DIET COMPOSITION OF ASSOCIATED TO AN URBAN FOREST PATCH IN NORTHERN VENEZUELA Cristina Sainz-Borgo

SUMMARY

Studies about diet composition are of importance to under- Ants were consumed mainly in the dry season, and Coleoptera, stand the biology and ecological strategies of birds. The pres- Clusia, and Diptera during the wet season. Atalotriccus pilaris ent study aims to quantitatively describe the diet of 33 was the most common captured bird, with high prevalence of (4 orders and 16 families) that inhabit a semi-decid- in its feces and occasional fruit consumption. Formiciv- uous urban forest patch in Caracas, Venezuela, and its vari- ora grisea, Thamnophilus doliatus and Campyloramphus tro- ations between dry and rain seasons. One hundred and thir- chilirostris, among others, were found to be strictly insectivo- ty seven fecal samples were collected from September 2013 to rous; while Columbina talpacoti, Leptotila verreauxi and Tiaris July 2014 using mist nets. The most abundant families in fecal bicolor were predominantly granivorous. Thraupis episcopus, T. samples were Tyrannidae (45 samples), Thraupidae (18), Tham- glaucocolpa, Coereba flaveola, Cychlaris gujanensis, Euphonia nophillidae (12), Turdidae (12) and Galbulidae (10). The 63.5% trinitatis and Saltator coerulescens had the highest fruit content of fecal samples contained only insects, 14.5% fruit and seeds, in their diet. The study is the first work generating information 12.4% fruits and insects, and 9.5% seeds and insects. The most about the diet of birds living in urban habitats in Venezuela. abundant food items were insects from the Formicidae Further research is necessary to understand the processes of and the Coleoptera , and fruits from the Clusia . adaptation of birds to urban habitats in the neotropics.

Introduction have demonstrated the conve- and Zuria, 2011; Reis et al., people and has a great di- nience of feces’ studies to 2012) and many showed that versity of birds: about 300 Diet studies are necessary determine feeding guilds in cities retain a considerable species have been recorded for the understanding of the birds (Rouges and Blake, diversity of bird species that find refuge in many biological and ecological strat- 2001; Piratelli and Pereira, (Clergeau et al., 1998; parks and other green areas egies of birds. In Venezuela, 2002; Carvallo Lima, 2008; Marzluff et al., 2001). of city (Aveledo, 1968; few studies about the diet of Navas, 2009). The disadvan- However, few explore how Goodwin 1987; Fundación birds have been carried out, tage of this technique is that urban habitats can affect the La Salle, 1997; Caula and restricted to dry forests and certain food items may be diet of birds. The majority of Levin, 1999; Levin et al., arid zones (Poulin et al., misrepresented due to differ- studies are restricted to a sin- 2000; FJBC-SCAV, 2006; 1994, Quilarque et al., 2010, ences in digestibility (Voiter gle species, mainly Falco- SCAV, 2007; Sainz-Borgo Pérez et al., 2001). In the neo- et al., 2003). Carlisle and niformes and owls (Yalden, and Levin, 2012; Sainz- tropics, however, there are Holberton (2006) found that 1980; Tatner, 1983; Gavett and Borgo, 2012, 2014, 2015). abundant studies, mostly by increasing the number of Wakeley, 1986; Roth and The aim of this work was based on stomach contents fecal samples between five Lima, 2003; Delgado and to study the diet composition using emetics (Loiselle and and 17, the results obtained Calderón, 2007; Hernández- of a bird community associat- Blake, 1990; Pérez et al., are similar to the number of Muñoz and Mancina, 2011). ed with an urban patch of 2001; Duraes and Marini, taxa detected in regurgitated Several studies have reported semi-deciduous forest, using 2005; Gaiotti and Pinho, samples. that certain bird species tend quantitative analysis of their 2013) and on stomach con- Studies on urban birds are to consume anthropogenic fecal contents. tents of collected birds becoming more relevant due to food (Ottoni et al., 2009) such (Remsen et al., 1993; the growth of urban areas and as bread and food scraps Methods Rosenberg, 1993; Lópes et al., the concomitant increase in (Rollinson et al., 2003). 2005). The use of emetics has anthropic effects on bird biol- In Venezuela, there is Study area the disadvantage that they ogy. In the neotropics, several scarce information about ur- may cause accidental death of studies have focused on ban birds (Caula et al. 2003; The study involved two the studied specimens, while urban bird communities 2010; Seijas et al., 2011; Sanz field visits per month, from fecal analysis is a non-inva- (Stiles, 1990; Rivera-Gutiérrez, and Caula, 2014), and none September 2013 to July 2014, sive method that does not en- 2006; Villegas and Garitano- about their diets. Caracas is a to a 2ha patch of semi-decid- danger birds. Several studies Zavala, 2010; Carbó-Ramírez city with over five million uous, seasonal, premontane

