The Condor 96:354-361 0 The Cooper Omithological Society 1994

DIETS OF LAND FROM NORTHEASTERN VENEZUELA ’

BRIGITTEPOULIN, G~~TAN LEEEBVREAND RAYMOND MCNEIL Dgpartementde sciencesbiologiques, lJniversit& de Montrtial C.P. 6128, succursalecentre-ville, Montr&al, QuebecH3C 3J7 Canada

Abstract. We estimate diets of 68 species inhabiting dry seasonal habitats and mangrovesof northeasternVenezuela, basedon 3,4 19 birds forced to regurgitateusing tartar emetic. Most birds were generalist feeders, including a wide variety of both invertebrate and plant taxa in their diet. Coleopterans,ants, and larvae were the most frequent invertebrate preys. Hummingbirds had low nectar intakes and differed from other species by feeding extensively on small soft-bodied . Most species fed on fruits to a variable extent. Actually, several speciestended to be more frugivorous at our study sites than in previous reports. Key words: Arid habitats;diet; mangroves:Venezuela.

INTRODUCTION zuela. In Guarapo, three study areaswere delim- Direct examination of diets is generally under- ited within 7 km along a humidity gradient from represented in studies of avian ecology (Rosen- the coast to inland areas and correspond to a berg and Cooper 1990). In particular, the diet of thorn scrub, a thorn woodland, and a deciduous many neotropical speciesis poorly known (Col- forest (Sarmiento 1972, 1976). In Laguna de Co- lins et al. 1990, Karr and Brawn 1990, Loiselle cos, sampling was done in a thorn forest and in and Blake 1990). Food exploitation is neverthe- black mangrove (Avicennia germinans) wood- less central to our understanding of avian com- land. munity organization. Many studies carried out At all study sites, birds were mist-netted twice in tropical latitudes have related bird abundance monthly during at least a complete annual cycle and phenology to feeding habits (e.g., Snow and between September 1984 and August 1987. Re- Snow 1964, Orians 1969, Karr 1976, Greenberg gurgitation samples were obtained by adminis- 1981, Bell 1982, Wong 1986, Loiselle 1988). In tering tartar emetic to wild-caught birds (see most cases,species were assignedto feedingguilds Poulin et al. [ 19941 for details of methodology). using , individual observations,or data Food items were identified to order or family drawn from the literature. Information on diets (invertebrates) or to species(fleshy fruits). Dry was slight and collected during a small portion fruits were counted when possible and assigned of the annual cycle. to species,but most of them were not identified Here we estimate the diet of 68 bird species taxonomically. Because nectar is 100% assimi- found in the major habitats of northeastern Ven- lable (Remsen et al. 1986) its consumption was ezuela (i.e., thorn scrub, thorn woodland, thorn evaluated through the presenceof pollen grains forest, deciduous forest, and mangrove wood- in emetic samples. lands) (Sarmiento 1976). Diet samples were ob- RESULTS tained twice monthly over two annual cycles by forcing 3,4 19 birds to regurgitateusing antimony SPECIESDIET potassium tartrate (Poulin et al. 1994). The intake of invertebrate and plant food is de- tailed for each species in Appendices 1 and 2, METHODS respectively. Although not appearing in the ta- This study was carried out in Guarapo bles, we found a fish in a sample of the kingfisher (10”39’00”N, 63”41’55”W) and Laguna de Cocos Choroceryleamericana. We do not have samples (10”29’33”N, 63”45’OO”W) on the Araya Penin- from carnivorous species,but on three occasions sula, in the state of Sucre, northeastern Vene- in mangroves an owl (Glaucidium brasilianum) was captured along with its prey: a cicada, a bat, and a (Conirostrum bicolor). ’ ’ Received9 November1993. Accepted 15 Novem- Diets of the most abundant speciesare sum- ber 1993. marized below by grouping the speciesthat fed

