Ecological and dietary correlates of stable hydrogen isotope ratios in fur and body water of syntopic tropical bats

Ecology

Volumn 94, Issue 2, 2013, Pages 346-355

  Voigt, Christian C ^a   Schneeberger, Karin ^a   Luckner, Anja ^a  

^a LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

Author keywords

Connectivity; Costa Rica; Discrimination; Geolocation; Hydrogen stable isotopes; Keratin; La Selva Biological Station; Migration; Neotropical bats; Trophic level

Indexed keywords

HYDROGEN;

BAT; COMPARATIVE STUDY; CORRELATION; DATA ACQUISITION; DIET; ENDOGENOUS GROWTH; HYDROGEN ISOTOPE; MIGRATION; MOVEMENT; PHYLOGENETICS; SPECIES DIVERSITY; STABLE ISOTOPE; TROPICAL FOREST;

ANIMAL; ARTICLE; BAT; BODY WATER; CHEMISTRY; DIET; ECOSYSTEM; FEEDING BEHAVIOR; FRUIT; HAIR; INSECT; PHYSIOLOGY; SPECIES DIFFERENCE; TROPIC CLIMATE;

ANIMALS; BODY WATER; CHIROPTERA; DIET; ECOSYSTEM; FEEDING BEHAVIOR; FRUIT; HAIR; HYDROGEN; INSECTS; SPECIES SPECIFICITY; TROPICAL CLIMATE;

ANIMALIA; ARTIBEUS;

EID: 84876130609     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/12-1187.1     Document Type: Article

References (65)

