Advertisement

International Journal of Primatology

, Volume 33, Issue 3, pp 673–701 | Cite as

Stable Isotope Techniques and Applications for Primatologists

  • Brooke E. Crowley
Article

Abstract

Stable isotope biogeochemistry is useful for quantifying the feeding ecology of modern and extinct primates. Over the past three decades, substantial advances have been made in our knowledge of the physiological causes of isotopic patterns as well as effective methodology to prepare samples for isotopic analysis. Despite these advances, the potential of stable isotope biogeochemistry has yet to be fully exploited by primate researchers, perhaps due to the prolific and somewhat daunting nature of the isotopic literature. I here aim to present a cogent overview of stable isotope applications to nonhuman primate feeding ecology. I review the factors that influence ecological patterns in carbon, nitrogen, and oxygen stable isotopes. I present methods for collecting and preparing samples of tooth enamel and bone mineral hydroxyapatite, bone collagen, fur and hair keratin, blood, feces, and urine for isotope analysis. I discuss both the existing and potential applications of these isotopic patterns to primate feeding ecology. Lastly, I point out some of the pitfalls to avoid when interpreting and comparing isotopic results.

Keywords

δ13δ15δ18Hydroxyapatite Proteinaceous tissues Stable isotope Trophic discrimination 

Notes

Acknowledgments

I thank Gabe Bowen, Kena Fox-Dobbs, Sora Lee Kim, Carolyn Kurle, and Patrick Wheatley, for consultation on sample preparation techniques, and Lawrence Crowley, Sally Goddard, Matthew Weirauch and three anonymous reviewers for critical review of the manuscript. I also thank Erin Vogel and Janine Chalk for inviting me to contribute to this special issue.

Supplementary material

10764_2012_9582_MOESM1_ESM.docx (23 kb)
Table S1 (DOCX 23.4 kb)
10764_2012_9582_MOESM2_ESM.docx (22 kb)
Table S2 (DOCX 21.8 kb)
10764_2012_9582_MOESM3_ESM.docx (17 kb)
Table S3 (DOCX 16.5 kb)
10764_2012_9582_MOESM4_ESM.docx (15 kb)
Table S4 (DOCX 14.8 kb)