[3541 DIETS OF LAND BIRDS FROM VENEZUELA 355 regularly on specific food types, i.e., nectar, in- erageof 17 fruits (1,684/100) per emetic sample, sects,fruits, and seeds. taken from 18 different plant species.This mock- In most nectarivorous species,the proportion ingbird neverthelessfed on a wide variety of in- of samples with pollen was inversely related to vertebrates, mainly large ground-dwelling ar- intake (Appendices 1 and 2) suggest- thropods.Thraupisglaucocolpa was characterized ing that the presenceof pollen reflects a reason- by a lower intake ofarthropod compared to other able overall estimate of nectar consumption. With mixed-feeders (Table 1). Among the Tyrannidae, the exception of Glaucis hirsuta that showed a Elaenia parvirostris, Phaeomyias murina and clear preference for nectar, most hummingbirds Myiarchus tyrannulus were the most frugivo- fed extensively on small, soft-bodied arthropods. rous. The Dendrocolaptidae and Formicariidae As many as 8.8 and 6.5 arthropods were iden- also fed on fruits, but to a lesser extent. tified on average in Amazilia tobaci and Leucip- Two unidentified dry fruit specieswere taken pusfallax, the two most abundant species.Hum- by 15 bird species,although only Tiaris bicolor mingbirds differed from other speciesby feeding and Coryphospinguspileatus can be considered mainly on small Diptera, wasps, and , granivores. Tiaris bicoloralone fed on seedsfrom whereas only Leucippusfallax fed consistently 13 different species,whereas arthropods (mainly on Coleoptera. Some hummingbirds occasion- insect larvae, Homoptera, Coleoptera, and Isop- ally fed on seeds and fleshy fruits. These were tera) were observed in only 23% of the samples. probably not taken accidentally, since 24 seeds Coryphospinguspileatus fed more regularly on were found in a single sample from Amazilia , especially Coleoptera and ants. tobaci. Among , Coerebaflaveola in- cluded in a wide range of resourcesamong nectar, FOOD EXPLOITATION AT THE fruits, seeds,and invertebrates, with insect larvae COMMUNITY LEVEL the most important prey in the last category. The number of species feeding on specific in- Among insectivores, Hypnelus ruficollis and vertebrate taxa was highest for Coleoptera (52) Thamnophilus doliatus fed on a great variety of ants (45) insect larvae (44), spiders (37) and large invertebrates. Woodcreepers (Xiphorhyn- wasps (35) (Table 2). Most birds represented by thus and Lepidocolaptes)fed mainly on non-fly- large sample size fed on several invertebrate taxa, ing arthropods. Formicivora grisea was an op- but still showeda clear preferencefor Coleoptera portunistic feederas suggestedby the high number and Hymenoptera (ants) (Table 2). These two of taxa taken (Table l), as well as its consumption invertebrate taxa alone accounted for 60% of all of winged ants and termites. Atalotriccuspilaris, invertebrate items found in emetic samples and also fed on a wide variety of invertebrate taxa, representedthe first- and second-mostimportant but mostly on small Coleoptera. Feeding gener- prey for 32 and 22 birds species, respectively alism was particularly notable in mangroves (Table 2). Actually, speciesfeeding more exten- where both residents (Conirostrum bicolor, Cer- sively on other invertebrate taxa were mostly thiaxis cinnamomea, Fluvicolapica) and nearctic hummingbirds (Diptera, wasps, Araneae) and migrants (Seiurus noveboracensis,Protonotaria mangrove species(Homoptera, Lepidoptera). citrea, Setophaga ruticilla) included an impres- The mean number of items within a sample sive number of invertebrate taxa in their diet varied accordingto the different invertebrate taxa relative to the number of emetic samples (Table (Fig. 1). Large invertebrates, such as isopods, 1). Few insectivores specialized on specifictaxa, millipedes, centipedes,scorpions, dragonflies, and but Sublegatusmodestus showed a clear prefer- orthopteranstended to be representedby a single ence for ants which accounted for 80% of all item in samples. Many of the most frequent taxa arthropods taken. in the birds’ diet such as Coleoptera, insect lar- Some small frugivorous-insectivorous species, vae, wasps,and spiderswere representedby only such as Phaeomyias murina and Hylophilusfla- two or three items on average per sample. Dip- vipes,included a large diversity of plant species tera and ants tended to be represented by four as well as arthropod taxa in their diet (Table 1). or five items. Finally, termites, winged ants, and Tachyfonusrufus fed extensively on fruits from insect eggsall occurred in high numbers within several species,but showeda clear preferencefor a same sample. large ants among invertebrates. Mimus gilvuswas Most birds also fed on vegetable matter to a another highly frugivorous specieswith an av- variable extent. Of 68 bird species,only 2 1 never 356 B. POULIN, G. LEFEBVRE AND R. MCNEIL

TABLE 1. Occurrenceand diversity of the different food types in the diet of the bird speciesrepresented by more than five emetic samples.

Percent of emetic samples with Number of taxa taken Number of Inverte- IlWXt~- Bird species samples brates “2: Seeds’ POllelI brates E2 Seeds

Glaucishirsuta 8 38 100 4 0 Chlorostilbonmellisugus 42 86 50 6 0 Leucippusfallax 121 91 2 2 55 11 3 Amazilia tobaci 48 4 33 9 :, Hypnelusrujicollis 8 :: 13 9 1 : Melanerpesrubricapillus 9 89 67 3 6 0 Certhiaxis cinnamontea 17 100 12 0 Xiphorhynchuspicus 24 100 4 8 : Lepidocolaptessouleyetii2 17 100 6 10 :, Thamnophilusdoliatus 21 100 11 12 : 0 Formicivora grisea 114 99 2 1 16 2 1 Phaeomyiasmurina 153 82 81 1 13 19 1 Sublegatusmodestus 139 100 19 3 11 9 Myiopagis viridicata 6 100 17 5 2 :, Elaenia parvirostris 14 50 93 3 7 0 Atalotriccuspilaris 124 99 10 4 15 6 Idioptilon margaritaceiventris 6 100 17 6 2 : Tolmomyiasflaviventris2 12 100 8 8 7 1 1 Cnemotriccusfuscatus 25 100 12 4 8 1 Fluvicolapica2 19 100 11 : 0 Myiarchus tyrannulus 37 84 51 3 10 12 1 Troglodytesaedon 100 8 0 0 Polioptila plumbea 8: 99 3 4 11 1 2 Mimus gilvus 100 67 91 1 10 18 olivaceus 45 98 27 2 13 6 : Hylophilusjlavipes 125 85 83 4 13 14 Setophagaruticilla= 15 100 11 0 : Protonotariacitrea2 34 97 3 10 1 0 Seiurusnoveboracensis2 98 100 16 0 0 Coerebaflaveola 503 85 12 3 64 11 8 Conirostrumbicolo? 118 100 1 14 1 : Thraupisglaucocolpa 40 20 100 3 11 0 Tachyfonusr&is 71 93 80 6 7 13 2 Coryphospinguspileatus 113 75 5 59 8 4 8 Cardinalis phoeniceus 80 83 48 84 10 6 Sporophilalineola 6 100 : 0 2 Tiaris bicolor 231 23 8 95 10 5 13 Icterus nigrogularis 9 22 7 3 0

