Professional Documents
Culture Documents
.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact support@jstor.org.
The Association for Tropical Biology and Conservation is collaborating with JSTOR to digitize, preserve and
extend access to Biotropica.
http://www.jstor.org
1994
ABSTRACT
forplant phenologyare proposedto resolveproblemsin describing
A new classification
and conceptualframework
in 254 lowlandtropicalrain foresttreesof 173 species
tropicalpatterns.A long-term(12 yr) surveyof flowering
and complexpatterns.Analysis
fromthe La Selva BiologicalStationin Costa Rica showedhighlydiverse,irregular,
methodsratherthan
of this surveydata reliedprimarilyon graphicalanalysesthat provide data representation
differsfrompreviousones in three
numericalsummariesthat providedata reductionmethods.The classification
of the time series,based on explicittime and amplitudescales,so
frequency
ways. It uses, as the primarycriterion,
that irregular
temporalsequencesare revealed.It featuresa systemof subsidiaryclassesbased on otherquantitative
separatespatterns
Finally,theconceptualframework
duration,amplitude,date,and synchrony.
descriptors:
regularity,
at each level of analysisso thatadding the time seriesat one levelproducesa time seriesforthe nexthigherlevel.
Levels are hierarchical
fromthe flowerto the individual,population,and communitywith additionalnon-nested
levels such as the guild. The fourbasic classes-continual,subannual,annual, and supra-annual--areapplied to
forquantitativedescription
systemprovidesa logical framework
patternsat any level of analysis.The classification
of phenologicalbehaviorleadingto morestandardizedcomparisons.Thus we can see thattropicalphenologydiffers
fromtemperatephenologyin two majorways. In tropicalspecies,the natureof the patternmay changefromone
levelof analysisto the next,whichis not typicalof temperatespecies.In manytropicalspecies,phenologicalpatterns
varymorewidelyoverthe geographicrangeof a speciesthan theydo in temperatespecies.
guild; individual;La Selva BiologicalStation;lowlandtropicalrain
community;
Keywords: classification;
flowering;
population;tropicaltrees.
forest;phenology;
tropicalphenologyhas
temperatezone. In contrast,
discipline,in
beenan impreciseand oftenconfusing
littlestudiedand
partbecauseit has been relatively
in partbecauseit has beenhandicappedby thelack
termsand methods.Thispaperproofstandardized
and conceptualframework
posesa newclassification
thatprovidesa logicalsystemforquantitativedeapproachtopheA typological
scription
ofpatterns.
patternsthat may repnologynot only identifies
but also providesa unit
resentadaptivesyndromes
of analysisthatservesas a contextfororganizing
The systemcan be used forany reinformation.
curringeventin plant or animal lifecyclesin any
regionof theworld.We have developedit hereon
patternsin lowlandtropical
the basis of flowering
treesbutanyotherphenologicalcharacter
rainforest
(e.g., leafingor fruiting).
can be substituted
Most ofthephenologicalworkin lowlandtrophas beenconductedat thecommunity
icalrainforest
of the forest,
I Received 7 October 1992; revisionaccepted 4 June level to show the overallseasonality
cycles
fruiting
oftenwiththegoal of understanding
1993.
141
142
Newstrom,Frankie,and Baker
PREVIOUS CLASSIFICATIONS
Severalclassifications
havebeenproposedtodescribe
that intropicalflowering
patterns.Classifications
criteriaare not
corporateadditionalnonflowering
discussedhere,suchas thosewithleafing(Reich &
Borchert1984) or with life form(Sarmiento&
Monasterio1983). There are threemain classificationsbasedon flowering
alone.The most
patterns
based on date or season,
widelyused classification,
phenology
(Croat
has beenimported
fromtemperate
1975, 1978; Tomlinson1980). Temperate-based
break down when
concepts,however,frequently
of tropicalplantsas has been
applied to characters
thecase withbranching
patterns
(Tomlinson& Gill
1973) and deciduousness(Richards 1952, Longofflowman & Jenik1987). The onlyclassification
forthe tropics
eringphenologydevisedspecifically
is thatof Gentry(1974). This has been the most
satisfactory
to date of thoseavailableand has been
used fairlywidely(e.g., Morellatoand Leitao-Filho
1990, Oliviera et atl. 1991). The strikingshortin thewetand drytropics
liveddisplaysofflowering
based on duinspiredanothertypeof classification
ration.This has been used in discussionsof pollinatorforagingbehaviorand reproductive
biology
(e.g., Frankieet ail. 1974, Augspurger1980, Bawa
1983).
a classification
to describetypesof floweringfor
The
Bignoniaceaein relationto pollinationsystems.
fivemajor classes,(big bang, multiplebang, cornucopia, steadystate,and an unnamedpattern),
a mixtureofcriteria
suchas individual
incorporated
levelamplitude,date,duration,and populationlevel synchrony.
temAlthoughthissystemidentifies
poral sequences well, it does not encompass the
range of diversityfound in our data. The classes
have been used impreciselyin the literaturebecause
some authors have used them for patterns that do
BASEDON DURATION.-Systemsbased
CLASSIFICATIONS
on durationdistinguish
betweenextremesof short
and long durationof flowering,
e.g., "seasonal" vs.
"extended" (Frankie et al. 1974), "mass" vs.
"steady state" (Augspurger 1983), and "mass" vs.
