Abstract
Allomaternal care is widely observed among primate species. Although diverse allomothering behavioral repertoire and types of caretakers have been reported, it remains unclear what social or physiological conditions may trigger such care in each individual. For a better understanding of mechanisms that give rise to allomaternal care in primates, more observational reports are needed with information on social or physiological conditions of caretakers. Here I report two cases of intensive allomaternal care in two different populations of Japanese macaques (Macaca fuscata). The two adult females provided intensive allomaternal care including carrying, grooming, and nursing towards others’ infants. Their allomaternal care began 20 or 29 days prior to their own partum and lasted for 84 days at the most. This study firstly showed that nursing forms part of the allomothering behavioral repertoire, and allomaternal caretakers can be individuals that are prior to the time of their own partum in Japanese macaques. Their intensive allomaternal care may stem from their good nutritional conditions, increased concentrations of several hormones, or disappearance of the newborn infants’ biological mothers.
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References
Anestis SF (2010) Hormones and social behavior in primates. Evol Anthropol 19:66–78
Bercovitch FB, Widdig A, Berard JD, Nuernberg P, Kessler MJ, Schmidtke J, Trefilov A, Krawczak M (2002) Multiple sirehood in free-ranging twin rhesus macaques (Macaca mulatta). Am J Primatol 57:31–34
Berman CM (1982) The ontogeny of social relationships with group companions among free-ranging infant rhesus monkeys I. Social networks and differentiation. Anim Behav 30:149–162
Chapman CA, Chapman LJ (1986) Development of howling monkey twins (Alouatta palliata) in Santa Rosa National Park, Costa Rica. Primates 27:377–381
Cozzolino R, Cordischi C, Aureli F, Scucchi S (1992) Environmental temperature and reproductive seasonality in Japanese macaques (Macaca fuscata). Primates 33:329–336
Ellsworth JA, Andersen C (1997) Adoption by captive parturient Rhesus macaques: Biological vs. adopted infants and the cost of being a ‘‘twin’’ and rearing ‘‘twins’’. Am J Primatol 43:259–264
Fairbanks LA (1990) Reciprocal benefits of allomothering for female vervet monkeys. Anim Behav 40:553–562
Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge
Gould L (2000) Adoption of a wild orphaned ringtailed lemur infant by natal group members: adaptive explanations. Primates 41:413–419
Hasegawa T, Hiraiwa M (1980) Social interactions of orphans observed in a free-ranging troop of Japanese macaques. Folia Primatol 33:129–158
Hein PR, Schatorje J, Frencken H, Segers MFG, Thomas CMG (1991) The effect of chronic oral methadone treatment on monkey chorionic gonadotropin, estradiol, dehydroepiandrosterone sulfate, progesterone, prolactin and cortisol levels during pregnancy in the cynomoigus monkey (Macaca fascicularis). Eur J Obstet Gynecol Reprod Biol 38:145–150
Hiraiwa M (1981) Maternal and alloparental care in a troop of free- ranging Japanese monkeys. Primates 22:309–329
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
Ishizuka S, Takemoto H, Sakamaki T, Tokuyama N, Toda K, Hashimoto C, Furuichi T (2020) Comparisons of between-group differentiation in male kinship between bonobos and chimpanzees. Sci Rep 10:251
Kawamura S (1958) The matriarchal social order in the Minoo-B group—a study on the rank system of Japanese macaques. Primates 1:149–156
Kumar A, Solanki GS (2014) Role of mother and allomothers in infant independence in capped langur Trachypithecus pileatus. J Bombay Nat Hist Soc 111:3–9
Kurita H, Sugiyama Y, Ohsawa H, Hamada Y, Watanabe T (2008) Changes in demographic parameters of Macaca fuscata at Takasakiyama in relation to decrease of provisioned foods. Int J Primatol 29:1189–1202
Leca JB, Gunst N, Huffman MA (2007) Japanese macaque cultures: inter- and intra-troop behavioural variability of stone handling patterns across 10 troops. Behaviour 144:251–281
Link A, Palma AC, Velez A, de Luna AG (2006) Costs of twins in free-ranging white-bellied spider monkeys (Ateles belzebuth belzebuth) at Tinigua National Park, Colombia. Primates 47:131–139
Matsumoto-Oda A (1995) First record of a twin birth in chimpanzees of the Mahale Mountains National Mark, Tanzania. Afr Study Monogr 16:159–164
Muroyama Y (1994) Exchange of grooming with allomothering in female patas monkeys. Behaviour 128:103–119
Nakagawa N, Matsubara M, Shimooka Y et al (2015) Embracing in a wild group of Yakushima macaques (Macaca fuscata yakui) as an example of social customs. Curr Anthropol 56:104–120
