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Vertical stratification of Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae) revealed by stable carbon isotopes

Published online by Cambridge University Press:  10 March 2011

Katja Rex ,
Robert Michener ,
Thomas H. Kunz  and
Christian C. Voigt
Katja Rex*
Affiliation:
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany
Robert Michener
Affiliation:
Center for Ecology and Conservation Biology, Department of Biology, Boston University, Boston, Massachusetts 02215, USA
Thomas H. Kunz
Affiliation:
Center for Ecology and Conservation Biology, Department of Biology, Boston University, Boston, Massachusetts 02215, USA
Christian C. Voigt
Affiliation:
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany
*
1Corresponding author. Email: katjarex@web.de
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Abstract:

Tropical rain forests harbour the most diverse plant and animal assemblages known to science, but our understanding of assemblage structure and species interactions is limited. Bats, as the only flying mammals, have the potential to exploit resources from all strata in forest communities. Thus, fruit-eating phyllostomid bats often have been categorized into canopy-, subcanopy- and understorey-foraging species, based largely upon the height at which they were most frequently captured. Here we challenge this classification and use stable carbon isotopes to assess foraging height of bat species at an Amazonian rain-forest site in Ecuador and at a Caribbean lowland rain-forest site in Costa Rica for comparison with data from mist-net captures. The proportion of the heavy stable carbon isotope 13C in relation to the lighter 12C isotope increases in plants from ground level to the canopy (0.12‰ m−1–0.18‰ m−1), and these differences in stable carbon isotope signatures are reflected in the body tissue of phytophagous bats. We used the stable carbon isotope ratio (δ13C) of wing tissue to estimate the foraging heights of 54 phyllostomid species in two Neotropical bat assemblages. Based on stable isotope data, phyllostomid species exploit food resources at all vertical strata of the forest. Capture height was not a reliable predictor of foraging height and suggests that bats most likely use lower strata to commute between foraging sites to avoid predators. Vertical stratification is likely to be a key factor promoting niche partitioning, thus promoting high local species richness in many tropical animal assemblages.

Keywords

canopyforaging behaviourresource partitioningstable carbon isotopesunderstorey
Type
Research Article
Information
Journal of Tropical Ecology , Volume 27 , Issue 3 , May 2011 , pp. 211 - 222
Copyright
Copyright © Cambridge University Press 2011

