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Pollinational-Mutualism Strategy of Ficus Erecta Var. Beecheyana and Blastophaga Nipponica in Seasonal Guandaushi Forest Ecosystem, Taiwan

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Pollinational-Mutualism Strategy of Ficus Erecta Var. Beecheyana and Blastophaga Nipponica in Seasonal Guandaushi Forest Ecosystem, Taiwan Botanical Studies (2006) 47: 307-318. ECOLOGY Pollinational-mutualism strategy of Ficus erecta var. beecheyana and Blastophaga nipponica in seasonal Guandaushi Forest Ecosystem, Taiwan Hsy-YuTZENG1,*,Fu-YuanLU2,Chern-HsiungOU3,King-CherngLU3,andLi-JungTSENG3 1Hengchun Center, Taiwan Forestry Research Institute, 203 Kungyuan Rd., Hengchun 94644, Pingtung, TAIWAN 2Department of Forestry and Natural Resources, National Chiayi University, 300 University Rd., Chiayi 60004, TAIWAN 3Department of Forestry, National Chunghsing University, 250 Kuokwang Rd., Taichung 40227, TAIWAN (Received November 23, 2004; Accepted January 26, 2006) ABSTRACT. ThisstudyinvestigatespollinationmutualismbetweenF. erectavar.beecheyanaandits obligatepollinatorBlastophaga nipponicausingdetailedphenologydatafromtheseasonalGuandaushiForest Station.ThesymbioticcycleresembledthatoftheF. caricaandB. psenesinsouthernFrance.Blastophaga nipponicaemergedfromtheD-phasesyconiaofover-wintermalecropsandenteredthereceptivemale syconia to lay its eggs during the spring male main crop reproductive period. Several weeks later, dozens of offspringemergedandpollinatedthereceptivesyconiaofthesummerfemalemajorcrop.Afewpollinators entered the receptive male syconia to oviposite, and their offspring wintered inside the male fig as larvae or pupae.Thefigtreescouldcontrolthedevelopmentalperiodofwasp-producingsyconiaduringpollination. The peak of B-phase syconia (pollinators pollinate or set eggs) of both genders appeared earlier than the abundant D-phase syconia (pollinators released) by about two to three weeks. On the other hand, the flowering syconia of both genders occurred abundantly, staggered about two to four weeks after heavy rainfall, and the fly-out pollinators would pollinate or lay eggs during this period. This fig flowering phenology accommodates theshorterlifespanoftheobligatespecies-specialpollencarriertoenterthereceptivesyconiaforeffective ovipositionorseed-setting.Ficus erectavar.beecheyanaandB. nipponica thushaveasuccessfulmutualism strategyofpollinationattheGuandaushiForestStation. Keywords: Blastophaga nipponica;Ficus erectavar.beecheyana;GuandaushiForestEcosystem;Mutualism; Pollination. INTRODUCTION waspsthenpollinatethefemaleflowers.Inturn,wasp reproduction is dependent on the fig, as its larvae feed on Atotalca.750Ficusspeciesworldwidearedistributed galling flowers (Ramírez, 1970; Galil, 1973; 1977; Janzen, intropicaltosubtropicalareas(Corner,1965;Berg,1989), 1979;VanNoortandCompton,1996). andeachspeciesistypicallypollinatedbyfemalesofits Figtreescanbeclassifiedaseithermonoeciousor ownspecificspeciesoffigwasp(Galil,1973;Wiebes, dioecious,witheachgroupcomprisingroughly50%of 1979;VanNoortandCompton,1996).Therelationship thespecies(Corner,1965;Berg,1989).Inmonoecious between Ficus species and their pollinating wasps fig trees, male and female flowers line the inner wall of (Agonidae,Chalcidoidea,Hymenoptera)isconsidered thesamesyconium.Femaleflowers,differinginstyle tobeanextremeinstanceofplant-animalco-evolution and length, comprise the imperfect heterostyle (Verkerke, (Janzen,1979).Figtreesaredefinedbythesyconium 1989).Additionally,theovulesoffemaleflowerscan (syncarp or fig), a unique enclosed inflorescence, which bepollinatedforseed-productionandovipositedforfig islinedwithseveraldozentothousandsoftiny,unisexual waspdevelopingthegall,inwhichlarvaefeed(Bronstein, flowers (Berg, 1989; Verkerke, 1989; Tzeng et al., 2001). 1988). Several weeks later, adult fig wasps emerge and Thisisalsothearenaforinteractionswithfigwasps. matewhilestillinthesyconium.Thewinglessmalescan The morphologically specific fig wasp enters the syconia thencutatunneloutofthesyconia,oftendyinginside throughthebract-linedentranceoftheostiole,oftenlosing thenatalsyconium.Thefemalepollen-carrieremerges theirwingsandantennaeintheprocess.Thepollen-loaded from the now-mature male flowers, either through passive ducting or packing special pollen pockets and depart to *Correspondingauthor:e-mail:[email protected]. search for receptive syconia (Galil and Eisikowitch, 1968; 308 Botanical Studies, Vol. 47, 2006 Bronsteinetal.,1990).Becausemonoecyhavesyconia, or oviposite on the female flowers during a 2- to 3-week withripenessissynchronizedwithinanindividualtree period(Khadarietal.,1995;Tzeng,1997).Kjellbergetal. andaretypicallyasynchronousbetweentrees,thefemale (1987)elucidatedthestabilityofthesymbioticrelationship pollinatorsflyingoutofthesyconiamustsearchfor between the dioecious figs F. caricaL.andBlastophaga anotherreceptivesyconiumonanothertreetooviposite psenes L. and their pollinators during seasonal