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Disability and Dominance Rank in Adult Female and Male Japanese Macaques (Macaca fuscata)

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Abstract

More than 30 years ago, Fedigan (Primate paradigms: sex roles and social bonds, 2nd, 1992 edn. Eden Press, Montreal, 1982) recognized and emphasized that social dominance was not just a reflection of physical size, strength and aggression in nonhuman primates but rather involved a multitude of complex factors and social dynamics. In the free-ranging group of Japanese macaques (Macaca fuscata) on Awaji Island, Japan, physical disabilities in the form of congenital limb malformations (CLMs) affect around 17% of the population. This group provides an opportunity to examine dominance rank in relation to physical impairment. Here, we present an analysis of dominance rank in the adult female and adult male Japanese macaques in the Awajishima group using behavioural data collected in 2005, 2006 and 2007 on 38 adult females (12 with CLMs) and in 2015 on 22 adult males (7 with CLMs). Once we controlled for matrilineal kinship, we found that disabled females tended to hold somewhat lower than expected dominance ranks. In contrast, disabled males were interspersed throughout the rank order, and disability was not associated significantly with dominance rank. However, age class had a statistically significant effect on dominance rank in males, such that older males tended to rank higher than younger males. Our results underscore Fedigan’s insights by demonstrating some of the complexities of dominance relationships in the context of the extensive physical variation shown in this group of Japanese macaques.

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Notes

  1. 1.

    Six of the interactions among the females were also observed during informal “peanut tests” that TN and HN conducted spontaneously during provision feeding.

References

  • Abbott DH, Keverne EB, Bercovitch FD, Shively CA, Medoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T Jr, Sapolsky RM (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43:67–82

    Article  CAS  Google Scholar 

  • Alberts SC, Watts HE, Altmann J (2002) Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Anim Behav 65:821–840

    Article  Google Scholar 

  • Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunites to paternity success. Anim Behav 72:1177–1196

    Article  Google Scholar 

  • Berard JD (1999) A four-year study of the association between male dominance rank, residency status, and resproductive activity in rhesus macaques (Macaca mulatta). Primates 40(1):159–175

    Article  CAS  Google Scholar 

  • Berard JD, Nürnberg P, Epplen JT, Schmidtke J (1993) Male rank, reproductive behavior, and reproductive success in free-ranging rhesus macaques. Primates 34(4):481–498

    Article  Google Scholar 

  • Bercovitch FB, Berard JD (1993) Life-history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behav Ecol Sociobiol 32(2):103–109

    Article  Google Scholar 

  • Bergstrom ML, Fedigan LM (2010) Dominance among female white-faced capuchin monkeys (Cebus capucinus): hierarchical linearity, nepotism, strength and stability. Behaviour 147:899–931

    Article  Google Scholar 

  • Bergstrom ML, Fedigan LM (2013) Dominance style of female white-faced capuchins. Am J Phys Anthropol 150:591–601

    Article  Google Scholar 

  • Chapais B (1988a) Experimental matrilineal inheritance of rank in female Japanese macaques. Anim Behav 36(4):1025–1037

    Article  Google Scholar 

  • Chapais B (1988b) Rank maintenance in female Japanese macaques: Experimental evidence for social dependency. Behaviour 104(1):41–58

    Article  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Cuozzo FP, Sauther ML (2004) Tooth loss, survival, and resource use in wild ring-tailed lemurs (Lemur catta): implications for inferring conspecific care in fossil hominids. J Hum Evol 46:623–631

    Article  Google Scholar 

  • Dey CJ, Quinn JS (2014) Individual attributes and self-organizational processes affect dominance network structure in pukeko. Behav Ecol 25(6):1402–1408

    Article  Google Scholar 

  • Dey CJ, Tan QYJ, O'Connor CM, Reddon AR, Caldwell JR, Balshine S (2015) Dominance network structure across reproductive contexts in the cooperatively breeding cichlid fish Neolamprologus pulcher. Curr Zool 61(1):45–54

