Mammalian Biology

, Volume 77, Issue 1, pp 22–31 | Cite as

Bat frugivory in two subtropical rain forests of Northern Argentina: Testing hypotheses of fruit selection in the Neotropics

  • Mariano S. SánchezEmail author
  • Norberto P. Giannini
  • Rubén M. Barquez
Original Investigation


Phyllostomid bats are prominent components of mammalian assemblages in the Neotropics. With many species specialized in frugivory, phyllostomids represent major partners of fleshy-fruited plants in the mutualism of seed dispersal. Here we present dietary data from two subtropical rainforests of Argentina, where fruit diversity is low and thus offer unique opportunities to test hypotheses of diet selection originally proposed for species-rich tropical assemblages. Particularly, we tested whether frugivorous phyllostomids exhibit pronounced dietary specialization in core plant taxa where fruit offer is greatly reducedascomparedtotropical rainforests.We analyzed dietary overlap and nichebreadth of subtropical frugivorous bats on the basis of >1000 dietary records plus >500 samples from a previous study in the region.Weshow thatinthe subtropics, frugivores from different genera remain faithful to their respective core plant taxa with few exceptions, rather than shifting toward alternative fruit resources available in the study sites. This supports predictions of specialization, which is confirmed to have a deep historical origin. The response of phyllostomid ensembles to restricted fruit diversity is at the level of species composition: absence of species for which preferred fruits do not occur in the sites. Taken together, these data lend strong support to hypotheses that explain coexistence of frugivorous phyllostomids on the basis of dietary specialization on core plant taxa with chiropterochorous fruits.


