Seasonal Variation in the Diet of the Bat Anoura caudifer (Phyllostomidae: Glossophaginae) at the Southern Limit of its Geographic Range

Acta Chiropterologica, 15(1): 77–84, 2013 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/150811013X667876 Seasonal variation in the diet of the bat Anoura caudifer (Phyllostomidae: Glossophaginae) at the southern limit of its geographic range MARÍLIA A. S. BARROS1, 2, 4, ANA MARIA RUI3, and MARTA ELENA FABIÁN1 1Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Bento Gonçalves 9500, 91.540-000 Porto Alegre (RS), Brazil 2 Present address: Departamento de Fisiologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Campus Universitário Lagoa Nova s/nº, 59.078-970 Natal (RN), Brazil 3 Departamento de Ecologia, Zoologia e Genética, Instituto de Biologia, Universidade Federal de Pelotas, Campus Universitário Capão do Leão s/nº, CP 354, 96.001-970 Pelotas (RS), Brazil 4Corresponding author: E-mail: barrosmas@gmail.com Glossophagine bats feed mainly on flower products, but often eat also insects and fruits. The composition of their diet may change according to climate seasonality. In the present study we analyzed the diet of the bat Anoura caudifer at the southernmost limit of its geographic distribution, the Atlantic Forest of southern Brazil. We identified food items and plant species consumed by A. caudifer and tested the hypothesis that its diet varies seasonally. We collected fecal material monthly from October 2003 to September 2004 in a day roost of A. caudifer. We obtained a total of 1,166 fecal samples: 1,029 (88%) samples contained pollen, 592 (51%) contained insects, and 196 (17%) contained seeds. The hypothesis that diet varies seasonally was corroborated. There was high consumption of nectar and pollen in all seasons, especially in spring (98%), high consumption of insects mainly in summer and autumn (60%), and high consumption of fruits in winter (41%) and summer (24%). Anoura caudifer consumed pollen and nectar of 10 plant species, mainly of Marcgravia polyantha, and fruits of six species, mainly of Piper gaudichaudianum. Anoura caudifer has primarily a pollinivorous/insectivorous diet at the southern limit of its distribution, and, in contrast to other studies, it also eats fruits at some times of the year. Visits to flowers of 10 species, four of which not matching the syndrome of chiropterophily, and consumption of fruits of six species indicate a generalistic behavior of A. caudifer in the study area. This flexibility may have been crucial to the maintenance of A. caudifer populations at the southern limit of its distribution, and also for the persistence of batpollinated plants in local ecosystems. Key words: Atlantic Forest, Brazil, Eucalyptus, foraging, Marcgravia polyantha, nectar-feeding bat INTRODUCTION Bats of the subfamily Glossophaginae (family Phyllostomidae) are predominantly nectarivorous and pollinate hundreds of plant species in the Neotropics (Vogel, 1969; Fleming et al., 2009). They have many morphological, physiological, and behavioral adaptations for the consumption of pollen and nectar: a protruding rostrum, dental reduction, a long and extensible tongue with papillae at the tip, hovering flight, and the ability of digesting pollen (Howell, 1974b; Freeman, 1995; Herrera and Del Río, 1998; Tschapka and Dressler, 2002; Winter and von Helversen, 2003). Similarly, many plant species have adaptations to attract pollinating bats, such as flowers with dull color, strong smell and nocturnal anthesis, which characterize the syndrome of chiropterophily (Faegri and Van Der Pijl, 1979). The genus Anoura comprises eight species (Muchhala et al., 2005; Simmons, 2005; MantillaMeluk and Baker, 2006). Although these species have different adaptations for nectarivory, they may also include insects and fruits in their diet (Gardner, 1977; Nowak, 1994; Carstens et al., 2002). Most studies on the diet of this genus refer to A. geoffroyi, which is considered a primarily insectivorous species that may also eat pollen, nectar and fruits (Howell, 1974a; Sazima, 1976; Gardner, 