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Primates

, Volume 55, Issue 1, pp 25–34 | Cite as

Variation in hair δ13C and δ15N values in long-tailed macaques (Macaca fascicularis) from Singapore

  • Michael A. Schillaci
  • J. Margaret Castellini
  • Craig A. Stricker
  • Lisa Jones-Engel
  • Benjamin P. Y.-H. Lee
  • Todd M. O’Hara
Original Article

Abstract

Much of the primatology literature on stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) has focused on African and New World species, with comparatively little research published on Asian primates. Here we present hair δ13C and δ15N isotope values for a sample of 33 long-tailed macaques from Singapore. We evaluate the suggestion by a previous researcher that forest degradation and biodiversity loss in Singapore have led to a decline in macaque trophic level. The results of our analysis indicated significant spatial variability in δ13C but not δ15N. The range of variation in δ13C was consistent with a diet based on C3 resources, with one group exhibiting low values consistent with a closed canopy environment. Relative to other macaque species from Europe and Asia, the macaques from Singapore exhibited a low mean δ13C value but mid-range mean δ15N value. Previous research suggesting a decline in macaque trophic level is not supported by the results of our study.

Keywords

Stable isotopes δ13δ15Primates Macaques Macaca fascicularis Singapore 

Notes

Acknowledgments

We thank the National Parks Board (Singapore), especially Sharon Chan, for supporting the project. We thank Dr. James Louden and Dr. Mark Schurr for their insightful comments and criticisms of earlier drafts. Trapping and data-collection procedures used for this study were approved by the institutional animal care and use committee of the University of Toronto (protocol no. 20005356). Partial funding for this project was provided by the University of Toronto Scarborough, and the University of Toronto Connaught Fund (awarded to M.A.S.). Thanks are due to Cayce Gulbransen (U.S. Geological Survey) for conducting the stable isotope analyses. The content of this paper is solely the responsibility of the authors and does not necessarily represent the views of our funders. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

