Inter-individual variation in the diet within a group of Japanese macaques and its relationship with social structure investigated by stable isotope and DNA analyses

Abstract

We investigated individual variation in diet in relation to age-sex class and kin relationship in 28 of 40 members of a small group of wild Japanese macaques (Macaca fuscata). We used stable isotope ratios from hair as an index of individual dietary profiles, genetic relatedness as an index of kin relationship, and mitochondrial DNA (mtDNA) haplotype as a marker of being an immigrant or native member of the group. The range of carbon and nitrogen stable isotope ratios from hair of individual macaques (δ13C: −24.1‰ to −22.6‰, δ15N:3.8–5.5‰), which reflected their diet over a period of ~ 6 months, implied small individual variation in diet. The results of PERMANOVA implied that there were no significant effects of age class, sex, or mtDNA haplotype on hair stable isotope ratios between individuals, or on the variation in individual diet. However, the isotope values of males with mtDNA haplotypes that differed from those of the native females appeared to differ from those of other group members, which implies that immigrant males might have had a different diet profile from that of native group members. Furthermore, there was a weak correlation trend between genetic relatedness and differences in stable isotope ratios between pairs of individuals. Differences in stable isotope values were more marked in pairs with a more distant genetic relationship. This implies that within the group, closely related kin tended to forage together to avoid competing for food. However, this effect might have been weak because the size of the group was small relative to the size of the food patches, thereby reducing competition.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Agetsuma N (2001) Relation between age-sex classes and dietary selection of wild Japanese monkeys. Ecol Res 16:759–763

    Google Scholar 

  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  3. Chapman CA, Chapman LN (2000) Determinant of group size in primates: the importance of travel cost. In: Boinski S, Garber PA (eds) On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 24–41

    Google Scholar 

  4. 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

    Google Scholar 

  5. 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 13C, 15N, and %N. Am J Phys Anthropol 129:204–214

    PubMed  Google Scholar 

  6. Core Team R (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  7. Crowley BE, Carter ML, Karpanty SM, Zihlman AL, Koch PL, Dominy NJ (2010) Stable carbon and nitrogen isotope enrichment in primate tissues. Oecologia 164:611–626

    PubMed  PubMed Central  Google Scholar 

  8. Crowley BE, Thoren S, Rasoazanabary E, Vogel ER, Barrett A, Zohdy S, Blanco MB, McGroogan KC, Arrigo-Nelson SJ, Irwin MT, Wright PC, Radespiel U, Godfrey LR, Koch PL, Dominy NJ (2011) Explaining geographic variation in the isotope composition of mouse lemurs (Microcebus). J Biogeogr 38:2106–2121

    Google Scholar 

  9. Crowley BE, Rasoazanabary E, Godfrey R (2014) Stable isotopes compliment focal individual observation and confirm dietary variability in reddish-gray mouse lemur (Microcebus griseorufus) from southwestern Madagascar. Am J Phys Anthrop 155:77–90

    PubMed  Google Scholar 

  10. Crowley BE, Reitsema LJ, Oelze VM, Sponheimer M (2016) Advances in primate stable ecology—achievements and prospects. Am J Primatol 78:995–1003

    CAS  PubMed  Google Scholar 

  11. Dammhahn M, Kappeler PM (2010) Scramble or contest competition over food in solitary foraging mouse lemur (Microcebus spp.): new insights from stable isotopes. American J Phys Anthropol 141:181–189

    Google Scholar 

  12. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    CAS  Google Scholar 

  13. Fahy GE, Richards M, Riedel J, Hublin J-J, Boesch C (2013) Stable isotope evidence of meat eating and hunting specialization in adult male chimpanzees. PNAS 110:5829–5833

    CAS  PubMed  Google Scholar 

  14. Fahy GE, Richards M, Riedel J, Hublin J-J, Boesch C (2014) Stable nitrogen isotope analysis of dentine serial sections elucidate sex differences in weaning patterns of wild chimpanzees (Pan troglodytes). Am J Phys Anthropol 153:642–653