1977; Willig et al., 1993; Ortega and Alarcón-D., 2008). Oneyear studies carried out in Mexico, Ecuador, and Brazil reported the presence of pollen and insects in the diet of A. geoffroyi, but no fruits (Pedro and Taddei, 1997; Muchhala and Jarrín-V., 2002; 78 M. A. S. Barros, A. M. Rui, and M. E. Fabián Caballero-Martínez et al., 2009). Fruit consumption has been documented in Costa Rica (Howell and Burch, 1974) and Brazil (Zortéa, 2003). The diet of A. cultrata is probably similar to that of A. geoffroyi, with intensive insect consumption (Gardner, 1977; Tamsitt and Nagorsen, 1982). Anoura fistulata is highly specialized in consuming nectar and pollen from plants which it co-evolved with, and complements its diet with insects (Muchhala et al., 2005; Muchhala, 2006a). Anoura caudifer (E. Geoffroy, 1818), the focus of the present study, has a broad distribution in the Neotropics, from northern South America to southern Brazil and northwestern Argentina (Simmons, 2005). It is a generalistic species that occurs in mesic tropical forests from the sea level to an elevation of 1,500 m a.s.l., and it is frequently captured in several locations within its range (Oprea et al., 2009). Although A. caudifer is a common species with broad geographic distribution, its diet is poorly known. Most information available has been obtained by Pedro and Taddei (1997) in a tropical area of southeastern Brazil, Muchhala and Jarrín-V. (2002) in cloud forests on the western slopes of the Ecuadorian Andes, and Zortéa (2003) in central Brazil. These studies reported mainly the consumption of pollen/nectar and insects. There is only one record of fruit consumption in central Brazil. Most of the information on the diet of A. caudifer is found in pollination studies (Sazima and Sazima, 1987, 1995; Buzato et al., 1994; Sazima et al., 1999; Varassin et al., 2001; Muchhala, 2006b, 2008; Muchhala and Potts, 2007), indicating a relevant role of the species in plant reproduction in the Neotropics. The diet of glossophagine bats may vary throughout the year, with changes in the frequencies of pollen/nectar, fruits, and insects. This variation is related to local seasonality, which influences patterns of resource availability. Studies examining this issue have been carried out mainly in tropical regions where fluctuations in rainfall determine a dry and a rainy season. Seasonal variation in diet has been observed in the six most abundant phyllostomid bat species in the tropical dry forest of Costa Rica (Heithaus et al., 1975), in Glossophaga longirostris in an arid area in the Venezuelan Andes (Soriano et al., 1991), and in Lonchophylla dekeyseri in the Brazilian Cerrado in the mid-western Brazil (Coelho and Marinho-Filho, 2002). In these regions, glossophagine species prefer flower products in the dry season and fruits in the rainy season. Zortéa (2003) found out that Glossophaga soricina eats mainly insects in the dry season and increases fruit ingestion in the rainy season in a Cerrado area of Brazil. In a Costa Rican tropical lowland rainforest, Glossophaga commissarisi shifted to a more frugivorous diet after the main flowering peak (Tschapka, 2004). The present study was carried out in southern Brazil, at the southern limit of the Atlantic Forest (IBGE, 1986). The region has four well-defined seasons, with seasonal temperature fluctuations and evenly distributed rains throughout the year (Sevegnani and Baptista, 1996). Nine phyllostomid bat species are found in the area, including two glossophagines: G. soricina and A. caudifer. The study area is the southernmost point of occurrence known for A. caudifer (Fabián et al., 1999). Our objectives were to analyze the diet of A. caudifer at the southern limit of its geographic range, and to identify the food items and plant species consumed by this species throughout the year. We tested the hypothesis that the diet of A. caudifer varies seasonally in response to temperature fluctuations. MATERIALS AND METHODS Study Area The study was carried out in the Maquiné River Valley, in a private area of the Fundação Estadual