sign in sign up
<<
Home , Ceratosolen, Ficus, Ficus aurea, Ficus variegata (plant), Moraceae

Joumalof (I1996) 23, 467-475

Phenologyof Ficusvariegata in a seasonalwet tropicalforest at Cape Tribulation,

HUGH SPENCER', GEORGE WEIBLENI 2* AND BRIGITTA FLICK' 'Cape TribulationResearch Station, Private Mail Bag5, Cape Tribulationvia Mossman,Queensland 4873, Australiaand 2 The Harvard UniversityHerbaria, 22 Divinity Avenue,Cambridge, Massachusetts 02138, USA

Abstract. We studiedthe phenologyof 198 maturetrees dioecious , female and male initiatedtheir of the dioecious figFicus variegataBlume () in a maximalfig crops at differenttimes and floweringwas to seasonally wet tropical rain forestat Cape Tribulation, some extentsynchronized within sexes. Fig productionin Australia, from March 1988 to February 1993. the female (seed-producing)trees was typicallyconfined productionwas highlyseasonal and correlatedwith rainfall. to the wet season. Male (-producing)trees were less Treeswere annually deciduous, with a pronouncedleaf drop synchronizedthan femaletrees but reacheda peak level of and a pulse of new growthduring the August-September figproduction in the monthsprior to the onset of female drought. At the population level, figs were produced figproduction. Male treeswere also morelikely to produce continuallythroughout the study but there were pronounced figscontinually. Asynchrony among male figcrops during annual cyclesin figabundance. Figs were least abundant the dry season could maintainthe pollinatorpopulation duringthe early dry period (June-September)and most under adverseconditions through within- and among- abundant fromthe late dry season (October-November) wasp transfers. throughthe wet season (December-April).The annualpeak Key words. Australia, Cape Tribulation,dioecy, in reproductionactually reflectedtwo staggeredpeaks variegata, figs, flowering asynchrony, phenology, arisingfrom gender differencesin fig phenology.In this seasonality.

Seasonalityin fig productionhas oftenbeen noted in INTRODUCTION phenologicalstudies that report asynchronous flowering and Fig treeshave complexreproductive phenologies, resulting continualfig production at thepopulation-level (Newton & in part from the distinctivesystem of . The Lomo, 1979; Milton et al., 1982; Baijnath & Ramcharun, pollinationof figs,being accomplished only by -specific 1983;Corlett, 1984, 1987, 1993; Nair & Abdurahiman,1984; of the familyAgaonidae, is regardedas one of the van Shaick, 1986; Kjellberget al., 1987; Bronstein,1989; fewdocumented cases of an obligatorymutualism between Windsoret al., 1989). The degreeof seasonalityin fruiting a and its (Bronstein, 1992). The fig patternsvaries geographically, from a slighttrend in () is an enclosed receptacle containing many (Milton et al., 1982) to more extremecases in Southern flowersand fig wasps, whose larvae depend entirelyon France(Kjellberg et al., 1987)and (Bronstein,1989). developing fig seeds for food. The short-lived,pollen- The breedingsystem of a figspecies (eithermonoecious carryingfemale wasps emergefrom ripe figs,and must or dioecious) can also influencereproductive phenology, locate otherreceptive figs in whichto lay theireggs. This especiallyin seasonal habitats.In monoecious species,fig interactionrequires that figs in differentdevelopmental seeds and wasps are produced withinthe same fig. In phasesare continuallypresent in a population;otherwise the dioecious species, however,wasp and seed productionis figwasp populationwould become locally extinct. Flowering segregatedbetween male and female trees, respectively asynchronyand continualfruiting at the populationlevel, (Valdeyron& Lloyd, 1979; Berg,1989; Weiblen,Spencer & combinedwith flowering synchrony and sub-annualfruiting Flick, 1995). Many authorshave suggestedthat seasonal at theindividual level, is characteristicof figs(Janzen, 1979; climaticvariation is less problematicfor dioecious figs than Newstrom,Frankie & Baker, 1994). However,many cases formonoecious figs (Valdeyron & Lloyd, 1979; Kjellberget of within-treeasynchrony have been documented(Baijnath al., 1987;Bronstein, 1989; Kjellberg & Maurice,1989; Patel, & Ramcharun,1983, 1988; Bronstein,1989; Bronstein& Hossaert-McKey& McKey, 1993). In dioecious figs,each Patel, 1992; Corlett,1984, 1987, 1993). sex can take advantage of differentconditions favouring eitherseed or wasp production.Female trees flowerand fruitduring conditions optimal for seed productionand * Correspondingauthor. dispersal. Male trees produce figs more often than the

( 1996 BlackwellScience Ltd 467

This content downloaded from 134.84.10.156 on Tue, 15 Jul 2014 17:19:07 PM All use subject to JSTOR Terms and Conditions 468 HughSpencer, George Weiblen and BrigittaFlick 70 900 1- 800 60-60 iTL 700 50 -C 600 c 40 500 o ,^'' t40 400 (D, 30 co