References

  1. Agoramoorthy G, Hsu MJ (2006) Population status of long-tailed macaques (Macaca fascicularis) in Singapore. Mammalia 70(3/4):300–302CrossRefGoogle Scholar
  2. Brook BW, Sodhi NS, Ng PKL (2003) Catastrophic extinctions follow deforestation in Singapore. Nature 424:420–423PubMedCrossRefGoogle Scholar
  3. Codron D, Lee-Thorp JA, Sponheimer M, de Ruiter D, Codron J (2006) Inter- and intrahabitat variability of chacma baboons (Papio ursinus) in South African savannas based on fecal δ13C, δ15N, and %N. Am J Phys Anthropol 129:204–214PubMedCrossRefGoogle Scholar
  4. Corlett RT (1992) The ecological transformation of Singapore, 1819–1900. J Biogeogr 19:411–420CrossRefGoogle Scholar
  5. Crowley BE (2012) Stable isotope techniques and applications for primatologists. Int J Primatol 33:673–701CrossRefGoogle Scholar
  6. Crowley BE, Godfrey LR, Irwin MT (2011) A glance to the past: subfossils, stable isotopes, seed dispersal, and lemur species loss in southern Madagascar. Am J Primatol 73:25–37PubMedCrossRefGoogle Scholar
  7. Crowley BE, McGoogan KC, Lehman SM (2012) Edge effects on foliar stable isotope values in a Madagascan tropical dry forest. PLoS ONE 7(9):e44538PubMedCentralPubMedCrossRefGoogle Scholar
  8. Davison G, Tan R, Lee B (2012) Wild Singapore. John Beaufoy, UKGoogle Scholar
  9. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351CrossRefGoogle Scholar
  10. Engel G, O’Hara TM, Cardona-Marek T, Heidrich J, Chalise MK, Kyes R, Jones-Engel L (2010) Synanthropic primates in Asia: potential sentinels for environmental toxins. Am J Phys Anthropol 142:453–460PubMedCentralPubMedCrossRefGoogle Scholar
  11. Fooden J (1982) Ecogeographic segregation of macaque species. Primates 23:574–579CrossRefGoogle Scholar
  12. Fry B, Brand W, Mersch FJ, Tholke K, Garritt R (1992) Automated analysis system for coupled δ13C and δ15 N measurements. Anal Chem 64:288–291Google Scholar
  13. Gibson L (2011) Possible shift in macaque trophic level following a century of biodiversity loss in Singapore. Primates 52:217–220PubMedCrossRefGoogle Scholar
  14. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197CrossRefGoogle Scholar
  15. Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95:388–394CrossRefGoogle Scholar
  16. Jenkins SG, Partridge ST, Stephenson TR, Farley SD, Robbins CT (2001) Nitrogen and carbon isotope fractionation between mothers, neonates, and nursing offspring. Oecologia 129:336–341Google Scholar
  17. Kohn MJ (2010) Carbon isotope composition of terrestrial C3 plants as indicators of (paleo)ecology and (paleo)climate. Proc Natl Acad Sci USA 107:19691–19695PubMedCrossRefGoogle Scholar
  18. Lee BPY-H, Chan S (2011) Lessons and challenges in the management of long-tailed macaques in urban Singapore. In: Gumert MD, Fuentes A, Jones-Engel L (eds) Monkeys on the edge: ecology and management of log-tailed macaques and their interface with humans. Cambridge University Press, UK, pp 307–313Google Scholar
  19. Loudon JE, Sponheimer M, Sauther ML, Cuozzo FP (2007) Intraspecific variation in hair δ13C and δ15 N values of Ring-tailed lemurs (Lemur catta) with known individual histories, behavior, and feeding ecology. Am J Phys Anthropol 133:978–985PubMedCrossRefGoogle Scholar
  20. Medina E, Minchin P (1980) Stratification of δ13C values of leaves in Amazonian rain forests. Oecologia 45:377–378CrossRefGoogle Scholar
  21. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1125–1140Google Scholar
  22. Nakagawa M, Hyodo F, Nakashizuka T (2007) Effect of forest use on trophic levels of small mammals: an analysis using stable isotopes. Can J Zool 85:472–478CrossRefGoogle Scholar
  23. Nakashita R, Hamada Y, Hirasaki E, Suzuki J, Oi T (2013) Characteristics of stable isotope signature of diet in tissues of captive Japanese macaques as revealed by controlled feeding. Primates. doi: 10.1007/s10329-013-0346-6 PubMedGoogle Scholar
  24. O’Leary MH (1981) Carbon isotope fractionation in plants. Phytochemistry 20:553–567CrossRefGoogle Scholar
  25. O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336CrossRefGoogle Scholar
  26. O’Regan HJ, Chenery C, Lamb AL, Stevens RE, Rook L, Elton S (2008) Modern macaque dietary heterogeneity assessed using stable isotope analysis of hair and bone. J Hum Evol 55:617–626PubMedCrossRefGoogle Scholar
  27. Reitsema LJ (2012) Introducing fecal stable isotope analysis in primate weaning studies. Am J Primatol 74:926–939PubMedCrossRefGoogle Scholar
