Influences of Fruit Diversity and Abundance on Bird Use of Two

Home , Cecropia, Phoradendron, Schefflera

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 quantified foraging activity of five 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 five focal bird species. We found a significant 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, Schefflera, 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 findings 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 frugı´voras en dos plantaciones de cafe´ de sombra en Ciales, Puerto Rico. Ambas plantaciones contenıán parches de bosque de crecimiento secundario, pero se diferenciaban por el tipo de sombra: una era ‘‘ru´stica’’ con una gran diversidad de especies de sombra, incluyendo muchas especies de plantas frutales, y la otra era un ‘‘policultivo comercial’’ sombreada casi uńicamente por Inga vera. En cada sitio, cuantificamos la actividad de forrajeo de cinco especies de aves frugı´voras (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 ma´s del 50 por ciento de la dieta de cuatro de las cinco especies de aves en estudio. Encontramos diferencias significativas en el nu´mero 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´ ru´stico. En general, la actividad de forrajeo estuvo positivamente correlacionada con la abundancia de frutos a trave´s de los sitios de estudio. El forrajeo de las aves estuvo centrado en especies de plantas de los geńeros Cecropia, Guarea, Schefflera, y Phoradendron, que juntas abarcaron por encima del 50 por ciento de los registros de frugivorıá. Especies de plantas en estos geńeros fructificaron por un perıódo de tiempo ma´s 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 cafeénha´bitats adecuados para las aves, y sugiere que las plantas frutales nativas deberian ser incorporadas en las granjas de cafe´ para la conservacioń de las aves.