H 2 20~~~~~~~~~~~~~~~~0 / 0

100

jun jul aug sep oct nov dec jan feb mar apr may jun Month

FIG. 1. The mean monthlyrainfall (mm) and mean monthlypercentage of fig-bearingtrees in a populationof 198 reproductiveindividuals of E variegata.Rainfall averages are from1980-92 data forCape Tribulation.Bars indicatestandard errors. females,maintaining the local pollinatorpopulation under Temperaturesrange froma minimumof 10?C in the dry adverse conditionswhile donating pollen to female figs season to a maximumof 40?C in the wet season, withhigh under optimal conditions. Currently,there is much humiditythroughout the year. speculationbut few data to supporta hypothesisthat the The humid and seasonally wet climate supports lush evolutionarytransition from monoecy to dioecyrepresents vegetationclassified by Tracey (1982) as lowland complex an adaptation to seasonal environments(Corlett, 1987, mesophyllvine forest. The region is among the most 1993; Kjellberget al., 1987; Berg, 1989). floristicallydiverse in Australia,with over 125 species of Amongmore than 300 speciesof dioeciousfigs worldwide treesper ha (A. Small, unpub. data). Figs are abundant, (Berg, 1989), fewhave been studiedin detail (see appendix bothas hemi-epiphyticstranglers and as free-standingtrees. in Bronstein,1989). The fruitingphenologies of several Of the twelveFicus species reportedfor Cape Tribulation dioecious species are correlatedwith seasonal conditions, (Jessup& Guymer,1985), E variegataand E congestaare such as: the edible figE carica,in France (Kjellberget al., the most commondioecious species. 1987), E fistulosain Hong Kong (Corlett, 1987) and E grossularioidesin Singapore(Corlett, 1993). These studies BIOLOGY OF also show some degree of sexual differentiationin phenologicalpatterns, but thereis a need for more data E variegata is a pioneer tree mostly occurringalong describingthe phenologicalresponses of dioecious figsto watercourses,although some individuals are found in seasonal variability.With this objective in mind, we relativelyopen forestas isolated trees(Corner, 1933). The examinedthe phenologyof a dioecious figpopulation in a older trees are usually buttressed,particularly on river seasonallywet tropical environment. We selectedE variegata banks,where the more elaborate buttresses reach up to 4 m because of its abundance at the studysite, and because a above the ground.In undisturbedrain forest,canopy trees parallelstudy suggested that this species might be a vitalfood can attain trunkdiameters of up to 1 m at breastheight. resourcefor the local tube-nosedbat, Nyctimenerobinsoni Mature trees are cauliflorous,bearing a profusionof figs (unpub. data, H. Spencer). on the trunkand major branches. Mature fruitare about 30-40 mm in diameterand are borne on pedicels 15-25mm in lengthwhich arise from STUDY SITE clustersof woody spurs. Fig-bearing spurs increase in length The study area, Cape Tribulation,is situatedin the far and branchingcomplexity with age. Spursrange from a few northeast of Queensland,Australia on the Coral Sea coast mmlong, with one or twofigs, to over 150mm with multiple (16?05' S, 145?27'E). Cape Tribulationis backedby a coastal branchesbearing more than thirty figs each. The positioning range,rising to 1000metres, enclosing a shalloweast-facing of thefig-bearing spurs within trees is highlyvariable. Some basin which contains the study site. The basin floor is treesproduce figs predominantly along the trunk, and others comprisedof unconsolidatedrock and sediments,with the produce figsalong the branches.Crop size is also highly result that many streams are ephemeral and flow variable among individuals,ranging from trees with fewer undergroundduring the dry season. The local climateis than ten spurs, to trees with profuse spurs capable of seasonally wet and tropical,with an average rainfallof carryinghundreds of figsper metreof branchlength. 4000mm per year, falling mostly in the period from E variegata is morphologicallygynodioecious and December to May (Figs 1 and 2a). May to Novemberis functionallydioecious, with populations comprised of the dryperiod, with as littleas 100mm rainfallper month. femaleindividuals and hermaphrodites(Weiblen, Spencer

? BlackwellScience Ltd 1996,Journal of Biogeography, 23, 467-475

This content downloaded from 134.84.10.156 on Tue, 15 Jul 2014 17:19:07 PM All use subject to JSTOR Terms and Conditions Ficusvariegata phenology inAustralia 469

(a) 1001 0 -1000 9~~~

XE 80 800

0 Ci) cD 60 0600 K

40 o19 1199

120 200 (5

0 1 *0 (b) MAMJJASONDJFMAMJ JASONDJFMAMJ JASONDJFMAMJ JASONDJF 1989 1990 1991 1992 1993

(b) 21 100- - 100 co

Q0080 cD 80 0o CO CD

U)60 0606 ~~~~~~~~~~~0cD E 00 0 a1)

'0 40 40 00

ar) 0 C 2 20 20 =r

MAMJJASONDJFMAMJ JASONDJFMAMJ JASONDJFMAMJ JASONDJF 1989 1990 1991 1992 1993

FIG. 2. (a) Monthlyrainfall and population-levelfruiting phenology of F variegata.The percentageof fig-bearingtrees in the population and totalrainfall (mm) are reportedfor each monthfrom March 1989 to February1993. At thebottom of thefigure, black bars approximate the annual wet seasons and whitebars indicatethe interval between rainy episodes. (b) Seasonal patternsof femaleand male figproduction at Cape Tribulation.Percentages of fig-bearingtrees are based on thirtymale and fifty-fivefemale trees.