de Pesquisa Agropecuária (FEPAGRO), Maquiné, state of Rio Grande do Sul, southern Brazil. The Maquiné River Valley carves into the eastern slope of the Brazilian Serra Geral, close to the Atlantic Ocean; it is very narrow and covers a large altitudinal gradient of almost 900 m in less than 30 km (Sevegnani and Baptista, 1996). The region is located at the southern limit of the stricto sensu Atlantic Forest, in the ‘Floresta Ombrófila Densa’ (dense rainforest) physiognomy (IBGE, 1986). Currently, there seems to be a process of vegetation recovery, as broad areas are occupied by secondary forest in different developmental stages. The region has a Cfa or humid subtropical climate, according to the Köppen system (Moreno, 1961). Based on data from the local meteorological station (1959–1987), the average annual temperature is 20°C; the average temperature in the coldest month (June) is 15.5°C, and in the hottest month (February) it is 24.6°C. The average annual rainfall is 1,661 mm and it is evenly distributed throughout the year (Sevegnani and Baptista, 1996). We studied a colony of A. caudifer that used as a day roost the attic of a masonry garage, with a clay-shingled roof and a wooden ceiling (29°39’32”S, 50°12’46”W). The colony used this day roost throughout the year, and the maximum number of individuals found was 11. The roost was located at the edge of a continuous secondary forest, consisting of a mosaic of forest patches at different successional stages. The surroundings were composed of residential and agricultural areas, which contribute to the occurrence of a high number of cultivated exotic plants. Diet of Anoura caudifer Data Collection and Analysis We visited the roost once a month, from October 2003 to September 2004, to collect fecal samples. We covered approximately 2 m2 of the surface below the daytime perch with a thick plastic film, which was replaced at each visit. We stored each fecal pellet separately in a small plastic bag and considered it as an independent sample. This was possible due to the dry consistency of the feces, which formed pellets. In the laboratory, we examined the fecal samples under a Meiji stereoscopic microscope to identify the food items consumed. We prepared permanent slides for all fecal samples to detect pollen, using glycerinated gelatin (Thomas, 1988). We observed pollen grains under a Zeiss light microscope to identify morphotypes. We identified the seeds and pollen found in feces using a reference collection of fruit and flowers of plant species from the study area, palynological collections, and the help of experts. We considered only the presence or absence of each kind of food in each sample, not the quantity (Voigt et al., 2009). Statistical analyses were conducted using PASW Statistics 18 (Statistical Package for the Social Sciences/SPSS Inc.). We used the following statistical tests: 1. chi-square to test for seasonal variations in the diet of A. caudifer; and 2. residual analysis tests (Haberman, 1973) to identify which seasons were responsible for a significant chi-square statistic. The values of adjusted residuals were compared to the critical value of normal distribution at a significance level of 0.05 (i.e., z = 1.96). RESULTS Diet Composition We collected 1,166 fecal samples and quantified the occurrence of pollen grains, insect parts, and seeds. Pollen grains were present in 1,029 samples (88.2%), insects in 592 samples (50.8%), and seeds in 196 samples (16.8%). These three different food types could be found either alone or together in a sample. The difference among consumption frequencies was statistically significant (χ2 = 1,192.97, d.f. = 2, P < 0.001). 