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Trophic niche differentiation and microhabitat utilization revealed by stable isotope analyses in a dry-forest bat assemblage at Ankarana, northern Madagascar

Published online by Cambridge University Press:  16 December 2013

Melanie Dammhahn  and
Steven M. Goodman
Melanie Dammhahn*
Affiliation:
Behavioral Ecology & Sociobiology Unit, German Primate Center (DPZ), Leibniz Institute for Primate Research, Kellnerweg 4, D-37077 Göttingen, Germany
Steven M. Goodman
Affiliation:
Association Vahatra, BP 3972, Antananarivo 101, Madagascar Field Museum of Natural History, Science and Education, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA
*
1Corresponding author: Email: mdammha@gwdg.de
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Abstract:

Bats are important components in tropical mammal assemblages. Unravelling the mechanisms allowing multiple syntopic bat species to coexist can provide insights into community ecology. However, dietary information on component species of these assemblages is often difficult to obtain. Here we measured stable carbon and nitrogen isotopes in hair samples clipped from the backs of 94 specimens to indirectly examine whether trophic niche differentiation and microhabitat segregation explain the coexistence of 16 bat species at Ankarana, northern Madagascar. The assemblage ranged over 4.4‰ in δ15N and was structured into two trophic levels with phytophagous Pteropodidae as primary consumers (c. 3‰ enriched over plants) and different insectivorous bats as secondary consumers (c. 4‰ enriched over primary consumers). Bat species utilizing different microhabitats formed distinct isotopic clusters (metric analyses of δ13C–δ15N bi-plots), but taxa foraging in the same microhabitat did not show more pronounced trophic differentiation than those occupying different microhabitats. As revealed by multivariate analyses, no discernible feeding competition was found in the local assemblage amongst congeneric species as compared with non-congeners. In contrast to ecological niche theory, but in accordance with studies on New and Old World bat assemblages, competitive interactions appear to be relaxed at Ankarana and not a prevailing structuring force.

Keywords

Ankaranacanopy effectChiropteracoexistencecommunity structurecongeneric speciesdry deciduous forestMadagascar
Type
Research Article
Information
Journal of Tropical Ecology , Volume 30 , Issue 2 , March 2014 , pp. 97 - 109
Copyright
Copyright © Cambridge University Press 2013 

