Mammalian Biology

, Volume 77, Issue 1, pp 32–40 | Cite as

Enriching agroecosystems with fruit-producing tree species favors the abundance and richness of frugivorous and nectarivorous bats in Veracruz, Mexico

  • Alejandro Antonio Castro-LunaEmail author
  • Jorge Galindo-González
Original Investigation


We evaluated how the abundance and richness of frugivorous and nectarivorous bat species differs among three types of common agroecosystems (diversified coffee plantations, simple coffee plantations and pastures) in Veracruz, Mexico, that represent a gradient of structural and floristic complexity. Using mixed effects models we demonstrated that both the richness and the total abundance of bats was higher in the diversified coffee plantations. We detected similar patterns on comparing the abundance of the four most abundant bat species. Neither season nor the season-agroecosystem interaction had any effect on the comparisons made. Using multiple regressions we found that the richness of plants that are useful to both people and bats had the most explanatory power for the richness and total abundance of frugivorous and nectarivorous bats, as well as for the abundance of Carollia sowelli, Glossophaga soricina and Sturnira spp. Our results indicate that agroecosystems value for conservation of fruit and nectar-eating bats increases as the fruit-bearing trees increases. For the effective conservation of these guilds of bats in tropical agroecosystems, a strategy of diversification with fruit-bearing species is highly recommended; such a strategy would benefit both agricultural producers and wildlife.