79 different from the average frequency calculated for the entire sample (adjusted residual: summer = 0.2). Insects were the second most important food in spring, summer, and autumn (Fig. 1). The highest frequency of this food type was found in summer (60.1%) and autumn (59.6%), and the lowest in winter (34.5%) (adjusted residuals: summer = 3.7; autumn = 3.4; winter = -5.8). The frequency of insect consumption in spring (47.5%) was not significantly different from that of the entire sample (adjusted residual: spring = -1.4). Among the three food types, fruit consumption showed the highest seasonal variation (Fig. 1). The highest frequency of this item was found in winter (41.3%) and summer (24.0%), and the lowest frequency in autumn (3.3%) and spring (3.5%) (adjusted residuals: winter = 11.7; summer = 3.8; autumn = -6.9; spring = -7.8). Plant Species Anoura caudifer used at least 16 plant species of 12 families: pollen/nectar of ten species, and fruits of six species (Table 1). When only the plant genus could be identified, more than one species could be present in the sample. Only one morphotype of pollen (Sp.1) and one of seed (Sp.2) were not identified (Table 1). We found a significant variation in the number of months in which each of the 16 plant species were present in the diet of A. caudifer, as well as in the frequency of annual consumption (Table 1). The five most important plant species consumed longer and 350 Pollen Seasonal Variation in Diet The diet of A. caudifer showed marked seasonal variation. There were significant differences in the consumption of the three types of food between seasons (pollen: χ2 = 164.99, P < 0.001; insects: χ2 = 47.09, P < 0.001; fruits: χ2 = 198.22, P < 0.001; d.f. = 3 for each test). The most common item in all seasons was pollen (Fig. 1). The highest frequency of this resource was found in spring (98.2%) and autumn (95.6%), and the lowest frequency in winter (66.3%) (adjusted residuals: spring = 6.8; autumn = 4.4; winter = -12.2). The consumption frequency of pollen/ nectar in summer (88.5%) was not significantly Number of samples 300 Insects 250 Fruits 200 150 100 50 0 Spring Summer Autumn Winter FIG. 1. Food types identified in fecal samples of A. caudifer in different seasons, from October 2003 to September 2004, in an Atlantic Forest area of southern Brazil. Spring — October, November, and December; Summer — January, February, and March; Autumn — April, May, and June; Winter — July, August, and September 80 M. A. S. Barros, A. M. Rui, and M. E. Fabián TABLE 1. Number of months, number of samples (n), and frequency of plant species (%) in the diet of A. caudifer, from October 2003 to September 2004, in an Atlantic Forest area of southern Brazil Plant species Marcgravia polyantha Inga sp. Pseudobombax grandiflorum Eucalyptus sp. Vriesea sp. Piper gaudichaudianum Celtis sp. Abutilon sp. Sp.1 Ficus cestrifolia Cecropia glaziovii Sp.2 Ficus luschnathiana Magnolia ovata Roupala montana Cecropia pachystachya Family Marcgraviaceae Leguminosae Malvaceae Myrtaceae Bromeliaceae Piperaceae Cannabaceae Malvaceae – Moraceae Urticaceae – Moraceae Magnoliaceae Proteaceae Urticaceae at higher frequency provided the bats with flower products. The only plant consumed in all 12 months of the study was Marcgravia polyantha. Fruits of Piper gaudichaudianum were found longer and at the highest frequency. All other plant species were present in the diet of A. caudifer for fewer six months, at a frequency below 6% (Table 1). Spring was the season with the largest number of plant species providing pollen/nectar (10 species), followed by summer (8 species), and both autumn and winter (6 species each). Seasonality marked the consumption of flower products by A. caudifer. Only M. polyantha, Inga sp., Pseudobombax grandiflorum, and Eucalyptus sp. were consumed throughout the year. Fruits from five plant species were consumed in summer, two species in autumn and winter, and only one in spring. No fruit species was consumed in all seasons (Table 2). DISCUSSION Diet Composition The diet of A. caudifer at the southern limit of its range is composed of pollen/nectar, insects, and fruits. The present study is the first to report regular fruit consumption in this species. In the Brazilian Cerrado and the cloud forest of Ecuador, A. caudifer consumed only flower products and insects, and there was no evidence of fruit consumption in 12 months of sampling (Pedro and Taddei, 1997; Muchhala and Jarrín-V., 2002). In an Atlantic