Nordic Society Oikos

Spatial and Temporal Variation in Frugivory at a Neotropical fig, Ficus pertusa
Author(s): Judith L. Bronstein and Karen Hoffmann
Reviewed work(s):
Source: Oikos, Vol. 49, No. 3 (Jul., 1987), pp. 261-268
Published by: Wiley-Blackwell on behalf of Nordic Society Oikos
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FL 32611. (Morrison 1978).Some species of fruitbats show marked preferencesfor figs (Ridley activityindicatethata diverseassemblage of potential seed dispersersvisits a tree duringa single ripening 1930.Ficus pertusa. in Panama theymay con- stitute70% of the total diet of Artibeusjamaicensis period (McClure 1966.Fivetreeswereobservedfor242h overa 5-moperiod. Herbst 1986). andHoffmann.CNRS.A totalof26 speciesofbirdsin10familiestookF pertusa Thevis- fruit. Jordano1983. Figs accounted forby farthe largest whileindividualfigtreesripenfruitssynchronously. 5051.France. Hoffmann.OIKOS 49: 261-268. itors'identity. Observations of singlefruitcropsare oftenusedto identifyseed-disperserassem- blages. 1982. of Florida. variation infrugivory at a Neotropicalfig. Old World primatesrelyon figsas well (Rudran likelyto representthe entiresuiteof species withwhich a particularfig interacts. F-34033 Montpellier. estimatingthat figs individualtreeduringa singlereproductivecycleare un- sustain40% of the total frugivorebiomass at his study site. Cruz 1974. Milton et al.MI 48109. Route de Mende. Terborgh(1983) has described in successiveseasons (Janzen 1979. Scott and Martin1984). Heithaus et al.) are "keystoneresources"for some timeduringthe year. Short-term observationsof animal monlytaken by manyspecies of birds. variable interactions withitspresent-day disperser assemblagearelesslikelytobe products of coevolution.Furthermore. theirimportancein the diets of squirrelmonkeysand Bronstein1986).relativeimportance of different and adaptivefeatures dispersers. 1971. Univ. Panama (Milton 1980) and Mexico (Estrada and and individualtreesrarelyfruitat thesame timeof year Coates-Estrada 1984). L. Morton frugivoresto figs themselves.Copenhagen 1987 in frugivory variation Spatialand temporal at a Neotropical fig. of a fruit display. Brockelman 1982. 1984) and Old World (Terborgh and Diamond 1970. Breitwisch 1983. B. Figs typicallyproduce 1979. Lack 1976.aseasonalfruit crops. K.Spatialandtemporal J. Bronstein(correspondence)and K.Compared withitsobligate. Ann Arbor. J.such observa- 1978. 1985) indicate that figsare com- 1983. vertebratesin tropical habitats worldwide (Terborgh Whereas theircentralrole in vertebratedietsis well- 1986).Raemaekers 1979).L. USA).the frugivoresseen at an capuchins in lowland Amazonia. Jordano Gautier-Hion et al. Wheelwrightet al.Dept of Biology. Milton and Dintzis 1981. whichbearslarge. Crome 1978.all terrestrialspecies of frugivorousvertebrateseat some species of figsat Fruitingfigs(Ficus spp.. huge crops of low-nutritive fruits(Hladik et al. Ficuspertusa JudithL.littleis known of the importanceof different (Snow and Snow 1971.species-specific pollination F. Snow 1981. Surveys of bird diets in both the New World studied.P. Therefore. Presentaddress of KH: Dept of Zoology.). pertusa'shighly mutualism.of Michi- gan. abundance. Gainesville. 1984). However. USA (PresentaddressofJLB: CentreEmberger.Oikos 49: 261-268. andimportance byan indexofthenumber (estimated of fruits removed)allvariedamongtreesandovertimeforindividual trees. Bronsteinand Karen Hoffmann Bronstein. 1987.Univ.Weinvestigated patternsofseasonalchangeandspatialvariationinthecom- positionofthedisperser assemblageofoneneotropicalfigspecies(Ficuspertusa L. Introduction typicalmainlandtropicalforests. dif- proportionof fruitin the diets of howler monkeysin ferenttreeswithina populationfruitout of synchrony. Dinerstein 1983. Janzen(1979) suggeststhatin tionsdo not reveal thepotentialimportanceof different Accepted27 January 1987 © OIKOS OIKOS 49:3 (1987) 261 .

