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Food resource partitioning in syntopic nectarivorous bats on Puerto Rico

Published online by Cambridge University Press:  24 April 2014

J. Angel Soto-Centeno*
Affiliation:
Division of Mammalogy, American Museum of Natural History, New York, NY 10024, USA Department of Biology, Eastern Michigan University, Ypsilanti, MI 48197, USA
Donald L. Phillips
Affiliation:
US Environmental Protection Agency, Office of Research and Development, National Health and Environmental Effects Research Laboratory, Western Ecology Division, Corvallis, OR 97333, USA
Allen Kurta
Affiliation:
Department of Biology, Eastern Michigan University, Ypsilanti, MI 48197, USA
Keith A. Hobson
Affiliation:
Environment Canada, 11 Innovation Blvd., Saskatoon, Saskatchewan, S7N 3H5, Canada
*
1Corresponding author. Email: asoto-centeno@amnh.org

Abstract:

Understanding the dietary needs of syntopic species is essential for examining species coexistence and resource partitioning. We analysed stable isotopes of carbon (δ13C) and nitrogen (δ15N) to estimate the diet of two putative nectarivorous bats on Puerto Rico, the brown flower bat (Erophylla bombifrons) and the Greater Antillean long-tongued bat (Monophyllus redmani). Isotopic ratios of δ13C and δ15N were obtained from whole blood of both species of bat and tissues of available plant foods and insect prey over 15 wk at the same locality. We used a concentration-dependent Bayesian mixing model to determine probability distributions of feasible dietary contributions for major potential foods used by each species of bat. Additionally, separate dietary estimates were conducted for males and non-reproductive, pregnant and lactating females to determine differences due to reproductive condition. Insects were an important source of protein for M. redmani, whereas E. bombifrons obtained most of its protein from plants. In both species of bat, lactating females had lower assimilated nitrogen than males, suggesting more reliance on plants for protein. We observed no intraspecific differences in assimilated carbon among reproductive conditions. Flight and lactation are energetically expensive and may explain the increased consumption of high-energy foods, such as fruit or nectar, in lactating female bats. Comparison of isotopes between E. bombifrons and M. redmani illustrate the differential use of food resources by these insular syntopic species of bat.

Type
Research Article
Creative Commons
This is a work of the U.S. Government and is not subject to copyright protection in the United States.
Copyright
Copyright © Cambridge University Press 2014