Forest area of southeastern Brazil, ten specimens of Resource pollen/nectar pollen/nectar pollen/nectar pollen/nectar pollen/nectar fruit pollen/nectar pollen/nectar pollen/nectar fruit fruit fruit fruit pollen/nectar pollen/nectar fruit Months 12 10 11 8 6 6 5 4 3 5 3 2 1 2 3 1 n 881 324 312 236 206 146 66 39 32 21 14 14 10 9 7 3 % 75.6 27.8 26.8 20.2 17.7 12.5 5.7 3.3 2.7 1.8 1.2 1.2 0.9 0.8 0.6 0.3 A. caudifer had fragments of insects and pollen in their guts, but showed no evidence of fruit consumption (Sazima, 1976; Teixeira and Peracchi, 1996). A review on the plants used as food by A. caudifer revealed 32 records of nectarivory but none of frugivory (Fabián et al., 2008). Seasonal Variation in Diet We corroborated our hypothesis that the diet of A. caudifer varies seasonally in southern Brazil. Seasonal variation in the consumption of flower products and fruits may be attributed to the phenology of the food-plants. This hypothesis must be further tested, as we did not collect phenological data in the area because the diet of the species was still unknown. However, studies carried out in other regions reported that the diet of glossophagine bats varies seasonally from predominantly nectarivorous to frugivorous, following the flowering and fruiting peaks of plant species throughout the year (Soriano et al., 1991; Coelho and Marinho-Filho, 2002; Tschapka, 2004). The basis of the diet of A. caudifer in the region is composed of flower products that are frequently consumed (>88%) in all seasons, though less frequently in winter (66.3%). Probably, winter is the season with the lowest availability of flower products to A. caudifer in the area, both in number of species in blossom and in total availability of resources. In winter, we found pollen of only six plant species in fecal samples of A. caudifer, whereas in spring we found the pollen of ten species. The frequency of pollen from all plants Diet of Anoura caudifer 81 TABLE 2. Number of samples (n) and frequency (%) of plant species in the diet of A. caudifer in different seasons, from October 2003 to September 2004, in an Atlantic Forest area of southern Brazil Plant species Pollen Marcgravia polyantha Inga sp. Pseudobombax grandiflorum Eucalyptus sp. Vriesea sp. Celtis sp. Abutilon sp. Sp.1 Magnolia ovata Roupala montana Fruits Piper gaudichaudianum Ficus cestrifolia Cecropia glaziovii Sp.2 Ficus luschnathiana Cecropia pachystachya Spring (n = 343) n % Summer (n = 296) n % Autumn (n = 275) n % Winter (n = 252) n % 337 93 47 5 6 53 11 26 6 1 98.3 27.1 13.7 1.5 1.7 15.5 3.2 7.6 1.7 0.3 212 108 15 12 163 11 – 6 3 – 71.6 36.5 5.1 4.1 55.1 3.7 – 2.0 1.0 – 212 86 162 153 37 2 – – – – 77.1 31.3 59.0 55.6 13.5 0.7 – – – – 120 37 88 66 – – 28 – – 6 47.6 14.7 35.0 26.2 – – 11.1 – – 2.4 – 12 – – – – – 3.5 – – – – 50 9 7 16.9 3.0 2.4 – 3.4 1.0 2 – 7 – – – 0.7 – 2.5 – – – 94 – – 14 – – 37.3 – – 5.6 – – species consumed decreased in winter, except for Abutilon sp. (11.1%). The consumption of pollen/ nectar by A. caudifer in southeastern Brazil is high, with a frequency of 62.5% in the dry season and 83.3% in the rainy season (Pedro and Taddei, 1997); in the Ecuadorian Andes the consumption of pollen/nectar is also high, with an annual frequency of 91% (Muchhala and Jarrín-V., 2002). Anoura caudifer may consume fruits opportunistically, at moments of high fruit availability or low availability of flower products. The high consumption of fruits in winter (41.3%), mainly of P. gaudichaudianum (37.3%), may be related to a low availability of flower products combined with a fruiting peak of this species. In summer, the bats consumed fruits of five plant species with a frequency of 24%. Probably, fruits of different plant species are abundant in summer, and do not require much time and energy to be located and consumed. Fruit consumption in A. caudifer may be considered occasional and opportunistic, as this species has only adaptations for nectarivory and pollinivory. In addition, from a physiological perspective, bats of the subfamily Glossophaginae have lower energy assimilation from a fruit