’ Refers either to dry fruits or to fleshy fruits whose seeds were pounded in samples. 2 Species mostly or entirely sampled in mangrove habitat. fed on plant food. Of these, 17 specieswere rep- the first choice of only two species,both insec- resented by three emetic samples or less, and tivorous (Sublegatus modestusand Atalotriccus three were species occupying mangrove areas pilaris). On the other hand, Lycium nodosumwas (mangrove fruit pods are not consumed by pas- the preferred fruit of two highly fmgivorous spe- serines, Smith 1987). Tournefortia scandeus, cies (Mimus gilvus and Elaenia parvirostris). Al- Lycium nodosum,and Pilosocereusmoritzianus though fruits of Erythroxylum cumanensewere were the most important fruits in the birds’ diet taken by 15 bird species,only Tachyfonusrufus (Table 3). Fruits from many plant specieswere fed extensively on them. Erythroxylum sp., on taken by several bird species,but each bird spe- the contrary, was the preferredfruit of three small cies tended to have its own preferred fruit (Table mixed-feeders but overall was taken by four bird 3). Although Tournefortia scandeuswas the most speciesonly. The same pattern was observed for important fruit in the birds’ diet in terms of emetic Trichilia trijoliata. Granivores, suchas Tiaris bi- samplesas well as number of bird species,it was colorand Coryphospinguspileatus,showed a clear DIETS OF LAND BIRDS FROM VENEZUELA 351

TABLE 2. Importance of the different invertebrate taxa in the birds’ diet.

InvertebrateIntake Number of bird species Number of Number of Number of First Second TaX3 items emeticsamples bird species choice’ choice

Gastropoda 51 34 12 Decapoda; crabs 17 12 4 Isopoda 6 6 Scorpionoidea 3 3 : Araneae 410 173 37 1 2 Ixodidae (ticks) 6 6 6 Diplopoda (millipedes) 15 13 6 Chilopoda (centipedes) 3 3 Odonata 12 10 : Orthoptera 45 34 14 Isoptera 221 19 13 1 Psocoptera 3 2 2 187 118 28 Homoptera 257 127 25 1 2 Neuroptera 2 1 Coleoptera 3,21; 1,127 52 22 10 Lepidoptera 78 54 17 1 Diptera 613 150 23 3 2 Hymenoptera; ants 3,150 664 45 10 11 Hymenoptera; winged ants 215 30 11 Hymenoptera; wasps 690 250 35 1 3 Insect eggs 250 44 11 1 1 Insect pupae 15 13 6 Insect larvae 1,064 360 44 3 11

’ Basedon the numberof invertebratestaken by speciesthat fed on at least 10 invertebrateitems.

1

FIGURE 1. Mean number of items per emetic sample for each invertebrate taxa. TABLE 3. Importance of the different fruit speciesin the birds’ diet.

Fruit intake Number of bird species Number of Number of First Second Plant species emetic samples bird species choice’ choice