& Flick, 1995). For reasons outlinedin Weiblen,Spencer stylesare long and the wasp is unable to reach the ovules, & Flick (1995), we referto the two sexes of treesas female but she stillpollinates a fractionof the figflorets. Female and male. Female fruithave a sweetodour whichis absent wasps (foundresses)presumably die withinthe figcavity. in male .Female fruitcolour variesfrom green to red, Wasps enteringfemale figs do not leave offspringbut they and does not to appear to be correlatedwith fruit maturity. do pollinatethe florets that produce seed. In contrast,male As with otherfigs, E variegatais pollinatedby a host- figs produce no seeds; instead they host the pollinator specific agaonid wasp (Wiebes, 1994). offspringand donatepollen to femalefigs (Weiblen, Spencer appendiculatusMayr enters the fig (syconium) at the & Flick, 1995). appropriatetime of femaleflower receptivity, by pushing throughthe closed ostiolar bracts and into the syconium SAMPLING PROCEDURE cavity.Once inside,the wasp pollinatesthe stigmatic surfaces of the fig floretswith pollen collected from her natal At Cape Tribulation,218 maturetrees of F variegatawere syconium.In the figsof male trees,the stylesare shortand located and numberedwithin the studysite, which covered the wasp lays eggs in the vicinityof figovules by inserting approximately140 ha. The leafing,flowering and fruiting her ovipositorinto the style.In the figsof femaletrees, the status of each tree was assessed using a six-pointscoring

? BlackwellScience Ltd 1996,Journal of Biogeography, 23, 467-475

This content downloaded from 134.84.10.156 on Tue, 15 Jul 2014 17:19:07 PM All use subject to JSTOR Terms and Conditions 470 HughSpencer, George Weiblen and BrigittaFlick

TABLE 1. Indices for leaf maturity,fig abundance and figmaturity for E variegatawere estimatedindependently. Fig abundance was estimatedas a percentageof the totalcrop capacityfor each individualtree. Fig diameterserved as an indicatorfor fig maturity stage, since the size of figsis roughlycorrelated with the developmentalphases (A-E; Galil & Eisikowitch,1968).

Value Leaf maturityindex Fig Fig diameterindex Fig maturity(developmental phase) abundance index

0 No No figs No figs 1 Buds 0-5% 1-3 mm Pre-receptivephase: earlyfloral development; ostiole closed (A) 2 New leaves 5-10% 4-10 mm Female phase:female receptivity; wasps penetrate ostiole, pollinate,and oviposit(B) 3 Mature leaves 10-20% 11-30mm Interfloralphase: figseeds and wasp larvae develop (C) 4 Mixed mature& 20-40% >30 mm Male phase: pollen-carrying,fertilized female wasps emerge senescentleaves frommale figs;female figs become fleshy(D) 5 Senescentleaves 40-100% Fallen figs Post-floral:female figs dispersed; male figsdrop fromtrees (E)

procedure(Table 1). Given the presenceof asynchronous averaged over a 4-year period. Although there was crops on manytrees, we recordedthe stage of maturityfor considerablevariation in fruitingamong years,an obvious the most abundant age class of fig on the tree but also seasonal fruitingpattern for the populationwas indicated recordedany otherstages of figmaturity. by thepercentage of treesthat carried figs each month(Fig. Fig abundance is difficultto estimatein a cauliflorous 2a). The onset of fig productionat the population level tree,given the dense packing of on thehighly branched precededthe onset of the rainyseason by about 2 months, spurs.We used a percentilescale, based on the maximum but the peak period of population-levelfig production crop size that a particulartree was likelyto support.We coincidedwith the wet season in each year. assessed the abundance of figsin relationto the densityof fig-bearingspurs within the tree,and estimatedabundance SEXUAL DIFFERENCES IN REPRODUCTIVE as a percentageof the total crop capacity for that tree. PHENOLOGY Percentageswere then assigned a rank between0 and 5 (Table 1). For example,if everyspur on a tree bore figs The timingof peak figproduction at the populationlevel then the tree was consideredto be producingat 100% of differedbetween male treesand femaletrees (Fig. 2b). Most its capacity,and was ranked'5' forfig abundance. male treesinitiated fig production about 2 monthsbefore The presenceof asynchronousfig crops within individual the peak in figproduction for femaletrees. The bimodal trees was recordedby a yes (1) or no (0) response. For patternof figinitiation in E variegatawas consistentacross example, an asynchronouscrop mightconsist of figsin all 4 years of the study,and is suggestiveof within-sex maturitystages 2 and 5 withinthe same tree(see Table 1). floweringsynchrony. The populationof male treesappeared As a crudeestimate of tree size and age,we also measuredthe to initiatefig production about 2 monthsprior to the onset diameterat breastheight (d.b.h.) ofeach tree.Measurements of the wet season, whilethe peak in the percentageof fig- were made at 1.5 m fromground level whereverpossible; bearingfemale trees coincides with periods of peak rainfall. however,it was necessaryin some cases to measured.b.h. In each year except 1989, therewere fewor no fig-bearing above the buttresses.Trees with a d.b.h. greaterthan 25 cm femaletrees duringthe dry monthsof Julyand August, were included in our census. The sexes of eighty-fiveof whilea smallfraction of themale treesbore figsin different 198 fruitingtrees in the study(43%) were determinedby stagesof development. examiningripe and fallenfigs. We identifieda totalof thirty Sexual differentiationin phenologicalpatterns is further males and fifty-fivefemales. illustratedby the variable behaviour of some individual Over the four-yearstudy, from March 1989 to February trees (Fig. 3). Male tree no. 22 produced figs almost 1993, trees were assessed at approximately 1-month continually,often at 100% of its capacityin spite of dry- intervals.The numberof treesin the censuswas increased season conditions. Male tree no. 196 produced figs as thestudy progressed, from 148 treesin 1989,until a total sporadically,but peaks in figabundance during each latedry of 218 treeswas reachedin April 1991. During the census season are suggestiveof annual regularityin figproduction. period, a few trees were lost throughstorm damage or Female treeno. 23 producedfigs sub-annually, but almost fungal disease. Fifteentrees that showed no evidence of withoutexception, during rainy episodes. The patternfor figproduction during the census were excluded fromour female tree no. 201 also suggestsan annual cycle of fig analysis. productionduring the wet season. We compared measures of fig abundance, asynchrony and d.b.h. betweenthirty male and fifty-fivefemale trees FIG PHENOLOGY AT THE POPULATION using the pooled monthlydata from4 yearsof the census LEVEL (Table 2). Mann-WhitneyU-tests compared the index of Fig. 1 shows the mean monthlyrainfall and the mean figabundance, the proportionof asynchronouscrops and monthlypercentage of fig-bearingtrees for 198 individuals d.b.h. between the sexes. While male and female trees