    Article  Google Scholar 

  • Drews C (1993) The concept and definition of dominance in animal behaviour. Behaviour 125(3/4):283–313

    Article  Google Scholar 

  • Fedigan LM (1982) Primate paradigms: sex roles and social bonds, 2nd, 1992 edn. Eden Press, Montreal

    Google Scholar 

  • Fushing Lab and McCowan Lab (2015) Introduction to perc package. University of California, Davis https://cran.r-project.org/web/packages/Perc/vignettes/Perc.html

    Google Scholar 

  • Hamada Y, Yamamoto A (2010) Morphological characteristics, growth, and aging in Japanse macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Primatology monographs. Springer, Tokyo, pp 27–52

    Google Scholar 

  • Inoue E, Takenaka O (2008) The effect of male tenure and female mate choice on paternity in free-ranging Japanese macaques. Am J Primatol 70:62–68

    Article  Google Scholar 

  • Inoue-Murayama M, Inoue E, Watanabe K, Takenaka A, Murayama Y (2010) Behavior-related candidate genes in Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Primatology Monographs. Springer, Tokyo, pp 293–301

    Chapter  Google Scholar 

  • Jack K, Fedigan LM (2006) Why be alpha male? Dominance and resproductive success in wild white-faced capuchins (Cebus capucinus). In: Estrada A, Garber P, Pavelka M, Luecke L (eds) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior and conservation. Kluwer Press, pp 387–386

    Google Scholar 

  • Kaigaishi Y, Nakamichi M, Yamada K (2016) Cooperative problem solving in Japanese macaques in Awajishima group. Paper presented at the primate research supplement: the 31st congress of Primate Society of Japan. J-Stage:A1

    Google Scholar 

  • Kasumovic MM, Mason AC, Andrade MCB, Elias DO (2010) The relative importance of RHP and resource quality in contests with ownership asymmetries. Behav Ecol 22(1):39–45

    Article  Google Scholar 

  • Kawamura S (1958) The matriarchal social order in the Minoo-B group. Primates 1(2):149–156

    Article  Google Scholar 

  • Kokko H (2013) Dyadic contests: modeling fights between two individuals. In: Animal contests. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9781139051248.004

    Chapter  Google Scholar 

  • Koyama N (1967) On dominance and kinship of a wild Japanese monkey troop in Arashiyama. Primates 8:189–216

    Article  Google Scholar 

  • Koyama N (1970) Changes in dominance rank and division of a wild Japanese monkey troop in Arashiyama. Primates 11:335–390

    Article  Google Scholar 

  • Koyama T, Fujii H, Yonekawa F (1981) Comparative studies of gregariousness and social structure among seven feral Macaca fuscata groups. In: Chiarelli AB, Corruccine RS (eds) Primate behavior and sociobiology. Springer-Verlag, Berlin, pp 52–63

    Chapter  Google Scholar 

  • Kummer H, Goodall J (1985) Conditions of innovative behaviour in primates. Philos Trans R Soc Lond B 308:203–214

    Article  Google Scholar 

  • Majolo B, Lehmann J, de Bortoli VA, Schino G (2012) Fitness-related benefits of dominance in primates. Am J Phys Anthropol 147:652–660

    Article  CAS  Google Scholar 

  • Manson JH (1992) Measuring female mate choice in Cayo Santiago rhesus macaques. Anim Behav 44:405–416

    Article  Google Scholar 

  • Manson JH (1995) Do female Rhesus macaques choose novel males? Am J Primatol 37:285–296

    Article  Google Scholar 

  • McDonald DB, Shizuka D (2013) Comparative transitive and temporal orderliness in dominance networks. Behav Ecol. https://doi.org/10.1093/beheco/ars192:511-520

