPHOTAENIAE TAKE UP MA
TERIALS FROM THE EMBRYOTROPH THESE DRAWINGS ILLUSTRATE TROPHOTAENIAE IN GOODEIDS &ROM 4URNER C REPRODUCED WITH
PERMISSION OF *OHN 7ILEY 3ONS )NC
! 6ENTRAL VIEW OF AN EMBRYO OF 'OODEA LUITPOLDII ILLUSTRATING TROPHOTAENIAE CLUSTERED AROUND THE ANAL OPENING
" )N THIS EARLY EMBRYO #HARACODON LATERALIS THE YOLK SAC IS RECEDING AND THE PERICARDIAL SAC IS AT ITS MAXIMAL SIZE 4RO
PHOTAENIAE ARE GROWING RAPIDLY AND BECOMING VASCULARIZED 4HE EXTENSIVE PORTAL NETWORK ON THE PERICARDIAL SAC IS NOT
ILLUSTRATED
# 4HE YOLK IS ALMOST EXHAUSTED IN THIS EMBRYO OF :OOGONETICUS QUITZEOENSIS 4HE VASCULAR PERICARDIAL SAC HAS BEGUN TO RECEDE
AND IS BEING REPLACED FUNCTIONALLY BY THE RAPIDLY DEVELOPING TROPHOTAENIAE
$ !N EMBRYO OF :OOGONETICUS QUITZEOENSIS IN LATE GESTATION 4HE TROPHOTAENIAE ARE HIGHLY VASCULAR AND SERVE FOR RESPIRATION
AND THE ABSORPTION OF NUTRIENTS
!BBREVIATIONS (4 HEART /P / OPERCULAR OPENING 0#3AC PERICARDIAL SAC 4R TROPHOTAENIAE 9K YOLK
#(!04%2
&IGURE 3CHEMATIC REPRESENTATION OF AN ADULT FEMALE OF !MECA SPLENDENS ILLUSTRATING THE RELATIVE SIZE AND POSITION
OF THE OVARY WITHIN THE BODY CAVITY "OTH THE EMBRYOS AND THE ANTERIOR THIRD OF THE OVARY HAVE BEEN DELETED TO ILLUSTRATE THE
INTERNAL OVARIAN ANATOMY "AR CM &ROM 3CHINDLER AND 7OURMS A REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
!BBREVIATIONS /$ OVIDUCT /& OVARIAN FOLD /, OVARIAN LUMEN /- MESOVARIUM // OOCYTE /3 OVARIAN SEPTUM
/7 OVARIAN WALL 50 URINOGENITAL PORE
A
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF GRAVID OVARIES OF GOODEIDS &ROM 3CHINDLER REPRO
DUCED WITH PERMISSION
! 3EGMENTS OF THE INTERNAL OVARIAN EPITHELIUM OF 8ENOTOCA EISENI COVER OPPOSITE FOLDS ON THE OVARIAN SEPTUM #APILLARIES IN A
NEAR
SURFACE POSITION ARE ENCLOSED BY ATTENUATED CYTOPLASMIC PROCESSES 4HE DEMARCATION BETWEEN THE DARKER SUBEPITHELIAL
ZONE AND THE MULTILOCULAR CORE OF THE OVARIAN FOLDS IS MARKED BY A SERIES OF ARROWHEADS 8
" 4HREE CELLS OF THE INTERNAL OVARIAN EPITHELIUM OF 8ENOTOCA EISENI ARE CONNECTED BY APICAL JUNCTIONAL COMPLEXES AND MAY
BE HIGHLY INTERDIGITATED "UNDLES OF INTERMEDIATE lLAMENTS CRISS
CROSS THE CYTOPLASM .UMEROUS ELECTRON
LUCENT VESICLES
AND A FEW ELEMENTS OF THE GRANULAR ENDOPLASMIC RETICULUM ARE DISTRIBUTED THROUGHOUT THE CYTOPLASM 8
# 4HE mATTENED INTERNAL OVARIAN EPITHELIUM AND THE ENDOTHELIUM OF A SUBJACENT CAPILLARY IN THE OVARY OF 'IRARDINICHTHYS
VIVIPARUS EXHIBIT ENDOCYTOTIC OR EXOCYTOTIC ACTIVITY ARROWS 8
)NSET
4HE LUMINAL SURFACE OF THE INTERNAL OVARIAN EPITHELIUM SHOWS A COATED PIT ARROW AND TWO SMALL UNCOATED
INVAGINATIONS ARROWHEADS 4HE CYTOPLASM CONTAINS AN INCLUSION OF LIPOID MATERIAL 8
!BBREVIATIONS % ERYTHROCYTE %N ENDOTHELIUM # CAPILLARY )/% INTERNAL OVARIAN EPITHELIUM /, OVARIAN LUMEN
6)6)0!2)49
#(!04%2
6)6)0!2)49
@
&IGURE -ICROGRAPHS OF SECTIONS OF THE NEAR
TERM OVARY OF THE GOODEID !MECA SPLENDENS &ROM ,OMBARDI AND 7OURMS
A REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 0HOTOMICROGRAPH OF A LONGITUDINAL SECTION THROUGH THE OVARIAN WALL )T IS COMPOSED OF FOUR LAYERS THE OVARIAN PERITO
NEUM OP A MUSCULAR LAYER MU OF OUTER LONGITUDINAL AND INNER CIRCULAR MUSCLE lBRES CONNECTIVE TISSUE STROMA CT AND
THE INTERNAL OVARIAN EPITHELIUM IOE OL OVARIAN LUMEN 8
" 3CANNING ELECTRON MICROGRAPH OF THE INTERNAL OVARIAN EPITHELIUM IOE THAT LINES THE OVARIAN LUMEN 4HE EPITHELIUM IS THROWN
INTO A SERIES OF IRREGULAR FOLDS MARGINAL CLEFTS ARROWS DELINEATE INDIVIDUAL CELLS 8
# )N THIS TRANSMISSION ELECTRON MICROGRAPH THE INTERNAL OVARIAN EPITHELIUM IS SEPARATED BY A THIN MODERATELY FOLDED BAS
AL LAMINA BL FROM A CONNECTIVE TISSUE STROMA CONTAINING A CAPILLARY CA COLLAGENOUS lBRES CO AND lBROBLASTS FB
4HE LATERAL SURFACES OF THE EPITHELIAL CELL ARE INTERDIGITATED AND SEALED APICALLY BY JUNCTIONAL COMPLEXES 4HE CYTOPLASM OF
THE EPITHELIAL CELL CONTAINS LARGE VESICLES ARROWS DERIVED FROM THE GRANULAR ENDOPLASMIC RETICULUM MF MARGINAL FURROW
NU NUCLEUS OL OVARIAN LUMEN 8
$ 4RANSMISSION ELECTRON MICROGRAPH OF AN INTERNAL OVARIAN EPITHELIAL CELL CONTAINING VESICLES THAT ARE STUDDED WITH RIBOSOMES
ARROW 4HESE VESICLES ARE ENLARGED CISTERNAE OF THE GRANULAR ENDOPLASMIC RETICULUM GER AND HAVE A MODERATELY ELECTRON
DENSE GRANULAR MATRIX )NTERMEDIATE lLAMENTS ARE PRESENT IN THE SURROUNDING CYTOPLASM 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF REPRESENTATIVE SECTIONS OF THE INTERNAL OVARIAN EPITHELIUM FROM GRAVID
FEMALES OF THREE SPECIES OF GOODEID lSH !LL ARE SIMPLE EPITHELIA WITH HIGHLY INTERDIGITATED LATERAL CELL MEMBRANES 4HE DOMED
EPITHELIAL CELLS ARE REMINISCENT OF A TRANSITIONAL EPITHELIUM !LL EPITHELIA ARE WELL VASCULARIZED &ROM (OLLENBERG AND 7OURMS
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !LLOOPHORUS ROBUSTUS .OTE THE APPARENT CYTOPLASMIC BUDDING FROM THE APICAL REGION OF THE CELL AT THE FAR LEFT 8
" :OOGONETICUS QUITZEOENSIS 8
# 'OODEA ATRIPINNIS .OTE THE LIPID ACCUMULATION IN THE CENTRE CELL $ARK ANNULI IN THE LIPID DROPLETS ARE THE RESULT OF
FERROCYANIDE POSTlXATION 8
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE INTERNAL OVARIAN EPITHELIUM FROM A GRAVID FEMALE GOODEID !LLOOP
HORUS ROBUSTUS )NTERCELLULAR SPACES ARE OFTEN OCCUPIED BY CELLS THAT ARE PROBABLY LEUCOCYTES &ROM (OLLENBERG AND 7OURMS
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 8
" 4HERE ARE MULTIPLE 'OLGI COMPLEXES AND SMALL GRANULES ARROWHEADS IN THE CELL ON THE RIGHT 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF INTERNAL OVARIAN EPITHELIAL CELLS IN SECTIONS OF THE OVARY OF THE GOODEID
TELEOST 8ENOOPHORUS CAPTIVUS &ROM 3CHINDLER +UJAT AND DE 6RIES REPRODUCED WITH PERMISSION OF THE AUTHORS
! )N A NON
GRAVID OVARY THE EPITHELIAL CELLS ARE CUBOIDAL TO COLUMNAR INSET AND ARE EITHER COMPACT AND DARK OR OEDEMATOUS
AND LIGHT !PICAL TIGHT JUNCTIONS AND LARGE DESMOSOMES OF THE JUNCTIONAL COMPLEXES ARE SEEN "UNDLES OF INTERMEDIATE
lLAMENTS CRISS
CROSS THE CELLS APPARENTLY CONVERGING ON THE DESMOSOMAL PLAQUES 4HE CYTOPLASM CONTAINS CONSPICUOUS
DENSE BODIES WITHOUT MEMBRANOUS DEMARCATION 8
)NSET 8
6)6)0!2)49
&IGURE #ONTINUED
" 4HE INTERNAL OVARIAN EPITHELIUM )/% OF A GRAVID OVARY BECOMES STRETCHED DUE TO SWELLING OF THE CONNECTIVE TISSUE THEREBY
CAUSING PROTRUSION OF CAPILLARIES # WHOSE ENDOTHELIUM IS SHOWN BETWEEN THE ARROWHEADS ,ARGE NUMBERS OF VESICLES AND
VACUOLES ARE SCATTERED THROUGHOUT THE CYTOPLASM OF THE EPITHELIAL CELL 8
# 4HE CYTOPLASM OF AN INTERNAL OVARIAN EPITHELIAL CELL FROM A GRAVID OVARY CONTAINS MANY INVAGINATED VACUOLES "UNDLES OF
INTERMEDIATE lLAMENTS CRISS
CROSS THE CELL "LEB
LIKE PROTRUSIONS BUD OFF FROM THE LUMINAL SURFACE 8
$ 3EVERAL LAMELLAE OF GRANULAR ENDOPLASMIC RETICULUM ARE SEEN IN THE CYTOPLASM OF THIS CELL FROM THE INTERNAL OVARIAN EPI
THELIUM %NDOCYTOTIC ACTIVITY IS VISIBLE AT THE BASAL PLASMA MEMBRANE ARROWS 4HE BASAL LAMINA IS HARDLY DISTINGUISHABLE
FROM THE GROUND SUBSTANCE OF THE UNDERLYING CONNECTIVE TISSUE 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS SHOWING JUNCTIONAL AND SUBEPITHELIAL FEATURES OF THE INTERNAL OVARIAN EPITHE
LIUM FROM GRAVID FEMALE GOODEIDS !LL ARE TAKEN FROM !LLOOPHORUS ROBUSTUS EXCEPT " WHICH IS FROM :OOGONETICUS QUITZEOENSIS
&ROM (OLLENBERG AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! (IGHLY INTERDIGITATED LATERAL CELL MEMBRANES BETWEEN ADJACENT CELLS 8
" $ESMOSOMES BETWEEN CELLS ARE UNUSUALLY PROMINENT WITH THICK ATTACHMENT PLAQUES ON THE CYTOPLASMIC SURFACES AND BUNDLES
OF INTERMEDIATE lLAMENTS EXTENDING INTO THE CYTOPLASM FROM THE PLAQUES 8
# !PICAL TIGHT JUNCTIONS ARE SOMETIMES ABSENT BETWEEN CELLS ,ATERAL MEMBRANES MAINTAIN A CONSTANT DISTANCE FROM ONE
ANOTHER WITHOUT FUSION OF THE OUTER LEAmETS 8
$ $ESMOSOME IMMEDIATELY ADJACENT TO THE OVARIAN LUMEN 8
% #OLLAGEN BUNDLES AND A lBROBLAST IN THE SUBEPITHELIAL SPACE 8
& #OLLAGEN lBRES EXHIBITING THEIR CHARACTERISTIC PERIODICITY 8
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF BUNDLES OF TONOlLAMENTS INTERMEDIATE lLAMENTS IN A SECTION OF BASAL
CYTOPLASM FROM A CELL OF THE INTERNAL OVARIAN EPITHELIUM OF A GRAVID FEMALE GOODEID TELEOST 'OODEA ATRIPINNIS 4ONOlLAMENTS
PERMEATE THE CYTOPLASM AT ALL LEVELS AND IN ALL ORIENTATIONS 8 &ROM (OLLENBERG AND 7OURMS REPRODUCED WITH
PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF AN INTERNAL OVARIAN EPITHELIAL CELL OF THE GOODEID 8ENOTOCA
EISENI AFTER INTRAOVARIAN EXPOSURE TO CATIONIZED FERRITIN FOR SIX HOURS ,ABELLING OF THE APICAL SURFACE OCCURS ONLY AT INTERVALS
)NTRACELLULAR LOCALIZATION OF THE TRACER IS MOST DENSE IN LARGE SOMEWHAT MULTIVESICULATED VACUOLES OF THE LYSOSOMAL APPARA
TUS 3OME TRACER IS SEQUESTERED IN RELATIVELY ELECTRON
LUCENT VESICLES ARROWHEADS #LUSTERS OF FERRITIN MOLECULES ARE PASSING
THE BASAL LAMINA ARROWS 8 &ROM 3CHINDLER REPRODUCED WITH PERMISSION
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF POSSIBLE APOCRINE SECRETION IN INTERNAL OVARIAN EPITHELIAL CELLS OF TWO
SPECIES OF GRAVID GOODEIDS &ROM (OLLENBERG AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE APICAL PORTION OF AN EPITHELIAL CELL FROM 'OODEA ATRIPINNIS CONTAINS LIPID DROPLETS AND A NUCLEUS .U ! LARGE BLEB
APPEARS TO BE ABOUT TO PINCH OFF FROM THE REST OF THE CELL ARROWHEADS TO BE RELEASED INTO THE OVARIAN LUMEN OL 8
" ! LONG NARROW CYTOPLASMIC EXTENSION FROM AN EPITHELIAL CELL OF :OOGONETICUS QUITZEOENSIS PROJECTS INTO THE OVARIAN LUMEN
4HE CELL JUNCTIONS ON THE LEFT AND RIGHT LATERAL MEMBRANES ARE UNUSUALLY CLOSE TO ONE ANOTHER SUGGESTING THAT THE EXTENDED
CYTOPLASM MAY SOON BE SLOUGHED 8
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE INTERNAL OVARIAN EPITHELIUM OF A GRAVID GOODEID 3KIFlA
BILINEATA 4HE EPITHELIUM OVERLYING A CAPILLARY IS ATTENUATED 8 &ROM 3CHINDLER AND +UJAT REPRODUCED WITH PER
MISSION
6)6)0!2)49
&IGURE $RAWINGS FROM THE DISSECTED GRAVID OVARY OF THE
JENYNSIID *ENYNSIA LINEATA WHERE EMBRYOS SUCKLE ON hNIPPLESv
FORMED FROM THE LUMINAL WALL ,ONG RICHLY VASCULAR BRANCH
ING FOLDS OF THE LUMINAL WALL FORM VILLI OVARIALES THAT GROW INTO
ONE OPERCULAR CLEFT OF THE EMBRYO ESTABLISHING CONTACT BETWEEN
MATERNAL NUTRITIVE TISSUE AND THE EMBRYONIC DIGESTIVE TRACT &ROM
4URNER D REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
! !N EMBRYO IN LATE GESTATION ATTACHED TO A VILLUS OVARIALIS
4HE OVARIAN TISSUE EXTENDS THROUGH THE OPERCULAR OPENING
INTO THE PHARYNGEAL CAVITY AND A SMALL PORTION PROTRUDES FROM
THE MOUTH
" !N EMBRYO IN LATE GESTATION TO ILLUSTRATE AN OPEN OPERCULAR
CLEFT
!BBREVIATIONS /0/ OPERCULAR OPENING /64 OVARIAN TISSUE
&IGURE 0HOTOMICROGRAPHS OF SEMI
THIN SECTIONS OF VILLI OVARIALES FROM THE JENYN
SIID *ENYNSIA LINEATA &ROM 3CHINDLER AND DE
6RIES B REPRODUCED WITH PERMISSION
OF *OHN 7ILEY 3ONS )NC
! #ROSS SECTION AT THE TIP OF A VILLUS 4WO
INTRAVILLOUS SEPTA ARROWHEADS SUBDIVIDE
THE CORE OF THE VILLUS INTO LOCULI 4HE mAT
INTRAOVARIAN EPITHELIUM
IS UNDERLAIN BY
A NARROW BAND OF CONNECTIVE TISSUE CARRY
ING CAPILLARIES ARROWS 8
" !N OBLIQUE SECTION OF A VILLUS OVARIALIS
8
# ! VILLUS OVARIALIS 6/ EXTENDS FROM THE
OVARIAN WALL /7 INTO THE OVARIAN LUMEN
/, 4HE OVARIAN WALL CONTAINS A BLOOD
VESSEL "6 AND A NERVE ARROW LOCULI
PERMEATE THE LOOSE CONNECTIVE TISSUE OF
THE VILLUS 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF EPITHELIAL CELLS ON VILLI OVARIALES FROM THE JENYNSIID *ENYNSIA LINEATA
&ROM 3CHINDLER AND DE 6RIES B REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! %NDOCYTOTIC ACTIVITY IS INDICATED BY NUMEROUS ELEMENTS OF A VACUOLAR COMPLEX INCLUDING COATED VESICLES ARROWHEADS
CUP
SHAPED VACUOLES ARROWS AND A 'OLGI COMPLEX 8
" 4HE GAP BETWEEN INTRAOVARIAN EPITHELIAL CELLS ALLOWS TRANSEPITHELIAL PASSAGE OF COARSE MATERIAL
%NDOCYTOTIC ACTIVITY
ARROWHEAD IS EVIDENT AT THE SURFACE OF THE OVARIAN LUMEN /, 8
# -OST ADJACENT CELLS OF THE INTRAOVARIAN EPITHELIUM INTERDIGITATE 8
6)6)0!2)49
&IGURE 0HOTOGRAPHS OF LATE TERM EMBRYOS OF VARIOUS SPECIES OF GOODEID lSHES 2IBBON AND ROSETTE TROPHOTAENIAE EXTEND
FROM PERIANAL LIPS 4OP !LLOOPHORUS ROBUSTUS MIDDLE LEFT :OOGONETICUS QUITZEOENSIS THE SMALLEST GOODEID SPECIES BOTTOM
LEFT 'OODEA ATRIPINNIS BOTTOM RIGHT )LYODON FURCIDENS 8 &ROM (OLLENBERG AND 7OURMS REPRODUCED WITH PERMIS
SION OF *OHN 7ILEY 3ONS )NC
&IGURE $RAWING OF A RECONSTRUCTION OF THE ABSORP
TIVE PROCESSES AND ADJACENT PARTS OF AN EMBRYO OF A ZOAR
CID lSH 0ARABROTULA DENTIENS 8 &ROM 4URNER
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
!BBREVIATIONS !. ANUS !02 ABSORPTIVE PROCESSES 50
URINARY PORE
#(!04%2
&IGURE $EPICTIONS OF TROPHOTAENIAE IN THE GOO
DEID !MECA SPLENDENS &ROM ,OMBARDI AND 7OURMS
B REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
! 0HOTOMICROGRAPH OF A WHOLE MOUNT OF A MIDTERM
EMBRYO SHOWING WELL DEVELOPED HIGHLY VASCU
LARIZED TROPHOTAENIAE TR EXTENDING FROM THE ANAL
REGION AN 8
" 0HOTOMICROGRAPH OF A GLYCERINATED PREPARATION OF
A TROPHOTAENIAL RIBBON FROM A MIDTERM EMBRYO
%LEMENTS OF THE VASCULAR SUPPLY ARE VISIBLE WITH
IN THE CONNECTIVE TISSUE CORE LARGE VESSELS ARE
ORIENTED PARALLEL TO THE TROPHOTAENIAL AXIS WHILE
CAPILLARIES FORM A VASCULAR BED BENEATH THE OUTER
EPITHELIUM 8
# 3CANNING ELECTRON MICROGRAPH OF A CRYOFRACTURED
PREPARATION REVEALING THE INTERNAL STRUCTURE OF
THE CAUDAL TROPHOTAENIAL RIBBON .UMEROUS BLOOD
VESSELS LIE WITHIN THE CONNECTIVE TISSUE CORE TE
TROPHOTAENIAL EPITHELIUM 8
$ 3CANNING ELECTRON MICROGRAPH OF THE APICAL SURFACE
OF A TYPICAL CELL IN THE TROPHOTAENIAL EPITHELIUM
#ELLS POSSESS A DENSE MAT OF APICAL MICROVILLI
8
% $ETAIL OF THE PREPARATION IN &IGURE # 0ERIPHERAL
CAPILLARIES ARROWS LIE BENEATH THE SURFACE EPI
THELIUM TE 4ROPHOTAENIAL ARTERIES TA AND VEINS
TV ARE EMBEDDED WITHIN THE CONNECTIVE TISSUE
