Tropical Fruit-Eating and Their Food Plants: A Survey of a Costa Rican Lower Montane Forest Author(s): Nathaniel T. Wheelwright, William A. Haber, K. Greg Murray and Carlos Guindon Source: Biotropica, Vol. 16, No. 3 (Sep., 1984), pp. 173-192 Published by: The Association for Tropical Biology and Conservation Stable URL: http://www.jstor.org/stable/2388051 . Accessed: 28/03/2014 14:25

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This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions Tropical Fruit-eatingBirds and theirFood Plants: A Survey of a Costa Rican Lower Montane Forest1

Nathaniel T. Wheelwright2 Departmentof Zoology, Universityof Florida,Gainesville, Florida 3261 1, U.S.A. WilliamA. Haber Departmentof EntomologicalSciences, Universityof California,Berkeley, California 94720, U.S.A. K. Greg Murray Departmentof Zoology, Universityof Florida,Gainesville, Florida 3261 1, U.S.A. and Carlos Guindon Apartado 10165, San Jose,

ABSTRACT In the lowermontane forests of Monteverde,Costa Rica, at least 70 species relyon fruitsto differentdegrees. We present over 700 recordsof birds feedingon the fruitsof 171 plant speciesin a surveyof a singlesite intendedto complementSnow's (1981) world surveyof fruit-eatingby birds. The frequencywith which birds visitedplants and the characteristicsof the fruits (dimensions,color patterns, nutritional traits) are also described.The numberof bird speciesrecorded feeding on the fruitsof a particularplant specieswas positivelycorrelated with the size of the plant and with its commonness.Because biases may also be introducedby observingplant species for differentamounts of time, we distinguishthose plant species that were thoroughly studiedfrom others studied only casually. Plants in fivegenera (Acnistus, Citharexylum, Ficus, Hampea, and Sapium)attract more than 20 bird species;at about halfof all plant species,we observedfewer than threebird species.These resultsshould lead to a betterunderstanding of the characteristicsof neotropicalfruits and the diets of fruit-eatingbirds.

RESUMEN En los bosques montano-bajosde Monteverde,Costa Rica, 70 especiesde aves, por lo menos,dependen de frutos,en diferentes grados. Presentamosmas de 700 observacionesde aves alimentandosede los frutosde 171 especiesde plantas en un estudio efectuadoen un solo lugarcon la intenci6nde complementarel estudiode Snow (1981) a nivelmudial sobrefrugivoria en aves. Se describentambien la frecuenciacon que las aves visitabanlas plantasy las caracteristicasde los frutos(dimensiones, patrones de color,composici6n nutritional). El numerode especiesde aves que notamoscomiendo frutos de una especieen particularresult6 positivamenterelacionado con el tamaiiode la planta y con su abundancia.Como esta correlaciontambien dependia de la durci6n de la observaci6nde cada especie de planta, distinguimosentre las especiesque estudiamoscuidadosamente o solamentecasual- mente.Las plantasde cincogeneros (Acnistus, Citharexylum, Ficus, Hampea, y Sapium) atrayeronmas de 20 especiesde aves; en aproximadamentela mitad de todas las especiesde plantasobservamos menos de tresespecies de aves. Estos resultadospermiten un mejorentendimiento de las caracteristicasde los frutosneotropicales y de las dietas de las aves frugivoras.

AFTER SUBSTANTIAL FIELD RESEARCH stimulatedby the the- Studiesdiffer in taxonomicfocus (plants or birds),hier- oreticalpapers of Snow (1971) and McKey (1975), most archicalfocus (individuals, species, guilds, or communi- studieson fruit-eatingbirds have arrivedat a similarcon- ties),and method(comparative, experimental or theoret- dusion: the factorsgoverning diet choice and seed dis- ical). Each has made significantcontributions (for a review persal by birds are more complicatedand elusive than see Howe and Smallwood 1982). originallybelieved (cf. Sorenson1981, Howe and Vande There are clear tradeoffsbetween breadth of focus Kerckhove1979). In responseto the complexityof the and depthof results.Most researchershave favoredmore problem, researchershave taken distinctapproaches. detailedstudies by concentratingon individualplant or bird populations (Howe 1977, Howe 1981, Herrera 1981, Wheelwright1983), althoughothers have exam- ined groupsof interactingor ecologicallysimilar species I Received6 June 1983, revised10 November 1983, accepted (Wheelwright1984, Jenkins1969) or simple commu- 11 November 1983. nities(Sorensen 1981, Baird 1980). As a result,however, 2 Currentaddress: Section of Ecologyand Systematics,Cornell University,Ithaca, New York 14853, U.S.A. literaturesyntheses have had to relyon informationas-

BIOTROPICA 16(3): 173-192 1984 173

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 1. Fruit-eatingbirds of Monteverde, Costa Rica.

Gape Family Code Common name Scientificname width (mm) Cracidae BGb Black Guan Chamaepetesunicolor 31.0 Columbidae Bpb Band-tailedPigeon Columbafasciata 10.0 RP Red-billedPigeon C. flavirostris 10.0 DP Ruddy Pigeon C. subvinacea 10.0 SP Short-billedPigeon C. nigrirostris 9.5 WD White-tippedDove Leptotilaverreauxi 9.5 Cuculidae GA Groove-billedAni Crotophagasulcirostris 13.5 SC SquirrelCuckoo Piaya cayana Trogonidae RQa ResplendentQuetzal Pharomachrusmocinno 21.0 OTb Orange-belliedTrogon Trogonaurantiiventris 17.0 Momotidae BM Blue-crownedMotmot Momotusmomota 19.0 Capitonidae RB Red-headed Barbet Eubuccobourcierii PBb Prong-billedBarbet Semnornisfrantzii 17.0 Ramphastidae ETa EmeraldToucanet Aulacorhynchusprasinus 26.0 KTh Keel-billedToucan Ramphastossulfuratus 31.0 Picidae GW Golden-oliveWoodpecker Piculusrubiginosus 11.5 FWb Golden-frontedWoodpecker Melanerpesaurifrons 15.0 SW Smoky-brownWoodpecker Veniliornisfumigatus Pipridae LMa Long-tailed Manakin Chiroxiphia linearis 8.5 Cotingidae FP Rufous Piha Lipaugusunirufus MTb Masked Tityra Tityrasemifasciata 18.0 TBa Three-wattledBellbird Procniastricarunculata 25.0 CD CinnamonBecard Pachyramphusrufus Tyrannidae TKb TropicalKingbird Tyrannusmelancholicus 16.0 SF Sulfur-bellied Flycatcher Myiodynastesluteiventris 17.0 GF Golden-belliedFlycatcher M. hemichrysus 15.5 BF Boat-billedFlycatcher Megarhynchuspitangua 16.5 CF Social Flycatcher Myiozetetessimilis 13.0 DF Dusky-cappedFlycatcher Myiarchustuberculifer 12.0 YE Yellow-belliedElaenia Elaenia flavogaster 10.0 MEb MountainElaenia E. frantzii 8.5 OFb Olive-stripedFlycatcher Mionectesolivaceus 8.5 YCb YellowishFlycatcher Empidonaxflavescens 9.0 Corvidae BJb BrownJay Psilhorinusmorio 21.0 Muscicapidae BSa Black-facedSolitaire Myadestesmelanops 11.0 WRb White-throatedRobin Turdusassimilis 10.0 CRb Clay-coloredRobin T. grayi 14.0 MRa MountainRobin T. plebejus 12.0 STa Swainson'sThrush Catharusustulatus 10.5 RN Ruddy-cappedNightingale-Thrush C. frantzii BN Black-headedNightingale-Thrush C. mexicanus 10.5 ON Orange-billedNightingale-Thrush C. aurantiirostris 9.5 Ptilogonatidae Bya Black-and-yellowPhainoptila Phainoptilamelanoxantha 11.5 Vireonidae SV SolitaryVireo Vireosolitarius 8.5 YV Yellow-greenVireo V. flavoviridis 8.0 BV Brown-cappedVireo V. leucophrys Emberizidae CO Chestnut-headedOropendola Zarhynchuswagleri 18.0 BC BronzedCowbird Molothrusaeneus 11.5 NO NorthernOriole Icterusgalbula 10.0 RH Red-leggedHoneycreeper Cyanerpescyaneus 7.0 SD Scarlet-thighedDacnis Dacnis venusta 8.0 GCb Golden-browedChlorophonia Chlorophoniacallophrys 6.5 YT Yellow-throatedEuphonia Euphoniahirundinacea 7.0 TT Silver-throatedTanager Tangara icterocephala 9.0 CT Spangle-cheekedTanager T. dowii 9.0 GT" Blue-grayTanager Thraupisepiscopus 10.0 PT Palm Tanager T. palmarum 10.5 HT Hepatic Tanager Pirangaflava 12.5 UT SummerTanager P. rubra 11.0 CBa Common Bush-Tanager Chlorospingusophthalmicus 10.0 SB Sooty-cappedBush-Tanager C. pileatus 9.5