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References

LITERATURE CITED

ANTHONY, E. L. P. 1988. Age determination. Pp. 4758 in Kunz, T. H. (ed.). Ecological and behavioral methods for the study of bats. (First edition). Smithsonian Institution Press, Washington, DC.Google Scholar
BARCLAY, R. M. R. 1994. Constraints on reproduction by flying vertebrates: energy and calcium. American Naturalist 144:10211031.Google Scholar
BEN-DAVID, M. & FLAHERTY, E. A. 2012. Stable isotopes in mammalian research: a beginner's guide. Journal of Mammalogy 93:312328.CrossRefGoogle Scholar
BONACCORSO, F. J. 1979. Foraging and reproductive ecology in a Panamanian bat community. Bulletin of the Florida State Museum 24:359408.Google Scholar
BUMRUNGSRI, S., LEELAPAIBUL, W. & RACEY, P. A. 2007. Resource partitioning in sympatric Cynopterus bats in lowland tropical rain forest, Thailand. Biotropica 39:241248.CrossRefGoogle Scholar
DATZMANN, T., VON HELVERSEN, O. & MAYER, F. 2010. Evolution of nectarivory in phyllostomid bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia). BMC Evolutionary Biology 10:114.CrossRefGoogle ScholarPubMed
DAVIS, D. E. & GOLLEY, F. B. 1963. Energy dynamics of populations. Pp. 244265 in Davis, D. E. & Golley, F. B. (eds.). Principles in mammalogy. Reinhold Publishing, New York.Google Scholar
DELORME, M. & THOMAS, D. W. 1996. Nitrogen and energy requirements of the short-tailed fruit bat (Carollia perspicillata): fruit bats are not nitrogen constrained. Journal of Comparative Physiology B 166:427434.CrossRefGoogle Scholar
DENIRO, M. J. & EPSTEIN, S. 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45:341351.CrossRefGoogle Scholar
FINKE, M. D. 2007. Estimate of chitin in raw whole insects. Zoo Biology 26:105115.CrossRefGoogle ScholarPubMed
FLEMING, T. H., HOOPER, E. T. & WILSON, D. E. 1972. Three Central American bat communities: structure, reproductive cycles, and movement patterns. Ecology 53:555569.CrossRefGoogle Scholar
FLEMING, T. H., NUÑEZ, R. A. & LOBO, S. 1993. Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis. Oecologia 94:7275.CrossRefGoogle Scholar
FREEMAN, P. 1995. Nectarivorous feeding mechanisms in bats. Biological Journal of the Linnean Society 56:439463.CrossRefGoogle Scholar
GANNON, M. R., KURTA, A., RODRÍGUEZ-DURÁN, A. & WILLIG, M. R. 2005. Bats of Puerto Rico: an island focus and a Caribbean perspective. Texas Tech University Press, Lubbock. 224 pp.Google Scholar
GIANNINI, N. P. & KALKO, E. K. V. 2004. Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 2:209220.CrossRefGoogle Scholar
HERBST, L. H. 1986. The role of nitrogen from fruit pulp in the nutrition of the frugivorous bat Carollia perspicillata. Biotropica 18:3944.CrossRefGoogle Scholar
HERRERA, M. L. G., HOBSON, K. A., ADRIANA MANZO ESTRADA, D., SANCHEZ-CORDERO, V. & MENDEZ, G. 2001a. The role of fruits and insects in the nutrition of frugivorous bats: evaluating the use of stable isotope models. Biotropica 33:520528.CrossRefGoogle Scholar
HERRERA, M. L. G., HOBSON, K. A. M. L. M., RAMÍREZ, P. N., MÉNDEZ, C. G. & SÁNCHEZ-CORDERO, V. 2001b. Sources of protein in two species of phytophagous bats in a seasonal dry forest: Evidence from stable-isotope analysis. Journal of Mammalogy 82:352361.2.0.CO;2>CrossRefGoogle Scholar
HERRERA, M. L. G., GUTIERREZ, E., HOBSON, K., ALTUBE, B., DÍAZ, W. & SÁNCHEZ-CORDERO, V. 2002. Sources of assimilated protein in five species of New World frugivorous bats. Oecologia 133:280287.CrossRefGoogle ScholarPubMed
HOBSON, K. A., GIBBS, H. L. & GLOUTNEY, M. 1997. Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotope analysis. Canadian Journal of Zoology 75:17201723.CrossRefGoogle Scholar
HOBSON, K. A., STIRLING, I. & ANDRIASHEK, D. S. 2009. Isotopic homogeneity of breath CO2 from fasting and berry-eating polar bears: implications for tracing reliance on terrestrial foods in a changing Arctic? Canadian Journal of Zoology 87:5055.CrossRefGoogle Scholar