servationperiod.numberofminutes visit-1 ion 1350-1450m). 1984). individuals fluctuated greatly amongtreesandforindi- 262 OIKOS 49:3 (1987) .000fruits due to N.rarespecies.and therefore the ripening periodlasts cordedeveryotherdayforeachtreeduring2-4 h peri- from3 wkto3 moon different trees(Bronstein unpubl.forTree9 (47 h). visitlength was recorded as minutesuntil that time.Dinerstein(1983) 1984).Here we discusspatterns of variability and their identifiedall birdsseen removingfruitsduringthe ob- possiblecausesandconsequences.or had fallen.Trees4 and2 werein abandonedpasturesneardwellings.Observationswere made by ine spatialand temporalchangesin the identity and one personwatching withbinocularsfroma distanceof abundanceoffrugivorous FicuspertusaL.Howe observedbats takingF pertusafruits.Seed to pulpratio(0. All were pasturetrees.However.All observations weremadeduringday- encingthepotential forcoevolutionwithseeddispersers lighthours.Trees23.Feedingrateand visitation lengthdatawerethenused an estimateof the abso- tionalbetweentropicallowermontanemoistand wet to rank the birdsaccordingto lute numberof fruitsremovedfroma giventree. calculatedas follows: hemiepiphytic predictably butusuallyat leastonce per year.fleshypeduncles enclosing numerous fruit.17 d forTree4 (39 h).figspecies in Monteverde.08) is very used heregivesa relativeranking of nearlyall of the low relativeto otherMonteverde plants(Wheelwrightmostcommonvisitors. does notrecordthemas bat food. Ripe fruitsweigh1 g on averageand theirpulp 18 d forTree23 (40 obs. ods between6 and 10 a. It growsabundantly in pasturesand remnant patchesofprimary andsecondary forest throughout the Fi = Avg.and lasted untilmostfruitshad been removed inseeddispersal variability within thepopulation.frugivores seasonalandspatialvari- as seed dispersers: Observations began on each tree when ripening ationin the frugivore assemblagemayproducegreat started.The observercountedand tion. which may Methods have caused us to underestimatevisitlengths.numberfruits takenvisit-' community of Monteverde (10°12'N. freestandingor timated fruit removalindex(EFR) foreachspecieswas tree. Undisturbed forestin the area is Afternoon observations of Trees23 and 4 indicated and latex-filledto soft. Individual trees flower and fruit un. Seed num. (Bronstein unpubl. 4 and 20.fortrees23. locatedjust belowtheContinental Divideon thePacificslopeoftheCordillera de Tilaran. et al.Speciescomposition wasre- thefirstfruit. An es- forest(Holdridge1967).Latinbinomials are listedin theAppendix. Avg. 11 d forTree2 (40 h). influ. Feedingratedatawererecorded on al- moved.during EFRi = F. thenumber ofminutes pervisit. = avg. and thenumberpollinated(Bronstein in press).theproportion offruitsremoved byall vis- beraverages58fruit-1 butvariesgreatly withfruit contrastto all other The presentstudywas designedspecifically to exam.84°42'W.Fruit Vi = avg.Becausefeeding ratedatawerenotavailableforcertain lets)arespherical and8-14mmindiameter. Between10% and90% of ing.Fruitschangeovernight fromhard. fruits during1984wereusedforobservations.Therefore. We use commonnamesforall birdspeciesinthispa- The firstfivetreesin thestudypopulationto ripen per.activepastures.m.we never (Wheelwright and Costa Rica. hours). onlymorning observation datawerein- allfruitsina cropripenwithin 10d following ripening of cludedinthedataanalysis. visitlength(min visit-1) of species i cropsizesvaryfrom100 to over200.4 d ternatedays. In casual observationsover 2 yr.the method eter(Bronstein 1986).Schemske1983. thelatter Boththenumberof visitorspeciesand thenumberof abutteda disturbed woods. A morecomprehen. Observations weremadeon data). andopensitesthrough. Ficus pertusa is a small (10-15 m).redand juicy.of thetreecrownwas visible.Fruits (technically.Ifan individualhadnot leftby the end of the observationperiod.If notre. containsapproximately 8% solublecarbohydrates on a 19d forTree20 (76 h).However. x Vi x Ni. no less than25 metersand at a locationfromwhichmost birdsvisiting treesovera 5-month periodinone CostaRicanpopula.feeding rate= Avg. everymonthoftheyearat leastsomeindividuals inthe whereF.Averagesof the numberof fruitstaken per visitand Ficuspertusaoccupiesforested out itsrange(Mexicoto Paraguay)and is particularlythe numberof minutesper visitwere thenused to ob- abundantin CentralAmerica(Condit 1969.j = total numberof visitsby species i at tree variabilityinboththenumber ofinflorescences initiated j overtheentireobservation period.crops thatthevastmajority ofbirdswereactivein themorn- differ inripeningsynchrony. and 12 d wetweightbasis(Wheelwright et al.feedingrate(fruitsmin-~) of species i populationbear ripefruit(Bronsteinin press). 9 and 20 werelocatedin the Results middleofpartly cleared.ripe fruitsare retainedan averageof 4. To obtainfeedingrates.two variables sivedescriptionoftheripening anddispersal ecologyof weremeasured:thenumber offruitstakenpervisitand F pertusawillbe published elsewhere. 1984). Burger tain the average feedingrate foreach species: 1977).elevat.itorscould not be calculated.

