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Coexistence of morphologically similar bats (Vespertilionidae) on Madagascar: stable isotopes reveal fine-grained niche differentiation among cryptic species

Published online by Cambridge University Press:  30 December 2014

Melanie Dammhahn ,
Claude Fabienne Rakotondramanana  and
Steven M. Goodman
Melanie Dammhahn*
Affiliation:
Animal Ecology, Institute for Biochemistry and Biology, Faculty of Natural Sciences, University of Potsdam, Maulbeerallee 1, 14469 Potsdam, Germany
Claude Fabienne Rakotondramanana
Affiliation:
Association Vahatra, BP 3972, Antananarivo 101, Madagascar Département de Biologie Animale, Université d’Antananarivo, BP 906, Antananarivo 101, Madagascar
Steven M. Goodman
Affiliation:
Association Vahatra, BP 3972, Antananarivo 101, Madagascar Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA
*
1Corresponding author: Email: [email protected]
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Abstract:

Based on niche theory, closely related and morphologically similar species are not predicted to coexist due to overlap in resource and habitat use. Local assemblages of bats often contain cryptic taxa, which co-occur despite notable similarities in morphology and ecology. We measured in two different habitat types on Madagascar levels of stable carbon and nitrogen isotopes in hair (n = 103) and faeces (n = 57) of cryptic Vespertilionidae taxa to indirectly examine whether fine-grained trophic niche differentiation explains their coexistence. In the dry deciduous forest (Kirindy), six sympatric species ranged over 6.0‰ in δ15N, i.e. two trophic levels, and 4.2‰ in δ13C with a community mean of 11.3‰ in δ15N and −21.0‰ in δ13C. In the mesic forest (Antsahabe), three sympatric species ranged over one trophic level (δ15N: 2.4‰, δ13C: 1.0‰) with a community mean of 8.0‰ δ15N and −21.7‰ in δ13C. Multivariate analyses and residual permutation of Euclidian distances in δ13C–δ15N bi-plots revealed in both communities distinct stable isotope signatures and species separation for the hair samples among coexisting Vespertilionidae. Intraspecific variation in faecal and hair stable isotopes did not indicate that seasonal migration might relax competition and thereby facilitate the local co-occurrence of sympatric taxa.

Keywords

Chiropteracommunity structurecongeneric speciesecological nichesmigrationNeoromiciaPipistrellusScotophilusstable carbonstable nitrogen
Type
Research Article
Information
Journal of Tropical Ecology , Volume 31 , Issue 2 , March 2015 , pp. 153 - 164
Copyright
Copyright © Cambridge University Press 2014 