"extended" (Bawa 1983). As with categoriesbased
Plant Phenology
143
144
Newstrom,Frankie,and Baker
METHODS
Data collectionproceduresforthisprojectand site
forthe La Selva BiologicalStationin
information
Costa Rica have been describedin Frankieet ail.
(1974) and Newstromet ail. (1993). Using binoculars,monitorsmade monthlyobservationsof
on 457
and fruiting
leafing,budding,flowering,
tagged treesfromJanuary1969 to March 1981.
Only thosetreeswitha minimumof 5 consecutive
wereused fortheclassification,
yearsofobservations
173
in a sampleof 254 treesrepresenting
resulting
speciesin 59 families.In this sample, 11 species
by 4 to 6 trees,78 speciesby 2
wererepresented
by one tree.The amor 3 treesand theremainder
plitudescalehad threeclasses:none,light,and heavy
withrespectto thetypicalcropof flowers
flowering
foreach tree.Wherevertherewere threeor four
treesavailable fora givenspeciesin our data, we
estimateda populationlevelpatternby calculating
of treesin flowerat each intervalin
theproportion
the timeseries.Seasonsat La Selva have been classifiedas main dry fromJanuaryto May; early
wet fromMay to September;veranillo, an unpredictabledryseason, in Septemberor October;
and, late wet fromOctobertoJanuary(Newstrom
et ail. 1993).
patternsforma continBASIC CLASSIFICATION.-The
flowering.
uum fromcontinuousto veryinfrequent
fourbasic classesbased on freWe distinguished
quency,definedas thenumberof"on'"/"off"cycles
episode
per year(one cycleconsistsof a flowering
interval,Fig. 1). The
followedby a nonflowering
four basic classes are continual (floweringwith
sporadicbriefbreaks), subannual (floweringin
more than one cycleper year),annual (only one
majorcycleperyear),and supra-annual (one cycle
overmorethanoneyear)(Figs.1 and 2). Regularity,
is
as a secondarycriterion,
used in theclassification
epidefinedas the variancein lengthof flowering
intervals,
and consequently
sodes and nonflowering
ofthecyclesas well(Fig. 1). We initially
recognized
two main classes, regularand irregular,but are
in moredetail.
thiscriterion
quantifying
presently
suchas duThe classification
uses othercriteria
subdividethe
ration,amplitude,and dateto further
classes(see Newstromet al. 1993). For example,
we divideannual flowering
patternsintothreeduflow(< 1 mo), intermediate
rations:briefflowering
(>5 mo).
ering(1-5 mo), and extendedflowering
We base othersubcategorieson the shape of the
curveforamplitudeof flowering
(see Fig. 11.8 in
Newstromet ail. 1993). Furthersubdivisionsare
as themonthor season.
based on date,represented
00
00
00
ON
ON
0
4.4
60
00
ON
ON
-4
-.,
tc
0 00
r-
r-
00
CZ
44
CZ
-a
00
C) ." ON
0
0
CZZ
,
oo
00
00
ON
-4
tu
44
ol
0
CZ
0
7:1
-0 C:
Plant Phenology
CLASSES
FREQUENCY
Continual
145
24
12
24
36
48
60
72
84
96
108
120
132
Sub-annual
24-
12
24
36
48
60
72
84
96
108
120
132
12
24
36
48
60
72
84
96
108
120
132
1;
1;.
1,
96
108
120
132
04.
*3
Annual
'].
11;
12
0
?
11,
---,--
---.
24
36
,;11
48
60
72
84
2S~upra-annual
01
12
24
36
21
24
60
72
84
96
108
120
132
108
120
132
REGULARITYCLASSES
Regularpattern
12
48
36
48
60
72
84
96
Irregular
pattern
21
.. .. .
12
24
.. .. ..
36
. ; ..
48
. . . .;..
60
72
. .
.. ..
..
.. . . . . .
84
96
. ..
108
.. . .
120
132
146
Newstrom,Frankie,and Baker
Guatteriaaeruginosa
Continual
Tree 1043
1-llllllll l
ll lll
ll
HliiiHliiiltiii iiiii iii11111iilillilt,lll
ii
,
12
24
36
48
60
72
84
96
120
108
132
a)
Sub-annual
o0
2
r_: 0
-~
Protiumpittieri
.. .....
,
.......... 1...
~~~~~~~8
18
~Lonchocarpusoliganthus
I2
I.
12
t .......IlI.,II - .11111!l
.1111.,....1.1l!ll l11 1II1II ! 11 .
60
Annual
Tree 1102
24
36
48
60
I,
72
Tree 1004
11111
84
96
120
108
Sapranthuscampechianus
Supra-annual
132
Tree 2173
2-
.... .....
I
12
24
36
60
72
84
96
108
120
- . - .1
132
differentgraphical
onlysporadically
and briefly
(Figs. 2 and 3). Continualpatterns
haveseasonaltrendsforhigherprobabilityof heavyflowering
(e.g., in bothdryseasons
in Guatteriaaeruginosa(Fig. 3, upper half) and
both wet seasonsin Hamelia patens(see Fig. 11.7
in Newstromet al. 1993)).
