Abstract

The frugivorous phyllostomid bat genera Artibeus , Carollia and Sturnira are important seed dispersers in the Neotropics, and exhibit supposed preferences for fruits of the genus Ficus , Piper and Solanum , respectively. We performed a quantified literature review to test the hypothesis that interactions with plants are consistent throughout the bats´ geographic ranges. Through an extensive literature review we obtained a total of 4,448 records of fruit consumption from 180 publications. To test which fruits were most frequently consumed across the Neotropical region and in each of its component countries these data were organized by bat species and country. In general, considering the 176 botanical genera eaten by these bats, the results showed a high consumption frequency of Ficus (24.0%) by Artibeus , Piper (38.7%) by Carollia and Solanum (31.0%) by Sturnira . Additionally, our findings support the hypothesis of diet consistency throughout the geographic range of these genera. We suggest that this consistency is related to the wide distribution of the study groups (both bats and plants), the phenology of the zoochoric species consumed, the spatial fidelity of bats and the foraging patterns of the different bat species.

Keywords
Diet; frugivory; fruit phenology; geographic distribution; Phyllostomidae

Resumo

Os filostomídeos frugívoros Artibeus , Carollia e Sturnira são importantes dispersores de sementes na região Neotropical, se destacando por possuírem uma suposta preferência por frutos dos gêneros Ficus , Piper e Solanum , respectivamente. Nós realizamos uma metanálise para testar a hipótese de que as interações entre esses morcegos e plantas são consistentes ao longo de toda sua distribuição geográfica. Por meio de uma extensa revisão bibliográfica, foram compilados 4.448 registros de consumo de frutos provenientes de 180 publicações. Estes dados foram organizados por espécie de morcego e país, testando quais gêneros de frutos foram mais frequentes na região neotropical como um todo e em cada um dos seus países componentes. Num panorama geral, os resultados demonstraram alta frequência no consumo de Ficus (24,0%) por Artibeus , Piper (38,7%) por Carollia e Solanum (31,0%) por Sturnira , considerando 176 gêneros botânicos citados. O estudo corrobora, assim, a hipótese da consistência da dieta desses morcegos ao longo de toda a sua distribuição geográfica, sendo esta relacionada à ampla distribuição dos grupos (morcegos e plantas) envolvidos, à fenologia das espécies zoocóricas consumidas e à fidelidade espacial dos morcegos, esta, por sua vez, moldada pela capacidade de voo das diferentes espécies.

Palavras-chave
Dieta; distribuição geográfica; fenologia; frugivoria; Phyllostomidae

The family Phyllostomidae comprises 160 species that are widely distributed in the Neotropics, with 34 genera and approximately 120 species recorded as frugivorous and/or nectivorous (Simmons, 2005Simmons, N. B. 2005. Order Chiroptera, p.312-529. In: Wilson, D. E. & Reeder, D. M. eds. Mammal species of the world: A taxonomic and geographic reference. Baltimore, Johns Hopkins University Press. 2142p.; Gardner, 2008Gardner, A. L. 2008. Mammals of South America, Volume 1: Marsupials, Xenarthrans, Shrews, and Bats.Chicago, London, University of Chicago Press. 690p.). Members of this family are noted for their ecological functions, acting as controllers of insect populations, predators of small vertebrates and especially pollinators and seed dispersers (e.g.Fleming, 1988_____. 1988. The short-tailed fruit bat: A study in plant-animal interactions. Chicago, University Chicago Press. 380p.).

Since the 1930s frugivorous phyllostomids have been recognized as one of the most efficient mammalian seed dispersers in tropical forests (Ridley, 1930Ridley, H. N. 1930. The dispersal of plants throughout the world. Ashford, L. Reeve and Co., Ltd. 774p.). These animals feed on ripe fruit and do not generally destroy the seeds, passing them intact through the digestive system, defecating in flight (Charles-Dominique, 1991Charles-Dominique, P. 1991. Feeding strategy and activity budget of the frugivorous bat Carollia perspicillata (Chiroptera: Phyllostomidae) in French Guiana. Journal of Tropical Ecology 7:243-256.; Dumont, 2003Dumont, E. R. 2003. Bats and Fruit: An ecomorphological ap proach. In: Kunz, T. H. & Fenton, B. eds. Bat Ecology. Chicago, University of Chicago Press, p. 398-429.), which results in a widely spread seed dispersal.