Bats Conservation Coffee Pastures Phyllostomidae 


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  1. Altieri, M.A., 1999. The ecological role of biodiversity in agroecosystems. Agric. Ecosyst. Environ. 74, 19–31.CrossRefGoogle Scholar
  2. Arita, H.T., 1993. Rarity in Neotropical bats: correlations with taxonomy, diet, and body mass. Ecol. Appl. 3, 506–517.PubMedCrossRefGoogle Scholar
  3. Brosset, A., Charles-Dominique, P., Cockle, A., Cosson, J., Masson, D., 1996. Bat communities and deforestation in French Guiana. Can. J. Zool. 78, 1231–1239.Google Scholar
  4. Colwell, R.K., 2005. EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples. Version 7.5. , Scholar
  5. Crawley, M.J., 2002. Statistical Computing: An Introduction to Data Analysis Using S-Plus. John Wiley and Sons Ltd., Chichester.Google Scholar
  6. Challenger, A., 1998. Utilización y conservación de los ecosistemas terrestres de México. Pasado, presente y futuro. Comisión Nacional para el Uso y Conocimiento de la Biodiversidad, Instituto de Biología UNAM, Agrupación Sierra Madre AC, Mexico City.Google Scholar
  7. Dagang, A.B.K., Nair, P.K.R., 2003. Silvopastoral research and adoption in Central America: recent findings and recommendations for future directions. Agroforest. Syst. 59, 149–155.CrossRefGoogle Scholar
  8. Donald, P.F., 2004. Biodiversity impact of some agricultural commodity production systems. Conserv. Biol. 18, 17–37.CrossRefGoogle Scholar
  9. Estrada, A., Coates-Estrada, R., Meritt Jr., D., 1993. Bat species richness and abundance in tropical rain forest fragments and in agricultural habitats at Los Tuxtlas, Mexico. Ecography 16, 309–318.CrossRefGoogle Scholar
  10. Estrada, A., Coates-Estrada, R., Meritt Jr., D., 1994. Non flying mammals and landscape changes in the tropical rain forest region of Los Tuxtlas, Mexico. Ecography 17, 229–241.CrossRefGoogle Scholar
  11. Ewel, J.J., 1999. Natural systems as a model for the design of sustainable systems of land use. Agroforest. Syst. 45, 1–21.CrossRefGoogle Scholar
  12. Faria, D., Laps, R.R., Baumgarten, J., Cetra, M., 2006. Bat and bird assemblages from forestsandshade cacao plantations in two contrasting landscapes in the Atlantic forest of southern Bahia, Brazil. Biodivers. Conserv. 15, 587–612.CrossRefGoogle Scholar
  13. Fenton, M.B., Acharya, L.D., Audet, D., Hickey, M.B.C., Merriman, C., Obrist, M.K., Syme, D.M., Adkins, B., 1992. Phyllostomid bats (Chiroptera: Phyllostomidae) as indicators of habitat disruption in the Neotropics. Biotropica 24, 440–446.CrossRefGoogle Scholar
  14. 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
  15. Galindo-González, J., 2004. Clasificación delos murciélagosde la región de Los Tuxtlas, Veracruz, respecto a su respuesta a la fragmentación del hábitat. Acta Zool. Mex. (n. s.) 20, 239–243.Google Scholar
  16. Galindo-González, J., 2007. Efectos de la fragmentación del paisaje sobre las poblaciones de mamíferos, el caso de los murciélagos de Los Tuxtlas, Veracruz. In: Sánchez-Rojas, G., Rojas-Martínez, A.E. (Eds.), Tópicos en sistemática, biogeografía, ecología y conservación de mamíferos. Universidad Autónoma del Estado de Hidalgo, México, pp. 97–114.Google Scholar
  17. Galindo-González, J., Sosa, V.J., 2003. Bats species richness in man-made pastures in a fragmented tropical landscape. Southwest. Nat. 48, 579–589.CrossRefGoogle Scholar
  18. Gannon, M.R., 1994. A new technique for marking bats. Bat Res. News 34, 88–89.Google Scholar
  19. García, E.,1987. Modificaciones al sistema de clasificación climática de Köppen(para adaptarlo a las condiciones de la República Mexicana). Talleres de Offset Larios, Mexico City.Google Scholar
  20. García-Estrada, C., Damon, A., Sánchez-Hernández, C., Soto-Pinto, L., Ibarra-Núñez, G., 2006. Bat diversity in montane rainforest and shaded coffee under different management regimes in southeastern Chiapas, Mexico. Biol. Conserv. 132, 351–361.CrossRefGoogle Scholar
  21. 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
  22. Gonc¸ alves da Silva, A., Gaona, O., Medellín, R.A., 2008. Diet and trophic structure in a community of fruit-eating bats in Lacandon Forest, Mexico. J. Mammal. 89, 43–49.CrossRefGoogle Scholar