To citethemostdra- maticchanges. and manyfelluntouched fromeverytree._. The speciesremoving themostfruits werenotalways themostcommonvisitors (Tab.. thistimemigrant Swainson'sthrushesin- -10 5 creasedin abundanceandbecamethesinglemostcom- monspecies. Trees23 and 4. vidualtreesovertime(Fig. 8 .thesecondmostcom- 17 21 25 29 2 6 10 14 monspeciesin theearlyinterval of Tree2 (23%).5 feredgreatly in bothaveragefeeding rateand average length ofvisit(Tab. -15 trees.emeraldtoucanets 2- 1.whereasthehighestdiversity of 10 - 10 I''I A.4). 0 a) I 0) 10- B. OIKOS 49:3 (1987) 263 . 3).. The relativeabundanceof different visitors -5 shifted overtimeforeverytree. . butbrownjaysfellbelowthe thirdrankin themiddleand lateintervals. thetwo z Z10- Mar Apr -10 mostcommonspeciesat Tree2. Neither component of visitation was relatedto estimatedfruitcropsize. and2. ^ I 7 l 11 I 15 dance at Tree 23 in thefirstthirdof theobservation period.Q -5 -5 I .In spiteof an abundanceof ripefigs 10 D. whichbreaksdowntheobservation periodforeach treeintothreeequal intervals (early.. 2 - appearedto be overabundant relativeto thenumber of //. Ripe fruits I I*. 2 -25 on thistree. I_ Fig. Numberofbirdsobservedperhour(brokenline)and 4 8 12 16 20 24 28 1 number ofbirdspeciesobserved the perday(solidline)during May June observationperiodat eachoffiveFicuspertusatrees.. Tree 23 receivedthe -60 mostvisitsper hour. -40 Largecropsdidnotreceiveattention frommoreorfrom 6 -30 a greater diversityofvisitors(Tab.a mountain elaenia.butbecamethemostabundantspeciesduring 6 Feb Mar thelasttwo-thirds oftheperiod.. 4 25 . euphoniasand Swainson'sthrushes. 4._~. 20 25 ald toucanetswerethe mostabundantspeciesin the 2 -20 earlyinterval ofTree23. 1. -10 overlapped o . 11 I 15 I 19 .mountain robinsrankedfourth in abun- i 7 .wasob- servedduringtheentirelastinterval (15 obs. The middleand finalintervals ofobservation (28 March. although birdsse- lectedonlyripefruits.but amongitsvisitors emeraldtoucanetswere themostcommonduringthefirst two-thirds oftheob- servation period. 1). yetthesetreessharedrelatively fewcommon vis- itors..Brownjaysandemer- 't1 C. hours). 9 lapped(5-18 February).data). however. wereabsentfromTree 20. 8- At Tree2.Mountainrobinswere muchmorecommonat 23 27 31 4 8 12 16 20 Tree20.-._. Tree9 was visitedvery rarely. day-to-day fluctuations did not correspond in the numberof ripefruits to variability (Hoffmann and Bronstein. 1). 8- ! -20 0 Theseintervals do notcorrespond predictably to vari- I I . 20 6 .sharedtheirtwo most 10 abundantvisitorswhen theirfruiting periodsover- E.\ 15 E ationsinfruit displaysizessincefruit ripening ratesdif- feredamongtrees(Hoffmann and Bronstein.middle. 6. unpubl. 2)./ I . Temporalchangesin frugivore 28 1 5 9 13 17 Jan Feb speciescomposition amongtreesandforindividual treesare shownin Tab. fell Mar Apr below7% in thelastinterval.andlate).. -10 data). -15 euphoniaswerecommonduringtheearlyand middle periodsbut droppedin abundanceduringthe late period. unpubl.evenwhensimilartimeintervals are compared (Tab. The most commonvisitorsoftendifferedamong 8 . 23 50 visitorswasseenat Tree2 (Tab. 2.onlyone bird.I -10 foragers. becausespeciesdif- 4 - .21 April)roughly forTrees20 ) 4.Mountainrobins. 1).1-.

