Male affiliation bias towards orphans in Japanese macaques (Macaca fuscata) on Shodoshima Island
In: BehaviourDepartment of Biology, Faculty of Science, Toho University, 2-2-1 Miyama, Funabashi, Chiba, 274-8510, Japan
Japan Society for Promotion of Science, Kojimachi Business Center Building, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo, 102-0083, Japan
Search for other papers by Shintaro Ishizuka in
Current site
Google Scholar
Search for other papers by Eiji Inoue in
Current site
Google Scholar
Abstract
Male animals show affiliative behaviours towards immatures. Although male affiliation is often directed to their genetic offspring under paternity certainty, it is not always the case in promiscuous species living in multimale–multifemale groups. Male affiliations to immatures can be also influenced by the mother of the immature. However, it remains unclear whether the presence of the immature’s mother living in a group influences the patterns of male affiliations, probably because quantitative assessments of male affiliations towards orphans using a large sample size have been typically difficult. This study investigated male affiliations to juveniles in a promiscuous primate, Japanese macaques Macaca fuscata, on Shodoshima Island. We tested whether paternity and the presence/absence of the juvenile’s mother living in a group influence the probability of male affiliations to the juvenile. Additionally, we investigated the effects of affiliative relationships between male and the juvenile’s mother and dominance rank of the mother on the probability of male affiliations. The effect of paternity on the probability of male affiliations was not significant, suggesting that paternal care was generally absent due to the paternity uncertainty. Males showed affiliations to orphans more likely than to offspring of non-friend females, who formed weak affiliative relationships with the male. Orphans often encounter high mortality rates and may compensate for the loss of their mothers by receiving male affiliations. Males showed affiliations to offspring of friend females more likely than to offspring of non-friend females. For males, affiliations to juveniles may lead to future copulation opportunities with their mothers. Males showed low affiliations to offspring of high-ranking females probably because the offspring of high-ranking mothers receive aggressions from conspecifics less frequently and may not seek for male affiliations. This study provides important data for a better understanding of the factors that facilitate male affiliations in promiscuous species.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
-
Aere, S., Pedruzzi, L., Facondini, G., Böye, M., Palagi, E. & Lemasson, A. (2025). The curious case of rhesus macaques: despotism does not prevent third-party postconflict affiliation. — Anim. Behav. 219: 123022.
-
Alexander, B.K. (1970). Parental behavior of adult male Japanese monkeys. — Behaviour 36: 270-285.
-
Altmann, J. (1974). Observational study of behavior: sampling methods. — Behaviour 49: 227-265.
-
Andres, D., Clutton-Brock, T.H., Kruuk, L.E., Pemberton, J.M., Stopher, K.V. & Ruckstuhl, K.E. (2013). Sex differences in the consequences of maternal loss in a long-lived mammal, the red deer (Cervus elaphus). — Behav. Ecol. Sociobiol. 67: 1249-1258.
-
Baayen, R.H. (2008). Analyzing linguistic data: a practical introduction to statistics using R. — Cambridge University Press, New York, NY.
-
Berman, C.M. (1982). The social development of an orphaned rhesus infant on Cayo Santiago: Male care, foster mother–orphan interaction and peer interaction. — Am. J. Primatol. 3: 131-141.
-
Bhattacharjee, D., Cousin, E., Pflüger, L.S. & Massen, J.J. (2023). Prosociality in a despotic society. — iScience 26: 106587.
-
Boesch, C., Bole, C., Eckhardt, N. & Boesch, H. (2010). Altruism in forest chimpanzees: the case of adoption. — PLoS ONE 5: e8901.
-
Brooks, M.E., Kristensen, K., van Benthem, K.J., Magnusson, A., Berg, C.W., Nielsen, A., Skaug, H.J., Mächler, M. & Bolker, B.M. (2017). Modeling zero-inflated count data with glmmTMB. — BioRxiv: 132753.
-
Buchan, J.C., Alberts, S.C., Silk, J.B. & Altmann, J. (2003). True paternal care in multi-male primate society. — Nature 425: 179-181.
-
Burt, D.B., Coulter, P.F. & Ligon, D. (2007). Evolution of parental care and cooperative breeding. — In: Reproductive biology and phylogeny of birds, Part B: sexual selection, behavior, conservation, embryology and genetics (Jamieson, B.G.M., ed.). Science Publishers, Enfield, p. 295-326.
