J ournal of Fish Biology (1998) 52, 107117

Morphological variationbetweenredmullet populationsin

Greece
Z. M:xiis*, A. P. Aios1oiinis, P. P:N:cio1:xi, A. J . Tnronooi
:Nn C. Ti:N1:inxiiinis
*Department of Applied and Theoretical Sciences, University of Thessaly, Pedion Areos
38334, Volos, Greece; Department of Genetics, Development and Molecular Biology,
School of Biology, AristotleUniversity of Thessaloniki, 54006, Thessaloniki, Macedonia,
Greeceand Laboratory of Oceanography, Department of AgricultureCrop and Animal
Production, University of Thessaly, Pedion Areos 38334, Volos, Greece
(Received 14 March 1997, Accepted 4 August 1997)
Morphometric variation in 15charactersof thered mullet Mullusbarbatussamplesfromseven
Greek localities was examined using multivariate analysis. ANOVA, stepwise discriminant
analysis and cluster analysis revealed a rather high morphological variability between the
populations studied. Thediscriminant analysis revealed that about 80%of theexamined sh
couldbecorrectlyclassiedinto thesevenareas. Thisvariabilitycouldbeexplainedintermsof
genetic structuring of the populations and/or environmental conditions prevailing in each
geographic area in combination with sh migration and egg/larvae transportation from one
area to another. The results suggest that multivariate analysis when combined with other
important biological parameters of red mullet may have important implications for the
management of theGreek demersal sh resources. 1998 TheFisheries Society of theBritish I sles
Key words: Mullus barbatus; multivariateanalysis; morphometrics; Greek marinewaters.
INTRODUCTION
Red mullet Mullus barbatus L., is distributed in the eastern Atlantic, fromthe
British I slesto Senegal, aswell asthroughout theMediterranean andBlack Seas
(Whitehead et al., 1986). I n Greek waters, it ranks among the most commer-
cially important demersal sh, with a total catch of 3015t in 1994, representing
c. 152%of thetotal Greek marinecatch (Stergiou et al., 1998).
Multivariateanalysis of a set of phenotypic characters is regarded as a more
appropriatemethod than theuseof a singlecharacter for determiningmorpho-
logical relationships between populations of a species (Thorpe, 1976, 1987).
This method has also been proposed as an ecient tool in management
programmes concerned with stock identication of freshwater sh species, and
for investigatingtaxonomic problemsin sympatric populations(Beacham, 1985;
MacCrimmon & Claytor, 1986; Surreet al., 1986; Cawdery & Ferguson, 1988;
Karakousiset al., 1991, 1993). Fewstudieshavebeencarriedout onmarinesh
species using similar methods (Corti & Crosetti, 1996). Although the biology,
ecologyandsheriesof redmullet havebeenstudiedextensivelyinGreek waters
(Stergiouet al., 1992, 1998), therearenostudiesconcerningmultivariateanalysis
of morphological characters.
Author to whom correspondence should be addressed. Tel.: +30 42169781-4; fax: +30 42163383/
42163544.
107
00221112/98/010107+11 $25.00/0/jb970565 1998 TheFisheries Society of theBritish I sles
Theaimof this study was to examinethepattern and theextent of morpho-
metric variation in seven Greek red mullet populations, using multivariate
methods, and to test theeciency of thesemethods in stock identication.
MATERIALS AND METHODS
Samples werecollected by trawling (except thegill netted samples fromAmvrakikos)
between October 1995and March 1996fromvelocalitiesin theAegean Seaand two in
theI onian Sea (Fig. 1). Two hundred and seventy-vematureshes wereused for the
analysis. Sex was determined macroscopically whenever possible(TableI ).
Fifteenmorphometriccharactersweremeasuredoneachspecimen(TableI ) according
to Hubbs& Lagler (1967). All measurementsweretakento thenearest 01mm. Thefull
data les are available on request. As an unequal distribution of the two sexes was
observed in most populations, atwo-way analysisof variance(Zar, 1984) wasperformed
to check for apossibleeect of sexual dimorphismwithin each population. To minimize
any variation resulting from allometric growth, all morphometric measurements were
standardized according to:
e=logY b(logXlogX
L
)
where: e, standardized measurement; Y, character length; b, slopeof logY against logX
plot for each population; X, standard length of thespecimen; X
L
, mean standard length
L
evanti ne Sea
30 28 26 24 22
200
I
o
n
i
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n