HOLM, S. 1979. A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6:6570.Google Scholar
HOOD, W. R., OFTEDAL, O. T. & KUNZ, T. H. 2006. Variation in body composition of female big brown bats (Eptesicus fuscus) during lactation. Journal of Comparative Physiology B 176:807819.CrossRefGoogle ScholarPubMed
HOOD, W. R., VOLTURA, M. B. & OFTEDAL, O. T. 2009. Methods of measuring milk composition and yield in small mammals. Pp. 529553 in Kunz, T. H. & Parsons, S. (eds.). Ecological and behavioral methods for the study of bats. (Second edition). The Johns Hopkins University Press, Baltimore.Google Scholar
JENNESS, R. & STUDIER, E. 1976. Lactation and milk. Pp. 201218 in Baker, R. J., Knox Jones, J. & Carter, D. C. (eds.). Biology of bats in the New World family Phyllostomidae. Special publications of the Museum of Texas Technical University, Lubbock.Google Scholar
JONES, K. E., BARLOW, K. E., VAUGHAN, N., RODRÍGUEZ-DURÁN, A. & GANNON, M. R. 2001. Short-term impacts of extreme environmental disturbance on the bats of Puerto Rico. Animal Conservation 4:5966.CrossRefGoogle Scholar
KUNZ, T. H. 1987. Post-natal growth and energetics of suckling bats. Pp. 395420 in Fenton, M. B., Racey, P. A. & Rayner, J. M. V. (eds.). Recent advances in the study of bats. Cambridge University Press, Cambridge.Google Scholar
KUNZ, T. H. & KURTA, A. 1988. Capture methods and holding devices. Pp. 129 in Kunz, T. H. (ed.). Ecological and behavioral methods for the study of bats. (First edition). Smithsonian Institution Press, Washington.Google Scholar
KUNZ, T. H. & NAGY, K. A. 1988. Methods of energy budget analysis. Pp. 277302 in Kunz, T. H. (ed.). Ecological and behavioral methods for the study of bats. (First edition). Smithsonian Institution Press, Washington.Google Scholar
KUNZ, T. H., OFTEDAL, O. T., ROBSON, S. K., KRETZMANN, M. B. & KIRK, C. 1995. Changes in milk composition during lactation in three species of insectivorous bats. Journal of Comparative Physiology B 164:543551.CrossRefGoogle ScholarPubMed
KURTA, A., BELL, G. P., NAGY, K. A. & KUNZ, T. H. 1989. Energetics of pregnancy and lactation in free-ranging little brown bats (Myotis lucifugus). Physiological Zoology 62:804818.CrossRefGoogle Scholar
KURTA, A., KUNZ, T. H. & NAGY, K. A. 1990. Energetics and water flux of free-ranging big brown bats (Eptesicus fuscus) during pregnancy and lactation. Journal of Mammalogy 71:5965.CrossRefGoogle Scholar
LADLE, R. J., FIRMINO, J. V. L., MALHADO, A. C. M. & RODRÍGUEZ-DURÁN, A. 2012. Unexplored diversity and conservation potential of Neotropical hot caves. Conservation Biology 26:978982.CrossRefGoogle ScholarPubMed
LITVAITIS, J. A., TITUS, K. & ANDERSON, E. M. 1994. Measuring vertebrate use of terrestrial habitats and foods. Pp. 254274 in Bookhout, T. A. (ed.). Research and management techniques for wildlife and habitats. The Wildlife Society, Bethesda.Google Scholar
MANCINA, C. A. & HERRERA, M. L. G. 2010. Disparate feeding strategies used by syntopic Antillean nectarivorous bats to obtain dietary protein. Journal of Mammalogy 91:960966.CrossRefGoogle Scholar
MIRÓN, M. L. L., HERRERA, M. L. G., RAMÍREZ, P. 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 209:541548.CrossRefGoogle Scholar
NICOLSON, S. W. & THORNBURG, R. W. 2007. Nectar chemistry. Pp. 215264 in Nicolson, S. W., Nepi, M. & Pacini, E. (eds.). Nectaries and nectar. Springer-Verlag, Berlin.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
PHILLIPS, D. L. 2012. Converting isotope values to diet composition: the use of mixing models. Journal of Mammalogy 93:342352.CrossRefGoogle Scholar
PHILLIPS, D. L. & GREGG, J. W. 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261269.CrossRefGoogle ScholarPubMed
PHILLIPS, D. L. & KOCH, P. L. 2002. Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114125.CrossRefGoogle ScholarPubMed