174 Wheelwright,Haber, Murray,and Guindon

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 1. (Continued).

Gape Family Code Common name Scientificname width (mm) TS Buff-throatedSaltator Saltatormaximus 18.5 GS GrayishSaltator S. coerulescens 14.5 RG Rose-breastedGrosbeak Pheucticusludovicianus YG Yellow-facedGrassquit Tiaris olivacea 6.5 WS White-earedGround-Sparrow Melozoneleucotis 12.5 YF Yellow-throatedBrush-Finch Atlapetesgutturalis 10.5 CC Chestnut-cappedBrush-Finch A. brunneinucha RSb Rufous-napedSparrow Zonotrichiacapensis 8.0 YH Yellow-thighedFinch Pselliophorustibialis a Species studiedin detail; fruitdiet at Monteverdebelieved to be well representedin Table 2. b Species studied less systematically;fruit diet at Monteverdemoderately well known. Other species not studied systematically; feedingrecords represent miscellaneous observations. sembledfrom disparate studies in differenthabitats in (Wheelwright1983; cf.Snow 1970); observingand con- theirattempts to derivegeneral principles (Ricklefs 1977, ductingcensuses at fruitingtrees (cf. Howe 1977), es- Stiles1980, Herrera 1981, Thompson 1982). How well pecially15 speciesin the ; followingforaging does the samplingof a diverseliterature reflect actual flocksand monitoringfood deliveriesto nestlings;and patternsof frugivoryin communities? As a follow-upto recordingmiscellaneous observations. From 6/81 to 7/83 Snow's(1981) worldsurvey of fruit-eatingbybirds, we KGM trackedradio-collared birds to fruitingplants, col- presentobservations from a singlesite to allowan eval- lected fecal samples frommist-netted birds, and noted uationof the generality ofsuch surveys. Over 700 feeding miscellaneousfeeding records, particularly in the lower recordsgathered over a five-yearperiod involve 70 bird montanerain forest. Additional observations were shared speciesand 171 plantspecies from a lowermontane wet/ by otherbiologists working at Monteverde(R. and M. rainforest in CostaRica. Descriptions (color, dimensions, Laval, W. Busby,P. Feinsinger,K. Winnett-Murray,pers. nutrients)of thefruits eaten by birds accompany feeding comm.). With taxonomichelp fromthe Chicago Field records. Museum and the Missouri Botanical Garden, WAH identifiedmost of the plant species. STUDY SITE AND METHODS Gape widthsof birds,measured at the commissural pointson museumspecimens from the HarvardMuseum Our studyarea, Monteverde,Costa Rica (10?18'N, of ComparativeZoology and the Yale PeabodyMuseum 84048'W),lies on a relativelyflat plateau at an elevation of Natural History,are expressedas means of the sam- of 1350-1550 m. Itswestern border falls steeply to the ples, whichinduded at least one male and one female/ Pacificlowlands; to theeast it is boundedby theconti- species(N = 2-9 individuals/species).Fruit characteris- nentaldivide and theAtlantic slope. Rainfall, which oc- ticswere determined on a sample of representativefruits cursmainly between May and December,exceeds 2400 from1-20 individualplants. We used calipersto mea- mmin mostyears (x = 2485 mm).Because of the sharp surefresh fruit length and diameter,and a springbalance moisturegradient caused by the prevailing NE tradewinds to determinefresh mass. Nutritionalanalyses were per- passingover the divide, forest structure and speciescom- formedby the Palmar Plant and Soils Laboratoryat the positionchange markedly along the plateau within a 4 Universityof Alaska. Sugar concentrationwas estimated kmdistance from the "elfin" cloud forest on thedivide fromcrushed fruit pulp spread on a Bausch and Lomb to the taller,moist forest on the westernedge of the pocketrefractometer. Sample sizes varyin differentanal- plateau(see Lawton and Dryer 1980, for a morecomplete yses because we were unable to recordcomplete infor- descriptionof thesite). Our observationswere restricted mation for all plant species. to the 2700 ha MonteverdeCloud ForestReserve, the surroundingforests, and the woodlots and pastures of the SAMPLING BIASES communityitself (total area ca. 15 kiM2). WAH and CG initiatedthe study in late 1978 by Beforepresenting results, we should discussthe potential notingfeeding records during their forest phenology study. biasesof usingvarious methods in thisand otherstudies. In 20 monthsof field work from 6/79 until8/83, NTW Because of differentresearch emphases and techniques, collectedrecords using various techniques: seed-trapping the feedingrecords presented below underrepresentcer- beneaththe displayor nestperches of certainspecies taingroups of birdsand plantsand overrepresentothers. Fruit-eatingBirds and TheirFood Plants 175

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 2. Fruitspecies eaten by birdsof Monteverde, Costa Rica.

Bird speciesa Plant species BG BP RP RQ OT BM PB ET KT GW FW LM MT TB SF BF CF SubclassMagnoliidae ANNONACEAE c Guatteriaconsanguinea o c c MONIMIACEAE Siparunasp. A LAURACEAE c Beilschmiediacostaricensis u c c o c B. sp. BL o cB. sp. BC c c c c cNectandradavidsoniana o c c o o c c N. gentlei u u c u c o c N. hypoglauca u c c c c c N. salicina u c c c c N. sp. NC o c N. sp. NG o u c Ocoteaaustinii c c c c c 0. bernouliana o c u o c 0. klotzschiana u c c 0. tonduzii c c u c c c u c c c c c 0. wachenheimii c c c c c cO. sp. FL c c c c cO.sp.K2 u c c c dO. sp. RP u c c c d Perseaveraguensis O P. FL ? P. RS ? c Phoebemexicana c c c c c c P. neurophylla c u c o c c PIPERACEAE d Piperauritum u Pipersp. A o SABIACEAE Meliosmaidiopoda u o ? PAPAVERACEAE d Bocconiafrutescens o SubclassHamamelidae ULMACEAE c Tremamicrantha c o c o c c MORACEAE c Ficuspertusa c c c c c c F. tuerckheimii o o c o c o c c o c c c Trophismexicana u CECROPIACEAE (MORACEAE) d Cecropiaobtusifolia o c c URTICACEAE d Ureraelata c c c Subdass Caryophyllidae PHYTOLACCACEAE Phytolaccarivinoides o P. sp. A c

176 Wheelwright,Haber, Murray,and Guindon

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 2. (Extended).