diet compared to a nectar diet (Kelm et al., 2008). Results of the present study and the scarce information available in the literature suggest that insects are an important food of A. caudifer, a complement to its primarily nectarivorous/pollinivorous 10 3 diet. The proportion of insects in the samples was higher in summer and autumn (about 60%), whereas only 34.5% of the samples contained insects in winter. Such variation may also be attributed to the availability of this resource, as insect populations may be reduced in winter (Wolda, 1988). The study area has four well-defined seasons with variations in temperature. Such climate seasonality may influence the phenology of food-plants and insects. Anoura caudifer probably adopts an opportunistic behavior in the area, feeding on a combination of nectar/pollen, insects, and fruits according to its nutritional needs and the seasonal availability of each resource. Glossophagines have a markedly seasonal diet in different biomes of South and Central America, which is influenced by rainfall seasonality (Coelho and Marinho-Filho, 2002; Tschapka, 2004). There is a trend of higher pollen/nectar and insect consumption in the dry season and higher fruit consumption in the rainy season, a pattern that is closely related to changes in the availability of different types of food throughout the year (Fleming et al., 1972; Heithaus et al., 1975; Soriano et al., 1991; Ruiz et al., 1997; Tschapka, 2005). In the Brazilian Cerrado, a region with two distinct seasons in terms of rainfall, A. caudifer did not have a marked seasonality in diet, but showed a trend of higher insect consumption in the dry season (Pedro and Taddei, 1997). 82 M. A. S. Barros, A. M. Rui, and M. E. Fabián Plant Species Anoura caudifer used 16 different plant species in the study area. In Brazil, there are records of consumption of flowers of 25 plant species, mainly of the genera Vriesea (Bromeliaceae) and Bauhinia (Fabaceae) (Fabián et al., 2008). Although in the study area A. caudifer consumed fruits and flower products from a large set of plants, only few species were used for long periods and at high frequencies. Marcgravia polyantha was the species with the highest annual consumption frequency (75.6%) and the only species visited throughout the year. Many species of Marcgravia are chiropterophilous and pollinated by glossophagine bats (Tschapka and von Helversen, 1999; Zusi and Hamas, 2001; Tschapka et al., 2006), including A. caudifer (Sazima and Sazima, 1980; Dressler and Tschapka, 2002; Herrera et al., 2003). Anoura caudifer has been recognized as a pollinator of M. polyantha in an Atlantic Forest area in southeastern Brazil (Sazima et al., 1999). However, the present study is the first to describe the importance of M. polyantha in the diet of a glossophagine bat, suggesting that the species is an important resource in the Atlantic Forest. Flower products of Inga sp., P. grandiflorum, and Eucalyptus sp. were consumed throughout the year with an annual frequency higher than 20%. Pseudobombax grandiflorum and Eucalyptus sp. were important resources for A. caudifer in autumn and winter, seasons when the number of species present in feces is low, as well as the frequency of M. polyantha. Species of Inga and Pseudobombax have some characteristics of chiropterophily (Faegri and Van Der Pijl, 1979). A study carried out in an Atlantic Forest area in south-eastern Brazil pointed out A. caudifer as an effective pollinator of P. grandiflorum (Fischer et al., 1992). Eucalyptus species are exotic and cultivated in large-scale in Rio Grande do Sul. In the study area, there were no Eucalyptus plantations, although some individuals have been planted in the past for ornamental purposes. Eucalyptus sp. provides a highly seasonal nectar production and is usually pollinated by insects and birds (Faegri and Van Der Pijl, 1979). Anoura caudifer visited flowers of Vriesea sp. in spring, summer, and autumn, though their relative importance in its diet was higher in summer, when they were present in 55% of the feces examined. Probably, there