Hoffmann'swoodpeckersmade terspecificdifferencesin the proportionof swallowed fewervisitsthan brownjays. The accuracyof our rankingsmay be influencedby our rankingsmayoverestimatetheimportanceof touca- Tab. Tree Observation No.03 (17) Brown jay 0.23 (33) Sw thrush 0. B-h n thrush 0.55 (32) Mtn robin 0.2±0. al- yellow-crownedeuphonia.42(100) E toucanet 0. Phenologicalbreakdownof themostcommonfrugivorous birdspeciesvisitingduringtheearly. and patternsof birdvisitationforfiveFicus pertusatrees.8 min). Estimateswere made twiceand theiraverage value is tabulated.20). P > 0.60).09 (13) C-c robin 0. was not correlatedwithestimatedcrop size (T = -0.1 2 23 Mar-20 Apr 40 9.09 (13) Brown jay 0.10).3 vs Most visitsprobablywere in factrecordedsince there 1. but we estimatethattoucanetsremovedmore fruitsbe.8 a.4±0.07 (9) .5 fruitsmin-1).25 (28) E toucanet 0.9 9 4 May-2 Jun 47 11. the proportionof all visitsmade duringthat period and the numberof observationsmade are given. or observationhours (T = -0.42(131) Mtn robin 0.12 (13) 4 5-17 Feb 18 Feb-2 mar 3-14 Mar Mtn robin 0.06 (18) Social fc 0. seeds defecated whole and in germinablecondition.15 (16) B-g tanager 0.4) average fruitsize (T = -0.23 (3) Brownjay 0.middle.07 (4) B-g tanager 0.53 (10) E toucanet 0. moved more fruitsbecause each visitwas longer(4.7±0. differences (2) interspecific in theproportionof selected cause an averagevisitwas morethanthreetimeslonger.00 (1) Brownjay 0.33 (78) Y-c euphonia 0.16 (25) B-g tanager 0. range0-17). See Appendixforabbreviations. (1) theproportionof all visitsrecordedby the observer.12 (7) B-g tanager 0. thoughsome small. Mtn robin 0.07 (17) 20 15-27 Mar 28 Mar-9 Apr 10-21 Apr Mtn robin 0.15 (2) E toucanet 0.The numberof birdspecies observedwas Tab.38 (51) .55 (84) Brownjay 0.09 (1) Y-c euphonia 0. obs.06 (7) E toucanet 0.6 50544 16 9.2 4 4 Feb-14 Mar 39 9.28 (65) C-c robin 0. 0. or num- ber of observationhours(T = -0.23 (33) Y-c euphonia 0. 2.26 (34) . were seen half as oftenas mountainrobinsat Tree countingall fruitson 2-3 largebranchesand multiplying by the esti- mated numberof unitsof thatsize on the tree.07 (10) Mtn robin 0.8±0.05 (1) Fc sp.25 (28) Mtn robin 0.58 (67) Mtn robin 0.3 70680 11 6.73 (8) Mtn elaenia 1.10).70(383) Mtn robin 0. yet the woodpeckersre. Y-c euphonia 0. Crop characteristics notcorrelatedwithestimatedcropsize (Kendall's rankcorrelation. Tree Early Middle Late 23 28 Jan-3 Feb 4-10 Feb 11-18 Feb E toucanet 0.8 20 15 Mar-21 Apr 76 11.and late one-third of the observationperiod at each of fiveFicus pertusatrees. and (3) in- Similarly.07 (8) Brown jay 0.05 (1) 264 OIKOS 49:3 (1987) . b. Visitfrequency.6 5000 13 19. hard-to-observevisitorsmay have moved morefruitsbecause theyfedtwiceas fast(1. Mean ± standarddeviationlisted.26 (5) B-c motmot 0. fruitsactuallyremovedfromthe crownarea.10 (25) Mtn robin 0.For each birdspecies. Average fruit Estimated Numberof Visit frequency period hours size (mm)a crop size' bird species (birds h-1) 23 28 Jan-18 Feb 40 8. estimateswere made priorto the initationof ripening.1 vs been overlooked. The most commonvisitorto Tree 2 was the were so fewper minute(a medianof 1.38 (5) E toucanet 0. calculated froma sample of 14-29 ripe fruitsper tree. 1.1±0.6 3660 20 9.08 (12) 9 4-13 May 14-23 May 24 May-2 June E toucanet 0. yet mountain robins re.40.05 (28) H woodpecker 0.26 (81) E toucanet 0.T = -0.18 (2) C-c robin 0.3 49487 7 0.23 (54) Sw thrush 0.05).Species did differin theproportionof 0.06 (7) 2 23 Mar-1 Apr 2-11 Apr 12-20 Apr Y-c euphonia 0. selected fruitsremovedfromthe crown: in Tree 20.similarly. averagefruitsize (T = -0.