Bird speciesa DF YE ME OF BJ BS WR CR MR ST BY SD NO GC YT TT CT GT UT CB RG WS YF Totalb

u 4

c 1

5 1 4 c 7 o c 8 5 5 2 2 c 5 4 o 3 o c u c c 18 5 4 4 c 5 1

c 1 o c c c 9 c c 8

u 2 1

c 3

o c 4

o c c c u c o c o 16

o c o 8 c o o c o c o o o 21 1

0 0 0 0 c 0 10

c c o u c c c o o 13

u c c 0 5 1

Fruit-eatingBirds and TheirFood Plants 177

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 2. (Continued).

Bird speciesa Plant species BG BP RP RQ OT BM PB ET KT GW FW LM MT TB SF BF CF NYCTAGINACEAE Neea amplifolia ? ? Torrubiacostaricana o SubclassDilleniidae THEACEAE c Symplocarponbrenesii c c c c MARCGRAVIACEAE Marcgraviabrownei c CLUSIACEAE (GUTTIFERAE) Clusia alata c c MALVACEAE c Hampea appendiculata u u c o c c o d Malvaviscusarboreus c c u FLACOURTIACEAE Casearia sylvestris o cHasseltia floribunda o c c c o c c o c a Xylosmachloranthum c o o c X. flexuosa u o X. intermedium o CUCURBITACEAE sp. A o ERICACEAE Cavendishiacomplectans u C. melastomoides C. capitulata C. sp. A c o Satyriasp. A SAPOTACEAE Dipholisparvifolia ? ? SYMPLOCACEAE cSymplocoslimoncillo o o u c o S. sp. A u S. sp. B o MYRSINACEAE Ardisia compressa c c cA. palmana c c c c c Rapanea myricoides c u o c u c SubclassRosidae ROSACEAE c Prunusanularis c c P. sp. A c o P. cornifolia o cRubus rosaefolia c o c o THYMELAEACEAE Daphnopsisamericana c c o MYRTACEAE Eugeniasp. A o cEugeniasp. B o sp. SC u

178 Wheelwright,Haber, Murray,and Guindon

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 2. (Extended).

Bird speciesa DF YE ME OF BJ BS WR CR MR ST BY SD NO GC YT TT CT GT UT CB RG WS YF Totalb

1

o o c 7

o c c 4

c c u 5

o o c c o o c u u u o u u 22 3

1 c 0 c c c 14 c 0 c c c 0 c 11 u 0 c 5 c 0 c c 5

1

o c 3 c 1

2 c 1 0~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

C C 7 1 1

2 U C C C 0 0 C 11 c u c o 10

3 2 1 u c 10

0 c 5

1 1 1

Frujit-e.atingBirdsq andi Their Foodi Plants 179

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 2. (Continued).

Bird species- Plant species BG BP RP RQ OT BM PB ET KT GW FW LM MT TB SF BF CF

MELASTOMATACEAE Blakea grasilis c c Concostegiabernouliana c o o o c o o C. puberula o C. speciosa C. xalapensis c Miconia sp. A c Ossaea micrantha 0 0. sp. A 0 sp. CT sp. NC u OLACACEAE Linocieradominguensis 0 0 LORANTHACEAE Gaiadendronpunctatum dsp. A sp. B CELASTRACEAE dsp. A 0 0 c Perrotettialongistylis Maytenussp. A AQUIFOLIACEAE c Ilex lamprophylla c c EUPHORBIACEAE Hieronymaguatemalensis cSapium oligoneuron c c u 0 0 c c 0 c c RHAMNACEAE d Colubrinaceltidifolia 0 c VITACEAE sp. A 0 ERYTHROXYLACEAE Erythroxylonamplum 0 MALPIGHIACEAE d Bunchosiapilosa 0 B. sp. A c SAPINDACEAE c Cupania glabra c c c c d Matayba apetala c c Paullinia sp. A SIMAROUBACEAE Picramniacarpinterae 0 MELIACEAE c Guarea glabra 0 c 0 G. tonduzii c G. tuisiana c c Trichiliahavanensis 0 RUTACEAE Mappia racemosa 0 c M. sp. A 0 Zanthoxylumculantrillo c ? ?

180 Wheelwright,Haber, Murray,and Guindon

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 2. (Extended).

Bird speciesa DF YE ME OF BJ BS WR CR MR ST BY SD NO GC YT TT CT GT UT CB RG WS YF Totalb

o o 3 o c u c c o c 16 c c c 4 0 1 1 u c c c o 9 c c c o 6 c c 3 u 1 2

2

c 1 0 1 c 1

o 0 4 o 0 0 0 4 0 1

c o u 5

c 1 c c o c c o u o u 22

c c u o o 8

1

1

1 1

5 o c o c 6 0 1

1

c 4 c c c 4 2 1

2 1 c ~~~~~~~~~~~~~~~~~~~~2

Fruit-eatingBirds and TheirFood Plants 181

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 2. (Continued).

Bird speciesa Plant species BG BP RP RQ OT BM PB ET KT GW FW LM MT TB SF BF CF ARALIACEAE c Dendropanaxarboreus u c D. gonatopodus o d D. sp. FL o c D. querceti Schefflerarobusta Didymopanaxpittieri o o c Oreopanaxoerstedianum o c c c c u 0. xalapensis 0 0. sp. (KGM 82-90-2) SubclassAsteridae APOCYNACEAE d Stemmadeniaglabra o Tabernaemontanasp. A o SOLANACEAE cAcnistus arborescens c o o o c o c c c c c d Cestrummegalophyllum c c d C. racemosum c c C. sp. A o d Lycianthesmultiflora c c o d L. synanthera c d Solanumcordovense 0 0 C C S. hispidum 0 d S. nudum C 0 c S. umbellatum C d Witheringiasolanacea o u c W. coccoloboides u W. maculata o W. sp. A c liana sp. A c BORAGINACEAE d Tournefortiaglabra o VERBENACEAE ' Citharexylumintegerrimum c c o u c c o C. macradenium c c C c c GESNERIACEAE Alloplectustetragonus Besleriaformosa c B. triflora B. sp. A o Drymoniaconchocalyx D. rubra CAMPANULACEAE Burmeisterasp. A RUBIACEAE Cephaeliselata u c Chionecostaricensis u u o Coussareaaustin-smithii o u u C. sp. A u Faramea quercetorum o c Guettardapoasana c u c c Gonzalaguniarosea u Hamelia patens c Hoffmanniasp. A 0 H. sp. RL

182 Wheelwright,Haber, Murray,and Guindon

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 2. (Extended).

Bird species- DF YE ME OF BJ BS WR CR MR ST BY SD NO GC YT TT CT GT UT CB RG WS YF Totalb

o c 4 o 2 o c c c 6 c 1 o 1 o o c o 6 c o o o c o 13 c o c 4 c 1

c 3 1

o o c o c o c o c o o o o c u o u o o 43 c 3 2 1 c c 5 u c 3 o o c c o u 10 1 3 o c 4 u c u 7 c c 4 1 0 1 1

o 2

o c o o o c c o o o 23 0 c c u 0 10

u 1 1 c c 2 c u c 4 u c 2 u 1

1

u 3 3 3 1 1 c c c 7 c c u 4 o 2 1 C 1

Fruit-eatingBirds and TheirFood Plants 183

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 2. (Continued).