    Google Scholar 

  15. Fourie NH, Lee-Thorp JA, Ackermann RR (2008) Biogeochemical and craniometric investigation of dietary ecology, niche separation, and taxonomy of Plio-Pleistocene cercopithecoids from the Makapansgat Limeworks. Am J Phys Anthropol 135:121–135

    PubMed  Google Scholar 

  16. Furuichi T (1984) Symmetrical pattern in non-agonistic social interactions found in unprovisioned Japanese macaques. J Ethol 2:109–119

    Google Scholar 

  17. Furuichi T (1985) Inter-male association in a wild Japanese macaque troop on Yakushima Island, Japan. Primates 26:219–237

    Google Scholar 

  18. Hanya G (2003) Age differences in food intake and dietary selection of wild male Japanese macaques. Primates 44:333–339

    PubMed  Google Scholar 

  19. Houle A, Chapman CA, Vickery WL (2010) Intratree vertical variation of fruit density and the nature of contest competition in frugivores. Behav Ecol Sociobiol 64:429–441

    Google Scholar 

  20. Inagaki H, Nigi H (1988) Annual changes in hair length of the Japanese Money (Macaca fuscata fuscata). Primates 29:81–89

    Google Scholar 

  21. Inoue E, Inoue-Murayama M, Vigilant L, Tanenaka O, Nishida T (2008) Relatedness in wild chimpanzees: influence of paternity, male philopatry, and demographic factors. Am J Phys Anthrop 137:256–262

    PubMed  Google Scholar 

  22. Isbell LA, Young TP (2002) Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behaviour 139:177–202

    Google Scholar 

  23. Iwamoto T (1988) Food and energetic of provisioned wild Japanese macaques (Macaca fuscata). In: Fa JE, Southwick CH (eds) Ecology and Behaviour of Food-enhanced primate groups. Alan R. Liss, Inc., New York, pp 79–94

    Google Scholar 

  24. Janson CH, van Schaik CP (1988) Recognizing the many faces of primate food competition: methods. Behaviour 105:165–186

    Google Scholar 

  25. Kanthaswamy S, von Dollen A, Kurushima JD, Alminas O, Rogers J, Ferguson B, Leche NW, Allen PC, Smith DG (2006) Microsatellite markers for standardized genetic management of captive colonies of rhesus macaques (Macaca mulatta). Am J Primatol 68:73–95

    CAS  PubMed  Google Scholar 

  26. Kawamoto Y, Shotake T, Nozawa K, Kawamoto S, Tomari K, Kawai S, Shirai K, Morimitsu Y, Takagi N, Akaza H, Fujii H, Hagihara K, Aizawa K, Akachi S, Oi T, Hayashi S (2007) Postglacial population expansion of Japanese macaques (Macaca fuscata) inferred from mitochondrial DNA phylogeography. Primates 48:27–40

    PubMed  Google Scholar 

  27. Kawamoto Y, Tomari K, Kawai S, Kawamoto S (2008) Genetics of the Shimokita macaque population suggests an ancient bottleneck. Primates 49:32–40

    PubMed  Google Scholar 

  28. Kawamura S (1958) Matrilineal social rank in the Minoo-B troop: a study of the rank system of Japanese monkeys. Primates 1:149–156

    Google Scholar 

  29. Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783

    Google Scholar 

  30. Koike S, Nakashita R, Kozakai C, Nakajima A, Nemoto Y, Yamazaki K (2016) Baseline characterization of the diet and stable isotope signatures of bears that consume natural foods in central Japan. Eur J Wildl Res 62:23–31

    Google Scholar 

  31. Krigbaum J, Berger MH, Daegling DJ, McGraw WS (2013) Stable isotope canopy effect for sympatric monkeys at Taї Forest, Côte D’Ivoire. Biol Lett 9(2013):0466

    Google Scholar 

  32. Legendre P, Legendre L (1998) Numerical ecology, 2nd English Edition edn. Elsevier, Amsterdam

    Google Scholar 

  33. Lewis MC, West AG, O’Riain MJ (2018) Isotopic assessment of marine food consumption by natural-foraging chacma baboons on the Cape Peninsula, South Africa. Am J Phys Anthropol 165:77–93