Key words: avian foraging; bird-friendly coffee; Cecropia; frugivory; Guarea; Phoradendron; plant phenology; Puerto Rico; Schefﬂera; 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 Jardı´n Bota´nico 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 benefits 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 monospecific 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 influential 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 influence its suitabil- tigated diets and foraging activity of five 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- configuration of both study sites provided a useful ist among shade-tree species that could influence 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-specific attributes such as fruit of other fleshy-fruited plant species. We examined and flower 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 flower 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 flowering seasons, and their non- (18Њ15ЈN, 66Њ33ЈW; 650 m elev.) and the other at fleshy fruits are not attractive to frugivores (Slocum Frontoń (18Њ18ЈN, 66Њ32ЈW, 350 m elev.). Annual 2001). The value of other tree species, however, rainfall for the region fluctuates 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 Frontoń was a farmer’s decision to use particular shade species a commercial polyculture according to the classifi- depends mostly on regional farming practices, state cation of Moguel and Toledo (1999). Coffee plants policies, and the degree of ‘‘modernization’’ of the at both farms had an age of 30 to 40 years. Shade farm (sensu Perfecto et al. 1996). Rarely are shade trees at Cialitos were comprised predominantly of trees selected or recommended with a benefit for I. vera, Inga laurina, Andira inermis, Cecropia schre- wildlife in mind. At present, there are few studies beriana, Schefflera morototoni, Ocotea spp., Alchor- 604 Carlo, Collazo, and Groom nea latifolia, Cordia sulcata, and understory shrubs 315 adult individuals of fruiting plants was tagged of Miconia and Psychotria spp. The canopy of the within vegetation sampling plots, although rare commercial polyculture (Frontoń) was comprised species were tagged wherever found. Sample sizes predominantly of three species: I. vera, I. laurina, per study site were 190 trees in Cialitos (29 spp.) and A. inermis, with I. laurina uncommon. Un- and 125 in Frontoń (19 spp.). We recorded the derstory shrubs and fruiting trees, other than plant- number of ripe fruits for tagged plants once a ed bananas and oranges, were scarce at Frontoń. month from February through September. In ad- Coffee plantations were adjacent to patches of dition to tree and shrub species, we also monitored montane second-growth forest (hereafter forest) the epiphytes Anthurium scandens and Ripsalis bac- that had once been used as coffee plantations but cifera and hemiparasites Phoradendron spp. known were recovering for the past 30 to 40 years. These to be important food items for Euphonia spp. (Res- second-growth forest patches comprised 35 percent trepo et al. 2002). of the total plot area in Cialitos and 41 percent in Eight categories were used to estimate the Frontoń. A continuous grid of 30 x 30 m cells was monthly ripe and unripe fruit abundance of tagged established at each study site, incorporating both individuals (0 ϭ 0, 1 ϭ 1–10, 2 ϭ 10–50, 3 ϭ coffee plantation and forest, and extended for 9 ha 50–100, 4 ϭ 100–500, 5 ϭ 500–1000, 6 ϭ 1000– in Cialitos and 10 ha in Frontoń. Both study sites 5000, 7 ϭ 5000–10,000, and 8 Ͼ 10,000). We were imbedded in a landscape matrix in which sec- used the midpoint value of each category as an ondary forest cover was ca 65 percent (estimated estimate of fruit abundance for each species except from aerial photographs). for the 9th category or maximum abundance, for which we used a value of 10,000. We then multi- AVIAN ABUNDANCE AND FRUITING PLANT PHENOLOGY. plied the mean fruit abundance value for each spe- Abundance of focal avian species was estimated us- cies by its density in each habitat (i.e., coffee and ing 30 m radius point counts (Hutto et al. 1986). forest) at each site to obtain a fruit abundance in- Nine count stations were randomly selected within dex (hereafter FAI) of ripe fruit/ha. each site using a minimum spacing of 120 m between stations. Of these, Cialitos had five count FORAGING OBSERVATIONS. Foraging observations stations in coffee and four in forest habitat, while were recorded for five hours per day, twice a week, Frontoń had five in coffee and three in forest. Birds three weeks per month (30 h/mo), for eight were counted the first week of each month from 0600 to 1000 h by visual and auditory detection months in Cilaitos and seven months in Frontoń. for ten minutes. The order of point station visits To record foraging observations, a random grid was shifted each month to avoid morning hour- point was chosen on every sampling occasion as a biases that could alter detection probabilities. Birds starting point. From this point, the observer moved flushed from within count stations due to the ap- for five hours, beginning one hour after sunrise, proach of an observer were recorded as detections. guided by visual and auditory cues from focal birds. Estimates of plant species composition and Focal species were the five most common resident density (individuals/ha) were obtained in 11 m ra- species for which foraging samples were large dius circular plots (N ϭ 36 at each site) in which enough for statistical analyses: Loxigilla portoricen- plant species, vegetative cover, number of stems, sis, Nesospingus speculiferus, Vireo altiloquous, Spin- and DBH were quantified. Percentage canopy cov- dalis portoricensis, and Euphonia musica (hereafter er was estimated using ocular tubes at cardinal po- Loxigilla, Nesospingus, Vireo, Spindalis, and Eupho- sitions (N, E, S, and W) 5 m from a plot’s center nia). Once a focal bird species was detected, we (James & Shugart 1970). Stems less than 2.5 cm followed it until the first feeding attempt was com- DBH were counted only within a radius of 5 m. pleted and classified the observation according to Four plots were established at each point-count sta- food item and its location within the plot (i.e., tion following the procedures of Martin and Gue- coffee or forest). We did not make sequential ob- pel (1993). A central plot was located at each point servations on the same individual bird to avoid count station while the other three were placed 25 problems associated with nonindependent data m from the center plot at 120, 240, and 360Њ. (Hejl et al. 1990); however, it is possible that on We monitored fruiting at as many adult plants any given day, we observed an individual bird more as possible, trying to tag ten individuals per site for than once at a different location within the study each species. For several species, however, rarity site. We also recorded fruit consumption of non- precluded achieving such sample size. A total of focal avian species when possible. Fruits and Avian Use of Shade Coffee Plantations 605