Bird speciesa Plant species BG BP RP RQ OT BM PB ET KT GW FW LM MT TB SF BF CF

H. sp. RF Palicoureagaleottiana c P. sp. YY Psychotriaacuminata o c P. parasitica P. sp. BO o P. sp. LP o c P. sp. WB CAPRIFOLIACEAE d Viburnumcostaricanum o c o c ASTERACEAE (COMPOSITAE) d Clibadiumsp. A c o d C. sp. B c SubclassArecidae (PALMAE) ChoCamaedoreasp. A c u ARACEAE Anthuriumsp. A o A. sp. B o A. sp. C o Subdass Commelinidae COMMELINACEAE Campeliazanonia u POACEAE (GRAMINAE) Lasiacis sp. A o SubclassLiliidae SMILACACEAE Smilax sp. A o Miscellaneousspecies Epiphyte o o

Number of speciesof fruitseaten 26 11 4 38 14 9 30 95 16 7 6 37 14 29 6 10 6 a Two-lettercodes forbird speciesare definedin Table 1. b Totals forbird speciesfeeding on fruitsinclude the recordsin Table 3. c >2 h observationof commonsp. in appropriatehabitat plus repeated(210) censuses. d <2 h observationof commonsp. in appropriatehabitat but 210 censusesof plantswith ripe fruit. c= commonlyobserved. u = uncommonlyobserved. o = occasionally(rarely) observed.

For example,the Lauraceae and the birds that feed on searcheffort and thenumber of bird species seen feeding theirfruits are well known,whereas the Rubiaceae and on thefruits of a particularspecies (Spearman Rank Cor- birdsassociated with understory shrubs are generally poorly relation:r, = 0.42; P < 0.001; N = 148 spp.;all statis- known.If we rankplant speciesby the amountof time ticaltests are non-parametric and aredescribed in Siegel, theywere observed (miscellaneous observations only; few- 1956; cf.Kantak 1979). Theseresults imply more of a er than 10 censusesor less than 2 hoursof observations; biasthan actually exists because we triedto allocatemore or at least 10 censusesplus 2 or morehours of observa- researcheffort toplant species already known (on the basis tion), thereis a strongpositive correlation between re- ofindependent evidence) to be importantin birds'diets.

184 Wheelwright,Haber, Murray,and Guindon

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 2. (Extended).

Bird speciesa DF YE ME OF BJ BS WR CR MR ST BY SD NO GC YT TT CT GT UT CB RG WS YF Totalb

c 1 1 2 c c 2 1 2 0 1

c 0 0 0 8

u c 4 1

2

o 2

1

1

1

o 3

8 4 20 9 13 51 12 10 44 13 13 4 4 14 7 4 13 6 4 29 4 6 7 709

In otherwords, many plant speciesmonitored only hap- observedfeeding on its fruits(Spearman Rank Correla- hazardlywere apparently ignored by birdsas well: fruits tion: P < 0.00 1 forall species[rs = 0.49, N = 1711, for were not fed to nestlings,seeds failedto appear in seed thosestudied in some detail[rs = 0.47, N = 691, and for traps,etc. (cf. Wheelwright1983). Among 15 speciesin thosestudied more intensively {r, = 0.60, N = 421; P < the Lauraceae,there was no correlationbetween research 0.01 forthe Lauraceae[r, = 0.63, N = 151). Neverthe- effort(4-38 hoursof observation/treespecies) and num- less, the fruitsof rareplants seldom compriseda major ber of bird species observed (P > 0.10; Wheelwright portionof birds' diets, as judged by seed-trappingand 1985). recoveringfecal samples. Likewise, rare birds are probably A relatedproblem is thatof unequal abundancesof less importantseed dispersersfor most plants than com- differentspecies of plants or birds.After assigning each monbirds, all else beingequal (althoughsee Wheelwright plantspecies to one of fourcategories (rare, uncommon, and Orians 1982). common,or abundant,based on population estimates Our varied techniquescontribute a thirdsource of made duringcensuses), a correlationalso existsbetween bias, thatof unequal samplingof birds'diets. Recovering commonnessof a plantspecies and numberof birdspecies fecalsamples from mist-netted birds and usingseed traps

Fruit-eatingBirds and TheirFood Plants 185

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 3. Fruit specieseaten by birdswith fewer than four "disperserchoice" by plants that could not have been feedingrecords. gained by narrower,more systematic studies. The physicalcharacteristics of the fruits of plant species Bird studied(excluding the bulkyfruits of the Lauraceae) do spe- not differsignificantly from those of co-occurringfruits ciesa Fruitspecies thatshare the generalsyndrome of bird-dispersal(odor- DP Sapiumoligoneuron less, persistent,juicy, often brightly colored: see van der SP Sapiumoligoneuron, Citharexylum integerrimum Pijl 1972; Janson1983) but forwhich we have no feed- WD Acnistusarborescens GA Prunusannularis, Acnistus aborescens, Citharexylum ing records(Mann WhitneyU test: P > 0.05 foreach integerrimum characteristic;N = 183 spp.). Therefore,our focalplant SC Acnistusarborescens, Witheringia coccoloboides speciesprobably represent an unbiased sample of fruits RB Ocoteatonduzii of bird-dispersedplants at Monteverde. SW Acnistusarborescens FP Conostegiabernouliana CD Rubusrosaefolia RESULTS AND DISCUSSION TK Ocoteatonduzii, Colubrina celtidifolia, Acnistus arbo- rescens Snow's (1981) global surveyof publishedfeeding records GF Conostegiabernouliana, Sapium oligoneuron fortropical fruit-eating birds listed the fruitsof 420 gen- YC Chusqueasp. A (Poaceae) RN Miconia sp. A era in 100 plant families.We have takena differentbut BN Ossaea micrantha complementaryperspective by examininga smallergeo- ON Urera elata, Rubus rosaefolia,Citharexylum integer- graphicalarea in greaterdetail. At least 70 bird species rimum of the lowermontane forests of Monteverde,Costa Rica SV Melastomataceaesp. NC, Cupania glabra feedon fruits(Table 1). Fruit-eatingbirds at Monteverde YV Bocconiafrutescens, Acnistus arborescens, Citharexylum integerrimum representat least 19 familiesand sevenorders (Table 1). BV Hampea appendiculata Nine of the bird specieswere studied in detail and their RH Tremamicrantha, Stemmadenia glabra, Acnistus arbo- feedinghabits are believedto be well known.Seventeen rescens other bird species were studied less systematicallybut CO Acnistusarborescens, Solanum nudum BC Acnistusarborescens were commonlyobserved (Table 2). The diets of the PT Cecropiaobtusifolia remainingbird species are known only fromincidental HT Solanumumbellatum observations(Table 3). SB Rubus rosaefolia,Miconia sp. A., Oreopanaxoerste- We recordedan averageof 10. 1 fruitspecies eaten dianum per birdspecies, or a totalof 709 feedingrecords (Tables TS Rubusrosaefolia, Acnistus arborescens GS Hampea appendiculata,Acnistus arborescens 2 and 3). Table 4 describesthe physical characteristics of YG Acnistusarborescens the fruitseaten by birds.Eighty-nine plant generain 52 CC Citharexylumintegerrimum, Burmeistera sp. A familiesare represented,including 30 generaand seven RS Acnistusarborescens, Citharexylum integerrimum familieswhose fruits are eatenby birdsbut whichare not YH Miconia sp. A, Witheringiasolanaceae mentionedby Snow (1981), plus anothernine genera a Two-lettercodes forbird speciesare definedin Table 1. previouslyrecorded by Snow only for the Old World tropics(Tables 2 and 3). Plant familiesare arrangedin Table 2 accordingto phylogeneticorder following Cron- quist (1981) in orderto illustratepossible coevolved re- appear to be the most effectivemeans of obtainingrep- lationshipsat highertaxonomic levels (order,subclass). resentativediet samples.Consequently, the diets of bird Few researcherspresently expect the evolutionof tight, species for which we could use such techniques(e.g., one-to-onemutualisms between individual species of plants Myadestesmelanops, Phainoptila melanoxantha, Procnias and fruit-eatingbirds (Snow 1981, Howe and Vande tricarunculata,Chiroxiphia linearis) are much better Kerckhove 1981, Thompson 1982, Wheelwrightand knownthan those of vagrants(e.g., Eubuccobourcierii) or Orians 1982). Instead,they anticipate more generalre- migrants(e.g., Piranga rubra).The limitationsof differ- lationships,such as the mutual dependenceof birdsand entsampling techniques probably explain the narrow fruit a guild of fruitspecies. For example,birds in the genera dietsof the lattertwo groups. Ptilonopus,Ducula (Crome 1975), Procnias(Snow 1973), Despitethese limitations, it seemsworthwhile to pres- and Pharomachrus(Wheelwright 1983) feed heavilyon ent the informationon fruit-eatingbirds that existsfor fruitsof the Lauraceaeas a group,but are not restricted one species-richtropical forest,Monteverde, especially to any particularspecies. given the paucityof community-widestudies in other Unlike Snow (1981), we have not classifiedbirds as tropicalforests (Snow 1981). The breadthof our data specializedor unspecialized.No such clear distinctions base may allow insightsinto diet choice by birds and appear in our data (Table 2). To assignbirds to a par- 186 Wheelwright,Haber, Murray,and Guindon