KEYWORDS / Birds / Feces / Feeding Guilds / Seasonal Variation / Received: 05/30/2015. Modified: 01/22//2016. Accepted: 01/25/2016.

Cristina Sainz-Borgo. Biologist, Sciences, Universidad Simón Venezuela. Address: Departa- Bolívar, Apartado 89000, Universidad Central de Bolívar, Venezuela. Professor, mento de Biología de Orga- Caracas 1080A, Venezuela e- Venezuela. Ph.D. in Biological Universidad Simón Bolívar, nismos, Universidad Simón mail: [email protected]

FEBRUARY 2016, VOL. 41 Nº 2 0378-1844/14/07/468-08 $ 3.00/0 119 COMPOSICIÓN DE LA DIETA DE LAS AVES ASOCIADAS A UN PARCHE DE BOSQUE URBANO EN EL NORTE DE VENEZUELA Cristina Sainz-Borgo RESUMEN

El estudio de la composición de la dieta de las aves per- sia y Diptera mayoritariamente durante la estación lluviosa. mite comprender sus estrategias biológicas y ecológicas. Atalotriccus pilaris fue el ave con mayor cantidad de captu- El objetivo del presente estudio consistió en realizar una ras, encontrándose que consumía mayoritariamente insectos y descripción cuantitativa de la dieta de 33 especies de aves ocasionalmente frutas. Las especies insectívoras estrictas fue- (pertenecientes a 4 órdenes y 16 familias) que habitan en un ron Formicivora grisea, Thamnophilus doliatus y Campylor- parche de bosque semideciduo urbano en la ciudad de Cara- hamphus trochilirostris, entre otras; mientras que Thraupis cas, Venezuela; y de su variación entre las estaciones de se- episcopus, T. glaucocolpa, Coereba flaveola, Cychlaris guja- quía y lluvia. Fueron colectadas 137 muestras de heces desde nensis, Euphonia trinitatis y Saltator coerulescens tuvieron septiembre 2013 a julio 2014. Las familias más abundantes los contenidos más altos de frutas en su dieta. El presente fueron Tyrannidae (45 muestras), Thraupidae (18), Thamno- estudio es el primer trabajo en generar información sobre la phillidae (12), Turdidae (12) and Galbulidae (10). Los ítems dieta de aves que viven en ambientes urbanos en Venezuela. alimentarios más abundantes fueron hormigas y escarabajos, Una mayor cantidad de estudios sobre esta línea de investi- y frutas del genero Clusia. Las hormigas fueron consumidas gación son necesarios para entender los procesos de adapta- principalmente durante la estación seca, y Coleoptera, Clu- ción de las aves en ambientes urbanos del neotropico.