Acanthaceae Ruella tuberosa 1 1 Boraginaceae Tournefortiascandeus 96 16 Cordia curassaviea 4 3 Bromeliaceae Bromelia pinguin 40 6 Burseraceae Burserakarsteniana 19 6 Cactaceae Subpilocereussp. 8 2 Acanthocereustetragonus 2 Pilosocereusmoritzianus 6: 13 3 1 Opuntia2 3 Melocactuscaesius 52 ; 1 2 Capparidaceae Capparis odoratissima 58 9 2 1 Cucurbitaceae Doyerea emetocatartica 51 6 Erythroxylaceae Erythroxylum cumanense 53 15 Erythroxylum sp. 58 4 Euphorbiaceae Croton rhamnifolius 4 2 Flacourtiaceae Casearia sylvestris 1 1 Leguminosae Pithecellobiumoblongurn 4 3 Malpighiaceae Malpighia glabra 1 1 Malvaceae Gossypiumhirsutum 3 2 Sida acuta 1 Trichilia trlfoliata 46 : 1 1 Nyctaginaceae Guapira microfila 18 8 Rutaceae Zanthoxylon pterota 34 11 Simarubaceae Castela erecta 2 1 Solanaceae Solanum gardneri 4 3 Lycium nodosum 78 18 3 2 Capsicumsp. 2 2 Solanum agrarium 20 10 Theophrastaceae Jacquinia revoluta 25 5 1 Unidentified (seven species’) 70 22 1 ’ ’ Basedon the numberof samplesfrom the bird speciesthat fed on fruits on at leastfive occasions. 2 Opuntia caracasana and Opuntia elatror. DIETS OF LAND BIRDS FROM VENEZUELA 359 preference for Cactaceae (Pilocereus and Melo- predominance of coleopterans, ants, larvae, and cactus) among fleshy fruits. Fruits from Capparis spiders also suggeststhat most bird speciesfor- odoratissima were taken by several speciesfrom aged by gleaning. In arid habitats, only hum- different size and food habits. Fruits from Bro- mingbirds and Myiarchus tyrannulus were oc- melia pinguin were taken by large birds only. All casionally observed hawking or flycatching for other identified fruit speciesaccounted for less their prey. In mangroves, however, several spe- than 20% of fruit intake. cies regularly caught their prey on the wing. Frugivory has been reported for many tropical DISCUSSION species,but most studies relate to birds feeding Few quantitative data exists on the importance at individual fruiting trees. Several of our species of nectar, arthropods, and fruits in the diets of feeding extensively on fleshy fruits such as Mi- nectarivores(Collins et al. 1990). Among the most mus &us, Tachyfonus rujiis, Phaeomyias mu- unexpectedresults was the intake of dry and fleshy rina, and the genera Thraupis and Elaenia are fruits by hummingbirds. Fruits might be even recognizedas mainly fiugivorous (Haverschmidt more important in their diet since these birds 1968, Snow and Snow 197 1, Traylor and Fitz- also extract juice from the pulp of cactus fruits patrick 198 1, Scott and Martin 1984, Belton (Lack 1976, Wendelken and Martin 1988). 1985, Moermond and Denslow 1985). Partial Hummingbirds were also characterizedby a large frugivory has also previously been observed for amount of soft-bodied arthropods in their diet. Amazilia, Melanerpes, Camptostoma, Sublega- Indications of hummingbirds feeding on arthro- tus, Myiopagis, Myiarchus, Pitangus, Myioze- pods are accumulating (Wolf 1970, Young 197 1, tetes, Vireo, Protonotaria, Molothrus, and Icterus Leek 1972, Snow and Snow 1972, DesGranges (Diamond and Terborgh 1967; Haverschmidt 1979, Mobb 1979, Montgomerie and Redsell 1968; Leek 1971, 1972; Cruz 1974; Howe 1977; 1980, Remsen et al. 1986, Baltosser 1989). Our Morton 1977; Traylor and Fitzpatrick 198 1; Scott results agree with those of Remsen et al. (1986) and Martin 1984; Trainer and Will 1984; Belton suggestingthat arthropod intake by humming- 1985; Moermond and Denslow 1985; Foster birds is particularly frequent in arid regions. 1987; Wendelken and Martin 1988). Intake of Most insectivorous species abundant at our fleshy fruits by Formicariidae, an insectivorous study sites fed on a variety of arthropod taxa, tropical family, had previously been noted for suggestingthat dietary specialization of insecti- Thamnophilus doliatus (Haverschmidt 1968, vores is not prevalent in tropical dry habitats. Morton 1973, Keeler-Wolf 1986) as well as Su- The high frequency of Coleoptera, Hymenop- kesphorus and Percnostola (Haverschmidt 1968) tera, insect larvae, and Aranaea in the diets of but this is the first report for Formicivora. Among many speciesmost likely reflectsdiet opportun- Dendrocolaptidae, another typically insectivo- ism. Sampling of arthropods through different rous tropical family, we provide the first report methods (Poulin et al. 1992) showed that Cole- of fruit intake by Lepidocolaptes and Xiphorhyn- optera was the most abundant taxa in both light thus. Neither we could find previous reports of traps and sweep-net samples.Ants were the first- fruit intake by Leucippus (Trochilidae), Hypnelus and third-most abundant taxa in pitfall traps and (Bucconidae), Polioptila (Sylviinae), and Coni- sweep-net,respectively. Spiderswere the second- rostrum (Thraupinae). Because Conirostrum bi- most important taxa in sweep-net and pitfall color was captured in mangroves only, its con- traps. Finally, wasps were the third-most im- sumption of fruit implies occasional movements portant taxa in both light-traps and Malaise traps. to adjacent thorn forest. The Bananaquit (Coere- Only insect larvae did not follow this trend. Al- ba jlaveola), a speciesof diverse feeding habits though being the second-most important inver- (Skutch 1954, Gross 1958, Snow andSnow 1971, tebrate prey in the birds’ diet, they accounted for Leek 1971, Cruz 1974, Feinsinger et al. 1985) lessthan 5% of all arthropods sampled by sweep- fed more frequently on fleshy fruits at our study net. Actually, insect larvae were abundant only sites than in previous reports. The same holds during a two-month period that correspondedto for Hylophilus jlavipes that fed extensively on the birds’ breeding season. Consequently, most fleshy fruits and for which few reports of frugiv- birds fed opportunistically on Coleoptera and ory exist (Morton 1973). Our results also dem- Formicidae year-round, but showeda clear pref- onstrate that several members of the Tyrannidae erence for larvae during breeding activity. The known as primarily insectivorous such as Atalo- 360 B. POULIN, G. LEFEBVRE AND R. MCNEIL