The subannual flowering
patternis the most
irregularand poorlyunderstood.The pattern,as
shownin Protium
pittieri(Burseraceae),has several
unpredictable
flowering
cyclesperyear(Figs. 2 and
3). Althougha few yearshave only one cycleof
flowering,
mostyearshave several.This illustrates
of long timeseries(at least 5 yr)to
theimportance
fullydescribepatternsin tropicalphenology,althoughsome patternsmay be inferred
fromshort
termpopulationstudies.Three distinctive
features
this pattern:flowering
characterize
episodes occur
at anytimeof theyear,bothflowering
episodesand
nonflowering
intervals
varygreatlyin duration,and
Plant Phenology
CONTINUAL
Protium
pittieri
Lonchocarpus
oliganthus
Sapranthus
campechianus
Tree 1102
Tree 1004
Tree2173
JFMAMJ
JASOND
JFMAMJ
JASOND
JASOND
JFMAMJ
Tree 1043
1.0
SUPRA-ANNUAL
111111.I.
'11i111
Guatteria
aeruginosa
CIO
ANNUAL
SUB-ANNUAL
147
0.5
0.0-
JFMAMJJASOND
69
70
71
81
72
73
74
t8 75
>-4 76
77
.00.
.0000000000.so**.*.....
@001
----00----
78
00
*
@ 00
00.-
000
*0*
79
80
JFMAMJJASOND
000
0.
0.0
**0
000@
0 000000
00.000
@000O000
@0
@0
@0
0000
@0000
@
0
JFMAMJJASOND
JFMAMJJASOND
JFMAMJJASOND
Month
FIGURE 3. (a) Upper panel: Bar graphsshowingseasonalityin fourbasic flowering
patternsas proportionof years
forone treefrom
in whichheavyor lightflowering
occurredforeach monthof theyear.Each graphshowsflowering
1969 to 1980 fromeach of fourspeciesin the lowlandtropicalrain forestat the La Selva BiologicalStation.Light
dark shading = heavyflowering.(b) Lower panel: Matrixgraphs(yr by mo) showing
shading = lightflowering,
durationand date in fourbasic flowering
patterns.Each graphshowsone treeforthe same speciesas the seasonality
blanks= no flowering,
lightshaded circles= lightflowering,
bargraphsabove. Dark shaded circles= heavyflowering,
dots = missingdata.
Newstrom,Frankie,and Baker
148
Lonchocarpusoliganthus
Tree1003
Annual
12
2
2~
24
36
48
60
72
84
96
108
120
Tree 1004
Annual
12
24
36
48
60
84
72
96
108
120
132
Annual
144
Tree1196
..........
12
144
132
24
1 .......I
36
48
.. ..
. 11 .
60
. 11
72
11 1 .
84
96
108
120
144
132
1.0 1
00.
......
12
.. . .
24
.. . . .
36
. . . .
48
.. . .
60
l
. . . .
72
.. . . .
84
. . . .
96
.. .. .
108
III
.. . . .
120
. .
132
. .
.
144
flowering
everytwo to severalyearsThese patterns
have too fewdata to determinethe regularity,
duration,or seasonalityof flowering
and will not be
discussedfurtherin this paper (see discussionin
Newstromet al. 1993).
THE CONCEPTUAL
FRAMEWORK
Plant Phenology
149
Guarea rhopalocarpa
Sub - annual
ot
1III.
11.111
12
Male tree1020
24
.1,11
36
ll
.,
l .
48
,11
60
1,1
72
1 1 ,1
84
1I
108
96
Sub - annual
t:
12
24
36
48
60
72
1111,1,1~
84
11
~~~~~~~1
108
96
12
...
.. . .
..........
24
144
.;_
1.111
120
132
144
Femaletree1149
Sub - annual
0.H.....
132
Femaletree1048
oq
d~~~~~~~~~~~~~~
120
36
48
60
72
84
96
... ......
108
120
..
132
144
-f
1.0
os~~~~~~~~~
12
24
|
36
||
48
||
60
72
1|||1111
84
96
108
1 11 1110ll1l.I1 1111
120
132
144
rhopalocarpa
(Fig. 5), a dioeciousunderstory
treeat
La Selva, appearto have sufficient
populationlevel
synchrony
to producea subannualpopulationpatternwith 119 trees (Bullock et al. 1983). The
in thiscase,occursmorein thenonflowsynchrony,
eringintervalsthanin the flowering
episodes,suggestingthat conditionsinhibitingfloweringmay
governthe pattern(see Newstromet al. 1993 for
further
discussion).In contrast,moreasynchronous
populationswould producea morenearlycontinual
pattern,such as we have estimatedfromfourtrees
of Compsoneura
sprucei,an understory
dioecioustree
at La Selva (Fig. 6). In thisspecies,two typesof
individualpatterns,subannualand annual,appear
to be correlated
withgender(see Bullock 1982 and
Newstromet al. 1993), althoughmore data are
needed to confirmthis.The genderdifference
fol-
150
Newstrom,Frankie,and Baker
Compsoneurasprucei
Sub - annual
Male tree1009
2-
12
24
36
48
60
72
84
96
108
Sub - annual
120
132
144
Male tree1141
2-
1 I
i
11, I
12
I 111
.1
24
36
48
60
72
96
84
108
HI 11111
I IIIII I
,C
.4
132
144
Femaletree1118
Sub- annual
21-
120
I11,11
1I
I! 1III
H0-11.11.1l
0
12
24
36
48
60
72
84
96
108
120
132
144
Annual
Femaletree2054
. . . . . . I . . . . . . I . .... . . . . . I . . I
o . . .. ..
12
24
36
48
60
72
84
. . . . . . . . . . . . . . . .I. . . . . . I. . . . . . .