-
Chaffin, C.L., Friedlen, K. & de Waal, F.B.M. (1995). Dominance style of Japanese macaques compared with rhesus and stumptail macaques. — Am. J. Primatol. 35: 103-116.
-
Clutton-Brock, T.H. (1991). The evolution of parental care. — Princeton University Press, Princeton, NJ.
-
De Vries, H., Stevens, J.M. & Vervaecke, H. (2006). Measuring and testing the steepness of dominance hierarchies. — Anim. Behav. 71: 585-592.
-
Dinno, A. (2024). dunn. test. R package version 1.3.6. R Foundation for Statistical Computing, Vienna.
-
Dobson, A. (2002). An introduction to generalized linear models. — Chapman & Hall/CRC, London.
-
Eaton, G.G., Johnson, D.F., Glick, B.B. & Worlein, J.M. (1986). Japanese macaques (Macaca fuscata) social development: Sex differences in juvenile behavior. — Primates 27: 141-150.
-
Fooden, J. & Aimi, M. (2003). Birth-season variation in Japanese macaques, Macaca fuscata. — Primates 44: 109-117.
-
Gartland, K.N., Brand, C.M., Ulibarri, L.R. & White, F.J. (2020). Variation in adult male–juvenile affiliative behavior in Japanese macaques (Macaca fuscata). — Folia Primatol. 91: 610-621.
-
Gartland, K.N., Biggs, N., Shreeve, C.M. & White, F.J. (2021). Dominance rank, female choice, and reproductive success in semi-free ranging adult male Japanese macaques (Macaca fuscata). — Am. J. Primatol. 83: e23294.
-
Goldenberg, S.Z. & Wittemyer, G. (2017). Orphaned female elephant social bonds reflect lack of access to mature adults. — Sci. Rep. 7: 14408.
-
Gouzoules, H. (1984). Social relations of males and infants in a troop of Japanese monkeys: a consideration of causal mechanisms. — In: Primate paternalism (Taub, D.H., ed.). Van Nostrand Reinhold, New York, NY, p. 127-145.
-
Gubernick, D.J. & Teferi, T. (2000). Adaptive significance of male parental care in a monogamous mammal. — Proc. Roy. Soc. Lond. Ser. B: Biol. Sci. 267: 147-150.
-
Hamilton III, W.J., Busse, C. & Smith, K.S. (1982). Adoption of infant orphan chacma baboons. — Anim. Behav. 30: 29-34.
-
Hasegawa, T. & Hiraiwa, M. (1980). Social interactions of orphans observed in a free-ranging troop of Japanese monkeys. — Folia Primatol. 33: 129-158.
-
Hayakawa, S. (2008). Male–female mating tactics and paternity of wild Japanese macaques (Macaca fuscata yakui). — Am. J. Primatol. 70: 986-989.
-
Huffman, M.A. (1987). Consort intrusion and female mate choice in Japanese macaques (Macaca fuscata). — Ethology 75: 221-234.
-
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.
-
Inoue, M., Takenaka, A., Tanaka, S., Kominami, R. & Takenaka, O. (1990). Paternity discrimination in a Japanese macaque group by DNA fingerprinting. — Primates 31: 563-570.
-
Inoue, M., Mitsunaga, F., Nozaki, M., Ohsawa, H., Takenaka, A., Sugiyama, Y., Shimizu, K. & Takenaka, O. (1993). Male dominance rank and reproductive success in an enclosed group of Japanese macaques: with special reference to post-conception mating. — Primates 34: 503-511.
-
Ishizuka, S. & Inoue, E. (2023). Sex-specific effects of juvenile offspring on their mothers’ social relationships with other females in Japanese macaques (Macaca fuscata) on Shodoshima Island. — Int. J. Primatol. 44: 500-516.
-
Ishizuka, S., Inoue, E. & Kaji, Y. (2024). Paternity success for resident and non-resident males and their influences on paternal sibling cohorts in Japanese macaques (Macaca fuscata) on Shodoshima Island. — PLoS ONE 19: e0309056.
-
Itani, J. (1959). Paternal care in the wild Japanese monkey, Macaca fuscata fuscata. — Primates 2: 61-93.