1. Albrecht, L., C. F. J. Meyer, and E. K. V. Kalko. 2007. Differential mobility in two small phyllostomid bats, Artibeus watsoni and Micronyteris microtis, in a fragment neotropical landscape. Acta Theriologica 52:141-149.
2. Anthony, E. L. P. 1988. Age determination in bats. Pages 47-58 in T. H. Kunz, editor. Ecological and behavioral methods for the study of bats. Smithsonian Institution Press, Washington, D.C., USA.
3. Betini, G. S., K. A. Hobson, L. I. Wassenaar, and D. R. Norris. 2009. Stable hydrogen isotope (dD) values in songbird nestlings: Effects of diet, temperature, and body size. Canadian Journal of Zoology 87:767-772.
4. Birchall, J., T. O'Conell, T. H. E. Heaton, and R. E. M. Hedges. 2005. Hydrogen isotope ratios in animal body protein reflect trophic level. Journal of Animal Ecology 74:877-881.
5. Bonaccorso, F. J., et al. 2006. Evidence for exploitative competition: Comparative foraging behavior and roosting ecology of short-tailed fruit bats (Phyllostomidae). Biotropica 39:249-256.
6. Bowen, G. J., J. R. Ehleringer, L. A. Chesson, A. H. Thompson, D. W. Podlesak, and T. E. Cerling. 2009. Dietary and physiological controls on the hydrogen and oxygen isotope ratios of hair from mid-20th century indigenous populations. American Journal of Physical Anthropology 139:494-504.
7. Bowen, G. J., L. I. Wassenaar, and K. A. Hobson. 2005. Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337-348.
8. Bradbury, J. W., and S. L. Vehrencamp. 1976. Social organization and foraging in Emballonurid bats. I. Field studies. Behavioral Ecology and Sociobiology 1:337-381.
9. Chamberlain, C. P., J. D. Blum, R. T. Holmes, X. Feng, T. W. Sherry, and G. R. Graces. 1997. The use of isotope tracers for identifying populations of migratory birds. Oecologia 109:132-141.
10. Cormie, A. B., H. P. Schwarzc, and J. Gray. 1994. Relation between hydrogen isotopic ratios of bone collagen and rain. Geochimica et Cosmochimica Acta 48:377-391.
11. Cryan, P. M., M. A. Bogan, R. O. Rye, G. P. Landis, and C. L. Kester. 2004. Stable hydrogen isotope analysis of bat hair as evidence for seasonal molt and long-distance migration. Journal of Mammalogy 85:995-1001.
12. Ehleringer, J. R., G. J. Bowen, L. A. Chesson, A. G. West, D. W. Podlesak, and T. E. Cerling. 2008. Hydrogen and oxygen isotope ratios in human hair are related to geography. Proceedings of the National Academy of Sciences USA 105:2788-2793.
13. Erzberger, A., A. G. Popa-Lisseanu, G. U. C. Lehmann, and C. C. Voigt. 2011. Potential and limits in detecting altitudinal movements of bats using stable hydrogen isotope ratios of fur keratin. Acta Chiropterologica 13(2):431-438.
14. Estep, M. F., and H. Dabrowski. 1980. Tracing food webs with stable hydrogen isotopes. Science 209:1537-1538.
15. Fraser, K. C., E. A. McKinnon, A. W. Diamond, and L. Chavarria. 2011. The influence of microhabitat, moisture and diet on stable-hydrogen isotope variation in a Neotropical avian food web. Journal of Tropical Ecology 27:563-572.
16. Garland, T., A. W. Dickerman, C. M. Janis, and J. A. Jones. 1993. Phylogenetic analysis of covariance by computer simulation. Systematic Biology 42:265-292.
17. Grafen, A. 1989. The phylogenetic regression. Philosophical Transactions of the Royal Society B 326:119-157.
18. Hobson, K. A. 1999. Tracing origins and migration of wildlife using stable isotopes: A review. Oecologia 120:314-326.
19. Hobson, K. A., L. Atewell, and L. I. Wassenaar. 1999. Influence of drinking water and diet on the stable-hydrogen isotope ratios of animal tissues. Proceedings of the National Academy of Sciences USA 96:8003-8006.
20. Hobson, K. A., G. J. Bowen, L. I. Wassenaar, Y. Gerrand, and H. Lormee. 2004. Using stable hydrogen and oxygen isotope measurements of feathers to infer geographical origins of migrating European birds. Oecologia 141:477-488.
21. Hobson, K. A., H. Lormee, S. L. Van Wilgenburg, L. I. Wassenaar, and J. M. Boutin. 2009. Stable isotopes (dD) delineate the origins and migratory connectivity of harvested animals: The case of European woodpigeons. Journal of Applied Ecology 46:572-581.
