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Phenology of Ficus Variegata in a Seasonal Wet Tropical Forest At Joumalof Biogeography (I1996) 23, 467-475 Phenologyof Ficusvariegata in a seasonalwet tropicalforest at Cape Tribulation,Australia 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 species, female and male trees initiatedtheir of the dioecious figFicus variegataBlume (Moraceae) 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. Leaf the female (seed-producing)trees was typicallyconfined productionwas highlyseasonal and correlatedwith rainfall. to the wet season. Male (wasp-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-tree abundant fromthe late dry season (October-November) wasp transfers. throughthe wet season (December-April).The annualpeak Key words. Australia, Cape Tribulation,dioecy, Ficus 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 pollination. The Lomo, 1979; Milton et al., 1982; Baijnath & Ramcharun, pollinationof figs,being accomplished only by host-specific 1983;Corlett, 1984, 1987, 1993; Nair & Abdurahiman,1984; wasps 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 plant and its pollinator (Bronstein, 1992). The fig patternsvaries geographically, from a slighttrend in Panama (syconium) 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 Florida (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 FICUS VARIEGATA 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
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