triccus, Idioptilon, Euscarthmus, Tolmomyias, BELTON,W. 1985. Birds of Rio Grande do Sul Brazil. Cnemotriccus and Contopus regularly fed on Part 2. Formicariidae throughCorvidae. Bull. Am. Mus. Nat. Hist. 180:1-241. fruits. Our study sites were located in a semiarid COLLINS,B. G., J. GREY,AND S. MCNEE. 1990. For- region with considerable variation in rainfall and aging and nectar use in nectarivorous bird com- food abundance over the year (Lefebvre 1992, munities. Stud. Avian Biol. 13:11 O-l 2 1. Poulin et al. 1992) and the intake of vegetable CRUZ, A. 1974. Feeding assemblagesof Jamaican matter by many speciesoccurred predominantly birds. Condor 76:103-107. D~OND, J. M., AND J. W. TERBORGH.1967. Ob- during the dry season when arthropod abun- servationson bird distribution and feedingassem- dance was lowest. In seasonalarid habitat on the blages along the rio Callaria, Department of Lo- Yucatan Peninsula, Lopez Omat and Lynch reto. Peru. Wilson Bull. 79:273-282. (1990) also noted that most birds were generalist DESGRA&+ES,J.-L. 1979. Organization of a tropical nectar-feeding bird guild in a variable environ- feedersdepending extensively on vegetable food. ment. Living Bird 17:199-236. Although some plants were clearly more im- FEINSINGER,P., L. A. SWARM,AND J. A. WOLFE. 1985. portant in the overall bird diet, fruit preferences Nectar-feeding birds on Trinidad and Tobago: varied among the different bird species. Fruit comparison of diverse and depauperate guilds. choice was probably a combination of several Ecol. Monogr. 55:1-28. FOSTER,M. S. 1987. Feedingmethods and efficiencies factors, including the bird and fruit morphology, of selectedfrugivorous birds. Condor 89:566-580. as well as their respective seasonality. For in- GREENBERG,R. 1981. The abundanceand seasonality stance, fruit production of Lycium nodosum, a of forest canopy birds on Barre Colorado Island, speciestaken by 18 bird species,occurred in the Panama. Biotropica 13:24l-25 1. GROSS,A. 0. 1958. Life history of the Bananaquit early dry seasonwhen arthropod abundance was of Tobago island. Wilson Bull. 70:257-279. low and few plant specieswere fruiting. HAVERSCHMIDT.F. 1968. Birds of Surinam. Oliver & In seasonalhabitats of northeastern Venezue- Boyd, London. la, most species fed on a wide variety of re- HOWE,H. F. 1977. Bird activity and seed dispersal sources,including both vegetal and foods of a tropical wet forest tree. Ecology 58:539-550. HOYOS.F. J. 1985. Flora de la Isla de Mama&a. in their diet. While the most fi-ugivorous species Monografia no. 34, Sociedady Fundaci6n La Salle included arthropods in their diets, several typi- de Ciencias Naturales, Caracas.

cally insectivorous speciesfed at least occasion- KARR. J. R. 1976. Seasonalitv.II resource availabilitv. __ ally on fruits. Indeed, food exploitation by many and community diversity in tropical bird com- specieswas quite variable over time (Poulin et munities. Am. Nat. 110:973-994. KARR,J. R., AND J. D. BRAWN. 1990. Food resources al. 1992) as well as between habitats (Poulin et of understory birds in central Panama: quantifi- al., in press). We believe that many land birds cation and effectson avian populations.Stud. Avi- show more feeding plasticity than is generally an Biol. 13:58-64. assumed, increasing the need for local dietary KEELER-WOLF, T. 1986. The Barred Antshrike (Thamnophilusdoliatus) on Trinidad and Tobago: studies. habitat niche expansion of a generalist forager. Oecologia 70:309-3 17. ACKNOWLEDGMENTS LACK,D. 1976. Island biology, illustrated by the land This study was supportedby the Natural Sciencesand birds of Jamaica.Univ. of California Press.Berke- Engineering Research Council of Canada. Fonds ley. F.C.A.R. (Gouvemement du Quebec),and the’univer- LECK,C. F. 1971. Overlap in the diet of some neo- site de Montreal. We are also grateful to colleaguesof tropical birds. Living Bird 10:89-106. the Universidad de Oriente, in particular Luis Jose LECK, C. F. 1972. Observations of birds at Cecropia Cumana for his invaluable assistancein identifying trees in Puerto Rico. Wilson Bull. 84:498-500. plant specimens and Jose Ramon Rodriguez S. who LEFEBVRE,G. 1992. Dynamique temporelle et spa- was responsiblewith Raymond McNeil for the collab- tiale de l’avifaune migratrice et residentedes man- orative agreement between both universities. groves cotieres du Venezuela. These de Doctoral (Ph.D.), Universite de Montreal, Montreal. LITERATURE CITED LOISELLE,B. A. 1988. Bird abundanceand seasonality in a Costa Rican lowland forest canopy. Condor AOU. 1983. Check-list ofNorth American birds. 6th 90~761-772. ed. American Ornithologists’ Union, Washington, __ LQISELLE,B. A., AND J. G. BLAKE. 1990. Diets of understory fruit-eating birds in Costa Rica: sea- BALT~&R, W. H. 1989. Nectar availability and hab- sonalityand resourceabundance. Stud. Avian Biol. itat selection by hummingbirds in Guadalune 13:91-103. Canyon. Wilson-Bull. 101:5‘59-578. LOPEZORNAT, A., AND J. F. LYNCH. 1990. Landbird BELL,H. L. 1982. A bird community of lowland for- communities of the coastaldune scrub in the Yu- est in New Guinea. 2. Seasonality.Emu 82:65-74. catanPeninsula: species composition, ecology, and DIETS OF LAND BIRDS FROM VENEZUELA 361