96
108
120
132
144
120
132
144
1.0 3.5
12
24
36
48
60
72
84
96
108
Plant Phenology
151
1983, Rathcke & Lacey 1985, Pleasants 1990, annual(Fig. 8). This mixedsequencehad no gaps,
Newstromet al. 1993). Changesin amplitudeof extensiveoverlap,and a strongunimodalseasonal
by Stiles(1978)
affectthe numbersand level of activity peak. This examplewas illustrated
flowering
of the pollinators(Bawa 1983, Rathcke& Lacey as an averageforthe fouryearsratherthana time
ofthespeciesmay series,butpresumably
1985). Finally,thepermutations
theorderofspeciesflowering
be retainedin the same orderfromyearto yearif eachyearchangesbecauseoftheinherent
irregularity
cued, as of subannualpatterns.The mixedpatternhas not
each speciesis stronglyand differentially
with markedregular beenwell-studied
is commonin environments
but itprobablydominatesin polfivetypesof pollinator linatorguildsoflowlandtropicalrainforest
seasons.We have identified
because
(Table 1).
guild patternsusingour classification
of the prevalenceof subannualflowering
patterns
patternat the (Newstromet al. 1993). The staggeredsequence
The staggeredannual flowering
guild level is one of the mostfamiliarbecauseit is maydominatein moreseasonalecosystems
suchas
so commonin the temperatezone. In the tropics, temperate
and tropicaldryforests.
The effects
of an
it occursin both wet and dryforests.The pattern overlappingmixedmultispecies
sequencewithunof annual populationpat- predictablespeciespermutations
comprisesa progression
on pollinatorspeternsin a sequenceof speciesthatextendsforonly cializationand foragingpatternshave not been inpart of the year.For example,in lowlandtropical vestigated.
rainforest
at La Selvabeetlepollinatedspeciesflower
Some mixedcontinualflowering
patternsat the
in a staggeredsequenceforpartof theyear(Young guildlevelhavedramaticamplitudepeaksat supraintervalor annualfrequencies.
1986, 1990). Duringthe nonflowering
This guildpatternhas beendegap the beetlesare dormant.In the tropicaldry scribedforthrippollinatedspeciesin Malaysia(Chan
forestin Guanacaste,Centrisand otherlarge bee & Appanah 1980; Appanah & Chan 1981; Appollinatedspeciesflowerin a staggeredsequence panah 1985, 1990; Yap & Chan 1990; La Frankie
offlowering & Chan 1991). Aftermanyyearsof sporadiclight
duringthedryseasonwhena profusion
a staggeredbut slightlyoverlappingseoccurson leaflesstrees(Frankieetal. 1976, 1983). flowering,
The bees are in diapauseduringthegap in thewet quence (Ashtonet al. 1988) of six Shoreaspecies
At thistime,
season.Whetheror not thesepatternshave signif- burstintofull,highintensity
flowering.
tested.The theshort-lived
icantoverlaphas not been statistically
thrippollinators
havean exponential
of speciesare similareach year.
permutations
populationexplosion.At othertimes,otherspecies
The staggered
continualflowering
patternat the thatflowermorefrequently
at low or intermediate
guildleveloccursinhermit
pollinated amplitudesmaintainthe thripsat low population
hummingbird
speciesat La Selva (Stiles1978). This patterncom- levels.
prisesa yearlongcontinualsequenceof 10 different
A specializedcontinualflowering
patternat the
specieswith annual populationpatterns(Fig. 7). guild level in figspeciescomprisesbothsubannual
Only one minorgap occurredin 1973 in thisex- and supra-annualindividualpatternsat the indiample whenCostusruber(species5) did notflower. vidual level(Miltonet al. 1982, Michaloud 1988,
These speciesdid not overlapsignificantly
(Stiles Windsoret al. 1989). In thiscase the guild level
1979, 1985; Cole 1981; Pleasants1990 and see is equivalentto the populationlevel because the
discussionin Newstromet al. 1993). Yearly bi- pollinationsystemis speciesspecific.The continual
modal peaks in amplitudeof flowering(Fig. 7, patternat the guild level is essentialforfig-wasp
withhermithumming- survivaland thesubannualpatternat theindividual
lowerpanel) are correlated
bird breedingand moultingtimes (Stiles 1975, level may be selectedbecause it enhancesthe pol1977, 1978, 1980, 1985). The orderof permu- linatorattractant
and promotesoutcrossing
(Janzen
tationsof specieswas similareach yearwithonly 1979, Bronstein1989, Frank 1989, Bronsteinet
minorvariations(Fig. 7).
al. 1990, Newstromet al. 1993).
The mixed continualflowering
patternat the
guild level withannual cyclesof amplitudepeaks THE COMMUNITY LEVEL.-Although the community
withthestaggered
contrasts
continualpatternmain- level pattern has been examined for a number of
ly because of the extensiveoverlapand the disor- lowlandtropicalrainforests
(e.g.,Koelmeyer1959,
dered permutationof species each year. For ex- Medway 1972, Dieterlen1978, CruzAlencaretal.
ample,27 speciesofplantspollinatedbynonhermit 1979, Putz 1979, Van Schaik 1986) the rangeof
hummingbirds
at La Selva (Stiles 1978), consistof diversity
in populationand individualpatternshas
flow- not been well described.The profileof individual
overlappingpopulationswithmanydifferent
eringpatternsincludingcontinual,subannual,and patterns,
calculatedas therelativeabundanceofeach
Newstrom,Frankie,and Baker
152
1
*6000
060
*660
e00
060
060
060
006600000
06
106
as
6S
66
0 6
a@
60
10
66
@6
060
00600
060
0 6
JFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASOND
0.6
C)
0.4-
C
C
o
0.2-
0.