? BlackwellScience Ltd 1996,Journal of Biogeography, 23, 467-475

This content downloaded from 134.84.10.156 on Tue, 15 Jul 2014 17:19:07 PM All use subject to JSTOR Terms and Conditions Ficus variegataphenology in Australia 471

Tree Z (Male)

{D0ULDD DOofDoBoDO flflu OODD,oOO 0 DU0a0 Do MAMJJASONDJ FMAMJJASONDJ FMAMJJASONDJ FMAMJJASONDJ F 1989 1990 1991 1992 1993

Tree23 (Female) 5 n

- 00 co0 00 Do0 .000 D 0aO D 0 MAMJJASONDJ FMAMJJASONDJFMAMJ JASONDJFMAMJJASONDJ F 1989 1990 1991 1992 1993

Tree 196 (Male)

MAMJJASON DJ FMAMJJASONDJ FMAMJJASONDJ FMAMJJASONDJ F 1989 1990 1991 1992 1993

FIG. 3. Patternsof figabundance in two male and two femaletrees of F variegata at Cape Tribulation.Values forfig abundance (see Table 1) reflectthe frequencyand amplitudeof floweringand fruitingfrom 1989 to 1993. The smallestbars indicatethe intervalsbetween fig crops and gaps in the temporalsequence indicatemissing data. We could not determinethe exact phases of floweringand fruitingfor individualtrees, due to pronounceddevelopmental asynchrony of figcrops withintrees (Newstrom et al., 1994).

TABLE 2. Fig abundance,the proportionof treesbearing asynchronous fig crops and diameterat breastheight (d.b.h.) in thirtymale and fifty-fourfemale trees of F variegataat Cape Tribulation.Pooled data for the index of figabundance, the proportionof treesbearing asynchronousfig crops in any particularmonth and d.b.h. werecompared using Mann-Whitney U-tests.

Male trees Female trees Test statistic

X (SD) N X (SD) N Uor F P value

Fig abundance 1.39 (1.52) 804 1.14 (1.40) 1480 4.42 <0.001 Asynchrony 0.36 (0.48) 494 0.24 (0.47) 743 4.67 <0.001 d.b.h. (cm) 56.1 (21.3) 30 49.1 (23.7) 55 1.70 NS

NS = P>0.05.

did not differsignificantly in girth,male trees produced LEAF PHENOLOGY significantlylarger fig crops on average,according to our measure of fig abundance as a percentageof the total In the seasonally wet tropical environmentat Cape fruitingcapacity for a given tree. We also found that a Tribulation,E variegatawas deciduous(Fig. 4). Leaf drop higherproportion of male treescarried asynchronous crops was highlyseasonal, occurring chiefly during the dry season than femaletrees. of late August and early September.This period was

? BlackwellScience Ltd 1996,Journal of Biogeography, 23, 467-475

This content downloaded from 134.84.10.156 on Tue, 15 Jul 2014 17:19:07 PM All use subject to JSTOR Terms and Conditions 472 HughSpencer, George Weiblen and BrigittaFlick 1 0.9 - 0.8 *5 senescent 0.7 -*4 old ~j0.6 j 3 mature 0.5 ~~~~~~~~~~~~~~~~~~~32 new K. E3~~~~~~~~~~~~~~1 buds FIG. 04.Sesnlla rdcini aigt tCp rbuain epotdtefeunydsrbtosO leafless 0.3

0.1 0 jun jul aug sep oct nov dec jan feb mar apr may jun Month FIG. 4. Seasonalleaf production in F variegataat Cape Tribulation.We plottedthe frequency distributions of leafmaturity stages by poolingthe data for 198 trees monitored for 4 years.