  28. Sandberg PA, Louden JE, Sponheimer M (2012) Stable isotope analysis in primatology: a critical review. Am J Primatol 74:969–989PubMedCrossRefGoogle Scholar
  29. Schillaci MA, Schillaci ME (2009) Estimating the probability that the sample mean is within a desired fraction of the standard deviation of the true mean. J Hum Evol 56:134–138PubMedCrossRefGoogle Scholar
  30. Schillaci MA, Jones-Engel L, Lee BPY-H, Fuentes A, Aggimarangsee N, Engel GA, Sutthiipat T (2007) Morphology and somatometric growth of long-tailed macaques (Macaca fascicularis fascicularis) in Singapore. Biol J Linn Soc 92:675–694CrossRefGoogle Scholar
  31. Schillaci MA, Saravia S, Lee BPY-H, Matheson C (2011a) Preliminary report on mitochondrial DNA variation in Macaca fascicularis from Singapore. Raffles Bul Zool 59:101–108Google Scholar
  32. Schillaci MA, Lee BPY-H, Castellini JM, Reid MJC, O’Hara TM (2011b) Lead levels in long-tailed macaque (Macaca fascicularis) hair from Singapore. Primates 52:163–170PubMedCrossRefGoogle Scholar
  33. Schoeninger MJ (2010) Toward a δ13C isoscape for primates. In: West JB, Bowen GJ, Dawson TE, Tu KP (eds) Isoscapes: understanding movement, pattern, and process on Earth through isotope mapping. Springer, New York, pp 319–333CrossRefGoogle Scholar
  34. Schoeninger MJ, DeNiro MJ (1984) Nitrogen and carbon isotopic composition of bone collegen from marine and terrestrial animals. Geochim Cosmochim Acta 48:625–639CrossRefGoogle Scholar
  35. Schoeninger MJ, Iwaniec UT, Glander KE (1997) Stable isotope ratios monitor diet and habitat use in New World monkeys. Am J Phys Anthropol 103:69–83PubMedCrossRefGoogle Scholar
  36. Schoeninger MJ, Iwaniec UT, Nash LT (1998) Ecological attributes recorded in stable isotop ratios of arboreal prosimian hair. Oecologia 113:222–230CrossRefGoogle Scholar
  37. Schoeninger MJ, Moore J, Sept JM (1999) Subsistence strategies of two “savanna” chimpanzee populations: the stable isotope evidence. Am J Primatol 49:297–314PubMedCrossRefGoogle Scholar
  38. Schurr MR, Fuentes A, Luecke E, Cortes J, Shaw E (2012) Intergroup variation in stable isotope ratios reflect anthropogenic impact on the Barbary macaques (Macaca sylvanus) of Gibraltar. Primates 53:31–40PubMedCrossRefGoogle Scholar
  39. Sha JCM, Hanya G (2013) Diet, activity, habitat use, and ranging of two neighboring groups of food-enhanced long-tailed macaques (Macaca fascicularis). Am J Primatol. doi: 10.1002/ajp.22137 PubMedGoogle Scholar
  40. Sha JCM, Gumert MD, Lee BPY-H, Fuentes A, Rajathurai S, Chan S, Jones-Engel L (2009a) Status of the long-tailed macaque Macaca fascicularis in Singapore and implications for management. Biodiversity Conserv 18:2909–2926CrossRefGoogle Scholar
  41. Sha JCM, Gumert MD, Lee BPY-H, Jones-Engel L, Chan S, Fuentes A (2009b) Macaque-human interactions and the societal perceptions of macaques in Singapore. Am J Primatol 71:825–839PubMedCrossRefGoogle Scholar
  42. Sponheimer M, Loudon JE, Codron D, Howells ME, Pruetz JD, Codron J, de Ruiter DJ, Lee-Thorp JA (2006) Do “savanna” chimpanzees consume C4 resources? J Hum Evol 51:128–133PubMedCrossRefGoogle Scholar
  43. Van der Merwe NJ, Medina E (1989) Photosynthesis and 13C/12C ratios in Amazonian rain forests. Geochim Cosmochim Acta 53:1091–1094CrossRefGoogle Scholar
  44. Virginia RA, Delwiche CC (1982) Natural 15N abundance of presumed N2-fixing and non-N2-fixing plants from selected ecosystems. Oecologia 54:317–325CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2013

Authors and Affiliations

  • Michael A. Schillaci
    • 1
  • J. Margaret Castellini
    • 2
  • Craig A. Stricker
    • 3
  • Lisa Jones-Engel
    • 4
  • Benjamin P. Y.-H. Lee
    • 5
    • 6
  • Todd M. O’Hara
    • 7
  1. 1.Department of AnthropologyUniversity of Toronto ScarboroughTorontoCanada
  2. 2.Institute of Marine Science, School of Fisheries and Ocean SciencesUniversity of Alaska FairbanksFairbanksUSA
  3. 3.U.S. Geological SurveyFort Collins Science CenterDenverUSA
  4. 4.National Primate Research CenterUniversity of WashingtonSeattleUSA
  5. 5.Durrell Institute of Conservation and Ecology, School of Anthropology and ConservationUniversity of KentCanterburyUK
  6. 6.Conservation DivisionNational Parks BoardSingaporeSingapore
  7. 7.Department of Biology and Wildlife, Institute of Arctic BiologyUniversity of Alaska FairbanksFairbanksUSA

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