9±0. Scott and Martin 1984).2 12 7. Brockelman fourtimesduringthisstudy.1±0.0±0. Prattand Stiles1983). Jordano1983. hard figseeds whole and in germin. B-c motmot aFlycatcherspp. bSwthrush couldnotbe determined.3±2.. aFlycatcher aRobinspp.We can speculate Spatial and temporalvariabilityin the disperserassem. poral variabilityin the identityand abundance of vis- and thereforeassume that all common visitorspassed itorsand the numberof fruitstheyremovedfromFicus the small (1 mm).2 5 3. Breitwisch1983.See Appendixforabbreviationcodes. 0-b n thrush R-lhoneycreeper aRobin spp.4 55 5. Howe duringtheirlongvisits(cf.5±0. The orange-chinnedparakeet does destroyfig generalizationsabout the disperser coterie and the seeds (Janzen 1981). which frequentlydropped wood 1982.0±0. 1981). and of and Estabrook 1977.8 1 9.6 3 1. Speciescomprising> 10% ofthetotalnumberofvisitors. 1982.0 2 Mountainelaenia 0. pertusatrees. Averagefeeding min-) andaveragevisitlength rate(fruits (minvisit-) ofthemostcommon frugivorousbirdsobserved visitingFicuspertusafromJanuary to April.3 69 Socialflycatcher 0. Howe and Small- the three tanager species. This five- press). Species Feedingrate n Visitlength n Clay-coloredrobin 2. Discussion Causes of variability infruitremoval.8±0.8±0. number ofindividuals inparentheses.6±1.0 6 Brownjay 1. Janzen of short-termobservationson a singlefruitcropto make 1979).8 27 OIKOS 49:3 (1987) 265 .5 164 Emeraldtoucanet 1. aFlycatcherspp.on some of the factorsinfluencingpatternsof variation blage at trees with superabundant.8 25 Orange-chinnedparakeet 0. Ramirez 1976.Means.relativeimportance.low-nutritive fruit in the identity. Speciesdesignations b.7±3.2 23 19.1 15 8.. S-tdacnis D-c fc bB-hn thrush B-c chlorophonia R-b grosbeak B-cmotmot B-tsaltator aRobinspp.3 22 1.Howe 1984) butrarelydocumented(but see partiallyeaten fruits(cf.8 32 Yellow-crownedeuphonia 0.5±0.Howe 1980. Janzen 1979.g. spp.Tab. 4.5±1. Rank Tree23 Tree4 Tree20 Tree2 Tree9 1 E toucanet(133) Mtnrobin(131) Mtnrobin(521) Mtnrobin(70) E toucanet(18) 2 Mtnrobin(255) E toucanet(32) E toucanet(32) Y-c euphonia(118) C-crobin(1: 3 B-gtanager(44) Y-ceuphonia(24) H woodpecker (13) B-gtanager(44) Brownjay (5) 4 Brownjay (49) Mtnelaenia(10) C-c robin(17) C-c robin(24) Y-ceuphonia(1) 5 Y-ceuphonia(22) C-c robin(4) Brownjay (25) E toucanet(3) 6 C-c robin(23) Socialfc(1) 0-c parakeet(4) Brownjay (18) 7 Mtnelaenia(17) B-gtanager(6) Socialfc(11) 8 Socialfc(22) Y-c euphonia(3) Mtnelaenia(9) 9 H woodpecker (7) W-trobin B-cchlorophonia No.Levey in Howe and DeSteven 1979. Ridley 1930.1984. a.3±0.Such variabilitycalls intoquestiontheuse able condition(cf.8±0.3±0.3.standarderrorsofmeans.g.0±0.4 6 4. Snow and Snow 1971. nets.4±1.2 41 Mountainrobin 1.1 18 Blue-graytanager 0.and frequencyof Tab.1 15 4. McKey 1975.6±0. We never observed broken seeds in figpieces monthstudydemonstratedextensivespatial and tem- and fecal materialwe collected under F pertusatrees. Belowthelinearelistedthosespeciesseenon fewerthanfiveoccasionsorspeciesforwhichno feedingratedata are available.whichdefecatedmanyseeds on or underthe tree has been implicitlyassumed (e. Birdrankings number byestimated offruits removed from treeovertheobservationperiod(EFR).andsamplesizesare listed. but we observedthisspecies only adaptive featuresof a fruitdisplay (e.1±0.4 22 Hoffmann's woodpecker 1. oriole S-tdacnis Mtnelaenia S-bfc B-c motmot St fc Y-b elaenia B-c motmot B-tsaltator S-tdacnis M tityra St fc aFlycatcher spp.