-
Kawai, M. (1958). On the rank system in a natural group of Japanese monkeys, I: The basic and the dependent rank. — Primates 1: 111-130. (in Japanese with English abstract).
-
Kawai, M., Azuma, S. & Yoshiba, K. (1967). Ecological studies of reproduction in Japanese monkeys (Macaca fuscata). — Primates 8: 35-73.
-
Kawamura, S. (1958). The matriarchal social order in the Minoo-B group: a study on the rank system of Japanese macaque. — Primates 1: 149-156. (in Japanese with English abstract).
-
Kerhoas, D., Kulik, L., Perwitasari-Farajallah, D., Agil, M., Engelhardt, A. & Widdig, A. (2016). Mother–male bond, but not paternity, influences male–infant affiliation in wild crested macaques. — Behav. Ecol. Sociobiol. 70: 1117-1130.
-
Kuběnová, B., Ostner, J., Schülke, O., Majolo, B., Šmilauer, P., Waterman, J., Tkaczynski, P. & Konečná, M. (2019). The male and female perspective in the link between male infant care and mating behaviour in Barbary macaques. — Ethology 125: 914-924.
-
Kulik, L., Amici, F., Langos, D. & Widdig, A. (2015). Sex differences in the development of social relationships in rhesus macaques (Macaca mulatta). — Int. J. Primatol. 36: 353-376.
-
Lahdenperä, M., Mar, K.U. & Lummaa, V. (2016). Short-term and delayed effects of mother death on calf mortality in Asian elephants. — Behav. Ecol. 27: 166-174.
-
Langergraber, K.E., Mitani, J.C., Watts, D.P. & Vigilant, L. (2013). Male–female socio-spatial relationships and reproduction in wild chimpanzees. — Behav. Ecol. Sociobiol. 67: 861-873.
-
Langos, D., Kulik, L., Mundry, R. & Widdig, A. (2013). The impact of paternity on male–infant association in a primate with low paternity certainty. — Mol. Ecol. 22: 3638-3651.
-
Lemasson, A., Palombit, R.A. & Jubin, R. (2008). Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments. — Behav. Ecol. Sociobiol. 62: 1027-1035.
-
Lukas, D. & Clutton-Brock, T.H. (2013). The evolution of social monogamy in mammals. — Science 341: 526-530.
-
Matsubara, M. (2003). Costs of mate guarding and opportunistic mating among wild male Japanese macaques. — Int. J. Primatol. 24: 1057-1075.
-
Matsumura, S. (1999). The evolution of “egalitarian” and “despotic” social systems among macaques. — Primates 40: 23-31.
-
Ménard, N., Segesser, F., Scheffrahn, W., Pastorini, J., Vallet, D., Gaci, B., Martin, R.D. & Gautier-Hion, A. (2001). Is male–infant caretaking related to paternity and/or mating activities in wild Barbary macaques (Macaca sylvanus)? — C.R. Acad. Sci. 324: 601-610.
-
Minge, C., Berghänel, A., Schülke, O. & Ostner, J. (2016). Patterns and consequences of male–infant relationships in wild Assamese macaques (Macaca assamensis). — Int. J. Primatol. 37: 350-370.
-
Møller, A.P. & Birkhead, T.R. (1993). Certainty of paternity covaries with paternal care in birds. — Behav. Ecol. Sociobiol. 33: 261-268.
-
Morrison, R.E., Eckardt, W., Colchero, F., Vecellio, V. & Stoinski, T.S. (2021). Social groups buffer maternal loss in mountain gorillas. — ELife 10: e62939.
-
Moscovice, L.R., Heesen, M., Di Fiore, A., Seyfarth, R.M. & Cheney, D.L. (2009). Paternity alone does not predict long-term investment in juveniles by male baboons. — Behav. Ecol. Sociobiol. 63: 1471-1482.
-
Moscovice, L.R., Di Fiore, A., Crockford, C., Kitchen, D.M., Wittig, R., Seyfarth, R.M. & Cheney, D.L. (2010). Hedging their bets? Male and female chacma baboons form friendships based on likelihood of paternity. — Anim. Behav. 79: 1007-1015.