J FMAMJ
J AS ONDJ
FMAMJ
J AS ONDJ
FMAMJ
J ASONDJ
FMAMJ
J AS OND
typeof flowering
patternforLa Selva, shows that
moretreeshad subannual(55%) and annual(29%)
flowering
patternsthancontinual(7%) and supraannual (9%) ones (Fig. 9). Within the treecommunityat La Selva, canopyand subcanopystrata
have different
profiles(Newstrom et al. 1991).
Differenttypesof tropicalrain forestsmay have
different
profilesin relationto changesin rainfall
distribution
or floristic
composition.For example,
supra-annualflowering
patternsmay dominatein
dipterocarpforestsof Malaysia. Major ecosystems
in phenologicalprofiles.For
show largedifferences
instance,temperateforestshave annualcommunity
patternswithspecieshavingtwo main population
patterns(annual and supra-annual)in contrastto
lowland tropicalrain foreststhat have continual
Plant Phenology
-a
Af
Aft8
all
communitypatternswith species representing
fourtypesof populationpatterns.
sS,-
3~~~~
61
717
8
10
19
15
21
16
122
17
23
18*24
19
20
21
22
23
24
26
27
!!=
J F MAM
0.6
J J A S ON D
00
*~
*_14
0.2-
0.0
J FMAMJ
153
J AS OND
patternat the
FIGURE 8. Mixed continualflowering
guild level in nonhermithummingbirdfood plants averaged over 4 yrs from 1971 to 1975 in the lowland
tropicalrainforestat the La Selva BiologicalStation.The
guild patterncomprisescontinualfloweringin species
in speciesnumber
number1 and 2, subannualflowering
in speciesnumber7 to 27.
3 to 6, and annual flowering
The populationsof 27 speciesfloweredwithno gaps and
extensiveoverlap.The permutationspresumablychange
timein
each yearbecause of the unpredictableflowering
subannualpatterns.Speciesare: I = Cephaelistomentosa,
2 = Hamelia patens, 3 = Symzphonia
glohulifera,4 =
Colurmnea
5 = Colusmnea
linearis,6 = Vrienicaraguensis,
sea gladioliflora,7 = Aechmeamexicana,8 = S-hlegelia
sp., 9 = Aechmeamaria-reginae.10 = Gesneriac-eaesp.,
11 = Gurania levyana, 12 = Gurania c-ostaricensis,
13
= Odontonema
14 = Aechmeanudi-aulis,15 =
tubiforme,
Renealmiaexalta, 16 = Heliconiamariae,17 = Erythrina
cochleata,18 = Cephaeliselata, 19 = Heliconialatispatha.
20 = Besleriasp., 21 = Renealmiacernua,22 = Guzm,ania
23 = Warscewicziacoccinea,24 = Heli-onia
monostachia,
imbricata,25 = Heliconiasarapiquensis,26 = Alloplectus
coriaceus,27 = Razisea spicata. (Adapted fromFigure4
in Stiles 1978.)
154
Newstrom,Frankie,and Baker
in a continualpatternwithlightestflowering
in the
dryseasons,while in the tropicaldry forest,trees
of thisspeciesflowerin an annual patternwithno
in the dryseason (Frankieet al. 1974).
flowering
This patternshiftsuggeststhat lack of moisture
inhibitsflowering
in thisspecies.The influenceof
on flowering
patternshas been inhydroperiodicity
vestigatedinmanytropicaldryforest
species(Borchert 1980, 1983, 1991; Reich & Borchert1982,
1984) but has notbeen studiedin lowlandtropical
rainforestspecies.
The reversepatternshiftoccursin otherspecies.
These changeto a lowerfrequency
of flowering
in
thewettropicsthanin thedrytropics.Forexample,
in both Andira inermisand Ceiba pentandratrees
flowerlessfrequently,
in raresupra-annualpatterns,
inside the lowland tropicalrain forestand more
in alternate
frequently,
supra-annualpatterns,
in the
tropicaldryforestand along edges of the lowland
tropicalrainforest(see Newstromet al. 1993). In
Africa,C. pentandraflowered
regularly
in an annual
patternin the dry forestand in a supra-annual
patternin thewet forest(Baker 1965). Shoreaspecies in Malaysiademonstrate
a similarpatternwith
treesfloweringmost oftenand regularlyin drier
in wet forests,
forests,
supra-annually
and hardlyat
all in swamp forests(Yap & Chan 1990). This
suggeststwopossiblemechanisms:
a dryperiodmay
be requiredforfloralbud induction("xeroinduction, Bernieretal. 1981) orhigherlightconditions
may promotegreaterflowering
frequency.Experimentalevidencefor"xeroinduction'of flowersin
the lowland tropicalrain forestexistsforthe herbaceous Geophilarenaris(Bronchart1963, Bernier
et al. 1981) but thishas not been investigated
for
trees.
A change fromirregularsubannual flowering
patternto two regularcrops per yearwith introduction of droughthas been reportedfor Citrus
trees(Monselise& Goldschmidt1982) but, otherwise,reportsofchangesinvolvingsubannualfloweringarerarebecausethispatternhas notpreviously
been well recognized.