Fig seeds not dispersed abilityarelikelytobe important inthedispersal ecology awayfromthecrownbyanimalsclearlyhavealmostno ofotherwidespread treesbearinglargecropsofanimal.Burgess.species-specific. fruitnumbers. HoweandEstabrook1977. Pasturetreesingeneralfruit moreheavily thanaverage.certainforest birds(Snow1981. Sargent(CornellUniv.Jermy 1984. pers. birds:figsarelowinseedbulkandareeasilysplitopen Acknowledgements . to thefigbetterthanrelativevisitation ratesorfeeding Evenwithin therestricted localityandpasturehabitats ratesmight. Althoughants(Ro- is inevitable forspeciessuchas F pertusathatarewide. K. betweentwotypesofmutualism is illustratedclearlyby Visitation droppedmarkedly 1983).Itsrelationship withitspollinator waspis of relativelygreat fruitabundancein Monteverde obligate.and theidentity of neighboringseeds in suitablemicrosites forgermination (Janzen plantfruiting simultaneously. wright etal.thenprobably byrodents(J.Wheelwright 1983).Dietarybreadthsand foraging trast.Schemske 1983.whosepreliminary observations 1983ledtotheplanning ofthisstudy.a traitconstant withincropsbuthighly vari.Howe1984).Leightonand Leighton1983. J.Severalresearchers We observedthegreatest numberand diversity ofvis. during weregenerously mentsandusefulinformation providedbyB.The iden. mutual- otherlocal plantsare in fruit. pertusatrees Spatialvariation infrugivore presenceandabundance duringthisstudy(Clayton1984).F.however. (1984)commonly observed fivebirdspecies Our rankings ofbirdspecieson thebasisofnumberof on F pertusa treesintheupperforested regions ofMon. Wal- man 1982.. Intercorrelationsto specializeon figsyear-round. Marchand earlyApril. pers.have recently pointedout thatwhenanimals'prefer- itorsin February. Likewise. As habitatdestruction amongfruitsize.rankings do notprovideinformation directlyrelevant to tityofvisitors waspotentially affectedbyfactors suchas thereproductive biologyof F pertusabecausetheydo thelocationofterritories andnests.. however.and mayin factbe chanceasso- 1973).Thisis a time Ficuspertusa. andthisensuresthatat leastsome ation may also have been relatively unimportant to oftheirseedswillcontinue to be dispersed.however. Bronstein. Holmes(Dartmouth College). D.birdvisitors to F pertusa.D.whenfew encesforplantsare notdistinct and constant. highly variableoverspaceandtime. range.Thiscontrast (suchas the resplendent quetzal. pertusatreeon thebasisof ripe identity and abundanceof visitors maybe less typical.E. fruit size. G.g.chanceof germinating.sitedifferences seemedcrucial. andtheOrga- variationsin nizationforTropicalStudiesforlogisticalassistance.Theseresultsclearlydemonstrate. Newswanger.theproximity