References

  1. Ambrose, S. H. (1990). Preparation and characterization of bone and tooth collagen for isotopic analysis. Journal of Archaeological Science, 17, 431–451.CrossRefGoogle Scholar
  2. Ambrose, S. H., & Norr, L. (1993). Experimental evidence for the relationship of the carbon isotope ratios of whole diet and dietary protein to those of bone collagen and carbonate. In J. B. Lambert & G. Grupe (Eds.), Prehistoric human bone: Archaeology at the molecular level (pp. 1–37). Berlin: Springer Verlag.Google Scholar
  3. Barbour, M. G. (2007). Stable oxygen isotope composition of plant tissue: a review. Functional Plant Biology, 34, 83–94.CrossRefGoogle Scholar
  4. Barboza, P. S., & Parker, K. L. (2006). Body protein stores and isotopic indicators of N balance in female reindeer (Rangifer tarandus) during winter. Physiological and Biochemical Zoology, 79, 628–644.PubMedCrossRefGoogle Scholar
  5. Barrow, L. M., Bjorndal, K. A., & Reich, K. J. (2008). Effects of preservation method on stable carbon and nitrogen isotope values. Physiological and Biochemical Zoology, 81, 688–693.PubMedCrossRefGoogle Scholar
  6. Bearhop, S., Adams, C. E., Waldron, S., Fuller, R. A., & MacLeod, H. (2004). Determining trophic niche width: A novel approach using stable isotope analysis. Journal of Animal Ecology, 73, 1007–1012.CrossRefGoogle Scholar
  7. Bowen, G. J., Chesson, L., Nielson, K., Cerling, T. E., & Ehleringer, J. R. (2005). Treatment methods for the determination of δ2H and δ 18O of hair keratin by continuous-flow isotope-ratio mass spectrometry. Rapid Communications in Mass Spectrometry, 19, 2371–2378.PubMedCrossRefGoogle Scholar
  8. Bryant, J. D., & Frölich, P. N. (1995). A model of oxygen isotope fractionation in body water of large mammals. Geochimica et Cosmochimica Acta, 59, 4523–4537.CrossRefGoogle Scholar
  9. Carter, M. (2001). Sensitivity of stable isotopes ( 13 C, 15 N, and 18 O) in bone to dietary specialization and niche separation among sympatric primates in Kibale National Park, Uganda. Ph.D. dissertation, University of Chicago.Google Scholar
  10. Cerling, T. E., & Harris, J. M. (1999). Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia, 120, 347–363.CrossRefGoogle Scholar
  11. Cerling, T. E., Hart, J. A., & Hart, T. B. (2004). Isotope ecology in the Ituri forest. Oecologia, 138, 5–12.PubMedCrossRefGoogle Scholar
  12. Cerling, T. E., Mbua, E., Kirera, F. M., Manthi, F. K., Grine, F. E., Leakey, M. G., et al. (2011). Diet of Paranthropus boisei in the early Pleistocene of East Africa. Proceedings of the National Academy of Sciences, 108, 9337–9341.Google Scholar
  13. Cernusak, L. A., Pate, J. S., & Farquhar, G. D. (2004). Oxygen and carbon isotope composition of parasitic plants and their hosts in southwestern Australia. Oecologia, 139, 199–213.PubMedCrossRefGoogle Scholar
  14. Chamberlain, C. P., Waldbauer, J. R., Fox-Dobbs, K., Newsome, S. D., Koch, P. L., Smith, D. R., et al. (2005). Pleistocene to recent dietary shifts in California condors. Proceedings of the National Academy of Sciences of the USA, 102, 16707–16711.PubMedCrossRefGoogle Scholar
  15. Clementz, M. T., Fox-Dobbs, K., Wheatley, P. V., & Doak, D. F. (2009). Revisiting old bones: Coupled carbon isotope analysis of bioapatite and collagen as an ecological and palaeoecological tool. Geological Journal, 44, 605–620.CrossRefGoogle Scholar
  16. Codron, J., Codron, D., Lee-Thorp, J. A., Sponheimer, M., Bond, W. J., de Ruiter, D., et al. (2005). Taxonomic, anatomical, and spatio-temporal variations in the stable carbon and nitrogen isotopic compositions of plants from an African savanna. Journal of Archaeological Science, 32, 1757–1772.CrossRefGoogle Scholar
  17. Codron, D., Lee-Thorp, J. A., Sponheimer, M., de Ruiter, D., & Codron, J. (2006). Inter-and intrahabitat dietary variability of Chacma baboons (Papio ursinus) in South African savannas based on fecal δ13C, δ15N, and %N. American Journal of Physical Anthropology, 129, 204–214.PubMedCrossRefGoogle Scholar
