Abstract
We determined the magnitude of isotopic fractionation of carbon and nitrogen stable isotope ratios (as enrichment factors, Δδ13C and Δδ15N, respectively) between the tissues and diets of captive Japanese macaques (Macaca fuscata) using a controlled feeding experiment, to provide basic data for reconstructing their feeding habits. The Δδ13C and Δδ15N values, respectively, were 0.9 ± 0.2 ‰ (mean ± standard deviation, SD) and 3.0 ± 0.3 ‰ for whole blood, 1.3 ± 0.2 ‰ and 4.3 ± 0.3 ‰ for plasma, and 0.8 ± 0.2 ‰ and 3.0 ± 0.2 ‰ for red blood cells. However, the Δδ13C and Δδ15N values for hair were 2.8 ± 0.3 ‰ and 3.4 ± 0.2 ‰, respectively. No difference was detected in the δ13C and δ15N values of hair sampled from different parts of the body. We investigated the effects of diet on δ13C in growing hair by alternating the diet of the macaques each month between two diets that differed markedly in δ13C. Hair regrown after shaving repeatedly recorded the δ13C of the diet consumed during the time of hair growth. On the other hand, hair naturally grown during the diet-change experiment did not show a clear pattern. One possible reason is that the hair had grown abnormally under unnatural indoor conditions and showed complicated isotope signatures. To reconstruct the long-term feeding history of Japanese macaques, we need to further clarify the relationships between the stable isotope signature of diet and various body tissues.
Similar content being viewed by others
Change history
11 June 2013
An Erratum to this paper has been published: https://doi.org/10.1007/s10329-013-0366-2
References
Ambrose SH, 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: Lambert JB, Grupe G (eds) Prehistoric human bone: archaeology at the molecular level. Springer, Berlin, pp 1–37
Caut S, Angulo E, Courchamp F (2008) Discrimination factors (Δ15N and Δ13C) in an omnivorous consumer: effect of diet isotopic ratio. Funct Ecol 22:255–263
Chikaraishi Y, Ogawa NO, Kashiyama Y, Takano Y, Suga H, Tomitani A, Miyashita H, Ohkouchi N (2009) Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol Oceanogr Methods 7:740–750
Chikaraishi Y, Ogawa NO, Doi H, Ohkouchi N (2011) 15N/14N ratios of amino acids as a tool for studying terrestrial food webs: a case study of terrestrial insects (bees, wasps, and hornets). Ecol Res 26:835–844
Codron D, Luyt J, Lee-Thorp JA, Sponheimer M, de Ruiter D, Codron J (2005) Utilization of savanna-based resources by Plio-Pleistocene baboons. S Afr J Sci 101:245–248
Codron D, Lee-Thorp JA, Sponheimer M, 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. Am J Phys Anthrop 129:204–214
Codron D, Lee-Thorp JA, Sponheimer M, de Ruiter D, Codron J (2008) What insights can baboon feeding ecology provide for early hominid niche differentiation? Int J Primatol 29:757–772
Crowley BE (2012) Stable isotope techniques and applications for primatologists. Int J Primatol 33:673–701
Crowley BE, Carter ML, Karpanty SM, Zihlman AL, Koch PL, Dominy NJ (2010) Stable carbon and nitrogen isotope enrichment in primate tissues. Oecologia 164:611–616
Crowley BE, Thorén S, Rasoazanabary E, Vogel ER, Barrett MA, Zohdy S, Blanco MB, McGoogan KC, Arrigo-Nelson SJ, Irwin MT, Wright PC, Radespiel U, Godfrey LR, Koch PL, Dominy NJ (2011) Explaining geographical variation in the isotope composition of mouse lemurs (Microcebus). J Biogeogr 38:2106–2121
Dalerum F, Angerbjörn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
Fogel ML, Tuross N (2003) Extending the limits of paleodietary studies of humans with compound specific carbon isotope analysis of amino acid. J Archaeol Sci 30:535–545
Gibson L (2011) Possible shift in macaque trophic level following a century of biodiversity loss in Singapore. Primates 52:217–220
Hare PE, Fogel ML, Stafford TW Jr, Mitchell AD, Hoering TC (1991) The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. J Archaeol Sci 18:277–292
Hilderbrand GV, Farley SD, Robbins CT, Hanley TA, Titus K, Servheen C (1996) Use of stable isotopes to determine diet of living and extinct bears. Can J Zool 74:2080–2088