    PubMed  Google Scholar 

  34. Litivaitis JA (2000) Investigating food habits of terrestrial vertebrate. In: Fuller TK (ed) LB Boitani. Research techniques in animal ecology. Columbia University Press, New York, pp 21–34

    Google Scholar 

  35. Loudon JE, Sponheimer M, Sauther ML, Cuozzo FP (2007) Intraspecific variation in hair δ13C and δ15N values of ring-tailed lemurs (Lemur catta) with known individual histories, behavior, and feeding ecology. Am J Phys Anthropol 133:978–985

    PubMed  Google Scholar 

  36. Loudon JE, Sandberg PA, Wrangham RW, Fahey B, Sponheimer M (2016) The stable isotope ecology of Pan in Uganda and beyond. Am J Primatol 78:1070–1085

    CAS  PubMed  Google Scholar 

  37. Majolo B, Ventura R, Koyama NF, Hardie SM, Jones BM, Knapp LA, Schino G (2009) Analysing the effects of group size and food competition on Japanese macaque social relationships. Behaviour 146:113–137

    Google Scholar 

  38. Martin P, Bateson P (1987) Measuring Behaviour – an introductory guide. Cambridge University Press, Cambridge

    Google Scholar 

  39. Medina E, Minchin P (1980) Stratification of δ13C values of leaves in Amazonian rain forests. Oecologia 45:377–378

    CAS  PubMed  Google Scholar 

  40. Minagawa M (1992) Reconstruction of human diet from δ13C and δ15 N in contemporary Japanese hair: a stochastic method for estimating multi-source contribution by double isotopic tracers. Appl Geochem 7:145–158

    CAS  Google Scholar 

  41. Minagawa M (2001) Dietary pattern of prehistoric Japanese populations inferred from stable carbon and nitrogen isotopes in bone protein. Bull Natl Mus Jpn Hist 86:333–357 (in Japanese)

    Google Scholar 

  42. Minagawa M, Akazawa T (1988) Food intake by Jomon people. Iden 42:15–23 (in Japanese)

    Google Scholar 

  43. 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

    CAS  Google Scholar 

  44. Miyama K (2005) Nitrogen stable isotope of plants in mountain ecosystem. Bachelor thesis: Tokyo University of Agriculture and Technology, Tokyo, Japan, 10 pp. (in Japanese)

  45. Mori A (1995) Rank and age related feeding strategy observed through field experiments in the Koshima group of Japanese macaques. Primates 36:11–26

    Google Scholar 

  46. Nakagawa N (2000) Foraging energetic in Patas monkeys (Erythrocebus patas) and Tantalus monkeys (Cercopithecus aethiops tantalus): implications for reproductive seasonality. Am J Primatol 52:169–185

    CAS  PubMed  Google Scholar 

  47. Nakashita R (2006) Reconstruction of the feeding history of Asiatic black bear (Ursus thibetanus) by carbon and nitrogen stable isotope. Doctoral dissertation: Tokyo University of Agriculture and Technology

  48. Nakashita R, Hamada Y, Hirasaki E, Suzuki J, Oi T (2013) Characteristics of stable isotope signature of diet in the tissues of captive Japanese monkeys, revealed by controlled feeding. Primate 54:271–281

    Google Scholar 

  49. Nakayama Y, Matsuoka S, Watanuki Y (1999) Feeding rates and energy deficit of juvenile and adult Japanese monkeys in a cool temperate area with snow coverage. Ecol Res 14:291–301

    Google Scholar 

  50. Narita R. (2003) Dietary analysis on Asiatic black bears by stable isotope signature—importance of animal matter. Master’s thesis: Kyoto University, p 37, Kyoto, Japan

  51. Nicholson AJ (1954) An outline of the dynamics of animal population. Aust J Zool 2:9–65

    Google Scholar 

  52. O’Regan HJ, Chenery C, Lamb A, Stevens RE, Rook L, Elton S (2008) Modern macaque dietary heterogeneity assessed using stable isotope analysis of hair and bone. J Hum Evol 55:617–626

    PubMed  Google Scholar 

  53. Oelze VM (2016) Reconstructing temporal variation in great ape and other primate diets: a methodological framework for isotope analysis in hair. Am J Primatol. https://doi.org/10.1002/ajp.22497