TABLE 3. Kendall rank correlationsbetween rainfall, leaf maturity,fig maturity, fig abundance and d.b.h. foreighty-five mature trees of F variegatamonitored at Cape Tribulationfrom 1989 to 1993. Calculationoftr followed Kendall & Gibbons (1990). Each significancetest involvesa separaterisk of a typeI error.

Female trees Male trees x y P value P value

Leaf maturity Monthlyrainfall 0.059 <0.001 0.050 <0.05 Fig abundance Monthlyrainfall 0.160 <0.001 -0.052 <0.05 Fig maturity Monthlyrainfall 0.117 <0.001 0.119 <0.001 Leaf maturity Fig abundance -0.175 <0.001 -0.278 <0.001 Fig maturity Fig abundance -0.017 NS -0.053 NS Fig maturity Leaf maturity 0.153 <0.001 0.147 <0.001 Fig abundance d.b.h. 0.094 <0.001 0.065 <0.01

NS = P>0.05. followed by a flush of new leaves and the peak in fig temporalscales of correlationover 4 years (and evaluate abundance. Emergence of new growth occurred during thelikelihood of temporalautocorrelation), we used a more October. New leaves dominated the fig canopy from simplisticapproach. Correlations were calculated separately Novemberto March,prior to and duringthe wet season. The for male and female sub-populations, due to the frequencyof treeswith senescent leaves in the population phenologicaldifference between the sexes.The stageof leaf increasedwith the onset of the dry season in May. Leaf maturitywas significantlypositively correlated with rainfall drop coincidedwith the period of lowestrainfall, but not across months,although the relationshipwas less strong necessarilyof lowestsoil wateravailability, which is likelyto formale trees,which tended to retainmore leaves during the occurduring the late dry season, from October to November. dryseason. Fig abundanceon femaletrees was significantly The period of leaf abscission to bud-burstwas relatively positivelyassociated with rainfall,but for male trees fig short,usually about 7-10 days,and theperiod during which abundance showed a significantnegative relationship with figleaves attained mature status was approximately30 days. rainfall.This is consistentwith our observationsthat: (1) We under-sampledthe numberof treesin early stages of male trees retain more figs during the dry monthsthan leaf developmentbecause our monthlycensus often missed females,and (2) themale sub-populationinitiates its annual the developmentalstages of shorterduration. figcrop prior to theonset of the rainy season. Developmental phase (figmaturity), however, was positivelycorrelated with rainfallfor both the male and femalesub-populations. We RELATIONSHIPS AMONG PHENOLOGICAL believethat this correlation reflects the of male figs TRAITS duringthe earlywet months(December-January), and the For the statistical analysis of relationships among ripening of female figs during the later wet months categorical variables we used Kendall rank correlations (February-March).Leaf maturitywas negativelycorrelated (Table 3). Althoughtime series analysis could examinethe withfig abundance in both sexes,which could be explained

? BlackwellScience Ltd 1996,Journal of Biogeography, 23, 467-475

This content downloaded from 134.84.10.156 on Tue, 15 Jul 2014 17:19:07 PM All use subject to JSTOR Terms and Conditions Ficusvariegata phenology inAustralia 473

TABLE 4. Kendall partialX forrank correlations from Table 3. PartialX measuresthe agreementbetween two variables(x,y) independently of the influenceof a thirdvariable (z).

Female trees Male trees x y z X P value X P value

Rainfall Fig abundance d.b.h. 0.160 <0.001 -0.062 <0.01 Rainfall Fig maturity d.b.h. 0.117 <0.001 0.046 NS Rainfall Leaf maturity d.b.h. 0.059 <0.001 0.052 <0.05 Fig abundance Fig maturity Rainfall -0.036 NS -0.047 NS Fig abundance Leaf maturity Rainfall -0.187 <0.001 -0.276 <0.001 Fig maturity Leaf maturity Rainfall 0.147 <0.001 0.142 <0.001 Rainfall Fig maturity Fig abundance 0.121 <0.001 0.116 <0.001 Rainfall Leaf maturity Fig abundance 0.089 <0.001 0.037 NS Fig maturity Leaf maturity Fig abundance 0.152 <0.001 0.138 <0.001 Rainfall Fig abundance Fig maturity 0.163 <0.001 -0.046 0.05 Rainfall Leaf maturity Fig maturity 0.042 <0.05 0.033 NS Fig abundance Leaf maturity Fig maturity -0.174 <0.001 -0.273 <0.001 Rainfall Fig abundance Leaf maturity 0.173 <0.001 -0.040 NS Rainfall Fig maturity Leaf maturity 0.109 <0.001 0.113 <0.001 Fig abundance Fig maturity Leaf maturity 0.010 NS -0.013 NS

