BIOTROPICA 36(4): 602±614 2004 In¯uences of Fruit Diversity and Abundance on Bird Use of Two Shaded Coffee Plantations1 TomaÂs A. Carlo 2,3,5, Jaime A. Collazo2 and Martha J. Groom2,4 2Department of Zoology and North Carolina Fish and Wildlife Cooperative Research Unit, North Carolina State University, Raleigh, North Carolina 27695, U.S.A. 3Ecology and Evolutionary Biology Dept., University of Colorado, Boulder, Colorado 80309±0334, U.S.A. 4Interdisciplinary Arts and Sciences, University of Washington, Bothell, and Department of Biology, University of Washington, Seattle, Washington 98195, U.S.A. ABSTRACT We studied avian foraging at two shaded coffee plantations in Ciales, Puerto Rico. Both coffee plantations contained patches of second-growth forest but differed in shade types; one was a rustic plantation with a species-diverse shade including many fruiting plant species and the other was a commercial polyculture shaded almost solely by Inga vera. We quanti®ed foraging activity of ®ve fruit-eating bird species (Euphonia musica, Loxigilla portoricensis, Nesospingus speculiferus, Spindalis portoricensis, and Vireo altiloquous) and monthly fruit abundance in the coffee plantation and adjacent second-growth forest habitats at each site. Fruits comprised more than 50 percent of the diets for four of ®ve focal bird species. We found a signi®cant difference in the number of foraging records for focal bird species between coffee and forest habitats in the commercial polyculture but found few differences between these habitats in the rustic coffee farm. Overall, foraging activity was positively correlated with the abundance of fruits across study sites. Bird foraging was concentrated on plant species in the genera Cecropia, Miconia, Schef¯era, Phoradendron, and Guarea, which together accounted for over 50 percent of frugivory records. Plant species in such genera fruited over prolonged time periods and provided birds with a fairly constant fruit supply. Our ®ndings underscore the importance of fruiting plant species in making coffee plantations suitable habitat for birds and suggest that native fruiting plants be incorporated in coffee farms for avian conservation. RESUMEN Estudiamos el forrajeo de aves frugõÂvoras en dos plantaciones de cafe de sombra en Ciales, Puerto Rico. Ambas plantaciones contenõÂan parches de bosque de crecimiento secundario, pero se diferenciaban por el tipo de sombra: una era ``ruÂstica'' con una gran diversidad de especies de sombra, incluyendo muchas especies de plantas frutales, y la otra era un ``policultivo comercial'' sombreada casi uÂnicamente por Inga vera. En cada sitio, cuanti®camos la actividad de forrajeo de cinco especies de aves frugõÂvoras (Euphonia musica, Loxigilla portoricensis, Nesospingus speculiferus, Spin- dalis portoricensis, Vireo altiloquous), y la abundancia mensual de frutos en los cafetales y en los bosques adyacentes. Las frutas comprendieron maÂs del 50 por ciento de la dieta de cuatro de las cinco especies de aves en estudio. Encontramos diferencias signi®cativas en el nuÂmero de registros de forrajeo de especies de aves entre los habitats de cafe y bosque en el policultivo comercial, pero encontramos pocas diferencias entre estos habitats en la granja de cafe ruÂstico. En general, la actividad de forrajeo estuvo positivamente correlacionada con la abundancia de frutos a traveÂs de los sitios de estudio. El forrajeo de las aves estuvo centrado en especies de plantas de los geÂneros Cecropia, Guarea, Schef¯era, y Phoradendron, que juntas abarcaron por encima del 50 por ciento de los registros de frugivorõÂa. Especies de plantas en estos geÂneros fructi®caron por un perõÂodo de tiempo maÂs prolongado y surtieron constantemente a las aves de frutas. Nuestros hallazgos resaltan la importancia de las especies de plantas frutales en convertir las plantaciones de cafeÂenhaÂbitats adecuados para las aves, y sugiere que las plantas frutales nativas deberian ser incorporadas en las granjas de cafe para la conservacioÂn de las aves. Key words: avian foraging; bird-friendly coffee; Cecropia; frugivory; Guarea; Phoradendron; plant phenology; Puerto Rico; Schef¯era; shaded coffee plantations. SHADED COFFEE PLANTATIONS HAVE BEEN CHARACTER- an agricultural practice reconciled with conserva- IZED AS FRIENDLY HABITAT FOR BIRDS, a rare case of tion interests (Brash 1987, Wunderle & Wade 1993, Perfecto et al. 1996, Greenberg, Bichier, An- 1 Received 14 May 2003; revision accepted 3 June 2004. gon, & Reitsma 1997, Greenberg, Bichier, & Stir- 5 Corresponding author: Herbario JardõÂn BotaÂnico de ling 1997, Wunderle & Latta 1998). Some shaded Puerto Rico, Universidad de Puerto Rico, P.O. Box 364984, San Juan, Puerto Rico 00936±4984, U.S.A.; coffee plantations may serve as refuge habitat