  • Millette JB, Sauther ML, Cuozzo FP (2009) Behavioral responses to tooth loss in wild ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Special Reserve, Madagascar. Am J Phys Anthropol 140:120–134

    Article  Google Scholar 

  • Nakamichi M, Shizawa Y (2003) Distribution of grooming among adult females in a large, free-ranging group of Japanese macaques. Int J Primatol 24(3):607–625

    Article  Google Scholar 

  • Nakamichi M, Yamada K (2010) Lifetime social development in females. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Primatology monographs. Springer, Tokyo, pp 241–270

    Google Scholar 

  • Nakamichi M, Fujii H, Koyama T (1983) Development of a congenitally malformed Japanese monkey in a free-ranging group during the first four years of life. Am J Primatol 5:205–210

    Article  Google Scholar 

  • Nakamichi M, Itoigawa N, Imakawa S, Machida S (1995a) Dominance relations among adult females in a free-ranging group of Japanese monkeys at Katsuyama. Am J Primatol 37:241–251

    Article  Google Scholar 

  • Nakamichi M, Kojima Y, Itoigawa N, Imakawa S, Machida S (1995b) Interactions among adult males and females before and after the death of the alpha male in a free-ranging troop of Japanese macaques. Primates 36(3):385–396

    Article  Google Scholar 

  • Nakamichi M, Nobuhara H, Nobuhara T, Nakahashi M, Nigi H (1997) Birth rate and mortality rate of infants with congenital limb malformations of the limbs in the Awajishima free-ranging group of Japanese monkeys (Macaca fuscata). Am J Primatol 42:225–234

    Article  CAS  Google Scholar 

  • Ostner J, Nunn CL, Schülke O (2008) Female reproductive synchrony predicts skewed paternity across primates. Behav Ecol 19:1150–1158

    Article  Google Scholar 

  • Parker GA (1974) Assessment strategy and the evolution of fighting behaviour. J Theor Biol 47:223–243

    Article  CAS  Google Scholar 

  • Reader SM, Laland KN (2001) Primate innovation: sex, age and social rank differences. Int J Primatol 22(5):787–805

    Article  Google Scholar 

  • Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308(29 April):648–652

    Article  CAS  Google Scholar 

  • Schaller G (1963) The year of the gorilla. Chicago University Press, Chicago

    Google Scholar 

  • Shizuka D, McDonald DB (2015) The network motif architecture of dominance hierarchies. J R Soc Interface 12:20150080

    Article  Google Scholar 

  • Sprague DS (1992) Life history and male intertroop mobility among Japanese macaques (Macaca fuscata). Int J Primatol 13(4):437–454

    Article  Google Scholar 

  • Sprague DS, Suzuki S, Takahashi H, Sato S (1998) Male life history in natural populations of Japanese macaques: migration, dominance rank, and troop participation of males in two habitats. Primates 39(3):351–363

    Article  Google Scholar 

  • Stokes EJ, Byrne RW (2001) Cognitive capacities for behavioural flexibility in wild chimpanzees (Pan troglodytes): the effect of snare injuries on complex manual food processing. Anim Cogn 4:11–28

    Article  Google Scholar 

  • Suzuki S, Hill DA, Sprague DS (1998) Intertroop transfer and dominance rank structure of nonnatal male Japanese macaques in Yakushima, Japan. Int J Primatol 19(4):703–722

    Article  Google Scholar 

  • Takahashi H (2002) Changes in dominance rank, age, and tenure of wild Japanese macaque males in Kinkazan A Troop during seven years. Primates 43(2):133–138

    Article  Google Scholar 

  • Takahata Y, Suzuki S, Agetsuma N, Okayasu N, Suguira H, Takahashi H, Yamagiwa J, Izawa K, Furuichi T, Hill D, Maruhashi T, Saito C, Sato S, Sprague DS (1998) Reproduction of wild Japanese macaque females of Yakushima and Kinkazan Islands: a preliminary report. Primates 39(3):339–349