NS = P>0.05. by the factthat figs are most abundanton individualtrees Table 4 wereof the same directionand level of significance duringthe earlierdevelopmental stages, before the leaves as in Table 3. have attained mature status. Fig abundance and developmentalphase werenegatively, but not significantly, DISCUSSION correlatedpossibly due to the fact that figcrops decrease in size as theyreach maturity.The reductionin crop size Phenologicaldata have a reputationfor being notoriously appears to resultfrom abscission of non-pollinatedfigs, or difficultto analyse,and our data are no exception.We rely fromthe premature removal of figsby frugivorousbats and on the terminologyof Newstromet al. (1994) to highlight .Fig abundanceand treesize (as estimatedby d.b.h.), several limitationsof our phenologicalcensus. Syconium werepositively correlated, suggesting that larger trees tended developmentfrom flower receptivity to fruitmaturity took to bear larger fig crops. We also establishedthe rather about 6-7 weeks,and for this reason our monthlycensus obvious relationshipbetween fig and leaf maturity,namely did not followindividual cycles of figproduction through thattrees with older leaves tendedto carryolder figs. all stages of development.Furthermore, it was impossible As withall multivariatedata, thereexists the possibility to follow individual fig crops from the initiationstage that correlations between two variables result from to maturity,due to asynchronousflowering and fruiting correlationswith an additional variable. We computed patternswithin many trees. Another difficulty was thatnot Kendall's partial rank coefficient(-c) to test for pairwise all treeswere surveyed in each monthof the study.Despite associationsbetween variables after removing the effects of our best effortsto obtain completecensus data, observers a thirdvariable (Table 4). did not always successfullylocate and surveyall treesin Calculations of partial X followedKendall & Gibbons thepopulation. Also, we did not determinethe sex of every (1990), and sample size was sufficientlylarge thatpartial X treein thepopulation, thereby reducing our powerto detect could be compared against the normal distribution sexualdifferentiation ofphenological patterns. In spiteof the (Maghsoodloo & Pallos, 1981). Correlationsof tree-related irregularitiesin our census, population-levelphenological variableswith rainfall in Table 3 persistedwhen d.b.h. was patternswere evident.In all, our data represent5166 tree held constant,except in thecase of rainfalland figmaturity censusevents for 198 individualsthat produced figs during in male trees (Table 4). In everycase, the significanceof the study. associations among the tree-related variables (fig The E variegatapopulation at Cape Tribulationproduces abundance,fig maturity, and leafmaturity) were unaffected figs continually,although there are pronounced annual by accountingfor rainfall (Table 4). However,the positive peaks in amplitudethat are stronglycorrelated with rainfall. correlationbetween leaf maturity in male treesand monthly Trees were deciduous,and vegetativephenology in female rainfallwas not significantafter removingthe effectof treeswas also highlycorrelated with rainfall.Patterns of figabundance. Also, the negativeassociation betweenfig figand leaf productionin E variegataare consistentwith abundance in male treesand rainfalllost significanceafter threegeneral patterns reported in the literaturefor figsin controllingfor the effectof leaf maturity.In both sexes, seasonal environments.First, leaf drop oftenoccurs during correlationsof monthlyrainfall with fig abundance and leaf dryperiods and leaves oftenemerge during the transition maturitywere weakened after the effectof figmaturity was fromdry to wet conditions(van Shaick, 1986; Windsoret removed.In all other cases, the correlationsreported in al., 1989; Milton,1991). Secondly,increased fig production

? BlackwellScience Ltd 1996,Joumal of Biogeography, 23, 467-475

This content downloaded from 134.84.10.156 on Tue, 15 Jul 2014 17:19:07 PM All use subject to JSTOR Terms and Conditions 474 HughSpencer, George Weiblen and BrigittaFlick