  18. Codron, D., Lee-Thorp, J., Sponheimer, M., de Ruiter, D., & Codron, J. (2008). What insights can baboon feeding ecology provide for early hominin niche differentiation? International Journal of Primatology, 29, 757–772.CrossRefGoogle Scholar
  19. Crowley, B. E., Carter, M. L., Karpanty, S. M., Zihlman, A. L., Koch, P. L., & Dominy, N. J. (2010). Stable carbon and nitrogen isotope enrichment in primate tissues. Oecologia, 164, 611–626.PubMedCrossRefGoogle Scholar
  20. Crowley, B. E., Godfrey, L. R., & Irwin, M. T. (2011). A Glance to the past: Subfossils, stable isotopes, seed dispersal, and lemur species loss in southern Madagascar. American Journal of Primatology, 73, 25–37.PubMedCrossRefGoogle Scholar
  21. Crowley, B. E., Thorén, S., Rasoazanabary, E., Vogel, E. R., Barrett, M. A., Zohdy, S., et al. (2011). Explaining geographical variation in the isotope composition of mouse lemurs (Microcebus). Journal of Biogeography, 38, 2106–2121.CrossRefGoogle Scholar
  22. 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.PubMedGoogle Scholar
  23. Dansgaard, W. (1964). Stable isotopes in precipitation (pp. 436–468). XVI: Tellus.Google Scholar
  24. 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
  25. 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
  26. Deschner, T., Fuller, B. T., Oelze, V., Ortmann, S., Richards, M. P., & Hohmann, G. (2010). Monitoring nutritional stress with urinary δ15N and C/N ratios in captive bonobos. American Journal of Physical Anthropology, 50(Supplement), 70.Google Scholar
  27. Dobush, G. R., Ankney, C. D., & Krementz, D. G. (1985). The effect of apparatus, extraction time, and solvent type on lipid extractions of snow geese. Canadian Journal of Zoology, 63, 1917–1920.CrossRefGoogle Scholar
  28. Dutton, A., Wilkinson, B. H., Welker, J. M., Bowen, G. J., & Lohmann, K. C. (2005). Spatial distribution and seasonal variation in 18O/16O of modern precipitation and river water across the conterminous USA. Hydrological Processes, 19, 4121–4146.CrossRefGoogle Scholar
  29. Fourie, N. H., Lee-Thorp, J. A., & Ackermann, R. R. (2008). Biogeochemical and craniometric investigation of dietary ecology, niche separation, and taxonomy of Plio-Pleistocene cercopithecoids from the Makapansgat Limeworks. American Journal of Physical Anthropology, 135, 121–135.PubMedCrossRefGoogle Scholar
  30. Fox-Dobbs, K., Stidham, T. A., Bowen, G. J., Emslie, S. D., & Koch, P. L. (2006). Dietary controls on extinction versus survival among avian megafauna in the late Pleistocene. Geology, 34, 685–688.CrossRefGoogle Scholar
  31. Francey, R. J., Allison, C. E., Etheridge, D. M., Trudinger, C. M., Enting, I. G., Leuenberger, M., et al. (1999). A 1000-year high precision record of δ13C in atmospheric CO2. Tellus Series B, 51, 170–193.CrossRefGoogle Scholar
  32. Fricke, H. C., & O’Neil, J. R. (1996). Inter- and intra-tooth variation in the oxygen isotope composition of mammalian tooth enamel: Some implications for paleoclimatological and paleobiological research. Palaeogeography, Palaeoclimatology, Palaeoecology, 126, 91–99.CrossRefGoogle Scholar
  33. Froehle, A. W., Kellner, C. M., & Schoeninger, M. J. (2010). FOCUS: Effect of diet and protein source on carbon stable isotope ratios in collagen: follow up to Warinner and Tuross (2009). Journal of Archaeological Science, 37, 2662–2670.CrossRefGoogle Scholar
  34. Gannes, L. Z., Martínez del Rio, C., & Koch, P. L. (1998). Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comparative Biochemistry and Physiology, 119A, 725–757.Google Scholar
  35. Godfrey, L. R., Crowley, B. E., & Dumont, E. R. (2011). Thinking outside the box: A lemur’s take on hominin craniodental evolution. Proceedings of the National Academy of Sciences, 108, E743.CrossRefGoogle Scholar
  36. Grine, F. E. (1986). Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. Journal of Human Evolution, 15, 783–822.CrossRefGoogle Scholar