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References

LITERATURE CITED

AGUIRRE, L. F., HERREL, A., VAN DAMME, R. & MATTHYSEN, E. 2002. Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community. Proceedings of the Royal Society of London Series B 269:1271–1278.CrossRefGoogle Scholar
AGUIRRE, L. F., HERREL, A., VAN DAMME, R. & MATTHYSEN, E. 2003. The implications of food hardness for diet in bats. Functional Ecology 17:201–212.Google Scholar
ANDRIAFIDISON, D., KOFOKY, A., MBOHOAHY, T., RACEY, P. A. & JENKINS, R. K. B. 2007. Diet, reproduction and roosting habits of the Madagascar free-tailed bat, Otomops madagascariensis Dorst, 1953 (Chiroptera: Molossidae). Acta Chiropterologica 9:445–450.Google Scholar
ANDRIANAIVOARIVELO, R. A., RANAIVOSON, N., RACEY, P. A. & JENKINS, R. K. B. 2006. The diet of three synanthropic bats (Chiroptera: Molossidae) from eastern Madagascar. Acta Chiropterologica 8:439–444.Google Scholar
ANDRIANAIVOARIVELO, R. A., RAMILIJAONA, O. R., RACEY, P. A., RAZAFINDRAKOTO, N. & JENKINS, R. K. B. 2011. Feeding ecology, habitat use and reproduction of Rousettus madagascariensis Grandidier, 1928 (Chiroptera: Pteropodidae) in eastern Madagascar. Mammalia 75:69–78.Google Scholar
BLOCH, C. P., STEVENS, R. D. & WILLIG, M. R. 2011. Body size and resource competition in New World bats: a test of spatial scaling laws. Ecography 34:460–468.Google Scholar
CARDIFF, S. G. 2006. Bat cave selection and conservation at Ankarana, northern Madagascar. MA thesis, Columbia University, New York. 65 pp.Google Scholar
CARDIFF, S. G. & BEFOUROUACK, J. 2003. The Réserve Spéciale d'Ankarana. Pp. 1501–1507 in Goodman, S. M. & Benstead, J. P. (eds.). The natural history of Madagascar. University of Chicago Press, Chicago.Google Scholar
CERLING, T. E., HART, J. A. & HART, T. B. 2004. Stable isotope ecology in the Ituri Forest. Oecologia 138:5–12.Google Scholar
CHASE, J. M. & LEIBOLD, M. A. 2003. Ecological niches. Linking classical and contemporary approaches. University of Chicago Press, Chicago. 212 pp.CrossRefGoogle Scholar
CLARK, P. J. & EVANS, F. C. 1954. Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35:445–453.Google Scholar
DAMMHAHN, M. & KAPPELER, P. M. (2013). Stable isotope analyses reveal dense trophic species packing and clear niche differentiation in a Malagasy primate community. American Journal of Physical Anthropology. doi: 10.1002/ajpa.22426.Google Scholar
DAMMHAHN, M., SOARIMALALA, V. & GOODMAN, S. M. 2013. Trophic niche differentiation and microhabitat utilization in a species-rich montane forest small mammal community of eastern Madagascar. Biotropica 45:111–118.CrossRefGoogle Scholar
DENIRO, M. J. & EPSTEIN, S. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42:495–506.Google Scholar
DENIRO, M. J. & EPSTEIN, S. 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45:341–351.Google Scholar
EGGERS, T. & JONES, T. H. 2000. You are what you eat . . . or are you? Trends in Ecology and Evolution 15:265–266.Google Scholar
FENTON, M. B. 1990. The foraging behaviour and ecology of animal-eating bats. Canadian Journal of Zoology 68:411–422.CrossRefGoogle Scholar
FLEMING, T. H., NUNEZ, R. A. & STERNBERG, L. S. 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.Google Scholar
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
GOODMAN, S. M. 2011. Les chauves-souris de Madagascar. Association Vahatra, Antananarivo. 129 pp.Google Scholar
GOODMAN, S. M., ANDRIAFIDISON, D., ANDRIANAIVOARIVELO, R., CARDIFF, S. G., IFTICENE, E., JENKINS, R. K. B., KOFOKY, A., MBOHOAHY, T., RAKOTONDRAVONY, D., RANIVO, J., RATRIMOMANARIVO, F., RAZAFIMANAHAKA, J. & RACEY, P. A. 2005. The distribution and conservation of bats in the dry regions of Madagascar. Animal Conservation 8:153–165.CrossRefGoogle Scholar