  23. Harvey, C.A., Medina, A., Sánchez, D.M., Vílchez, S., Hernández, B., Saenz, J.C., Maes, J.M., Casanoves, F., Sinclair, F.L., 2006. Patterns of animal diversity in different forms of tree cover in agricultural landscapes. Ecol. Appl. 16, 1986–1999.PubMedCrossRefGoogle Scholar
  24. Harvey, C.A., Komar, O., Chazdon, R., Ferguson, B.G., Finegan, B., Griffith, D.M., Martínez-Ramos, M., Morales, H., Nigh, R., Soto-Pinto, L., Van Breugel, M., Wishnie, M., 2008. Integrating agricultural landscapes with biodiversity conservation in the Mesoamerican hotspot. Conserv. Biol. 22, 8–15.PubMedCrossRefGoogle Scholar
  25. Heithaus, 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.CrossRefGoogle Scholar
  26. Hernández-Montero, J.R., 2008. Riqueza, abundancia, equidad y composición de plantas dispersadas por murciélagos filostómidos en cafetales bajo sombra y fragmentos de bosque mesófilo de montaña en el centro de Veracruz. BSc. Dissertation. Universidad Veracruzana, Xalapa.Google Scholar
  27. Jose, S., 2009. Agroforestry for ecosystem services andenvironmental benefits. Agroforest. Syst. 76, 1–10.CrossRefGoogle Scholar
  28. Kingston, T., 2009. Analysis of species diversity of bat assemblages. In: Kunz, T.H., Parsons, S. (Eds.), Ecological and Behavioral Methods for the Study of Bats. Johns Hopkins University Press, Baltimore, Maryland, pp. 195–215.Google Scholar
  29. Kunz, T.H., Tidemann, C.R., Richards, G.C., 1996. Capturing small volant mammals. In: Wilson, D.E., Cole, F.R., Nichols, J.D., Rudran, R., Foster, M.S. (Eds.), Measuring and Monitoring Biological Diversity: Standard Methods for Mammals. Smithsonian Institution Press, Washington, DC, pp. 122–146.Google Scholar
  30. Lambin, E.F., Geist, H.J., Lepers, E., 2003. Dynamics of land-use and land-cover change in tropical regions. Annu. Rev. Environ. Resour. 28, 205–241.CrossRefGoogle Scholar
  31. Longino, J.T., Colwell, R.K., 1997. Biodiversity assessment using structured inventory: capturing the ant fauna ofa lowland tropical rainforest. Ecol. Appl. 7, 1263–1277.CrossRefGoogle Scholar
  32. Magurran, A.E., 2004. Measuring Biological Diversity. Blackwell Publishing, Oxford.Google Scholar
  33. Manson, R.H., Hernández-Ortiz, V., Gallina, S., Mehltreter, K., 2008. Agroecosistemas cafetalerosde Veracruz: biodiversidad, manejoy conservación. INECOL, Instituto Nacional de Ecología, SEMARNAT, Mexico City.Google Scholar
  34. MathSoft, 1999. S-Plus 2000. MathSoft, Data Analysis Products Division, Seattle.Google Scholar
  35. Medellín, R.A., Arita, H.T., Sánchez, O., 2008. Identificación de los murciélagos de México, clave de campo. Asociación Mexicana de Mastozoología, Mexico City.Google Scholar
  36. Mello, M.A.R., Kalko, E.K.V., Silva, W.S., 2008. Diet and abundance of the bat Sturnira lilium in a Brazilian Atlantic forest. J. Mammal. 89, 485–492.CrossRefGoogle Scholar
  37. Miller, M.S., Russell, R.E., 2003. Species-specific responses to landscape heterogeneity: improving estimates of connectivity. In: Swihart, R.K., Moore, J.E. (Eds.), ConservingBiodiversity in Agricultural Landscapes: Model Based PlanningTools. Purdue University Press, West Lafayette, pp. 121–138.Google Scholar
  38. Moguel, P., Toledo, V.M., 1999. Biodiversity conservation in traditional coffee systems of Mexico. Conserv. Biol. 13, 11–21.CrossRefGoogle Scholar
  39. Moreno, C.E., Halffter, G., 2000. Assessing the completeness of bat biodiversity inventories using species accumulation curves. J. Appl. Ecol. 37, 149–158.CrossRefGoogle Scholar
  40. Morrison, D.W., 1978. Lunar phobia in a Neotropical fruit bat, Artibeus jamaicensis (Chiroptera: Phyllostomidae). Anim. Behav. 26, 852–855.CrossRefGoogle Scholar
  41. Mueller-Dombois, D., Ellemberg, H., 1974. Aims and Methods of Vegetation Ecology. John Wiley and Sons, New York.Google Scholar
  42. Ortiz-Ceballos, G., 2004. El agroecosistema café: crisis de mercado y sustentabilidad. Ph.D. Dissertation. Colegio de Posgraduados, Montecillos.Google Scholar
  43. Perfecto, I., Rice, R.A., Greenberg, R., van der Voort, M.E., 1996. Shade coffee: a disappearing refuge to biodiversity. Bioscience 46, 598–608.CrossRefGoogle Scholar
  44. Perfecto, I., Maas, A., Dietsch, T., Vandermeer, J., 2003. Conservation of biodiversity in coffee agroecosystems: a tri-taxa comparison in southern Mexico. Biodivers. Conserv. 12, 1239–1252.CrossRefGoogle Scholar