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions ticularcategory, one would need to knowmore about the Cruz 1981). Othermajor food sourcesfor birds are the relativeimportance of differentfruits or alternativefoods arillatefruits of Sapium oligoneuronand Hampea appen- in thediet. Lacking such information, we have attempted diculata, whichboth draw 22 bird species(cf. Guarea, insteadto estimatethe importance of a givenplant species Howe and De Steven1979). Ocoteatonduzii (Lauraceae) to a bird species by notinghow commonlybirds were is unusual among "high investment,high quality" fruits observedfeeding on its fruits(Table 2). Because plant (Table 4) in havingits seeds dispersedby at least 18 bird and birdspecies differ in theirconspicuousness, common- species.It failsto supportthe predictions of some models ness, and suitabilityfor differentsampling techniques, (McKey 1975, Howe and Estabrook 1977) because it broad conclusions,even froma single site, should be attractsmany species,including generalists such as fly- made with some caution. Comparisonsare best made catchersand migratingthrushes. During a fourmonth withingroups in whichsuch confoundingvariables have period, 0. tonduziifruits comprised 59.0 percent(N = been controlledto some degree.Therefore, we have dis- 1393) of thefruits eaten by male Three-wattledBellbirds tinguishedthe bird and plantspecies that were thoroughly (Procniastricarunculata) at fivecalling perches (Wheel- studiedfrom others studied only casually (Table 2). The wrightunpubl. data) and 63.8 percent(N = 58) of those birdspecies listed for well-studied plants (42 plantspecies, deliveredto nestlingResplendent Quetzals (Pharomachrus designatedby "c" in Table 2) are responsiblefor an es- mocinno)at two nests(Wheelwright 1983). timated95 percent(or more) of fruitsremoved by birds. Among plant families,the Lauraceae and Moraceae Thoserecorded at moderatelywell-studied plants (27 plant supportparticularly large numbersof fruit-eatingbirds. species,designated by "d") probablycontribute a major- The Rubiaceae,Melastomataceae, and Solanaceaealso in- ityof fruitremoval by birds.Bird speciesrecorded at the cludemany bird-dispersed species, but withthe exception remaining(102) plant speciesremove an unknownpro- of Acnistusthey tend to producesmall crops fed upon portionof fruits. chieflyby understorybirds. Nonetheless,they probably For many (36.9%) plant species,we have feeding constitutea majorportion of thediets of understory/sub- recordsinvolving only a single bird species. For about canopyspecies such as solitairesand manakins.For ex- halfof the species,we have recordsinvolving fewer than ample, 26.2 percentof 844 fruitseaten by male Long- threebird species. For only 8.9 percentof the plant species tailedManakins at sevendisplay perches represented eight did we observemore than 10 birdspecies. In mostcases, speciesin the Solanaceae, 8.9 percentrepresented three the observationof a small numberof bird speciesprob- speciesin the Melastomataceae,and 5.2 percentrepre- ably reflectsthe rarityor inconspicuousnessof the plant sentedfive species in the Rubiaceae (Wheelwrightun- species,or its infrequentuse by birds,rather than a spe- publ. data). cializedor coevolvedrelationship with a small numberof Feedingrecords reflect unequal degreesof frugivory seed dispersers.A perplexingexception is Solanumum- among differentgroups. Non- accounted for a bellatum(Solanaceae), an abundantshrub that produces fargreater number of feedingrecords (Tables 2 and 3) clustersof yellowfruits relished by two dissimilarbird thanexpected by theirnumber of species(mean number species-Emerald Toucanets (Aulacorhynchusprasinus) of fruitspecies eaten/bird species = 14.8; x2 Two-Sam- and Yellow-throatedEuphonias (Chiroxiphia linearis) (as ple Test: P < 0.001). Similarly,sub-oscines (versus os- well as variousbat species:E. Dinerstein,pers. comm.)- cines) and thrushes(versus other passerines) ate a wider but ignored,at leastwhile alternative fruits are available, than averagerange of fruitspecies (x = 10.0 and 17.1 by almostall otherspecies. We foundsignificant positive fruitspecies/bird species, respectively; x2 Two-Sample correlationsbetween plant size (herb,shrub, or tree)and Tests: P < 0.05 and P < 0.001, respectively).The same the numberof bird species observed(Spearman Rank resultshold evenif fruitrecords involving the morethor- Correlation:r, = 0.40, P < 0.00 1, N = 133 plantspecies). oughlystudied Lauraceae are excluded.Note that these Certainplant species attract a disproportionatelylarge and otherresults should be viewedin thecontext of sam- numberof bird species. Snow (1981) singled out the plingbiases, discussed above, although they are consistent plant genera Cecropia,Ficus, and Trema,which are also with widelyaccepted impressions of the food habits of popular among birds at Monteverde.Other key genera neotropicalbirds (e.g., Skutch 1967). are Acnistus(Solanaceae), Sapium (Euphorbiaceae),Cy- Birdspecies that depend mainly on fruitsfor food are tharexylum(Verbenaceae), Hasseltia (Flacourteaceae), no more likelyto be polygamousor sexuallydimorphic Conostegia(Melastomataceae), and Hampea (Malvaceae) in plumagethan birdsthat eat littleor no fruit,in spite (Tables 2 and 3). The speciesin mostof thesegenera are of expectationsto thecontrary (Snow 1971). We divided colonizersof disturbedhabitats (tree fall gaps, landslides, birdspecies into four groups based on thenumber of fruit abandonedpastures) and producelarge crops of medium- speciesrecorded in theirdiet (0, 1-9, 10-19, 20 or more; sized fruits.Acnistus arborescens, a common small tree Tables 2 and 3). Of course,some more directmeasure with wateryorange berries produced asynchronously, is of theimportance of fruitswould be preferableto number fedupon heavilyby at least43 birdspecies (cf. Dunalia, of specieseaten. Such informationis difficultto get for Fruit-eatingBirds and Their Food Plants 187

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 4. Characteristicsoffruits eaten by birds at Monteverde,Costa Rica.