22. Hobson, K. A., and L. I. Wassenaar. 1997. Linking breeding and wintering grounds of neotropical migrant songbirds using stable hydrogen isotopic analysis of feathers. Oecologia 109:142-148.
23. Hobson, K. A., L. I. Wassenaar, B. Mila, I. Lovette, C. Dingle, and T. B. Smith. 2003. Stable isotopes as indicators of altitudinal distributions and movements in an Ecuadorean hummingbird community. Oecologia 136:302-308.
24. Hoffmann, F. F., J. Hejduk, B. Caspers, B. M. Siemers, and C. C. Voigt. 2007. In the mating system of Saccopteryx bilineata, bioacoustic constraints impede male eavesdropping on female echolocation calls for their surveillance. Canadian Journal of Zoology 85:863-872.
25. Hoffmann, F. G., and J. Baker. 2003. Comparative phylogeography of short-tailed bats (Carollia: Phyllostomidae). Molecular Ecology 12:3403-3414.
26. Jones, K. E., A. Purvis, A. MacLaron, O. R. P. Bininda-Emonds, and N. B. Simmons. 2002. A phylogenetic supertree of the bats (Mammalia: Chiroptera). Biological Review 77:223-259.
27. Kalko, E. K. V., D. Friemel, C. O. Handley, and H.-U. Schnitzler. 1999. Roosting and foraging behavior of two Neotropical gleaning bats, Tonatia silvicola and Trachops cirrhosus (Phyllostomidae). Biotropica 31:344-353.
28. Langin, K., M. W. Reudink, P. P. Marra, D. R. Norris, T. K. Kyser, and L. M. Ratcliffe. 2007. Hydrogen isotopic variation in migratory bird tissues of known origin: Implication for geographic assignment. Oecologia 152:449-457.
29. LaVal, R. K., and B. Rodriguez. 2002. Murcie?lagos de Costa Rica. Bats of Costa Rica. INBio (Instituto Nactional de Biodiversidad), Santo Domingo de Heredia, Costa Rica.
30. Lifson, N., and R. McClintock. 1966. Theory of the use of the turnover rates of body water for measuring energy and material balance. Journal of Theoretical Biology 12:46-74.
31. Minagawa,M., and E. Wada. 1984. Stepwise enrichment of 15N along food chains: Further evidence and the relation between d15N and animal age. Geochimica et Cosmochimica Acta 48:1135-1140.
32. Nagy, K. A. 1983. The doubly labeled water (3HH18O) method: A guide to its use. Publication 12-1418, University of California Press, Los Angeles, California, USA.
33. O'Brien, D. M., and M. Wooller. 2007. Tracking human travel using stable oxygen and hydrogen isotope analyses of hair and urine. Rapid Communication in Mass Spectrometry 21:2422-2430.
34. O'Grady, S. P., A. R. Wende, C. H. Remien, L. O. Valenzuela, L. E. Enright, L. A. Chesson, E. D. Abel, T. E. Cerling, and J. R. Ehleringer. 2010. Aberrant water homeostasis detected by stable isotope analysis. PLoS ONE 5(7):e11699.
35. Orme, D., R. Freckleton, G. Thomas, T. Petzoldt, S. Fritz, and N. Isaac. 2011. Caper: Comparative analyses of phylogenetics and evolution in R. R package version 0.4. http://CRAN.R-project.org/package=caper
36. Ossa, G., S. Kramer-Schadt, A. J. Peel, A. K. Scharf, and C. C. Voigt. 2012. The movement ecology of the straw-colored fruit bat, Eidolon helvum, in sub-Saharan Africa assessed by stable isotopes ratios. PLoS ONE 7(9):e45729.
37. Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature 401:877-884.
38. Pietsch, S. J., K. A. Hobson, L. I. Wassenaar, and T. Tutken. 2011. Tracking cats: Problems with placing feline carnivores on d18O, dD isoscapes. PLoS ONE 6:e24601.
39. Podlesak, D. W., A.-M. Torregrossa, J. R. Ehleringer, M. D. Dearing, B. H. Passey, and T. E. Cerling. 2008. Turnover of oxygen and hydrogen isotopes in the body water, CO2, hair, and enamel of a small mammal. Geochimica et Cosmochimica Acta 72:19-35.
40. Popa-Lisseanu, A. G., et al. 2012. A triple isotope approach to predict breeding origins of European bats. PLoS ONE 7(7):e38083.
41. Price, T. 1997. Correlated evolution and independent contrasts. Philosophical Transactions of the Royal Society of London B 352:519-529.
42. R Development Core Team. 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www. R-project.org/
43. Revell, L. J. 2012. Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3:217-223.
44. Rex, K., B. I. Czaczkes, R. Michener, T. H. Kunz, and C. C. Voigt. 2010. Specialisation and omnivory in diverse mammalian assemblages. Ecoscience 17:37-46.