Sturnira Artibeus Carollia Diet selection Fruit morphology 


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  1. Aguiar, L.M.S., Marinho-Filho, J., 2007. Bat frugivory in a remnant of southeastern Brazilian Atlantic forest. Acta Chiropterologica 9, 251–260.CrossRefGoogle Scholar
  2. Aguirre, L.F., 2002. Structure of a neotropical savanna bat community. Journal of Mammalogy 83, 775–784.CrossRefGoogle Scholar
  3. Ascorra, C., Solari, S., Wilson, D.E., 1996. Diversidad y ecología de los quirópteros en Pakitza. In: Wilson, D.E., Sandoval, A. (Eds.), Manu. The Biodiversity of South¬eastern Peru. Editorial Horizonte, Lima, Perú, pp. 593–612.Google Scholar
  4. Baker, R.J., Hoofer, S.R., Porter, C.A., Van Den Bussche, R.A., 2003. Diversifications among new words leaf-nosed bats: an evolutionary hypothesis and classifications inferred from digenomic congruence of DNA sequence. Occasional Papers, vol. 230. Museum of Texas Tech University, pp. 1–32.Google Scholar
  5. Baker, R.J., Porter, C.A., Patton, J.C., Van Den Bussche, R.A., 2000. Systematics of bats of the family Phyllostomidae based on RAG2 DNA sequences. Occasional Papers, vol. 202. Museum of Texas Tech University, pp. 1–16.Google Scholar
  6. Barquez, R.M., 2005. Orden Chiroptera Blumenbach, 1779. In: Barquez, R.M., Díaz, M.M., Ojeda, R.A. (Eds.), Mamíferos de Argentina, sistemática y distribución. Sociedad Argentina para el Estudio de los Mamíferos, pp. 56–86.Google Scholar
  7. Bernard, E., 2001. Vertical stratification of bat communities in primary forests of central Amazon, Brazil. Journal of Tropical Ecology 17, 115–126.CrossRefGoogle Scholar
  8. Bernard, E., Fenton, M.B., 2002. Species diversity of bats (Mammalia: Chiroptera) in forest fragments, primary forests, and savannas in Central Amazonia, Brazil. Canadian Journal of Zoology 80, 1124–1140.CrossRefGoogle Scholar
  9. Bonaccorso, F.J., 1979. Foraging and reproductive ecology in a Panamanian bats community. Bulletin of the Florida State Museum Biological Sciences 24, 359–408.Google Scholar
  10. Brosset, A., Charles-Dominique, P., 1990. The bats from French Guiana: a taxonomic, faunistic and ecological approach. Mammalia 54, 509–560.Google Scholar
  11. Brown, A.D., 1995. Fenología y caída de hojarasca en las selvas montanas del Parque Nacional El Rey, Argentina. In: Brown, A.D., Grau, H.R. (Eds.), Investigación, conservación y desarrollo en selvas subtropicales de montanña. Laboratorio de Investigaciones Ecológicas de Las Yungas, Universidad Nacional de Tucumán, Argentina, pp. 93–102.Google Scholar
  12. Brown, A.D., Grau, H.R., Malizia, L.R., Grau, A., 2001. Argentina. In: Kappelle, M., Brown, A.D. (Eds.), Bosques nublados del Neotrópico. Instituto Nacional de Biodiversidad, San José de Costa Rica, pp. 623–659.Google Scholar
  13. Burkart, R., Bárbaro, N.O., Sánchez, R.O., Gomez, D.A., 1999. Ecorregiones de la Argentina. Administración de Parques Nacionales, Buenos Aires, Argentina.Google Scholar
  14. Cabrera, A., 1976. Regiones fitogeográficas de Argentinas. Enciclopedia Argentina de Agricultura, Jardinería y Flora. Editorial ACME, Buenos Aires, Argentina.Google Scholar
  15. Cabrera, A.L., Willink, A., 1980. Biogeografía de América Latina. Secretaría General de la OEA. Monogr. Cient. Serie Biología n 13, Washington, DC.Google Scholar
  16. Croat, T.B., 1978. Flora of Barro Colorado Island. Stanford University Press, Stanford, California.Google Scholar
  17. Deginani, N.B., 2001. Las species argentinas del género Passiflora (Passifloraceae). Darwiniana 39, 43–129.Google Scholar
  18. dos Reis, N.R., Muller, M.F., 1995. Bat diversity of forests and open areas in a subtropical region of south Brazil. Ecología Austral 5, 31–36.Google Scholar
  19. Estrada, A., Coates-Estrada, R., 2002. Bats in continuous forest, forest fragments and in an agricultural mosaic habitat-island at Los Tuxtla, Mexico. Biological Conservation 103, 237–245.CrossRefGoogle Scholar
  20. Fischer, K.E., Chapman, C.A., 1993. Frugivores and fruit syndromes: differences in patterns at the genus and species level. Oikos 66, 472–482.CrossRefGoogle Scholar
  21. Fleming, T.H., 1986. Opportunism versus specialization: the evolution of feeding strategies in frugivorous bats. In: Estrada, A., Fleming, T.H. (Eds.), Frugivores and Seed Dispersal. Dr. W. Junk Publ., pp. 105–118.Google Scholar
  22. Fleming, T.H., 1988. The short-tailed fruit bat: a study in plant–animal interactions. Wildlife Behav. Ecol. Ser. Chicago Univ. Press.Google Scholar
  23. Fleming, T.H., 1991. The relationship between body size, diet, and habitat use in frugivorous bats, genus Carollia (Phyllostomidae). Journal of Mammalogy 72, 493–501.CrossRefGoogle Scholar