ofthe notconsider thelikelihood thateachspeciesdepositsfig treeto forested areas. Figs'year-round fruiting pattern alsosubjectsindivid. Although natu- trees(Herrera1981. andtightly coevolved(Janzen (Wheelwright 1983). Beehler. Jan- zen.However. Murray.Manyofthesesourcesofvari.figs'copious and asynchronous (Bronstein in press)mayhaveobscuredtheeffects of fruiting willprobablymakethemincreasingly critical eachon ratesoffruit removal.Consequencesforseed dispersal.g.). C.We thankS.particular B.Bronstein 1987). Tab.andP.whoallowedus to workon theirproperty. Bronstein lace. 266 OIKOS 49:3 (1987) .Terborgh 1983)areknown correlated withripefruit size(Tab.P. Itshouldbe noted.Milton1980.). Hoffmann. unpubl.Wethanktheresidents ofMonteverde.neither andLeighton1983. Martinezdel Rio. Heideman. becauseripefruits wereclearlyoverabundant forbirds.fruit sizevari.of Michigan.Birdsmight be expectedto blagesfeeding on figs.). Haber. visitfrequency nordiversity ofvisitors wassignificantlyMorrison 1978.Constructive com- but attractfewervisitorsthanexpected(D. ciations.manyanimalshave morerestricted veryfewfallenF pertusafruits wereevertaken.Howe 1984.itsinteractions withthebirdswe observedaredi- rangesmay both change duringbreeding(Morton verseand variable.Howe andVandeKerkhove1981. thatevensuch ofthisstudy.Funding and K. 1).andR.Leighton able amongcrops(Bronstein in press). 3) and altitudinal migrants Orians1982.D. Trostleand S. in and eatenpiecemeal(Snow and Snow 1971. Janzen. Shepherd.However.In fact.fruits removedthuspotentially reflect theirimportance teverdethatwe neversawat ourstudysite1 kmaway.thevariability weobservedinthe visitan individual F. Intraspecific variationin fruitqualityand quantity Thepatterns offruitremovalfromF pertusain Mon- havebeenhypothesized tobe criticalindetermining the teverdeareundoubtedly different nowthantheywould identity ofvisitors and frequency ofvisitsto individual havebeenpriorto humandisturbance.J. thatthe ual treesto seasonal fluctuations in local frugivore frequency andnatureoffruit removalfromF pertusais populations andavailability ofalternative foodsources.Brockel.bertsand Heithaus1986)and manymammals(Janzen spread geographically and toleratea broad habitat 1979)commonly movefallenfruits ofotherfigspecies.comm. Bonaccorso.and rangesthanF pertusaon a local scale as well:Wheel.In con- wellas thebreeding seasonof 1979. Levey. wasprovided bytheDeptofBiologyandtheRackhamSchool fruitnumbers maynothavebeenmeaningful inthiscase of GraduateStudiesof theUniv.and ripeningrate continues.B. Gorchov.Howe destroy mostifnotall seedsbeneathfigs(Slater1972) 1980). Wheelwright and theSwainson'sthrush.Beehler1983)and mammals(e.foodforvertebrates. J. Fig-seed-specific lygaeidbugs dispersed fruits (e. ralhistorians haveoftennotedsimilarly diverseassem- HoweandSmallwood1982).residentspecieswere ismsarelikelyto be chanceassociations ratherthanco- joinedat thistimebybothlatitudinal migrants (suchas evolvedinteractions (Janzen1980.Forexample. and wereubiquitousbeneathfruiting F.