COMPOSIÇÃO DA DIETA DAS AVES ASSOCIADA A UMA TRECHO DE FLORESTA URBANA NO NORTE DA VENEZUELA Cristina Sainz-Borgo RESUMO

Estudos da dieta são de importância para a compreensão Clusia na maior parte durante a estação chuvosa. As espécies da biologia e ecologia de aves. Este estudo é uma descrição com o maior número de sacas era Atalotriccus pilaris, sendo quantitativa da dieta de 33 espécies de pássaros (pertencen- consumido principalmente insetos e ocasionalmente frutas. Es- tes a quatro ordens e 16 famílias) que vivem em um trecho pécies insectívoras rigorosos foram Formicivora grisea, Tham- de floresta semi-decídua urbana na cidade de Caracas, Vene- nophilus doliatus e Campylorhamphus trochilirostris. Thraupis zuela e sua variação ao longo do ano. Foram coletadas 137 episcopus, T. glaucocolpa, C. flaveola, Cychlaris gujanensis, amostras fecais de setembro 2013 a julho de 2014. As famílias Euphonia trinitatis e Saltator coerulescens teve o mais alto mais abundantes foram Tyrannidae (45 amostras), Thraupidae conteúdo frutas em sua dieta. O presente estudo é o primeiro (18), Thamnophillidae (12), Turdidae (12) and Galbulidae (10). trabalho na geração de informações sobre a dieta de aves que Os itens alimentares mais abundantes foram formigas e besou- vivem em habitats urbanos na Venezuela. Mais deste tipo de ros, e frutas do gênero Clusia. As formigas foram consumidos pesquisa são necessários para entender os processos de adap- principalmente durante a estação seca, e Coleoptera, Diptera e tação das aves nos habitats urbanos na região neotropical.

forest located at the Expe- grasses and shrubs, mixed Data collection glass tube containing 4ml of rimental Station Arboretum with abundant trees. Tree 70% ethanol. The items in the (Instituto de Biología Ex- species are predominantly Eight mist nets (12×2.8, diet were identified to order perimental, Universidad deciduous, while in the shrub 36mm mesh) were used along or family using a stereo-mi- Central de Venezuela, Cara- layer there are abundant the main path of the study croscope (Wild Heerbrugg- cas, Venezuela, 1100m, vines, thorny shrubs and ever- area, placed twice a month MSA), in the Ornithology 10°30’36”N - 66°53’ 92”W), green species (Hokche and from September 2013 to July Laboratory, Universidad located within a residential Ramírez, 2006). More than 2014. The mist nets were Simón Bolívar, Caracas, zone. The study covered the 300 plant species of 77 fami- opened from 6:30 to 15:30 and Venezuela,. The plant samples end of 2013 wet season lies have been reported, checked every 15min. All cap- were identified using the Lau (September-October), the fol- the most abundant families tured birds were classified ac- (2010) data base. lowing dry season (December being Asteraceae, Fabaceae, cording to the South America The relative occurrence 2013-April 2014) and the be- Poaceae, Euphorbiacea, Mi- Classification Committee (Ro) of each category was ginning of the 2014 wet sea- mosaceae, Malvaceae and (SACC) (Remsen et al., 2016). calculated as number of son (May-July), with precipi- Rubiacea (López and Ra- For feces collection, indi- samples in which the catego- tation ranging from 500 to mírez, 2004), and xerophilous vidual birds were placed ry occurred divided by the 1000mm per year and an tem- species of the Cactaceae and during 20min in a plastic total number of samples; perature between 19 and Agavaceae families (Ewell container (20×30cm) with a while the relative abundance 27°C. The vegetation is sec- et al., 1976). The study area mesh at the bottom and (Ra) of each category was ondary, consisting of two lay- is surrounded by residential topped with black fabric to calculated as a number of ers: an upper stratum where buildings and vehicular reduce stress. After that peri- diet items of each category trees 8-18m high predominate, transit took place during od, the bird was released and divided by the total numbers while the bottom contains collection. feces were collected in a 8ml of diet items in the sample,