CONCLUSIONS
The effectiveness
of a classification
schemedepends
ofthecriteria
that
on severalfactors:theimportance
are givenpriority
fordelineatingcategories,
thedegreeofsimilarity
amongmembersin each category,
and the degreeof difference
amongcategories(i.e.,
The more consistent
frequencyof intermediates).
the associationsamong descriptorsfor categories,
If the charthe more successfulthe classification.
6050 -
40 z
30 g
0
20-
10
acteristics
are distributedrandomlyamong classes
or if classesintergradein a continuum,the classificationhas less usefulness.The most important
stricture
about classifications,
however,is thatthey
usedthattheylimitcreative
do notbecomeso rigidly
perceptionwhenevernew contextsare moreappropresent
priate(Bohm & Peat 1987). We therefore
as a convenient
thisclassification
wayto bringorder
to the complexityof phenologicalpatternsin the
wet tropicsand not as a replacementforprevious
classifications.
has
The main contribution
of thisclassification
in tropicalpatternsat
been to clarify
thedifferences
different
levelsof analysisand to providea logical
The resultsof our quansystemforquantification.
titativedescriptionforpatternsusing the variables
of frequency,
duration,amplitude,date,
regularity,
will be publishedelsewhere.Using
and synchrony,
frequency
of "on"/'off" cyclesbased on an annual
time scale as the criterionfordividingthe classes
ratherthan yearlyseasonal averagesportraystemforirregporal sequencesmoreclearly,particularly
ular subannualand supra-annualpatterns.The explicittimeand amplitudescalespermitstandardized
comparisonsamong studies. For example, differ-
Plant Phenology
155
LITERATURE CITED
E., AND P. A. HUXLEY. 1990. The applicationof phenologyto agro-forestry
research.ICRAF Working
Paper No. 63: 1-50.
APPANAH, S. 1982. Pollinationof androdioeciousXerosperrnum
intermedium
Radlk. (Sapindaceae) in a rainforest.
Biol. J. Linn. Soc. 18: 11-34.
1985. Generalflowering
in the climaxrain forestsof South-eastAsia. J. Trop. Ecol. 1: 225-240.
1990. Plant-pollinator
in a Malaysianrain forest.In K. S. Bawa and M. Hadley (Eds.).
interactions
Reproductivebiologyof tropicalforestplants,pp. 85-101. UNESCO and Parthenon,Paris, Franceand
Carnforth,
England.
Malays. For. 44: 234-252.
, AND H. T. CHAN. 1981. Thrips:the pollinatorsof some dipterocarps.
ASHTON, P. S. 1988. Dipterocarpbiologyas a window to the understanding
of tropicalforeststructure.
Annu.
Rev. Ecol. Syst. 19: 347-370.
, T. GIVNISH, AND S. APPANAH. 1988. Staggeredflowering
in the Dipterocarpaceae:
new insightsintofloral
inductionand the evolutionof mast fruiting
in the aseasonaltropics.Am. Nat. 132: 42-66.
AUGSPURGER, C. K.
1980. Mass-flowering
of a tropicalshrub (Hybanthusprunifolius):influenceon pollinator
attraction
and movement.Evolution34: 475-488.
AKUNDA,
156
Newstrom,Frankie,and Baker
effects
of tropicalplants:experimental
of pollinatorsand seed predators
* 1981. Reproductivesynchrony
(Violaceae). Ecology62: 775-788.
on Hybanthus
prtnifolius
* 1983. Phenology,flowering
synchrony,
and fruitset of six neotropicalshrubs.Biotropica15: 257-267.
product.In D. Brokesha
BAKER, H. G. 1965. The evolutionof thecultivatedkapok tree:a probableWest African
Studies,
(Ed.). Ecologyand economicdevelopmentin tropicalAfrica,pp. 185-216. InstituteforInternational
of California,Berkeley,California.
ResearchSeriesno. 9, University
in tropicalplants.In C. E. Jonesand R. J. Little(Eds.). Handbook of
BAWA,K. S. 1983. Patternsof flowering
experimental
pollinationbiology,pp. 394-410. Van NostrandReinhold,New York, New York.
, AND M. HADLEY (Eds.). 1990. Reproductivebiologyof tropicalforestplants.UNESCO and Parthenon,
England.
Parisand Carnforth,
R. A., J. M. CHAMBERS, AND A. R. WILKS. 1988. The new S language.Wadsworthand Brooks/Cole,
BECKER,
PacificGrove,California.
and distribution
of Ficus.Experientia(Basel) 45: 605-611.
BERG,C. C. 1989. Classification
Volume I: theinitiationof flowers.
of flowering.
BERNIER, G., J-M. KINET, AND R. M. SACHS. 1981. The physiology
CRC Press,Inc., Boca Raton, Florida.
BantamBooks, New York, New York.
BOHM, D., AND F. D. PEAT. 1987. Science,order,and creativity.
and age-related
changesofshootgrowthin seasonaland nonseasonalclimates.
BORCHERT, R. 1978. Feedbackcontrol
pp. 497-515. Cambridge
In P. B. Tomlinsonand M. H. Zimmerman(Eds.). Tropicaltreesas livingsystems,
Press,Cambridge,England.
University
poeppigiana0. F. Cook. Ecology61:
of tropicaltrees:Erythrina
. 1980. Phenologyand ecophysiology
1065- 1074.
in tropicaltrees.Biotropica15: 81-89.