oftenfollows rainfall (Newton & Lomo, 1979; Baijnath & For example,in Compsoneurasprucei (Myristicaceae) and Ramcharun,1983; van Shaick,1986). Thirdly, fig production Guarea rhopalocarpa(Meliaceae), dioecious understorey appears to follow leaf development (Milton, 1991). treesin , male treeshave sub-annualflowering However,this temporalsequence is not universalamong patterns and females have annual floweringpatterns figs. Correlations between vegetative and reproductive (Bullock,1982; Bullock, Beach & Bawa, 1983).The tendency phenologies occurred in some figs, including F aurea for males to produce more crops per year than females (Bronstein& Patel, 1992) and F yoponensis(Milton et al., occursin E exasperata,which produces six crops of wasps 1982),but not in F capensis(Baijnath & Ramcharun,1983) and one to two crops of seed figs per year (Nair & or the Panamanian stranglerfigs of Windsoret al. (1989). Abdurahiman,1984). In F variegata,male trees seem to In F variegata,the reproductive phenologies of male and produce figcrops more frequentlythan females(Fig. 3). femaletrees were different.This has been noted for other Also, male E variegatatrees produce a greaterproportion dioecious figs (Valdeyron & Lloyd, 1979; Berg, 1989), of asynchronouscrops thanfemales (Table 2). This pattern including:F carica in France (Kjellberg et al., 1987), F differsfrom that of dioecious E grossularioidesin Singapore, exasperata in (Nair & Abdurahiman,1984) and F characterizedby male within-treesynchrony and female fistulosaand F grossularioidesin Singapore(Corlett, 1987, within-treeasynchrony (Corlett, 1993). The climatic 1993). We argue below thatpopulation-level differences in differencebetween seasonal Cape Tribulationand aseasonal theflowering and fruitingpatterns of male and femaletrees Singapore could account for the differentphenological makes adaptive sense in seasonal environmentssuch as responses, since Singapore lacks predictable cues for Cape Tribulation. synchrony(Corlett, 1993). In fact, tropical phenological patternscan vary widelyover the geographicrange of a species (Newstrom et al., 1994). It would thereforebe SEASONALITY AND DIOECIOUS FIGS instructiveto compare the phenological patterns of F The dioecious figsare centeredin the Paleotropics,where variegatain seasonal and aseasonal parts of its range.Hill theyoften occur in habitatssuch as seasonallywet forests, (1967) reportedthat F variegatain seasonal Hong Kong along riverbanksand in periodicallysubmerged areas (Berg, was deciduous,and thatfig crops weresynchronous within 1989). Kjellberg& Maurice (1989) proposedthat dioecious male trees.However, Hill (1967) did not distinguishpatterns figs respond differentlyto seasonal variability than at the populationlevel fromindividual patterns, which are monoecious figs,due to the separationof seed and wasp differentfor E variegataat Cape Tribulation. productionbetween trees. In dioecious Ficus, each gender Male trees were more likelyto bear asynchronousfig specializes in making either seeds or wasps, but wasp crops than females,but we do not know exactlywhich production translates directly into male reproductive developmentphases overlappedwithin trees, and whether functionsince wasps are the pollen vectors.Kjellberg & these would be ecologically important.Bronstein et al. Maurice(1989) predictedthat female figs would be produced (1990) statedthe need for detailed phenological data because during the wet season, presumably under the most the ecological consequences of asynchronydepend on favourableconditions for seed production, and durationand intervalbetween reproductive episodes. The establishment.On the otherhand, male treesmaintain a consequences of within-treeflowering asynchrony for local wasp population by producingfigs during adverse pollinationand dispersalin dioecious species depends on conditions.A peak in male fig productionpreceding the genderas well as on the timingand frequencyof sexual wet season can increasethe pollinator population, releasing phase overlap. pollen-carryingwasps at a timewhen the majority of female In dioecious species,within-tree asynchrony in male figs figsare receptiveto .This patternbenefits male has the advantage of promotingmale fitnessthrough individuals (not simply the population as a whole) by increasedpollen donation without the negative effect of self increasingtheir reproductive success through the donation pollination(Milton, 1991). Also, female trees can flower of pollen to females. asynchronouslywithout the cost of selfpollination resulting The population-levelphenology of F variegatais similar fromwithin-tree wasp transfers(Patel et al., 1993). Staggered to the phenologicalpattern for dioecious figsproposed by femalefig crops could enhancethe chances of frugivorous Kjellberg& Maurice (1989), and parallels the patternsof and increase the probabilityof seedling F carica (Kjellberg et al., 1987) and F exasperata (Nair & establishmentin temporallypatchy microsites, such as light Abdurahiman,1984). A femaletree produces one to several gaps (Milton, 1991; Corlett,1993). More detailed studies figcrops duringthe optimal season for seed production, are needed to closelyexamine the degreeof sexual phase whilesome male treesbear figscontinually. Continual male overlap in dioecious fig populations and its ecological figproduction at the populationlevel is a consequenceof consequences. floweringasychrony at the individuallevel. In additionto enhancingthe fitnessof male individuals,crop asynchrony ACKNOWLEDGMENTS can maintain a local wasp population during the less favourabledry season. We predictthat the annual peak in We thank the volunteerswho participatedin the census male figripening (and wasp-release)should be synchronous over the 4 years: Tim DeVier Green, Anne Lane, Sybille withthe annual peak in femalefig receptivity. Petzold and many others. Also thanks to Hans Newstromet al. (1994) notedin generalthat phenological Nieuwenhuizen,who kindlyallowed us access to his rainfall patternsin dioecious species may be sexuallydimorphic. records for Cape Tribulation,and to Colin and Dawn

? BlackwellScience Ltd 1996,Journal of Biogeography, 23, 467-475

This content downloaded from 134.84.10.156 on Tue, 15 Jul 2014 17:19:07 PM All use subject to JSTOR Terms and Conditions Ficus variegata phenologyin Australia 475