Artibeus Leach, 1821, Carollia Gray, 1838 and Sturnira Gray, 1842, are among the most abundant and diverse bat genera in the Americas (Kalko & Handley, 2001Kalko, E. K. V. & Handley Jr. C. O. 2001. Neotropical bats in the canopy: diversity, community structure and implications for conservation strategies. Plant Ecology 153:319-333.; Gardner, 2008Gardner, A. L. 2008. Mammals of South America, Volume 1: Marsupials, Xenarthrans, Shrews, and Bats.Chicago, London, University of Chicago Press. 690p.). They have great ecological importance due to their dispersal of pioneer plants (Fleming, 1988_____. 1988. The short-tailed fruit bat: A study in plant-animal interactions. Chicago, University Chicago Press. 380p.; Henry & Jouard, 2007Henry, M. & Jouard, S. 2007. Effect of bat exclusion on patterns of seed rain in tropical rainforest in French Guiana. Biotropica 39:510-518.) and according to several authors (e.g.Fleming, 1988_____. 1988. The short-tailed fruit bat: A study in plant-animal interactions. Chicago, University Chicago Press. 380p.; Kalko et al ., 1996Kalko, E. K. V.; Handley Jr. C. O. & Handley, D. 1996. Organization, diversity and long-term dynamics of a Neotropical bat com munity. In: Cody, M. L. & Smallwood, J. A. eds. Long-term studies of vertebrate communities.New York, Academic Press, p. 503-553.; Wendeln et al., 2000Wendeln, M. C.; Runkle, J. R. & Kalko, E. K. V. 2000. Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica 32:489-501.; Mikich, 2002Mikich, S. B. 2002. A dieta dos morcegos frugívoros (Mammalia, Chiroptera, Phyllostomidae) de um pequeno remanescente de Floresta Estacional Semidecidual do sul do Brasil. Revista Brasileira de Zoologia 19:239-249.; Mello et al., 2008Mello, M. A. R.; Kalko, E. K. V. & Silva, W. R. 2008. Movements of the bat Stu rnira lilium and its role as a seed disperser of Solanaceae in the Brazil ian Atlantic Forest. Journal of Tropical Ecology 24:225-228.; Andrade et al., 2013Andrade, T. Y.; Thies, W.; Rogeri, P. K.; Kalko, E. K. V. & Mello, M. A. R. 2013. Hierarchical fruit selection by Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae). Journal of Mammalogy 94:1094-1101.) predominantly consume fruits of Ficus L. (Moraceae), Piper L. (Piperaceae) and Solanum L. (Solanaceae), respectively.

Along this same line of reasoning, studies by Mikich et al. (2003Mikich, S. B.; Bianconi, G. V.; Maia, B. H. L. N. S. & Teixeira, S. D. 2003. Attraction of the fruit-eating bat Carollia p erspicillata to Piper ga udichaudianum essential oil. Journal of Chemical Ecology 29:2379-2383.) and Bianconi et al. (2007Bianconi, G. V.; Mikich, S. B.; Teixeira, S. D. & Maia, B. H. L. N. S. 2007. Attraction of fruit-eating bats with essential oils of fruits: a potential tool for forest restoration. Biotropica 39:136-140.) addressed the use of smell in finding food, and showed positive results in the attraction of the genera Carollia and Artibeus with the provision of essential oils extracted from Piper and Ficus fruits. The results proved so effective that it was possible to propose such essential oils as a tool for the recovery of degraded areas, due to the associated increase in seed rain in these locations. However, monitoring the recruitment of seedlings is needed to evaluate the efficiency of the method (see Reid & Holl, 2013Reid, J. L. & Holl, K. D. 2013. Arrival ≠ Survival. Restoration Ecology 21:153-155.).