  37. Handley, L. L., Austin, A. T., Robinson, D., Scrimgeour, C. M., Raven, J. A., Heaton, T. H. E., et al. (1999). The N-15 natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Australian Journal of Plant Physiology, 26, 185–199.CrossRefGoogle Scholar
  38. Hare, P. E., Fogel, M. L., Stafford, T. W., Mitchell, A. D., & Hoering, T. C. (1991). The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. Journal of Archaeological Science, 18, 277–292.CrossRefGoogle Scholar
  39. Heaton, T. H. E. (1999). Spatial, species, and temporal variations in the 13C/12C ratios of C3 plants: Implications for palaeodiet studies. Journal of Archaeological Science, 26, 637–649.CrossRefGoogle Scholar
  40. Hedges, R. E. M., & van Klinken, G. J. (2000). “Consider a spherical cow…” — on modeling and diet. In S. H. Ambrose & M. A. Katzenberg (Eds.), Biogeochemical approaches to paleodietary analysis (pp. 211–241). New York: Kluwer Academic/Plenum Press.Google Scholar
  41. Herrera, M. 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.CrossRefGoogle Scholar
  42. Herrera, L. G., Hobson, K. A., & Martínez, J. C. (2006). Tracing the origin of dietary protein in tropical dry forest birds. Biotropica, 36, 735–742.CrossRefGoogle Scholar
  43. Hoefs, J. (1997). Stable isotope geochemistry (4th ed.). New York: Springer-Verlag.Google Scholar
  44. Howland, M. R., Corr, L. T., Young, S. M. M., Jones, V., Jim, S., van der Merwe, N. J., et al. (2003). Expression of the dietary isotope signal in the compound-specific δ13C values of pig bone lipids and amino acids. International Journal of Osteoarchaeology, 13, 54–65.CrossRefGoogle Scholar
  45. Hyodo, F., Matsumoto, T., Takematsu, Y., Kamoi, T., Fukuda, D., Nakagawa, M., et al. (2010). The structure of a food web in a tropical rain forest in Malaysia based on carbon and nitrogen stable isotope ratios. Journal of Tropical Ecology, 26, 205–214.CrossRefGoogle Scholar
  46. Jim, S., Ambrose, S. H., & Evershed, R. P. (2004). Stable carbon isotopic evidence for differences in the dietary origin of bone cholesterol, collagen and apatite: Implications for their use in palaeodietary reconstruction. Geochimica et Cosmochimica Acta, 68, 61–72.CrossRefGoogle Scholar
  47. Keeley, J. E., & Rundel, P. W. (2003). Evolution of CAM and C4 carbon-concentrating mechanisms. International Journal of Plant Science, 164, S55–S77.CrossRefGoogle Scholar
  48. Knott, C. D. (1997). Field collection and preservation of urine in orangutans and chimpanzees. Tropical Biodiversity, 4, 95–102.Google Scholar
  49. Koch, P. L. (2007). Isotopic study of the biology of modern and fossil vertebrates. In K. Lajtha & B. Michener (Eds.), Stable isotopes in ecology and environmental science (pp. 99–154). Boston: Blackwell.CrossRefGoogle Scholar
  50. Koch, P. L., Tuross, N., & Fogel, M. L. (1997). The effects of sample treatment and diagenesis on the integrity of carbonate in biogenic hydroxyapatite. Journal of Archaeological Science, 24, 417–429.CrossRefGoogle Scholar
  51. Kohn, M. J. (2010). Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo)ecology and (paleo)climate. Proceedings of the National Academy of Sciences of the USA, 107, 19691–19695.PubMedCrossRefGoogle Scholar
  52. Kohn, M. J., & Cerling, T. E. (2002). Stable isotope compositions of biological apatite. In M. J. Kohn, J. Rakovan, & J. M. Hughes (Eds.), Phosphates: Geochemical, geobiological, and materials importance. Reviews in Mineralogy and Geochemistry, 48 (pp. 455–488). Washington, DC: Mineralogical Society of America.Google Scholar
  53. Kohn, M. J., Schoeninger, M. J., & Valley, J. W. (1998). Variability in herbivore tooth oxygen isotope compositions: reflections of seasonality or developmental physiology? Isotope Geosciences, 152, 97–112.Google Scholar
  54. Kurle, C. (2002). Stable-isotope ratios of blood components from captive northern fur seals (Callorhinus ursinus) and their diet: applications for studying the foraging ecology of wild otariids. Canadian Journal of Zoology, 80, 902–909.CrossRefGoogle Scholar