120 FEBRUARY 2016, VOL. 41 Nº 2 averaged for all samples pilaris) consumed a higher eleven different families of (Melastomataceae), Palicourea (Martini and Duraes, 2005). diversity of diet items in the insects, as well as Clusia and (Rubiaceae), and Lauraceae Permanova analyses were wet season than in the dry Loranthaceae seeds (Table I). were also commonly found in conducted with the program one, whereas three species Strict insectivores were F. fecal samples. Non-identified Primer v5 (Clarke and Gorley, (Ramphocaenus melanurus, grisea, R. melanurus, small flowers were found in 2006) using the fecal sam- Thryophilus rufalbus and Thamnophilus doliatus, T. ru- samples of C. flaveola, C. fus- plings data by bird family, in Saltator coerulescens) con- falbus, Grallaricula ferru- catus and T. glaucocolpa. The order to determine if seasonal- sumed more items in the dry gineipectus, P. squamulatus, samples of E. trinitatis con- ity had some effect on diet. season (Figure 3, Table I). Synallaxis albescens, Campy- tained abundant Loranthaceae The food items were used as The Permanova analysis in- loramphus trochilirostris, seeds, which were also con- variables and seasons and bird dicated that there was an inter- Cranioleuca subcristata, and sumed by E. flavogaster, C. species were considered fac- action between the factors Rhodinocihla rosea. obsoletum, C. fuscatus, H. fla- tors. To check for differences (species × season, P=0.013) in Samples from C. subcristata vipes, and A. pilaris. in diet between dry and wet Tyrannidae, showing that there contained only insects, except In the feces of C. talpacoti, seasons a Chi-square (c2) test are differences in the diet of in one sample where seed frag- Tiaris bicolor and Cyanocompsa was used. species between seasons. In ments were found during the cyanoides seed fragments and the rest of birds evaluated, wet season. In a similar case, arthopods in smaller proportions Results no interactions were detected one sample of P. squamulatus were found. In the samples (Permanova, Thraupidae: contained a Loranthacea seed. from Leptotila verreauxi only From a total of 227 cap- P=0.052, Formicariidae: In one sample from F. grisea seed fragments were found. tures, 60% provided useful P=0.517). Significant differenc- two individuals of the family fecal samples, belonging to 33 es in birds abundance were Phoridae (Diptera) were found. Discussion species, 4 orders and 16 fami- found between seasons for fru- Several items were registered lies (Table I). Bird families givorous-insectivorous (N wet only once: Araneae, The bird community in the having the largest numbers of season=34, N dry season=14, Curculionidae and Blatodea, study area was dominated by fecal samples were Tyrannidae c2 P=0.0035) and for insectiv- consumed by A. pilaris; insectivores, similar to what (45 samples), Thraupidae (18), orous (N wet season=21, N Lampyridae by T. aedon; has been observed in other Thamnophillidae (12), dry season=25, c2 P=0.028). Diplopodae, Homoptera, and neotropical forests (Terborgh Turdidae (12) and Galbulidae The frugivorous and granivo- stones by F. grisea; and an ant et al., 1990; Poulin et al., (10). The more abundant spe- rous-insectivorous did not nymph by T. doliatus (Table I). 1994; Duraes and Marini, cies were Atalotriccus pilaris show differences in abundance T. nudigenis, C. flaveola, 2005). During the wet season (N=28), Coereba flaveola (22), in dry and wet seasons Cychlaris gujanensis, Euphonia several species, especially in- Galbula ruficauda (16), (c2 P=0.135 and P=0.739 trinitatis and Hylophilus flavi- sectivorous, consume a greater Formicivora grisea (14), respectively). pes consumed mostly fruits, variety of food items, a fact Turdus nudigenis (14) and and in lesser proportions in- that has been reported for dif- Camptostoma obsoletum (13). Feeding guilds sects. A. pilaris, C. obsoletum ferent birds assemblages We have identified 32 different and Pitangus sulphuratus were (Leck, 1972; Blake and food items (Tables I, II, In insectivorous birds, the considered mainly insectivorous Loiselle, 1991; van Schaik Figure 1). Of the fecal sam- most abundant food items with occasional fruits con- et al., 1993; Poulin et al., ples, 63.5% contained only were Coleoptera (found in 85 sumed. Strict frugivorous were 1994; Williams and Middleton, insects, 14.5% fruit and seeds, samples), Formicidae (35) and Thraupis episcopus, T. glauco- 2007). Also, a marked season- 12.4% fruits and insects, and Diptera (30) (Tables II). The colpa, S. coerulescens and E. ality was found in several food 9.5% mostly seeds. most common bird species flavogaster. items. For example, ant con- Captures in the wet season was A. pilaris, which con- Clusia (Clusiaceae) was the sumption is greater in the dry were 120 (53%) and in dry sumed the major variety of most frequently fruit consumed, season, while Coleoptera, season 107 (47%). Richness food items consisting of but seeds of Clydemia Diptera and Clusia seeds are was greater during the rainy season than the dry season (28 vs 21 bird species respec- tively). The number of fecal samples collected in the two seasons differed: in the wet season 87 feces samples were collected, whereas only 45 samples were obtained in dry season. Food items with the highest values of Ro and Ra were Coleoptera, Formicidae, fruit pulp, Diptera, and seed fragments (Table II). Ants were consumed mainly in the dry season, and Coleoptera, Clusia, and Diptera during wet season (Figure 2). Four species (Columbina talpacoti, Figure 1. Number of food items contained in the fecal samples from the birds in an urban premontane forest G. ruficauda, F. grisea and A. patch in Caracas, Venezuela. (NI: non identified).