The preference of Artibeus , Carollia and Sturnira for Ficus , Piper and Solanum fruits, respectively, is commonly cited and a recent study (Andrade et al., 2013Andrade, T. Y.; Thies, W.; Rogeri, P. K.; Kalko, E. K. V. & Mello, M. A. R. 2013. Hierarchical fruit selection by Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae). Journal of Mammalogy 94:1094-1101.) has demonstrated these preferences by combining a literature database with field experiments. Nevertheless, how bat-plant relationships behave across the spatial distribution of these three bat genera has not been investigated. It is known, however, that the phyllostomids in question are exclusively Neotropical (Gardner, 2008Gardner, A. L. 2008. Mammals of South America, Volume 1: Marsupials, Xenarthrans, Shrews, and Bats.Chicago, London, University of Chicago Press. 690p.) and that the three fruit genera are spread across much of the world, with Ficus (800 species) and Piper (approximately 1000 species) being pantropical and Solanum (approximately 1500 species) distributed in all continents of the globe (Jaramillo & Manos, 2001Jaramillo, M. A. & Manos, P. S. 2001. Phylogeny and patterns of floral diversity in th e genus Piper (Piperaceae). American Journal of Botany 88:706-716.; Shanahan et al., 2001Shanahan, M.; So, S.; Compton, S. G. & Corlett, R. 2001. Fig-eating by vertebrate frugivores: a global review. Biological Reviews 77:529-572.; Knapp et al., 2004Knapp, S.; Bohs, L.; Nee, M. & Spooner, D. M. 2004. Solanaceae: a model for linking genomics and biodiversity. Comparative and Functional Genomics 5:285-291.). Ficus is intraspecifically asynchronous, producing an abundance of ripe fruit in the same individual, which is generally available for only a few weeks (Morrison, 1978Morrison, D. W. 1978. Influence of habitat on the foraging distances of the fruit bat, Artibeu s jamaicensis. Journal of Mammalogy 59:622-624.). In contrast, Piper and Solanum are synchronous and provide lower amounts of fruit per night, but over a longer period (Dumont, 2003Dumont, E. R. 2003. Bats and Fruit: An ecomorphological ap proach. In: Kunz, T. H. & Fenton, B. eds. Bat Ecology. Chicago, University of Chicago Press, p. 398-429.).

The objective of the present study is to fill this gap through a quantified literature review of the interactions between these bat and plant genera throughout the Neotropics. We use these widely distributed genera to test the hypothesis of consistency of diet across the geographic range, which is associated with the broad distribution of the groups (bats and plants), the phenology of the species consumed and also the spatial fidelity of the phyllostomids.

MATERIAL AND METHODS

The study consisted of a literature review and data compilation of fruit consumption by representatives of the genera Artibeus , Carollia and Sturnira throughout their distributional range. Therefore, we performed a search in Web of Science (http://apps.webofknowledge.com) with the following keywords and combinations thereof: "Artibeus ", "Carollia ", "Sturnira ", "Chiroptera", "bat", "diet", "fruit"", "frugivory" and "plant". We also used information obtained from the Database of Neotropical Bat/Plant Interactions (2013)Database of Neotropical Bat/Plant Interactions. 2013. Available at <Available at http://www.nybg.org/botany/tlobova/mori/batsplants/database/dbase_main.htm >. Accessed on 30 December 2013.
http://www.nybg.org/botany/tlobova/mori/... , a database created in 2001 with information on dispersal and pollination by Neotropical bats.

The collected information was organized in a spreadsheet with the following entries: bat (species and/or genus), fruit consumed (species, genus and/or family), location, country, recording method and source. Each entry of a plant species (or genus/family when species unknown) accounted for one record. Records could be based on direct observations, analysis of stomach contents and/or analysis of fecal samples.

To identify the fruit genera with a significantly greater number of consumption records for each bat genus a chi-square test was used, with a α significance probability of P < 0.05. The same procedure was used to compare the number of records among countries. Prior analyses, all duplicate information, derived from compilations of primary data sources (i.e. review articles, studies referring to data collected and published in other sources), were excluded.

The data were first tabulated as cited in the source and the taxonomy subsequently standardized according to Simmons (2005Simmons, N. B. 2005. Order Chiroptera, p.312-529. In: Wilson, D. E. & Reeder, D. M. eds. Mammal species of the world: A taxonomic and geographic reference. Baltimore, Johns Hopkins University Press. 2142p.) for bats, and following Forzza et al. (2013Forzza, R. C.; Leitman, P. M.; Costa, A. F.; Carvalho Jr. A. A.; Peixoto, A. L.; Walter, B. M. T.; Bicudo, C.; Zappi, D.; Costa, D. P.; Lleras, E.; Martinelli, G.; Lima, H. C.; Prado, J.; Stehmann, J. R.; Baumgratz, J. F. A.; Pirani, J. R.; Sylvestre, L.; Maia, L. C.; Lohmann, L. G.; Queiroz, L. P.; Silveira, M.; Coelho, M. N.; Mamede, M. C.; Bastos, M. N. C.; Morim, M. P.; Barbosa, M. R.; Menezes, M.; Hopkins, M.; Secco, R.; Cavalcanti, T. B. & Souza, V. C. 2013. Lista de Espécies da Flora do Brasil. Available at <Available at http://floradobrasil.jbrj.gov.br/2013 >. Accessed on 30 December 2013.
http://floradobrasil.jbrj.gov.br/2013... ) for native Brazilian plant species and The Plant List (2013)The Plant List. 2013. Available at <Available at http://www.theplantlist.org >. Accessed on 23 October 2013.
http://www.theplantlist.org... for other plant species included in the spreadsheet.