STATISTICAL ANALYSES. We summarized structural counts. For fruit preference analyses, we deferred data of vegetation plots as follows. Height of can- to Carlo et al. 2003, a broader ecological study of opy trees and percent canopy cover were averaged avian frugivory and seed dispersal that covers the across vegetation plots within each habitat site (e.g., same study sites and data used here. Cialitos and Fronton forests). Stem counts were grouped into five DBH classes (Martin & Guepel RESULTS 1993) and summed across vegetation plots, divided by area sampled within habitat sites, and expressed The study sites differed in plant species composi- as stems/ha. To compare canopy height and cover tion, fruit abundance, and some structural param- among habitat sites, we used one-way ANOVA. To eters of vegetation. Cialitos had higher species den- test for differences in the frequency distribution of sity with 36 recorded fruiting plant species in its stems by DBH classes, we used a 4 x 5 contingency forest habitat and 28 species in the coffee planta- table (4 habitat sites x 5 DBH classes). tion, with many individuals fruiting in both habi- We summarized foraging records and fruit tats at any time (Table 1 and Fig. 1). Note that 7 abundance data (FAIs) by month and habitat site. additional fruiting plant species were found in Cia- To test for differences in the number of avian for- litos and 3 in Frontoń (see below) during the aging records between habitats at each site, we used months of study, although they were herbaceous or a one-sample Wilcoxon signed-rank test. To run shrubby rare plants and not included in the phe- the tests, we used the difference for each month nology sample. Cialitos forest and coffee habitats between the expected and observed proportion of shared 66 percent of the fruiting plant species, and foraging records for each focal bird species in coffee of the remaining, 30 percent were found only in and forest habitats at each site (all food items con- forest and 4 percent in coffee. Frontoń had 22 sidered). We used the percentage of habitat area as fruiting plant species in the forest habitat and 12 the expected value (i.e., Cialitos coffee 35%, Cia- in the coffee plantation. Frontoń forest and coffee litos forest 65%, Frontoń coffee 59%, and Frontoń shared 44 percent of plant species, with 44 percent forest 41%). The rationale for the test is that if exclusively in the forest and 12 percent exclusively birds foraged indiscriminately between coffee and in the coffee. Fruiting plants found only in forest forest habitats, then it would have been equally habitats accounted for 6 percent of avian foraging likely to observe positive and negative differences records in Cialitos in contrast with 22.6 percent in of similar magnitude (rank) across months at each Frontoń. Fruiting plant species found only in cof- study site. Because differences in focal bird species fee habitats accounted for 0 percent of avian for- abundance at habitat sites could have affected ob- aging records in Cialitos and 0.07 percent of observation probabilities, we weighted foraging re- servations in Frontoń. In five months out of eight, cords of each focal bird species by multiplying it Frontoń coffee had less than half the fruit abun- by the reciprocal of its abundance within the hab- dance and species diversity of Frontoń’s secondary itat site. Avian abundance weights were the average forest, Cialitos forest, or Cialitos coffee (Fig. 1). of monthly detections of focal bird species recorded Hence, coffee and forest habitats at Cialitos were at point-count stations of habitat sites. more similar in ripe fruit abundance and species To examine the relationship between ripe fruit composition than habitats at Frontoń (Fig. 1 and abundance and bird foraging records, we used Table 1), where key fruiting plant species like S. Spearman’s rank correlation. For these analyses, we morototoni were missing from coffee but present in pooled monthly study site data on avian foraging forest habitat (Fig. 2 and Table 1). and fruit abundance into a single matrix, parti- Ripe fruit abundance at both sites was highest tioned by habitat type and site. Although fruit during April–June (Fig. 1A). The large standard abundance data from consecutive months are not error for mean ripe fruits/month reflects a high statistically independent, we believe that the anal- monthly turnover of fruiting species and individ- yses are insightful given that individual birds could uals in the sample. The overall fruiting pattern was cross freely between coffee and forest patches, as affected by both the abundance of adult plants and well as into neighboring areas. Therefore, at the the particular fruiting modes of plant species. For scale of study, birds were free to track monthly example, some species were recorded with ripe fruit changes in resource abundance at coffee and forest for just one or two months (e.g., Ocotea leucoxylon, habitats of each site. For this analysis, we also used O. floribunda, and Cordia sulcata), while others the abundance-weighted foraging records of each fruited during the entire study (e.g., Cecropia and avian species per habitat site obtained from point Guarea; Fig. 2). Fruit abundance of a few species, 606 Carlo, Collazo, and Groom % IN % FR ń Coffee % FA Fronto ird species in selected plant ń in Puerto Rico. Frugivory . ha ———— ———— ———— ———— ———— Ind % IN % FR ń Forest % FA Fronto ha Ind % IN % FR % FA Cialitos Coffee ha Ind % IN % FR % FA Cialitos Forest .01.02.08.01 — —— ———— ——— 1.20.40.50.0———— ——— — — —— ———— 1.90.00.00.3— 1.90.23.30.2— 9.60.10.40.20.90.84.80.1— 1.90.00.00.21.30.90.10.02.47.92.50.5———— ha .— — ——0.21.20.10.50.0———— — 3.8—— 49.9 3.8 4.4 0.0 21.8 18.7 7.3 0.2 52.3 23.6 9.9 1.1 32.628.8 0.2 0.2 2.2 0.7 2.2 2.2 9.2 58.6 0.2 0.2 2.2 0.7 2.2 2.2 77.2 1.2 4.6 4.2 14.0 2.3 7.6 3.5 5.5 86.8 0.0 4.8 0.0 1.7 2.3 12.3 15.3 0.1 5.1 0.9 0.7 0.4 5.0 0.1 21.4 0.2 21.0 2.3 1.3 0.1 1.7 0.0 65.2 4.9 4.1 3.5 14.9 2.2 0.7 0.5 2.4 4.8 2.9 1.2 Ind spp. 35.1 3.7 5.9 0.3 121.1 2.4 9.9 0.2 — — — — Portion of avian foraging observations and fruit abundance in active coffee farms and in adjacent second-growth forest at Cialitos and Fronto (FR) and insectivory (IN) values are the percentage of foraging observations (standardized across coffee and forest habitats at each site) of focal b species. The proportion of fruit abundance (FA) is the standardized fruit abundance index (FAI) of plant species across habitats at each site Plant Species spp. 126.6 0.3 6.2 0.0 42.5 0.3 6.2 0.0 22.6 0.1 2.3 0.0 spp. 17.3 0.1 0.0 0.9 5.7 0.1 0.3 0.1 24.9 2.4 0.0 1.1 1.3 24.1 2.9 0.0 spp. 1.9 12.6 3.5 0.3 1.2 14.8 3.1 0.5 — — — — Other spp. 313.0 12.6 3.0 2.9 572.0 16.4 0.3 0.2 55.5 8.5 3.0 1.1 14.2 1.7 0.0 Schefflera morototoni Piper amalago Guarea guidonia Inga vera Miconia Ocotea Phoradendron Casearia sylsvestris Cecropia schreberiana Cordia sulcata Dendropanax arboreus Ficus Clusia rosea TABLE 1. Alchornea latifolia Fruits and Avian Use of Shade Coffee Plantations 607