Hilderbrand GV, Hanley TA, Robbins CT, Schwartz CC (1999) Role of brown bears (Ursus arctos) in the flow of marine nitrogen into a terrestrial ecosystem. Oecologia 121:546–550
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326
Hobson KA, Clark RG (1992a) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188
Hobson KA, Clark RG (1992b) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197
Inagaki H, Nigi H (1988) Annual changes in hair length of the Japanese Money (Macaca fuscata fuscata). Primates 29(1):81–89
Jim S, Jones V, Ambrose SH, Evershed RP (2006) Quantifying dietary macronutrient sources of carbon for bone collagen biosynthesis using natural abundance stable carbon isotope analysis. Br J Nutr 95:1055–1062
Keeling CI, Nelson DE (2001) Changes in intramolecular stable carbon isotope ratios with age of the European cave bear (Ursus spelaeus). Oecologia 127:495–500
Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27
Kraft RA, Jahren AH, Saudek CD (2008) Clinical-scale investigation of stable isotopes in human blood: δ13C and δ15N from 406 patients at the Johns Hopkins Medical Institutions. Rapid Commun Mass Spectrom 22:3683–3692
Kurle CM (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. Can J Zool 80:902–909
Lorrain A, Graham B, Menard F, Popp B, Bouillon S, Breugel P, Cherel Y (2009) Nitrogen and carbon isotope values of individual amino acids: a tool to study foraging ecology of penguins in the Southern Ocean. Mar Ecol Prog Ser 391:293–306
Loudon JE, Sponheimer M, Sauther ML, Cuazzo FP (2007) Intraspecific variation in hair δ13C δ15N values of ring-tailed lemur (Leur catta) with known individual histories, behavior, and feeding ecology. Am Phys Anthropol 133:978–985
Martínez del Rio C, Wolf N, Carleton C, Gannes Z (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between delta 15N and animal age. Geochim Cosmochim Acta 48:1135–1140
Mizukami R, Goto M, Izumiyama S, Hayashi H, Yoh M (2005a) Estimation of feeding history by measuring carbon and nitrogen stable isotope ratios in hair of Asiatic black bears. Ursus 16:93–101
Mizukami R, Goto M, Izumiyama S, Yoh M, Ogura N, Hayashi H (2005b) Temporal diet changes recorded by stable isotopes in Asiatic black bear (Ursus thibetanus) hair. Isotopes Environ Health Stud 41:87–94
Nakashita R (2006) Reconstruction of the feeding history of Asiatic black bear (Ursus thibetanus) by carbon and nitrogen stable isotopes. Doctoral dissertation. Tokyo University of Agriculture and Technology, Tokyo, Japan
Narita R, Sasaki K, Goda K, Maeda N, Takayanagi A (2006) Turnover of stable isotopes in Hokkaido brown bear (Ursus arctos yesoyensis). Mamm Stud 31:59–63
Nash SH, Kristal AR, Boyer BB, King IB, Metzgar JS, O’Brien DM (2009) Relation between stable isotope ratios in human red blood cells and hair: implications for using the nitrogen isotope ratio of hair as a biomarker of eicosapentaenoic acid and docosahexaenoic acid. Am J Clin Nutr 90:1642–1647
O’Brien DM, Boggs CL, Fogel ML (2005) The amino acids used in reproduction by butterflies: a comparative study of dietary sources using compound-specific stable isotope analysis. Physiol Biochem Zool 78:819–827
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. J Hum Evol 55:617–626
Oelze VM, Fuller BT, Richards MP, Fruth B, Surbeck M, Hublin JJ, Hohmann G (2011) Exploring the contribution and significance of animal protein in the diet of bonobos by stable isotope ratio analysis of hair. Proc Natl Acad Sci 108:1–6
Raghavan M, McCullagh JS, Lynnerup N, Hedges RE (2010) Amino acid δ13C analysis of hair proteins and bone collagen using liquid chromatography/isotope ratio mass spectrometry: paleodietary implications from intra-individual comparison. Rapid Commun Mass Spectrom 24:541–548
Ramsay MA, Hobson KA (1991) Polar bears make little use of terrestrial food webs: evidence from stable-carbon isotope analysis. Oecologia 86:598–600
Robbins CT, Felicetti LA, Sponheimer M (2005) The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 144:534–540