CORE &IBROBLASTS AND A lBROUS EXTRACELLULAR MATRIX
ARE PRESENT WITHIN THE CONNECTIVE TISSUE CORE CT
8
& 3CHEMATIC REPRESENTATION OF TISSUE ORGANIZATION IN
THE TROPHOTAENIAL PLACENTA 3OME REGIONS OF THE TRO
PHOTAENIAL RIBBONS SEEN HERE IN CROSS SECTION 42
LIE IN DIRECT APPOSITION TO THE INTERNAL OVARIAN EPI
THELIUM /6 LINING THE OVARIAN LUMEN
4HE SIX BARRIERS TO THE TRANSFER OF MATERIALS FROM MA
TERNAL TO THE EMBRYONIC BLOODSTREAM ARE SHOWN IN
THE UPPER RIGHT ENDOTHELIAL LINING OF CAPILLAR
IES WITHIN THE OVARIAN CONNECTIVE TISSUE STROMA
OVARIAN CONNECTIVE TISSUE STROMA INTERNAL OVARIAN
EPITHELIUM TROPHOTAENIAL EPITHELIUM TROPHOTAE
NIAL CONNECTIVE TISSUE CORE ENDOTHELIUM OF TROPHO
TAENIAL CAPILLARIES
6)6)0!2)49
&IGURE 0HOTOMICROGRAPHS OF SEMITHIN SECTIONS OF TROPHOTAENIAE OF THE GOODEID 8ENOOPHORUS CAPTIVUS &ROM 3CHINDLER
AND DE 6RIES B REPRODUCED WITH PERMISSION OF THE AUTHORS
! +IDNEY
SHAPED CROSS SECTION OF A TROPHOTAENIA )TS CORE CONSISTS OF LOOSE MESENCHYMAL CONNECTIVE TISSUE CONTAINING THIN
WALLED BLOOD VESSELS ARROWS AND A CAPILLARY PLEXUS ARROWHEADS BENEATH THE EPITHELIUM 4HE CIRCLE INDICATES A SMALL
SEGMENT OF STRATIlED EPITHELIUM 8
" 4ROPHOTAENIAL EPITHELIUM SHOWING CLOSELY APPOSED ABSORPTIVE CELLS ) AND THOSE ISOLATED BY LARGE INTERCELLULAR SPACES ))
$ENSELY STAINED BASAL CELLS ARROWS UNDERLIE MOST OF THE ABSORPTIVE EPITHELIUM 8
# 3EGMENT OF BILAYERED SQUAMOUS EPITHELIUM BETWEEN ARROWHEADS )TS LEVEL IS SLIGHTLY RECESSED BELOW THE SURFACE OF
THE BORDERING ABSORPTIVE CELLS 8
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS TO ILLUSTRATE THE MOSAIC OF ABSORPTIVE CELLS AND PAVEMENT CELLS ON THE SURFACE
OF TROPHOTAENIA FROM NEAR
TERM EMBRYOS OF THE GOODEID 'IRARDINICHTHYS VIVIPARUS &ROM 3CHINDLER AND DE 6RIES A
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE ISLAND OF PAVEMENT CELLS AT THE CENTRE IS DISTINGUISHED BY THE lNGERPRINT PATTERN OF MICRORIDGES ON THE SURFACE OF
INDIVIDUAL CELLS WHOSE BOUNDARIES ARE WELL DElNED &ORESTS OF MICROVILLI COVER THE SURFACES OF THE SURROUNDING ABSORPTIVE
CELLS 8
" 2IDGED PAVEMENT CELLS NESTLE SINGLY AND AS CLUSTERS AMONG THE ABSORPTIVE CELLS WHOSE SURFACE IS STUDDED WITH MICROVILLI
8
6)6)0!2)49
&IGURE -ICROGRAPHS OF SECTIONS OF TROPHOTAENIAE OF THE GOODEID 3KIFlA BILINEATA TO SHOW THE DISTRIBUTION OF CAPILLARIES
! TO # ARE PHOTOMICROGRAPHS $ AND % ARE TRANSMISSION ELECTRON MICROGRAPHS &ROM 3CHINDLER AND +UJAT REPRODUCED
WITH PERMISSION
! #ROSS SECTION THROUGH THE MIDDLE OF A TROPHOTAENIA 4HE CORE IS lLLED WITH LOOSE MESENCHYMAL CONNECTIVE TISSUE CONTAIN
ING A FEW SINUSOIDAL BLOOD VESSELS 4HE EXTERNAL EPITHELIUM IS THIN AND CLOSELY UNDERLAIN BY A CAPILLARY NETWORK ARROWS
8
" $ISTAL CROSS SECTION OF A TROPHOTAENIA 8
# 4HE CONNECTIVE TISSUE CORE AT THE TROPHOTAENIAL TIP IS RELATIVELY DENSE AND CONTAINS SEVERAL WANDERING CELLS 4HE EXTERNAL
EPITHELIUM IS COMPOSED OF TALLER CELLS AT THIS LOCATION -ANY CELLS APPEAR TO BE DEGENERATING AND SLOUGHING OFF 8
$ 4HIS SEGMENT OF SQUAMOUS EXTERNAL TROPHOTAENIAL EPITHELIUM IS UNDERLAIN BY A CAPILLARY # 4HE MONOLAYER OF ABSORPTIVE
CELLS PARTLY RESTS ON mAT BASAL CELLS
8
% 4ROPHOTAENIAL EPITHELIUM IS COMPOSED OF TROPHOTAENIAL ABSORPTIVE CELLS 4!# WITH SPARSELY SPACED MICROVILLI AND
UNDERLYING BASAL CELLS "# RESTING ON THE BASEMENT LAMINA $EEP CHANNELS
BETWEEN THE ABSORPTIVE CELLS ARE OPEN TO
THE INTERCELLULAR SPACE )#3 "ASAL CELLS LACK INVAGINATIONS OF THEIR MEMBRANES 8
#(!04%2
B
A
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH TROPHOTAENIAL ABSORPTIVE CELLS IN A NEAR
TERM EMBRYO
GOODEID 'IRARDINICHTHYS VIVIPARUS &ROM 3CHINDLER AND DE 6RIES A REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
! -ICROPINOCYTOTIC ACTIVITY IS EVIDENT IN THE BASAL REGION OF AN ABSORPTIVE CELL 4HE CELL RESTS ON A BASAL LAMINA "- AND
IS UNDERLAIN BY A FENESTRATED ARROWHEADS CAPILLARY # ! COATED VESICLE #6 IS IN CONTACT WITH THE BASAL PLASMALEMMA
! MITOCHONDRION - IS ENCIRCLED BY AN OPEN BILAYERED MEMBRANOUS ANNULUS &REE RIBOSOMES 2 AND THE A PORTION OF THE
NUCLEUS . ARE SHOWN 8
" !BUNDANT MITOCHONDRIA ARE PACKED IN THE APICAL CYTOPLASM OF THIS ABSORPTIVE CELL IMMEDIATELY BENEATH THE BRUSH BORDER
AND A NARROW BAND CONTAINING ONLY SMALL VESICLES 4HE INDENTED SPHERICAL NUCLEUS . OCCUPIES THE BASAL PART OF THE CELL
!DJACENT CELLS ARE SEPARATED BY BULGES OF THE INTERCELLULAR SPACE )#3 -EMBRANOUS LAMELLAE TRAVERSE THE CYTOPLASM
0ERIPHERAL SMOOTH MEMBRANES ARROWHEADS RESEMBLE THE PLASMALEMMA RATHER THAN ENDOPLASMIC RETICULUM 8
# ! STRATIlED PAVEMENT EPITHELIUM FORMS IRREGULAR ISLANDS OF RIDGED CELLS BETWEEN THE ABSORPTIVE CELLS 4HIS IS A PORTION
OF A CELL OF THE COVERING STRATUM OF THE MULTILAYERED EPITHELIUM "ELOW THE PERIPHERAL lBRILLAR ZONE THE CYTOPLASM CON
TAINS ABUNDANT MOSTLY AGRANULAR SLIGHTLY DISTENDED ERGASTOPLASMIC MEMBRANES ELONGATED IN PARALLEL WITH THE CELL SURFACE
.UMEROUS SMALL VESICLES APPEAR TO BE PINCHED OFF FROM THE CONSPICUOUS 'OLGI COMPLEX ' ! SLENDER CELLULAR PROCESS
BRIDGES THE EXPANDED INTERCELLULAR SPACE )#3 TO THE UNDERLYING STRATUM 8
6)6)0!2)49
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH TWO TYPES OF TROPHOTAENIAL EPITHELIAL CELLS FROM THE
GOODEID 8ENOOPHORUS CAPTIVUS "ASAL CELLS HAVE ELECTRON
DENSE CYTOPLASM AND LIE ON THE PARTLY SPLIT BASAL LAMINA ARROWS
4HE OVERLYING ABSORPTIVE CELLS SHOW AN APICAL MICROVILLOUS BORDER APICOLATERAL JUNCTIONAL COMPLEXES AND DESMOSOMES BE
TWEEN ADJACENT CELLS ! SYSTEM OF OPEN LAMELLAR MEMBRANES ARROWHEADS PARALLELS THE LATERAL PLASMA MEMBRANES 4HE ABSORP
TIVE CELLS EXHIBIT CYTOPLASMIC ZONATION :ONE ) THE ENDOCYTIC APICAL ZONE COMPRISES THE EXPOSED PLASMA MEMBRANES INCLUDING
BOTH THE MICROVILLI AND THE INVAGINATIONS OF THE SURFACE VESICLES AND VACUOLES AND AN OSMIOPHILIC TUBULAR SYSTEM :ONE ))
THE SUPRANUCLEAR ZONE IS DOMINATED BY MITOCHONDRIA AND FREQUENTLY BY LARGE ELECTRON
OPAQUE BODIES :ONE ))) THE NUCLEAR
ZONE USUALLY HAS A 'OLGI COMPLEX ' LOCATED BASOLATERAL TO THE NUCLEUS :ONE )6 THE BASAL ZONE BECOMES INCREASINGLY DEVOID
OF ORGANELLES AS GESTATION PROGRESSES AND MAY BE REDUCED TO CYTOPLASMIC PROCESSES PENETRATING THE UNDERLYING BASAL CELLS
8 &ROM 3CHINDLER AND DE 6RIES B REPRODUCED WITH PERMISSION OF THE AUTHORS
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF SECTIONS THROUGH TROPHOTAENIAL EPITHELIAL CELLS FROM THE GOODEID
!MECA SPLENDENS &ROM ,OMBARDI AND 7OURMS B REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !N ABSORPTIVE CELL UNDERLAIN BY A SQUAMOUS BASAL CELL &OUR AREAS OF CYTOPLASMIC ZONATION CAN BE RECOGNIZED IN THE AB
SORPTIVE CELL :ONE APICAL SURFACE ZONE :ONE APICAL CORTICAL ZONE ENDOCYTOTIC COMPLEX :ONE SUPRANUCLEAR
ZONE CONTAINING LARGE MEMBRANOUS INCLUSIONS AND MITOCHONDRIA AND :ONE THE NUCLEAR
SUBNUCLEAR ZONE !GRANULAR AND
GRANULAR ENDOPLASMIC RETICULUM OCCUPIES THE PARANUCLEAR REGION 4HE 'OLGI COMPLEX LIES IN A LATERAL OR BASAL POSITION
4HE SQUAMOUS BASAL CELLS POSSESS ELECTRON
LUCENT CYTOPLASM ARROW 4HE EPITHELIAL CELLS ARE SEPARATED FROM A CAPILLARY CA
BY A DELICATE BASAL LAMINA 8
" !PICAL REGION OF AN ABSORPTIVE CELL -ICROVILLI MV EXTEND FROM HE CONVOLUTED CELL SURFACE 4HE OUTER LEAmET OF THE PLASMA
LEMMA IS COATED WITH A lNE lBRILLAR MATERIAL 4HE APICAL CANALICULAR SYSTEM AC CONTAINS TUBULAR PROlLES ARROW ASSOCIATED
WITH COLLECTING VESICLES -ITOCHONDRIA MI OF THE SUPRANUCLEAR ZONE ARE NUMEROUS AND SITUATED ADJACENT TO THE NUCLEUS NU
AV APICAL VESICLE 8
# 4HE LATERAL CYTOPLASM OF ADJACENT ABSORPTIVE CELLS CONTAINS THE TUBULAR CISTERNAL COMPLEX ARROWS AND ELEMENTS OF
THE GRANULAR ENDOPLASMIC RETICULUM GER LP LATERAL PLASMALEMMA NU NUCLEUS 8
$ 4HE SUBNUCLEAR REGION OF AN ABSORPTIVE CELL CONTAINS NUMEROUS DENSE INCLUSIONS AND A WELL DEVELOPED 'OLGI COMPLEX GO
)NVAGINATIONS OF THE LATERAL CELL SURFACES FORM ELEMENTS OF THE TUBULAR CISTERNAL COMPLEX ARROW 4HE CELLS REST ON A BASAL
LAMINA BL DI DENSE INCLUSION 8
#(!04%2
&IGURE $IAGRAMS TO ILLUSTRATE TWO MORPHOLOGICALLY DISTINCT SPECIES SPECIlC LINES OF TROPHOTAENIAL ABSORPTIVE CELLS IN
THE GOODEIDS 'IRARDINICHTHYS VIVIPARUS AND 8ENOTOCA EISENI BASED ON THE PRESENCE OR ABSENCE OF A TYPICAL ENDOCYTOTIC APPA
RATUS AND THE UPTAKE OF CATIONIZED FERRITIN #& OR HORSERADISH PEROXIDASE (20 -ULTIVALENT #& HAS AN AFlNITY FOR THE TIPS OF
THE MICROVILLI AND IT ADHERES TO THE EXTERNAL PLASMALEMMAL LEAmET OF THE APICAL SACCULAR MEMBRANE INVAGINATIONS 3) OF THE
ABSORPTIVE CELLS IN ' VIVIPARUS )NTERNALIZED #& IS ACCUMULATED IN STORAGE VACUOLES 36 OR MULTIVESICULAR BODIES -6"
-OST OF THE ENDOCYTOSED #& IN ' VIVIPARUS BUT ONLY SOME #& CONTAINING VESICLES IN 8 EISENI ARE TRANSPORTED ACROSS THE TRO
PHOTAENIAL ABSORPTIVE CELLS PAST THE NUCLEUS . AND ARE EXOCYTOSED AT THE BASOLATERAL PLASMA MEMBRANES 2EACTION PRODUCT
OF (20 IS ACCUMULATED IN THE MULTIVESICULAR BODIES LOCATED IN THE APICAL CYTOPLASM OF THE ABSORPTIVE CELLS IN ' VIVIPARUS
)N 8 EISENI THE REACTION PRODUCT OF (20 PARTLY lLLS LARGE STORAGE VACUOLES THE APICAL DENSE CYTOPLASMIC TUBULES #4 AND
THE LATERAL LAMELLAR MEMBRANE COMPLEX ,-# 4HE BORDERS OF ADJACENT CELLS ARE SEALED APICALLY BY TIGHT JUNCTIONS 4*
&ROM 3CHINDLER AND DE 6RIES A REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
6)6)0!2)49
&IGURE $IAGRAMMATIC REPRESENTATIONS OF TROPHOTAENIAL ABSORPTIVE CELLS IN TWO SPECIES OF GOODEID lSHES &ROM +OKKALA
AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE ABSORPTIVE CELLS IN !MECA SPLENDENS ARE SPECIALIZED FOR THE ENDOCYTOSIS OF MACROMOLECULES AND CAN ALSO TRANSPORT SMALL
MOLECULES 4HE CELLS HAVE AN APICAL BRUSH BORDER OF MICROVILLI 4HE APICAL CYTOPLASM CONTAINS SMOOTH
SURFACED INVAGINA
TIONS OF THE PLASMALEMMA ! AND ASSOCIATED VESICLES AS WELL AS CLATHRIN
COATED PITS AND VESICLES 4UBULAR 4 AND SPHERICAL
3 ENDOSOMES ARE PRESENT 4HE REGION SUPERIOR TO THE NUCLEUS CONTAINS AN ARRAY OF ENDOSOMAL
LYSOSOMAL 0 6 COMPO
NENTS -ITOCHONDRIA - OCCUR BOTH ABOVE AND BELOW THE NUCLEUS $EEP INFOLDINGS ) OF THE BASAL PLASMALEMMA ARE SEEN
% ENDOPLASMIC RETICULUM ' 'OLGI COMPLEX
#(!04%2
&IGURE #ONTINUED
" 4HE CUBOIDAL EPITHELIAL CELLS IN 'OODEA ATRIPINNIS ARE SPECIALIZED FOR THE TRANSPORT OF SMALL MOLECULES AND DO NOT ENDOCY
TOSE LARGE MOLECULES THESE CELLS LACK AN ENDOCYTIC COMPLEX 2EGULARLY SPACED MICROVILLI ARE SUBTENDED BY A WIDE TERMINAL
WEB 4 "OTH APICAL AND BASAL MITOCHONDRIA - ARE ASSOCIATED WITH SMOOTH ENDOPLASMIC RETICULUM %N ! BASAL 'OLGI
COMPLEX ' IS SHOWN /NLY MODEST INFOLDINGS ) OF THE BASAL PLASMALEMMA ARE SHOWN 4HE CELL IS SEPARATED FROM A CAPIL
LARY # BY A THIN BASAL LAMINA "
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH OF TROPHOTAENIAL ABSORPTIVE CELLS IN THE GOODEID
8ENOOPHORUS CAPTIVUS &ROM 3CHINDLER AND DE 6RIES B REPRODUCED WITH PERMISSION OF THE AUTHORS
! 4UBULAR AND SACCULAR INVAGINATIONS ARE NUMEROUS IN THE ENDOCYTIC APICAL ZONE $EEPER IN THE CYTOPLASM ARE ABUNDANT
VESICLES VACUOLES AND DENSE TUBULAR PROlLES 4HE VACUOLAR MEMBRANES ARE OFTEN INVAGINATED ON ONE SIDE GIVING RISE TO
CRESCENT
SHAPED STRUCTURES ARROWHEADS 3OME PROlLES INDICATE EITHER FUSION OR PINCHING OFF OF TUBULES OR VESICLES FROM
LARGER VACUOLES ARROWS ! PAVEMENT CELL 0# OF THE STRATIlED EPITHELIAL COMPONENT IS SHOWN AT THE RIGHT 8
" 4WO TYPES OF TROPHOTAENIAL EPITHELIAL CELLS ARE SHOWN ABSORPTIVE CELLS WITH A MICROVILLOUS BORDER OVERLIE BASAL CELLS
WITH AN ELECTRON
DENSE CYTOPLASM :ONATION OF THE ABSORPTIVE CELLS IS SHOWN BY 2OMAN NUMERALS FROM THE APICAL ENDOCYTIC
ZONE ) SUPRANUCLEAR ZONE )) NUCLEAR ZONE ))) TO THE BASAL ZONE )6 4HE BASAL ZONE CONTAINS TWO LARGE VACUOLES 6
OF mOCCULENT MATERIAL 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF FREEZE
FRACTURE REPLICAS OF THE ABSORPTIVE EPITHELIUM COVERING EM
BRYONIC TROPHOTAENIAE IN THE GOODEID 8ENOTOCA EISENI &ROM 3CHINDLER AND DE 6RIES REPRODUCED WITH PERMISSION OF
3PRINGER
6ERLAG
! 3URVEY VIEW OF THE APICAL REGION OF A TROPHOTAENIAL ABSORPTIVE CELL 4HE FRACTURE PLANE PASSES VERTICALLY THROUGH THE SUPRA
NUCLEAR CYTOPLASM REVEALING THE STRUCTURAL COMPLEXITY OF THE ENDOCYTIC COMPLEX THAT OCCUPIES A BROAD CORTICAL ZONE BELOW
THE MICROVILLAR BORDER 3EVERAL MITOCHONDRIA - OCCUR IN THE DEEPER CYTOPLASM $ISTENDED INTRAEPITHELIAL SPACES
COM
PRESS THE MIDDLE OF THE CELLS 4HE LATERAL PLASMA MEMBRANE IS UNDERLAIN BY A LAMELLAR MEMBRANE COMPLEX ARROWHEADS
8
6)6)0!2)49
&IGURE #ONTINUED
" 4HIS MICROGRAPH PRIMARILY ILLUSTRATES THE 0
FACE APPEARANCE OF THE APICAL SURFACE OF A TROPHOTAENIAL ABSORPTIVE CELL
$EEP INVAGINATIONS HONEYCOMB THE SUBSURFACE CYTOPLASMIC MATRIX ALONG WITH LARGE NUMBERS OF SMALL VESICLES AND TUBULES
4HE DENSITY OF INTRAMEMBRANOUS PARTICLES IS GREATEST ON THE 0
FACES OF THE MICROVILLI 4HE CONTINUATION OF THEIR MEMBRANE
ON THE INTERMICROVILLOUS CELL SURFACE AND BEYOND INTO THE INVAGINATIONS SHOW REDUCED NUMBERS OF PARTICLES AND IT WOULD AP
PEAR THAT VOLUMINOUS INTEGRAL MEMBRANE PROTEINS GAIN ACCESS TO ENDOCYTIC PITS ARROWS ONLY IN SMALL QUANTITIES 8
# 2EPLICA OF THE MEMBRANE OF THE MICROVILLOUS AND INTERMICROVILLOUS REGIONS OF AN ABSORPTIVE CELL 4HE INVAGINATED SURFACE
ILLUSTRATES THE DISTRIBUTION OF INTRAMEMBRANOUS PARTICLES IN THE %
FACE "ESIDES PARTICLE
FREE AREAS ONLY A FEW RANDOMLY
SCATTERED PARTICLES ARE PRESENT 8
#(!04%2
&IGURE #ONTINUED
$ 4HE IMMEDIATE SUBSURFACE CYTOPLASM CONTAINS AN ABUNDANCE OF SMALL VESICULAR AND TUBULAR STRUCTURES 4HEIR 0
FACES
REGULARLY SHOW A FEW ODD MEMBRANE
ASSOCIATED PARTICLES WHEREAS THE CORRESPONDING %
FACES
ARE ALMOST DEVOID OF
INTRAMEMBRANOUS PARTICLES "OTH ENDS OF AN APICAL TUBULE SHOW BULBOUS DISTENSIONS ARROWHEADS INDICATING EITHER FUSION
WITH OR DETACHMENT OF VESICLES 8
% 4HIS REPLICA SHOWS THE 0
FACE OF AN ENDOSOME WITHIN THE APICAL ENDOCYTIC ZONE 3EVERAL INTRAMEMBRANOUS PARTICLES CLUSTER