non-focal bird (14 residents and 4 Neotropical migrants) species included 58 records in Frontoń and 52 in Cialitos. Of the five focal bird species records, 434 observations were on fruits, 13 on flower parts and/or nectar, 32 on leaf shoots, and 222 on in- vertebrates (Table 3). All focal bird species ate fruit and arthropods representing a spectrum of fruit use (Table 3). Frugivory exceeded 90 percent in Eup- honia and Spindalis, 80–90 percent in Loxigilla, 60–70 percent in Nesospingus, and 20–30 percent in Vireo (Table 3). Half of the foraging observations occurred on only a few plant species (Table 1), with focal bird species differing in relative use and preference for the fruits of such plants (Table 3; Carlo et al. 2003). Frugivory was recorded most frequently on Ce- cropia, Guarea, Miconia, Phoradendron, and Schef- flera (Table 1). Preferences for these plants were somewhat partitioned among focal bird species and FIGURE 1. Average ripe fruit abundance (A) and num- relatively consistent among sites (Table 3). For ex- ber of plant species recorded bearing ripe fruit (B) each ample, Nesospingus preferred Miconia spp. and Ce- month in coffee farms and in second-growth forest at cropia; Euphonia preferred Phoradendron spp.; Lo- Cialitos and Frontoń, Puerto Rico. xigilla preferred Guarea and Cecropia; Vireo preferred Guarea; and Spindalis preferred Cecropia, Miconia spp., and Schefflera. Further, these pre- such as Miconia spp., Ficus spp., Cecropia, and ferred fruits were either the first or second most Guarea, was spread out over time due to either frequently consumed fruiting plants in both study individual asynchrony (Ficus) or a repetition in the sites (Carlo et al. 2003). These plants were also fruiting cycle of individuals (Cecropia, Miconia, and important for non-focal bird species, resulting in Guarea). 63 percent of their foraging records. Overall, Ce- Site habitats also differed in structural param- cropia fruits were eaten by the greatest number of eters of vegetation. Canopy was highest at Cialitos species (12), including the migrants Dendroica ti- forest and lowest at Frontoń coffee (Table 2) al- grina and Dendroica caerulescens. Schefflera and though differences were not significant (one-way Guarea followed with 10 species, 3 of which were ANOVA, df ϭ 3, F ϭ 2.08, P ϭ 0.10). Percent migrants (Schefflera: Parula americana [nectar] and cover of canopy was highest in Cialitos forest and D. tigrina [fruits]; Guarea: Vireo flavirostris [fruits]). lowest in Frontoń coffee (Table 2; one-way ANO- Frugivory records on Phoradendron spp. (P. pipe- VA, df ϭ 3, F ϭ 2.39, P ϭ 0.07). Site habitats roides and P. hexastichum) amounted to 7 bird spe- also differed structurally as reflected by the fre- cies, including the migrant Vireo flavirostris. Mico- quency distribution of stems by DBH classes (␹2 nia fruits were consumed by 5 bird species. The ϭ 26.6, df ϭ 12, P Ͻ 0.01). Forest habitats had most common fruiting tree in coffee plantations more small stems (Ͻ2.5 cm) than coffee habitats was I. vera, which was used both as an arthropod (Table 2). Curiously, the trees with largest DBH foraging substrate and for its fruits, flower parts were found in the most dissimilar habitats: Cialitos (anthers), nectar, and leaf shoots. For example, forest and Frontoń coffee (Table 2). When the two Spindalis and Nesospingus consumed fruits, nectar, largest DBH categories are pooled together, Fron- and flower parts of I. vera. Still, despite being one toń coffee had more large stems per hectare than of the most common trees at both study sites, I. all other habitat sites (Table 2). vera was never as heavily used by focal bird species We collected a total of 811 foraging observa- as plants such as Cecropia, Guarea, Phoradendron tions, 701 on focal bird species and 110 on other spp., and Schefflera (Table 1). Despite their abun- resident and migratory bird species. Of the focal dance, coffee fruits were almost entirely ignored; bird species records, 555 were in Cialitos (N ϭ 240 we recorded only seven cases in which they were observation h, 8 mo) and 146 in Frontoń (N ϭ eaten (Vireo:3;Spindalis:3;Loxigilla: 1). We ob- 210 observation h, 7 mo). Foraging records on 18 tained frugivory records for almost all other fruit- 608 Carlo, Collazo, and Groom