GOODMAN, S. M., CARDIFF, S. G., RANIVO, J., RUSSELL, A. L. & YODER, A. D. 2006. A new species of Emballonura (Chiroptera: Emballonuridae) from the dry regions of Madagascar. American Museum Novitates 3538:1–24.Google Scholar
GOODMAN, S. M., RAMASINDRAZANA, B., MAMINIRINA, C. P., SCHOEMAN, M. C. & APPLETON, B. 2011. Morphological, bioacoustical, and genetic variation in Miniopterus bats from eastern Madagascar, with the description of a new species. Zootaxa 2880:1–19.Google Scholar
GOODMAN, S. M., TAYLOR, P. J., RATRIMOMANARIVO, F. & HOOFER, S. 2012 a. The genus Neoromicia (Family Vespertilionidae) in Madagascar, with the description of a new species. Zootaxa 3250:1–25.Google Scholar
GOODMAN, S. M., PUECHMAILLE, S. J., FRIEDLI-WEYENETH, N., GERLACH, J., RUEDI, M., SCHOEMAN, M. C., STANLEY, W. T. & TEELING, E. C. 2012 b. Phylogeny of emballonurini bats (Family Emballonuridae): new genus and new species of Emballonuridae from Madagascar. Journal of Mammalogy 93:1440–1455.Google Scholar
HERRERA, L. G., HOBSON, K. A., MANZOA, A. A, A., ESTRADAB, D. B, D., SÁNCHEZ-CORDERO, V. & MÉNDEZC, G. C, G. 2001. The role of fruits and insects in the nutrition of frugivorous bats: evaluating the use of stable isotope models. Biotropica 33:520–528.Google Scholar
HERRERA, L. G., GUTIERREZ, E., HOBSON, K. A., ALTUBE, B., DIAZ, W. G. & SANCHES-CORDERO, V. 2002. Sources of assimilated protein in five species of New World frugivorous bats. Oecologia 133:280–287.CrossRefGoogle ScholarPubMed
HUBBELL, S. P. 2001. The unified neutral theory of species abundance and diversity. Princeton University Press, Princeton. 448 pp.Google Scholar
HUTCHINSON, G. E. 1957. Concluding remarks. Cold Spring Harbor Symposium. Quantitative Biology 22:415–427.Google Scholar
JACKSON, A. L., INGER, R., PARNELL, A. C. & BEARHOP, S. 2011. Comparing isotopic niche widths among and within communities. SIBER – Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80:595–602.CrossRefGoogle ScholarPubMed
KINGSTON, T. 2009. Analysis of species diversity of bat assemblages. Pp. 158–176 in Kunz, T. H. & Parsons, S. (eds.). Ecological and behavioral methods for the study of bats. The Johns Hopkins University Press, Baltimore.Google Scholar
KREBS, C. J. 1998. Ecological methodology. Addison-Welsey Educational Publishers, Menlo Park. 654 pp.Google Scholar
LAYMAN, C. A., ARRINGTON, D. A., MONTANA, C. G. & POST, D. M. 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48.Google Scholar
MAUFFREY, J. F. & CATZEFLIS, F. 2003. Ecological and isotopic discrimination of syntopic rodents in a Neotropical forest of French Guiana. Journal of Tropical Ecology 19:209–214.Google 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.Google Scholar
MEDINA, E. & MINCHIN, P. 1980. Stratification of δ13C values of leaves in Amazonian rain forests. Oecologia 45:377–378.CrossRefGoogle ScholarPubMed
NORBERG, U. M. 1994. Wing design, flight performance, and habitat use in bats. Pp. 205–239 in Wainwright, P. C. & Reilly, S. M. (eds.). Ecological morphology. Integrative organismal biology. University of Chicago Press, Chicago.Google Scholar
PETERSON, R. L., EGER, J. L. & MITCHELL, L. 1995. Chiroptères. Faune de Madagascar volume 84. Muséum national d'Histoire naturelle, Paris. 204 pp.Google Scholar
PICOT, M., JENKINS, R. K. B., RAMILIJAONA, O., RACEY, P. A. & CARRIÈRE, S. M. 2007. The feeding ecology of Eidolon dupreanum (Pteropodidae) in eastern Madagascar. African Journal of Ecology 45:645–650.Google Scholar
RAKOTOARIVELO, A. A., RANAIVOSON, N., RAMILIJAONAO., R. O., R., KOFOKY, A. F., RACEY, P. A. & JENKINS, R. K. B. 2007. Seasonal food habits of five sympatric forest microchiropterans in western Madagascar. Journal of Mammalogy 88:959–966.Google Scholar
RAKOTOARIVELO, A. A., RALISATA, M., RAMILIJAONAO., R. O., R., RAKOTOMALALA, M. R., RACEY, P. A. & JENKINS, R. K. B. 2009. The food habits of a Malagasy giant: Hipposideros commersoni (E. Geoffroy, 1813). African Journal of Ecology 47:283–288.Google Scholar