FEBRUARY 2016, VOL. 41 Nº 2 121 TABLE I BIRDS DIET OF URBAN FOREST PATCH LOCATED AT THE EXPERIMENTAL STATION ARBORETUM, CARACAS, VENEZUELA* Diet items Nº fecal samples Bird species Wet Dry Wet season Dry season season season Columbidae Nid seed fragments, Leaf fragments, Columbina talpacoti (G) fragments Nid seed fragments 1(4) 1(2) Leptotila verreauxi (G) Nid seed fragments 1(1) 0(0) Trochilidae Amazilia tobaci (NI) Arthropod fragments, Coleoptera 1(5) 0(2) Picidae Picumnus squamulatus (I) Formicidae, Coleoptera Formicidae, Loranthaceae seeds 1(1) 2(7) Galbulidae Coleoptera, Diptera, eggs, Galbula ruficauda (I) Lepidoptera, Orthoptera, Apidae Coleoptera 9(14) 1(2) Thamnophilidae Thamnophilus doliatus (I) Orthoptera, Formicidae, ant nymph Orthoptera, Formicidae, Coleoptera 1(4) 2(2) Orthoptera, Coleoptera, Isoptera, Formicivora grisea (I) Orthoptera, Formicidae, Coleoptera, Phoridae, Diptera, Insect egg, 4(11) 5(5) Hemiptera, Araneae, Diptera Hymenoptera, Formicidae Grallaridae Grallaricula ferrugineipectus (I) Coleoptera 1(1) 0(0) Furnariidae Cranioleuca subcristata (I) Coleoptera, Nid seed fragments 2(7) 0(1) Synallaxis albescens (I) Coleoptera, Hemiptera 1(1) 0(0) Campylorhamphus trochilirostris (I) Formicidae, Coleoptera 3(3) 0(3) Tyrannidae Orthoptera, Lepidoptera, Isoptera, Curculionidae, Araneae, Blatodea, Coleoptera, Lepidoptera, Atalotriccus pilaris (I) Apidae, insect eggs, Formicidae, Hymenoptera, Orthoptera, Formicidae 12(12) 8(16) Clusia seeds, Coleoptera, Diptera, Coleoptera, Diptera, Hemiptera, Orthoptera, Clusia seeds, Cnemotriccus fuscatus (I) Formicidae, Coleoptera, Hymenoptera 7(7) 1(1) Loranthaceae seeds, Formicidae, NI seed fragments Seed fragments, Lorantacea seeds, Elaenia flavogaster (F) Palichourea seeds 4(7) 1(7) Pitangus sulphuratus (FI) Formicidae, fruit pulp 0(0) 1(1) Lathrotriccus euleri (I) Formicidae 1(1) 0(0) Coleoptera, Formicidae, Loranthaceae Camptostoma obsoletum (FI) seeds, Diptera, fruit pulp, Nid seed Formicidae, Coleoptera, insect eggs 9(10) 1(1) fragments Vireonidae Hylophilus flavipes (F) Loranthaceae seeds, fruit pulp 0(0) 1(1) Cychlaris gujanensis (F) Clusia seeds, fruit pulp 0(0) 1(1) Troglodytidae Thryophilus rufalbus (I) Formicidae, Coleoptera Formicidae, Coleoptera, Diptera 2(3) 1(2) Orthoptera, Formicidae, Coleoptera, Troglodytes aedon (I) Lepidoptera, Hemiptera, Apidae, Orthoptera, Formicidae, Coleoptera, 2(9) 1(5) Diptera, Elateroidea Hemiptera, insect eggs, Diptera Polioptilidae Orthoptera, Formicidae, Lepidoptera, Ramphocaenus melanurus (I) Orthoptera, Coleoptera, Hymenopter Apidae, Hymenoptera, insect eggs, 1(1) 5(5) Diptera, fruit pulp Thraupidae Thraupis episcopus (F) Clydemia seed, Clusia seeds 0(0) 2(2)