FIGURE 2. Monthly fruit abundance index (FAI) of selected plant species individuals in areas of active coffee production (coffee) and in second-growth forest (forest) at Cialitos and Fronto´n coffee farms in Puerto Rico.

ing plant species bearing fleshy fruits in the study between coffee and forest habitats at the two study sites, although less frequently. Some of such occa- sites. Monthly records were more numerous in sec- sionally consumed plants also proved to be pre- ond-growth forests than in coffee plantations at ferred resources, but various factors including short both sites, but more clearly in Frontoń (Fig. 3). fruiting seasons, rarity, and hierarchical interactions This is in spite of the fact that visibility was higher with other preferred plant species reduced their in coffee plantations because of the lower canopy overall impact at our study site (Carlo et al. 2003). density (Table 2). In Frontoń, Vireo was the only Feeding frequency of focal bird species differed focal bird species observed foraging in the coffee

TABLE 2. Summary of structural vegetation data for coffee and forest habitats in Cialitos and Fronto´n, Puerto Rico. Data were obtained from 36 circular sampling plots 11 m in diameter (Martin & Guepel 1993).

Site Habitat Structural Fronto´n Fronto´n Cialitos Cialitos Parameters Coffee Forest Coffee Forest Avg. Canopy Height (m Ϯ SE) 8.58 (Ϯ0.68) 9.29 (Ϯ0.50) 10.02 (Ϯ0.55) 10.06 (Ϯ0.55) Avg. Canopy Cover (% Ϯ SE) 64.7 (Ϯ3.91) 74.2 (Ϯ5.54) 72.18 (Ϯ4.10) 83.45 (Ϯ4.59) Stems/ha DBH Ͻ2.5 cm (%) 3595.8 (45) 6960.1 (61) 4203.8 (46) 5300 (59) Stems/ha DBH 2.5–8 cm (%) 1123.3 (14) 2310.4 (20) 2203.8 (24) 859.5 (9) Stems/ha DBH 8–23 cm (%) 2258.3 (29) 1789.2 (16) 2369.4 (26) 2014.3 (23) Stems/ha DBH 23–38 cm (%) 706.4 (9) 289.5 (2) 299.4 (3) 374.2 (4) Stems/ha DBH Ͼ38 cm (%) 301.1 (3) 69.5 (1) 70.06 (1) 350.3 (5) Fruits and Avian Use of Shade Coffee Plantations 609

TABLE 3. Main constituents of the diets for ﬁve bird species at two study sites composed of coffee and forest habitats in north–central Puerto Rico.