zoogeographicaffinities. Vida Silvestre Neotropi- tropical and subtropical South America. J. Ecol. cal 2:21-31. 60:367-410. MOBB,S. 1979. Methods used by Trochilidae (hum- SARMIENTO,G. 1976. Evolution of arid vegetationin mingbirds)when capturinginsects. Aviculture Mag. tropicalAmerica, p. 65-99. In D. W. Goodall [ed.], 85:26-30. Evolution of desert biota. Univ. of Texas Press, MOERMOND, T. C., AND J. S. DENSLOW. 1985. Neo- Austin, TX. tropical frugivores: patterns of behavior, mor- Scorr., P. E.., AND R. F. MARTIN. 1984. Avian con- phology and nutrition, with consequencesfor fruit sumption of Bursera, Ficus, and Ehretia fruit in selection, p. 865-897. In P. A. Buckley, M. S. Yucatan. Biotropica 16:319-323. Foster, E. S. Morton, R. S. Ridgely, and N. G. SKUTCH.A. F. 1954. Life histories of Central Amer- Smith teds.], Neotropical ornithology. Omithol. ican birds. Pacific CoastAvifauna, No. 3 1. Cooper Monogr. No. 36. American Ornithologists’ Union, Ornithological Society, Berkeley, CA. Washington, DC. SMITH,T. J., III. 1987. Seed predation in relation to MONTGOMERIE,R. D., AND C. A. REDSELL.1980. A tree dominance and distribution in mangrove for- nesting hummingbird feeding solely on arthro- ests. Ecology 68:266-273. pods. Condor 82:463-464. _ SNOW.B. K.. AND D. W. SNOW. 1971. The feedina MORTON,E. S. 1973. On the evolutionary advantages ecology of tanagersand honeycreepersin Trini- and disadvantagesof fruit eating in tropical birds. dad. Auk 88:291-322. Am. Nat. 107:8-21. SNOW,B. K., ANDD. W. SNOW. 1972. Feeding niches MORTON.E. S. 1977. Intratrooical miaration in the of hummingbirds in a Trinidad valley. J. Anim. Yellow-green Vireo and Piratic Flycatcher. Auk Ecol. 41:471-485. 94:97-106. SNOW,D. W., AND B. K. SNOW. 1964. Breeding sea- ORIANS,G. H. 1969. The number of bird speciesin sons and annual cycles of Trinidad land-birds. some neotropical forest. Ecology 50:783-796. Zoologica (New York) 49: l-39. PHELPS,W. H., AA R. MEYERDE S;HAUENSEE.1979. TRAINER,J. M., ANDT. C. WILL. 1984. Avian meth- Una guia de lasaves de Venezuela.Princeton Univ. ods of feeding on Burserasimaruba (Burseraceae) Press, Princeton, NJ. fruits in Panama. Auk 101:193-195. POULIN, B., G. LEFEBVRE, AND R. MCNEIL. 1992. TIUYLOR, M. A., JR., AND J. W. FITZPATRICK. 1981. Tropical avian phenologyin relation to abundance A survey of the tyrant flycatchers.Living Bird 19: and exploitation of food resources.Ecology 73: 7-50. 2295-2309. TRUJILLO, B., AND M. PONCE. 1988. Lista inventario POULIN,B., G. LEFEBVRE,AND R. MCNEIL. In press. de Cactaceae silvestres en Venezuela con sinoni- Characteristics of feeding guilds and variation in mia y otros aspectos relacionados. Emstia 47:1- diets ofbird species ofth&eadjacent tropical sites. 20. Biotrooica. WENDELKEN. P. W., AND R. F. MARTIN. 1988. Avian POULIN, BI:G. LEFEBVRE,AND R. MCNEIL. 1994. Ef- consumption of the fruit of the cacti Stenocereus fect and efficiency of tartar emetic in determining eichlamii and Pilocereusmaxonii in Guatemala. the diet of tropical land birds. Condor 96:98-104. Am. Midl. Nat. 119:235-243. REMSEN, J. V., F. G. STILES, AND P. E. SCOTT. 1986. WOLF, L. L. 1970. The impact of seasonal flowering Frequency of arthropods in stomachs of tropical on the biology of some tropical hummingbirds. hummingbirds. Auk 103:436-444. Condor 72:1-14. ROSENBERG,K. V., AND R. J. COOPER. 1990. Ap- WONG, M. 1986. Trophic organization of understory proachesto avian diet analysis.Stud. Avian Biol. bird in a Malaysian dipterocarp forest. Auk 103: 13:80-90. 100-l 16. SARMIENTO, G. 1972. Ecological and floristic con- YOUNG,A. M. 1971. Foragingfor insectsby a tropical vergence between seasonal plant formation of hummingbird. Condor 73~36-45. 362 B. POULIN, G. LEFEBVRE AND R. MCNEIL

APPENDIX 1. Number of items taken from each invertebrate categoryby each bird species.