122 FEBRUARY 2016, VOL. 41 Nº 2 Diet items Nº fecal samples Bird species Wet Dry Wet season Dry season season season Thraupis glaucocolpa (F) Coleoptera, flowers 1(1) 0(0) Tiaris bicolor (GI) Nid seed fragments, Coleoptera Nid seed fragments 3(5) 3(3) Coleoptera, Diptera, Flowers, fruit Coereba flaveola (FI) pulp, Clusia seeds, Formicidae, Fruit pulp, Coleoptera 5(8) 4(13) Isoptera, Diptera Incertae sedis Rhodinocichla rosea (I) Coleoptera 1(1) 0(0) Fruit pulp, Clusia seeds, Saltator coerulescens (F) Clusia seeds, fruit pulp Loranthaceae seeds 1(2) 4(5) Saltator striatipectus (I) Coleoptera 1(2) 0(4) Cardinalidae Cyanocompsa cyanoides (G) Coleoptera, Nid seed fragments 2(2) 0(0) Parulidae Parkesia noveboracensis (I) Formicidae, Coleoptera 1(1) 0(0) Fringillidae Euphonia trinitatis (F) Loranthaceae seeds 0(0) 1(1) Turdidae Formicidae, fruit pulp, Nid seed Coleoptera, Clusia seeds, fruit pulp, Nid Turdus nudigenis (FI) fragments, Clusia seeds seed fragments, Formicidae, Vespidae 9(9) 3(6) * Feeding guilds were assigned based on the items found in the feces. G: granivorous, NI: nectarivorous-insectivorous, I: insectivorous, FI: frugi- vorous-insectivorous. In parenthesis in the columns of fecal samples are the number of total captures (N). Nid: non identified.