Maps were made using the political boundaries of the countries of the Neotropical region, with the distribution of the fruit genera consumed (cf . Jaramillo & Manos, 2001Jaramillo, M. A. & Manos, P. S. 2001. Phylogeny and patterns of floral diversity in th e genus Piper (Piperaceae). American Journal of Botany 88:706-716. - Piper , Knapp et al., 2004Knapp, S.; Bohs, L.; Nee, M. & Spooner, D. M. 2004. Solanaceae: a model for linking genomics and biodiversity. Comparative and Functional Genomics 5:285-291. - Solanum , Lobova et al., 2003Lobova, T. A.; Mori, S. A.; Blanchard, F.; Peckham, H. & Charles-Dominique P. 2003Cecropia as a food resource for bats in French Guiana and the significance of fruit structure in seed dispersal and longevity. American Journal of Botany 90:388-403. - Cecropia , Shanahan et al., 2001Shanahan, M.; So, S.; Compton, S. G. & Corlett, R. 2001. Fig-eating by vertebrate frugivores: a global review. Biological Reviews 77:529-572. - Ficus ), which was then overlaid on that of the bat genera, following Gardner (2008Gardner, A. L. 2008. Mammals of South America, Volume 1: Marsupials, Xenarthrans, Shrews, and Bats.Chicago, London, University of Chicago Press. 690p.). The maps show the Wallaceana configuration of the Neotropical region (Cox, 2001Cox, C. B. 2001. The biogeographic regions reconsidered. Journal of Biogeography 28:511-523.). The distribution of both fruits and bats was presented at the scale of the whole country, regardless of whether their documented coverage included all or only a portion of that territory. This decision was made due to the lack of detailed information presented in most of the sources consulted. We selected only the most common fruit genera consumed by each bat genera for mapping.

RESULTS

The literature review resulted in 180 studies and 4,448 records of fruit consumption by the three bat genera. Of these, 3,243 were used in analyzes and 1,205 were excluded as they were duplicate records reported by different sources. Altogether, 176 genera from 62 botanical families were reported. A total of 22 bat species were recorded for Artibeus (N=11), Carollia (N= 5) and Sturnira (N= 6).

All three studied bats were found to consume a wide range of fruit genera and families: Artibeus consumed fruit from 51 families, 135 genera and 268 species, Carollia from 44 families, 78 genera and 220 species, and Sturnira from 32 families, 54 genera and 165 species. Nevertheless, almost 24.0% (n= 376) of all records for Artibeus were represented by Ficus (χ ²= 292.41, P<0.00001). The same was true for 38.7% (n= 425) of all records for Carollia , which belonged to Piper (χ ²= 1183.63, P<0.00001) and 31.0% (n=162) of all records for Sturnira , which were represented by Solanum (χ ²= 247.17, P<0.00001). Cecropia Loefl. (Urticaceae) was the second (Artibeus ) or third (Carollia and Sturnira ) most frequently consumed fruit genus by these bats (Fig. 1).

When the geographic distribution of these four fruit genera was superimposed on that of the three bat general (Fig. 2), considerable overlap was found, although bats do not occupy all Neotropical areas where these fruit are available.

Fig. 1
Number of records for the four fruit genera most frequently consumed by Artibeus , Carollia and Sturnira (total number of records for each bat species) based on literature review.

Fig. 2
Distribution of three bat genera (Artibeus , Carollia and Sturnira - solid gray) and the four most frequent plant genera (Cecropia , Ficus , Piper and Solanum - dotted pattern) in their diet in the Neotropical region. Sources: bat distribution follows Gardner (2008); plant distribution follows Jaramillo & Manos (2001) for Piper ; Knapp et al. (2004) for Solanum , Lobova et al. (2003) for Cecropia ; Shanahan et al. (2001) for Ficus.

When the data were analyzed by country, Ficus was the most consumed fruit species by Artibeus in Bolivia, Brazil, Costa Rica, Cuba, Guatemala, Mexico and Panama. However, when compared to the other fruit genera consumed the difference was significant only in countries with a large total number of fruit consumption records. This was true for Brazil (n= 924), Costa Rica (n= 638), Panama (n= 304) and Mexico (n= 205), but not for French Guiana (n= 556), where the consumption of fruits from the genus Cecropia predominated (Tab. I).