Number of invertebrate items (size in mm) Gas- Deca- sc.x- chilo- Gdo- or- or- PSO- tro- poda; Iso- pion- Am- Am- Ixodi-Diplo- poda nata thop tbop I,“,” c4g poda crabs jada oidea neae neae dae poda (IO- (IO- tern tera Bird species’ (O-10) (O-10) (5-10) (5-30) (O-5) (5-15) (O-5) (>20) 25) 25) (O-5) (5-25) (5-15) (O-5)

Coccyzus melacoryphus Glaucis hirsuta 1 1 Chrysolampis mosquitus : 1 Chlorostilbon mellisugus 25 1 Thalurania furcata Leucippus fallax 110 5 1 Amazilia chionopectus 5 2 Amazilia fimbriata Amazilia tobaci 74 4 2 Hypnelus ruficollis 2 1 1 Galbula ruficauda Melanerpes rubricapillus Synallaxis albescens Certhiaxis cinnamomea 1 27 1 4 1 Xiphorhynchus picus 1 1 Lepidocolaptes souleyetii 1 1 1 2 1 3 118 Campylorhamphus trochilirostris Thamnophilus doliatus 1 1 1 Formicivora grisea 2 1 2 2 : 71 Myrmeciza longipes Camptostoma obsoletum Phaeomyias murina 1 1 3 Sublegatus modestus 3 1 Myiopagis viridicata 2 Elaenia parvirostris Euscarthmus meloryphus Mionectes oleagineus 1 Atalotriccus pilaris 1 Idioptilon margaritaceiventris Tolmomyiasflaviventris 4 Cnemotriccus fuscatus 1 2 Myiophobus fasciatus Fluvicola pica 3 1 Myiarchus tyrannulus 2 1 1 Myiarchus venezuelensis Pitangus sulphuratus 1 Myiozetetes similis Steldigopterix ruficollis Troglodytes aedon 1 Polioptila plumbea :. 1 Turdus leucomelas 1 Turdus nudigensis Mimus gilvus 1 8 1 Vireo gilvus Vireo olivaceus 1 1 1 5 Hylophilusflavipes 1 1 2 Cyclarhis gujanensis Parula pitiayumi Dendroica petechia Dendroica striata Setophaga ruticilla 2 1 3 Protonotaria citrea 8 1 Seriurus noveboracensis 35 14 29 2 10 6 3 Coereba flaveola 13 1 2 Conirostrum bicolor 2 3 26 1 7 DIETS OF LAND BIRDS FROM VENEZUELA 363

APPENDIX 1. Extended.

Number of invertebrateitems (sizein mm) Hyme- He- Ho- Neu- Cole- Lepi- Ilop- HWe- He- mip- Ho- mop- rap- Cole- op- Lepi- dop- Hyme- Hyme- tera; Hyme- nop- mip- tern mop- tera ten OP- tera dop- tera Dip- Dip- nopterq*optera; winged noptera;km; Insect Insect Insect Insect tera (5- tera (5- (l& tera (5- tera (S- tera tera ants ants ants wasps wasps egg pupae larvae larvae (O-5) 25) (O-5) 30) 15) (O-5) 20) (O-5) 20) (O-5) (5-25) (O-5) (5-20) (O-10) (O-5) (5-15) (O-5) (O-10) (O-5) (5-30)

1 1 1 1 1 2 34 2 19 2 1 11 1 2 12 106 1 1 330 3 I 2 236 2 5 1 2 1 12 22 1 5 2 161 4 2 183 3 6 1 4 1 1 9 5 2 1 I 1 9 1 158 20 3 1 2 18 2 10 2 4 5 2 41 20 2 34 40 3 15 1 2 1 30 19 16 28 19 7 6 1 3 2 3 2 1 1 3: 17 1 18 49 4 1 7 19 18 5 279 16 2 4 3 2 179 85 94 2 8 1 4 32 1 5 4 3 7 20 10 7 1 236 7 1 2 1 62 14 2 15 12 1 8 42 4 4 1 185 48 1 944 358 52 5 12 12 1 6 5 4 10 : 1 21 2 8 10 3 2 1 3 1 25 11 13 399 10 4 4 59 36 5 14 21 23 6 3 23 1 23 2 1 3 1 3 5 2 16 6 1 44 12 1 1 1 70 14 15 37 5 6 1 4 2 1 1 1 1 45 18 3 4 5 2 32 1 2 13 2 3 9 7 1 3 11 1 13 1 1 4 2 2

1 10 8 1 4 2 1 4 4 3 4 5 1 221 3 44 21 32 24 4 11 3 3 19 4 5 1 1 3 6 13 31 31 68 7 1 8 1 14 1 4 1 2 53 6 1 1 5 5 14 1 44 7 3 5 1 114 4 22 12 1 3 2; 22 2 13 57 1 3 8 1 2 5 1 4 1 2 2 2 17 20 1 2 5 1 1 1 1 7 42 11 2 2 3 27 2 24 2 285 6 3 10 9: 8 3 120 9; 16 2 6 11 242 2 7 102 9 8 8 2 (98 162 4 11 2 262 3 9 10 49 3 7 42 24 51 364 B. POULIN, G. LEFEBVRE AND R. MCNEIL

APPENDIX 1. Continued.