were different species of Vriesea sp. in the study area, which had a combined annual frequency of 17.7%. Some Vriesea species are chiropterophilous and pollinated by glossophagine bats (Vogel, 1969). In the Atlantic Forest of southeastern Brazil, there are records of A. caudifer pollinating five species of Vriesea (Sazima and Sazima, 1995; Sazima et al., 1999; Fabián et al., 2008). In Brazilian rainforest, Abutilon spp. have intermediate characteristics between chiropterophily and ornitophily: the flowers are yellow, pink or purple, open at dusk and remain bowl-shaped through the night, and from morning they narrow the entrance and adopt a bell-shape (Buzato et al., 1994). These flowers are pollinated by hummingbirds during the day and by bats at night, and there are records of pollination of two species of Abutilon by A. caudifer in the Atlantic Forest (Buzato et al., 1994; Sazima et al., 1999). The other flowers identified in the diet of A. caudifer had an annual consumption frequency lower than 6%. These species did not have characteristics of chiropterophily and are probably not pollinated by glossophagine bats. The use of these species may reflect an opportunistic behavior of the bats when the availability of other flowers is low. The fruits consumed by A. caudifer (Ficus, Piper, and Cecropia) are all chiropterochorous and broadly used by phyllostomid bats, including glossophagine species (Fabián et al., 2008; Lobova et al., 2009). Both species of Ficus have globose infructescences ≈ 1 cm in diameter, P. gaudichaudianum have spicate and erect infructescences ≈ 7 × 0.5 cm, and the infructescences of Cecropia species are clusters of spikes ≈ 8–15 × 1 cm. In the study area, the five fruit species consumed by A. caudifer comprise the basis of the diet of frugivorous bats, mainly those of the genera Artibeus and Sturnira (A. M. Rui, unpublished data). Anoura caudifer may be also a seed disperser together with primarily frugivorous species, mainly during fruiting peaks. Final Considerations The diet of A. caudifer at the southern limit of its distribution in southern Brazil may be considered nectarivorous, pollinivorous, and insectivorous. A flexible diet had already been observed in this species in other areas (Pedro and Taddei, 1997; Muchhala and Jarrín-V., 2002). However, in southern Brazil, the diet of A. caudifer is complemented with fruits, mainly at times of nectar shortage or fruit abundance. Anoura caudifer seems to have a generalistic foraging behavior, with a diet that comprises at least 16 plant species and insects. Opportunism in the use of flower products and the inclusion of fruits in the diet may have been Diet of Anoura caudifer crucial for the persistence of A. caudifer populations at the southern limit of its distribution during deforestation and habitat fragmentation in the past decades. ACKNOWLEDGEMENTS Fundação Estadual de Pesquisa Agropecuária do Estado do Rio Grande do Sul (FEPAGRO) gave us a permit to carry out the study within the Centro de Pesquisa FEPAGRO Litoral Norte, Maquiné. The agronomic engineers Guido Sander (in memoriam) and Rodrigo Favreto provided us with logistic support in the field. Ari Delmo Nilson helped us to collect pollen from plants at Jardim Botânico de Porto Alegre, which were very useful for our reference collection. Maria Luisa Lorscheitter (Departamento de Botânica, Universidade Federal do Rio Grande do Sul) and Soraia Girardi Bauermann (Laboratório de Palinologia, Universidade Luterana do Brasil) identified pollen, and Paulo Brack (Departamento de Botânica, Universidade Federal do Rio Grande do Sul) identified plants. Sidia M. Callegari-Jacques (Departamento de Genética, Universidade Federal do Rio Grande do Sul) helped with the statistical analysis. Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) granted A. M. Rui a Recent Doctoral fellowship. LITERATURE CITED BUZATO, S., M. SAZIMA, and I. SAZIMA. 1994. Pollination of three species of Abutilon (Malvaceae) intermediate between bat and hummingbird flower syndromes. 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