    Article  PubMed  Google Scholar 

  54. Oelze VM, Fuller BT, Richards MP, Fruth B, Surbeck M, Hubblin J, Hofmann 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 USA 108:1–6

    Google Scholar 

  55. Oelze VM, Head JS, Robbins MM, Richard M, Boesch C (2014) Niche differentiation and dietary seasonality among sympatric gorillas and chimpanzees in Loango National Park (Gabon) revealed by stable isotope analysis. J Hum Evol 66:95–106

    PubMed  Google Scholar 

  56. Oftedal OT, Whiten A, Southgate D, Soest PV (1991) The nutritional consequences of foraging primates: the relationship of nutritional intakes to nutrient requirements. Philos Trans R Soc Lond B Biol Sci 334:161–170

    CAS  PubMed  Google Scholar 

  57. Oi T (2014) Inter-species relationship between Asiatic black bears and Japanese macaques, a deduction from the comparison of feeding behaviors. Reichorui Kenkyu [Primate Research] 29:123–135 (in Japanese with English summary)

    Google Scholar 

  58. Otani Y, Sawada A, Hanya G (2014) Short-term separation from groups by male Japanese macaques: cost and benefits in feeding behavior and social interaction. Am J Primatol. https://doi.org/10.1002/ajp.22241

    Article  PubMed  Google Scholar 

  59. Otsu and Shiga Association for Monkey Management (2006) Management Plan for Otsu-E (Keiji-1) Japanese Macaque Group. Otsu City Government (in Japanese)

  60. Portman OW (1970) Nutritional requirements (NRC) of nonhuman primates. In: Harris RS (ed) Feeding and nutrition of non-human primates. Academic Press, New York, pp 98–115

    Google Scholar 

  61. Primate Research Institute (2008) Guideline for field research of non-human primates. (http://www.pri.kyoto-u.ac.jp/research/guide-e2008.html)

  62. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    PubMed  PubMed Central  Google Scholar 

  63. Reitsema LJ (2012) Introducing fecal stable isotope analysis in primate weaning studies. Am J Primatol 74:926–939

    CAS  PubMed  Google Scholar 

  64. Saito C (1996) Dominance and feeding success in female Japanese macaques, Macaca fuscata: effects of food patch size and inter-patch distance. Anim Behav 51:967–980

    Google Scholar 

  65. Schillaci MS, Castellini JM, Stricker CA, Jones-Engel L, Lee BPH, O’Hara TM (2014) Variation in hair δ13C and δ15N values in long-tailed macaques (Macaca fascicularis) from Singapore. Primated 55:25–34

    Google Scholar 

  66. Schillaci MS, Lintlop J, Sumra M, Pizarro M, Jones-Engel L (2019) Hair cortisol and stable carbon and nitrogen isotope ratios in barbary macaques (Macaca Sylvanus) from Gibraltar. Rapid Commun Mass Spectrom 33:831–838

    CAS  PubMed  Google Scholar 

  67. Schoeninger MJ, DeNiro MJ (1983) Stable nitrogen isotope ratios of bone collagen reflect marine and terrestrial components of prehistoric human diet. Science 220:1381–1383

    CAS  PubMed  Google Scholar 

  68. Schoeninger MJ, Iwaniec UT, Glander KE (1997) Stable isotope ratios indicate diet and habitat use in New world monkeys. Am J Phys Anthropol 103:69–83

    CAS  PubMed  Google Scholar 

  69. Schoeninger MJ, Moore J, Sept JM (1999) Subsistence strategy of two “Savanna” chimpanzee populations: the stable isotope evidence. Am J Primatol 49:297–314

    CAS  PubMed  Google Scholar 

  70. Schoeninger MJ, Most CA, Moore JJ, Somerville AD (2016) Environmental variables across Pan troglodytes study sites correspond with the carbon, but not the nitrogen, stable isotope rations of Chimpanzee hair. Am J Primatol 78:1055–1069

    CAS  PubMed  Google Scholar 

  71. Schurr MR, Fuentes A, Luecke E, Cortes J, Shaw E (2011) Intergroup variation in stable isotope ratios reflects anthropogenic impact on the Barbary macaques (Macaca sylvanus) of Gibraltar. Primates. https://doi.org/10.1007/s10329-011-0268-0