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References

LITERATURE CITED

ALBUJA, L. 1999. Murciélagos del Ecuador. (Second edition.). Circetrónic Companía Limitada Offset; Quito. Pp. 288.Google Scholar
BAKER, R. J. 2002. A new Central American species from the Carollia brevicauda complex. Occasional Papers Museum of Texas Tech University 217:1–12.Google Scholar
BASS, M., FINER, M., JENKINS, C. N., KREFT, H., CISNEROS-HEREDIA, D. F., McCRACKEN, S. F., PITMAN, N. C. A., ENGLISH, P. A., SWING, K., VILLA, G., DiFIORE, A., VOIGT, C. C. & KUNZ, T.H. 2010. Global conservation significance of Ecuador's Yasuní National Park. PLoS One 5:e8767.CrossRefGoogle ScholarPubMed
BERNARD, E. 2001. Vertical stratification of bat communities in primary forests of Central Amazon, Brasil. Journal of Tropical Ecology 17:115–126.CrossRefGoogle Scholar
BONACCORSO, F. J. 1978. Foraging and reproductive ecology in a Panamanian bat community. Bulletin of the Florida State Museum, Biological Sciences 24:359–408.Google Scholar
BONACCORSO, F. J., WINKELMANN, J. R., SHIN, D., AGRAWAL, C. I., ASLAMI, N., BONNEY, C., HSU, A., JEKIELEK, P. E., KNOX, A., KOPACH, S. J., JENNINGS, T. D., LASKY, J. R., MENESALE, S. A., RICHARDS, J. H., RUTLAND, J. A., SESSA, A., ZHAUROV, L. & KUNZ, T. H. 2007. Evidence for exploitative competition: comparative foraging behavior and roosting ecology of short-tailed fruit bats (Phyllostomidae). Biotropica 39:249–256.CrossRefGoogle Scholar
BUCHMANN, N., BROOKS, J. R. & EHLERINGER, J. R. 2002. Predicting daytime carbon isotope ratios of atmospheric CO2 within forest canopies. Functional Ecology 16:49–57.CrossRefGoogle Scholar
CERLING, T., HART, J. & HART, T. 2004. Stable isotope ecology in the Ituri Forest. Oecologia 138:5–12.CrossRefGoogle ScholarPubMed
DENIRO, M. J. & EPSTEIN, S. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42:495–506.CrossRefGoogle Scholar
FARQUHAR, G., DEHLERINGER, J. R. & HUBICK, K. T. 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40:503–537.CrossRefGoogle Scholar
FLEMING, T. H. 1986. Opportunism versus specialization: the evolution of feeding strategies in frugivorous bats. Pp. 105–118 in Estrada, A. & Fleming, T. H. (eds.). Frugivores and seed dispersal. Dr. W. Junk Publishers, Dordrecht.CrossRefGoogle Scholar
FLEMING, T. H. 1988. The short-tailed fruit bat: a study in plant–animal interactions. University of Chicago Press, Chicago.Google Scholar
FLEMING, T. H. 1995. The use of stable isotopes to study the diets of plant-visiting bats. Symposium of the Zoological Society, London 67:99–110.Google Scholar
FLEMING, T. H., NUNEZ, R. A. & STERNBERG, L. 1993. Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis. Oecologia 94:72–75.CrossRefGoogle Scholar
HANDLEY, C. O. 1967. Bats of the canopy of an Amazonian forest. Atas do Simpósio sobre a Biota Amazonica 5:211–215.Google Scholar
HENRY, M., BARRIÈRE, P., GAUTIER-HION, A. & COLYN, M. 2004. Species composition, abundance and vertical stratification of a bat community (Megachiroptera: Pteropodidae) in a West African rain forest. Journal of Tropical Ecology 20:21–29.CrossRefGoogle Scholar
HERRERA, L. G., FLEMING, T. H. & STERNBERG, L. 1998. Trophic relationships in a neotropical bat community: a preliminary study using carbon and nitrogen isotopic signatures. Tropical Ecology 39:23–29.Google Scholar
HERRERA, L. G., HOBSON, K. A., MIRÓN-M., L., RAMÍREZ-P., N., MÉNDEZ-C., G. & SÁNCHEZ-CORDERO, V. 2001. Sources of protein in two species of phytophagous bats in a seasonal dry forest: evidence from stable isotope analysis. Journal of Mammalogy 82:352–361.2.0.CO;2>CrossRefGoogle Scholar
HERRERA, L. G., GUTIERREZ, E., HOBSON, K. A., ALTUBE, B., DÍAZ, W. G. & SÁNCHEZ-CORDERO, V. 2002. Sources of assimilated protein in five species of New World frugivorous bats. Oecologia 133:280–287.CrossRefGoogle ScholarPubMed
HODGKISON, R., BALDING, S. T., ZUBAID, A. & KUNZ, T. H. 2003. Fruit bats (Chiroptera: Pteropodidae) as seed dispersers and pollinators in a lowland Malaysian rain forest. Biotropica 35:491–502.CrossRefGoogle Scholar
HODGKISON, R., BALDING, S. T., ZUBAID, A. & KUNZ, T. H. 2004. Habitat structure, wing morphology, and the vertical stratification of Malaysian fruit bats. Journal of Tropical Ecology 20:667–673.CrossRefGoogle Scholar
HUMPHREY, S. R., BONACCORSO, F. J. & ZINN, T. L. 1983. Guild structure of surface-gleaning bats in Panama. Ecology 64:284–294.CrossRefGoogle Scholar
KALKO, E. K. V. & HANDLEY, C. O. 2001. Neotropical bats in the canopy: diversity, community structure and implications for conservation. Plant Ecology 153:319–333.CrossRefGoogle Scholar
KALKO, E. K. V., HERRE, E. A. & HANDLEY, C. O. 1996. Relation of fig fruit characteristics to fruit-eating bats in New and Old World Tropics. Journal of Biogeography 23:565–576.CrossRefGoogle Scholar
KUNZ, T. H. & LUMSDEN, L. F. 2003. Ecology of cavity and foliage roosting bats. Pp. 3–89 in Kunz, T. H. & Fenton, M. B. (eds.). Bat ecology. The University of Chicago Press, Chicago.Google Scholar
LAMBERT, F. R. L. 1989. Fig-eating by birds in a Malaysian lowland forest. Journal of Tropical Ecology 5:401–412.CrossRefGoogle Scholar
MCCUTCHAN, J. H., LEWIS, W. M., KENDALL, C. & MCGRATH, C. C. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390.CrossRefGoogle Scholar