IN SOME MEMBRANE AREAS CIRCLES 8
& 4HE ARROW INDICATES THE CONNECTION BETWEEN AN ENDOSOME AND AN APICAL TUBULE )NTRAMEMBRANOUS PARTICLES ARE CLUSTERED ON
THE 0
FACE 8
' 4HIS LARGE ENDOSOME IS CONNECTED TO AN APICAL TUBULE ARROW 3MALL PITS ARROWHEADS IN THE 0
FACE INDICATE THE PRESENCE
OF FURTHER CONNECTIONS WITHIN TUBULES 8
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE APICAL PORTION OF A TROPHOTAENIAL ABSORPTIVE CELL OF
THE GOODEID 8ENOOPHORUS CAPTIVUS AFTER EXPOSURE TO HORSERADISH PEROXIDASE AND CATIONIZED FERRITIN FOR ONE HOUR (20
REACTION
PRODUCT IS ENRICHED WITHIN SOME VACUOLES IN THE DEEPER PARTS OF THE APICAL ENDOCYTIC COMPLEX /THER VACUOLES ALMOST EXCLU
SIVELY CONTAIN #& LIGHT ARROWS 3URFACE INVAGINATIONS ANDOR PINOCYTIC VESICLES ARROWS ARE lLLED WITH #&
AGGLOMERATES
/THER VESICLES OF THE SAME SIZE ARE DOUBLE
LABELLED ARROWHEADS #&
MOLECULES ARE PRESENT IN MOST APICAL TUBULES
8 &ROM 3CHINDLER AND DE 6RIES A REPRODUCED WITH PERMISSION OF THE AUTHORS
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE APICAL REGIONS OF TROPHOTAENIAL ABSORPTIVE CELLS
OF THE GOODEID !MECA SPLENDENS lXED AFTER A PERIOD OF CONTINUOUS EXPOSURE TO HORSERADISH PEROXIDASE &ROM ,OMBARDI AND
7OURMS C REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! !FTER MINUTES EXPOSURE REACTION PRODUCT IS PRESENT WITHIN A FEW APICAL VESICLES AND ELEMENTS OF THE APICAL CANALICULAR
SYSTEM ARROWS 8
" !FTER MINUTES EXPOSURE UPTAKE OCCURS BY WAY OF ENDOCYTOSIS OF THE APICAL PLASMA MEMBRANE ARROWS 2EACTION PROD
UCT IS PRESENT WITHIN APICAL CANALICULI AND COLLECTING VESICLES ,ARGE SUPRANUCLEAR LYSOSOMES SITUATED ABOVE THE NUCLEUS
SHOW NO PEROXIDASE ACTIVITY 8
# !FTER MINUTES EXPOSURE THE REACTION PRODUCT IS PRESENT WITHIN APICAL CANALICULI COLLECTING VESICLES AND LARGE SUPRA
NUCLEAR VESICLES 8
6)6)0!2)49
&IGURE #ONTINUED
$ !FTER MINUTES THE REACTION PRODUCT IS PRESENT WITHIN THE APICAL CANALICULAR SYSTEM COLLECTING VESICLES AND ENLARGED
SUPRANUCLEAR LYSOSOMES 8
% !N ENTIRE ABSORPTIVE CELL IS SHOWN AFTER ONE HOURS EXPOSURE 4HE REACTION PRODUCT IS PRESENT WITHIN APICAL CANALICULI
COLLECTING VESICLES AND GREATLY ENLARGED SUPRANUCLEAR LYSOSOMES #OLLECTING VESICLES FUSE WITH SUPRANUCLEAR VESICLES
ARROW 2ESIDUAL BODIES CONTAINING mOCCULENT MATERIAL ARE PRESENT 0EROXIDASE ACTIVITY IS ALMOST EXCLUSIVELY LOCALIZED IN
THE SUPRANUCLEAR REGION OF THE CELL %XOGENOUS PEROXIDASE ACTIVITY IS NOT DETECTED WITHIN THE TROPHOTAENIAL CONNECTIVE TISSUE
OR VASCULAR ELEMENTS 8
!BBREVIATIONS AC APICAL CANALICULI BL BASAL LAMINA CA CAPILLARY CV COLLECTING VESICLES IS INTERCELLULAR SPACE MV MICRO
VILLI NU NUCLEUS RB RESIDUAL BODY SV SUPRANUCLEAR VESICLES
#(!04%2
&IGURE $IAGRAMMATIC SUMMARY OF THE PROPOSED
PATHWAY BY WHICH PROTEINS ARE TRANSFERRED ACROSS THE TRO
PHOTAENIAL PLACENTA IN THE GOODEID !MECA SPLENDENS
! THE SYNTHESIS AND RELEASE OF PROTEIN CONTAINING SECRETIONS
BY CELLS OF THE INTERNAL OVARIAN EPITHELIUM " UPTAKE OF OVAR
IAN SECRETIONS BY THE TROPHOTAENIAL EPITHELIUM BY ENDOCYTO
SIS # TRANSFER AND PASSAGE OF PROTEIN COMPONENTS THROUGH
THE APICAL CANALICULAR SYSTEM AND ITS PROGRESSIVE ACCUMULA
TION IN COLLECTING VESICLES $ FUSION OF COLLECTING VESICLES
WITH STANDING SUPRANUCLEAR SECONDARY LYSOSOMES % GROWTH
OF STANDING LYSOSOMES BY ACCRETION OF COLLECTING VESICLES
ANDOR OTHER LYSOSOMES & ENZYMATIC HYDROLYSIS OF PROTEINS
WITHIN STANDING LYSOSOMES ' DISCHARGE OF THE PRODUCTS OF
PROTEIN HYDROLYSIS AMINO ACIDS AND PEPTIDES VIA LATERAL
AND BASAL CELL SURFACES ( PASSAGE OF COMPONENTS OF LOW
MOLECULAR WEIGHT ACROSS THE BASAL MATRIX AND CONNEC
TIVE TISSUE CORE AND THEIR ENTRY INTO THE EMBRYONIC VASCU
LAR SYSTEM BY TRANSPORT ACROSS THE CAPILLARY ENDOTHELIUM
&ROM ,OMBARDI AND 7OURMS C REPRODUCED WITH
PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH TWO TROPHOTAENIAL ABSORPTIVE CELLS OVERLYING A BASAL CELL
IN THE TROPHOTAENIAL EPITHELIUM OF THE GOODEID 8ENOOPHORUS CAPTIVUS FOLLOWING EXPOSURE TO HORSERADISH PEROXIDASE ! SYSTEM
OF INTERCELLULAR SPACES CONTINUOUS WITH THE INFOLDINGS OF THE BASOLATERAL MEMBRANES OF THE ABSORPTIVE CELLS EXTENDS BETWEEN
THE ABSORPTIVE AND BASAL CELLS &ROM 3CHINDLER AND DE 6RIES A REPRODUCED WITH PERMISSION OF THE AUTHORS
!BBREVIATIONS !%# APICAL ENDOCYTIC COMPLEX "# BASAL CELL 4!# TROPHOTAENIAL ABSORPTIVE CELL 36 SUPRANUCLEAR VACUOLE
8
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A
SECTION THROUGH THE STRATIlED TROPHOTAENIAL EPITHELIUM
OF THE GOODEID 8ENOOPHORUS CAPTIVUS 4HE OVARIAN LU
MEN /, IS SHOWN AT THE TOP (UGE INTERCELLULAR SPACES
)#3 HAVE APPEARED BETWEEN THE STRATIlED PAVEMENT CELLS
!DJOINING CELLS ARE CONNECTED BY CYTOPLASMIC PROCESSES
4HE ARROW INDICATES INTERDIGITATIONS BETWEEN ADJACENT CELLS
4HE EPITHELIUM IS SEPARATED FROM LOOSE SUBEPITHELIAL CON
NECTIVE TISSUE BY A DELICATE BASAL LAMINA ", 8
&ROM 3CHINDLER AND DE 6RIES B REPRODUCED WITH
PERMISSION OF THE AUTHORS
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS SHOWING PROGRESSIVE DISTENSION OF THE INTERCELLULAR SPACES IN THE TROPHO
TAENIAL ABSORPTIVE EPITHELIUM OF A GOODEID h#HARACODONv EISENI &ROM -ENDOZA REPRODUCED WITH PERMISSION OF
*OHN 7ILEY 3ONS )NC
! 4HE TROPHOTAENIAL EPITHELIUM AT AN EARLY STAGE OF ITS CELL CYCLE )NTERCELLULAR SPACES ARE SLIGHTLY DISTENDED .OTE THE STRATIlCA
TION OF ORGANELLES 8
#(!04%2
&IGURE #ONTINUED
" ! REGION OF THE EPITHELIUM WITH WELL DEVELOPED INTERCELLULAR SPACES ! BLOOD VESSEL IS CLOSELY APPOSED TO THE BASAL LAMINA
OF THE EPITHELIUM 8
# 4HE EPITHELIAL CELLS ARE EXTREMELY DISTORTED BY THE ENLARGED INTERCELLULAR SPACES %PITHELIAL CONTACT WITH THE BASAL LAMINA
IS MINIMAL 4HE TIGHT JUNCTION CONTINUES TO SEAL THE APICAL SURFACE 8
!BBREVIATIONS ", BASAL LAMINA "6 BLOOD VESSEL #% CELLULAR EXTENSIONS %6 VESICLE OF THE ENDOPLASMIC RETICULUM
)3 INTERCELLULAR SPACE -/ hMOTTLED VESICLEv -6 MICROVILLI . NUCLEUS 4* TIGHT JUNCTION
6)6)0!2)49
&IGURE )NTERCELLULAR SPACES IN THE TROPHOTAENIAL EPITHELIUM MAY HAVE AN EXCRETORY ROLE IN STORING WASTES OR PLAY A PAS
SIVE ROLE IN THE ACQUISITION OF IMMUNITY 4HESE ARE TRANSMISSION ELECTRON MICROGRAPH OF SECTIONS THROUGH OF NEAR
TERM EMBRYOS
OF THE GOODEID 'IRARDINICHTHYS VIVIPARUS &ROM 3CHINDLER AND DE 6RIES A REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
! 4HE LATERAL PLASMALEMMAS OF ABSORPTIVE CELLS ARE LINED WITH LAMELLAR STRUCTURES AND MEMBRANOUS BLEBS ARE EXTRUDED INTO
THE INTERCELLULAR SPACE 2%2 GRANULAR ENDOPLASMIC RETICULUM 8
" ! SINGLE LAYER OF mATTENED CELLS RESTING ON THE BASAL LAMINA "- UNDERLIES THE ABSORPTIVE EPITHELIUM 4HESE BASAL CELLS
ARE CONNECTED BY HIGHLY CONVOLUTED INTERDIGITATIONS ARROW ! LEUCOCYTE , CAN BE SEEN IN THE INTERCELLULAR SPACES )#3
BETWEEN THE TWO TYPES OF EPITHELIAL CELLS ANOTHER IS PRESENT IN THE TROPHOTAENIAL STROMA 8
# ,EUCOCYTES LARGELY HETEROPHILIC GRANULOCYTES OCCUPY THE CONNECTIVE TISSUE CORE OF A TROPHOTAENIA 8
#(!04%2
&IGURE %MBRYOS OF THE MATROTROPHIC POECILIID
(ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS
REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 3CANNING ELECTRON MICROGRAPH OF A MID STAGE EM
BRYO 4HE HOOD LIKE EXPANSION OF THE PERICAR
DIAL SAC HAS INVESTED THE HEAD OF THE EMBRYO
!RROWHEADS INDICATE THE POSITION WHERE THE LATERAL
MARGINS OF THE EXPANDED PERICARDIAL SAC HAVE FUSED
DORSOMEDIALLY 4HE PORTAL PLEXUS UNDERLIES THE REGION
OUTLINED BY DOTS 8
" $RAWING OF A MID STAGE EMBRYO ILLUSTRATING THE PORTAL
PLEXUS UNDERLYING THE YOLK AND PERICARDIAL SAC SURFACES
AND THE EXTENT TO WHICH THE PERICARDIAL SAC INVESTS THE
HEAD OF THE EMBRYO
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SUR
FACE EPITHELIUM OF A LATE STAGE EMBRYO OF THE MATROTROPHIC
POECILIID (ETERANDRIA FORMOSA 4HE EPITHELIUM IS A PATCH
WORK OF ABSORPTIVE CELLS AND CELLS THAT DO NOT APPEAR TO BE
ABSORPTIVE &ROM 'ROVE AND 7OURMS REPRODUCED
WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 4HE POSTEROLATERAL SURFACE CONSISTS OF CLUSTERS OF CELLS
WITH MICROVILLI INTERSPERSED AMONG CELLS LACKING MI
CROVILLI 4HE CELLS LACKING MICROVILLI HOWEVER DISPLAY
SURFACE FOLDS 8
" 4HE LATERAL SURFACE OF THE TAIL CONSISTS OF CELLS WITH AND
WITHOUT MICROVILLI AND THOSE LACKING MICROVILLI DISPLAY
SURFACE FOLDS 8
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE SURFACE EPITHELIUM OF A MID STAGE EMBRYO OF THE MATRO
TROPHIC POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
! )N THE BILAMINAR SURFACE EPITHELIUM COVERING THE PERICARDIAL SAC THE SUPERlCIAL CELLS POSSESS APICAL MICROVILLI NUMEROUS
ELECTRON LUCENT VESICLES ELV AND EXTENSIVE GRANULAR ENDOPLASMIC RETICULUM 2%2 THE GRANULAR ENDOPLASMIC RETICULUM IN
THE BASAL CYTOPLASM OCCURS AS STACKS OF PARALLEL CISTERNAE "ASAL CELLS ARE THINNER AND POSSESS FEW ORGANELLES 4HE ENDOTHE
LIUM OF A VESSEL OF THE PORTAL PLEXUS IS CLOSELY ASSOCIATED WITH THE SURFACE EPITHELIUM 8
)NSET A COATED VESICLE AND PIT AT THE APICAL SURFACE OF THE SUPERlCIAL CELL 8
" %LECTRON LUCENT VESICLES ELV ARE SHOWN IN THE CYTOPLASM OF A SUPERlCIAL CELL 8
# !N ELECTRON LUCENT VESICLE IN A SUPERlCIAL CELL DISPLAYS A COATED REGION ARROWHEAD 8
$ %LECTRON LUCENT VESICLE ELV WITH A BLEB LIKE EXTENSION CIRCLE 8
% !N ELECTRON LUCENT VESICLE CONTAINING MYELIN lGURES 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE SURFACE EPITHELIUM COVERING THE NON
VASCULAR LATERAL
SURFACE OF A MID
STAGE EMBRYO JUST CAUDAL TO THE PECTORAL lN AND DORSAL TO THE PERICARDIAL AND YOLK SACS OF THE MATROTROPHIC
POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
! 3UPERlCIAL CELL SHOWING DENSE
STAINING DSV AND ELECTRON
LUCENT VESICLES $ENSE
STAINING VESICLES VARY IN THE STRUCTURE
OF THEIR CONTENTS AND IN THEIR SHAPE 8
)NSET SHOWS A DENSE
STAINING VESICLE WITH HETEROGENEOUS CONTENTS 8
" ! MULTIVESICULAR BODY IN A SUPERlCIAL EPITHELIAL CELL 8
# #OATED VESICLES ARROWHEADS IN THE CYTOPLASM OF A SUPERlCIAL CELL 8
$ % #ONTACT BETWEEN ADJACENT SUPERlCIAL CELLS IS CHARACTERIZED BY APICAL JUNCTIONAL COMPLEXES AND EXTENSIVE INTERDIGITATION
OF THE LATERAL PLASMA MEMBRANES 8
&
!N APICAL JUNCTIONAL COMPLEX BETWEEN ADJACENT SUPERlCIAL CELLS 8
6)6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE SUR
FACE EPITHELIUM OF AN EMBRYO OF THE MATROTROPHIC POECILIID (ETERANDRIA
FORMOSA &ROM 'ROVE AND 7OURMS REPRODUCED WITH PERMISSION OF
*OHN 7ILEY 3ONS )NC
! "ASAL CELL OF THE SURFACE EPITHELIUM OF A MID STAGE EMBRYO SHOWING
A CILIUM AND ITS BASAL BODY 4HE DENSE EXTRACELLULAR GRANULES ARROW
HEADS MAY REPRESENT YOLK 8
" ! BASAL CELL FROM THE SURFACE EPITHELIUM OF A MID STAGE EMBRYO SHOWING
A COATED PIT ARROWHEAD AT ITS APICAL SURFACE 8
# 3URFACE EPITHELIUM OF A LATE STAGE EMBRYO FROM A REGION SIMILAR TO THAT
SHOWN IN &IGURE ! 4HE EPITHELIUM CONSISTS OF SUPERlCIAL AND BAS
AL CELLS 4HE SUPERlCIAL CELLS LACK MICROVILLI AND ARE THINNER THAN ABSORP
TIVE SUPERlCIAL CELLS WITH MICROVILLI
)NSET CYTOPLASMIC lLAMENTS ARROWHEAD IN THE APICAL CYTOPLASM OF A
SUPERlCIAL CELL 8
$ 3URFACE EPITHELIUM OF A LATE STAGE EMBRYO FROM A REGION SIMILAR TO THAT
SHOWN IN &IGURE ! ILLUSTRATING THE JUNCTION BETWEEN AN ABSORPTIVE
CELL BEARING MICROVILLI AND A NON MICROVILLOUS CELL !LTHOUGH THE MOR
PHOLOGY OF THE TWO TYPES OF SUPERlCIAL CELLS DIFFERS STRIKINGLY THERE IS
NO APPARENT DIFFERENCE IN THE MORPHOLOGY OF THE BASAL CELLS 4HE BASAL
LAMINA IS INDICATED BY ARROWHEADS 8
#(!04%2
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE SURFACE EPITHELIUM OF A MID STAGE EMBRYO OF THE MATRO
TROPHIC POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS REPRODUCED WITH PERMISSION OF *OHN 7ILEY
3ONS )NC
! " 0UTATIVE CHLORIDE CELLS CONTAIN NUMEROUS MITOCHONDRIA AND AN EXTENSIVE SYSTEM OF TUBULAR CHANNELS THAT COMMUNICATE
WITH THE LATERAL AND BASAL EXTRACELLULAR SPACES CIRCLES IN " 4WO CHLORIDE CELLS IN ! ARE IN CONTACT WITH THE BASAL LAMINA
4HE CHLORIDE CELLS IN " EXTEND TO THE APICAL SURFACE OF THE EPITHELIUM WHERE THEY ARE CONNECTED TO ADJACENT SUPERlCIAL
CELLS BY JUNCTIONAL COMPLEXES ARROWHEADS 8
# "LOOD VESSEL OF THE PORTAL PLEXUS IS CLOSELY APPOSED TO THE BASAL SURFACE OF THE SURFACE EPITHELIUM 8
$ !N ENDOTHELIAL CELL OF THE PORTAL PLEXUS IS CLOSELY APPLIED TO A BASAL CELL OF THE SURFACE EPITHELIUM OF THE PERICARDIAL SAC
4HE ENDOTHELIAL AND EPITHELIAL CELLS ARE SO CLOSE TO ONE ANOTHER THAT THEIR TWO BASAL LAMINAE
CANNOT BE DISTINGUISHED
.UMEROUS PITS AND VESICLES IN THE ENDOTHELIAL CELL ARROWHEADS SUGGEST TRANSCYTOTIC MOVEMENT ACROSS THESE CELLS
8
6)6)0!2)49
&IGURE %XCHANGE WITH THE EMBRYOTROPH TAKES PLACE THROUGH SKIN COVERING THE RICHLY VASCULARIZED lN FOLDS OF GOODEIDS
&ROM -ENDOZA REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
0LATE 0HOTOMICROGRAPHS FROM 'OODEA LUITPOLDII
! #ROSS SECTION OF A
MM EMBRYO SHOWING THE DORSAL AND VENTRAL lN FOLDS
" 3ECTION OF THE VENTRAL lN FOLD SHOWING THE EXTENSIVE SUBEPITHELIAL VASCULAR STROMA
# 4HE SAME lN FOLD AT A HIGHER MAGNIlCATION
$ 3URFACE VIEW OF A STAINED WHOLE MOUNT OF A lN FOLD OF A
MM EMBRYO SHOWING ITS EXTENSIVE VASCULARIZATION 4HE BASE OF
THE FOLD IS AT THE LEFT THE FREE EDGE AT THE RIGHT
#(!04%2
0LATE $RAWINGS TO ILLUSTRATE lN FOLDS
%
#OMPARISON OF lN FOLDS OF
MM EMBRYOS OF TWO GOODEIDS 'OODEA AND !LLOPHORUS
& ' ( 4HREE STAGES OF EMBRYOS OF 'OODEA LUITPOLDII SHOWING THE DEVELOPMENT AND RESORPTION OF THE lN FOLDS 4HE ARROW
INDICATES THE DORSAL lN FOLD
6)6)0!2)49
&IGURE 6ASCULARIZED SPATULATE EXPANSIONS OF THE
INTERRADIAL lN WEB ON THE DORSAL lN OF EMBRYOS OF EMBI
OTOCIDS ARE PRESUMED TO FUNCTION IN MATERNAL FOETAL EX
CHANGE &ROM 7EBB &ISHERIES AND /CEANS #ANADA
2EPRODUCED WITH THE PERMISSION OF THE -INISTER OF 0UBLIC
7ORKS AND 'OVERNMENT 3ERVICES
! 0HOTOGRAPH SHOWING THE APPEARANCE OF A YOUNG STRIPED
SEAPERCH %MBIOTOCA LATERALIS AT THE MIDDLE OF GESTATION