    Article  PubMed  Google Scholar 

  72. Sponheimer M, Loudon JE, Codon D, Howell ME, Pruetz JD, Codron J, de Ruiter DJ, Lee-Thorp JA (2006) Do “savanna” chimpanzees consume C4 resources? J Hum Evol 51:128–133

    CAS  PubMed  Google Scholar 

  73. Sponheimer M, Codon D, Passey BH, de Ruiter DJ, Cerling TE, Lee-Thorp JA (2009) Using carbon isotope to track dietary change in modern, historical, and ancient primates. Am J Phys Anthropol 140:661–670

    PubMed  Google Scholar 

  74. Sprague DS, Suzuki S, Takahashi H, Sato S (1998) Male life history in natural population of Japanese macaques: migration, dominance rank, and troop participation of males in two habitats. Primates 39:351–363

    Google Scholar 

  75. Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Google Scholar 

  76. Sukmak M, Malaivijitnond S, Schülke O, Ostner J, Hamada Y, Wajjwaku W (2014) Preliminary study of the genetic diversity of eastern Assamese macaques (Macaca assamensis assamensis) in Thailand based on mitochondrial DNA and microsatellite markers. Primates 55:189–197

    PubMed  Google Scholar 

  77. Taniguchi H (2015) How the physical properties of food influence it selection by infant Japanese macaques inhabiting a snow-covered area. Am J Primatol 77:285–295

    PubMed  Google Scholar 

  78. Terbogh J, Johnson CH (1986) Socioecology of primate groups. Ann Rev Ecol Syst 17:111–135

    Google Scholar 

  79. Thackeray JF, Henzi SP, Brain CK (1996) Stable carbon and nitrogen isotope analysis of bone collagen in Papiocynocephalus ursinus: comparison with ungulates and Homo sapiens from southern and East African environments. S Afr J Sci 92:209–221

    CAS  Google Scholar 

  80. Tsuji Y (2010) Regional, temporal, and interindividual variation in the feeding ecology of Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer, Tokyo, pp 99–127

    Google Scholar 

  81. Tsuji Y, Takatsuki S (2012) Interannual variation in nut abundance is related to agonistic interactions of foraging female Japanese macaques (Macaca fuscata). Int J Primatol 33:489–512

    Google Scholar 

  82. van Schaik CP (1989) The ecology of social relationships among female primates. In: Staden V, Foley RA (eds) Comparative socioecology. The behavioural ecology of human and other mammals. Blackwell, Oxford, pp 195–218

    Google Scholar 

  83. van Schaik CP, van Noordwijk MA (1986) The hidden costs of sociality: intra-group variation in feeding strategies in Sumatran long-tailed macaques (Macaca fascicularis). Behaviours 99:296–315

    Google Scholar 

  84. Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300

    Google Scholar 

  85. Yamagiwa J, Hill DA (1998) Intraspecific variation in the social organization of Japanese macaques: past and present scope of field studies in natural habitats. Primates 39:257–273

    Google Scholar 

Download references

Acknowledgements

We appreciate the kind support of the Shiga prefectural government and the Otsu city government in collecting samples and background data. We thank Dr. N. Nakagawa for useful advice on a previous draft of the manuscript, and Ms. S. Segawa and Ms. S. Ohkubo for support during sample preparation. All aspects of this research adhered to the Guidelines of Field Research on Non-Human Primates established by the Primate Research Institute, Kyoto University (Primate Research Institute 2008), for the ethical treatment of nonhuman primates.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Toru Oi.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Verify currency and authenticity via CrossMark

Cite this article

Oi, T., Hamasaki, Si., Seino, H. et al. Inter-individual variation in the diet within a group of Japanese macaques and its relationship with social structure investigated by stable isotope and DNA analyses. Primates 62, 103–112 (2021). https://doi.org/10.1007/s10329-020-00840-3

Download citation

Keywords

  • Japanese macaque
  • Food habit
  • Individual variation
  • Stable isotope analyses
  • Genetic relatedness
  • mtDNA