Piper was the genus most consumed by Carollia in Brazil, Costa Rica, Guatemala, Guyana, Mexico, Panama, Peru, Bolivia and Mexico, with the latter two only being non-significant (Tab. I). Solanum was the most consumed fruit genus by Sturnira in Argentina, Bolivia, Brazil, French Guiana, Mexico and Peru, whereas Piper was more frequently consumed in Costa Rica and Guatemala (Tab. I).

The majority of the most intensively sampled countries showed more records of the preferred plant genera, while those countries with fewer records and publications did not show the pattern observed for the Neotropics (Fig. 1 and Tab. I). Among the latter (all with <5 studies) were the French Antilles, Colombia, El Salvador, Guyana, Jamaica, Puerto Rico, Trinidad and Tobago, Uruguay and Venezuela (Tab. I).

DISCUSSION

Our findings confirm consistency in the consumption of Ficus , Piper and Solanum fruits throughout the Neotropical range of Artibeus , Carollia and Sturnira, respectively. However, in some countries, this pattern was not evident, probably due to the small number of studies on the diet of bats conducted there, as in most regions with a large sampling effort (with the exception of French Guiana) the pattern was consistent.

The exclusively Neotropical pioneer genus Cecropia (Lobova et al., 2003Lobova, T. A.; Mori, S. A.; Blanchard, F.; Peckham, H. & Charles-Dominique P. 2003Cecropia as a food resource for bats in French Guiana and the significance of fruit structure in seed dispersal and longevity. American Journal of Botany 90:388-403.) was among the four most commonly consumed genera by the bats, particularly Artibeus . This is probably related to its phylogenetic proximity with the family Moraceae (Zhang et al. , 2011Zhang S.; Soltis, D. E.; Yang, Y.; Li, D. & Yi, T. 2011. Multi-gene analysis provides a well-supported phylogeny of Rosales. Molecular Phylogenetics and Evolution 60:21-28.), the family that includes Ficus . Other genera appeared to be more frequently consumed within certain regions, such as Vismia Vand. (Hypericaceae) in Brazil and Panama, Spondias L. (Anacardiaceae) in Cuba, El Salvador and Panama, and Philodendron Schott (Araceae) in French Guiana.

Some of the species (Carica papaya L. and Syzygium jambos (L.) Alston, for example) consumed by these bats are exotic and their consumption and subsequent dispersion may impact native flora (Minor & Gardner, 2011Minor, E. S. & Gardner, R. H. 2011. Landscape connectivity and seed dispersal characteristics inform the best management strategy for exotic plants. Ecological Applications 21:739-749.; Voigt et al., 2011Voigt, F. A.; Farwig, N. & Johnson, S. D. 2011. Interactions between the invasive tree Mel ia azedarach (Meliaceae) and native frugivores in South Africa. Journal of Tropical Ecology 27:355-363.). Bats seem to respond positively to fruit availability (Lobova et al., 2009Lobova, T. A.; Geiselman, C. K. & Mori, A. S. 2009. Seed dispersal by bats in the Neotropics New York, New York Botanical Garden Press. 465p.), reinforcing the need for planning in both urban and rural areas to protect native flora from invasions (Barros et al., 2006Barros, R. S. M.; Bisaggio, E. L. & Borges, R. C. 2006. Morcegos (Mammalia, Chiroptera) em fragmentos florestais urbanos no município de Juiz de Fora, Minas Gerais, sudeste do Brasil. Biota Neotropica 6:1-6.).