4HE MOST PROMINENT VESSELS lN VEINS ANASTOMOSE AT
THE BASE OF THE MEDIAN AND CAUDAL lNS PASSING INTO
THE BODY TO JOIN THE CAUDAL VEIN 4HE LIGHTER APPEAR
ING ARTERIES LEAVE THE DORSAL AORTA PASSING TO THE lNS
4HE lN RAYS ARE TRANSPARENT AND CANNOT BE DISTINGUISHED
4HE GUT CAN BE CLEARLY SEEN
" $RAWINGS ILLUSTRATING CHANGES TO YOUNG EMBIOTOCIDS
DURING GESTATION
4OP
4HE STRIPED SEAPERCH %MBIOTOCA LATERALIS AT MID
GESTATION SHOWING THE EXTENSIVE VENOUS SYSTEM
PARTICULARLY OF THE lNS AND SPATULATE EXTENSIONS
4HE ARTERIAL SYSTEM AND lN RAYS HAVE BEEN OMIT
TED 4HE GUT SHOWN STIPPLED STILL PROTRUDES AT THIS
STAGE
#ENTRE ,ATE GESTATION PILE PERCH 2HACOCHILUS VACCA
4HE VEINS IN THE lNS ARE STILL PROMINENT AND THE
SPATULATE lN EXTENSIONS ARE STILL PRESENT &IN ARTER
IES AND RAYS ARE OMITTED
"OTTOM 4HE PILE PERCH 2HACOCHILUS VACCA JUST AFTER BIRTH
4HE BODY IS COVERED BY SCALES 6ESSELS IN THE lNS
ARE REDUCED &IN RAYS ARE SHOWN 4HE SPATULATE
EXTENSIONS OF THE MEDIAN AND CAUDAL lNS HAVE
LARGELY BEEN ABSORBED
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS TO ILLUSTRATE ADAPTATIONS FACILITATING RESPIRATORY EXCHANGE IN THE lNS OF
THE VIVIPAROUS SURFPERCH -ICROMETRUS MINIMUS &ROM $OBBS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
! &LAPS ON THE POSTERIOR DORSAL lN APPEAR AS EXPANSIONS OF THE INTER
RADIAL lN WEB 8
" 4HE APICAL PLASMALEMMA OF EPIDERMAL CELLS AT THE BASE OF THE DORSAL lN BEAR MICRORIDGES THAT INCREASE THE SURFACE AREA
FOR EXCHANGE 4HE BULGES BETWEEN THE EPIDERMAL CELLS ARE PROBABLY MUCOUS CELLS 8
# 4HE SURFACE OF EPIDERMAL CELLS ON THE lN mAPS BEARS MICRORIDGES THAT RESEMBLE THOSE ON THE EPITHELIUM COVERING GILL
lLAMENTS 8
2%&%2%.#%3
!BRAHAM - ET AL 4HE CELLULAR ENVELOPE OF OOCYTES IN TELEOSTS #ELL 4ISSUE 2ES
!BRAHAM - ET AL -UCO FOLLICLE CELLS OF THE JELLY COAT IN THE OOCYTE ENVELOPE OF THE SHEATlSH 3ILURUS GLANIS ,
* -ORPHOL
!FZELIUS "! , .ICANDER AND ) 3JDN &INE STRUCTURE OF EGG ENVELOPES AND THE ACTIVATION CHANGES OF CORTICAL ALEVOLI IN
THE RIVER LAMPREY ,AMPETRA mUVIATILIS * %MBRYOL %XPER -ORPHOL
!LDERDICE $& */4 *ENSEN AND &0* 6ELSEN -EASUREMENT OF HYDROSTATIC PRESSURE IN SALMONID EGGS #AN * :OOL
!LDRIDGE $# $EVELOPMENT OF %UROPEAN BITTERLING IN THE GILLS OF FRESHWATER MUSSELS * &ISH "IOL
!MANZE $ AND ! )YENGAR 4HE MICROPYLE A SPERM GUIDANCE SYSTEM IN TELOST FERTILIZATION $EVELOPMENT
!NDERSON % 4HE FORMATION OF THE PRIMARY ENVELOPE DURING OOCYTE DIFFERENTIATION IN TELEOSTS * #ELL "IOL
!NDERSON % #ORTICAL ALVEOLI FORMATION AND VITELLOGENESIS DURING OOCYTE DIFFERENTIATION IN THE PIPElSH 3YNGNATHUS FUSCUS
AND THE KILLIlSH &UNDULUS HETEROCLITUS * -ORPHOL
!NDREUCCETTI 0 ET AL )NTERCELLULAR BRIDGES BETWEEN GRANULOSA CELLS AND THE OOCYTE IN THE ELASMOBRANCH 2AYA ASTERIAS
!NAT 2EC
!RAVINDAN #- AND +' 0ADMANABHAN &ORMATION OF THE MICROPYLE IN 4ILAPIA MOSSAMBICA 0ETERS AND 3TIGMATOGOBIUS
JAVANICUS "LKR !CTA :OOL 3TOCKH
!SAHINA + + 4AGUCHI AND 4 (IBIYA )N VITRO EFFECT OF VARIOUS STEROIDS ON lNAL MATURATION IN OOCYTES OF AGOHAZE GOBI
#HASMICHTHYS DOLICHOGNATHUS AND #HICHIBU GOBY 4RIDENTIGER OBSCURUS )N 0ROCEEDINGS OF THE &IRST #ONGRESS OF THE !SIA
AND /CEANIA 3OCIETY FOR #OMPARATIVE %NDOCRINOLOGY !/3#% % /HNISHI 9 .AGAHAMA AND ( )SHIZAKI EDS .AGOYA
.AGOYA 5NIVERSITY #ORP 0RINTING 3ECTION PP
!TZ *7 )NTERSEXUALITY IN lSHES #HAPTER IN )NTERSEXUALITY IN 6ERTEBRATES )NCLUDING -AN #. !RMSTRONG AND
!* -ARSHALL EDS ,ONDON !CADEMIC 0RESS PP
!ZEVEDO # VOLUTION DES ENVELOPPES OVOCYTAIRES AU COURS DE LOVOGENSE CHEZ UN 4LOSTEN VIVIPARE 8IPHOPHORUS
HELLERI * -ICROSC 0ARIS
!ZEVEDO # AND ! #OIMBRA %VOLUTION OF NUCLEOLI IN THE COURSE OF OOGENESIS IN A VIVIPAROUS TELEOST 8IPHOPHORUS
HELLERI "IOL #ELL
"ABU . AND ." .AIR &OLLICULAR ATRESIA IN !MBLYPHARYNGODON CHAKAIENSIS : -IKROSK !NAT &ORSCH
"AGENAL 4" AND % "RAUM %GGS AND EARLY LIFE HISTORY #HAPTER IN -ETHODS FOR !SSESSMENT OF &ISH 0RODUCTION IN
&RESH 7ATERS )"0 (ANDBOOK NO ND ED 7% 2ICKER ED /XFORD "LACKWELL 3CIENTIlC 0UBLICATIONS PP
"ALL *. 2EPRODUCTION IN FEMALE BONY lSHES 3YMP :OOL 3OC ,ONDON
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:OO 3UPPL
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#HAN 34( ! 7RIGHT AND *' 0HILLIPS 4HE ATRETIC STRUCTURES IN THE GONADS OF THE RICE
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#HEN +# +4 3HAO AND *3 9ANG 5SING MICROPYLAR ULTRASTRUCTURE FOR SPECIES IDENTIlCATION AND PHYLOGENETIC INFERENCE
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3KATES AND 2AYS 07 'ILBERT 2& -ATHEWSON AND $0 2ALL EDS "ALTIMORE 4HE *OHNS (OPKINS 0RESS PP
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$ODD *- 4HE STRUCTURE OF THE OVARY OF NONMAMMALIAN VERTEBRATES #HAPTER IN 4HE /VARY ND ED VOL ) 'ENERAL
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'REELEY -3 $2 #ALDER AND 2! 7ALLACE #HANGES IN TELEOST YOLK PROTEINS DURING OOCYTE MATURATION CORRELATION OF
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'RIER ( /VARIAN GERMINAL EPITHELIUM AND FOLLICULOGENESIS IN THE COMMON SNOOK #ENTROPOMUS UNDECIMALIS 4ELEOSTEI
#ENTROPOMIDAE * -ORPHOL
'RIERSON *0 AND !# .EVILLE (ELICOIDAL ARCHITECTURE OF lSH EGG
SHELL 4ISSUE #ELL
'REENWOOD 0( *2 .ORMAN A (ISTORY OF &ISHES RD ED ,ONDON %RNEST "ENN ,IMITED PP
'ROE 7ICHTRUP , AND ( 'REVEN 5PTAKE OF FERRITIN BY THE TROPHOTAENIAE OF THE GOODEID lSH !MECA SPLENDENS -ILLER
AND &ITZSIMONS 4ELEOSTEI #YPRINODONTIFORMES #YTOBIOS
'ROE 7ICHTRUP , AND ( 'REVEN 5LTRASTRUCTURAL ASPECTS OF THE TROPHOTAENIAL EPITHELIUM IN !MECA SPLENDENS -ILLER AND
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'ROVE "$ AND *0 7OURMS 4HE FOLLICULAR PLACENTA OF THE VIVIPAROUS lSH (ETERANDRIA FORMOSA ) 5LTRASTRUCTURE AND
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'URAYA 33 (ISTOCHEMICAL STUDIES ON THE YOLK
NUCLEUS IN lSH OOGENESIS : :ELLFORSCH -IKROSK !NAT
'URAYA 33 (ISTOCHEMICAL OBSERVATIONS ON THE INTERSTITIAL GLAND CELLS OF DOGlSH OVARY 'EN #OMP %NDOCRINOL
'URAYA 33 2ECENT ADVANCES IN THE MOROPHOLOGY CYTOCHEMISTRY AND FUNCTION OF "ALBIANIS VITELLINE BODY IN ANIMAL
OOCYTES )NT 2EV #YTOL
2%&%2%.#%3
'URAYA 33 2ECENT PROGRESS IN THE STRUCTURE ORIGIN COMPOSITION AND FUNCTION OF CORTICAL GRANULES IN ANIMAL EGG
)NT 2EV #YTOL
'URAYA 33 4HE #ELL AND -OLECULAR "IOLOGY OF &ISH /OGENESIS -ONOGRAPHS IN $EVELOPMENTAL "IOLOGY VOL
(7 3AUER ED "ASEL 3 +ARGER !' PP
'URAYA 33 AND 3 +AUR #ELLULAR SITES OF STEROID SYNTHESIS IN THE OVIPAROUS TELEOST lSH #YPRINUS CARPIO , A HISTO
CHEMICAL STUDY 0ROC )NDIAN !CAD 3CI !NIM 3CI
(AGENMAIER (% 4HE HATCHING PROCESS IN lSH EMBRYOS ))) 4HE STRUCTURE POLYSACCHARIDE AND PROTEIN CYTOCHEMISTRY
OF THE CHORION OF THE TROUT EGG 3ALMO GAIRDNERI 2ICH !CTA (ISTOCHEM
(AGIWARA 3 AND ,! *AFFE %LECTRICAL PROPERTIES OF EGG CELL MEMBRANES !NN 2EV "IOPHYS "IOENG
(CKER ' 4HE MORPHOLOGY OF APOPTOSIS #ELL 4ISSUE 2ES
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THE )NDIAN CATlSH -YSTUS VITTATUS 'EN #OMP %NDOCRINOL
(AMAGUCHI 3 ! LIGHT
AND ELECTRON
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LATIPES #ELL 4ISSUE 2ES
(AMAGUCHI 3 #HANGES IN THE MORPHOLOGY OF THE GERMINAL DENSE BODIES IN PRIMORDIAL GERM CELLS OF THE TELEOST /RYZIAS
LATIPES #ELL 4ISSUE 2ES
(AMAZAKI 43 ET AL ! GLYCOPROTEIN FROM THE LIVER CONSTITUTES THE INNER LAYER OF THE EGG ENVELOPE ZONA PELLUCIDA INTERNA
OF THE lSH /RYZIAS LATIPES $EV "IOL
(AMAZAKI 4 ) )UCHI AND + 9AMAGAMI ! SPAWNING FEMALE
SPECIlC SUBSTANCE REACTIVE TO ANTI
CHORION EGG
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(AMAZAKI 43 ) )UCHI AND + 9AMAGAMI 0RODUCTION OF A hSPAWNING FEMALE
SPECIlC SUBSTANCEv IN HEPATIC CELLS AND
ITS ACCUMULATION IN THE ASCITES OF THE ESTROGEN
TREATED ADULT lSH /RYZIAS LATIPES * %XPER :OOL
(AMLETT 7# 0RENATAL ABSORPTIVE SURFACES IN SELACHIANS )N )NDO
0ACIlC &ISH "IOLOGY 0ROCEEDINGS OF THE 3ECOND
)NTERNATIONAL #ONFERENCE ON )NDO
0ACIlC &ISHES 4 5YENO 2 !RAI 4 4ANIUCHI AND + -ATSUURA EDS 4OKYO )CHTHYOLOGICAL
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(AMLETT 7# #OMPARATIVE MORPHOLOGY OF THE ELASMOBRANCH PLACENTAL BARRIER !RCH "IOL "RUX
(AMLETT 7# %VOLUTION AND MORPHOGENESIS OF THE PLACENTA IN SHARKS * %XPER :OOL 3UPPL
(AMLETT 7# /NTOGENY OF THE UMBILICAL CORD AND PLACENTA IN THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE
%NVIRON "IOL &ISHES
(AMLETT 7# ET AL 0ERMEABILITY OF EXTERNAL GILL lLAMENTS IN THE EMBRYONIC SHARK %LECTRON MICROSCOPIC OBSERVATIONS
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(AMLETT 7# ET AL A 5TEROGESTATION AND PLACENTATION IN ELASMOBRANCHS * %XPER :OOL
(AMLETT 7#ET AL B &INE STRUCTURE OF THE TERM UMBILICAL CORD IN THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENO
VAE * 3UBMICROSC #YTOL 0ATHOL
(AMLETT 7# ET AL A 5LTRASTRUCTURE OF UTERINE TROPHONEMATA ACCOMMODATION FOR UTEROLACTATION AND GAS EXCHANGE IN
THE SOUTHERN STINGRAY $ASYATIS AMERICANA #AN * :OOL
(AMLETT 7# ET AL B 5LTRASTRUCTURE OF THE OVIDUCAL GLAND IN THE YELLOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS WITH
OBSERVATIONS ON A NOVEL INCLUSION * !NAT
(AMLETT 7# ET AL A 3URVEY OF OVIDUCAL GLAND STRUCTURE AND FUNCTION IN ELASMOBRANCHS * %XPER :OOL
(AMLETT 7# ET AL B 2EPRODUCTIVE ACCOMMODATIONS FOR GESTATION IN THE !TLANTIC GUITARlSH 2HINOBATOS LENTIGINOSUS
2HINOBATIDAE * %LISHA -ITCHELL 3CI 3OC
(AMLETT 7# AND -+ (YSELL 5TERINE SPECIALIZATIONS IN ELASMOBRANCHS * %XPER :OOL
(AMLETT 7# - *EZIOR AND 2 3PIELER 5LTRASTRUCTURAL ANALYSIS OF FOLLICULOGENESIS IN THE OVARY OF THE YELLOW SPOTTED
STINGRAY 5ROLOPHUS JAMAICAENSIS !NN !NAT
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2HIZOPRIONODON TERRAENOVAE * 3UBMICROSC #YTOL 0ATHOL
(AMLETT 7# &* 3CHWARTZ AND ,*! $I$IO 3UBCELLULAR ORGANIZATION OF THE YOLK SYNCYTIAL
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2%&%2%.#%3
(AMLETT 7# AND *0 7OURMS 5LTRASTRUCTURE OF THE PRE
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(AMLETT 7# *0 7OURMS AND *3 (UDSON A 5LTRASTRUCTURE OF THE FULL
TERM SHARK YOLK SAC PLACENTA ) -ORPHOLOGY AND
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(AMLETT 7# *0 7OURMS AND *3 (UDSON B 5LTRASTRUCTURE OF THE FULL
TERM SHARK YOLK SAC PLACENTA )) 4HE SMOOTH
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(AMLETT 7# *0 7OURMS AND *3 (UDSON C 5LTRASTRUCTURE OF THE FULL
TERM SHARK YOLK SAC PLACENTA ))) 4HE MATERNAL
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(AMLETT 7# *0 7OURMS AND *7 3MITH 3TINGRAY PLACENTAL ANALOGUES STRUCTURE OF TROPHONEMATA IN 2HINOPTERA
BONASUS * 3UBMICROSC #YTOL
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PP PP AND PLATES
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-7 (ARDISTY AND )# 0OTTER EDS ,ONDON !CADEMIC 0RESS )NC PP
(ART .( &ERTILIZATION IN TELEOST lSHES MECHANISMS OF SPERM
EGG INTERACTIONS )NT 2EV #YTOL
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MICROSCOPE AND FREEZE
FRACTURE STUDY OF THE EGG CORTEX OF "RACHYDANIO RERIO
#ELL 4ISSUE 2ES
(ART .( AND - $ONOVAN &INE STRUCTURE OF THE CHORION AND SITE OF SPERM ENTRY IN THE EGG OF "RACHYDANIO * %XPER
:OOL
(ART .( 2 0IETRI AND - $ONOVAN 4HE STRUCTURE OF THE CHORION AND ASSOCIATED SURFACE lLAMENTS IN /RYZIAS
EVIDENCE FOR THE PRESENCE OF EXTRACELLULAR TUBULES * %XPER :OOL
(ART .( AND *3 7OLENSKI !CTIN IN THE CORTEX OF THE TELEOST EGG * #ELL "IOL A
(ART .( AND 3& 9U #ORTICAL GRANULE EXOCYTOSIS AND CELL SURFACE REORGANIZATION IN EGGS OF "RACHYDANIO * %XPER
:OOL
(ART .( 3
& 9U AND 6 'REENHUT /BSERVATIONS ON THE CORTICAL REACTION IN EGGS OF "RACHYDANIO RERIO AS SEEN WITH
THE SCANNING ELECTRON MICROSCOPE * %XPER :OOL
(ENDERSON .% 4HE URINARY AND GENITAL SYSTEMS OF TROUT * &ISH 2ES "D #ANADA
(IRAI ! &INE STRUCTURES OF THE MICROPYLES OF PELAGIC EGGS OF SOME MARINE lSHES *AP * )CHTHYOL
(IRAI ! &INE STRUCTURE OF THE EGG MEMBRANES IN FOUR SPECIES OF 0LEURONECTINAE *AP * )CHTHYOL
(IRAI ! AND 4 9AMAMOTO -ICROPYLE IN THE DEVELOPING EGGS OF THE ANCHOVY %NGRAULIS JAPONICA *AP * )CHTHYOL
(IROSE + 4HE ULTRASTRUCTURE OF THE OVARIAN FOLLICLE OF MEDAKA /RYZIAS LATIPES : :ELLFORSCH -IKROSK !NAT
(IROSE + ET AL )N VITRO BIOCONVERSIONS OF STEROIDS IN THE MATURE OVARY OF THE HAGlSH %PTATRETUS BURGERI #OMP "IOCHEM
0HYSIOL "
(IROSE + AND 2 )SHIDA %FFECTS OF CORTISOL AND HUMAN CHORIONIC GONADOTROPHIN (#' ON OVULATION IN AYU 0LECOGLOSSUS
ALTIVELIS 4EMMINCK 3CHLEGEL WITH SPECIAL RESPECT TO WATER AND ION BALANCE * &ISH "IOL
(ISAW &, *R AND &, (ISAW #ORPORA LUTEA OF ELASMOBRANCH lSHES !NAT 2EC
(OAR 73 2EPRODUCTION IN TELEOST lSH -EM 3OC %NDOCRINOL
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!CADEMIC 0RESS )NC PP
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0RESS )NC PP
(OAR 73 AND 9 .AGAHAMA 4HE CELLULAR SOURCES OF SEX STEROIDS IN TELEOST GONADS !NN "IOL !NIM "IOCH "IOPHYS
(OGAN *# !N ULTRASTRUCTURAL ANALYSIS OF hCYTOPLASMIC MARKERSv IN GERM CELLS OF /RYZIAS LATIPES * 5LTRASTRUCT 2ES
(OLLENBERG & AND *0 7OURMS 5LTRASTRUCTURE AND PROTEIN UPTAKE OF THE EMBRYONIC TROPHOTAENIAE OF FOUR SPECIES OF
GOODEID lSHES 4ELEOSTEI !THERINIFORMES * -ORPHOL
2%&%2%.#%3
(OLLENBERG & AND *0 7OURMS %MBRYONIC GROWTH AND MATERNAL NUTRIENT SOURCES IN GOODEID lSHES 4ELEOSTEI
#YPRINODONTIFORMES * %XPER :OOL
(OSOKAWA + %LECTRON MICROSCOPIC OBSERVATION OF THE FORMATION OF THE CHORION IN 0AGRAS MAJOR :OOL -AG
(OSOKAWA + %LECTRON MICROSCOPIC OBSERVATION OF CHORION FORMATION IN THE TELEOST .AVODON MODESTUS :OOL 3CI
VAN DEN (URK 2 AND * 0EUTE #YCLIC CHANGES IN THE OVARY OF THE RAINBOW TROUT 3ALMO GAIRDNERI WITH SPECIAL REFERENCE
TO SITES OF STEROIDOGENESIS #ELL 4ISSUE 2ES
VAN DEN (URK 2 AND * 0EUTE &UNCTIONAL ASPECTS OF THE POSTOVULATORY FOLLICLE IN THE OVARY OF THE !FRICAN CATlSH #LARIAS