PHILLIPS, D. L., NEWSOME, S. D. & GREGG, J. W. 2005. Combining sources in stable isotope mixing models: alternative methods. Oecologia 144:520527.CrossRefGoogle ScholarPubMed
RACEY, P. A. 1988. Reproductive assessment on bats. Pp. 3146 in Kunz, T. H. (ed.). Ecological and behavioral methods for the study of bats. (First edition). Smithsonian Institution Press, Washington.Google Scholar
REX, K., CZACZKES, B. I., MICHENER, R., KUNZ, T. H. & VOIGT, C. C. 2010. Specialization and omnivory in diverse mammalian assemblages. Ecoscience 17:3746.CrossRefGoogle 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 27:211222.CrossRefGoogle Scholar
RODRÍGUEZ-DURÁN, A. 1998. Nonrandom aggregations and distribution of cave-dwelling bats in Puerto Rico. Journal of Mammalogy 79:141146.CrossRefGoogle Scholar
RODRÍGUEZ-DURÁN, A. & SOTO-CENTENO, J. A. 2003. Temperature selection by tropical bats roosting in caves. Journal of Thermal Biology 28:465468.CrossRefGoogle Scholar
SIKES, R. S., GANNON, W. L. & 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 92:235253.CrossRefGoogle Scholar
SILVA-TABOADA, G. 1979. Los murciélagos de Cuba. Editorial Academia, La Habana. 423 pp.Google Scholar
SIMMONS, N. B. 2005. Order Chiroptera. Pp. 312529 in Wilson, D. E. & Reeder, D. M. (eds.). Mammal species of the world: a taxonomic and geographic reference. (Third edition). The Johns Hopkins University Press, Baltimore.Google Scholar
SOTO-CENTENO, J. A. 2004. Dietary ecology of two nectarivorous bats, Erophylla sezekorni and Monophyllus redmani, on Puerto Rico. MS Thesis, Eastern Michigan University, Ypsilanti. 62 pp.Google Scholar
SOTO-CENTENO, J. A. & KURTA, A. 2006. Diet of two nectarivorous bats, Erophylla sezekorni and Monophyllus redmani (Phyllostomidae), on Puerto Rico. Journal of Mammalogy 87:1926.CrossRefGoogle Scholar
STERN, A. A., KUNZ, T. H., STUDIER, E. H. & OFTEDAL, O. T. 1997. Milk composition and lactational output in the greater spear-nosed bat, Phyllostomus hastatus. Journal of Comparative Physiology B 167:389398.CrossRefGoogle ScholarPubMed
THOMAS, D. W. 1988. Analysis of diets of plant visiting bats. Pp. 211220 in Kunz, T. H. (ed.). Ecological and behavioral methods for the study of bats. (First edition). Smithsonian Institution Press, Washington.Google Scholar
TSCHAPKA, M. 2005. Reproduction of the bat Glossophaga commissarisi (Phyllostomidae: Glossophaginae) in the Costa Rican rain forest during frugivorous and nectarivorous periods. Biotropica 37:409415.CrossRefGoogle Scholar
VOIGT, C. C. 2003. Low turnover rates of carbon isotopes in tissues of two nectar-feeding bat species. Journal of Experimental Biology 206:14191427.CrossRefGoogle ScholarPubMed
VOIGT, C. C. & MATT, F. 2004. Nitrogen stress causes unpredictable enrichments of 15N in two nectar-feeding bat species. Journal of Experimental Biology 207:17411748.CrossRefGoogle ScholarPubMed
VOIGT, C. C. & SPEAKMAN, J. R. 2007. Nectar-feeding bats fuel their high metabolism directly with exogenous carbohydrates. Functional Ecology 21:913921.CrossRefGoogle Scholar
VOIGT, C. C., SÖRGEL, K. & DECHMANN, D. K. N. 2010. Refueling while flying: foraging bats combust food rapidly and directly to power flight. Ecology 91:29082917.CrossRefGoogle ScholarPubMed
WELCH, K. C., HERRERA, M. L. G. & SUAREZ, R. K. 2008. Dietary sugar as a direct fuel for flight in the nectarivorous bat Glossophaga soricina. Journal of Experimental Biology 211:310316.CrossRefGoogle ScholarPubMed
WHITAKER, J. O. 1988. Food habits of insectivorous bats. Pp. 171190 in Kunz, T. H. (ed.). Ecological and behavioral methods for the study of bats. (First edition). Smithsonian Institution Press, Washington.Google Scholar
WHITE, T. C. R. 1993. The inadequate environment: nitrogen and the abundance of mammals. Springer-Verlag, Berlin. 425 pp.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 90:14691477.CrossRefGoogle Scholar