-
Murray, C.M., Stanton, M.A., Lonsdorf, E.V., Wroblewski, E.E. & Pusey, A.E. (2016). Chimpanzee fathers bias their behaviour towards their offspring. — Roy. Soc. Open Sci. 3: 160441.
-
Nakamichi, M. (1989). Sex differences in social development during the first 4 years in a free-ranging group of Japanese monkeys, Macaca fuscata. — Anim. Behav. 38: 737-748.
-
Nakamichi, M. & Yamada, K. (2010). Lifetime social development in female Japanese macaques. — In: The Japanese macaques (Nakagawa, N., Nakamichi, M. & Sugiura, H., eds). Springer, Tokyo, p. 241-270.
-
Nakamichi, M., Ueno, M. & Yamada, K. (2021). Male care in a free-ranging group of Japanese macaques (Macaca fuscata). — Primates 62: 971-980.
-
Nguyen, N., Van Horn, R.C., Alberts, S.C. & Altmann, J. (2009). “Friendships” between new mothers and adult males: adaptive benefits and determinants in wild baboons (Papio cynocephalus). — Behav. Ecol. Sociobiol. 63: 1331-1344.
-
Nunn, C.L. (1999). The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. — Anim. Behav. 58: 229-246.
-
Ostner, J., Vigilant, L., Bhangavatula, J., Franz, M. & Schülke, O. (2013). Stable heterosexual bonds in a promiscuous primate. — Anim. Behav. 86: 623-631.
-
Palombit, R.A., Seyfarth, R.M. & Cheney, D.L. (1997). The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. — Anim. Behav. 54: 599-614.
-
Rosenbaum, S. & Silk, J.B. (2022). Pathways to paternal care in primates. — Evol. Anthropol. 31: 245-262.
-
Rosenbaum, S., Hirwa, J.P., Silk, J.B., Vigilant, L. & Stoinski, T.S. (2015). Male rank, not paternity, predicts male–immature relationships in mountain gorillas, Gorilla beringei beringei. — Anim. Behav. 104: 13-24.
-
Ruiz-Lambides, A.V., Weiß, B.M., Kulik, L., Stephens, C., Mundry, R. & Widdig, A. (2017). Long-term analysis on the variance of extra-group paternities in rhesus macaques. — Behav. Ecol. Sociobiol. 71: 1-11.
-
Seyfarth, R.M. (1978). Social relationships among adult male and female baboons. II. Behaviour throughout the female reproductive cycle. — Behaviour 64: 227-247.
-
Silk, J., Cheney, D. & Seyfarth, R. (2013). A practical guide to the study of social relationships. — Evol. Anthropol. 22: 213-225.
-
Smuts, B.B. & Gubernick, D.J. (1992). Male–infant relationships in nonhuman primates: paternal investment or mating effort? — In: Father–child relations. Cultural and biosocial context (Hewlett, B.S., ed.). Aldine de Gruyter, New York, NY, p. 1-30.
-
Smuts, B.B. (2017). Sex and friendship in baboons. — Routledge, New York, NY.
-
Soltis, J., Thomsen, R. & Takenaka, O. (2001). The interaction of male and female reproductive strategies and paternity in wild Japanese macaques, Macaca fuscata. — Anim. Behav. 62: 485-494.
-
Takahata, Y. (1982). Social relations between adult males and females of Japanese monkeys in the Arasiyama B troop. — Primates 23: 1-23.
-
Takahata, Y., Huffman, M.A., Suzuki, S., Koyama, N. & Yamagiwa, J. (1999). Why dominants do not consistently attain high mating and reproductive success: a review of longitudinal Japanese macaque studies. — Primates 40: 143-158.
-
Thierry, B. (2007). Unity in diversity: lessons from macaque societies. — Evol. Anthropol. 16: 224-238.
-
Ueno, M., Yamada, K. & Nakamichi, M. (2015). Emotional states after grooming interactions in Japanese macaques (Macaca fuscata). — J. Comp. Psychol. 129: 394-401.
-
Van Horn, R.C., Wahaj, S.A. & Holekamp, K.E. (2004). Role-reversed nepotism among cubs and sires in the spotted hyena (Crocuta crocuta). — Ethology 110: 413-426.