GARIEPINUS AFTER INDUCED OVULATION !N ULTRASTRUCTURAL AND ENZYME HISTOCHEMICAL STUDY #ELL 4ISSUE 2ES
(URLEY $! AND +# &ISHER 4HE STRUCTURE AND DEVELOPMENT OF THE EXTERNAL MEMBRANE IN YOUNG EGGS OF THE BROOK TROUT
3ALVELINUS FONTINALIS -ITCHILL #AN * :OOL
(YLLNER 3* ET AL /ESTRADIOL
` INDUCES THE MAJOR VITELLINE ENVELOPE PROTEINS IN BOTH SEXES IN TELEOSTS * %NDOCRINOL
(YLLNER 3* " .ORBERG AND # (AUX )SOLATION PARTIAL CHARACTERIZATION INDUCTION AND THE OCCURRENCE IN PLASMA OF
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&ISH !QUAT 3CI
(YLLNER 3* # 3ILVERSAND AND # (AUX &ORMATION OF THE VITELLINE ENVELOPE PRECEDES THE ACTIVE UPTAKE OF VITELLOGENIN
DURING OOCYTE DEVELOPMENT IN THE RAINBOW TROUT /NCORHYNCHUS MYKISS -OL 2EPROD $EV
)NOUE 3 ET AL ,OCALIZATION OF POLYSIALOGLYCOPROTEIN AS A MAJOR GLYCOPROTEIN COMPONENT IN CORTICAL ALVEOLI OF THE UNFERTIL
IZED EGGS OF 3ALMO GAIRDNERI $EV "IOL
)NOUE 3 AND 9 )NOUE &ERTILIZATION ACTIVATION
INDUCED
TO
K$A DEPOLYMERIZATION OF POLYSIALOGLYCOPROTEIN
A DISTINCT COMPONENT OF CORTICAL ALVEOLI OF RAINBOW TROUT EGGS * "IOL #HEM
)SHIJIMA 3 9 (AMAGUCHI AND 4 )WAMATSU 3PERM BEHAVIOR IN THE MICROPYLE OF THE MEDAKA EGG :OOL 3CI
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DURING HARDENING $EVELOP 'ROWTH $IFFER
)UCHI ) AND + 9AMAGAMI -AJOR GLYCOPROTEINS SOLUBILIZED FROM THE TELEOSTEAN EGG MEMBRANE BY THE ACTION OF THE
HATCHING ENZYME "IOCHIM "IOPHYS !CTA
)WAMATSU 4 -ORPHOLOGY OF lLAMENTS ON THE CHORION OF OOCYTES AND EGGS IN THE MEDAKA :OOL 3CI
)WAMATSU 4 -EDAKA OOCYTES ROTATE WITHIN THE OVARIAN FOLLICLES DURING OOGENESIS $EV 'ROWTH $IFFER
)WAMATSU 4 3TUDIES ON FERTILIZATION IN THE TELEOST ) $YNAMIC RESPONSES OF FERTILIZED MEDAKA EGGS $EVELOP 'ROWTH
$IFFER
)WAMATSU 4 &ERTILIZATION IN lSHES #HAPTER IN &ERTILIZATION IN 0ROTOZOA AND -ETAZOAN !NIMALS ** 4ARN AND ! #ANO
EDS "ERLIN (EIDELBERG 3PRINGER
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)WAMATSU 4 ET AL %FFECT OF MICROPYLAR MORPHOLOGY AND SIZE ON RAPID SPERM ENTRY INTO THE EGGS OF THE MEDAKA
:OOL 3CI
)WAMATSU 4 ET AL 3TUDIES OF OOCYTE MATURATION OF THE MEDAKA /RYZIAS LATIPES ))) #YTOPLASMIC AND NUCLEAR CHANGES
OF OOCYTE DURING IN VITRO MATURATION !NNOT :OOL *AP
)WAMATSU 4 ET AL /OGENESIS IN THE MEDAKA /RYZIAS LATIPES STAGES OF OOCYTE DEVELOPMENT :OOL 3CI
)WAMATSU 4 ET AL 4IME SEQUENCE OF EARLY EVENTS IN FERTILIZATION IN THE MEDAKA EGG $EVELOP 'ROWTH $IFFER
)WAMATSU 4 ET AL %FFECT OF MICROPYLAR MORPHOLOGY AND SIZE ON RAPID SPERM ENTRY INTO THE EGGS OF THE MEDAKA
:OOL 3CI
)WAMATSU 4 3 )SHIJIMA AND 3 .AKASHIMA -OVEMENT OF SPERMATOZOA AND CHANGES IN MICROPYLES DURING FERTILIZATION
IN MEDAKA EGGS * %XPER :OOL
)WAMATSU 4 AND ( +EINO 3CANNING ELECTRON MICROSCOPIC STUDY ON THE SURFACE CHANGE OF EGGS OF THE TELEOST /RYZIAS
LATIPES AT THE TIME OF FERTILIZATION $EVELOP 'ROWTH $IFFER
)WAMATSU 4 AND 3 .AKASHIMA $YNAMIC GROWTH OF OOCYTES OF THE MEDAKA /RYZIAS LATIPES ) ! RELATIONSHIP BETWEEN
ESTABLISHMENT OF THE ANIMAL
VEGETAL AXIS OF THE OCCYTE AND ITS SURROUNDING GRANULOSA CELLS :OOL 3CI
2%&%2%.#%3
)WAMATSU 4 3 .AKASHIMA AND + /NITAKE 3PIRAL PATTERNS IN THE MICROPYLAR WALL AND lLAMENTS ON THE CHORION IN EGGS
OF THE MEDAKA /RYZIAS LATIPES * %XPER :OOL
)WAMATSU 4 AND 4 /HTA "REAKDOWN OF THE CORTICAL ALVEOLI OF MEDAKA EGGS AT THE TIME OF FERTILIZATION WITH A PARTICULAR
REFERENCE TO THE POSSIBLE ROLE OF SPHERICAL BODIES IN THE ALVEOLI 2OUXS !RCH
)WAMATSU 4 AND 4 /HTA &INE STRUCTURE OF LOACH OOCYTES DURING MATURATION IN VITRO $EVELOP 'ROWTH $IFFER
)WAMATSU 4 AND 4 /HTA %LECTRON MICROSCOPIC OBSERVATION ON SPERM PENETRATION AND PRONUCLEAR FORMATION IN THE lSH
EGG * %XPER :OOL
)WAMATSU 4 AND 4 /HTA A /N A RELATIONSHIP BETWEEN OOCYTE AND FOLLICLE CELLS AROUND THE TIME OF OVULATION IN THE MEDAKA
/RYZIAS LATIPES !NNOT :OOL *AP
)WAMATSU 4 AND 4 /HTA B 3CANNING ELECTRON MICROSCOPIC OBSERVATIONS ON SPERM PENETRATION IN TELEOSTEAN lSH * %XPER
:OOL
)WAMATSU 4 9 3HIBATA AND 4 +ANIE #HANGES IN CHORION PROTEINS INDUCED BY THE EXDATE RELEASED FROM THE EGG CORTEX AT
THE TIME OF FERTILIZATION IN THE TELEOST /RYZIAS LATIPES $EVELOP 'ROWTH $IFFER
)WAMATSU 4 9 9OSHIMOTO AND 9 (IRAMOTO A #YTOPLASMIC #A RELEASE INDUCED BY MICROINJECTION OF #A AND EFFECTS
OF MICROINJECTED DIVALENT CATIONS ON #A SEQUESTRATION AND EXOCYTOSIS OF CORTICAL ALVEOLI IN THE MEDAKA EGG $EV "IOL
)WAMATSU 4 9 9OSHIMOTO AND 9 (IRAMOTO B -ECHANISM OF #A RELEASE IN MEDAKA EGGS MICROINJECTED WITH INOSITOL
TRIPHOSPHATE AND #A $EV "IOL
)WAMATSU 4 . 9OSHIZAKI AND 9 3HIBATA #HANGES IN THE CHORION AND SPERM ENTRY INTO THE MICROPYLE DURING FERTILIZATION
IN THE TELEOSTEAN lSH /RYZIAS LATIPES $EVELOP 'ROWTH $IFFER
)WASAKI 9 (ISTOCHEMICAL DETECTION OF 6 ` HYDROXYSTEROID DEHYDROGENASE IN THE OVARY OF THE MEDAKA /RYZIAS LATIPES
DURING ANNUAL REPRODUCTIVE CYCLE "ULL &AC &ISH (OKKAIDO 5NIV
*AFFE ,& #ALCIUM EXPLOSIONS AS TRIGGERS OF DEVELOPMENT !NN .9 !CAD 3CI
*ALABERT " )N VITRO OOCYTE MATURATION AND OVULATION IN RAINBOW TROUT 3ALMO GAIRDNERI NORTHERN PIKE %SOX LUCIUS AND
GOLDlSH #ARASSIUS AURATUS * &ISHERIES 2ES "D #ANADA
*ALABERT " AND 2 "ILLARD TUDE ULTRASTRUCTURALE DU SITE DE CONSERVATION DES SPERMATOZODES DANS LOVAIRE DE 0OECILIA
RETICULATA 0OISSON 4LOSTEN !NN "IOL !NIM "IOCH "IOPHYS
*ALABERT " AND $ 3ZLLSI )N VITRO OVULATION OF TROUT OOCYTES EFFECT OF PROSTAGLANDINS ON SMOOTH MUSCLE LIKE CELLS OF
THE THECA 0ROSTAGLANDINS
*IANG * 1 ET AL /RGANIZATION OF CYTOPLASMIC MICROTUBULES DURING MATURATION OF GOLDlSH OOCYTES :OOL 3CI
*OHNSON %: AND 2' 7ERNER 3CANNING ELECTRON MICROSCOPY OF THE CHORION OF SELECTED FRESHWATER lSHES * &ISH "IOL
*OHNSTON 0- 4HE EMBRYONIC HISTORY OF THE GERM CELLS OF THE LARGEMOUTH BLACK BASS -ICROPTERUS SALMOIDES SALMOIDES
,ACPDE * -ORPHOL
*OLLIE 70 AND ,' *OLLIE A 4HE lNE STRUCTURE OF THE OVARIAN FOLLICLE OF THE OVOVIVIPAROUS POECILIID lSH ,EBISTES
RETICULATUS ) -ATURATION OF FOLLICULAR EPITHELIUM * -ORPHOL
*OLLIE 70 AND ,' *OLLIE B 4HE lNE STRUCTURE OF THE OVARIAN FOLLICLE OF THE OVOVIVIPAROUS POECILIID lSH ,EBISTES
RETICULATUS )) &ORMATION OF THE FOLLICULAR PSEUDOPLACENTA * -ORPHOL
*OLLIE 70 AND ,' *OLLIE A %LECTRON MICROSCOPIC OBSERVATIONS ON THE YOLK SAC OF THE SPINY DOGlSH 3QUALUS ACANTHIAS
* 5LTRASTRUCT 2ES
*OLLIE 70 AND ,' *OLLIE B %LECTRON MICROSCOPIC OBSERVATIONS ON ACCOMMODATIONS TO PREGNANCY IN THE UTERUS OF
THE SPINY DOGlSH 3QUALUS ACANTHIAS * 5LTRASTRUCT 2ES
+AGAWA ( ET AL %STRADIOL ` PRODUCTION IN AMAGO SALMON /NCORHYNCHUS RHODURUS OVARIAN FOLLICLES ROLE OF THE THECAL
AND GRANULOSA CELLS 'EN #OMP %NDOCRINOL
+AGAWA ( AND 9 .AGAHAMA )N VITRO EFFECTS OF PROSTAGLANDINS ON OVULATION IN GOLDlSH #ARASSIUS AURATUS "ULL *AP
3OC 3CI &ISHERIES
+AGAWA ( AND + 4AKANO 5LTRASTRUCTURE AND HISTOCHEMISTRY OF GRANULOSA CELLS OF PRE AND POST OVULATORY FOLLICLES IN
THE OVARY OF MEDAKA /RYZIAS LATIPES "ULL &AC &ISH (OKKAIDO 5NIV ;)N *APANESE WITH %NGLISH ABSTRACT
AND lGURE LEGENDS=
2%&%2%.#%3
+AGAWA ( + 4AKANO AND 9 .AGAHAMA #ORRELATION OF PLASMA ESTRADIOL ` AND PROGESTERONE LEVELS WITH ULTRASTRUCTURE
AND HISTOCHEMISTRY OF OVARIAN FOLLICLES IN THE WHITE SPOTTED CHAR 3ALVELINUS LEUCOMAENIS #ELL 4ISSUE 2ES
+ANAMORI ! 3 !DACHI AND 9 .AGAHAMA $EVELOPMENTAL CHANGES IN STEROIDOGENIC RESPONSES OF OVARIAN FOLLICLES
OF AMAGO SALMON /NCORHYNCHUS RHODURUS TO CHUM SALMON GONADOTROPIN DURING OOGENESIS 'EN #OMP %NDOCRINOL
+ANAMORI ! AND 9 .AGAHAMA A $EVELOPMENTAL CHANGES IN THE PROPERTIES OF GONADOTROPIN RECEPTORS IN THE OVARIAN
FOLLICLES OF AMAGO SALMON /NCORHYNCHUS RHODURUS DURING OOGENESIS 'EN #OMP %NDOCRINOL
+ANAMORI ! AND 9 .AGAHAMA B )NVOLVEMENT OF CYCLIC ADENOSINE MONOPHOSPHATE IN THE CONTROL OF FOLLICULAR
STEROIDOGENESIS OF AMAGO SALMON /NCORHYNCHUS RHODURUS 'EN #OMP %NDOCRINOL
+ARASAKI 3 !N ELECTRON MICROSCOPE STUDY ON THE CRYSTALLINE STRUCTURE OF THE YOLK PLATELETS OF THE LAMPREY EGG
* 5LTRASTRUCT 2ES
+ESSEL 2' !NNULATE LAMELLAE A LAST FRONTIER IN CELLULAR ORGANELLES )NT 2EV #YTOL
+ESSEL 2' ET AL 4HE PRESENCE AND DISTRIBUTION OF GAP JUNCTIONS IN THE OOCYTE FOLLICLE CELL COMPLEX OF THE ZEBRAlSH
"RACHYDANIO RERIO * 3UBMICROSC #YTOL
+ESSEL 2' (7 "EAMS AND (. 4UNG 2ELATIONSHIPS BETWEEN ANNULATE LAMELLAE AND lLAMENT BUNDLES IN OOCYTES OF
THE ZEBRAlSH "RACHYDANIO RERIO #ELL 4ISSUE 2ES
+ESSEL 2' 2, 2OBERTS AND (. 4UNG )NTERCELLULAR JUNCTIONS IN THE FOLLICULAR ENVELOPE OF THE TELEOST "RACHYDANIO
RERIO * 3UBMICROSC #YTOL 0ATHOL
+HOO +( 4HE CORPUS LUTEUM OF GOLDlSH #ARASSIUS AURATUS , AND ITS FUNCTIONS #AN * :OOL
+HOO +( 4HE HISTOCHEMISTRY AND ENDOCRINE CONTROL OF VITELLOGENESIS IN GOLDlSH OVARIES #AN * :OOL
+ILLE 2! &ERTILIZATION OF THE LAMPREY EGG %XPER #ELL 2ES
+ING 7 ET AL 0LASMA LEVELS OF GONADAL STEROIDS DURING lNAL OOCYTE MATURATION OF STRIPED BASS -ORONE SAXATILIS , 'EN
#OMP %NDOCRINOL
+ING -6 $, "ERLINSKY AND #6 3ULLIVAN )NVOLVEMENT OF GONADAL STEROIDS IN lNAL OOCYTE MATURATION OF WHITE PERCH
-ORONE AMERICANA AND WHITE BASS - CHRYSOPS IN VIVO AND IN VITRO STUDIES &ISH 0HYSIOL "IOCHEM
+ING 7 0 4HOMAS AND #6 3ULLIVAN (ORMONAL REGULATION OF lNAL MATURATION OF STRIPED BASS OOCYTES IN VITRO
'EN #OMP %NDOCRINOL
+ITAJIMA + ET AL #OMPARATIVE STRUCTURES OF THE APOPOLYSIALOGLYCOPROTEINS FROM UNFERTILIZED AND FERTILIZED EGGS OF
SALMONID lSHES "IOCHEMISTRY
+ITAJIMA + AND 3 )NOUE ! PROTEINASE ASSOCIATED WITH CORTICES OF RAINBOW TROUT EGGS AND INVOLVED IN FERTILIZATION
INDUCED DEPOLYMERIZATRION OF POLYSIALOGLYCOPROTEINS $EV "IOL
+ITAJIMA + 3 )NOUE AND 9 )NOUE )SOLATION AND CHARACTERIZATION OF A NOVEL TYPE OF SIALOGLYCOPROTEINS HYOSOPHORIN
FROM EGGS OF MEDAKA /RYZIAS LATIPES NONAPEPTIDE WITH A LARGE . LINKED GLYCAN CHAIN AS A TANDEM REPEAT UNIT $EV "IOL
+ITAJIMA + 9 )NOUE AND 3 )NOUE 0OLYSIALOGLYCOPROTEINS OF 3ALMONIDAE lSH EGGS #OMPLETE STRUCTURE OF K$A
POLYSIALOGLYCOPROTEIN FROM THE UNFERTILIZED EGGS OF RAINBOW TROUT 3ALMO GAIRDNERI * "IOL #HEM
+JESBU /3 ET AL &ECUNDITY ATRESIA AND EGG SIZE OF CAPTIVE !TLANTIC COD 'ADUS MORHUA IN RELATION TO PROXIMATE BODY
COMPOSITION #AN * &ISH !QUAT 3CI
+JESBU /3 AND ( +RYVI /OGENESIS IN COD 'ADUS MORHUA , STUDIED BY LIGHT AND ELECTRON MICROSCOPY * &ISH "IOL
+JESBU /3 ( +RYVI AND " .ORBERG /OCYTE SIZE AND STRUCTURE IN RELATION TO BLOOD PLASMA STEROID HORMONES IN
INDIVIDUALLY MONITORED SPAWNING !TLANTIC COD * &ISH "IOL
+NIGHT $0 ET AL #HANGES IN MACROMOLECULAR ORGANIZATION IN COLLAGEN ASSEMBLIES DURING SECRETION IN THE NIDAMEN
TAL GLAND AND FORMATION OF THE EGG CAPSULE WALL IN THE DOGlSH 3CYLIORHINUS CANICULA 0HIL 4RANS 2OY 3OC ,ONDON "
+NIGHT $0 ET AL 3PINNERETS IN lSH EXTRUDE SHEET MATERIAL WITH COMPLEX MOLECULAR ORIENTATIONS "IOMIMETICS
+NIGHT $0 AND $ &ENG &ORMATION OF THE DOGlSH EGG CAPSULE A COEXTRUDED MULTILAYER LAMINATE "IOMIMETICS
2%&%2%.#%3
+NIGHT $0 AND $ &ENG A )NTERACTION OF COLLAGEN WITH HYDROPHOBIC PROTEIN GRANULES IN THE EGG CAPSULE OF THE DOGlSH
3CYLIORHINUS CANICULA 4ISSUE #ELL
+NIGHT $0 AND $ &ENG B 3OME OBSERVATIONS ON THE COLLAGEN lBRILS OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS
CANICULA 4ISSUE #ELL
+NIGHT $0 $ &ENG AND - 3TEWART 3TRUCTURE AND FUNCTION OF THE SELACHIAN EGG CASE "IOL 2EV
+NIGHT $0 AND 3 (UNT &IBRIL STRUCTURE OF COLLAGEN IN EGG CAPSULE OF DOGlSH .ATURE
+NIGHT $0 AND 3 (UNT &INE STRUCTURE OF THE DOGlSH EGG CASE A UNIQUE COLLAGENOUS MATERIAL 4ISSUE #ELL
+NIGHT $0 AND 3 (UNT ! KINKED MOLECULAR MODEL FOR THE COLLAGEN CONTAINING lBRILS IN THE EGG CASE OF THE DOGlSH
3CYLIORHINUS CANICULA 4ISSUE #ELL
+NIGHT &- ET AL &OLLICULAR PLACENTA AND EMBRYONIC GROWTH OF THE VIVIPAROUS FOUR EYED lSH !NABLEPS * -ORPHOL
+OBAYASHI $ ET AL 3TEROIDOGENESIS IN THE OVARIAN FOLLICLES OF THE MEDAKA /RYZIAS LATIPES DURING VITELLOGENESIS AND
OOCYTE MATURATION :OOL 3CI
+OBAYASHI - ET AL $EVELOPMENT OF SENSITIVITY TO MATURATION INDUCING STEROIDS IN THE OOCYTES OF THE DAILY SPAWNING
TELEOST THE KISU 3ILLAGO JAPONICA 'EN #OMP %NDOCRINOL
+OBAYASHI 7 A %LECTRON MICROSCOPIC OBSERVATION OF THE BREAKDOWN OF CORTICAL VESICLES IN THE CHUM SALMON EGG * &AC
3CI (OKKAIDO 5NIV 3ER 6) :OOL
+OBAYASHI 7 B #OMMUNICATIONS OF OOCYTE GRANULOSA CELLS IN THE CHUM SALMON OVARY DETECTED BY TRANSMISSION ELECTRON
MICROSCOPY $EVELOP 'ROWTH $IFFER
+OBAYASHI 7 AND 43 9AMAMOTO &INE STRUCTURE OF THE MICROPYLAR APPARATUS OF THE CHUM SALMON EGG WITH A DISCUSSION
OF THE MECHANISM FOR BLOCKING POLYSPERMY * %XPER :OOL
+OBAYASHI 7 AND 43 9AMAMOTO &INE STRUCTURE OF THE MICROPYLAR CELL AND ITS CHANGE DURING OOCYTE MATURATION IN
THE CHUM SALMON /NCORHYNCHUS KETA * -ORPHOL
+OBAYASHI 7 AND 43 9AMAMOTO ,IGHT AND ELECTRON MICROSCOPIC OBSERVATIONS OF SPERM ENTRY IN THE CHUM SALMON EGG
* %XPER :OOL
+OBAYASHI 7 AND 43 9AMAMOTO &ACTORS INDUCING CLOSURE OF THE MICROPYLAR CANAL IN THE CHUM SALMON EGG * &ISH
"IOL
+OCH %! ET AL 4HE HAGlSH OOCYTE AT LATE STAGES OF OOGENESIS STRUCTURAL AND METABOLIC EVENTS AT THE MICROPYLAR REGION
4ISSUE #ELL
+OKKALA ) AND *0 7OURMS )N VIVO mUORESCENCE IMAGING OF THE FUNCTIONAL ORGANIZATION OF TROPHOTAENIAL PLACENTAL CELLS
OF GOODEID lSHES * -ORPHOL
+OOB 4* $EPOSITION AND BINDING OF CALCIUM AND MAGNESIUM IN EGG CAPSULES OF 2AJA ERINACEA -ITCHILL DURING FORMATION
AND TANNING IN UTERO #OPEIA
+OOB 4* AND )0 #ALLARD 2EPRODUCTION IN FEMALE ELASMOBRANCHS )N #OMPARATIVE 0HYSIOLOGY VOL /OGENESIS
3PERMATOGENESIS AND 2EPRODUCTION 2+( +INNE ED "ASEL +ARGER PP
+OOB 4* AND )0 #ALLARD 2EPRODUCTIVE ENDOCRINOLOGY OF FEMALE ELASMOBRANCHS LESSONS FROM THE LITTLE SKATE
2AJA ERINACEA AND SPINY DOGlSH 3QUALUS ACANTHIAS * %XPER :OOL
+OOB 4* AND $, #OX %GG CAPSULE CATECHOL OXIDASE FROM THE LITTLE SKATE 2AJA ERINACEA -ITCHILL "IOL "ULL
+OOB 4* AND $, #OX )NTRODUCTION AND OXIDATION OF CATECHOLS DURING THE FORMATION OF THE SKATE 2AJA ERINACEA
EGG CAPSULE * -ARINE "IOL !SSOC 5+
+OOB 4* AND $, #OX 3TABILIZATION AND SCLEROTIZATION OF 2AJA ERINACEA EGG CAPSULE PROTEINS %NV "IOL &ISHES