WA.U. Bradbury.Oikos48: 39-46.Bull.NY. Scientificname Common name Abbreviation Resident/ Migrant FamilyPsittacidae Brotogerisjugularis Orange-chinnedparakeet 0-c parakeet R FamilyMotmotidae Momotusmomota Blue-crownedmotmot B-c motmot R FamilyRhamphastidae Aulacorhynchusprasinus Emerald toucanet E toucanet R FamilyPicidae Melanerpeshoffmannii Hoffmann'swoodpecker H woodpecker R FamilyCotingidae Tityrasemifasciata Masked tityra M tityra R FamilyTyrannidae Myiozetetessimilis Social flycatcher Social Fc R Myiodynastesluteiventris Sulphur-belliedflycatcher S-b Fc R Myiarchustuberculifer Dusky-cappedflycatcher D-c Fc R Elaenia frantzii Mountain elaenia Mtn elaenia R Elaenia flavogaster Yellow-belliedelaenia Y-b elaenia R FamilyCorvidae Psilorhinusmorio Brown jay . J. 343- Ornithological 351. R FamilyMuscicapidae Turdusplebejus Mountainrobin Mtn robin R Turdusgrayi Clay-coloredrobin C-c robin R Turdusassimilis White-throatedrobin W-trobin R Catharusmexicanus Black-headed nightingalethrush B-h n thrush R Catharusaurantiirostris Orange-billednightingalethrush 0-b n thrush R Catharusustulatus Swainson'sthrush Sw thrush M FamilyEmberizidae Cyanerpescyaneus Red-leggedhoneycreeper R-l honeycreeper R Dacnis venusta dacnis Scarlet-thighed S-t dacnis R Icterusgalbula Northernoriole No. via.. . ecologyof an assemblage of zuela...Frugivores at a fruiting Ficusvinein a est.Biotropica 13: 70-76.AllenPress.ChironPress. J. 1969. L. 1978. KS.Fig(Ficustrigonata) fruit consumption and F. Agr.. Condit.. 1982. .W. Ecol. in southernThailand. seed dispersalby howlingmonkeys (Alouattapalliata)in W. R.Ecology. Cruz.Naturalselection andsocial Dinerstein. Bronstein.A.OTS Press. pp. SiamSoc. Beehler. pp. 138-169. 1983.Mexico.. 1977. (ed. Ph.Ficus drupacea. Sci. andRackhamSchool .Ph.Con- . . checklist of OTS Coursebook 83-1.Limitsto fruitproduction in a monoecious fig: press. OIKOS 49:3 (1987) 267 . Vasquez-Yanes.Pri- Brockelman. C. August.6thed. 1986. . Wheelwright. 1983.. . southern Cameroontropicalwetforest. W.D.C.Ficus.. consequences ofan obligatemutualism.1987.withabbreviationsused in tables. ofBiol..Observation ofanimalsfeeding ina thetropical rainforest ofLos Tuxtlas. D. ecologyof fruitbatsand behavior.Foraging seeddispersal byArtibeus jamaicensis inthe llanos ofVene. andTinkle.Am. theUniv. Nat. 3: 195-212. . In: Alexander. R. (eds). andOrozco-Sego- Hist.J.O. 1984. 1984.Frugivory andpolygamy inbirdsofparadise.W.P.Calif. NorthAmericanbirds. 40: 94-215. 1981.Durham. Berkeley.Appendix. birds.Biotropica15: Estrada. Taxonomyfollowsthe American OrnithologicalUnion (1983).Lawrence.NC. 1983. Tropicalbiology:an ecologicalapproach.Maintenance of species-specificity in a neotropical partofa doctoral dissertation submitted bytheseniorauthorto fig-pollinatorwaspmutualism.Coevolution and constraints in a neo. Clayton. D.A. R.Reproductive R.A.Comparison offrugivory byhowling monkeys mutualism. E. J.The lygaeidfaunaofFicuspertusa. American Union1983. 1984.. - stranglerfig. 1974.ofMichigan. Seattle.Aust.. 6: 77-91..MI. Univ. CA.B. Diss. Coates-Estrada. 30: 33-44. Y. V. H.The evolution - ofleks.Moraceae.). dor 76: 103-107.theexoticspecies.Auk 100: 1-12. Resident (R) or migrant(M) statusof each species is also listed.Div.ofMichigan Div. Breitwisch. and Coates-Estrada.TheA. matology . seasonality offruit production in a CostaRicancloudfor- R.Fruiteatingand 125-128.Bot. D.andN.In: Si- References mon.Fieldiana. Crome. Sci. J. 1981. AnnArbor. Scientificand commonnames of birdsobservedat figtrees. oriole M Euphonia luteicapilla Yellow-crownedeuphonia Y-c euphonia R Thraupisepiscopus Blue-graytanager B-g tanager R Chlorophoniaoccipitalis Blue-crownedchlorophonia B-c chlorophonia R FamilyFringillidae Saltatormaximu Buff-throated saltator B-t saltator R Pheucticusludovicianus Rose-breastedgrosbeak R-b grosbeak M Rathcke. Riley. birdsinlowlandrainforest innorthern Queensland. Burger. (Alouatta palliata) and bats (Artibeusjamaicensis) in the tropicalfig-pollinatorwasp Univ.ofWashington.I.Feedingassemblages ofJamaican J. Thispaperrepresents . Diss. C.

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