Cialitos Frontoń % % Bird Species Food Type in Diet (N) Food Type in Diet (N) Euphonia musica Phoradendron spp. 0.66 (55) Cecropia schreberiana 1 (1) Anthurium scandens 0.16 (13) — — Arthropods 0.11 (9) — — Other fruits (5 spp.) 0.07 (6) — — Loxigilla portoricensis Guarea guidonia 0.25 (17) Guarea guidonia 0.46 (11) Alchornea latifolia 0.21 (14) Cecropia schreberiana 0.17 (4) Other fruits (9 spp.) 0.35 (24) Other fruits 0.29 (7) Arthropods 0.19 (13) Arthropods 0.08 (2) Nesospingus speculiferus Arthropods 0.41 (44) Arthropods 0.33 (2) Miconia spp. 0.22 (24) Cecropia schreberiana 0.33 (2) Cecropia schreberiana 0.06 (7) Other fruits (2 spp.) 0.33 (2) Other fruits (12 spp.) 0.39 (32) Spindalis portoricensis Schefflera morototoni 0.32 (56) Cecropia schreberiana 0.48 (17) Cecropia schreberiana 0.16 (29) Schefflera morototoni 0.20 (7) Other fruits (9 spp.) 0.32 (56) Other fruits (8 spp.) 0.23 (8) Arthropods 0.02 (3) Arthropods 0.06 (3) Vireo altiloquous Arthropods 0.66 (79) Arthropods 0.80 (67) Garea guidonia 0.13 (15) Cecropia schreberiana 0.06 (5) Clusia rosea 0.09 (11) Guarea guidonia 0.06 (5) Other fruits (15 spp.) 0.13 (15) Other fruits (3 spp.) 0.08 (7)

farm more frequently than the forest habitat for DISCUSSION one month (Fig. 3). In Cialitos, all focal bird species were recorded feeding in the coffee more often FRUIT ABUNDANCE AND BIRD FORAGING ACTIVITY. than in forest at least in one month (Fig. 3), and Similar patterns of bird use characterized our two only Loxigilla showed a significant difference in its study sites, with more intense avian foraging in sec- foraging between coffee and forest habitats (Fig. 3). ond-growth forests than in coffee plantations. In contrast, in Frontoń, two out of three focal bird Some focal bird species, however, made higher use species showed a significant sub-utilization of the of coffee plantations than forests in several months. coffee farm with the two other focal bird species This was the case in the Cialitos rustic coffee plan- also showing a forest-oriented foraging pattern, but tation where we observed Spindalis, Euphonia, and we lacked a sufficient sample size for testing (Fig. Loxigilla more frequently in the coffee plantation 3). Therefore, relative to its forest habitat, the Cia- than in forest habitat for quite a few months, es- litos coffee farm appears more attractive to more pecially when abundance of preferred fruits was focal bird species during more months than the highest in the active coffee portion of the site (i.e., Frontoń coffee farm. Foraging records were posi- February, August, and September; Figs. 2 and 3). tively correlated with the abundance of ripe fruits This was in contrast to the Frontoń coffee plan- in four of the five focal bird species (including a tation, which was used more often than the forest marginally significant correlation for Euphonia; Fig. habitat by Vireo (the least frugivorous species) for 4). When plotting the total (pooled spp.) monthly just one month. Overall, at the Frontoń coffee foraging records of each habitat versus the abun- plantation the abundance of preferred fruits was dance of fruit, sites followed the general pattern: low (e.g., Cecropia, Guarea, and Phoradendron) and Cialitos forest Ͼ Cialitos coffee Ͼ Fronton forest poorly distributed through the months of study ϾFrontoń coffee (Figs. 1A and 4); however, the (e.g., Ocotea spp. had fruit for less than two greatest and clearest difference in both foraging re- months). Because most focal bird species ate fruits cords and fruit abundance was between Frontoń frequently, it is likely that the availability of ripe coffee farm (the poorest in fruit diversity and abun- fruit at each habitat site over time was in part re- dance) and all other habitat sites. sponsible for the differences in foraging frequency 610 Carlo, Collazo, and Groom