  55. Lambert, J. E., Chapman, C. A., Wrangham, R. W., & Conklin-Brittain, N. L. (2004). Hardness of Cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. American Journal of Physical Anthropology, 125, 363–368.PubMedCrossRefGoogle Scholar
  56. Lee-Thorp, J. A., & van der Merwe, N. J. (1991). Aspects of the chemistry of modern and fossil biological apatites. Journal of Archaeological Science, 18, 343–354.CrossRefGoogle Scholar
  57. Lee-Thorp, J. A., Sealy, J. C., & van der Merwe, N. J. (1989). Stable carbon isotope ratio differences between bone collagen and bone apatite, and their relationship to diet. Journal of Archaeological Science, 16, 585–599.CrossRefGoogle Scholar
  58. Lee-Thorp, J. A., van der Merwe, N. J., & Brain, C. K. (1989). Isotopic evidence for dietary differences between two extinct baboon species from Swartkrans. Journal of Human Evolution, 18, 183–190.CrossRefGoogle Scholar
  59. Lee-Thorp, J. A., Sponheimer, M., & van der Merwe, N. J. (2003). What do stable isotopes tell us about hominid dietary and ecological niches in the Pliocene. International Journal of Osteoarchaeology, 13, 104–113.CrossRefGoogle Scholar
  60. Levin, N. E., Cerling, T. E., Passey, B. H., Harris, J. M., & Ehleringer, J. R. (2006). A stable isotope aridity index for terrestrial environments. Proceedings of the National Academy of Sciences of the USA, 103, 11201–11205.PubMedCrossRefGoogle Scholar
  61. Loudon, J. E., Sponheimer, M., Sauther, M. L., & Cuozzo, F. P. (2007). Intraspecific variation in hair δ13C and δ15N values of ring-tailed lemurs (Lemur catta) with known individual histories, behavior, and feeding ecology. American Journal of Physical Anthropology, 183, 978–985.CrossRefGoogle Scholar
  62. Luz, B., & Kolodny, Y. (1985). Oxygen isotope variations in phosphates of biogenic apatites, IV: mammal teeth and bones. Earth and Planetary Science Letters, 75, 29–36.CrossRefGoogle Scholar
  63. Marshall, A. J., & Wrangham, R. W. (2007). Evolutionary consequences of fallback foods. International Journal of Primatology, 28, 1219–1235.CrossRefGoogle Scholar
  64. Marshall, J. D., Brooks, J. R., & Lajtha, K. (2007). Sources of variation in the stable isotopic composition of plants. In R. Michener & K. Lajtha (Eds.), Stable isotopes in ecology and environmental science (2nd ed., pp. 22–60). Boston: Blackwell.CrossRefGoogle Scholar
  65. Martínez del Rio, C., Wolf, N., Carleton, S. A., & Gannes, L. Z. (2009). Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews of the Cambridge Philosophical Society, 84, 91–111.CrossRefGoogle Scholar
  66. McGee, E. M., & Vaughn, S. E. (2003). Variations in stable isotope composition in Propithecus diadema edwardsi from disturbed and undisturbed rainforest habitats in Ranomafana National Park, Madagascar. American Journal of Physical Anthropology, 36(Supplement), 149–150.Google Scholar
  67. Moore, J. W., & Semmens, B. X. (2008). Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters, 11, 470–480.PubMedCrossRefGoogle Scholar
  68. Muzuka, A. (1999). Isotopic compositions of tropical East African flora and their potential as source indicators of organic matter in coastal marine sediments. Journal of African Earth Sciences, 28, 757–766.CrossRefGoogle Scholar
  69. Nelson, S. V. (2007). Isotopic reconstructions of habitat change surrounding the extinction of Sivapithecus, a Miocene hominoid, in the Siwalik Group of Pakistan. Palaeogeography, Palaeoclimatology, Palaeoecology, 243, 204–222.CrossRefGoogle Scholar
  70. Nelson, B. K., DeNiro, M. J., Schoeninger, M. J., & DePaolo, D. J. (1986). Effects of diagenesis on strontium, carbon, nitrogen, and oxygen concentration and isotopic composition of bone. Geochimica et Cosmochimica Acta, 50, 1941–1949.CrossRefGoogle Scholar