S
e
a
36
40
38
42
1
1
0
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6
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6
Sporades
Basi n
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A
e
g
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S
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a
200
200
200
600
5
7
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4
2
Fic. 1. Location of red mullet sample sites: 1, Thermaikos; 2, Corfu; 3, Allonissos; 4, Amvrakikos; 5,
Kavala; 6, Platanias; 7, Chalkida. Somebathymetric contours arealso shown.
108 z. x:xiis r1 :i.
of thespecimens examined. According to Reist (1985) this transformation best reects
shapevariation amonggroupsindependently of sizefactors. Therefore, total length and
standard length of each specimen wereexcluded fromthenal analysis.
The coecient of variation (CV%) was computed for each character according to:
CV%=(D
s
100)/x, where D
s
, standard deviation, and x, mean of the transformed
measurements of morphometric characters in each population (Zar, 1984). I n each
sample, morphological variability was estimated by the multivariate generalization of
thecoecient of variation (CV
p
) (Van Valen, 1978) according to: CV
p
=100S
x
/M
x
,
whereS
x
, varianceof each morphometric variable; M
x
, mean squared.
To identify whether there were any statistically signicant dierences between the
seven populations for each character, a one-way analysis of variance (ANOVA) (Zar,
1984) was performed. Principal component analysis (PCA) was used to test for the
contribution of the 13 morphological characters in the conguration of variance.
Forward stepwise discriminant analysis (DA), based on the generalized Mahalanobis
distance, was used to determine the similarity between populations and the ability of
these characters to identify the specimens correctly. To investigate the phenotypic
relationshipsbetweentheexaminedpopulationsadendrogramwasconstructed, basedon
Mahalanobis distances, using UPGMA cluster analysis (Sneath & Sokal, 1973).
Mahalanobis distances were compared to the geographical distances using Mantels
(1967) test, to determine whether there was any correlation between geographical
distribution and morphological variability.
All statistical analyses wereperformed usingSPSS PC
+
(1989), NTSYS (Rohlf, 1990)
and SYSTAT (1992).
RESULTS
The only dimorphic traits found using the two-way ANOVA on
untransformedmeasurementswerethetotal andstandardlengths. Femaleswere
generally larger than males. The mean length diered signicantly (t-test,
P<005) between sexes only in the Thermaikos, Corfu and Allonissos popu-
lations. Since all measurements were transformed and the eect of size was
removed, all analyses wereperformed for combined sexes.
The mean values of all characters examined (Table I ) diered signicantly
(ANOVA, P<005) between the seven populations. The PCA analysis
extracted three factors with eigenvalues >1, explaining 586% of the variance
(TableI I ). Usingacut-o valueof 06for thefactor loadings, factor 1expressed
characters associated with the head (preorbital and postorbital distances and
head length), whereas factor 2 expressed variables associated with the ns
(heights of dorsal and anal ns and length of pectoral n) and the caudal
pedunclelength.
The rst and second canonical variables contributed 6424 and 1834%,
respectively, to thevariance(Fig. 2). Thecharacters of primary importancein
distinguishing between the groups were the pectoral n length for the rst
canonical variableandthedorsal nbaselengthfor thesecondone. Usingthese
morphometriccharacterseachspecimencouldbeclassiedcorrectlyto theseven
populationswithanaccuracy of 7927%(TableI I I ). Giventhat theaccuracy of
DA was often higher in the initial than for subsequent samples, a DA was
performed on only half of the original sample and then repeated on the other
half. However, classication results for both analyses showed no dierences
(8214 and 8296% for the rst and the second half of the original sample,
respectively).
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C
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(
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C
V
%
2

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3

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2

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D
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(
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C
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%
5

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(
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C
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9

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1
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C
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7

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5
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n
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t
h
1
2

8
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(
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8
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1
2

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0

6
6
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1
3

1
8
(
0

6
0
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1
2

6
4
(
0

5
6
)
1
2

8
8
(
0

6
6
)
1
3

3
9
(
1

6
8
)
1
3

4
3
(
0

6
4
)
C
V
%
6

2
4
5

4
4

5
5
4

4
3
5

1
2
1
2

5
4
4

7
6
P
e
c
t
o
r
a
l

n
l
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t
h
2
3

8
3
(
1

4
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)
2
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5
3
(
0

8
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)
2
7

3
8
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0

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2
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8
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1

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1
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1
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2
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)
2
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9
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9
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(
1

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C
V
%
6

0
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3

4
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3

1
4
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6
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5

1
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5

0
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2
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5