Number of invertebrate items (size in mm) Gas- Deca- Scor- Chile- Odo- Or- Or- PSO- tro- poda, ISO- pion- Am- Am- Ixodi- Diplo- poda nata thop- thop- Isop- cop- pada crabs poda oidea neae neae dae poda (lb (lC- tera tera tera tera Bird species’ (C-10) (O-10) (5-10) (5-30) (O-5) (5-15) (O-5) (>20) 25) 25) (O-5) (5-25) (5-15) (C-5)

Thraupis glaucocolpa Tachyfonusrufis 3 Coryphospinguspileatus : 4 Saltator albicollis Cardinalis phoeniceus 1 Volatina jacarina Tiaris bicolor 2 1 10 Molothrus bonariensis 5 Icterus nigrogularis 1 1 2

’ ’ Nomenclature following AOU (1983) and Phelps and Meyer de Schauensee (1979). DIETS OF LAND BIRDS FROM VENEZUELA 365

APPENDIX 1. Extended. Continued.

Number of invertebrateitems (sizein mm) HylW- He- Ho- Neu- Cole- Lepi- IlClp- HyllE- He- mip- Ho- mop- rep- Cole- op. Lepi- dop- Hyme- Hyme- tera; Hyme- nop- mip- tera mop- tern tera OP- tern dop- ten Dip_ Dip- nopteq nopteq wingednopte~~ tera; Insect Insect Insect Insect tera (5- tera wasps wasps eggs pupae larvae larvae (c-5) 25) (c-5) Y-0) (:g :E) i5-0) (‘F-Y) (250s $-?) (Z) (E) (E%) (I?& (o-5) (5-15) (c-5) (O-10) (S5) (5-30)

1 3 1 1 8 I 55 193 4 6 4 71 13 32 15 5 1 5 16 2 1 17 9 26 34 1 1 2 4 1 1 15 11 1 2 5 1 2 5 4 29 4 1 5 2 6 3 2 7 366 B. POULIN, G. LEFEBVRE AND R. MCNEIL

APPENDIX 2. Number of emetic samples containing each identified plant’ and percentageof samples with fleshy fruits, seeds,and pollen for each bird species.

Number of emetic samples ACan- Bur- Cap- &S- Doy- EV tho- Bra- sera paris twin Croton erea tkrox- Ery- Gqssy- cereus melia kars- odor- Cap- Syl- Cm- Cordia rkam- emeto- ykm throx- p;;ry retra- pin- ten- atis- sicum w-s- tela curas- nifo- afar- cum- ylum Bird species gonu.7 guin iana sima SP. tris e-recta savica liw tica nenx SP. SUtum Glaucishirsuta Chlorostilbonmellisugus Thalurania furcata Leucippusfallax 1 Amazilia jimbriata Amazilia tobaci Hypnelus rujicollis 1 Melanerpesrubricapillus 1 Xiphorhynchuspicus Lepidocolaptessouleyetii 1 Thamnophilusdoliatus Formicivora grisea Camptostomaobsoletum Phaeomyiasmurina 2 9 1 2 20 40 2 Sublegatusmodestus 1 1 1 : Myiopagis viridicata 1 Elaenia parvirostris 1 2 2 Elaenia strepera Euscarthmusmeloryphus Atalotriccuspilaris Idioptilon margaritaceiventris 1 Tolmomyiasflaviventris Cnemotriccusfuscatus 1 Contopuscinereus Myiarchus tyrannulus 1 4 I 3 3 Pitangussulphuratus 1 Myiozetetessimilis Chiroxiphia lanceolata Polioptila plumbea Mimus gilvus 3 10 15 2 11 12 1 Vireo olivaceus 2 4 2 Hylophilusflavipes 8 15 14 4 16 Protonotaria citrea Coerebaflaveola 1 1 Conirostrumbicolor Thraupis glaucocolpa 2 8 4 Tachyfonusr-u&s 21 16 Coryphospinguspileatus Saltator albicollis 1 Cardinalis phoeniceus 5 5 3 1 1 Volatina jacarina Sporophila lineola Tiaris bicolor 1 Molothrus bonariensis Icterus nigrogularis 1 ’ Nomenclaturefollowing Hoyos (1985) exceptfor cactaceaeas per Trujillo and Ponce(1980) 2 Opuntia caracasana and Opuntia elatior. ’ ’ Referseither to dry fruits or to fleshyfruits whoseseeds were pounded in samples. DIETS OF LAND BIRDS FROM VENEZUELA 367

APPENDIX 2. Extended.

Number of emetic samoles

0 0 100 0 0 50 0 0 50 1 2 55 0 i 100 0 4 33 13 0 0 I 1 1 1 61 0 0 4 i 6 0 0 11 0 1 1 2 1 : 1 0 0 0 I 7 1 3 29 81 1 0 1 9 1 9 : 19 3 1 i 1 6 1 1 ;3’ : 0 100 0 3 60 0 i 2 2 6 1 10 1 17 % 8 8 8 0 1 1 12 1 100 i : 1 1 2 2 3 51 3 0 50 50 100 0 i 1 100 0 2 3 4 i 2 9 24 1 5 7 1 1 7 4 91 1 0 2 2 27 2 0 3 2 1 3 1 10 5 83 3 i i 2 1 24 I 19 12 64 1 i 0 12 1 1 2 100 0 0 2 1 7 1 4 1 9 80 6 0 2 4 2 1 5 59 0 1 100 0 0 1 13 10 1 3 1 2 48 84 0 50 : 0 100 0 22 16 1 2 8 95 0 15 50 0 1 1 22 0 0