  71. O’Brien, D. M., & Wooller, M. J. (2007). Tracking human travel using stable oxygen and hydrogen isotope analyses of hair and urine. Rapid Communications in Mass Spectrometry, 21, 2422–2430.PubMedCrossRefGoogle Scholar
  72. O’Connell, T. C., & Hedges, R. E. M. (1999). Investigations into the effect of diet on modern human hair isotopic values. American Journal of Physical Anthropology, 108, 409–425.PubMedCrossRefGoogle Scholar
  73. O’Grady, S. P., Enright, L. E., Barnette, J. E., Cerling, T. E., & Ehleringer, J. R. (2010). Accuracy and precision of a laser-spectroscopy approach to the analysis of δ2H and δ18O in human urine. Isotopes in Environmental and Health Studies, 46, 476–483.PubMedCrossRefGoogle Scholar
  74. O’Grady, S. P., Wende, A. R., Remien, C. H., Valenzuela, L. O., Enright, L. E., Chesson, L. A., et al. (2010). Aberrant water homeostasis detected by stable isotope analysis. PLoS One, 5, e11699.PubMedCrossRefGoogle Scholar
  75. O’Regan, H., Chenery, C., Lamb, A., Stevens, R., Rook, L., & Elton, S. (2008). Modern macaque dietary heterogeneity assessed using stable isotope analysis of hair and bone. Journal of Human Evolution, 55, 617–626.PubMedCrossRefGoogle Scholar
  76. Parker, K. L., Barboza, P. S., & Stephenson, T. R. (2005). Protein conservation in female caribou (Rangifer tarandus): effects of decreasing diet quality during winter. Journal of Mammalogy, 86, 610–622.CrossRefGoogle Scholar
  77. 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.PubMedCrossRefGoogle Scholar
  78. Passey, B. H., Robinson, T. F., Ayliffe, L. K., Cerling, T. E., Sponheimer, M., Dearing, M. D., et al. (2005). Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. Journal of Archaeological Science, 32, 1459–1470.CrossRefGoogle Scholar
  79. Peters, L. I., & Yakir, D. (2008). A direct and rapid leaf water extraction method for isotopic analysis. Rapid Communications in Mass Spectrometry, 22, 2929–2936.PubMedCrossRefGoogle Scholar
  80. Phillips, D. L., & Gregg, J. W. (2003). Source partitioning using stable isotopes: coping with too many sources. Oecologia, 136, 261–269.PubMedCrossRefGoogle Scholar
  81. Phillips, D. L., Newsome, S. D., & Gregg, J. W. (2005). Combining sources in stable isotope mixing models: alternative methods. Oecologia, 144, 522–527.CrossRefGoogle Scholar
  82. Rothman, J. M., Chapman, C. A., & Van Soest, P. J. (2011). Methods in primate nutritional ecology: A user’s guide. International Journal of Primatology. doi: 10.1007/s10764-011-9568-x.
  83. Schoeninger, M. J. (2010). Toward a δ13C isoscape for primates. In J. B. West, G. J. Bowen, T. E. Dawson, & K. P. Tu (Eds.), Isoscapes: Understanding movement, pattern, and process on earth through isotope mapping (pp. 319–333). New York: Springer Science+Business Media.Google Scholar
  84. Schoeninger, M. J., & DeNiro, M. J. (1984). Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta, 48, 625–639.CrossRefGoogle Scholar
  85. Schoeninger, M., Iwaniec, U. T., & Glander, K. E. (1997). Stable isotope ratios indicate diet and habitat use in New World Monkeys. American Journal of Physical Anthropology, 103, 69–83.PubMedCrossRefGoogle Scholar
  86. Schoeninger, M. J., Iwaniec, U. T., & Nash, L. T. (1998). Ecological attributes recorded in stable isotope ratios of arboreal prosimian hair. Oecologia, 113, 222–230.CrossRefGoogle Scholar
  87. Schulze, E. D., Lange, O. L., Ziegler, H., & Gebauer, G. (1991). Carbon and nitrogen isotope ratios of mistletoes growing on nitrogen and non-nitrogen fixing hosts and on CAM plants in the Namib desert confirm partial heterotrophy. Oecologia, 88, 457–462.CrossRefGoogle Scholar
  88. Simmen, B., Bayart, F., Rasamimanana, H., Zahariev, A., Blanc, S., & Pasquet, P. (2010). Total energy expenditure and body composition in two free-living sympatric lemurs. PLoS One, 5, e9860.PubMedCrossRefGoogle Scholar
  89. Smith, C. C., Morgan, M. E., & Pilbeam, D. (2010). Isotopic ecology and dietary profiles of Liberian chimpanzees. Journal of Human Evolution, 58, 43–55.PubMedCrossRefGoogle Scholar