2
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4

7
5
4

6
4
4

2
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3

9
0
The correlation between geographic and Mahalanobis distances (Fig. 3)
became statistically signicant (r=0592, P<005) only when the two I onian
populations wereexcluded.
DISCUSSION
I t is certain that parameters related to thetiming of thesampling, thesexual
dimorphism, theallometric growth and thestateof maturity of theshes could
impose some major limitations on the study of morphological relationships
between geographical populations. This study attempted to minimizevariances
caused by theseparametersthrough thetransformation of theoriginal measure-
mentsandbychoosingonlymatureshesfor theanalysis. Nevertheless, thefact
that thesampleswerecollectedat varioustimesof theyear couldcreatedierent
morphological groupsdueto dierent dimensionsrelatedto gonaddevelopment
and stomach fullness of theshes. All samples werecollected between October
and March, whereasthereproductiveseason of red mullet in Greecetakesplace
between May and September (Papaconstantinou et al., 1981). I n addition,
samples fromAllonissos, Platanias and Chalkida which have been collected at
dierent times of the year (October 1995, December 1995 and March 1996
respectively) showedagreater phenotypicrelationshipthanthesecollectedat the
T:nir I I . Results of principal components analysis (PCA) and factor loadings for each
morphometric variable on the three extracted PCA factors after varimax normalized
rotation
Factor Eigenvalue
PCT of
variance
Cumulative
PCT
1 442456 340 340
2 200228 154 494
3 119008 92 586
Characters Factor 1 Factor 2 Factor 3
Maximumbody depth 035791 009052 048306
Minimumbody depth 028481 027115 037595
Caudal pendunclelength 012308 078787 011119
Head length 083885 011571 012585
Diameter of eye 012526 009444 056564
Preorbital distance 090736 005115 006224
Postorbital distance 087070 022617 016361
Predorsal n distance 071718 018214 040226
Dorsal n height 019471 066036 021967
Dorsal n baselength 002997 030699 064523
Anal n height 013320 078211 028267
Anal n baselength 000520 014473 060754
Pectoral n length 006093 074802 039251
112 z. x:xiis r1 :i.
sametimeof year (Corfu, Amvrakikos, March 1996; and Thermaikos, Kavala,
J anuary 1996) (Fig. 3). Theseindications suggest that theresults would not be
aected by thetiming of thesampling.
Within theaccuracy limits of theexperimental procedure, therewas extensive
interpopulation variation in morphometric characters of the seven red mullet
geographical populations (Fig. 2). The characters of primary importance in
4
2
Canoni cal vari abl e I
C
a
n
o
n
i
c
a
l