+OOB 4* AND 7# (AMLETT -ICROSCOPIC STRUCTURE OF THE GRAVID UTERUS IN THE LITTLE SKATE 2AJA ERINACEA * %XPER :OOL
+ORSGAARD " 4HE CHEMICAL COMPOSITION OF FOLLICULAR AND OVARIAN mUIDS OF THE PREGNANT BLENNY :OARCES VIVIPARUS ,
#AN * :OOL
+OSMATH ) 2! 0ATZNER AND ( !DAM 4HE STRUCTURE OF THE MICROPYLES OF THE EGGS OF -YXINE GLUTINOSA AND %PTATRETUS
BURGERI #YCLOSTOMATA :OOL !NZ
2%&%2%.#%3
+OSMATH ) 2! 0ATZNER AND ( !DAM A 2EGRESSION IM /VAR VON -YXINE GLUTINOSA , #YCLOSTOMATA ))
%LEKTRONENMIKROSKOPISCHE 5NTERSUCHUNGEN AN DEN ATRETISCHE &OLLIKELN : -IKROSK
!NAT &ORSCH
+OSMATH ) 2! 0ATZNER AND ( !DAM B 2EGRESSION IM /VAR VON -YXINE GLUTINOSA , #YCLOSTOMATA )6 (ISTOCHEMISCHE
5NTERSUCHUNGEN AN DEN ATRETISCHEN &OLLIKELN : -IKROSK
!NAT &ORSCH
+OSMATH ) 2! 0ATZNER AND ( !DAM A 2EGRESSION IM /VAR VON -YXINE GLUTINOSA , #YCLOSTOMATA ))) 5NTERSUCHUNGEN
DER &EINSTRUKTUR POST
OVULATORISCHER &OLLIKEL :OOL !NZ
+OSMATH ) 2! 0ATZNER AND ( !DAM B 2EGRESSION IM /VAR VON -YXINE GLUTINOSA , #YCLOSTOMATA 6 (ISTOCHEMISCHE
5NTERSUCHUNGEN AN DEN POST
OVULATORISCHEN &OLLIKELN :OOL !NZ
+OYA 9 4 (AMATSU AND 4 -ATSUBARA !NNUAL REPRODUCTIVE CYCLE AND SPAWNING CHARACTERISTICS OF THE FEMALE KICHIJI
ROCKlSH 3EBASTOLOBUS MACROCHIR &ISHERIES 3CI
+OYA 9 AND 4 -ATSUBARA 5LTRASTRUCTURAL OBSERVATIONS ON THE INNER OVARIAN EPITHELIA OF KICHJII ROCKlSH 3EBASTOLOBUS
MACROCHIR WITH SPECIAL REFERENCE TO THE PRODUCTION OF GELATINOUS MATERIAL SURROUNDING THE EGGS "ULL (OKKAIDO .ATL &ISH
2ES )NST
+OYA 9 ( -UNEHARA AND + 4AKANO 3ECRETION ABILITIES OF EPITHELIA OF OVARIAN WALL AND OVIGEROUS LAMELLA LINING
THE OVARIAN CAVITY OF MASKED GREENLING (EXAGRAMMOS OCTOGRAMMUS *AP * )CHTHYOL
+OYA 9 ( -UNEHARA AND + 4AKANO 3PERM STORAGE AND DEGRADATION IN THE OVARY OF A MARINE COPULATING SCULPIN
!LCICHTHYS ALCICORNIS 4ELEOSTEI 3CORPAENIFORMES ROLE OF INTERCELLULAR JUNCTIONS BETWEEN INNER OVARIAN EPITHELIAL CELLS
* -ORPHOL
+OYA 9 + 4AKANO AND ( 4AKAHASHI 5LTRASTRUCTURAL OBSERVATIONS ON SPERM PENETRATION IN THE EGG OF ELKHORN SCULPIN
!LCICHTHYS ALCICORNIS SHOWING INTERNAL GAMETIC ASSOCIATION :OOL 3CI
+OYA 9 + 4AKANO AND ( 4AKAHASHI !NNUAL CHANGES IN lNE STRUCTURE OF INNER EPITHELIAL LINING OF THE OVARY OF A MARINE
SCULPIN !LCICHTHYS ALCICORNIS 4ELEOSTEI 3CORPAENIFORMES WITH INTERNAL GAMETIC ASSOCIATION * -ORPHOL
+RAJHANZL ! 6 (OREJSI AND * +OCOUREK A 3TUDIES ON LECTINS 8,) )SOLATION AND CHARACTERIZATION OF A BLOOD GROUP "
SPECIlC LECTIN FROM THE ROE OF THE POWAN #OREGONUS LAVARETUS MARAENA "IOCHIM "IOPHYS !CTA
+RAJHANZL ! 6 (OREJSI AND * +OCOUREK B 3TUDIES ON LECTINS 8,)) )SOLATION PARTIAL CHARACTERIZATION AND COMPARISON
OF LECTINS FROM THE ROE OF lVE lSH SPECIES "IOCHIM "IOPHYS !CTA
+RAJHANZL ! ET AL A $IRECT VISUALIZATION OF ENDOGENOUS LECTINS IN lSH OOCYTES BY GLYCOSYLATED mUORESCENT CYTOCHEMICAL
MARKERS (ISTOCHEM *
+RAJHANZL ! ET AL B !N IMMUNOmUORESCENCE STUDY ON THE OCCURRENCE OF ENDOGENOUS LECTINS IN THE DIFFERENTIATING OOCYTES
OF SILVER CARP (YPOPHTHALMICHTHYS MOLITRIX 6ALENC AND TENCH 4INCA TINCA , (ISTOCHEM *
+RISTOFFERSSON 2 3 "ROBERG AND - 0EKKARINEN (ISTOLOGY AND PHYSIOLOGY OF EMBRYOTROPHE FORMATION EMBRYONIC
NUTRITION AND GROWTH IN THE EEL
POUT :OARCES VIVIPARUS , !NN :OOL &ENN
+UCHNOW +0 AND *2 3COTT 5LTRASTRUCTURE OF THE CHORION AND ITS MICROPYLE APPARATUS IN THE MATURE &UNDULUS HETEROCLI
TUS 7ALBAUM OVUM * &ISH "IOL
+UDO 3 5LTRASTRUCTURAL OBSERVATIONS ON THE DISCHARGE OF TWO KINDS OF GRANULES IN FERTILIZED EGGS OF #YPRINUS CARPIO AND
#ARASSIUS AURATUS $EVELOP 'ROWTH $IFFER
+UDO 3 %NZYMO
CYTOCHEMICAL OBSERVATIONS ON THE CORTICAL CHANGE IN THE EGGS OF #YPRINUS CARPIO AND #ARASSIUS AURATUS
$EVELOP 'ROWTH $IFFER
+UDO 3 3PERM PENETRATION AND THE FORMATION OF A FERTILIZATION CONE IN THE COMMON CARP EGG $EVELOP 'ROWTH $IFFER
+UDO 3 5LTRASTRUCTURE AND ULTRACYTOCHEMISTRY OF THE FERTILIZATION ENVELOPE FORMATION IN THE CARP EGG $EVELOP 'ROWTH
$IFFER
+UDO 3 %NZYMATIC BASIS FOR PROTECTION OF lSH EMBRYOS BY THE FERTILIZATION ENVELOPE %XPERIENTIA
+UDO 3 A 5LTRACYTOCHEMICAL MODIlCATIONS OF SURFACE CARBOHYDRATES IN FERTILIZED EGGS OF THE COMMON CARP $EV 'ROWTH
$IFFER
+UDO 3 B 2ESPONSE TO SPERM PENETRATION OF THE CORTEX OF EGGS OF THE lSH 0LECOGLOSSUS ALTIVELIS $EV 'ROWTH $IFFER
+UDO 3 A 2OLE OF SPERM HEAD SYNDECAN AT FERTILIZATION IN lSH * %XPER :OOL
+UDO 3 B 0RESENCE OF PROTEINASE INHIBITOR IN THE VITELLINE ENVELOPE AND ITS ROLE IN EGGS OF THE lSH 4RIBOLODON HAKONENSIS
* %XPER :OOL
2%&%2%.#%3
+UDO 3 C 4HROMBIN INDUCES ASSEMBLY IN VITRO OF VITELLINE ENVELOPE COMPONENTS OF COMMON CARP EGGS * %XPER :OOL
+UDO 3 AND - )NOUE ! BACTERICIDAL EFFECT OF FERTILIZATION ENVELOPE EXTRACT FROM lSH EGGS :OOL 3CI
+UDO 3 AND - )NOUE "ACTERIAL ACTION OF FERTILIZATION ENVELOPE EXTRACT FROM EGGS OF THE lSH #YPRINUS CARPIO AND
0LECOGLOSSUS ALTIVELIS * %XPER :OOL
+UDO 3 AND - )NOUE %NZYME ACTIVITIES RESPONSIBLE FOR THE DEFENSE MECHANISM OF THE FERTILIZATION ENVELOPE
.ATURWISSENSCHAFTEN
+UDO 3 AND ! 3ATO &ERTILIZATION CONE OF CARP EGGS AS REVEALED BY SCANNING ELECTRON MICROSCOPY $EVELOP 'ROWTH
$IFFER
+UDO 3 ! 3ATO AND - )NOUE #HORIONIC PEROXIDASE ACTIVITY IN EGGS OF THE lSH 4RIBOLODON HAKONENSIS * %XPER :OOL
+UDO 3 AND # 4ESHIMA %NZYME ACTIVITIES AND ANTIFUNGAL ACTION OF FERTILIZATION ENVELOPE EXTRACT FROM lSH EGGS * %XPER
:OOL
+UDO 3 AND # 4ESHIMA !SSEMBLY IN VITRO OF VITELLINE ENVELOPE COMPONENTS INDUCED BY A CORTICAL ALVEOLUS SIALOGLYCO
PROTEIN OF EGGS OF THE lSH 4RIBOLODON KAKONENSIS :YGOTE
+UDO 3 AND 3 9AZAWA "INDING OF BACTERIAL TOXINS TO GLYCOPROTEINS IN THE ENVELOPES OF RAINBOW TROUT EGGS (ISTOCHEM
*
,AHNSTEINER & 4 7EISMANN AND 2! 0ATZNER #OMPOSITION OF THE OVARIAN mUID IN SALMONID SPECIES /NCORHYNCHUS
MYKISS 3ALMO TRUTTA LACUSTRIS 3ALVELINUS ALPINUS AND (UCHO HUCHO 2EPROD .UTR $EV
,AHNSTEINER & 4 7EISMANN AND 2! 0ATZNER 3TRUCTURE AND FUNCTION OF THE OVARIAN CAVITY AND OVIDUCT AND COMPOSITION
OF THE OVARIAN mUID IN THE BLEAK !LBURNUS ALBURNUS 4ELEOSTEI #YPRINIDAE 4ISSUE #ELL
,AMBERT *'$ ,OCATION OF HORMONE PRODUCTION IN THE OVARY OF THE GUPPY 0OECILIA RETICULATA %XPERIENTIA
,AMBERT *'$ A 4HE OVARY OF THE GUPPY 0OECILIA RETICULATA 4HE GRANULOSA CELLS AS SITES OF STEROID BIOSYNTHESIS 'EN
#OMP %NDOCRINOL
,AMBERT *'$ B 4HE OVARY OF THE GUPPY 0OECILIA RETICULATA 4HE ATRETIC FOLLICLE A CORPUS ATRETICUM OR A CORPUS LUTEUM
PRAEOVULATIONIS : :ELLFORSCH -IKROSK !NAT
,AMBERT *'$ AND 0'7* VAN /ORDT 0REOVULATORY CORPORA LUTEA OR CORPORA ATRETICA IN THE GUPPY 0OECILIA RETICULATA
! HISTOLOGICAL AND HISTOCHEMICAL STUDY 'EN #OMP %NDOCRINOL n
,ANCE 6 AND )0 #ALLARD ! HISTOCHEMICAL STUDY OF OVARIAN FUNCTION IN THE OVOVIVIPAROUS ELASMOBRANCH 3QUALUS ACAN
THIAS 'EN #OMP %NDOCRINOL
,ANG ) A %LECTRON MICROSCOPIC AND HISTOCHEMICAL STUDY OF THE POSTOVULATORY FOLLICLES OF 0ERCA mUVIATILIS , 4ELEOSTEI
'EN #OMP %NDOCRINOL
,ANG ) B %LECTRON MICROSCOPIC AND HISTOCHEMICAL INVESTIGATIONS OF THE ATRETIC OOCYTE OF 0ERCA mUVIATILIS , 4ELEOSTEI
#ELL 4ISSUE 2ES
,ANGE 2( !RE YOLK PHOSVITINS CARRIERS FOR SPECIlC CATIONS #OMPARATIVE MICROANALYSIS IN VERTEBRATE YOLK PLATELETS
: .ATURFORSCH C
,ANGE 2( 4HE LIPOPROTEIN CRYSTALS OF CYCLOSTOME YOLK PLATELETS -YXINE GLUTINOSA , ,AMPETRA PLANERI ;"LOCH=
, mUVIATILIS ;,= * 5LTRASTRUCT 2ES
,ANGE 2( ET AL ,IPOVITELLIN
PHOSVITIN CRYSTALS WITH ORTHORHOMBIC FEATURES THIN
SECTION ELECTRON MICROSCOPY GEL
ELECTROPHORESIS AND MICROANALYSIS IN TELEOST AND AMPHIBIAN YOLK PLATELETS AND A COMPARISON WITH OTHER VERTEBRATES
* 5LTRASTRUCT 2ES
,ANGE 2( : 'RODZINSKI AND 7 +ILARSKI 9OLK
PLATELET CRYSTALS IN THREE ANCIENT BONY lSHES 0OLYPTERUS BICHIR
0OLYPTERI !MIA CALVA , AND ,EPISOSTEUS OSSEUS , (OLOSTEI #ELL 4ISSUE 2ES
,ANGE 2( AND (
0 2ICHTER ! SYMMETRIC LIPOVITELLIN
PHOSVITIN DIMER IN CYCLOSTOME YOLK PLATELET CRYSTALS STRUCTURAL
AND BIOCHEMICAL OBSERVATIONS * -OLEC "IOL
,ARSEN ,/ 4HE LAMPREY EGG AT OVULATION ,AMPETRA mUVIATILIS , 'RAY "IOL 2EPROD
,ARSSON $'* 3* (YLLNER AND # (AUX )NDUCTION OF VITELLINE ENVELOPE PROTEINS BY OESTRADIOL
` IN TELEOST
SPECIES 'EN #OMP %NDOCRINOL
,EHRI '+ #YCLICAL CHANGES IN THE OVARY OF THE CATlSH #LARIAS BATRACHUS ,INN !CTA !NAT
2%&%2%.#%3
,EPORI .' 3EX DIFFERENTIATION HERMAPHRODITISM AND INTERSEXUALITY IN VERTEBRATES INCLUDING MAN 0ADUA 0ICCIN -EDICAL
"OOKS PP
,ESSMAN #! -ETABOLISM OF PROGESTOGENS DURING IN VITRO MEIOTIC MATURATION OF FOLLICLE ENCLOSED OOCYTES OF THE GOLDlSH
#ARASSIUS AURATUS * %XPER :OOL
,EVAVI :ERMONSKY " AND : 9ARON #HANGES IN GONADOTROPIN AND OVARIAN STEROIDS ASSOCIATED WITH OOCYTES MATURATION
DURING SPAWNING INDUCTION IN THE CARP 'EN #OMP %NDOCRINOL
,EWIS *# AND $" -C-ILLAN 4HE DEVELOPMENT OF THE OVARY OF THE SEA LAMPREY 0ETROMYZON MARINUS , * -ORPHOL
,I 9( ## 7U AND *3 9ANG #OMPARATIVE ULTRASTRUCTURAL STUDIES OF THE ZONA RADIATA OF MARINE lSH EGGS IN THREE GENERA
IN 0ERCIFORMES * &ISH "IOL
,INHART / AND 3 +UDO 3URFACE ULTRASTRUCTURE OF PADDLElSH EGGS BEFORE AND AFTER FERTILIZATION * &ISH "IOL
,IVNI . /VARIAN HISTOCHEMISTRY OF THE lSHES #YPRINUS CARPIO -UGIL CAPITO AND 4ILAPIA AUREA 4ELEOSTEI (ISTOCHEM
*
,OMBARDI * AND 4 &ILES %GG CAPSULE STRUCTURE AND PERMEABILITY IN THE VIVIPAROUS SHARK -USTELUS CANIS * %XPER :OOL
,OMBARDI * AND *0 7OURMS A 4HE TROPHOTAENIAL PLACENTA OF A VIVIPAROUS GOODEID lSH ) 5LTRASTRUCTURE OF THE INTERNAL
OVARIAN EPITHELIUM THE MATERNAL COMPONENT * -ORPHOL
,OMBARDI * AND *0 7OURMS B 4HE TROPHOTAENIAL PLACENTA OF A VIVIPAROUS GOODEID lSH )) 5LTRASTRUCTURE OF TROPHOTAE
NIAE THE EMBRYONIC COMPONENT * -ORPHOL
,OMBARDI * AND *0 7OURMS C 4HE TROPHOTAENIAL PLACENTA OF A VIVIPAROUS GOODEID lSH ))) 0ROTEIN UPTAKE BY TROPHOTAE
NIAE THE EMBRYONIC COMPONENT * %XPER :OOL
,NNING 3 #OMPARATIVE ELECTRON MICROSCOPIC STUDIES OF TELEOSTEAN EGGS WITH SPECIAL REFERENCE TO THE CHORION 3ARSIA
,NNING 3 AND * $AVENPORT 4HE SWELLING EGG OF THE LONG ROUGH DAB (IPPOGLOSSOIDES PLATESSOIDES LIMANDOIDES "LOCH
* &ISH "IOL
,NNING 3 % +JRSVIK AND * $AVENPORT 4HE HARDENING PROCESS OF THE EGG CHORION OF THE COD 'ADUS MORHUA , AND
LUMPSUCKER #YCLOPTERUS LUMPUS , * &ISH "IOL
,NNING 3 % +JRSVIK AND ) " &ALK 0ETERSEN ! COMPARATIVE STUDY OF PELAGIC AND DEMERSAL EGGS FROM COMMON MARINE
lSHES IN NORTHERN .ORWAY 3ARSIA
,OUREIRO - AND 2/ DE 3 %XTERNAL MORPHOLOGY OF THE CHORION OF THE ANNUAL lSHES #YNOLEBIAS #YPRINODONTIFORMES
2IVULIDAE #OPEIA
,UPO DI 0RISCO # "IOSINTESI DI ORMONI STEROIDI NELLOVARIO DI DUE SPECIE DI SELACI 3CYLIORHINUS STELLARIS OVIPARO
E 4ORPEDO MARMORATA OVOVIVIPARO 2IV "IOL ;CITED BY #HIEFl "ACCARI ET AL =
,YNGNES 2 "EITRGE ZUR +ENNTNIS VON -YXINE GLUTINOSA , ) BER DIE %NTWICKLUNG DER %IHLLE BEI -YXINE GLUTINOSA
: -ORPHOL KOL D 4IERE
,YGNES 2 BER ATRETISCHE UND HYPERTROPHISCHE 'EBILDE IM /VARIUM DER -YXINE GLUTINOSA , "IOLOGISCHES :ENTRALBLATT
-ANNING !* AND ,7 #RIM -ATERNAL AND INTERANNUAL COMPARISON OF THE OVULATORY PERIODICITY EGG PRODUCTION AND EGG
QUALITY OF THE BATCH SPAWNING YELLOWTAIL mOUNDER * &ISH "IOL
-ANWELL # &ETAL AND ADULT HEMOGLOBINS OF THE SPINY DOGlSH 3QUALUS SUCKLEYI !RCH "IOCHEM "IOPHYS
-ASUDA + ) )UCHI AND + 9AMAGAMI !NALYSIS OF HARDENING OF THE EGG ENVELOPE CHORION OF THE lSH /RYZIAS LATIPES
$EVELOP 'ROWTH $IFFER
-ATSUYAMA - 9 .AGAHAMA AND 3 -ATSUURA /BSERVATIONS ON OVARIAN FOLLICLE ULTRASTRUCTURE IN THE MARINE TELEOST
0AGRUS MAJOR DURING VITELLOGENESIS AND OOCYTE MATURATION !QUACULTURE
-ATTHEWS ,( 2EPRODUCTION IN THE BASKING SHARK #ETORHINUS MAXIMUS 'UNNER 0HIL 4RANS 2OY 3OC ,ONDON
3ER "
-AYER ) 3% 3HACKLEY AND *3 2YLAND !SPECTS OF THE REPRODUCTIVE BIOLOGY OF THE BASS $ICENTRARCHUS LABRAX , )
!N HISTOLOGICAL AND HISTOCHEMICAL STUDY OF OOCYTE DEVELOPMENT * &ISH "IOL
2%&%2%.#%3
-EISNER !$ ET AL -ORPHOLOGY AND HISTOLOGY OF THE MALE REPRODUCTIVE SYSTEM IN TWO SPECIES OF INTERNALLY INSEMI
NATING 3OUTH !MERICAN CATlSHES 4RACHELYOPTERUS LUCENAI AND 4 GALEATUS 4ELEOSTEI !UCHENIPTERIDAE * -ORPHOL
-EISNER !$ AND *2 "URNS 6IVIPARITY IN THE HALFBEAK 'ENERA $ERMOGENYS AND .OMORHAMPHUS 4ELEOSTEI
(EMIRAMPHIDAE * -ORPHOL
-ENDOZA ' 4HE lN FOLD OF 'OODEA LUITPOLDII A VIVIPAROUS CYPRINODONT TELEOST * -ORPHOL
-ENDOZA ' 4HE lNE STRUCTURE OF AN ABSORPTIVE EPITHELIUM IN A VIVIPAROUS TELEOST * -ORPHOL
-ERSON 22 ET AL /OCYTE DEVELOPMENT IN SUMMER mOUNDER SEASONAL CHANGES AND STEROID CORRELATES * &ISH "IOL
-ETTEN ( 3TUDIES ON THE REPRODUCTION OF THE DOGlSH 0HIL 4RANS 2OY 3OC ,ONDON "
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:OOL !NZ
0ARMENTIER (+ *'- VAN DEN "OOGAART AND ,0- 4IMMERMANS 0HYSIOLOGICAL COMPARTMENTATION IN GONADAL TISSUE
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2IEHL 2 AND - +OKOSCHA ! UNIQUE SURFACE PATTERN AND MICROPYLAR APPARATUS IN THE EGGS OF ,UCIOCEPHALUS SP
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2USAOUN - 4HE DOGlSH SHELL GLAND A HISTOCHEMICAL STUDY * %XPER -ARINE %COL
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LA 2OUSSETTE MATURIT !RCH D!NAT -ICROSC
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/STEICHTHYES 3ALMONIDAE #OMP "IOCHEM 0HYSIOL "
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3CHINDLER *& AND 5 DE6RIES A 5LTRASTRUCTURE OF EMBRYONIC ANAL PROCESSES ON 'IRARDINICHTHYS VIVIPARUS
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3CHROEDER 0# AND 0 0ENDERGRASS 4HE INHIBITION OF IN VITRO OVULATION FROM FOLLICLES OF THE TELEOST /RYZIAS LATIPES
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3COTT !0 AND !6- #ANARIO 3TATUS OF OOCYTE MATURATION INDUCING STEROIDS )N 0ROCEEDINGS OF THE 4HIRD )NTERNATIONAL
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3ELMAN + ET AL 3TAGES OF OOCYTE DEVELOPMENT IN THE ZEBRAlSH "RACHYDANIO RERIO * -ORPHOL
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3ELMAN + AND 2! 7ALLACE 2EVIEW #ELLULAR ASPECTS OF OOCYTE GROWTH IN TELEOSTS :OOL 3CI