andpollinatein(Galiletal.,1970;Janzen,1979;Wiebes, environments.However,nostudieshaveidentifiedthe 1979;Bronsteinetal.,1990;BronsteinandPatel,1992; relationshipbetweenthelifecycleofthepollinator—with Thomsonetal.,1997). theirshort-livedescapefromD-phasesyconia—andthe Dioeciousfigspecies,however,havedividedthe receptivesyconiaforbothgendersyearround.Thegoal productionofseedsandtherearingofpollinatorsinto ofthepresentstudyistoelucidatethesyconiaphenology twoinflorescenttypesonseparateplants:syconiamale ofF. erectaThunb.var. beecheyana (Hook. et Arn.) andfemalefigs.Maleandshort-stylefemaleflowers Kinganddeterminetherelationshipbetweenflowering- (gallflowers,forfigwaspovipositing),linethemale phasesyconiareproductionandthedynamicprocesses syconiumwhilelong-stylefemaleflowers(seedflowers oftheobligatepollinatorBlastophaga nipponicaGrandi. for seed production) and/or neutral flowers line the female under sporadic rainfall. Additionally, this study identifies syconium(Weiblenetal.,1995;Tseng,1999;Tzeng thepollination-mutualismecologybetweenafigandits etal.,2001).Short-andlong-stylefemaleflowersare pollinatorintheseasonalenvironmentattheGuandaushi differentiatedbylengthofstyle,morphology,structureof ForestStation. stigma and ovary (Verkerke, 1990; Beck and Lord, 1988a; Tsengetal.,2000;Tzengetal.,2001),andbypollination Studied site physiology (Verkerke, 1990; Beck and Lord, 1988b), ThestudiedareawaslocatedattheGuandaushiForest which displays the perfect heterostyle (Verkerke, 1989; Station of the Hue-Sun Experimental Forest Station (24º4’ 1990). N, 12 º80’E), one of the Long Term Ecological Research AdultfemalepollinatorsemergefromD-phasesyconia (LTER) sites in Central Taiwan (Figure 1). During the andsearchformalereceptivesyconiatoovipositorfemale studyperiodof1996,theaverageannualrainfall,relative receptivesyconiatopollinateduringtheirextremelyshort humidity,andyearlytemperaturewere2,596.9mm, lifespanrangingfromseveralhourstotwodays(Kjellberg 79.1%,and21.0°C,respectively(datafromthestation). etal.,1988;Tzeng,1997;Wu,1996;Tseng,1999).After Mostoftherainfall(96.2%oftotal)occurredduring pollinationoroviposition,thewaspusuallydiesinsidethe therainyandtyphoonseasons.Theaveragerainfall syconiumitlastvisited.Otherwise,unvisitedsyconiaare overtenyearswas2,683.3mm(Figure2,from1987to thenaborted. 1996),and93.2%occurredduringthewarm-wetseason. According to the classification of Thomthwite, this study DioeciousfigsmustproduceD-andB-phasemale area belongs to AB’wa’, a wet but warmed wintertrochene syconiaduringthesameperiodtomaintainacontinuous klima (Yu, 2001). The vegetation of the site is typical of pollinatorlifecycle(Anstettetal.,1995;Tzeng,1997; awarmforestandischaracterizedbyaFicus –Machilus Kameyamaetal.,1999),andpollinationsuccessis vegetationzoneatabout500-800m(Liu,1968;Su,1992; dependentonthecontinuouscyclicalproductionof Lu and Ou, 1994). pollinatorswithpollen-enteringreceptivesyconia(Chen, 1998;Tseng, 1999; Harrison et al., 2000). Syconia phenologyhasbeenshowntobeusefulininvestigating the influence of climatic fluctuation and biotic interactions in some studies on dioecious figs in seasonal environments which show sexual specialization (Valdeyron and Lloyd,1979;Spenceretal.,1996;Tzengetal.,2003; Chang,2003).Dioeciousfigsdonotnecessarilyensure outcrossing (Corlett, 1987), but the fig trees must imitate the morphology, color, and odor of their syconia to keep thefigwaspsfromdistinguishingmalefromfemale syconiaand,thereby,onlysettingeggs(Grafenand Godfray,1991;Wareetal.,1993;WareandCompton, 1994); they must also be prevented from recognizing the fig phenology between male and female trees (Kjellberg etal.,1987;KjellbergandMcKey,1989;Spenceretal., 1996;PatelandMcKey,1998;Harrisonetal.,2000; Tzeng et al., 2004). Theshortlifespanofapollinator(Kjellbergetal., Figure 1. ThestudiedareawaslocatedattheGuandaushi 1988;Wu,1996;Tseng,1999)andthereceptivesyconia ForestStationoftheHue-SunExperimentalForestStationin canpreventabortingwhenpollinatorsdonotpollinate CentralTaiwan. TZENG et al. — Pollinational-mutualism strategy of F. erecta var. beecheyana and B. nipponica in Taiwan 309 two days (Okamoto and Tashiro, 1981; Wu, 1996; Tzeng, 1997). The phenology of this fig indicated that the syconia productionofeachgenderwasadaptedtotheenvironment, anditwouldbehelpfulforseedproduction,germination, andmaintainingthepopulationoftheobligatepollinator, Bl. nipponica, respectively (Tzeng et al., 2004). MATERIALS AND METHODS Samples selection Atotalof71treesofF. erectavar.beecheyanawere marked (40 male and 31 female mature trees), from which30maturetrees(17maleand13female)were selected for pollination examination. The figs trees were somewhatcloselydistributedalongtheroadsideorunder a 36-year-old China fir (Cunninghamia lanceolata)inan artificialforestatthestudysite.Twotothreebranches Figure 2. The ecological climate diagram of Hue-Sun roughly50cmlongfromonetreeorawhole,small ExperimentalForestStation;(P)representsperhumid;(H)
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