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References

LITERATURE CITED

ALAGAILI, A. N., JAMES, D. A. & MOHAMMED, O. B. 2011. Timing and pattern of molt in Kuhl's bat, Pipistrellus kuhlii, in Saudi Arabia. Acta Chiropterologica 13:465–470.Google Scholar
AMBROSE, S. H. & DENIRO, M. J. 1986. The isotopic ecology of east African mammals. Oecologia 69:395–406.Google Scholar
BARRATT, E. M., DEAVILLE, R., BURLAND, T. M., JONES, G., RACEY, P. A. & WAYNE, R. K. 1997. DNA answers the call of pipistrelle bat species. Nature 387:138–139.CrossRefGoogle ScholarPubMed
BATES, P. J. J., RATRIMOMANARIVO, F. H., HARRISON, D. L. & GOODMAN, S. M. 2006. A description of a new species of Pipistrellus (Chiroptera: Vespertilionidae) from Madagascar with a review of related Vespertilioninae from the island. Acta Chiropterologica 8:299–324.Google Scholar
BATTISTINI, R. 1972. Madagascar relief and main types of landscape. Pp. 1–22 in Battistini, R. & Richard-Vindard, G. (eds.). Biogeography and ecology in Madagascar. W. Junk, The Hague.CrossRefGoogle 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
BOECKLEN, W. J., YARNES, C. T., COOK, B. A. & JAMES, A. C. 2011. On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution and Systematics 42:411–440.Google Scholar
BOURGEAT, F. 1996. Les grandes unités pédo-morphologiques dans la région de Morondava. Pp. 21–32 in Ganzhorn, J. U. & Sorg, J. P. (eds.). Ecology and economy of a tropical dry forest in Madagascar. Goltze, Göttingen.Google Scholar
CHASE, J. M. & LEIBOLD, M. A. 2003. Ecological niches. Linking classical and contemporary approaches. The University of Chicago Press, Chicago. 212 pp.Google Scholar
CROWLEY, B. E., THORÉN, S., RASOAZANABARY, E., VOGEL, E. R., BARRETT, M. A., ZOHDY, S., BLANCO, M. B., MCGOOGAN, K. C., ARRIGO-NELSON, S. J., IRWIN, M. T., WRIGHT, P. C., RADESPIEL, U., GODFREY, L. R., KOCH, P. L. & DOMINY, N. J. 2011. Explaining geographical variation in the isotope composition of mouse lemurs (Microcebus). Journal of Biogeography 38:2106–2121.CrossRefGoogle Scholar
DAMMHAHN, M. & GOODMAN, S. M. 2014. Trophic niche differentiation and microhabitat utilization revealed by stable isotope analyses in a dry-forest bat assemblage at Ankarana, northern Madagascar. Journal of Tropical Ecology 30:97–109.Google Scholar
DAMMHAHN, M. & KAPPELER, P. M. 2008. Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. International Journal of Primatology 29:1567–1589.Google Scholar
DAMMHAHN, M. & KAPPELER, P. M. 2010. Scramble or contest competition over food in solitarily foraging mouse lemurs (Microcebus spp.): new insights from stable isotopes. American Journal of Physical Anthropology 141:181–189.Google Scholar
DAMMHAHN, M. & KAPPELER, P. M. 2014. Stable isotope analyses reveal dense trophic species packing and clear niche differentiation in a Malagasy primate community. American Journal of Physical Anthropology 153:249–259.Google Scholar
DARWIN, C. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, London. 502 pp.Google 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.CrossRefGoogle Scholar
FAHR, J. & KALKO, E. K. V. 2011. Biome transitions as centres of diversity: habitat heterogeneity and diversity patterns of west African bat assemblages across spatial scales. Ecography 34:177–195.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.CrossRefGoogle Scholar
FRASER, E. E., LONGSTAFFE, F. J. & FENTON, M. B. 2013. Moulting matters: the importance of understanding moulting cycles in bats when using fur for endogenous marker analysis. Canadian Journal of Zoology 91:533–544.CrossRefGoogle Scholar
GOODMAN, S. M. 2011. Les chauves-souris de Madagascar. Association Vahatra, Antananarivo. 129 pp.Google Scholar