RAMASINDRAZANA, B. & GOODMAN, S. M. 2012. Bio-écologie des chauves-souris du Parc National de Tsimanampetsotsa. 1. Identification bioacoustique et habitat préférentiel. Malagasy Nature 6:103–116.Google Scholar
RAMASINDRAZANA, B., GOODMAN, S. M., SCHOEMAN, M. C. & APPLETON, B. 2011. Identification of cryptic species of Miniopterus bats (Chiroptera: Miniopteridae) from Madagascar and the Comoros using bioacoustics overlaid on molecular genetic and morphological characters. Biological Journal of the Linnean Society 104:284–302.Google Scholar
RAMASINDRAZANA, B., RAJEMISON, B. & GOODMAN, S. M. 2012. Bio-écologie des chauves-souris de Parc National de Tsimanampetsotsa. 2. Variation interspécifique et saisonnière du régime alimentaire. Malagasy Nature 6:117–124.Google Scholar
RATRIMOMANARIVO, F. H. 2007. Etude du régime alimentaire d'Eidolon dupreanum (Chiroptera: Pteropodidae) dans la région anthropisée des Hautes Terres du centre de Madagascar. Revue d'Ecologie (Terre Vie) 62:229–244.Google Scholar
RAZAKARIVONY, V. R., RAJEMISON, B. & GOODMAN, S. M. 2005. The diet of Malagasy Microchiroptera based on stomach contents. Mammalian Biology 70:312–316.Google Scholar
REX, K., KELM, D. H., WIESNER, K., KUNZ, T. H. & VOIGT, C. C. 2008. Species richness and 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. Specialization and omnivory in diverse mammalian assemblages. Ecoscience 17:37–46.Google Scholar
REX, K., MICHENER, R., KUNZ, T. H. & VOIGT, C. C. 2011. Vertical stratification of Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae) revealed by stable carbon isotopes. Journal of Tropical Ecology 27:211–222.Google Scholar
SCHNITZLER, H. U., MOSS, C. F. & DENZINGER, A. 2003. From spatial orientation to food acquisition in echolocating bats. Trends in Ecology and Evolution 18:386–394.CrossRefGoogle Scholar
SCHOEMAN, M. C. & JACOBS, D. 2011. The relative influence of competition and prey defences on the trophic structure of animalivorous bat ensembles. Oecologia 166:493–506.Google Scholar
SFENTHOURAKIS, S., TZANATOS, E. & GIOKAS, S. 2005. Species co-occurrence: the case of congeneric species and a causal approach to patterns of species associations. Global Ecology and Biogeography 15:39–49.Google Scholar
SIEMERS, B. M. & SCHNITZLER, H. U. 2004. Echolocation signals reflect niche differentiation in five sympatric congeneric bat species. Nature 429:657–661.Google Scholar
STEVENS, R. D. & WILLIG, M. R. 2000. Density compensation in New World bat communities. Oikos 89:367–377.Google Scholar
TURNER, T. F., COLLYER, M. L. & KRABBENHOFT, T. J. 2010. A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91:2227–2233.Google Scholar
VANDERKLIFT, M. A. & PONSARD, S. 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182.Google Scholar
VOIGT, C. C. 2010. Insights into strata use of forest animals using the ‘canopy effect’. Biotropica 42:634–637.Google Scholar
VOIGT, C. C. & KELM, D. H. 2006. Host preferences of the common vampire bat Desmodus rotundus assessed by stable isotopes. Journal of Mammalogy 87:1–6.CrossRefGoogle Scholar
VOIGT, C. C., REX, K., MICHENER, R. & SPEAKMAN, J. R. 2008. Nutrient routing in omnivorous animals tracked by stable carbon isotopes in tissue and exhaled breath. Oecologia 157:31–40.Google Scholar
VOIGT, C. C., KELM, D. H., BRADLEY, B. J. & ORTMANN, S. 2009. Dietary analysis of plant-visiting bats. Pp. 593–609 in Kunz, T. H. & Parsons, S. (eds.). Ecological and behavioral methods for the study of bats. The Johns Hopkins University Press, Baltimore.Google Scholar
WHITAKER, J. O., MCCRACKEN, G. F. & SIEMERS, B. M. 2009. Food habits analysis of insectivorous bats. Pp. 567–592 in Kunz, T. H. & Parsons, S. (eds.). Ecological and behavioral methods for the study of bats. The Johns Hopkins University Press, Baltimore.Google Scholar