  24. Fleming, T.H, 2005. The relationship between species richness of vertebrate mutualists and their food plantsin tropical and subtropical communities differs among hemispheres. Oikos 111, 556–562.CrossRefGoogle Scholar
  25. Fleming, T.H., Heithaus, E.R., 1981. Frugivorous bats, seed shadows and the structure of tropical forest. Biotropica, Reproductive Botany 13, 45–53.CrossRefGoogle Scholar
  26. Freeman, P.W., 2000. Macroevolution in microchiroptera: recoupling morphology and ecology with phylogeny. Evolutionary Ecology Research 2, 317–335.Google Scholar
  27. Gardner, A.L., 2007. Family Phyllostomidae Gray, 1825. In: Gardner, A.L. (Ed.), Mammals of South America, Volume1, Marsupials, Xenarthrans, Shrew, and Bats. The University of Chicago Press, Chicago and London, pp. 207–363.Google Scholar
  28. Giannini, N.P., 1999. Selection of diets and elevation by sympatric species of Sturnira in an Andean rainforest. Journal of Mammalogy 80, 1186–1195.CrossRefGoogle Scholar
  29. Giannini, N.P., Kalko, E.K.V., 2004. Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 105, 209–220.CrossRefGoogle Scholar
  30. Giannini, N.P., Kalko, E.K.V., 2005. The guild structure of animalivorous leaf-nosed bats of Barro Colorado Island, Panama, revisited. Acta Chiropterologica 7, 131–146.CrossRefGoogle Scholar
  31. Gorchov, D.L., Cornejo, F., Ascorra, C.F., Jaramillo, M., 1995. Dietary overlap between frugivorous birds and bats in the Peruvian Amazon. Oikos 74, 235–250.CrossRefGoogle Scholar
  32. Gotelli, N.J., Entsminger, G.L., 2006. EcoSim: null models software for ecology. Version 7.72. Acquired Intelligence and Kesey-Bear, Jericho, VT05465. Available from: <>.Google Scholar
  33. Hernández-Conrique, D., Iñiguez-Dávalos, L.I., Storz, J.F., 1997. Selective feeding by phyllostomid fruit bats in a subtropical montane cloud forest. Biotropica 29, 376–379.CrossRefGoogle Scholar
  34. Herrera, C.M., 1987. Vertebrate-dispersed plants of the Iberian Peninsula: a study of fruit characteristics. Ecological Monographs 57, 305–331.CrossRefGoogle Scholar
  35. Horn, H.S., 1966. Measurement of “overlap” in comparative ecological studies. The American Naturalist 100, 419–424.CrossRefGoogle Scholar
  36. Howe, H.F., Smallwood, J., 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13, 201–228.CrossRefGoogle Scholar
  37. Hueck, K., 1978. Los bosques de Sudamérica. GTZ, Eschborn, Germany.Google Scholar
  38. Humphrey, S.R., Bonaccorso, F.J., Zinn, T.L., 1983. Guild structure of surface-gleaning bats in Panama. Ecology 64, 284–294.CrossRefGoogle Scholar
  39. Jordano, P., 1995. Angiosperm fleshy fruits and seed dispersers : a comparative analysis of adaptation and constraints in plant–animal interactions. The American Naturalist 145, 163–191.CrossRefGoogle Scholar
  40. Kalka, M.B., Smith, A.R., Kalko, E.K.V., 2008. Bats limit arthropods and herbivory in a tropical forest. Science 320, 71.PubMedCrossRefGoogle Scholar
  41. Kalko, E.K.V., 1997. Diversity in tropical bats. In: Ulrich, H. (Ed.), Tropical Diversity and Systematics, Proc. Int. Symp. Biodiv. Syst. Tropical Ecosystems, Bonn 1994. Zool. Forschungsinst Mus. Alexander Koenig, Bonn.Google Scholar
  42. Kalko, E.K.V., Condon, M.A., 1998. Echolocation, olfaction and fruit display: how bats find fruit of flagellichorous cucurbits. Functional Ecology 12, 364–372.CrossRefGoogle Scholar
  43. Kalko, E.K.V., Handley Jr., C.O., 2001. Neotropical bats in the canopy: diversity, community structure, and implications for conservation. Plant Ecology 153, 319–333.CrossRefGoogle Scholar
  44. Kalko, E.K.V., Handley Jr., C.O., Handley, D., 1996a. Organization, diversity and longterm dynamics of a Neotropical bat community. In: Cody, M., Smallwood, J. (Eds.), Long-term StudiesinVertebrate Communities. Academic Press, LosAngeles, pp. 503–553.CrossRefGoogle Scholar
  45. Kalko, E.K.V., Herre, E.A., Handley Jr., C.O., 1996b. Relation of fig fruit characteristics to fruit-eating bats in the new and old world tropics. Journal of Biogeography 23, 565–576.CrossRefGoogle Scholar
  46. Klingbeil, B.T., Willig, M.R., 2009. Guild-specific responses of bats to landscape composition and configuration in fragmented Amazonian rainforest. Journal of Applied Ecology 46, 203–213.CrossRefGoogle Scholar
  47. Krebs, C.J., 1999. Ecological Methodology, 2nd ed. Addison-Wesley Educational Publishers Inc., Menlo Park, Calif.Google Scholar
  48. Lang, A.B., Kalko, E.K.V., RÖmer, H., Bockholdt, C., Dechmann, D.K.N., 2006. Activity levels of bats and katydids in relation to the lunar cycle. Oecologia 146, 659–666.PubMedCrossRefGoogle Scholar
  49. Lawlor, L.R., 1980. Structure and stabilityin natural and randomly constructed competitive communities. The American Naturalist 116, 394–408.CrossRefGoogle Scholar