Frugivory is a facultative mutualistic interaction as it benefits the consumer (which gains energy and nutrients) and the plant, which has its propagules transported far from the parent plant (Boucher et al., 1982Boucher, D. H.; James, S, & Keeler, K. H. 1982. The Ecology of Mutualism. Annual Review of Ecology, Evolution and Systematics 13:315-347.). According to some authors, species with broad geographic ranges experience different pressures depending on their location, thereby establishing different interactions and developing geographically distinct specializations (Thompson, 2005Thompson, J. N. 2005. The geographic mosaic of coevolution Chicago, University of Chicago Press . 400p.; Mello et al., 2011Mello, M. A. R.; Marquitti, F. M. D.; Guimarães Jr. P. R.; Kalko, E. K. V.; Jordano, P. & Aguiar, M. A. M. 2011. The missing part of seed dispersal networks: structure and robustness of bat-fruit interactions. Plos One 6:1-10.). However, in the case of the bats studied, it is clear that regardless of the climatic, geomorphologic, and floristic differences found throughout the Neotropics and all the plant diversity available (90,000 Neotropical plant species according to Gentry, 1982Gentry, A. H. 1982. Neotropical floristic diversity: phytogeographical connections between Central and South America, pleistocene climatic fluctuations, or an accident of the andean orogeny? Annals of the Missouri Botanical Garden 69:557-593.), the consumption of some fruit genera remained relatively unchanged. In equatorial Mexico, for example, these bats fed mainly on Ficus , Piper and Solanum (Olea-Wagner et al., 2007Olea-Wagner, A.; Lorenzo, C.; Naranjo, E.; Ortiz, D. & Leon-Paniagua, L. 2007. Diversity of fruits consumed by three species of bats (Chiroptera: Phyllostomidae) in the Lacandona rainforest, Chiapas, México. Revista Mexicana de Biodiversidad 78:191-200.), the same pattern observed in Argentina, a country with a subtropical climate (Sánchez et al., 2012Sánchez, M. A.; Giannini, N. P. & Barquez, R. M. 2012. Bat frugivory in two subtropical rain forests of Northern Argentina: Testing hypotheses of fruit selection in the Neotropics. Mammalian Biology 77:22-31.).

The consistency found in the diet of the studied phyllostomids throughout their distribution suggests a strong interaction with some food plants. One of the factors contributing to this interaction may be the seed dispersal syndrome. In fact, the three most consumed fruit genera all have several species that fall into the bat-dispersal syndrome (cf . van der Pijl, 1957) as their attributes are believed to facilitate the location and consumption by bats (Laska & Schmidt, 1986Laska, M. & Schmidt, U. 1986. Untersuchungen zur olfaktorischen orientierung bei der Brillenblattnase, Carollia p erspicillata (Chiroptera). Zeitschrift für Säugetierkunde 51:129-138.; Thies et al., 1998Thies, W.; Kalko, E. K. V. & Schnitzler, H. U. 1998. The roles of echolocation and olfaction in two Neotropical fruit-eating bats, Carollia p erspi cillata an d C. castanea, fee ding on Piper. Behavioral Ecology and Sociobiology 42:397-409.). Nevertheless, as shown by this study and Andrade et al. (2013Andrade, T. Y.; Thies, W.; Rogeri, P. K.; Kalko, E. K. V. & Mello, M. A. R. 2013. Hierarchical fruit selection by Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae). Journal of Mammalogy 94:1094-1101.), diet segregation at genus and species level suggests that other factors (chemical, behavioural, etc.) are acting as well.

A rarely discussed but interesting and relevant factor is the spatial fidelity of bats, which is shaped by the phenology and occurrence of their most consumed fruits (Bianconi et al., 2006Bianconi, G.V.; Mikich, S. B. & Pedro, W. A. 2006. Movements of bats (Mammalia, Chiroptera) in Atlantic Forest remnants in southern Brazil. Revista Brasileira de Zoologia 23:1199-1206.; Faria & Baumgarten, 2007Faria, D. & Baumgarten, J. 2007. Shade cacao plantations (Th eobroma cacao) and bat conservation in southern Bahia, Brazil. Biodiversity and Conservation 16:291-312.). For example, Carollia spp. exhibit greater constancy in the use of certain habitats compared with Artibeus , supposedly due to the spatial and temporal predictability of the Piper fruits (see above). Bat morphology may also be related to these foraging patterns, as due to the relatively small size of Carollia spp. (14-25 g) their flight capacity is more restricted to closed environments (Stockwell, 2001Stockwell, E. F. 2001. Morphology and flight manoeuvrability in New World leaf-nosed bats (Chiroptera: Phyllostomidae). Journal of Zoology 254:505-514.). The opposite occurs with Artibeus spp., which does not remain long in the same environment, probably due to the low abundance and asynchronous behavior of Ficus (Bianconi et al ., 2006). This pattern may also be related to their larger size (55-70 g) and greater potential for flight, which enables them to travel great distances in a single night in search of food (Stockwell, 2001; Dumont, 2003Dumont, E. R. 2003. Bats and Fruit: An ecomorphological ap proach. In: Kunz, T. H. & Fenton, B. eds. Bat Ecology. Chicago, University of Chicago Press, p. 398-429.).