TABLE II NUMBER TOTAL OF FOOD ITEMS, NUMBER OF FECES SAMPLES AND NUMBER OF SPECIES THAT CONSUME EACH ITEM IN A URBAN FOREST PATCH IN CARACAS, VENEZUELA Nº total Nº feces Nº bird Food item of item samples species Ro Ra Formicidae 226 35 15 0,26 0,2 Coleoptera 185 83 25 0,61 0,16 Clusia seeds 137 16 9 0,12 0,12 NI Insects 121 30 26 0,88 0,03 Diptera 108 30 9 0,22 0,09 Insect eggs 74 13 5 0,09 0,06 Loranthaceae seeds 53 8 7 0,06 0,05 Fruit pulp 37 31 9 0,23 0,03 Orthoptera 24 19 9 0,13 0,02 Lepidoptera 16 10 5 0,07 0,01 Apidae 13 6 4 0,04 0,01 Hymenoptera 11 8 5 0,08 0,01 Hemiptera 8 7 4 0,05 0,01 Figure 2. Food ítem abundance in fecal samples from the birds in the dry Vespidae 6 6 3 0,04 0,01 and wet seasons in an urban semi-deciduous forest patch in Caracas, Leaf fragments 6 6 6 0,01 0,01 Venezuela. Clydemia seeds 6 1 1 0,01 0,01 Palicourea seeds 6 2 2 0,01 0 Isoptera 4 4 4 0,01 0 more consumed during the wet of insectivorous birds tended Araneae 3 3 3 0,02 0 season. These results are con- to decrease. However, the Stone 3 1 1 0,02 0 sistent with previous findings Arboretum Experimental Flowers 3 3 3 0,02 0 about seasonal changes in ar- Station is connected to other Lauraceae 3 1 1 0,01 0 thropod availability on decid- green areas and parks, consti- Phoridae (Diptera) 2 1 1 0,01 0 uous forests (Wolda, 1978; tuting an ecological pathway Curculionidae 1 1 1 0,03 0 Blatodea 1 1 1 0,007 0 Wolda and Fisk, 1981), as through the city, which allows Ant nymph 1 1 1 0,007 0 well as with fluctuations in movements of birds between a Lampyridae 1 1 1 0,007 0 number of insectivorous birds continuum of green areas; but Pollen 1 1 1 0,007 0 with changes in food avail- probably, the connection be- Diplopod 1 1 1 0,007 0 ability (Frith and Frith, 1990). tween patches is not enough Homoptera 1 1 1 0,007 0 Stouffer and Bierregards to allow the maintenance of NI: non identified, Ro: relative occurrence, and Ra: relative abundance of (1995) found that in an isolat- diversity of insectivorous feeding items found in the feces of birds from the studied forest patch. ed forest patch the abundance present in pristine areas.