Wet seed Wet Wet Per- wt/ fruit fruit cent wet % diam. wt. Percentsug- fruit Crude % Family Species (cm) (g) Fruitdisplaya water ar wt % N fat TNCb Annonaceae Guatteriaconsanguinea 1.7 2.70 Black & red 86 5 0.09 1.1 3.3 21.0 Apocynaceae Stemmadeniaglabra 0.6 0.13 Black & orange 0.69 - - Tabernaemontanasp. A 0.8 0.25 Black & orange 12 0.48 - - Aquifoliaceae Ilexlamprophylla 0.5 0.07 Red 0.29 - - Aracaceae Chamaedoreasp. A 1.0 0.55 Black & orange 12 0.67 - - Araceae Anthuriumsp. A 0.6 0.13 Red 5 0.08 - - A. sp. B 0.8 0.52 Red & pink 4 0.35 - - A. sp. C 0.9 0.49 Orange 9 0.12 - - Araliaceae Dendropanaxarboreus 0.7 0.20 Black & white 0.05 - - D. gonatopodus 0.7 0.14 Black & white 8 0.43 - - D. sp. FL 0.5 0.08 Black & white 22 0.13 - - - Didymopanaxpittieri - - Black & white Oreopanaxoerstedianum 0.6 0.10 Black & white 31 0.20 - - 0. xalapensis 0.7 0.15 Black & white 13 0.27 - - Asteraceae Clibadiumsp. A 1.0 0.59 Black 4 0.05 - - C. sp. B 0.5 0.06 Black 6 0.17 - - Boraginaceae Tournefortiaglabra 0.7 0.16 White - 6 0.25 - - Campanulaceae Burmeistera sp. A 0.8 0.32 Red 5 0.06 - - Caprifoliaceae Viburnumcostaricensis 0.6 0.12 Black 17 0.42 - - Cecropiaceae Cecropiaobtusifolia - Green Celastraceae Sp. A 2.0 3.50 Red & orange 0.29 - - Perrottetialongistylis 0.6 - Red Maytenussp. A 0.6 - Black & white Clusiaceae Clusia elata 0.3 0.05 Red 5 0.60 - - Commelinaceae Campeliazanonia 0.8 1.20 Black 1 0.08 - - Cucurbitaceae Sp. A 1.3 1.65 Black 6 0.21 - - Ericaceae Cavendishiamelastomoides 1.1 0.65 Blue & white 14 0.05 - - C. sp. A 1.0 0.42 Red & pink 3 0.05 - - Erythroxylaceae Erythroxylonamplum 0.6 0.16 Red & yellow 21 0.44 - - Euphorbiaceae Sapiumoligoneuron 0.6 0.07 Red 0.86 - - Flacourtiaceae Casearia sylvestris 0.8 0.17 Orange & yellow 6 0.53 - - Hasseltiafloribunda 0.8 0.20 Dark red & red 90 4 0.20 1.3 0.9 37.8 Xylosmachloranthum 1.1 0.77 Black & red - 12 0.23 - - - X.flexuosa 0.9 0.40 Red 15 0.15 - - X. intermedium 0.6 0.15 Black 8 0.13 - - Gesneriaceae Beslariaformosa 0.8 0.31 Orange 6 0.05 - - Lauraceae Beilschmiediasp. BC 2.2 12.89 Black 69 - 0.48 1.1 11.6 10.2 B. costaricensis 2.3 12.42 Black 76 - 0.63 1.3 11.2 3.4 B. sp. BL 2.5 15.19 Black 64 - 0.52 - Nectandrasp. NC 1.0 1.08 Black & red 65 - 0.40 - - - N. davidsoniana 1.7 3.25 Black & red 77 9 0.57 1.2 25.3 11.0 N. gentlei 1.2 0.98 Black 63 - 0.49 1.6 36.1 9.0 N. hypoglauca 1.8 5.50 Black & red 67 - 0.52 1.5 32.2 17.9 N. salicina 1.9 7.42 Black & red 69 10 0.52 1.3 37.3 20.1 N. sp. NV 1.7 4.03 Black & red 67 - 0.52 - Ocoteaaustinii 1.1 1.31 Black & red 62 - 0.48 1.1 45.2 8.7 0. bernouliana 1.8 6.62 Black & red 86 6 0.58 2.3 5.8 7.9 0. sp. FL 2.2 9.28 Black & red 84 3 0.55 1.9 23.5 7.4 0. klotzschiana 1.8 5.98 Black & red 86 - 0.50 3.2 18.3 6.5 0. sp. K2 2.0 7.43 Black & red 78 - 0.54 2.4 26.9 17.0 0. sp. RP 1.2 1.37 Black & red 75 - 0.55 2.8 17.3 3.6 0. tonduzii 1.2 1.34 Black & red 66 14 0.43 1.0 29.4 16.7 0. wachenheimii 1.7 2.94 Black 76 12 0.56 1.4 31.1 17.7 Perseasp. RP 0.8 0.29 Blue 52 - 0.52 - P. veraguensis 1.1 0.67 Blue 58 - 0.67 - - - Phoebeneurophylla 1.3 1.62 Black & red 68 - 0.36 1.1 - 10.2 P. mexicana 1.2 1.38 Black & red 68 7 0.50 1.2 28.0 9.0

188 Wheelwright,Haber, Murray,and Guindon

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 4. (Continued).

Wet seed Wet Wet Per- wt/ fruit fruit cent wet % diam. wt. Percentsug- fruit Crude % Family Species (cm) (g) Fruitdisplaya water ar wt % N fat TNCb Liliaceae Smilaxsp. A 1.1 0.57 Red & orange 3 0.30 Loranthaceae Sp. A 0.5 - Black & orange Sp. B 0.5 0.05 Brown 12 0.20 Gaiadendronpunctatum 0.3 0.02 Yellow 0.50 Malpighiaceae Bunchosiasp. A 2.7 9.20 Green - 0.23 B. pilosa 1.8 2.17 Red & orange 0.33 Malvaceae Hampea appendiculata 1.1 0.50 Black & white 56 - 0.65 0.7 0.3 35.2 Malvaviscusarboreus 1.3 0.30 Red 91 5 0.10 - Marcgraviaceae Marcgraviabrownei 0.9 0.29 Red & yellow 17 0.10 - - - Melastomataceae Blakeasp. A 0.8 - Red 6 - - - Conostegiabernouliana 1.1 - Black 10 - - - C. xalapensis 0.9 0.30 Black 0.05 - - Ossaeasp. A 0.6 0.09 White - 7 0.05 0. micrantha 0.5 - Black & blue Meliaceae Guareatonduzii 0.8 0.48 Red & white - 0.94 - - G. tuisiana 2.2 7.45 Red & white 18 0.85 - - G. glabra - - Red & white - - Trichiliahavanensis 0.6 0.11 Red 0.64 - - Monimiaceae Siparunasp. A 0.4 0.03 Red & blue 0.67 - - Moraceae Ficuspertusa 1.0 1.00 Dark red & red 8 0.08 - - F. tuerckheimii 1.7 2.60 Red 6 0.08 - - Trophismexicana 0.8 0.21 Red 14 0.19 - - Myrsinaceae Ardisia compressa 0.9 0.37 Black & red 3 0.24 - - A. palmana 1.3 0.21 Black & red 88 8 0.24 0.6 2.6 30.6 Rapanea myricoides 0.4 0.01 Black Myrtaceae Eugeniasp. A 1.2 0.76 Black & red 7 0.36 - - E. sp. B 1.7 4.82 Red & orange 80 12 0.48 0.7 1.7 18.0 Nyctaginaceae Neeaamplifolia 1.2 1.19 Dark red & red 7 0.20 - - - Torrubiacostaricensis 0.7 0.28 Dark red & red - 13 0.36 Papaveraceae Bocconiafrutescens 0.3 0.25 Black & red & - 20 0.72 - - yellow Phytolaccaceae Phytolaccarivinoides 0.8 0.23 Black & red 9 0.17 - - P. sp. A 0.7 0.12 Black & red - - 1.00 - Piperaceae Piperauritum - - Green Poaceae Lasiacis - - Black Rhamnaceae Colubrina - - Orange Rosaceae Prunuscornifolia 1.7 2.78 Black & red 76 18 0.46 0.8 0.5 38.0 P. sp. A 1.5 1.40 Black & red - 12 0.29 P. annularis 1.5 2.24 Black & red - 12 0.24 Rubusrosaefolia 1.7 - Black 77 8 0.37 - Rubiaceae Chionecostaricensis 1.0 - Red Coussariaaustin-smithii 1.7 1.90 Black & blue 94 - 0.42 2.1 C. sp. A 1.4 - Black & blue Faramea quercetorum 1.1 0.90 Blue - 2 0.46 - Guettardapoassana 0.8 - Black & blue - - Hameliapatens 0.9 0.30 Black & red 10 0.03 - Hoffmanniasp. A 0.9 0.29 Black & red 2 0.03 - Palacoureagaleottiana 0.8 0.57 Black - 4 0.07 - Psychotriaacuminata 0.9 0.38 Black & yellow - 0.26 - P. sp. BO 1.1 0.71 Black & blue 3 0.11 - P. sp. LP 0.8 0.29 Red & yellow - 5 0.07 - P. sp. C 1.0 0.50 Red & orange - 4 0.18 Rutaceae Mappia racemosa 1.7 5.90 Black 77 8 0.37 2.0 1.2 M. sp. A 0.5 - Brown Zanthoxylumsp. A 0.4 0.03 Black - - 1.00 - Sabiaceae Meliosmaidiopoda 1.1 1.10 Yellow & white - 0.09 - - Sapindaceae Cupania glabra 0.8 - Red & orange