45. Rex, K., D. H. Kelm, K. Wiesner, F. Matt, T. H. Kunz, and C. C. Voigt. 2008. Structure of three Neotropical bat assemblages. Biological Journal of the Linnean Society 94:617-629.
46. Rothenworer, C., N. I. Becker, and M. Tschapka. 2011. Resource landscape and spatio-temporal activity patterns of a plant-visiting bat in a Costa Rican lowland rainforest. Journal of Zoology 283:108-116.
47. Rubenstein, D. R., C. P. Chamberlain, R. T. Holmes, M. P. Ayres, J. R. Waldbauer, G. R. Graces, and N. C. Tuross. 2002. Linking breeding and wintering ranges of a migratory songbird using stable isotopes. Science 295:1062-1065.
48. Schimmelmann, A., and M. J. DeNiro. 1986. Stable isotopic studies on chitin. 3. The D/H and O-18/O-16 ratios in arthropod chitin. Geochimica et Cosmochimica Acta 50:1485-1496.
49. Siemers, B. M., S. Greif, I. Borissov, S. L. Voigt-Heucke, and C. C. Voigt. 2011. Divergent trophic levels in two cryptic sibling bat species. Oecologia 166:69-78.
50. Simmons, N. B., and R. S. Voss. 1998. The mammals of Para? cou, French Guiana: A Neotropical lowland rainforest fauna. Part 1: Bats. Bulletin of the American Museum of Natural History 237:1-219.
51. Solomon, C. T., J. J. Cole, R. R. Doucett, M. L. Pace, N. D. Preston, L. R. Smith, and B. C. Weidel. 2009. The influence of environmental water on the hydrogen stable isotope ratio in aquatic consumers. Oecologia 161:313-324.
52. Speakman, J. R. 1997. Doubly labeled water-theory and practice. Chapman and Hall, London, UK.
53. Timm, R. M., and R. K. LaVal. 1998. A field key to the bats of Costa Rica. Occasional Publication 22. Center of Latin American Studies, University of Kansas, Lawrence, Kansas, USA.
54. Tschapka, M. 2004. Energy density patterns of nectar resources permit coexistence within a guild of Neotropical flowervisiting bats. Journal of Zoology 263:7-21.
55. Vanderklift, M. A., and S. Ponsard. 2003. Sources of variation in consumer diet d15N enrichment: A meta-analysis. Oecologia 136:169-182.
56. Voigt, C. C., Z. Akbar, T. H. Kunz, and T. Kingston. 2011. The origin of assimilated proteins in Old and New World phytophagous bats. Biotropica 43:108-113.
57. Voigt, C. C., A. Popa-Lisseanu, I. Niermann, and S. Kramer-Schadt. 2012. The catchment area of wind farms for European bats: A plea for international regulations. Biological Conservation 153:80-86.
58. Voigt, C. C., O. von Helversen, R. Michener, and T. H. Kunz. 2001. The economics of harem maintenance in the sac-winged bat, Saccopteryx bilineata. Behavioral Ecology and Sociobiology 50:31-36.
59. Vonhof, M. J., H. Whitehead, and M. B. Fenton. 2004. Analysis of Spix's disc-winged bat association patterns and roosting home ranges reveal a novel social structure among bats. Animal Behaviour 68:507-521.
60. Wassenaar, L. I., and K. A. Hobson. 2003. Comparative equilibration and online technique for determination of nonexchangeable hydrogen of keratins for use in animal migration studies. Isotopes Environment and Health Sciences 39:211-217.
61. Wassenaar, L. I., and K. A. Hobson. 2005. Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337-348.
62. Wolf, N., G. J. Bowen, and C. Martinez del Rio. 2011. The influence of drinking water on the dD and d18O values of house sparrow plasma, blood and feathers. Journal of Experimental Biology 214:98-103.
63. Wolf, N., S. Newsome, M. L. Fogel, and C. Martinez del Rio. 2012. An experimental exploitation of the incorporation of hydrogen isotopes from dietary sources into avian tissues. Journal of Experimental Biology 215:1915-1922.
64. Wunder, M. B. 2010. Using isoscapes to model probability surfaces for determining geographic origins. Pages 251-272 in J. B. West, G. J. Bowen, T. E. Dawson, and K. P. Tu, editors. Isoscapes: Understanding movement, pattern, and process on Earth through isotope mapping. Springer, Dordrecht, The Netherlands.
65. York, H. A., and S. A. Billings. 2009. Stable-isotope analysis of diets of short-tailed fruit bats (Chiroptera: Phyllostomidae: Carollia). Journal of Mammalogy 90:1469-1477.