FEBRUARY 2016, VOL. 41 Nº 2 123 consistent with numerous re- Ferraro, Pedro A. Borges L. ports of Euphonia as the prin- and two anonymous referees cipal seed disperser of this for suggestions on the manu- family (Restrepo et al., 2002; script; Sandra B. Giner F. for Ribeiro et al., 2013). fieldwork help; Luis Levin of Loranthaceae seeds were also the E. S. Arboretum for logis- found in several Tyrannidae tical support, Ruben Candia and in H. flavipes, as had for help on the identification been previously reported of Phoridae; and Pablo Lau for (Guerra and Marini, 2002). providing bibliography. Communities in disturbed habitats tend to be less diverse REFERENCES than in pristine areas, with differences in composition, Aveledo R (1968) Aves comunes del richness, and abundance, Valle de Caracas. In Crema M Figure 3. Number of food items consumed by several birds species du- among others. Urban birds are (Ed.) 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Furnariidae feeding on seeds Ferraro et al., 2007; ing guilds in temperate regions Carvallo Lima AL (2008) Ecologia and fruits (Poulin et al., 1994) Chatellenaz, 2008; García- there was an increase in om- Trófica de Aves Insetívoras de but none for this species. The Amado et al., 2011). In this nivorous abundance in urban Sub-Bosque em uma Área de Phoridae consumption by F. study, S. coerulescens consumed areas, but not so in the neo- Mata Atlântica, Minas Gerais, grisea were probably incidental only fruit; whereas S. striatipec- tropics (Lim and Sodhi 2004), Brasil. Thesis. Universidade while it was eating ants, be- tus only consumed Coleoptera. where there is greater avail- Federal Rural do Rio de cause they are parasitoids of In the literature, occasional con- ability of resources throughout Janeiro, Brasil. the insects (Porter et al., 1995; sumption of insects has been the year. In this sense, in or- Caula S, Levín L (1999) A Vuelo Morrison and Gilbert, 1999; reported in S. orenocensis, but der to understand the dynam- de Pájaro. Manual para Elizalde and Folgarait, 2011). its diet is mostly composed of ics of urban birds feeding in Convivir con las Aves en la The consumption of insects fruits and leaves (Garcia-Amado the neotropical region, this Ciudad. Universidad Central like Formicidae and Coleoptera et al., 2011). The difference may study is pioneer generating de Venezuela. Caracas, Vene- in addition to seeds by C. tal- be related to only one sample information about the diet of zuela. 47 pp. pacoti and T. bicolor has been obtained of S. striatipectus, birds living in urban habitats Caula S, De Nóbrega JR, Giner S previously reported in other from which it is difficult to in Venezuela. The birds in our (2003) La diversidad de aves species of these genera (Poulin make a generalization of the study area probably consume como elemento de una estrate- et al., 1994; Pérez et al., 2001); diet. In the case of S. coerules- different food items that the gia de conservación del Jardín in the case of ants, they were cens, where five samples of fe- same species would have in Botánico de Valencia, Vene- probably ingested by accident ces were obtained, despite it pristine areas, due to a limited zuela. Acta Biol. Venez. while foraging seeds, or as a being a mainly folivorous spe- availability of resources. 23: 1-13. protein and fat supplement cies, the abundance of fruit in Therefore, this kind of re- Caula S, Giner S, De Nóbrega JR (Gill, 2006). However, none of the diet probably corresponds search, as well as long-term (2010) Aves urbanas: un estudio these individuals were present to an opportunistic consump- studies of bird communities in comparativo en dos parques tro- in the breeding season, when it tion at a time when this re- urban habitats, are necessary picales con diferente grado de has been reported that these source was abundant. in different neotropical locali- intervención humana (Valencia, species consume proteins. C. flaveola consumed a ties in order to understand the Venezuela). FARAUTE Cs. Frugivorous-insectivorous wide variety of items, consis- processes of adaptation of Tecnol. 5: 1-13. birds were more abundant in tent with previous reports birds to urban habitats. Clarke KR, Gorley RN (2006) the wet season, as has been (Skutch, 1954; Gross, 1958; PRIMER v6: User Manual/ reported in other seasonal hab- Snow and Snow, 1971; Cruz, ACKNOWLEDGMENTS Tutorial. PRIMER-E, Plymouth, itats (Karr, 1976; Blake and 1974; Feinsingerp et al., 1985; UK. Loiselle, 1991). An exception Poulin et al., 1994). The abun- The author thanks Luis Clergeau P, Savarge JP, Mennechez G was P. sulphuratus, with a dance of Loranthaceae seeds Gonzalo Morales, Emilio A. (1998) Bird abundance and diver- single capture in the dry in E. trinitatis feces is Herrera, Adriana Rodríguez- sity along an urban-rural

124 FEBRUARY 2016, VOL. 41 Nº 2 gradient: a comparative study orenocensis. Rev. Venez. vertebrates by Neotropical pas- Quilarque E, Marín G, Carvajal M, between two cities on diffe- Ornitol 1: 6-13. serine birds. Lundiana 6: Ferrer H (2010) Componentes rent continents. Condor 100: Gavett AP, Wakeley JS (1986) Diets 57-66. de la dieta de Sporophila minu- 413-425. of House Sparrows in urban Marzluff JM, Bowman R, Donnelly ta, S. intermedia (Emberizidae), Clergeau P, Croci S, Jokimaki J, and rural habitats. Wilson Bull. R (2001) A historical perspecti- Myiozetetes similis y Elaenia Kaisanlahti-Jokimaki ML, 98: 137-144. ve on urban bird research: flavogaster (Tyrannidae), en un Dinetti M (2006) Avifauna ho- ecotono bosque palustre-basi- Gill F (2006) Ornithology. 3rd ed. trends, terms, and approaches. mogenisation by urbanisation: montano de Venezuela. Bol. Freeman. New York, USA. 758 pp. In Marzluff JM, Bowman R, analysis at different European Donnelly R (Eds) Avian Ctro. Inv. 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