3ELMAN + 2! 7ALLACE AND 6 "ARR /OGENESIS IN &UNDULUS HETEROCLITUS )6 9OLK VESICLE FORMATION * %XPER :OOL
3ELMAN + 2! 7ALLACE AND 6 "ARR /OGENESIS IN &UNDULUS HETEROCLITUS 6 4HE RELATIONSHIP OF YOLK VESICLES AND
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3HACKLEY 3% AND 0% +ING ,IPID YOLK SYNTHESIS IN A MARINE TELEOST "LENNIUS PHOLIS , #ELL 4ISSUE 2ES
3HELTON 7, &ATE OF THE FOLLICULAR EPITHELIUM IN $OROSOMA PETENENSE 0ISCES #LUPEIDAE #OPEIA
3HRIVASTAVA 33 &ORMATION OF THE CORPORA ATRETICA IN .OTOPTERUS NOTOPTERUS 0ALLAS !CTA :OOL 3TOCKH
3MITH #, AND 32 (ALEY %VIDENCE OF STEROIDOGENESIS IN POSTOVULATORY FOLLICLES OF THE TILAPIA /REOCHROMIS MOSSAM
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ACTIVATION OF EGGS
ADELPHOPHAGY
ADHESIVE APPARATUS
ADHESIVE CELLS AUTOLYSIS
ADHESIVE CELLS LAMPREY FOLLICLE
ADHESIVE COAT LAMPREY EGG
ADHESIVE COAT SHEATlSH
ADHESIVE DISC BLENNY EGG
ADHESIVE lLAMENTS
ADHESIVE SACCULES LAMPREY
AEQUORIN
AGE PIGMENT LIPOFUSCIN
).$%8
ATTACHMENT DISC
ATTACHMENT lLAMENTS GOBY
ATTACHMENT SITE SHARK PLACENTA
AUTOLYSIS THECA IN OVULATION LAMPREY
AUTONOMIC NERVES OVARY
AUTOSYNTHETIC ORIGIN OF YOLK PROTEINS
"
BAFmE PLATES OVIDUCTAL GLAND ELASMOBRANCH
BAFmE ZONE OVIDUCTAL GLAND ELASMOBRANCH
"ALBIANI BODY
BARRIER TO GASEOUS EXCHANGE APLACENTAL YOLK SAC VIVI
PARITY
BARRIER TO UTERINE TRANSPORT
BARRIER BLOODLUMINAL LUMINAL GESTATION
BARRIER BLOOD
FOLLICULAR
BARRIERS TO EXCHANGE OF NUTRIENTS
BATCH SPAWNER
BLOCK TO POLYSPERMY
BLOOD
EMBRYOTROPH PATHWAY IN LUMINAL GESTATION
BLOOD
FOLLICULAR BARRIER
BRANCHIAL PLACENTA
BREAKDOWN OF THE GERMINAL VESICLE
BUCCAL PLACENTA
BUCCOPHARYNGEAL TISSUES ABSORPTION IN VIVIPARITY
BUOYANCY
#
# STEROIDS
#! GRANULES
#A INmUX
CANDLE VIVIPAROUS ELASMOBRANCH
CANNIBALISM IN LAMNOID SHARKS
CAPSULE HAGlSH EGG
CAPSULE
WALL FORMING REGION OVIDUCTAL GLAND ELASMO
BRANCH
CEMENT
CERVIX ELASMOBRANCH
CHEMOATTRACTANT
CHLORIDE CELLS IN ABSORPTIVE EPITHELIA
CHORION
CHORION ATTENUATION
CHORION lLAMENTS
CHORION FORMATION
CHORION HAGlSH
CHORION HARDENING
CHORION LAMELLAE
CHORION LAYERING
CHORION SURFACE PATTERNS
CHORION TELEOST
CHORION VARIATIONS
CHORION VIVIPAROUS lSH
CHORIONS ANALYSIS OF HOMOGENATES
CHROMATIN IN ATRESIA
CHROMATIN NUCLEOLUS PHASE
CHROMOSOMES TETRAD
CIRCUMNUCLEAR RING
CLEAVAGE FOLLICULAR TELEOST
CLEFT OF PENETRATION
CLOACA CYCLOSTOME
CLUB ZONE OVIDUCTAL GLAND ELASMOBRANCH
COATED PITS IN OOLEMMA
COATED VESICLES IN OOLEMMA
COELOMIC mUID
COELOMIC SAC IN LUMINAL GESTATION
COELOMIC SAC ABSORPTION IN VIVIPARITY
COLLAGEN IN POSTOVULATORY FOLLICLES
COLLOID OSMOTIC PRESSURE
COMPARTMENTS IN LUMINAL GESTATION
CONTRACTIONS THECA
COPULATION
COPULATION ELASMOBRANCH
CORPORA ATRETICA
CORPORA ATRETICA ELASMOBRANCH
CORPORA LUTEA DEGENERATION
CORPORA LUTEA ELASMOBRANCH
CORPUS LUTEUM
CORPUS LUTEUM OF ATRESIA
CORPUS LUTEUM DISAPPEARANCE
CORPUS LUTEUM FORMATION
CORTEX GONADAL
CORTEX OVARY
CORTICAL ALVEOL IN EARLY VITELLOGENESIS
CORTICAL ALVEOLI
CORTICAL ALVEOLI IN ATRESIA
CORTICAL ALVEOLI OF ANIMAL POLE
CORTICAL ALVEOLI OF VEGETAL POLE
CORTICAL ALVEOLI COMPOSITION
CORTICAL ALVEOLI EXPULSION
CORTICAL ALVEOLI EXTRUSION
CORTICAL ALVEOLI GRADIENT
CORTICAL ALVEOLI LIMITING MEMBRANE
CORTICAL ALVEOLI REMNANTS
CORTICAL ALVEOLI STRUCTURE
CORTICAL ALVEOLUS STAGE
CORTICAL ENDOPLASMIC RETICULUM
CORTICAL OOPLASM
CORTICAL REACTION
CORTICAL REACTION TRIGGER
CORTICAL VESICLES EXOCYTOSIS
CRYSTALS IN YOLK GRANULES
CYSTOVARIAN OVARY TELEOST
CYTOCHALASIN "
CYTOPLASMIC BRIDGES
CYTOPLASMIC CONTINUITY
CYTOSKELETON
CYTOSKELETON IN OVULATION
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DAY LENGTH AND OVULATION
DElNITIVE FOLLICLE
DEGENERATING FOLLICLES ELASMOBRANCH
DELLE IN TELEOST FOLLICLE
DENSE CORED GRANULES
DEPOLARIZATION OF OOLEMMA
DESMOSOMES
DESMOSOMES PERITONEAL CELLS
DESMOSOMES RUDIMENTARY
DEVELOPING FOLLICLES ELASMOBRANCH
DEVELOPING FOLLICLES SEQUENTIAL ARRAY
DEVELOPMENT FOLLICULAR TELEOST
DIFFERENTIATION GONADAL
DIPLOTENE OOCYTES
$.! REPLICATION
DUCT OVIDUCTAL GLAND ELASMOBRANCH
DUCTUS VITELLO INTESTINALIS
%
EGG ACTIVATION
EGG CAPSULE IN SHARK PLACENTA
EGG CAPSULE IN VIVIPARITY ELASMOBRANCH
EGG CAPSULE WALL ELASMOBRANCH COMPOSITION
EGG CAPSULE ABSENCE IN BLUE SHARK
EGG CAPSULE ELASMOBRANCH
EGG CAPSULE ELASMOBRANCH LAYERS
EGG CAPSULE TANNING ELASMOBRANCH
EGG CAPSULE VIVIPAROUS SHARK
EGG CASE
EGG ENVELOPE IN FOLLICULAR GESTATION
EGG MEMBRANE IN FOLLICULAR GESTATION
EGG TRANSPORT
ELECTRON LUCENT LAYER :
EMBRYOTROPH
EMBRYOTROPH IN LUMINAL GESTATION
EMBRYOTROPH OSMOLARITY
EMBRYOTROPH TELEOST
EMBRYOTROPH UPTAKE
ENDOCYTOSIS
ENDOCYTOSIS IN LUMINAL GESTATION
).$%8
ENDOCYTOSIS IN TROPHOTAENIAL CELLS
ENDOCYTOSIS OF VITELLOGENIN
ENDOCYTOTIC VESICLES
ENDODERMAL EPITHELIUM SHARK
ENDOPLASMIC RETICULUM AGRANULAR
ENDOTHELIAL CELLS OF FOLLICULAR CAPILLARIES
ENDOTHELIAL CELLS OF LYMPH SPACES
ENDOTHELIAL CELLS CICHLID FOLLICLE
ENDOVARIAN CAVITY
ENLARGEMENT OF OOCYTES
ENTEROENDOCRINE CELLS
ENVELOPE IN VIVIPAROUS POECILIIDS
ENVELOPE PROTEINS IN PLASMA
ENVELOPE LAMPREY
ENVELOPE STURGEON
ENVELOPE SECONDARY
ENVELOPES
ENVELOPES FOLLICULAR
EPIGONAL ORGANS ELASMOBRANCH
EPITHELIUM OVARIAN LUMINAL
EXOCYTOSIS
EXOCYTOSIS OF CORTICAL VESICLES
EXOCYTOSIS CORTICAL REACTION
EXOCYTOSIS DEPOSITION OF SECONDARY ENVELOPE
EXOCYTOSIS DEPOSITION OF ZONA PELLUCIDA
EXOGENOUS NUTRIENTS UPTAKE
EXOGENOUSLY DERIVED YOLK PROTEIN PRECURSORS
EXPULSION OF EGG
EXTERNAL GILL lLAMENTS IN SHARK EMBRYOS
EXTRAEMBRYONIC COELOM
EXTRAVASCULAR SPACES FOLLICLE
&
FEMALE
SPECIlC SERUM PROTEIN
FERTILIZATION
FERTILIZATION CONE
FERTILIZATION EARLY STAGES
FERTILIZATION INTERNAL
FERTILIZATION INTERNAL ELASMOBRANCH
FERTILIZATION INTERNAL TELEOST
FERTILIZATION INTRAFOLLICULAR
FERTILIZATION LAMPREY
FERTILIZATION TELEOST
lBROUS TUFT LAMPREY
lLAMENTS MEDAKA EGG
lRST POLAR BODY
mUID OF OVULATION LAMPREY
mUID YOLK
FOETAL YOLK SAC BLUE SHARK
FOLLICLE FORMATION
).$%8
FOLLICLE OVARIAN
FOLLICULAR CELL MICROVILLI WITHDRAWAL
FOLLICULAR CELLS
FOLLICULAR CELLS AND MICROPYLAR CANAL
FOLLICULAR CELLS IN ATRESIA
FOLLICULAR CELLS IN AXIS FORMATION
FOLLICULAR CELLS IN ENVELOPE FORMATION
FOLLICULAR CELLS IN GESTATION
FOLLICULAR CELLS IN MACROMOLECULAR UPTAKE
FOLLICULAR CELLS IN MATROTROPHIC TELEOST
FOLLICULAR CELLS IN OVULATION
FOLLICULAR CELLS IN OVULATION LAMPREY
FOLLICULAR CELLS IN POSTOVULATORY FOLLICLES
FOLLICULAR CELLS IN POSTOVULATORY FOLLICLES HAGlSH
FOLLICULAR CELLS IN YOLK UPTAKE LAMPREY
FOLLICULAR CELLS CONTRACTIONS
FOLLICULAR CELLS ELASMOBRANCH
FOLLICULAR CELLS ENVELOPE FORMATION
FOLLICULAR CELLS FUNCTIONS
FOLLICULAR CELLS 'OLGI COMPLEX
FOLLICULAR CELLS HORMONES
FOLLICULAR CELLS HYPERTROPHY
FOLLICULAR CELLS INTERCELLULAR SPACES
FOLLICULAR CELLS INVASIVE
FOLLICULAR CELLS LAMPREY
FOLLICULAR CELLS LYSOSOMES
FOLLICULAR CELLS MECHANICAL FUNCTION
FOLLICULAR CELLS MICROPYLE HAGlSH
FOLLICULAR CELLS ORGANELLES
FOLLICULAR CELLS ORIGIN
FOLLICULAR CELLS PASSAGE OF MATERIALS
FOLLICULAR CELLS PHAGOCYTOSIS IN ATRESIA
FOLLICULAR CELLS POLARITY
FOLLICULAR CELLS REGRESSION
FOLLICULAR CELLS SEA BASS
FOLLICULAR CELLS SECONDARY ENVELOPE
FOLLICULAR CELLS STEROIDOGENESIS
FOLLICULAR DEVELOPMENT TELEOST
FOLLICULAR ENVELOPES
FOLLICULAR EPITHELIUM
FOLLICULAR EPITHELIUM IN CHORION FORMATION
FOLLICULAR EPITHELIUM IN FOLLICULAR GESTATION
FOLLICULAR EPITHELIUM IN MATROTROPHIC NUTRITION
FOLLICULAR EPITHELIUM IN NUTRIENT TRANSFER
FOLLICULAR EPITHELIUM IN OVULATION
FOLLICULAR EPITHELIUM IN POSTOVULATORY FOLLICLES
FOLLICULAR EPITHELIUM BARRIER
FOLLICULAR EPITHELIUM BASEMENT MEMBRANE
FOLLICULAR EPITHELIUM CICHLID
FOLLICULAR EPITHELIUM DOGlSH
FOLLICULAR EPITHELIUM ELASMOBRANCH
FOLLICULAR EPITHELIUM GUPPY PLACENTA
FOLLICULAR EPITHELIUM HAGlSH
FOLLICULAR EPITHELIUM HYPERTROPHY
FOLLICULAR EPITHELIUM LAMPREY
FOLLICULAR EPITHELIUM LIPID CELLS
FOLLICULAR EPITHELIUM ORIGIN
FOLLICULAR EPITHELIUM PASSAGE OF MATERIALS
FOLLICULAR EPITHELIUM PREOVULATORY CHANGES LAMPREY
FOLLICULAR EPITHELIUM RAY INTERCELLULAR JUNCTIONS
FOLLICULAR EPITHELIUM SEA BASS INTERCELLULAR JUNCTIONS
FOLLICULAR EPITHELIUM STRATIlED RAY
FOLLICULAR EPITHELIUM TELEOST
FOLLICULAR GESTATION
FOLLICULAR LAMINA SYNGNATHID OVARY
FOLLICULAR LIGAMENT HAGlSH
FOLLICULAR PLACENTA
FOLLICULAR PLACENTA POECILIID
FOLLICULAR RUPTURE LAMPREY
FOLLICULAR STEROIDOGENESIS
FOLLICULAR STEROIDOGENESIS ELASMOBRANCH
FOLLICULAR THECA
FOLLICULOGENESIS
FOLLICULOGENESIS ELASMOBRANCH
FUSION OF YOLK DROPLETS
'
GAP JUNCTIONS
GAP JUNCTIONS IN FOLLICULAR CAPILLARIES
GAP JUNCTIONS MESOTHELIAL CELLS
GELATINOUS MASS 3CORPAENIFORMES
GENITAL PORE CYCLOSTOME
GENITAL PORE TELEOST
GENITAL RIDGE
GENITAL SYSTEMS ORIGIN
GENTIAL PORE !GNATHA
GERM CELL NESTS LAMPREY
GERMINAL DENSE BODIES
GERMINAL EPITHELIUM
GERMINAL RIDGE
GERMINAL RIDGE HAGlSH
GERMINAL RIDGE SYNGNATHID OVARY
GERMINAL VESICLE
GERMINAL VESICLE BREAKDOWN
GERMINAL VESICLE IN VITELLOGENESIS
GERMINAL VESICLE BREAKDOWN
GERMINAL VESICLE MIGRATION
).$%8
GESTATION IN MATROTROPHIC TELEOST
GESTATION !NABLEPS
GESTATION ELASMOBRANCH
GESTATION FOLLICULAR
GESTATION LUMINAL
GESTATION SHARK
GESTATION TELEOST
GILLS ABSORPTION IN VIVIPARITY
GONADAL ANLAGE
GONADAL DIFFERENTIATION
GONADAL EPITHELIUM
GONADAL EPITHELIUM ELASMOBRANCH
GONADAL PRIMORDIA
GONADAL RIDGE
GONADOSOMATIC INDEX
GONADOTROPIN
GONADOTROPIN RECEPTORS
GONODUCT TELEOST
GONOPODIUM
GRADIENT OF CORTICAL ALVEOLI
GRANULOSA CELLS
GROUP
SYNCHRONOUS OVARIES
GROWTH OF OOCYTES
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GYMNOVARIAN OVARY TELEOST
HYDROLYSIS OF YOLK PROTEINS
HYOSOPHORIN
HYOSOPHORINASE
HYPERTROPHY OF FOLLICULAR CELLS IN POSTOVULATORY FOL
LICLES
(
HAEMATROPHIC EXCHANGE PLACENTAL
HAEMATROPHIC NUTRITION PLACENTAL SHARKS
HAEMATROPHIC PLACENTA ELASMOBRANCH
HAEMATROPHIC TRANSFER SHARK PLACENTA
HAEMOPOIETIC TISSUE ELASMOBRANCH
HARDENING CHORION
HATCHING
HATCHING ENZYME
HEAD lLAMENT LAMPREY SPERM
HEPATOSOMATIC INDEX
HERMAPHRODITISM
HETEROSYNTHETIC ORIGIN OF YOLK PROTEINS
(
HYOSOPHORIN
HISTOTROPH
HONEYCOMB CELL HAGlSH
HORMONE PRODUCTION IN POSTOVULATORY FOLLICLES
HORMONE SYNTHESIS TWO
CELL MODEL
HORMONE PITUITARY
HORMONES
HORMONES OF OVARIAN FOLLICLES
HUMAN CHORIONIC GONADOTROPIN
HYDRATION OF OOCYTE
HYDROCORTISONE
*
JELLY COAT
JUNCTIONAL COMPLEXES
JUNCTIONAL TYPES IN FOLLICULAR EPITHELIUM
JUXTANUCLEAR COMPLEX
JUXTANUCLEAR COMPLEX FUNCTION
)
IMMUNOLOGICAL BARRIER FOLLICULAR GESTATION
IMMUNOLOGICAL BARRIER OVIDUCT TELEOST
IMPLANTATION SHARK
INDUCED OVULATION
INSEMINATION
INTERCELLULAR BRIDGES
INTERCELLULAR BRIDGES FOLLICULAR EPITHELIUM RAY
INTERCELLULAR PASSAGE FOLLICULAR EPITHELIUM
INTERCELLULAR SPACES TROPHOTAENIAL EPITHELIUM
INTERNAL GAMETIC ASSOCIATION
INTERSEXUALITY
INTERSTITIAL CELLS OF THE OVARY
INTERSTITIAL GLAND CELLS
INTERSTITIAL TISSUE
INTROMITTENT ORGAN
ION TRANSPORT
IONIC REGULATION
ISTHMUS OVIDUCT ELASMOBRANCH
,
LAMELLAE OF EGG CAPSULE DOGlSH
LAMELLAE ZONA PELLUCIDA
LAMPBRUSH CHROMOSOMES
LECITHOTROPHY
LECITHOTROPHY COELACANTH
LECITHOTROPHY VIVIPAROUS ELASMOBRANCH
LECTINS
LECTINS IN CORTICAL REACTION
LEPTOTENE OOCYTES
LEUCOCYTES IN ATRESIA
,
HYOSOPHORIN
LIPID
LIKE CELLS IN FOLLICULAR EPITHELIUM
LIPID DROPLETS IN VITELLOGENESIS
LIPID DROPLETS FORMATION
LIPID IN CORTICAL ALVEOLUS STAGE
LIPID IN EARLY VITELLOGENESIS
LIPID MASS
LIPID YOLK DROPLETS
LIPOFUSCIN
LIPOVITELLIN
LUMINAL EPITHELIUM OVARY
LUMINAL EPITHELIUM OVARY SECRETION
LUMINAL GESTATION TELEOST
LUTEAL BODIES
LYMPHATIC COMPARTMENT OVARY
LYMPHATIC SPACES
LYSOSOMAL COMPARTMENT
LYSOSOME
LIKE BODIES
LYSOSOMES
LYSOSOMES IN FOLLICULAR CELLS
LYTIC ENZYMES IN OVULATION
MACROPHAGES
MARGINAL CLEFTS IN OVARIAN LUMINAL EPITHELIUM
MATROTROPHY
MATROTROPHY EXTREME
MATURATION
MATURATION DIVISION
MATURATION INDUCING STEROID
MATURATION
INDUCING HORMONE
MATURE EDGE SYNGNATHID OVARY
MEDULLA GONADAL
MEIOSIS
MEIOSIS RESUMPTION
MEIOTIC PROPHASE )
MEIOTIC SPINDLE FORMATION
MEMBRANE RESERVOIR UTERUS ELASMOBRANCH
MESODERM YOLK SAC SHARK
MESONEPHRIC DUCT ELASMOBRANCH
MESOTHELIUM
MESOVARIUM
METAPHASE )
METAPHASE ))
MICROAPOCRINE SECRETION
MICROlLAMENT BUNDLES IN VITELLOGENESIS
MICROlLAMENTS
MICROlLAMENTS CONTRACTILITY IN THECAL CELLS
MICROPINOCYTIC PITS IN PERITONEAL CELLS
MICROPINOCYTOSIS IN FOLLICULAR CAPILLARIES
MICROPINOCYTOSIS OOLEMMA
MICROPLICAE OF OOLEMMA
MICROPYLAR APPARATUS HAGlSH EGG
MICROPYLAR CANAL
MICROPYLAR CANAL NARROWING
MICROPYLAR CELL
).$%8
MICROPYLAR CELL IN AXIS DETERMINATION
MICROPYLAR CELL DEGENERATION
MICROPYLAR CELL STRUCTURE
MICROPYLAR CELL ULTRASTRUCTURE
MICROPYLAR FUNNEL HAGlSH
MICROPYLAR PLUG
MICROPYLAR PROCESS
MICROPYLE
MICROPYLE CLOSURE
MICROPYLE RESISTS POLYSPERMY
MICROPYLE ABSENCE IN VIVIPAROUS ELASMOBRANCH
MICROPYLE ABSENCE LAMPREY EGG
MICROPYLE BLENNY EGG
MICROPYLE FORMATION
MICROPYLE HAGlSH
MICROPYLE POSITIONING
MICROPYLE SURFACE PATTERNS
MICROPYLES CLADISTIC ANALYSES
MICROPYLES CLASSIlCATION
MICROPYLES MULTIPLE IN !CIPENSERIFORMES
MICRORIDGES IN TRANSPORT
MICROTUBULAR CYTOSKELETON
MICROTUBULE MIMICS
MICROTUBULE
LIKE ELEMENTS
MICROTUBULES
MICROTUBULES IN CHORIONIC lLAMENTS
MICROVESICLES IN FOLLICULAR CAPILLARIES
MICROVILLI IN PORE CANALS
MICROVILLI OF FOLLICULAR CELLS
MICROVILLI OF OOCYTE
MICROVILLI OF SPERM BINDING SITE
MICROVILLI OF SPERM ENTRY SITE
MICROVILLI DETACHMENT IN OVULATION
MICROVILLI GAP JUNCTIONS
MICROVILLI WITHDRAWAL FROM PORE CANALS
MICROVILLOUS CELLS
MIGRATION OF GERMINAL VESICLE
MIGRATION OF PRIMORDIAL GERM CELLS
-)(
-)3
MITOCHONDRIA WITH TUBULAR CRISTAE
MITOCHONDRIAL
ASSOCIATED GRANULAR MATERIAL
MITOTIC REST
MODEL OF HORMONAL SYNTHESIS
MONONUCLEAR PHAGOCYTES IN POSTOVULATORY FOLLICLES
MUCOPOLYSACCHARIDES LAMPREY FOLLICULAR CELLS
MUCOSOMES
-LLERIAN DUCT
-LLERIAN DUCT ELASMOBRANCH
MULTIPLE MICROPYLES IN !CIPENSERIFORMES
MULTIVESICULAR BODIES
.