Fruit-eatingBirds and Their Food Plants 189

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions TABLE 4. (Continued).

Wet seed Wet Wet Per- wt/ fruit fruit cent wet 0 diam. wt. Percentsug- fruit Crude % Family Species (cm) (g) Fruitdisplaya water ar wt % N fat TNCb Matayba apetala 0.8 - Black & orange Paulliniasp. A 0.9 0.25 Black & white 24 0.60 - - & red Simaroubaceae Picramniacarpenterae 1.1 Black & red Solanaceae Acnistusarborescens 0.8 0.24 Orange 13 0.08 Cestrumsp. A 0.8 0.22 Black 10 0.14 - - C. megaphyllum 0.8 0.53 Black & blue 7 0.21 - - C. racemosa 0.7 0.48 Black & blue 7 0.06 - - Lysianthesmultiflora 1.3 1.15 Red 89 9 0.13 2.1 1.3 15.6 L. synanthera 0.9 0.40 Yellow 0.13 - - Solanumcordovense 0.9 0.52 Black - 11 0.08 S. nudum 1.2 1.31 Yellow 12 0.20 - - S. umbellatum 1.3 1.11 Yellow 11 0.19 - - Witheringiasolanaceae 1.2 0.71 Orange - 5 0.17 - - W. coccoloboides 1.0 0.58 Orange 90 - 0.09 - W. sp. A 1.0 0.64 Orange - 4 0.05 W. maculata - - Red Symplocaceae Symplocoslimoncillo 1.0 0.90 Blue S. sp. A 1.9 5.26 Blue 18 0.43 - - S. sp. B Blue Theaceae Symplocarponsp. A 1.0 0.84 Blue - 9 0.19 Thymeliaceae Daphnopsis 0.8 0.23 White - 24 0.26 Ulmaceae Tremamicrantha 0.4 0.02 Orange - 12 0.50 Urticaceae Ureraelata 0.3 - Red 6 0.25 - - Verbenaceae Citharexylumintegerrimum 0.8 0.21 Black & yellow - 20 0.33 0.8 2.0 38.1 C. macradenium 1.1 0.70 Black & orange 75 20 0.13 0.3 2.5 38.4 Vitaceae Cissussp. A 1.1 0.52 Black 5 0.19 - - Unknown Epiphytesp. A 0.5 0.07 Brown 0.14 - - a "Fruitdisplay" representsthe color of ripe fruits.Species with "simple" displays(e.g., "red" and "black") have greenunripe fruitsand lack contrastinglycolored associated structures (see text). b Total nonstructuralcarbohydrates.

any birdspecies, but whereit is available,there seems to add the followinggenera to Snow's (1981) list: Chamae- be a good correspondencebetween number of fruitseaten petes,Elaenia, Mionectes,Myadestes, Phainoptila, Chlo- and degreeof frugivory(cf. Skutch 1967, Table 2). About rophonia,and Euphonia.The evidenceis inconclusivethat 10 percentof all Monteverdebird species are polygamous all pigeonsin the genus Columbaare seed predators(Ol- and about 20 percentare sexuallydichromatic. These son and Blum 1968); at MonteverdeC. fasciata in par- proportionsdo not differsignificantly among categories ticularmay be effectiveseed dispersersof many plants reflectingdegree of frugivory(x2 Two-SampleTest: P > withsmall seeds. Several Turdus and Catharusspecies eat 0.05). Of tenbird species that feed on 20 or morespecies fruitalmost exclusivelyduring some seasons and could of fruits,only two (Procnias tricarunculataand Chiro- be consideredfruit specialists at such times. xiphia linearis)are polygamousand onlythree (the same Diet choiceby birdsat Monteverdeand its selective two speciesplus Pharomachrusmocinno) are distinctlysex- influenceon the evolutionof fruittraits have been ana- ually dichromatic. lyzedelsewhere (Wheelwright 1985). Therefore,we sim- If birds are to be determinedas specializedon the ply providesummary statistics and manyof the original basis of thefrequency of fruitin theirdiets (Wheelwright data here. For the fruitsin Table 4, the means (and and Orians 1982) and not on thequality of seed dispersal standarddeviations) are as follows:weight 1.60 (?2.76) theydeliver (Howe and Estabrook1977) or the charac- g; diameters10.5 (?4.9) mm; sucroseequivalents mea- teristicsof the fruitsthey select (Snow 1981), we would suredby refractometer9.88 (?6.18) percent;and seed:

190 Wheelwright,Haber, Murray,and Guindon

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions fruitratios 0.32 (? 0.23). A blackfruit with contrastingly Lauraceae (in ordernot to bias the sample of fruitsin colored(not black, brown,or green)unripe fruits or as- Table 4 forwhich there is nutritionalinformation towards sociatedstructures (bracts, pedicels) is the mostcommon heavyor oily fruits).Ricklefs (1977), hamperedby the fruitdisplay; simple displaysof black or red fruitsthat same shortageof adequate data, could compareonly four are greenwhen unripe follow in frequency(Table 4). plant species fromdifferent habitats in his attemptto discriminategroups of bird species feedingat different trees.The problemsof samplingfrom a heterogeneous, CONCLUSION inadequateliterature continue to plague generalsurveys and createcontroversy (cf. Stiles 1980, Herrera 1982, When Herrera(1981) set out to comparethe qualityof Stilesand White 1982). The data presentedhere and in temperateand tropicalfruits, he could uncoverappropri- Janson(1983) should contributea morerealistic view of ate data foronly 15 tropicalplant species.Moreover, as the diversityof tropicalfruits and the complex choices he noted, those were hardlya representativesample of fruit-eatingbirds make betweenthem. tropicalfruits. Thirteen of the 15 species (87%) have single-seededfruits, as opposedto only1 13 of 263 species (43%) in thelower montane forests of Monteverde.Seed: ACKNOWLEDGMENTS fruitratios and Herrera's(1981) measureof fruitquality We thankthe residentsof Monteverdefor sharing observations dependstrongly on seed number,single-seeded fruits hav- and allowingus to studythe varietyof habitatsthat occur on ing relativelylittle pulp fora givenseed weight(cf. Table privatelyowned land withinthe community.K. Winnett-Mur- ray,J. Thompson,T. Moermond,and an anonymousreviewer 4). The majorconclusion of Herrera'spaper-that trop- made helpfulcomments on the manuscript.NTW receivedfi- ical and temperatefruits are equivalentin termsof overall nancialsupport from NSF, the N. Y. Zoological Society,and a profitability-isnot supportedwhen a more representa- CarrPostdoctoral Fellowship at theUniversity of Florida.WAH tive sample of tropicalfruits is used. Monteverdefruits and CG weresupported by the Universityof California,Berke- havefar lower overall profitabilities (x = 1.77, SD = 2.99, leyand an NSF grantto G. W. Frankie.KGM receivedsupport fromthe Universityof Florida,Sigma Xi, and an NSF grantto N = 13) than eitherthe temperateor tropicalsamples P. Feinsinger.For assistancein the identificationof a difficult reportedby Herrera(1981) (Mann-WhitneyU Test: P < flora,we thank the Chicago Field Museum and Missouri Bo- 0.01) once we exclude all but two randomlyselected tanicalGarden.