  50. Lim, B.K., Engstrom, M.D., Lee Jr., T.E., Patton, J.C., Bickham, J.W., 2004. Molecular differentiation of large species of fruit-eating bats (Artibeus) and phylogenetic relationships based on the cytochrome b gene. Acta Chiropterologica 6, 1–12.CrossRefGoogle Scholar
  51. Lobova, T.A., Geiselman, C.K., Moris, S.A., 2009. Seed dispersal by batsin the Neotropics. Memoirs of the New York Botanical Garden, vol. 101. The New York Botanical Garden.Google Scholar
  52. Lomáscolo, S.B., Schaefer, H.M., 2010. Signal convergence in fruits: a result of selection by frugivores?. Journal of Evolutionary Biology 23, 614–624.PubMedCrossRefPubMedCentralGoogle Scholar
  53. Lomáscolo, S.B., Speranza, P., Kimball, R.T., 2008. Correlated evolution of fig size and color supports the dispersal syndromes hypothesis. Oecologia 156, 783–796.PubMedCrossRefPubMedCentralGoogle Scholar
  54. Lopez, J.E., Vaughan, C., 2007. Food niche overlap among neotropical frugivorous bats in Costa Rica. Revista Biología Tropical 55, 301–313.Google Scholar
  55. Manly, B.F.J., 1997. Randomization, Bootstrap and Monte Carlo Methods in Biology, 2nd ed. Chapman and Hall, London, United Kingdom.Google Scholar
  56. Mantel, N., 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209–220.PubMedPubMedCentralGoogle Scholar
  57. Marinho-Filho, J.S., 1991. The coexistence of two frugivorous bat species and the phenology of their food plants in Brazil. Journal of Tropical Ecology 7, 59–67.CrossRefGoogle Scholar
  58. Mello, M.A.R., Kalko, E.K.V., Silva, W.R., 2008. Diet and abundance of the bat Sturnira lilium (Chiroptera) in a Brazilian montane Atlantic forest. Journal of Mammalogy 89, 485–492.CrossRefGoogle Scholar
  59. Minetti, J.L., Bobba, M.E., Hernández, C., 2005. Régimen espacial de temperaturas en el Noroeste de Argentina. In: Minetti, J.L. (Ed.), El Clima del Noroeste Argentino Laboratorio Climatológico Sudamericano (LCS). Editorial Magna, pp. 141–161.Google Scholar
  60. Palmeirim, J.M., Gorchov, D.L., Stoleson, S., 1989. Trophic structure of neotropical frugivore community:isthere competitions between birds and bats?. Oecologia 79, 403–411.PubMedCrossRefGoogle Scholar
  61. Pianka, E.R., 1973. The structure of lizard communities. Annual Review of Ecology and Systematics 4, 53–74.CrossRefGoogle Scholar
  62. R Development Core Team, 2004. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Available from: <, >.Google Scholar
  63. Sampaio, E.M., Kalko, E.K.V., Bernard, E., Rodríquez-Herrrera, B., Handley Jr., C.O., 2003. A biodiversity assessment of bats (Chiroptera) in a tropical lowland rainforestofcentral Amazonia, including methodological and conservation considerations. Studies on Neotropical Fauna and Environment 38, 17–31.CrossRefGoogle Scholar
  64. Simmons, N.B., Voss, R.S., 1998. The mammals of Paracou, French Guiana : a neotropical lowland rainforest fauna. Part 1. Bats. Bulletin of the American Museum of Natural History 237, 1–219.Google Scholar
  65. Srur, M., Gatti, F., Benesovsky, V., Herrera, J., Melzew, R., Camposano, M., 2007. Identificación, caracterización y mapeo de los ambientes del Parque Nacional Iguazú. Informe final. Centro de Investigaciones Ecológicas Subtropicales, Delegación Técnica Regional NEA. A.P.N. Parques Nacionales, Argentina.Google Scholar
  66. Pijl van der, L., 1972. Principles of Dispersal in Higher Plants. Springer-Verlag.Google Scholar
  67. Villalobos, F., Valerio, A.A., 2002. The phylogenetic relationships of the bat genus Sturnira Gray, 1842 (Chiroptera: Phyllostomidae). Mammalian Biology 67, 268–275.CrossRefGoogle Scholar
  68. Wetterer, A.L., Rockman, M.V., Simmons, N.B., 2000. Phylogeny of Phyllostomid bats (Mammalia: Chiroptera): data from diverse morphological systems, sex chromosomes, and restriction sites. Bulletin of the American Museum of Natural History 248, 1–200.CrossRefGoogle Scholar
  69. Zuloaga, F.O., Morrone, O. (Eds.), 1999. Catálogo de las Plantas Vasculares de la República Argentina II. Dicotyledoneae. Monographs in Systematic Botany from the Missouri Botanical Garden, vol. 74, pp. 1–1246.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2011

Authors and Affiliations

  • Mariano S. Sánchez
    • 1
    • 2
    Email author
  • Norberto P. Giannini
    • 1
    • 2
    • 3
  • Rubén M. Barquez
    • 1
    • 2
  1. 1.Consejo Nacional de Investigaciones Científicas y TécnicasArgentina
  2. 2.Programa de Investigaciones de Biodiversidad Argentina, Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de TucumánTucumánArgentina
  3. 3.Department of Mammalogy, American Museum of Natural HistoryNew YorkUSA

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