Nakamichi M (1983) Development of infant twin Japanese monkeys (Macaca fuscata) in a free-ranging group. Primates 24:576–583
Nakamichi M, Onishi K, Yamada K (2010) Old grandmothers provide essential care to their young granddaughters in a free-ranging group of Japanese monkeys (Macaca fuscata). Primates 51:171–174
Nakamura M, Hosaka K (2015) Orphans and allomothering. In: Nakamura M, Hosaka K, Itoh N, Zamma K (eds) Mahale chimpanzees: 50 years of research. Cambridge University Press, Cambridge, pp 421–432
Nigi H (1975) Menstrual cycle and some other aspects of Japanese monkeys (Macaca fuscata). Primates 16:207–216
Nishida T (1983) Alloparental behaviour in wild chimpanzees of the Mahale Mountains, Tanzania. Folia Primatol 41:1–33
Nozaki M (2009) Grandmothers care for orphans in provisioned troop of Japanese macaques (Macaca fuscata). Primates 50:85–88
Ogawa H (1998) Adoption and social interactions between a mother and ‘twin’ offspring in Macaca fuscata. Folia Primatol 69:100–105
Pavé R, Kowalewski MM, Zunino GE (2010) Adoption of an orphan infant in wild black and gold howler monkeys (Alouatta caraya). Mastozool Neotrop 17:171–174
Pereira ME, Izard MK (1989) Lactation and care for unrelated infants in forest-living ringtailed lemurs. Am J Primatol 18:101–108
Ren B, Li D, Garber PA, Li M (2012) Evidence of allomaternal nursing across one-male units in the Yunnan snub-nosed monkey (Rhinopithecus bieti). PLoS ONE 7:e30041
Saito C, Sato S, Suzuki S, Sugiura H, Agetsuma N, Takahata Y, Sasaki C, Takahashi H, Tanaka T, Yamagiwa J (1998) Aggressive intergroup encounters in two populations of Japanese macaques (Macaca fuscata). Primates 39:303–312
Schino G, Troisi A (2005) Neonatal abandonment in Japanese macaques. Am J Phys Anthropol 126:447–452
Schino G, Aureli F, D’Amato FR, D’Antoni M, Pandolfi N, Troisi A (1993) Infant kidnapping and co-mothering in Japanese macaques. Am J Primatol 30:257–262
Shimizu K, Lohstroh PN, Laughlin LS, Gee NA, Todd H, Shideler SE, Lasley BL (2001) Noninstrumented enzyme-linked immunosorbant assay for detection of early pregnancy in macaques. Am J Primatol 54:57–62
Sugiyama Y, Kurita H, Matsui T, Shimomura T (2011) Twinning frequency of Japanese macaques (Macaca fuscata) at Takasakiyama. Primates 52:19–23
Taberlet P (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189–3194
Toyoda A, Malaivijitnond S (2018) The first record of dizygotic twins in semi-wild stump-tailed macaques (Macaca arctoides) tested using microsatellite markers and the occurrence of supernumerary nipples. Mamm Study 43:207–212
Xia D, Li J, Matheson MD, Sun L, Sun B, Zhu Y (2012) First occurrence of twins in provisioned free-ranging Tibetan macaques (Macaca thibetana) at Huangshan, China. Primates 53:1–5
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
Zhang P, Watanabe K (2007) Extra-large clusters and social structure in Japanese macaques (Macaca fuscata) from Shodoshima Island, Central Japan. Am J Primatol 69:1119–1130
Acknowledgements
I thank Mr. A. Nishio, Ms. C. Saeki, Mr. M. Ishii, Ms. Y. Kaji, Mr. K. Hida, Ms. K. Miyashita, and Ms. K. Kuno for support in Choshikei Monkey Park on Shodoshima Island, and stuff of Takasakiyama National Zoo, especially Dr. H. Kurita and Mr. T. Shimomura, for support in the park, and Dr. K. Watanabe, Dr. T. Furuichi, Dr. Y. Tsuji for support with my field researches. I also thank the anonymous reviewers and the editor for their reviews and helpful comments on my manuscript. This study was financially supported by the Leading Graduate Program in Primatology and Wildlife Science of Kyoto University.
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This study was supported by the Leading Graduate Program in Primatology and Wildlife Science of Kyoto University.
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SI designed this study, collected behavioral and genetic data, wrote and revised the manuscript. The author gave final approval for publication.
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This study was conformed to the Guidelines for Field Research established by the Ethics Committee of the Primate Research Institute, Kyoto University. The study was approved by Choshikei Monkey Park, and Takasakiyama National Zoo.
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Ishizuka, S. Fake twins? Two cases of intensive allomaternal care by female Japanese macaques before and after their own partum. Primates 61, 351–355 (2020). https://doi.org/10.1007/s10329-020-00812-7
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DOI: https://doi.org/10.1007/s10329-020-00812-7