-
Villavicencio, C.P., Marquez, I.N., Quispe, R. & Vasquez, R.A. (2009). Familiarity and phenotypic similarity influence kin discrimination in the social rodent Octodon degus. — Anim. Behav. 78: 77-384.
-
Watts, H.E. & Holekamp, K.E. (2009). Ecological determinants of survival and reproduction in the spotted hyena. — J. Mammal. 90: 461-471.
-
West, H.E.R. & Capellini, I. (2016). Male care and life history traits in mammals. — Nature Commun. 7: 11854.
-
Widdig, A. (2007). Paternal kin discrimination: the evidence and likely mechanisms. — Biol. Rev. 82: 319-334.
-
Wittig, R.M., Crockford, C., Lehmann, J., Whitten, P.L., Seyfarth, R.M. & Cheney, D.L. (2008). Focused grooming networks and stress alleviation in wild female baboons. — Horm. Behav. 54: 170-177.
-
Xia, X. (1992). Uncertainty of paternity can select against paternal care. — Am. Nat. 139: 1126-1129.
-
Yamada, K., Nakamichi, M., Shizawa, Y., Yasuda, J., Imakawa, S., Hinobayashi, T. & Minami, T. (2005). Grooming relationships of adolescent orphans in a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama: a comparison among orphans with sisters, orphans without sisters, and females with a surviving mother. — Primates 46: 145-150.
-
Yamagiwa, J. & Hill, D.A. (1998). Intraspecific variation in the social organization of Japanese macaques: past and present scope of field studies in natural habitats. — Primates 39: 257-273.
-
Zipple, M.N., Altmann, J., Campos, F.A., Cords, M., Fedigan, L.M., Lawler, R.R., Lonsdorf, E.V., Perry, S., Pusey, A.E., Stoinski, T.S., Strier, K.B. & Alberts, S.C. (2021). Maternal death and offspring fitness in multiple wild primates. — Proc. Natl. Acad. Sci. USA. 118: e2015317118.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 437 | 177 | 25 |
| Full Text Views | 29 | 12 | 0 |
| PDF Views & Downloads | 65 | 27 | 0 |
Male affiliation bias towards orphans in Japanese macaques (Macaca fuscata) on Shodoshima Island
In: BehaviourDepartment of Biology, Faculty of Science, Toho University, 2-2-1 Miyama, Funabashi, Chiba, 274-8510, Japan
Japan Society for Promotion of Science, Kojimachi Business Center Building, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo, 102-0083, Japan
Search for other papers by Shintaro Ishizuka in
Current site
Google Scholar
PubMed
Search for other papers by Eiji Inoue in
Current site
Google Scholar
PubMed
Abstract
Male animals show affiliative behaviours towards immatures. Although male affiliation is often directed to their genetic offspring under paternity certainty, it is not always the case in promiscuous species living in multimale–multifemale groups. Male affiliations to immatures can be also influenced by the mother of the immature. However, it remains unclear whether the presence of the immature’s mother living in a group influences the patterns of male affiliations, probably because quantitative assessments of male affiliations towards orphans using a large sample size have been typically difficult. This study investigated male affiliations to juveniles in a promiscuous primate, Japanese macaques Macaca fuscata, on Shodoshima Island. We tested whether paternity and the presence/absence of the juvenile’s mother living in a group influence the probability of male affiliations to the juvenile. Additionally, we investigated the effects of affiliative relationships between male and the juvenile’s mother and dominance rank of the mother on the probability of male affiliations. The effect of paternity on the probability of male affiliations was not significant, suggesting that paternal care was generally absent due to the paternity uncertainty. Males showed affiliations to orphans more likely than to offspring of non-friend females, who formed weak affiliative relationships with the male. Orphans often encounter high mortality rates and may compensate for the loss of their mothers by receiving male affiliations. Males showed affiliations to offspring of friend females more likely than to offspring of non-friend females. For males, affiliations to juveniles may lead to future copulation opportunities with their mothers. Males showed low affiliations to offspring of high-ranking females probably because the offspring of high-ranking mothers receive aggressions from conspecifics less frequently and may not seek for male affiliations. This study provides important data for a better understanding of the factors that facilitate male affiliations in promiscuous species.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 437 | 177 | 25 |
| Full Text Views | 29 | 12 | 0 |
| PDF Views & Downloads | 65 | 27 | 0 |