1983. Phenologyand controlof flowering
p. 95. Vol. 5. CRC Press,Inc.,
In A. H. Halevy (Ed.). CRC handbookof flowering,
1986. Erythrina.
Boca Raton,Florida.
of trees,pp. 219-243.
and dormancy.In A. S. Raghavendra(Ed.). Physiology
1991. Growthperiodicity
JohnWiley & Sons, New York, New York.
surle developpement
de Geophilarenarisde Wild. etTh. Dur. dans les conditions
BRONCHART, R. 1963. Recherches
equatorial.Influencesur la mise a fleursd'une perteen eau disponible
ecologiquesd'un sous-boisforestier
du sol. Memoiresde la SocieteRoyaledes Sciencesde Liege. Ser. 5. 8(2): 1-179.
45: 622-637.
BRONSTEIN, J. L. 1989. A mutualismat the edge of its range.Experientia
, P. H. GOUYON, C. GLIDDON, F. KJELLBERG, AND C. MICHALOUD. 1990. The ecologicalconsequencesof
in monoeciousfigs:a simulationstudy.Ecology71: 2145-2156.
flowering
asynchrony
in theneotropicaldioecioustreeCompsoneura
sprucei.
and reproduction
BULLOCK, S. H. 1982. Populationstructure
Oecologia (Berl.) 55: 238-242.
and sexualdimorphismin Guarea rhopalocarpa
, J. H. BEACH, AND K. S. BAWA. 1983. Episodicflowering
Radlk. (Meliaceae) in a Costa Rican rainforest.Ecology64: 851-862.
I. Floweringbiology.
biologyof some Malaysiandipterocarps.
CHAN, H. T., AND S. APPANAH. 1980. Reproductive
Malays. For. 43: 132-143.
in Zamia skinneri,
patternsof reproduction
CLARK, D. A., AND D. B. CLARK. 1987. Temporaland environmental
a tropicalrain forestcycad.J. Ecol. 75: 135-149.
California.
CLEVELAND, W. S. 1985. The elementsof graphingdata. WadsworthPublishingCo., Monterey,
and flowering
phenologies.Am. Nat. 117: 993-997.
COLE, B. J. 1981. Overlap,regularity,
and contingency
of periodicphenomena.Ecology55: 1148-1153.
constancy
COLWELL, R. K. 1974. Predictability,
CROAT, T. B. 1975. Phenologicalbehaviorof habit and habitatclasseson Barro Colorado Island (Panama and
Canal Zone). Biotropica7: 270-277.
Press,Stanford,California.
. 1978. Floraof BarroColorado Island. StanfordUniversity
em floresta
CRUZALENCAR, J. DA, R. ANICETA DE ALMEIDA, N. P. FERNANDES. 1979. Fenologiade especies florestais
tropicalumida de terrafirmena Amaz6nia Central.Acta Amazonica9: 163-198.
DIETERLEN, F. 1978. Zur Phanologiedes aquatorialenRegenwaldesin Ost-Zaire(Kivu). Diss. Bot. 47: 5-120.
is a suicidalneotropicaltree.Nature 268: 624-626.
FOSTER, R. B. 1977. Tachigalia versicolor
dynamicsof figcommunities.Experientia(Basel) 45: 674-680.
FRANK, S. A. 1989. Ecologicaland evolutionary
1974. Comparativephenologicalstudiesof treesin tropicalwet
FRANKIE, G. W., H. G. BAKER, AND P. A. OPLER.
and dryforestsin the lowlandsof Costa Rica. J. Ecol. 62: 881-919.
of
P. A. OPLER, AND K. S. BAWA. 1976. Foragingbehaviorof solitarybees: implicationsforoutcrossing
a neotropicalforesttreespecies.J. Ecol. 64: 1049-1057.
and organizationof the largebee
- W. A. HABER, P. A. OPLER, AND K. S. BAWA. 1983. Characteristics
pollinationsystemin the Costa Rican dry forest.In C. E. Jones and R. J. Little (Eds.). Handbook of
experimental
pollinationbiology,pp. 441-447. Van NostrandReinhold,New York, New York.
in tropicalBignoniaceae.Biotropica6: 64-68.
GENTRY, A. H. 1974. Floweringphenologyand diversity
Costa Rican dryforestSphingidae.
HABER, W. A., AND G. W. FRANKIE. 1989. A tropicalhawkmothcommunity:
Biotropica21: 155-172.
to their
HUXLEY, P. A. 1983. Phenologyof tropicalwoody perennialsand seasonal crop plants with reference
pp. 503-525.
systems.In P. A. Huxley (Ed.). Plantresearchand agroforestry,
managementin agroforestry
ICRAF, Nairobi.
Annu. Rev. Ecol. Syst.7: 347-391.
JANZEN, D. H. 1976. Why do bamboos wait so long to flower?
Plant Phenology
157
1990.
Null-model tests for competitive displacement: the fallacy of not focusing on the whole
community.Ecology71: 1078-1084.
POWLESLAND, M. H., M. PHILIPP, AND D. G. LLOYD. 1985. Floweringand fruiting
patternsof threespecies of
Melicytus(Violaceae) in New Zealand. N. Z. J. Bot. 23: 581-596.
in New Zealand montaneshrubs.
PRIMACK, R. B. 1980. Phenological
variationwithinnaturalpopulations:flowering
J. Ecol. 68: 849-862.
1985. Patternsof flowering
phenologyin communities,populations,individuals,and singleflowers.In
J. White (Ed.). The populationstructure
ofvegetation,
pp. 571-593. Dr. W. Junk,Dordrecht,Netherlands.