    Article  Google Scholar 

  • Turner SE (2010) Consequences of congenital limb malformations and disability in adult female Japanese macaques (Macaca fuscata). Dissertation, University of Calgary, Calgary

    Google Scholar 

  • Turner SE, Gould L, Duffus DA (2005) Maternal behavior and infant congenital limb malformation in a free-ranging group of Macaca fuscata on Awaji Island, Japan. Int J Primatol 26(6):1435–1457

    Article  Google Scholar 

  • Turner SE, Fedigan LM, Nobuhara H, Nobuhara T, Matthews HD, Nakamichi M (2008) Monkeys with disabilities: prevalence and severity of congenital limb malformations in Macaca fuscata on Awaji Island. Primates 49(3):223–226

    Article  Google Scholar 

  • Turner SE, Fedigan LM, Matthews HD, Nakamichi M (2012) Disability, compensatory behavior, and innovation in free-ranging adult female Japanese macaques (Macaca fuscata). Am J Primatol 74:1–16. https://doi.org/10.1002/ajp.22029

    Article  Google Scholar 

  • Turner SE, Fedigan LM, Matthews HD, Nakamichi M (2014) Social consequences of disability in a nonhuman primate. J Hum Evol 68:47–57

    Article  Google Scholar 

  • Widdig A, Bercovitch FB, Streich WJ, Sauermann U, Nürnberg P, Krawczak M (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proc R Soc Lond B Biol Sci 271:819–829

    Article  Google Scholar 

  • Yoshihiro S, Goto S, Minezawa M, Muramatsu M, Saito Y, Sugita H, Nigi H (1979) Frequency of occurrence, morphology, and causes of congenital malformation of limbs in the Japanese monkey. Ecotoxicol Environ Saf 3:458–470

    Article  CAS  Google Scholar 

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Acknowledgements

SET would like to thank Linda M. Fedigan for her advising and mentorship over the years, the organizers of the Festschrift and editors of this book, the Nobuhara and Nakahashi family for permission to conduct research at the AMC and for sharing their time and knowledge and conducting peanut tests and K and K Okada and family for their kindness in Japan. SET gratefully acknowledges the funding provided by the Fonds de Récherche de Québec—Nature et Technologies (FRQNT postdoctoral fellowship), McGill University and PhD research funding from The Leakey Foundation, an Izaak Walton Killam Memorial Scholarship, the Animal Behavior Society, Province of Alberta Graduate Scholarships, the University of Calgary, the University of Calgary Dept. of Anthropology and NSERC (post-graduate scholarship B). SMR’s research is supported by McGill University, the Natural Sciences and Engineering Research Council of Canada (NSERC grants #418342-2012 and #429385-2012) and the Canada Foundation for Innovation (CFI grant #29433). Thanks to JF Addicott, LJN Brent, CJ Dey, KM Jack, HD Matthews, PO Montiglio, AR Reddon, NJ Turner and two anonymous reviewers for helpful comments on this project and earlier versions of the manuscript and for statistical and data management advice. Thanks for field assistance to Y Kamata, HD Matthews, KL Turner and NJ Turner. Thanks for the support of this project to K Yamada, K Onishi, Y Kaigaishi, K Valenta and the members of Simon Reader’s lab at McGill University especially M Cabrera, L Chouinard-Thuly, MF Guigueno, PO Montiglio, AR Reddon, PQ Sims and I Vassileva.

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Correspondence to Sarah E. Turner .

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Turner, S.E., Nakamichi, M., Nobuhara, T., Nobuhara, H., Reader, S.M. (2018). Disability and Dominance Rank in Adult Female and Male Japanese Macaques (Macaca fuscata). In: Kalbitzer, U., Jack, K. (eds) Primate Life Histories, Sex Roles, and Adaptability. Developments in Primatology: Progress and Prospects. Springer, Cham. https://doi.org/10.1007/978-3-319-98285-4_8

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