NASCENT CORTICAL ALVEOLI
NERVE BUNDLES OVARIAN
NESTS OF EARLY GERM CELLS
NIDAMENTAL GLAND OVIDUCT ELASMOBRANCH
NIPPLES SUCKLING IN LUMINAL GESTATON
NITROGENOUS WASTE IN EMBRYOS
NONATTACHING lLAMENTS MEDAKA EGG
NUAGE
NUCLEAR MEMBRANE IN ATRESIA
NUCLEAR PORES
NUCLEARCYTOPLASMIC RATIO
NUCLEOLI
NUCLEOLI MULTIPLE
NURSE CELLS ELASMOBRANCH
NURSE CELLS LAMPREY
NUTRIENT TRANSFER
NUTRIENT TRANSFER IN MATROTROPHIC TELEOST
NUTRITIVE EPITHELIUM IN LUMINAL GESTATION
/
OCCLUDING JUNCTIONS
OESTRADIOL
OESTRADIOL `
OESTRADIOL ` IN ELASMOBRANCHS
OESTRADIOL ` SYNTHESIS
OESTROGEN
OOCYTE ENLARGEMENT
OOCYTE ENVELOPES
OOCYTE ))
OOCYTE MICROVILLI WITHDRAWAL
OOCYTE NUCLEUS IN ATRESIA
OOCYTE VOLUME
OOCYTE EXPULSION
OOCYTE GROWTH
OOCYTE HAGlSH
OOCYTE HYDRATION
OOCYTE UPTAKE OF MATERIALS
OOGENESIS
OOGONIA
OOGONIA ENTERING MEIOTIC PROPHASE
OOGONIA HAGlSH
OOGONIA MEIOSIS
OOGONIA PIPElSH
OOLEMMA
).$%8
OOLEMMA IN ATRESIA
OOLEMMA DEPOLARIZATION
OOLEMMA EXOCYTOSIS
OOLEMMA INDENTATION
OOLEMMA MOSAIC
OOLEMMA UPTAKE BY MICROPINOCYTOSIS
OOPHAGY
OOPHAGY COELACANTH
OOPHAGY VIVIPAROUS ELASMOBRANCH
OOPLASM IN ATRESIA
OPERCULAR RING HAGlSH
ORIENTATION OF SPERMATOZOA
ORIGIN OF THE GENITAL SYSTEMS
ORNAMENTATION SECONDARY ENVELOPE
OSMOLARITY OF EMBRYOTROPH
OSMOLARITY OF PERIVITELLINE mUID
OSMOREGULATION IN ABSORPTIVE EPITHELIA
OSMOREGULATION IN APLACENTAL YOLK SAC VIVIPARITY
OSMOREGULATION IN MATROTROPHIC GESTATION
OSMOREGULATION IN PERIVITELLINE SPACE
OSMOREGULATION SHARK UTERUS
OSMOREGULATION UTERUS BLUE SHARK
OSMOTIC ENVIRONMENT UTERUS ELASMOBRANCH
OSMOTIC POTENTIAL
OSMOTIC UPTAKE OF WATER
OSMOTIC UPTAKE OF WATER LAMPREY FOLLICLE
OSTIUM TUBAE IN VIVIPARITY ELASMOBRANCH
OSTIUM ELASMOBRANCH
OSTIUM ELASMOBRANCH OVIDUCT
OVARIAN ARTERY
OVARIAN CAVITY
OVARIAN EPITHELIUM IN LUMINAL GESTATION
OVARIAN mUID
OVARIAN FOLLICLES
OVARIAN FOLLICLES DIAMETER
OVARIAN FOLLICLES HORMONES
OVARIAN HORMONES
OVARIAN LUMEN
OVARIAN LUMINAL EPITHELIUM
OVARIAN LUMINAL WALL TELEOST
OVARIAN MATURITY
OVARIAN STROMA
OVARY
OVARY IN FOLLICULAR GESTATION
OVARY CYSTOVARIAN
OVARY ELASMOBRANCH
OVARY GYMNOVARIAN
OVARY HAGlSH
OVARY LAMPREY
OVARY SYNGNATHID
).$%8
OVARY TELEOST
OVERRIPE EGGS
OVIDUCT
OVIDUCT IN OVIPARITY
OVIDUCT IN VIVIPARITY ELASMOBRANCH
OVIDUCT ELASMOBRANCH
OVIDUCT ELASMOBRANCH BASIC PLAN
OVIDUCT EPITHELIUM
OVIDUCT 3CORPAENIFORMES
OVIDUCT TELEOST
OVIDUCTAL GLAND IN VIVIPARITY ELASMOBRANCH
OVIDUCTAL GLAND ELASMOBRANCH
OVIDUCTAL GLAND ELASMOBRANCH CAPSULE PRODUCTION
OVIDUCTAL GLAND ELASMOBRANCH INNERVATION
OVIDUCTAL GLAND ELASMOBRANCH SPERM STORAGE
OVIDUCTAL GLANDS ZONATION ELASMOBRANCH
OVIGEROUS EPITHELIUM 3CORPAENIFORMES
OVIGEROUS FOLDS
OVIGEROUS FOLDS IN LUMINAL GESTATION
OVIGEROUS FOLDS TELEOST
OVIGEROUS STROMA 3CORPAENIFORMES
OVISAC
OVISAC TELEOST
OVULATION
OVULATION IN OVIPAROUS TELEOSTS
OVULATION LAMPREY
OVULATION LYTIC ENZYMES
OVULATION
INDUCING ENZYMES
OVUM
OVUM DISINTEGRATION IN ATRESIA
0
PACHYTENE STAGE OF PROPHASE )
PALLIAL SUBSTANCE
PAPILLARY ZONE OVIDUCTAL GLAND ELASMOBRANCH
PARACRINE FUNCTION
PARACRINE SYSTEM
PARAPLACENTAL SITES SHARK UTERUS
PAROVARIAN CAVITY
PARTURITION TELEOST
PATHWAY BLOOD
EMBRYOTROPH LUMINAL GESTATION
PAVEMENT CELLS TROPHOTAENIAL
PAVEMENT EPITHELIUM TROPHOTAENIAL
PEDUNCLE FOLLICLE BEARING
PENETRATION BY SPERMATOZOA
PENETRATION OF OOLEMMA
PERICARDIAL SAC IN LUMINAL GESTATION
PERICARDIAL SAC ABSORPTION IN VIVIPARITY
PERICYTES
PERIFOLLICULAR CAPILLARIES
PERINUCLEAR DENSE BODIES
PERINUCLEAR NUAGES
PERINUCLEAR RING
PERINUCLEAR RING OF MITOCHONDRIA
PERINUCLEOLUS PHASE
PERITONEAL CELLS
PERITONEAL FOLDS
PERIVITELLINE mUID OSMOLARITY
PERIVITELLINE SPACE
PERIVITELLINE SPACE CREATION
PERIVITELLINE SPACE LAMPREY
PERIVITELLINE SPACE SPHERICAL BODIES
PERIVITELLINE SPACE WATER UPTAKE
PHAGOCYTES IN POSTOVULATORY FOLLICLES
PHAGOCYTES IN POSTOVULATORY FOLLICLES HAGlSH
PHAGOCYTOSIS IN ATRESIA
PHEROMONES
PHOSPHOINOSITIDE CASCADE
PHOSVITIN
PINOCYTOSIS IN SMOOTH MUSCLE
PINOCYTOSIS FOLLICULAR CAPILLARIES
PINOCYTOTIC VESICLES
PITUITARY CONTROL
PITUITARY GONADOTROPIN
PLACENTA
PLACENTA !NABLEPS
PLACENTA BRANCHIAL
PLACENTA BUCCAL
PLACENTA ELASMOBRANCH
PLACENTA FOLLICULAR
PLACENTA GUPPY
PLACENTA HAEMATROPHIC ELASMOBRANCH
PLACENTA MATROTROPHIC
PLACENTA NON
DECIDUATE SELACHIAN
PLACENTA NON
INVASIVE SELACHIAN
PLACENTA POECILIID
PLACENTA SHARK
PLACENTA TROPHOTAENIAL
PLACENTA YOLK SAC
PLACENTAL BARRIER GUPPY
PLACENTAL BARRIER SHARK
PLACENTAL EFlCIENCY
PLACENTAL VIVIPARITY ELASMOBRANCH
PLACENTOTROPHY
PLASMA GONADOTROPIN ))
POLAR BODY
POLARITY
POLYRIBOSOMES AND ANNULATE LAMELLAE
POLYSIALOGLYCOPROTEINS
POLYSPERMY
POLYSPERMY PREVENTION HAGlSH
POLYSPERMY BLOCK
POLYSPERMY PREVENTION
PORE CANALS
PORE CANALS IN CHORION
PORE CANALS DISAPPEARANCE
PORE CANALS ELASMOBRANCH
PORE CANALS EXCHANGE OF METABOLITES
PORE CANALS FORMATION
PORE CANALS LAMPREY
PORE CANALS MICROVILLI
PORE CANALS WITHDRAWAL OF MICROVILLI
POST
'6"$
POSTOVULATORY CORPUS LUTEUM
POSTOVULATORY CORPUS LUTEUM FORMATION
POSTOVULATORY FOLLICLES
POSTOVULATORY FOLLICLES DEGENERATION
POSTOVULATORY FOLLICLES ELASMOBRANCH
POSTOVULATORY FOLLICLES HAGlSH
POSTOVULATORY FOLLICLES TELEOST
POSTVITELLOGENIC OOCYTES AXIS FORMATION
POTASSIUMSODIUM PUMP
PREFOLLICULAR CELLS
PRE
'6"$
PREVITELLOGENIC FOLLICLES ELASMOBRANCH
PRIMARY ENVELOPE
PRIMARY ENVELOPE HAGlSH
PRIMARY ENVELOPE LAMPREY
PRIMARY ENVELOPE REMNANTS
PRIMARY FOLLICLE HAGlSH
PRIMARY GROWTH
PRIMARY OOCYTE
PRIMORDIAL FOLLICLE
PRIMORDIAL GERM CELLS
PRIMORDIAL GERM CELLS MIGRATION
PROGESTERONE
PROGESTERONE IN ELASMOBRANCHS
PROGRAMMED CELL DEATH
PROPHASE ) OOCYTES
PROSTAGLANDIN &_
PROSTAGLANDINS IN OVULATION
PROTANDROUS HERMAPHRODITES
PROTEASOMES
PROTECTION FOR EGGS 3CORPAENIFORMES
PROTEIN INCORPORATION
PROTEIN PHOSPHATE
PROTEIN SYNTHESIS ZONA PELLUCIDA
PROTEIN YOLK
).$%8
PROTEOLYSIS
PROTEOLYTIC COMPLEXES
PROTOGYNOUS HERMAPHRODITES
2
RECEPTORS FOR SPERMATOZOA
RECOVERY AFTER SPAWNING
REGULATION OF STEROIDOGENESIS
REPRODUCTION RHYTHM
RIBOSOMES
RUPTURE OF FOLLICLE
RUPTURE OF FOLLICLE LAMPREY
3
SEALS EGG CAPSULE ELASMOBRANCH
SECONDARY ENVELOPE
SECONDARY ENVELOPE COATING
SECONDARY ENVELOPE FORMATION
SECONDARY ENVELOPE LAMPREY EGG
SECONDARY ENVELOPE ORNAMENTATION
SECONDARY LYSOSOMES
SECONDARY OOCYTE
SECRETORY TUBULE OVIDUCTAL GLAND ELASMOBRANCH
SEMINAL RECEPTACLE TELEOST
SEX REVERSAL
SHELL GLAND IN VIVIPARITY ELASMOBRANCH
SHELL GLAND OVIDUCT ELASMOBRANCH
SHELL HARDENING
SHELL HAGlSH OOCYTE
SITE OF OVULATION
SKIN ABSORPTION IN VIVIPARITY
SMOOTH MUSCLE IN POSTOVULATORY FOLLICLES
SMOOTH MUSCLE THECAL
SOMATIC MESODERM
SOMATIC PREFOLLICULAR CELLS
SPECIAL THECAL CELLS
SPECIAL THECAL CELLS IN POSTOVULATORY FOLLICLES
MICROPYLE
SPERM ATTACHMENT
SPERM BINDING SITE
SPERM DEPOSITION TELEOST
SPERM ENGULFMENT
SPERM ENTRY SITE
SPERM ENTRY LAMPREY
SPERM GUIDANCE
SPERM ORIENTATION LAMPREY
SPERM PENETRATION
SPERM POCKETS TELEOST
SPERM RECEPTOR
SPERM REJECTION
SPERM RETENTION TELEOST
SPERM STORAGE
SPERM STORAGE OVIDUCTAL GLAND ELASMOBRANCH
SPERM ASSOCIATED CELLS TELEOST
SPERMATOGONIA
SPERMATOPHORE ELASMOBRANCH
SPERMATOZOA
SPERMATOZOA AGGLUTINATON
SPERMATOZOA STURGEON
SPERMATOZOA SUPERNUMERARY
SPERMATOZOA TELEOST
SPERMATOZOON PENETRATION
SPINNERETS OVIDUCTAL GLAND ELASMOBRANCH
SPLANCHNIC MESODERM
STAGES OF OOCYTE DEVELOPMENT
STAGES OF OVARIAN MATURITY
STAGES OF POSTOVULATORY FOLLICLE
STEROID PRODUCING CELLS INNERVATION
STEROIDOGENESIS
STEROIDOGENESIS DURING ATRESIA
STEROIDOGENESIS IN FOLLICULAR CELLS
STEROIDOGENESIS IN INTERSTITIAL TISSUE
STEROIDOGENESIS IN OVARIAN FOLLICLES
STEROIDOGENESIS IN POSTOVULATORY FOLLICLES
STEROIDOGENESIS IN THECAL CELLS
STEROIDOGENESIS CICHLID
STEROIDOGENESIS CYCLOSTOMES
STEROIDOGENESIS ELASMOBRANCH
STEROIDOGENESIS FOLLICULAR
STEROIDOGENESIS GUPPY FOLLICLE
STEROIDOGENESIS TELEOST
STEROIDOGENESIS THECA
STEROIDOGENIC PATHWAY
STEROID PRODUCING CELLS
STIGMA
STROMA LAMPREY OVARY
STROMA OVARIAN
SUBFOLLICULAR SPACE
SUPERFOETATION
SUPERNUMERARY SPERM
SURFACE PITS
SWELLING OF EGGS
SYNAPTIC MEMBRANE SPECIALIZATIONS
SYNAPTONEMAL COMPLEXES
SYNCHRONOUS OVARIES
SYNGNATHID OVARIES
).$%8
4
TANNING EGG CAPSULE ELASMOBRANCH
TAXONOMIC KEY BASED ON MICROPYLES
TELOLECITHAL EGGS
TENDRILS EGG CAPSULE ELASMOBRANCH
TERMINAL ZONE OVIDUCTAL GLAND ELASMOBRANCH
TERTIARY ENVELOPE
TESTOSTERONE
TESTOSTERONE IN FEMALE ELASMOBRANCHS
TETRAD CHROMOSOMES
THECA
THECA EXTERNA
THECA FOLLICULI
THECA IN ATRESIA
THECA INTERNA
THECA INTERNA IN ATRESIA
THECA OF CORPUS LUTEUM
THECA CICHLID
THECA CONTRACTIONS
THECA ELASMOBRANCH
THECA HAGlSH
THECA HAGlSH FOLLICLE
THECA HORMONES
THECA LAMPREY
THECA POSTOVULATORY FOLLICLES
THECA POSTOVULATORY FOLLICLES HAGlSH
THECA SEROIDOGENESIS
THECA TELEOST
THECAL CELLS IN ATRESIA
THECAL CELLS IN POSTOVULATORY FOLLICLES
THECAL DEGENERATION LAMPREY
THECAL STEROIDOGENESIS LAMPREY
TIGHT JUNCTIONS IN FOLLICULAR EPITHELIUM
TIGHT JUNCTIONS FOLLICULAR CAPILLARIES
TIGHT JUNCTIONS PERITONEAL CELLS
TISSUE BARRIERS IN APLACENTAL YOLK SAC VIVIPARITY
TRANSCRIPTION
TRANSCYTOSIS
TRANSCYTOSIS IN FOLLICULAR GESTATION
TRANSCYTOSIS IN LUMINAL GESTATION
TRANSFER OF NUTRIENTS
TRANSIENT YOLK SPHERES
TRANSOSOMES
TRANSPORT IN FOLLICULAR GESTATION
TRANSPORT OF EGGS
TRANSPORT OF IONS
TRANSPORTING EPITHELIUM IN TROPHOTAENIAE
TROPHIC PATTERNS IN VIVIPARITY
TROPHODERMY
TROPHONEMATA ELASMOBRANCH
TROPHONEMATOUS CUPS SHARK
TROPHOTAENIAE
TROPHOTAENIAL ABSORPTIVE CELLS
TROPHOTAENIAL APICAL CANALICULAR SYSTEM
TROPHOTAENIAL EPITHELIAL CELLS
TROPHOTAENIAL PAVEMENT CELLS
TROPHOTAENIAL PAVEMENT EPITHELIUM
TROPHOTAENIAL PLACENTA
TUBULAR AGRANULAR ENDOPLASMIC RETICULUM
TUBULAR GLANDS OVIDUCTAL GLAND ELASMOBRANCH
TUBULAR MITOCHONDRIAL CRISTAE
TUNICA ALBUGINEA
TUNICA ALBUGINEA TELEOST OVARY
5
UMBILICAL ARTERY
UMBILICAL CORD
UMBILICAL STALK
UMBILICAL VEIN
UREA IN EMBRYOTROPH
URINARY DUCT CYCLOSTOME
URINARY SINUS CYCLOSTOME
URINOGENITAL PAPILLA
URINOGENITAL PAPILLA CYCLOSTOME
UROGENITAL SINUS ELASMOBRANCH
UTERINE COMPARTMENTS ELASMOBRANCH
UTERINE MILK ELASMOBRANCH
UTERUS IN VIVIPARITY ELASMOBRANCH
UTERUS ELASMOBRANCH
UTERUS ELASMOBRANCH OSMOTIC ENVIRONMENT
UTERUS GRAVID OVIPAROUS SKATE
6
VASCULAR BULBS IN FOLLICULAR PLACENTA
VASCULAR BULBS IN MATROTROPHIC PLACENTA
VASCULARIZATION FOLLICULAR
VEGETAL POLE
VESICULAR TRANSPORT IN LUMINAL GESTATION
VESTIBULE
VILLI OVARIALES IN LUMINAL GESTATION
VISCERAL MESOTHELIUM OVARY
VISCERAL PERITONEUM OVARY
VITELLINE ARTERY VEIN
VITELLINE BODY
VITELLINE ENVELOPE
VITELLINE ENVELOPE IN ATRESIA
VITELLINE ENVELOPE IN OVULATION
VITELLINE MEMBRANE
VITELLOGENESIS
VITELLOGENESIS IN MATROTROPHIC TELEOST
).$%8
VITELLOGENESIS EARLY
VITELLOGENESIS ELASMOBRANCH
VITELLOGENESIS STINGRAY
VITELLOGENIN
VITELLOGENIN ELASMOBRANCH
VIVIPARITY
VIVIPARITY COELACANTH
VIVIPARITY ELASMOBRANCH
VIVIPARITY ELASMOBRANCH APLACENTAL OOPHAGOUS VIVI
PARITY
VIVIPARITY ELASMOBRANCH APLACENTAL VIVIPARITY
VIVIPARITY ELASMOBRANCH APLACENTAL YOLK SAC VIVIPAR
ITY
VIVIPARITY ELASMOBRANCH PLACENTAL VIVIPARITY
VIVIPARITY ELASMOBRANCH TYPES
VIVIPARITY TELEOST
VIVIPARITY TROPHIC PATTERNS
7
WITHDRAWAL OF MICROVILLI AT OVULATION
9
YOLK DROPLETS FUSION
YOLK GRANULES
YOLK MASS IN ATRESIA
YOLK NUCLEUS
YOLK PLATELETS
YOLK POLYPEPTIDES
YOLK PRODUCTION
YOLK PROTEIN PRECURSORS EXOGENOUS
YOLK PROTEINS HYDROLYSIS
YOLK SAC IN LUMINAL GESTATION
YOLK SAC PLACENTA
YOLK SAC PLACENTA COELACANTH
YOLK SAC PLACENTA ELASMOBRANCH
YOLK SAC PLACENTA SHARK
YOLK SAC ABSORPTION IN VIVIPARITY
YOLK SAC BLUE SHARK
YOLK SAC SHARK
YOLK SPHERES
YOLK STALK SHARK
YOLK SYNCYTIUM SHARK
YOLK VESICLES
YOLK FORMATION
YOLK SPECIlC MARKER
YOLKY INCLUSIONS TYPES
:
ZONA PELLUCIDA
ZONA PELLUCIDA IN FOLLICULAR GESTATION
).$%8
ZONA PELLUCIDA IN FOLLICULAR PLACENTA
ZONA PELLUCIDA IN VITELLOGENESIS
ZONA PELLUCIDA IN VIVIPAROUS ELASMOBRANCH
ZONA PELLUCIDA IN VIVIPAROUS POECILIIDS
ZONA PELLUCIDA COMPACTION
ZONA PELLUCIDA COMPOSITION
ZONA PELLUCIDA CONVERSION TO CHORION
ZONA PELLUCIDA ELECTRON
DENSE LAYER
ZONA PELLUCIDA FORMATION
ZONA PELLUCIDA FORMATION ELASMOBRANCH
ZONA PELLUCIDA HAGlSH
ZONA PELLUCIDA INITIAL APPEARANCE
ZONA PELLUCIDA LAMPREY
ZONA PELLUCIDA LAYERING
ZONA PELLUCIDA STURGEON
ZONA PELLUCIDA SURFACE RIDGES
ZONA RADIATA
ZONATION OF OVIDUCTAL GLANDS ELASMOBRANCH
ZYGOTENE STAGE OF PROPHASE )
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