for e-mail: [email protected] many avian species, particularly Neotropical mi- 602 Fruits and Avian Use of Shade Coffee Plantations 603 grants, some of which have declining populations that provide guidance for the bene®ts of various (Brash 1987, Wunderle & Latta 1993, Greenberg, shade-tree species for birds. Plantations with I. vera Bichier, Angon, & Reitsma 1997, Greenberg, Bi- as the principal shade species have similar avian chier, & Sterling 1997, Wunderle & Latta 1998, species richness as natural forests in some Central Petit & Petit 2003). Yet, a wide variety of practices American locations (Greenberg, Bichier, Angon, & and plant community structures are included under Reitsma 1997, Greenberg, Bichier & Stirling the designation of ``coffee shade,'' and not all are 1997). In contrast, plantations shaded by Pseu- equally useful to bird communities. Shade coffee doalbizia berteroana have lower avian and arthro- plantations range from highly diverse remnants of pod diversity than plantations shaded with I. vera primary tropical forest to monospeci®c stands (Johnson 2000). Still, beyond these studies there is planted for their timber (Montenegro et al. 1997, little information to enlighten shade-tree selection, Moguel & Toledo 1999). Research indicates that especially regarding the selection of fruiting trees coffee grown under a more diverse canopy better that could attract birds. supports communities of birds and other animals The importance of fruits as avian food resourc- (Moguel & Toledo 1999). es is underscored by the fact that tropical landbird Fruit availability can be in¯uential to both hab- species are highly dependent on fruit, including itat quality and landscape movement of birds many migrants on wintering grounds (Karr 1971; (Blake & Hoppes 1986, Terborgh 1986, Levey Morton 1971, 1973; Greenberg 1981; Stiles 1988, Loiselle & Blake 1991, Levey & Stiles 1992, 1983). Hence, fruits may be vital resources regard- Rey 1995, Kinnaird et al. 1996). Therefore, the less of whether or not birds use them in a special- presence and composition of fruiting plant species ized or opportunistic way. In this study, we inves- in a coffee plantation should in¯uence its suitabil- tigated diets and foraging activity of ®ve species of ity for frugivorous birds, especially in providing resident fruit-eating birds in two shaded coffee highly preferred fruit resources (Carlo et al. 2003). plantations and adjacent forest in the north±central Shade-tree species composition is highly variable in mountains of Puerto Rico. We examined how dif- coffee plantations worldwide (Perfecto et al. 1996, ferences in fruit availability at these sites may affect Greenberg, Bichier, Angon & Reitsma 1997, Mo- bird use as foraging grounds. The size and spatial guel & Toledo 1999), yet important differences ex- con®guration of both study sites provided a useful ist among shade-tree species that could in¯uence opportunity to compare avian use of plantations in the bird use of a coffee plantation (Johnson 2000). relation to use of adjacent second-growth forest. The attractiveness of shade-tree species to birds Both plantations were primarily shaded by I. vera likely results from complex interactions between but differed in species composition and abundance bird diets and tree-speci®c attributes such as fruit of other ¯eshy-fruited plant species. We examined and ¯ower size, palatability, nutrient content, seed how differences in the fruiting environments at to pulp ratios, crop size, plant architecture, and the these sites may affect frequency of avian foraging. suitability to host arthropods (Levey 1987, Foster 1990, Stiles 1993, Johnson 2000). For example, METHODS Inga vera is widely used by birds, probably due to its capacity to ¯ower and fruit continuously or re- STUDY SITE. This study was conducted in 1998 at peatedly over time (Wunderle & Latta 1998). In two shaded coffee plantations in the municipality contrast, other popular shade species such as Eryth- of Ciales in the north±central mountains of Puerto rina poepigiana and Cordia alliodora have short and Rico. One plantation was located at Cialitos synchronous ¯owering seasons, and their non- (188159N, 668339W; 650 m elev.) and the other at ¯eshy fruits are not attractive to frugivores (Slocum FrontoÂn (188189N, 668329W, 350 m elev.). Annual 2001). The value of other tree species, however, rainfall for the region ¯uctuates between 150 and remains poorly documented. 200 cm. October and November are the wettest In spite of the important differences that the months, while March and April are the driest. Cia- selection of shade tree species may have for wildlife, litos was a rustic plantation, whereas FrontoÂn was a farmer's decision to use particular shade species a commercial polyculture