FIGURE 3. Monthly difference between expected and observed proportions of foraging records for five bird species in coffee habitats at two study plots composed of shade coffee with secondary forest patches at Frontoń and Cialitos, Puerto Rico. Positive values indicate that foraging records in the coffee plantations were higher than expected. Expected proportion of use of coffee habitats was set equal to the proportion of the habitat at each farm (Cialitos ϭ 0.65, Frontoń ϭ 0.59). We used Wilcoxon’s signed-rank test to test the null hypothesis of no trend (directionality) in bird foraging between coffee and forest habitats across the months of study (i.e., monthly differences are equally likely to go one way or the other). Avian species for which sample size was insufficient are denoted by *. between habitats (Blake & Loiselle 1991). We rec- concordant with those reported by other studies in ognize that because our study was not replicated in the region that include different localities and hab- space, it is possible that our results overestimated itats (Carlo et al. 2003, Saracco et al. 2004). the relationship between avian foraging and fruit Fruit crops were utilized in different propor- availability of habitats. Our results, however, are tions by focal bird species, with Cecropia, Cordia, Fruits and Avian Use of Shade Coffee Plantations 611

FIGURE 4. Correlation (Spearman’s rho) between monthly ripe fruit abundance and avian foraging activity (pooled food items) in areas of active coffee production and in second-growth forest at Frontoń and Cialitos, Puerto Rico. Unfilled circles ϭ Frontoń coffee; Filled circles ϭ Frontoń forest; unfilled diamonds ϭ Cialitos coffee; filled diamonds ϭ Cialitos forest.