GOODMAN, S. M., JENKINS, R. K. B. & RATRIMOMANARIVO, F. H. 2005. A review of the genus Scotophilus (Chiroptera: Vespertilionidae) on Madagascar, with the description of a new species. Zoosystema 27:867–882.Google Scholar
GOODMAN, S. M., RATRIMOMANARIVO, F. H. & RANDRIANANDRIANINA, F. L. H. 2006. A new species of Scotophilus (Chiroptera: Vespertilionidae) from western Madagascar. Acta Chiropterologica 8:21–37.Google Scholar
GOODMAN, S. M., RASELIMANANA, A. P. & WILME, L. (eds.) 2007. Inventaires de la faune et de la flore du couloir forestier d’Anjozorobe-Angavo. Recherche pour le développement, série science biologique 24: 1–217.Google Scholar
GOODMAN, S. M., TAYLOR, P. J., RATRIMOMANARIVO, F. & HOOFER, S. 2012. The genus Neoromicia (Family Vespertilionidae) in Madagascar, with the description of a new species. Zootaxa 3250:1–25.Google Scholar
GOODMAN, S. M., RAKOTONDRAMANANA, C. F., RAMASINDRAZANA, B., MONADJEM, A., SCHOEMAN, M. C., TAYLOR, A. C., NAUGHTON, K. & APPLETON, B. In press. An integrative approach to characterize Malagasy bats of the subfamily Vespertilioninae Gray, 1821, with the description of a new species of Hypsugo. Zoological Journal of the Linnean Society.Google Scholar
HUBBELL, S. P. 2001. The unified neutral theory of species abundance and diversity. Princeton University Press, Princeton. 392 pp.Google Scholar
KALKO, E. K. V. & SCHNITZLER, H. U. 1993. Plasticity in echolocation signals of European pipistrelle bats in search flight: implications for habitat use and prey detection. Behavioral Ecology and Sociobiology 33:415–428.Google Scholar
KOUBÍNOVÁ, D., IRWIN, N., HULVA, P., KOUBEK, P. & ZIMA, J. 2013. Hidden diversity in Senegalese bats and associated findings in the systematics of the family Vespertilionidae. Frontiers in Zoology 10:48.Google Scholar
KRÜGER, F., CLARE, E. L., GREIF, S., SIEMERS, B. M., SYMONDSON, W. O. C. & SOMMER, R. S. 2014. An integrative approach to detect subtle trophic niche differentiation in the sympatric trawling bat species Myotis dasycneme and Myotis daubentonii. Molecular Ecology 23:3657–3671.Google Scholar
LAM, M. M.-Y., MARTIN-CREUZBURG, D., ROTHHAUPT, K.-O., SAFI, K., YOHANNES, E. & SALVARINA, I. 2013. Tracking diet preferences of bats using stable isotope and fatty acid signatures of faeces. PLoS ONE 8:e83452.CrossRefGoogle ScholarPubMed
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
LOSOS, J. B. 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity. Ecology Letters 11:995–1007.Google Scholar
MACARTHUR, R. H. & LEVINS, R. 1967. The limiting similarity, convergence, and divergence of coexisting species. American Naturalist 101:377–385.Google Scholar
MARSHALL, J. D., BROOKS, R. & LAJTHA, K. 2007. Sources of variation in the stable isotopic composition of plants. Pp. 22–60 in Michener, R. & Lajtha, K. (eds.). Stable isotopes in ecology and environmental science. Blackwell Publishing, Malden.Google Scholar
MEDINA, E. & MINCHIN, P. 1980. Stratification of δ13C values of leaves in Amazonian rain forests. Oecologia 45:377–378.Google Scholar
MIRÓN, L. L., HERRERA, L. G., RAMIREZ, N. & HOBSON, K. A. 2006. Effect of diet quality on carbon and nitrogen turnover and isotopic discrimination in blood of a New World nectarivorous bat. Journal of Experimental Biology 209:541–548.Google Scholar
MOAT, J. & SMITH, P. 2007. Atlas of the vegetation of Madagascar. Royal Botanic Garden, Kew. 124 pp.Google Scholar
MONADJEM, A., TAYLOR, P. J., COTTERILL, F. P. D. & SCHOEMAN, M. C. 2010. Bats of central and southern Africa: a biogeographic and taxonomic synthesis. Wits University Press, Johannesburg. 596 pp.Google Scholar
MONADJEM, A., RICHARDS, L., TAYLOR, P. J. & STOFFBERG, S. 2013. High diversity of pipistrelloid bats (Vespertilionidae: Hypsugo, Neoromicia, and Pipistrellus) in a West African rainforest with the description of a new species. Zoological Journal of the Linnean Society 167:191–207.Google Scholar