Gray, who provided immenselocal support. The study Hill, D.S. (1967) Figs (Ficus spp.) of Hong Kong, 130 pp. Hong was supported by private donations to the AUSTROP Kong UniversityPress, Hong Kong. Foundation and a Thomas Watson Fellowshipto George Janzen,D.H. (1979) How to be a fig.Ann. Rev. Ecol. Syst. 10, 13-51. Weiblen. Yves Basset, JudithBronstein, Finn Kjellberg, Jessup,L.W. & Guymer,G.P. (1985) Vascularplants recorded from Aviva Patel and Paul Wilson reviewedearlier drafts of the the Cape Tribulationarea. QueenslandNat. 26, 2-25. . Kendall, M. & Gibbons,J.D. (1990) Rank correlationmethods, 5th edn, p. 260. Edward Arnold,London. Kjellberg, F., Gouyon, P.H., Ibrahim, M., Raymond, M. & Valdeyron,G. (1987) The stabilityof the symbiosisbetween REFERENCES dioecious figsand theirpollinators, a studyof Ficus carica L. and Blastophagapsenes L. Evolution,41, 693-704. Baijnath,H. & Ramcharun,S. (1983) Aspects of pollinationand Kjellberg,F. & Maurice, S. (1989) Seasonalityin the reproductive floraldevelopment in Ficuscapensis Thunb. (Moraceae). Bothalia, phenologyof Ficus: its evolutionand consequences.Experientia, 14, 883-888. 45, 653-660. Baijnath,H. & Ramcharun,S. (1988) Reproductivebiology and Maghsoodloo, S. & Pallos, L.L. (1981) Asymptoticbehavior of Chalcidsymbiosis in Ficus burtt-davyi(Moraceae). Monogr.Syst. Kendall's partial rank correlationcoefficient and additional Bot. Miss. Bot. Gard.25, 227-235. quantileestimates. J. Stat. Comput.Simul. 13, 41-48. Berg, C.C. (1989) Classification and distributionof Ficus. Milton, K. (1991) Leaf change and fruit production in six Experientia,45, 605-611. neotropicalMoraceae species.J. Ecol. 79, 1-26. Bronstein,J.L. (1989) A at the end of its range. Milton,K., Windsor,D.M., Morrison,D.W. & Estribi,M.A. (1982) Experientia,45, 622-637. Fruitingphenologies of two neotropicalFicus species.Ecology, Bronstein,J.L. (1992) Seed predatorsas mutualists:ecology and 63, 752-762. evolution of the fig/pollinatorinteraction. -plant Nair,P.B. & Abdurahiman,U.C. (1984) Populationdynamics of the interactions,vol. 4 (ed. by E.A. Bernays),pp. 1-47. CRC Press, figwasp Kradibiagestroi (Grandi) (HymenopteraChalcidoidea, Boca Raton, Florida. ) fromFicus exasperata Vahl. Proc. K Ned. Akad. Bronstein,J.L. & Patel, A. (1992) Causes and consequences of Wet.C, 87, 365-375. Newton,L.E. & Lomo, A. (1979) The pollinationof Ficus vogelii within-treephenological patterns in the Florida stranglingfig, in Ghana. Bot. J. Linn. Soc. 78, 21-30. (Moraceae). Am. J. Bot. 79, 41-48. Newstrom,L.E., Frankie, G.W. & Baker, H.G. (1994) A new Bronstein, J.L., Gouyon, P., Gliddon, C., Kjellberg, F. & classificationfor plant phenology based on floweringpatterns in Michaloud, G. (1990) The ecological consequencesof flowering lowland tropical rain forest trees at La Selva, Costa Rica. asynchronyin monoeciousfigs: a simulationstudy. Ecology, 71, Biotropica,26, 141-159. 2145-2156. Patel, A., Hossaert-McKey, M. & McKey, D. (1993) Ficus- Bullock,S.H. (1982) Populationstructure and reproductionin the pollinatorresearch in India: past, presentand future.Curr. Sci. neotropicaldioecious tree Compsoneurasprucei. Oecologia, 55, 65, 243-253. 238-242. Tracey,J.G. (1982) The vegetationof the humidtropical region of Bullock,S.H., Beach, J.H. & Bawa, K.S. (1983) Episodic flowering NorthQueensland, p. 124. Division of Plant Industries,CSIRO, and sexual dimorphismin Guarearhopalocarpa in a Costa Rican Melbourne. rain forest.Ecology, 64, 851-861. van Schaik, C.P. (1986) Phenologicalchanges in a Sumatranrain Corlett,R.T. (1984) The phenologyof Ficus benjaminaand Ficus forest.J. Trop.Ecol. 2, 327-347. microcarpain Singapore.J. SingaporeNat. Acad. Sci. 13, 30-31. Valdeyron,G. & Lloyd, D.G. (1979) Sex differencesand flowering Corlett,R.T. (1987) The phenologyof Ficusfistulosain Singapore. phenologyin the ,Ficus carica L. Evolution,33, Biotropica,19, 122-124. 673-685. Corlett, R.T. (1993) Sexual dimorphismin the reproductive Weiblen,G., Spencer,H. & Flick, B. (1995) Seed set and wasp phenologyof Ficus grossularioides Burm.f in Singapore.Malayan predationin dioecious Ficus variegatafrom an Australianwet Nat. J. 47, 149-155. tropicalforest. Biotropica, 27, 391-394. Corner,E.J.H. (1933) A revisionof the Malayan species of Ficus: Wiebes,J.T. (1994) The Indo-AustralianAgaonidae (pollinatorsof Covelliaand Neomorphe.Malayan BranchRoyal AsiaticSoc. 11, figs), p. 208. North-Holland,Amsterdam. 1-65. Windsor,D.M., Morrison,D.W., Estribi,M.A. & deLeon,B. (1989) Gaili, J. & Eisikowitch,D. (1968) Floweringcycles and fruittypes Phenologyof fruitand leaf productionby 'strangler'figs Barro of Ficus sycomorusin Israel. New Phytol.67, 745-758. Colorado Island, Panama. Experientia,45, 647-653.

? BlackwellScience Ltd 1996,Journal of Biogeography, 23, 467-475

This content downloaded from 134.84.10.156 on Tue, 15 Jul 2014 17:19:07 PM All use subject to JSTOR Terms and Conditions