Guarea, Miconia, and Phoradendron used in greater Ocotea spp. (O. floribunda and O. leucoxylon) had proportion relative to their fruit availability at all large crops packed into a two-month period, but habitat sites (Table 1). For example, at Frontoń, attracted only a few foragers during that time. The Cecropia had the highest proportion of use (20%) low popularity of Ocotea spp. may have been due in the forest habitat, followed by Guarea (13.3%). to the handling difficulties posed by its large seeds Although Cecropia and Guarea contributed little to relative to the rather small focal species. Similarly the total ripe fruit production at Frontoń, their ripe in Cialitos, fruits of C. sulcata were also available fruits were available for seven months. In contrast, for two months, but unlike Ocotea, it was frequent- 612 Carlo, Collazo, and Groom ly used by Spindalis while available. This suggests natives, it was not surprising that the two coffee that the impact of a fruiting plant species in our plantations were underused, particularly the plan- plots was not solely due to resource density depen- tation that contained a lower diversity and abun- dence, but was also influenced by its intrinsic at- dance of fruits. tractiveness to birds. This underscores the influence of preferences in shaping the foraging activity and CONSERVATION IMPLICATIONS. Shaded coffee plan- habitat use of birds. For example, fruiting trees of tations having a shade layer comprised mostly of I. C. sulcata in Cialitos were found mostly within the vera could be improved by selectively planting or coffee plantation. In February, C. sulcata fruits allowing the growth of species important to local comprised 35 percent of the foraging observations and migratory bird species. Such fruiting plants can of Spindalis in Cialitos across coffee and forest hab- be allowed to grow among the coffee shade or itats (thus, in February, C. sulcata was preferred by along roads and fences of the farm. It is unfortu- Spindalis; Carlo et al. 2003). Accordingly, that nate that some efforts to re-shade coffee plantations same month we recorded more foraging of Spin- in Central America are focused on non-fleshy fruit- dalis within the coffee plantation (Fig. 4). ing timber species like Cordia alliodora and Eryth- The most abundant coffee shade tree in our rina berteroana (Montenegro et al. 1997). These coffee farms was I. vera. It is a commonly used species are of relatively little value for the avifauna species in Puerto Rico and elsewhere and is consid- when compared to fleshy-fruited species. When ered an important resource for the avian commu- timber production is a goal, we believe it possible nity, not only for its flowers and fruits, but also as to obtain bird conservation value if plant species a host for arthropods (Wunderle & Latta 1998, that are also valuable for wildlife are employed. Johnson 2000). In our study, bird foraging on I. Some species that could fit such requirements are vera was not as frequent compared to other trees. Guarea guidonia, O. floribunda, and Petitia domin- Inga vera fruits were present during all time periods guensis. For example, Guarea is a relative of ma- at both study sites; however, its presence did not hogany, with very similar wood quality. It has been seem sufficient to attract many frugivores, espe- successfully tested in forestry experiments, at least cially when there were forested habitats nearby with in Puerto Rico (Weaver 2000). Although mahog- attractive fruiting plants available. Our findings any (Swietenia spp.) species grow somewhat taller suggest that, at least in Puerto Rico, the presence than Guarea, differences are not great and the ben- of plant species such as Cecropia, Guarea, Phora- efits that Guarea offer to wildlife are compensatory; dendron, and Schefflera in a coffee plantation could however, management of a coffee farm for optimal increase habitat use for a variety of fruit-eating bird habitat would need more than bird-friendly birds, including migrants. Because congeners are of timber plant species. As our findings indicate, pi- widespread occurrence throughout the Neotropics oneer tree species like Cecropia and Schefflera seem (Gentry 1993), it is possible that such plants will to act as magnets for many bird species. Epiphytes also be important in other coffee growing regions. such as A. scandens and hemiparasites such as Pho- The relative value of a shaded coffee plantation radendron spp. are also important (particularly to as bird foraging habitat is also likely to vary de- Euphonia spp.), as well as shrubby Miconia species. pending on the landscape matrix in which it is Of these plants, Phoradendron spp. are probably the found (Perfecto et al. 1996, Greenberg, Bichier, & most difficult to ‘‘manage’’ since they are hemipar- Sterling 1997). For example, Wunderle and Latta asites and many show strong host specificity (Au- (1998) found that a shaded coffee plantation with kema 2003). Conveniently, in Puerto Rico, I. vera I. vera as the sole shade species was heavily used by is a common host for Phoradendron racemosum and many Neotropical migratory warblers, as well as P. piperoides; C. schreberiana is a common host for resident avifauna in Hispaniola. Wunderle and Lat- P. hexastichum (also used occasionally by P. piperoi- ta (1998), however, point out that those planta- des and P. racemosum); and G. guidonia is a com- tions represented the only forest cover in the study mon host for Phoradendron anceps, P. berteroanum, region. So, even if the habitat was not the most and P. piperoides (T. A. Carlo and J. E. Aukema, suitable to foster bird use, it was the best choice in unpublished data). Hence, having Cecropia, Gua- the area. In contrast, our study sites were found in rea, and I. vera could provide hosts for at least three a landscape in which second-growth forests (mostly species of mistletoes and strengthen the network of abandoned shaded coffee plantations (Marcano- bird-attractive fruiting plant species, at least in Vega et al. 2002) covered over 65 percent of the Puerto Rican coffee plantations. region. Because focal birds had other habitat alter- The phenological characteristics of plant spe- Fruits and Avian Use of Shade Coffee Plantations 613 cies are critical when selecting plant species to cre- present, only the Migratory Bird Center of the ate a bird-attractive coffee farm. Species that fruit Smithsonian Institution certifies ‘‘Bird-Friendly௡’’ repeatedly throughout the year or in individual coffee farms (Smithsonian Migratory Bird Center asynchrony should be favored to ensure the avail- 2004), using a range of criteria known to affect ability of fruits over time. Because fruit preferences bird use of habitats. Criteria for certifying Bird- can be partitioned among bird species, it would be Friendly௡ coffee includes specific requirements on most effective to select a core of fruiting plant spe- canopy height, vertical strata diversity, Inga spp. cies that (1) captures the most visitation and pref- coverage, and shade-tree species diversity; however, erences of the avian community and (2) have ex- currently their criterion for bird-attractive fruiting tended and overlapping fruiting periods. In our plant species remains vague. We suggest that such study, Cecropia, Guarea, Miconia, and Phoraden- programs explicitly recommend the strategic plant- dron fulfilled those characteristics (Carlo et al. ing of fruiting species with extended fruiting sea- 2003). Species of short and synchronous fruiting sons that operate as feeding hubs for resident and periods such as Ocotea spp., P. domingensis, and C. migratory bird species. sulcata can be used as supplements to the core of principal fruiting plant species. Species with open ACKNOWLEDGMENTS foliages such as Cecropia and Schefflera are also ideal shade trees for coffee because they do not block Special thanks go to A. Jordań and J. Saracco for their large amounts of sunlight. Cecropia is also an im- assistance with fieldwork. L. Miranda and crew selected study sites and conducted vegetation surveys. The man- portant resource for fruit bat species (Charles- uscript benefited from reviews by J. M. Wunderle, L. Pet- Dominique 1986). it, A. Cruz, C. Martıńez del Rio, J. Aukema, J. Saracco, Current efforts to promote the marketing of J. Lichstein, and two anonymous reviewers. M. Vives pro- shade-grown coffee, such as the ones led by the vided help with plant taxonomy. Funding was provided by the Puerto Rico Department of Environmental Nat- Smithsonian Migratory Bird Center could further ural Resources, U.S. Fish and Wildlife Service, North improve conservation of resident and migratory Carolina State University, and the Biological Resources birds if fruit preferences are taken into account. At Division, USGS.

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