MOUSSY, C., HOSKEN, D. J., MATHEWS, F., SMITH, G. C., AEGERTER, J. N. & BEARHOP, S. 2013. Migration and dispersal patterns of bats and their influence on genetic structure. Mammal Review 43:183–195.Google Scholar
PARNELL, A. C., INGER, R., BEARHOP, S. & JACKSON, A. L. 2010. Source partitioning using stable isotopes: coping with too much variation. PloS ONE 5:e9672.Google Scholar
RAKOTOARIVELO, A. A., RANAIVOSON, N., RAMILIJAONA RAVOAHANGIMALALA, O., 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
RAKOTONDRAMANANA, C. F. & GOODMAN, S. M. 2011. Inventaire de chauves-souris dans la concession forestière de Kirindy CNFEREF, Morondava, Madagascar. Malagasy Nature 5:109–120.Google Scholar
RAKOTONDRAMANANA, C. F., GOODMAN, S. M., RAMASINDRAZANA, B. & SCHOEMAN, M. C. 2014. Vocalisations de Pipistrellus spp. sensu lato de Madagascar: Expérience sur l’effet de confinement. Malagasy Nature 8:80–88.Google Scholar
RASELIMANANA, A. P. & GOODMAN, S. M. 2007. Introduction. In Inventaires de la faune et de la flore du couloir forestier d’Anjozorobe-Angavo. Goodman, S. M., Raselimanana, A. P. & Wilmé, L. (eds.). Recherche pour le développement, série science biologique 24:1–19.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.CrossRefGoogle Scholar
SALVARINA, I., YOHANNES, E., SIEMERS, B. M. & KOSELJ, K. 2013. Advantages of using fecal samples for stable isotope analysis in bats: evidence from a triple isotopic experiment. Rapid Communications in Mass Spectrometry 27:1945–1953.Google 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
SIEMERS, B., GREIF, S., BORISSOV, I., VOIGT-HEUCKE, S. & VOIGT, C. 2011. Divergent trophic levels in two cryptic sibling bat species. Oecologia 166:69–78.Google Scholar
SIKES, R. S., GANNON, W. L. & THE ANIMAL CARE AND USE COMMITTEE OF THE AMERICAN SOCIETY OF MAMMALOGISTS. 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92:235–253.Google Scholar
SIMMONS, N. B. 2005. Order Chiroptera. Pp. 312–529 in Wilson, D. E. & Reeder, D. M. (eds.). Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore.Google Scholar
SORG, J.-P. & ROHNER, U. 1996. Climate and tree phenology of the dry deciduous forest of the Kirindy Forest. Pp. 57–80 in Ganzhorn, J. U. & Sorg, J. P. (eds.). Ecology and economy of a tropical dry forest in Madagascar. Goltze, Göttingen.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
VIOLLE, C., NEMERGUT, D. R., PU, Z. & JIANG, L. 2011. Phylogenetic limiting similarity and competitive exclusion. Ecology Letters 14:782–787.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. & MATT, F. 2004. Nitrogen stress causes unpredictable enrichment of 15N in two nectar-feeding bat species. Journal of Experimental Biology 207:1741–1748.Google Scholar
VOIGT, C. C., GRASSE, P., REX, K., HETZ, S. K. & SPEAKMAN, J. R. 2008. Bat breath reveals metabolic substrate use in free-ranging vampires. Journal of Comparative Physiology B 178:9–16.Google Scholar
VOIGT, C., HELBIG-BONITZ, M., KRAMER-SCHADT, S. & KALKO, E. K. V. 2014. The third dimension of bat migration: evidence for elevational movements of Miniopterus natalensis along the slopes of Mount Kilimanjaro. Oecologia 174:751–764.CrossRefGoogle ScholarPubMed
VON HELVERSEN, O., HELLER, K. G., MAYER, F., NEMETH, A., VOLLETH, M. & GOMBKÖTÖ, P. 2001. Cryptic mammalian species: a new species of whiskered bat (Myotis alcathoe n. sp.) in Europe. Naturwissenschaften 88:217–223.Google Scholar
WEST, J. B., BOWEN, G. J., CERLING, T. E. & EHLERINGER, J. R. 2006. Stable isotopes as one of nature's ecological recorders. Trends in Ecology and Evolution 21:408–414.Google Scholar
WIENS, J. J. & GRAHAM, C. H. 2005. Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics 36:519–539.Google 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