The significant consumption of Moraceae fruits - mainly figs - by Artibeus spp. is widely supported by previous studies (e.g.Morrison, 1978Morrison, D. W. 1978. Influence of habitat on the foraging distances of the fruit bat, Artibeu s jamaicensis. Journal of Mammalogy 59:622-624.; Bonaccorso, 1979Bonaccorso, F. J. 1979. Foraging and reproductive ecology in a Panamanian bat community. Bulletin of the Florida State Museum Biological Sciences 24:359-408.; Handley et al ., 1991Handley Jr. C. O.; Wilson, D. E. & Gardner, A. L. 1991. Demography and natural history of the common fruit bat Artibeus jamaicensis on Barro Colorado Island, Panamá Washington, Smithsonian Institution Press. 173p.). Ficus is a genus of canopy trees, widely distributed in the Neotropics from Mexico to Paraguay (Banack et al., 2002Banack, S. A.; Horn, M. H.; & Gawlick, A. 2002. Disperser-vs. establishment-limited distribution of a riparian fig tree (F icus insipida) in a Costa Rican tropicalrain Forest. Biotropica 34:232-243.), whose representatives are intraspecifically asynchronous, but present a "boom" of syconia maturation within the canopy, which generally contains thousands of fruits (Morrison, 1978Morrison, D. W. 1978. Influence of habitat on the foraging distances of the fruit bat, Artibeu s jamaicensis. Journal of Mammalogy 59:622-624.). Such an abundance of resources attracts consumers from various groups, including birds, primates and other mammals (see Shanahan et al., 2001Shanahan, M.; So, S.; Compton, S. G. & Corlett, R. 2001. Fig-eating by vertebrate frugivores: a global review. Biological Reviews 77:529-572. for a review). For this reason, figs are considered keystone species for frugivores (Terborgh, 1986Terborgh, J. 1986. Community aspects of frugivory in tropical f orests. In: Estrada, A. & Fleming, T. H. eds. Frugivores and seed dispersal. Dordrecht, W. Junk Publishers, p. 371-384.). Some authors relate the elevated consumption of Ficus by bats to: position occupied by these trees in the forest stratum (Bonaccorso, 1979Bonaccorso, F. J. 1979. Foraging and reproductive ecology in a Panamanian bat community. Bulletin of the Florida State Museum Biological Sciences 24:359-408.), nutritional composition (Wendeln et al., 2000Wendeln, M. C.; Runkle, J. R. & Kalko, E. K. V. 2000. Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica 32:489-501.; Dumont, 2003Dumont, E. R. 2003. Bats and Fruit: An ecomorphological ap proach. In: Kunz, T. H. & Fenton, B. eds. Bat Ecology. Chicago, University of Chicago Press, p. 398-429.), or opportunistic behavior related to the abundance of this resource (Heithaus et al., 1975Heithaus, E. R.; Fleming, T. H. & Opler, P. A. 1975. Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest. Ecology 56:841-854.; Bonaccorso, 1979Bonaccorso, F. J. 1979. Foraging and reproductive ecology in a Panamanian bat community. Bulletin of the Florida State Museum Biological Sciences 24:359-408.; Mello & Passos, 2008Mello, M. A. R. & Passos, F. C. 2008. Frugivoria em morcegos brasi leiros. In: Pacheco, S.; Marques, R. V. & Esbérard, C. E. L. eds. Morcegos do Brasil: biologia, sistemática, ecologia e conservação. Porto Alegre, Editora Armazém Digital. 568p.). Although this last factor should contribute to the maintenance of the Artibeus -Ficus relationship, selection for fruit of this genus occurs even when their abundance is lower than that of other fruits (Morrison, 1978Morrison, D. W. 1978. Influence of habitat on the foraging distances of the fruit bat, Artibeu s jamaicensis. Journal of Mammalogy 59:622-624.; Parolin et al., 2015Parolin, L. C.; Mikich, S. B. & Bianconi, G. V. 2015. Olfaction in the fruit-eating bats Artib eus lituratus and Carollia perspicillata: an experimental analysis. Anais da Academia Brasileira de Ciências 87:2047-2053.).