  90. Sponheimer, M., & Lee-Thorp, J. A. (2001). The oxygen isotope composition of mammalian enamel carbonate from Morea Estate, South Africa. Oecologia, 126, 153–157.CrossRefGoogle Scholar
  91. Sponheimer, M., Robinson, T., Ayliffe, L., Passey, B., Roeder, B., Shipley, L., et al. (2003). An experimental study of carbon-isotope fractionation between diet, hair, and feces of mammalian herbivores. Canadian Journal of Zoology, 81, 871–876.CrossRefGoogle Scholar
  92. Sponheimer, M., Robinson, T., Ayliffe, L., Roeder, B., Hammer, J., Passey, B., et al. (2003). Nitrogen isotopes in mammalian herbivores: hair δ15N values from controlled feeding study. International Journal of Osteoarchaeology, 13, 80–87.CrossRefGoogle Scholar
  93. Sponheimer, M., Loudon, J. E., Codron, D., Howells, M. E., Pruetz, J. D., Codron, J., et al. (2006). Do “savanna” chimpanzees consume C4 resources? Journal of Human Evolution, 51, 128–133.PubMedCrossRefGoogle Scholar
  94. Sponheimer, M., Passey, B. H., de Ruiter, D. J., Guatelli-Steinberg, D., Cerling, T. E., & Lee-Thorp, J. A. (2006). Isotopic evidence for dietary variability in the early hominin Paranthropus robustus. Science, 314, 980–982.PubMedCrossRefGoogle Scholar
  95. Sponheimer, M., Codron, D., Passey, B. H., de Ruiter, D. J., Cerling, T. E., & Lee-Thorp, J. A. (2009). Using carbon isotopes to track dietary change in modern, historical, and ancient primates. American Journal of Physical Anthropology, 140, 661–670.PubMedCrossRefGoogle Scholar
  96. Sternberg, L. S. L., Mulkey, S. S., & Wright, S. J. (1989). Oxygen isotope ratio stratification in a tropical moist forest. Oecologia, 81, 51–56.CrossRefGoogle Scholar
  97. Swap, R. J., Aranibar, J. N., Bowty, P. R., Gilhooly, W. P., III, & Macko, S. A. (2004). Natural abundance of 13C and 15N in C3 and C4 vegetation of southern Africa: Patterns and implications. Global Change Biology, 10, 350–358.CrossRefGoogle Scholar
  98. Thackeray, J. F., Henzi, S. P., & Brain, C. (1996). Stable carbon and nitrogen isotope analysis of bone collagen in Papio cynocephalus ursinus: Comparison with ungulates and Homo sapiens from southern and East African environments. South African Journal of Science, 92, 209–212.Google Scholar
  99. Tuross, N., Fogel, M. L., & Hare, P. E. (1988). Variability in the preservation of the isotopic composition of collagen from fossil bone. Geochimica et Cosmochimica Acta, 52, 929–935.CrossRefGoogle Scholar
  100. Tuross, N., Warinner, C., Kirsanow, K., & Kester, C. (2008). Organic oxygen and hydrogen isotopes in a porcine controlled dietary study. Rapid Communications in Mass Spectrometry, 22, 1741–1745.PubMedCrossRefGoogle Scholar
  101. Urey, H. C. (1947). The thermodynamic properties of isotopic substances. Journal of the Chemical Society, 562–581.Google Scholar
  102. van der Merwe, N. J., & Medina, E. (1989). Photosynthesis and 13C/12C ratios in Amazonian rain forests. Geochimica et Cosmochimica Acta, 53, 1091–1094.CrossRefGoogle Scholar
  103. Vogel, E. R., Crowley, B. E., Knott, C. D., Blakely, M. D., & Dominy, N. J. (2011). A non-invasive method for quantifying nitrogen balance in free ranging primates. International Journal of Primatology. doi: 10.1007/s10764-011-9543-6.
  104. Werner, R. A., & Schmidt, H.-L. (2002). The in vivo nitrogen isotope discrimination among organic plant compounds. Phytochemistry, 61, 465–484.PubMedCrossRefGoogle Scholar
  105. White, T. D., Ambrose, S. H., Suwa, G., Su, D. F., DeGusta, D., Bernor, R. L., et al. (2009). Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science, 326, 87–93.PubMedGoogle Scholar
  106. Zachos, J., Pagani, M., Sloan, L., Thomas, E., & Billups, K. (2001). Trends, rhythms, and aberrations in global climate 65 Ma to present. Science, 292, 686–693.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Departments of Geology and AnthropologyUniversity of CincinnatiCincinnatiUSA

Personalised recommendations