  45. Perfecto, I., Vandermeer, J., 2008. Biodiversity conservation in tropical agroecosystems: a new conservation paradigm. Ann. N.Y. Acad. Sci. 1134, 173–200.PubMedCrossRefGoogle Scholar
  46. Pinheiro, C.J., Bates, D., 2000. Mixed-effect Models in S and S-plus. Springer, New York.CrossRefGoogle Scholar
  47. Rice, R.A., Greenberg, R., 2000. Cacao cultivation and the conservation of biological diversity. Ambio 29, 167–173.CrossRefGoogle Scholar
  48. Rice, R.A., Ward, J.R., 1996. Coffee, Conservation and Commerce in the Western Hemisphere. Smithsonian Migratory Bird Center, Washington, DC.Google Scholar
  49. Roshier, D.A., Doerr, V.A.J., Doerr, E.D., 2008. Animal movement in dynamic landscapes: interaction between behavioural strategies and resource distributions. Oecologia 156, 465–477.PubMedCrossRefGoogle Scholar
  50. Russell, R.E., Swihart, R.K., Feng, Z., 2003. Population consequences of movement decisions in a patchy landscape. Oikos 103, 142–152.CrossRefGoogle Scholar
  51. Saldaña-Vázquez, R.A., Sosa, V.J., Hernández-Montero, J.R., López-Barrera, F., 2010. Abundance responses of frugivorous bats (Stenodermatinae) to coffee cultivation and selective logging practices in mountainous central Veracruz, Mexico. Biodivers. Conserv. 19, 2111–2124.CrossRefGoogle Scholar
  52. Semarnat, 2002. Norma Oficial Mexicana NOM-059-ECOL-2001. Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para suinclusión, exclusión ocambio-Listade especies en riesgo. In: Secretaría de Medio Ambiente y Recursos Naturales. Diario Oficial de la Federación (Segunda Sección). Miércoles 6 de marzo de.Google Scholar
  53. Simmons, N.B., Voss, R., 1998. The mammals of Paracou, French Guiana: a Neotropical lowland rainforest fauna—part 1: Bats. Bull. Am. Mus. Nat. Hist. 237, 1–219.Google Scholar
  54. Simmons, N.B., 2005. Order Chiroptera. In:Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World: A Taxonomic and Geographic Reference. Johns Hopkins University Press, Baltimore, pp. 312–529.Google Scholar
  55. Soto-Esparza, M., Gómez-Columna, M., 1990. Atlas climático del municipio de Xalapa. Instituto de Ecología. A. C, Xalapa, Veracruz, México.Google Scholar
  56. Tabarelli, M., 2010. Tropical biodiversity in human-modified landscapes : what is our trump card? Biotropica 42, 553–554.CrossRefGoogle Scholar
  57. Thies, 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 perspicillata and C. castanea (Phyllostomidae). Oikos 104, 362–376.CrossRefGoogle Scholar
  58. Tschapka, M., 2004. Energy density patterns of nectar resources permit coexistence within a guild of Neotropical flower-visiting bats. J. Zool. 263, 7–2.CrossRefGoogle Scholar
  59. Turner, M.G., Corlett, R.T., 1996. The conservation value of small, isolated fragments of lowland tropical rain forest. Trends Ecol. Evol. 11, 330–333.PubMedCrossRefGoogle Scholar
  60. Van der Maarel, E., 1979. Transformation of cover-abundance values in phytosociology and its effects on community similarity. Vegetatio 39, 97–114.CrossRefGoogle Scholar
  61. Vandermeer, J.H., 2002. Tropical Agroecosystems. CRC Press, Boca Raton.CrossRefGoogle Scholar
  62. Vandermeer, J.H., Perfecto, I., 2007. The agricultural matrix and the future paradigm for conservation. Conserv. Biol. 21, 274–277.PubMedCrossRefGoogle Scholar
  63. Waltert, M., Bobo, K.S., Sainge, M.N., Fermon, H., Mühlenberg, M., 2005. From forest to farmland: habitat effects on Afrotropical forest bird diversity. Ecol. Appl. 15, 1351–1366.CrossRefGoogle Scholar
  64. Williams-Linera, G., 1997. Phenology of deciduous and broadleaved-evergreen tree species in a Mexican tropical lower montane forest. Glob. Ecol. Biogeogr. 6, 115–127.CrossRefGoogle Scholar
  65. Williams-Linera, G., Manson, R.H., Isunza-Vera, E., 2002. La fragmentación del bosque mesófilo de montaña y patrones de uso del suelo en la región oeste de Xalapa, Veracruz, México. Madera y Bosques 8, 69–85.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2011

Authors and Affiliations

  • Alejandro Antonio Castro-Luna
    • 1
    Email author
  • Jorge Galindo-González
    • 1
  1. 1.Instituto de Biotecnología y Ecología Aplicada (INBIOTECA)Universidad VeracruzanaVeracruzMexico

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