Piperaceae and bats of the genus Carollia possess a high affinity and the literature abounds with records of Piper fruit consumption by these phyllostomids (e.g.Bonaccorso, 1979Bonaccorso, F. J. 1979. Foraging and reproductive ecology in a Panamanian bat community. Bulletin of the Florida State Museum Biological Sciences 24:359-408.; Fleming, 1988_____. 1988. The short-tailed fruit bat: A study in plant-animal interactions. Chicago, University Chicago Press. 380p.; Thies & Kalko, 2004Thies, W. & Kalko, E. K. V. 2004. Phenology of neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia p erspi cillata and C. castanea (Phyllostomidae). Oikos 104:362-376.; Sánchez et al., 2012Sánchez, M. A.; Giannini, N. P. & Barquez, R. M. 2012. Bat frugivory in two subtropical rain forests of Northern Argentina: Testing hypotheses of fruit selection in the Neotropics. Mammalian Biology 77:22-31.; the present study), with studies even proposing co-evolution between these genera (Thies & Kalko, 2004Thies, W. & Kalko, E. K. V. 2004. Phenology of neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia p erspi cillata and C. castanea (Phyllostomidae). Oikos 104:362-376.). The genus Piper comprises pioneer plants, common to degraded areas in the Neotropics (Lobova et al., 2009Lobova, T. A.; Geiselman, C. K. & Mori, A. S. 2009. Seed dispersal by bats in the Neotropics New York, New York Botanical Garden Press. 465p.). Their green smelly spike-shaped infructescences are typical examples of bat fruits (van der Pijl, 1957Van der Pijl, L. 1957. The dispersal of plants by bats (Chiropterochory). Acta Botanica Neerlandica 6:291-315.). Each individual plant produces few ripe fruits per night (Dumont, 2003Dumont, E. R. 2003. Bats and Fruit: An ecomorphological ap proach. In: Kunz, T. H. & Fenton, B. eds. Bat Ecology. Chicago, University of Chicago Press, p. 398-429., steady state pattern according to Snow, 1965Snow, D. W. 1965. A possible selective factor in the evolution of fruiting seasons in tropical forest. Oikos 15:274-281.), over relatively extended periods (usually two or three months) (Fleming, 1988_____. 1988. The short-tailed fruit bat: A study in plant-animal interactions. Chicago, University Chicago Press. 380p.). Nevertheless, different Piper species exhibit low phenological overlap allowing them to share dispersers and feed them all year round (Fleming, 1985Fleming, T. H. 1985. Coexistence of five sym patric Piper (Piperaceae) species in a Costa Rican dry forest. Ecology 66:688-700.). All these traits are believed to be important in maintaining Carollia spp. as the main consumers and dispersers of Piper spp. (Thies & Kalko, 2004Thies, W. & Kalko, E. K. V. 2004. Phenology of neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia p erspi cillata and C. castanea (Phyllostomidae). Oikos 104:362-376.).

The genus Sturnira also appears to primarily consume steady state fruits. Although several studies show their preferential consumption of Solanum (e.g.Giannini, 1999Giannini, N. P. 1999. Selection of diets and elevation by sympatric specie s of Sturnira in an Andean rainforest. Journal of Mammalogy 80:1186-1195.; Mello et al., 2008Mello, M. A. R. & Passos, F. C. 2008. Frugivoria em morcegos brasi leiros. In: Pacheco, S.; Marques, R. V. & Esbérard, C. E. L. eds. Morcegos do Brasil: biologia, sistemática, ecologia e conservação. Porto Alegre, Editora Armazém Digital. 568p.; Lobova et al., 2009Lobova, T. A.; Geiselman, C. K. & Mori, A. S. 2009. Seed dispersal by bats in the Neotropics New York, New York Botanical Garden Press. 465p.; but see Mikich, 2002Mikich, S. B. 2002. A dieta dos morcegos frugívoros (Mammalia, Chiroptera, Phyllostomidae) de um pequeno remanescente de Floresta Estacional Semidecidual do sul do Brasil. Revista Brasileira de Zoologia 19:239-249.), there are also several reports of interactions with the fruits of Piper (e.g. Giannini, 1999; Sánchez et al., 2012Sánchez, M. A.; Giannini, N. P. & Barquez, R. M. 2012. Bat frugivory in two subtropical rain forests of Northern Argentina: Testing hypotheses of fruit selection in the Neotropics. Mammalian Biology 77:22-31.). In fact, although we found that the Solanum was the genus most frequently consumed by Sturnira , the consumption of Piper fruits was also significant.

In the most intensively sampled localities the majority of fruit consumption by Artibeus , Carollia and Sturnira was recorded in the genera Ficus , Piper and Solanum. This finding confirms the spatial consistency of these supposed preferences. There are several non-mutually exclusive explanations for this phenomenon, including the broad distribution of the groups, the way these resources are offered and the spatial and temporal patterns in habitat use by bats, all of which favor these mutualistic encounters. Our results also indicate the need for a greater effort to fill knowledge gaps in countries where the diet of these frugivorous bats remains poorly sampled.

Acknowledgments

This paper is part of the dissertation of the first author. We thank Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA) and Embrapa Florestas for logistical support; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for a master's scholarship to LCP.

REFERENCES

Data availability

Publication Dates

History