v
a
r
i
a
b
l
e

I
I
2
0
2
4
4 0 2 4
4 2
7
6 3
5
1
Fic. 2. Discriminant analysis plot wherethe13 morphometric characters wereused. 1, Thermaikos; 2,
Corfu; 3, Allonissos; 4, Amvrakikos; 5, Kavala; 6, Platanias; 7, Chalkida. Circles include80%of
thespecimens.
T:nir I I I . Results of discriminant analysis classication showing the percentage of
specimens classied in each group
Group
1 2 3 4 5 6 7
1 Thermaikos 80 25 0 0 175 0 0
2 Corfu 0 90 5 25 0 25 0
3 Allonissos 0 25 70 0 0 225 5
4 Amvrakikos 25 25 0 90 5 0 0
5 Kavala 125 75 25 75 675 0 25
6 Platanias 0 5 5 0 25 775 10
7 Chalkida 0 0 86 0 0 114 80
Total of specimens correctly classied: 7927%.
xoinoiocic:i v:i:1ioN iN rn xiiir1 113
distinguishing between the seven populations as revealed by PCA, were those
related to head and n dimensions. However, these characters explained only
586%of thevariancebetweenthesevengroups, suggestingthat other characters
may represent additional sources of variance.
Conversely, intrapopulation variation waslessevident asindicated by thelow
CV%valuesfor each character separately (TableI ). Hence, sexual dimorphism,
reported elsewhere(Papaconstantinou et al., 1981), is overcomebecauseof the
transformation of theoriginal measurements; theabsenceof within-population
variation in morphological characters suggests that each sample consists of a
phenotypically homogeneous group. According to Soule & Couzin-Roudy
(1982) thereshould beanegativecorrelation between CV%and theestimatesof
heritability of morphological characters. Therelatively lowCV%values found
in the present study indicate a high heritability and a proportionally lower
contribution of environmental variance to morphological variability for each
character.
Accordingto theDA classication (TableI I I ), 7927%of thesh examined in
this study can be classied correctly into the seven groups, and for the two
populations fromthe I onian Sea the classication accuracy reaches 90%. The
classicationaccuracyfor thesepopulationswasrelativelyhighgiventhat similar
values have also been reported for isolated populations of brown trout Salmo
trutta L. (Karakousis et al., 1991) and for populations of North American
Atlantic salmon Salmo salar L. (Claytor & MacCrimmon, 1988).
I n general, morphological variability among dierent geographical popu-
lationscouldbeattributedto dierent geneticstructureof populationsand/or to
dierent environmental conditions prevailing in each geographic area. The
present populations were studied previously using starch gel electrophoresis
(Mamuriset al., unpublished). Fourteenenzymesystems, codedby20loci, were
investigated. According to isoenzyme data, these populations showed a high
degree of genetic similarity. Furthermore, the resultant matrix of Neis (1978)
4
Amvraki kos
5 3 2 0 1
Kaval a
Thermai kos
Corfu
Al l oni ssos
Chal ki da
Pl atani as
Fic. 3. UPGMA cluster analysisbasedonMahalanobis distancesbetweenthemorphometriccharacters.
114 z. x:xiis r1 :i.
geneticdistanceshowedno signicant correlation(P>005) whencomparedwith
Mahalanobisdistance, usingMantels(1967) test. However, onecannot exclude
the existence of undetected genetic structuring of these seven populations that
could account for morphological variation. I ndeed, it may be that enzyme
electrophoresis is too weak as a tool to reveal genetic dierences and therefore
more appropriate molecular techniques (Ferguson et al., 1995) are required to
screen thegenetic variation at thepopulation level.
An alternative hypothesis is that morphological variation may result from
phenotypic plasticity in response to trophic and environmental conditions
prevailing in each area. The geographical distance was correlated signicantly
with the Mahalanobis distances, at least for the ve Aegean samples. This
suggests that phenetic relationship between the populations decreases with
geographical distance. The observed phenetic relationship between geographi-
cally neighbouring populations could beattributed either to sh migration and
egg/larval transportation or to similar environmental conditions prevailing in
neighbouring areas. The postlarvae of red mullet are pelagic whereas the
adults are benthic, being found mainly on muddy bottoms at depths generally
down to 300m (Whitehead et al., 1986). The results of the DA (Fig. 2) and
thecluster analysis (Fig. 3) revealed thefollowingmajor dierentiations among
the seven populations, in order of importance: (a) between the populations
from central and north Aegean Sea (Platanias, Chalkida, Allonissos;
Thermaikos, Kavala), and (b) between the two populations from I onian Sea
(Amvrakikos; Corfu).
Amvrakikos gulf is a shallow, semi-enclosed basin connected with theI onian
Sea through a narrow channel (width 800m, sill depth 12m). I t is one of the
most eutrophic Greek gulfsand most probably subjected to largeenvironmental
variation when compared to theI onian Sea(Panayotidiset al., 1994). Thus, the
relatively lowrateof both egg/larval transportation and migration for theadult
sh, if thereis any, imposed by thenarrowness of thegulf outlet, as well as the
adaptation of red mullet to thelocal trophic and environmental conditions may
explain the relatively high morphological dierentiation observed between the
Amvrakikos and Corfu samples. I t is worth noting, however, that part of
the variation observed may be related also to trawling being prohibited in the
AmvrakikosGulf and, hence, redmullet isnot subject toshingmortality, which
imposes selection for smaller lengths at maturity.
The dierences observed in morphological characters between the samples
fromthenorth and central Aegean Sea may beattributed to thefollowing two
factors. Firstly, bathymetric constraints and especially a very narrowcontinen-
tal shelf leadingviaaverysteepcontinental slopetothebroadbut relativelydeep
(1000m) Sporades Basin (Fig. 1) may prevent large scale migration of red
mullet adultsbetweenthesamplingareasof thenorth(Thermaikos, Kavala) and
central (Allonissos, Platanias, Chalkida) Aegean Sea. Secondly, large-scale
gyres, which have been observed in various areas of the Thracian Sea and
ThermaikosGulf (Stergiouet al., 1998) andalargeclockwise(anticyclonic) eddy
that dominates the circulation in Sporades Basin, below the shelf-break depth
(200m) (Durrieu deMadron et al., 1992), may act asretention areasfor both
eggs and larvae, thus preventing their mass transportation to the southern
Aegean Sea.
xoinoiocic:i v:i:1ioN iN rn xiiir1 115
The link between phenotypic variability in red mullet and environmental
conditionsisalsostrengthenedbythecloseclusteringof thethreemost eutrophic
areas (Amvrakikos, Thermaikos, Kavala; Stergiou et al., 1998) (Fig. 3). I n
contrast, in the open sea localities of the second group (Platanias, Chalkida,
Allonissos, Corfu), theconditions aremorestableand clearly oligotrophic.
I n conclusion, themorphological variation in red mullet could beexplained in
terms of variation in environmental conditions, sh migration and egg/larval
transportation fromonearea to another.
The aspects discussed above when combined with the fact that important
biological parameters of red mullet (K, L
`
and mortality rates) in most of the
seven areas examined dier signicantly (Stergiou et al., 1998), may have
important implications for the management of the Greek demersal resources
(Stergiou, 1993; Stergiou et al., 1998).
The authors thank M. Lazaridou for valuable advice; K. Stergiou for many
fruitful discussions and useful suggestions; B. Theodorou for technical assistance.
Financial support fromtheGreek ministryof Development (PENED, 1995), isgratefully
acknowledged.
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