MEDINA, E. & MINCHIN, P. 1980. Stratification of δ13C values of leaves in Amazonian rainforests. Oecologia 45:377–378.CrossRefGoogle Scholar
MEDINA, E., STERNBERG, L. & CUEVAS, E. 1991. Vertical stratification of δ13C values in closed natural and plantation forests in the Luquillo mountains, Puerto Rico. Oecologia 87:369–372.CrossRefGoogle ScholarPubMed
NASSAR, J. M., BECK, H., STERNBERG, L. S. L. & FLEMING, T. H. 2003. Dependence on cacti and agaves in nectar-feeding bats from Venezuelan arid zones. Journal of Mammalogy 84:106–116.2.0.CO;2>CrossRefGoogle Scholar
NORBERG, U. M. & RAYNER, J. M. V. 1987. Ecological morphology and flight in bats (Mammalia: Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society of London B 316:335–427.Google Scholar
PEREIRA, M. J. R., MARQUES, J. T. & PALMEIRIM, J. M. 2010. Vertical stratification of bat assemblages in flooded and unflooded Amazonian forests. Current Zoology 56:469–478.CrossRefGoogle Scholar
PETERSON, B. J. & FRY, B. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18:293–320.CrossRefGoogle Scholar
POST, D. M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718.CrossRefGoogle Scholar
REX, K., KELM, D., WIESNER, K., KUNZ, T. H. & VOIGT, C. C. 2008. Structure of three Neotropical bat assemblages. Biological Journal of the Linnean Society 94:617–629.CrossRefGoogle Scholar
REX, K., CZACZKES, B. I., MICHENER, R., KUNZ, T. H. & VOIGT, C. C. 2010. Specialisation and omnivory in diverse mammalian assemblages. Ecoscience 17:37–46.CrossRefGoogle Scholar
RUBENSTEIN, D. R. & HOBSON, K. A. 2004. From birds to butterflies: animal movement patterns and stable isotopes. Trends in Ecology and Evolution 19:256–263.CrossRefGoogle ScholarPubMed
SCHAEFER, H. M., SCHMIDT, V. & WESENBERG, J. 2002. Vertical stratification and caloric content of the standing fruit crop in a tropical lowland forest. Biotropica 34:244–253.CrossRefGoogle Scholar
SCHULZE, C. H., LINSENMAIR, K. E. & FIEDLER, K. 2001. Understorey versus canopy: patterns of vertical stratification and diversity among Lepidoptera in a Bornean rain forest. Plant Ecology 153:133–152.CrossRefGoogle Scholar
SHANAHAN, M. & COMPTON, S. G. 2001. Vertical stratification of figs and fig-eaters in a Bornean lowland rain forest: how is the canopy different? Plant Ecology 153:121–132.CrossRefGoogle Scholar
SIMMONS, N. B. 2005. Chiroptera. Pp. 312–529 in Wilson, D. E. & Reeder, D. M. (eds.) Mammal species of the world. John Hopkins University Press, Baltimore.Google Scholar
STERNBERG, L., MULKEY, S. S. & WRIGHT, S. J. 1989. Ecological interpretation of leaf isotope ratios: influence of respired carbon dioxide. Ecology 70:1317–1324.Google Scholar
TERBORGH, J. & PETREN, K. 1991. Development of habitat structure through succession in an Amazonian floodplain forest. Pp. 28–46 in Bell, S. S., McCoy, E. D. & Mushinsky, H. R. (eds.). Habitat structure: the physical arrangement of objects in space. Chapman and Hall, London.CrossRefGoogle Scholar
TIESZEN, L. L., BOUTTON, T. W., TESDAHL, K. G. & SLADE, N. A. 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–37.CrossRefGoogle ScholarPubMed
TIMM, R. M., & LAVAL, R. K. 1998. A field key to the bats of Costa Rica. Occasional Publication Series, Center for Latin American Studies, The University of Kansas 22:1–30.Google Scholar
TIRIRA, D. 1999. Mamíferos del Ecuador. Museo de Zoología, Publicatión Especial 2, Quito, Ecuador. 392 pp.Google Scholar
VAN DER MERWE, N. J. & MEDINA, E. 1989. Photosynthesis and 13C/12C ratios in Amazonian rainforests. Geochimica et Cosmochimica Acta 53:1091–1094.CrossRefGoogle Scholar
VAN DER MERWE, N. J. & MEDINA, E. 1991. The canopy effect, carbon isotope ratios and foodwebs in Amazonia. Journal of Archaeological Science 18:249–259.CrossRefGoogle Scholar
VOIGT, C. C. 2011. Insights into strata use of forest animals using the ‘canopy effect’. Biotropica 42: 634–637.CrossRefGoogle Scholar
VOIGT, C. C. & KELM, D. H. 2006a. Host preference of the common vampire bat Desmodus rotundus assessed by stable isotopes. Journal of Mammalogy 87:1–6.CrossRefGoogle Scholar
VOIGT, C. C. & KELM, D. H. 2006b. Host preferences of bat flies: following the bloody path of stable isotopes in a host–parasite food chain. Canadian Journal of Zoology 84: 397–403.CrossRefGoogle Scholar
VOIGT, C. C., MATT, F., MICHENER, R. & KUNZ, T. H. 2003. Low turnover rates of carbon isotopes in tissues of two nectar-feeding bat species. Journal of Experimental Biology 206:1419–1427.CrossRefGoogle ScholarPubMed
VOIGT, C. C., ZUBAID, A., KUNZ, T. H. & KINGSTON, T. 2011. The origin of assimilated proteins in Old and New-World phytophagous bats. Biotropica 43:108–113.CrossRefGoogle Scholar
WALTHER, B. A. 2002. Vertical stratification and use of vegetation and light habitats by Neotropical forest birds. Journal of Ornithology 143:64–81.CrossRefGoogle Scholar
YORK, H. A. & BILLINGS, S. A. 2009. Stable-isotope analysis of diets of short-tailed fruit bats (Chiroptera: Phyllostomidae: Carollia). Journal of Mammalogy 90:1469–1477.CrossRefGoogle Scholar
ZUBAID, A. 1994. Vertical stratification of pteropodid bats in a Malaysian lowland rainforest. Mammalia 58:309–311.Google Scholar