LITERATURE CITED

BAIRD, J. W. 1980. The selectionand use of fruitby birdsin an easternforest. Wils. Bull. 92: 63-73. CROME, F. H. J. 1975. The ecologyof fruitpigeons in tropicalnorthern Queensland. Aust. Wildl. Rev. 2: 155-185. CRONQUIST, A. 1981. An integratedsystem of classificationof floweringplants. Columbia UniversityPress, New York. CRUZ, A. 1981. Bird activityand seed dispersalof a montaneforest tree (Dunalia arborescens)in Jamaica. Biotropica 13 (supplement"Reproductive Botany"): 34-44. HERRERA, C. M. 1981. Are tropicalfruits more rewardingto dispersersthan temperateones? Am. Nat. 118: 896-907. 1982. Some commentson Stile's paper on bird-disseminatedfruits. Am. Nat. 120: 819-822. HOWE, H. F. 1977. Bird activityand seed dispersalof a tropicalwet foresttree. Ecology 58: 539-550. 1981. Dispersalof a neotropicalnutmeg (Virola sebifera)by birds. Auk 98: 88-98. AND G. F. ESTABROOK. 1977. On intraspecificcompetition for avian dispersersin tropicaltrees. Am. Nat. 111: 817- 832. AND J. SMALLWOOD. 1982. Ecologyof seed dispersal.Ann. Rev. Ecol. Syst. 13: 201-228. AND D. DE STEVEN. 1979. Fruitproduction, migrant bird visitation,and seed dispersalof Guarea glabra in . Oecologia 39: 185-196. , AND G. A. VANDE KERCKHOVE. 1979. Fecundityand seed dispersalof a tropicaltree. Ecology 60: 180-189. JANSON, C. H. 1983. Adaptationof fruitmorphology to dispersalagents in neotropicalforest. Science 219: 187-189. JENKINS, R. 1969. Ecologyof threespecies of Saltatorswith special referenceto theirfrugivorous diet. Ph.D. Thesis. Harvard Univ. KANTAK, G. E. 1979. Observationson some fruit-eatingbirds in . Auk 96: 183-186. LAWTON, R., AND V. DRYER. 1980. The vegetationof the MonteverdeCloud ForestReserve. Brenesia 18: 101-116. McKEY, D. 1975. The ecologyof coevolvedseed dispersalsystems. In L. E. Gilbertand P. H. Raven (Eds.). Coevolutionof animalsand plants.Univ. of Texas Press,Austin. OLSON, S. L., AND K. E. BLUM. 1968. Avian dispersalof plantsin Panama. Ecology49: 565-566. RICKLEFS, R. E. 1977. A discriminantfunction analysis of assemblagesof fruit-eatingbirds in CentralAmerica. Condor 79: 228-231. SIEGEL, S. 1956. Nonparametricstatistics. McGraw-Hill Book Co., New York. SKUTCH, A. F. 1967. Life historiesof CentralAmerican highland birds. Nuttall OrnithologicalClub, No. 7. Cambridge,Mass. SNOW,B. K. 1970. A fieldstudy of the Bearded Beilbirdin Trinidad.Ibis 112: 299-329.

Fruit-eatingBirds and Their Food Plants 191

This content downloaded from 139.140.232.150 on Fri, 28 Mar 2014 14:25:40 PM All use subject to JSTOR Terms and Conditions SNOW, D. W. 1971. Evolutionaryaspects of fruit-eatingby birds.Ibis 113: 194-202. 1973. Distribution,ecology and evolutionof the beilbirds(Procnias, Cotingidae). Bull. Brit.Mus. (Nat. Hist.) 25: 9. 1981. Tropicalfrugivorous birds and theirfood plants:a worldsurvey. Biotropica 13: 1-14. SORENSEN, A. E. 1981. Interactionsbetween birds and fruitin a temperatewoodland. Oecologia 50: 242-249. STILES, E. W. 1980. Patternsof fruitpresentation and seed dispersalin bird-disseminatedwoody plants in the easterndeciduous forest.Am. Nat. 116: 670-688. , AND D. W. WHITE. 1982. Additionalinformation on bird-disseminatedfruits: response to Herrera'scomments. Am. Nat. 120: 823-827. THOMPSON, J. N. 1982. Interactionand coevolution.Wiley-Interscience, New York. VAN DER PIJL, L. 1972. Principlesof dispersalin higherplants. Springer-Verlag, New York. WHEELWRIGHT, N. T. 1983. Fruitsand the ecologyof ResplendentQuetzals. Auk 100: 286-301. 1984. The timingof floweringand fruitingin a guild of tropicalbird-dispersed trees. Oikos (in press). 1985. Fruitsize, gape width,and the diets of fruit-eatingbirds. Ecology(in press). AND G. H. ORIANS. 1982. Seed dispersalby : contrastswith pollen dispersal,problems of terminologyand constraintson coevolution.Am. Nat. 119: 402-413.

Notice for the Second International Legume Conference

The SecondInternational Legume Conference, held jointlyby the MissouriBotanical Garden and the Royal BotanicGardens, Kew, will take place on 23-27 June, 1986. Sessionswill be heldin theRidgway Center at theMissouri Botanical Garden, P.O. Box 299, St. Louis,Missouri 63166, USA. The Conferencetheme is the Biology of the Leguminosae.The aim of the meetingis to discussrecent advances in our understandingof the biologyof legumes,gained fromboth field and experimentalresearch, and coveringboth pure and applied pointsof view. The multidis- ciplinaryapproach of the Conferenceis designedto addressa wide varietyof researchinterests and to stimulatediscussion among specialists.The workinglanguage of the Conferencewill be English. Scheduled topics include: life historystudies; tree architecture;evolution and biology of inflorescencesand pollen; floralorganogenesis; ecology; ecological biogeography; pollen-stigma- styleinteractions; structure and functionof legumefruits and seeds; mycorrhizalrelationships; cyanogenesis;evolution of symbioticgenes; biologicalimplications of genome evolution;ant- domatia,aphid-legume, tick-legume, and bruchid-legumeco-evolution; biological changes in- duced by domestication;computerized data bases and biologicalresearch; international legume data bases. Participationin the Conferencewill be limitedto 350 persons.If you would like more informationor wish to submita proposalfor a posterpresentation, please contactDr. James L. Zarucchi,Legume ConferenceCoordinator, Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri63166, USA.

192 Wheelwright,Haber, Murray,and Guindon

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