Roth JD, Hobson KA (2000) Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary reconstruction. Can J Zool 78:848–852
Ryder ML (1973) Hair, Institute of Biology’s Studies in biology No. 41. Edward Arnold, London
Schoeller DA, Minagawa M, Slater R, Kaplan IR (1986) Stable isotopes of carbon, nitrogen and hydrogen in the contemporary north American human food web. Ecol Food Nutr 18:159–170
Schoeninger MJ, DeNiro MJ (1984) Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochim Cosmochem Acta 48:625–639
Schoeninger MJ, DeNiro MJ, Tauber H (1983) Stable nitrogen isotope ratios of bone collagen reflect marine and terrestrial components of prehistoric human diet. Science 220:1381–1383
Schoeninger MJ, Iwaniec UT, Grander KE (1997) Stable isotope ratios indicate diet and habitat use in new world monkeys. Am J Phys Anthropol 103:69–83
Schoeninger MJ, Iwaniec UT, Nash LT (1998) Ecological attributes recorded in stable isotope ratios of arboreal prosimian hair. Oecologia 113:222–230
Schoeninger MJ, Moore J, Sept JM (1999) Subsistence strategies of two “savanna” chimpanzee populations: the stable isotope evidence. Am J Primatol 49:297–314
Schurr MR, Fuentes A, Luecke E, Cortes J, Shaw E (2012) Intergroup variation in stable isotope ratios reflects anthropogenic impact on the Barbary macaques (Macaca syvanus) of Gibralter. Primates 53:31–40
Schwarcz HP (1991) Some theoretical aspects of isotopepaleodiet studies. J Archaeol Sci 18:261–275
Schwertl M, Auerswald K, Schnyder H (2003) Reconstruction of the isotopic history of animal diets by hair segmental analysis. Rapid Commun Mass Spectrom 17:1312–1318
Sponheimer M, Robinson T, Ayliffe L, Roeder B, Hammer J, Passey B, West A, Cerling T, Dearing D, Ehleringer J (2003a) Nitrogen isotopes in mammalian herbivores: hair δ15N values from a controlled feeding study. Int J Osteoarchaeol 13:80–87
Sponheimer M, Robinson T, Ayliffe L, Passey B, Roeder B, Shipley L, Lopez E, Cerling T, Dearing D, Ehleringer J (2003b) An experimental study of carbon-isotope fractionation between diet, hair, and feces of mammalian herbivores. Can J Zool 81:871–876
Sponheimer M, Loudon JE, Codron D, Howells ME, Pruetz JD, Codron J, Ruiter DJ, Lee-Thorp JA (2006) Do “savanna” chimpanzees consume C4 resources? J Hum Evol 51:128–133
Sponheimer M, Codron D, Passey BH, Ruiter DJ, Cerlinig TE, Lee-Thorp JA (2009) Using carbon isotopes to track dietary change in modern, historical, and ancient primates. Am J Phys Anthropol 140:661–670
Sutoh M, Yoneyama T, Koyama T (1987) Variation of Natural 13C abundances in the feces, blood and milk of domestic animals. Nihon Chikusangaku Kaihou 58:730–736 (in Japanese)
Tayasu I, Hirasawa R, Ogawa NO, Ohkouchi N, Yamada K (2011) New organic reference materials for carbon- and nitrogen-stable isotope ratio measurements provided by Center for Ecological Research, Kyoto University, and Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology. Limnology 12:261–266
Tieszen LL, Boutton TW, Tesdahl KG, Slada NA (1983) Fractionation and turnover of stable isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–37
van der Merwe NJ (1982) Carbon isotopes, photosynthesis, and archaeology. Am Sci 70:209–215
White CD, Schwarcz HP (1994) Temporal trends in stable isotopes for Nubian mummy tissues. Am J Phys Anthropol 93:165–187
Acknowledgments
This study was partly supported by the Cooperation Research Program of the Primate Research Institute, Kyoto University (to T.O.). We express our gratitude to Mr. K. Hayakawa for his support during the feeding experiment. The treatment of animals complied with the ethical standards in the guidelines laid down by the Primate Society of Japan and the Primate Research Institute.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Nakashita, R., Hamada, Y., Hirasaki, E. et al. Characteristics of stable isotope signature of diet in tissues of captive Japanese macaques as revealed by controlled feeding. Primates 54, 271–281 (2013). https://doi.org/10.1007/s10329-013-0346-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-013-0346-6