PUTZ,F. E. 1979. Aseasonalityin Malaysiantreephenology.Malays. For. 42: 1-24.
RATHCKE, B. 1983. Competitionand facilitation
amongplantsforpollination.In L. Real (Ed.). Pollinationbiology,
pp. 305-329. AcademicPress,New York, New York.
plants.Annu. Rev. Ecol. Syst. 16: 179-214.
, AND E. P. LACEY. 1985. Phenologicalpatternsof terrestrial
RAVEH,A., AND C. S. TAPIERO. 1980. Periodicity,
and the categoriesof qualitativetime
constancy,
heterogeneity
series.Ecology61: 715-719.
of the tropicaltree,Tabebuja neochrysantha
REICH, P. B., AND R. BORCHERT. 1982. Phenologyand ecophysiology
(Bignoniaceae).Ecology63: 294-299.
.
1984. Water stressand treephenologyin a tropicaldryforestin the lowlandsof Costa
, AND
Rica. J. Ecol. 72: 61-74.
RICHARDS, P. W.
1952. The tropicalrainforest.
CambridgeUniversity
Press,Cambridge,England.
SARMIENTO, G., AND M. MONASTERIO.
1983. Life formsand phenology.In F. Bouli&re.(Ed.). Ecosystemsof the
world:tropicalsavannas.Vol. 13: 79-108.
SILVERTOWN, J. W. 1980. The evolutionary
ecologyof mastseedingin trees.Biol. J. Linn. Soc. 14: 235-250.
environments:
STEARNS, S. C. 1981. On measuringfluctuating
predictability,
constancyand contingency.
Ecology
62: 185-199.
STILES, F. G. 1975. Ecology,flowering
phenology,and hummingbirdpollinationof some Costa Rican Heliconia
species.Ecology56: 285-301.
thefloweririg
. 1977. Coadaptedcompetitors:
seasonsofhummingbird-pollinated
plantsin a tropicalforest.
Science 196: 1177-1178.
. 1978. Temporalorganizationof flowering
among the hummingbirdfoodplantsof a tropicalwet forest.
Biotropica10: 194-2 10.
. 1979. Reply to Poole and Rathcke.Science203: 471.
158
Newstrom,Frankie,and Baker
APPENDIX:
TERMINOLOGY
patterns.
Quantitativedescriptions
definedand consistently
used termsfordescribing
Tropicalphenologylacksprecisely
willbe published
duration,amplitude,date,and synchrony
regularity,
of thepatternsusingthevariablesoffrequency,
independent,we are conductinga studyof theirinter-relationship.
elsewhere.As thesevariablesare not necessarily
and fruiting)
To avoid proliferation
of newtermswe use thesame termsforanyphenologicalevent(leafing,flowering,
in thefollowing
can be substitutedforflowering
leafingand fruiting
and forpatternsat all levelsof analysis;therefore,
definitions.We have avoided using termsthat introduceconfusionwith literaturefromotherfieldssuch as tree
of oscillationsin physics.For thisreason,the termsperiod,periodic
and the description
development,chronobiology,
as used in timeseriesanalysis.The
and phase are not used here.We preferto retaintheirmathematicaldefinitions
of flowering
and nonflowering
intervalreplacethedefinitions
phase
definitions
of flowering
episodeand nonflowering
given in Newstromet al. (1993).
on a tree,or flowering
or intensity
of response,such as numberof flowers
Amplitude is the quantityof activity,
amplitude
episodemayhave multipleflowering
A flowering
treesin a population,or speciesin a guild or community.
(e.g., Frankieet al. 1974, Opler et al.
peaks which can be measuredor estimatedqualitativelyor quantitatively
plants
however,may be practicalonlyin understory
1980, Augspurger1983). Countingnumberof inflorescences,
obscuremoresubtlefluctuations.
ariseshereas broadercategories
(e.g.,Bullocketal. 1983). The problemofresolution
episode
Cycle refersto the repeatingsequence of an eventthat is "on" and then "off' such as a flowering
followedby a nonflowering
interval.Each repetition
of thecyclemaybe variablein length(as in subannualflowering)
patterns,a largercycle
or nearlyequivalent(as in annualflowering).
For some of the morecomplexannualflowering
intervalswithinit, whichwe refer
of one majorflowering
episode per yearcontainsbrief"pauses" of nonflowering
to as the pulsed annualpatternafterOliveira et al. (1991). Monocarpicplantsdo not have repeatingcyclesat the
Foster1977; and some
cycleper lifetime(e.g., Tachigalia versicolor,
individuallevelbut ratheronlyone reproductive
bamboo species,Janzen 1976).
categoriesof
Duration is the lengthof timea unitremainsin a givenportionof the cycle.In our classification,
durationforflowering
(> 1 mo and < 5 mo), and extended(> 5 mo). The
episodesare brief(< 1 mo), intermediate
episode or
the durationof flowering
problemof resolutionarisesbecause a long censusintervalwill overestimate
of the numberof cyclesper unit time. Daily observationsare
nonflowering
intervalleadingto an underestimation
usuallyimpractical,however,and a 2 wk or 1 mo censusintervalis commonlyused in phenology.
episode.
Episode is the portionof the cycleduringwhichthe eventis "on" such as flowering
classesbased on an annual
frequency
Frequency is the numberof cyclesper unittime.We definedfourarbitrary
time scale:
continual= alwaysin flowerwith no or fewbriefinterruptions;
subannual= > 1 cycleper year;
Plant Phenology
159