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Birth in Free-ranging Macaca fuscata

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Abstract

The birth process is an integral part of reproductive success in mammals, yet detailed, quantitative descriptions of parturition in nonhuman primates are still rare. Observations of free-ranging births can help to elucidate factors involved in this critical event, to contribute to our understanding of how maternal and infant behaviors during parturition affect infant survival and to explain the evolution of human birth. We provide data on the parturition behavior of 4 multiparous Japanese macaques: 2 daytime live births that we photographed and video recorded at the Awajishima Monkey Center (AMC), Awaji Island, Japan in 2006; a daytime live birth video recorded in 1993 at the AMC; and a nocturnal breech stillbirth of a captive Macaca fuscata, video recorded at the Kyoto Primate Research Institute in 2006. Certain behaviors were similar among the females, such as touching of the vulva followed by licking of fingers, squatting during contractions, and average contraction durations. Parturient females facilitated the birth manually by guiding the emerging infant. There were also dissimilarities in the duration of the labor and birth stages, condition of the infant at birth, and the mother’s behavior immediately postpartum. The mother’s postpartum behavior ranged from almost entirely infant-focused to predominantly related to the consumption of the placenta. The 3 free-ranging females all showed considerable social tolerance during labor and birth. We argue that social proximity at parturition is more common in nonhuman primates than previously emphasized, and has potential adaptive advantages.

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References

  • Abegglen, H. & Abegglen, J.-J. (1976). Field observation of a birth in Hamadryas baboons. Folia Primatologica (Basel), 26, 54–56.

    Article  CAS  Google Scholar 

  • Adachi, M. Saito, R. & Tanioka, Y. (1982). Observation of delivery in the rhesus monkey. Primates, 23, 583–586.

    Article  Google Scholar 

  • Bowden, D. Winter, P. & Ploog, D. (1967). Pregnancy and delivery behavior in the squirrel monkey (Saimiri sciureus) and other primates. Folia Primatologica (Basel), 5, 1–42.

    Article  CAS  Google Scholar 

  • Brandt, E. M. & Mitchell, G. (1971). Parturition in primates: Behavior related to birth. In L. A. Rosenblum (Ed.), Primate behavior: Developments in field and laboratory research (Vol. 2, pp. 177–223). New York: Academic Press.

    Google Scholar 

  • Brandt, E. M. & Mitchell, G. (1973). Labor and delivery behavior in rhesus monkeys (Macaca mulatta). American Journal of Physical Anthropology, 38, 519–522.

    Article  CAS  PubMed  Google Scholar 

  • Caine, N. & Mitchell, G. (1979). Behavior of primates present during parturition. In J. Erwin, T. L. Maple & G. Mitchell (Eds.), Captivity and behavior (pp. 112–124). New York: Van Nostrand Reinhold.

    Google Scholar 

  • Chinnock, M. & Robson, S. (2007). Obstetric trainees’ experience in vaginal breech delivery. Obstetrics and Gynecology, 110, 900–903.

    PubMed  Google Scholar 

  • Chivers, D. J. & Chivers, S. T. (1975). Events preceding and following the birth of a wild siamang. Primates, 16, 227–230.

    Article  Google Scholar 

  • Condit, V. K. & Smith, E. O. (1994). Yellow baboon labor and parturition at the Tana River National Primate Reserve, Kenya. American Journal of Primatology, 33, 51–55.

    Article  Google Scholar 

  • Coss, R. G. McCowan, B. & Ramakrishnan, U. (2007). Threat-related acoustical differences in alarm calls by wild bonnet macaques (Macaca radiata) elicited by python and leopard models. Ethology, 113, 352–367.

    Article  Google Scholar 

  • Dias, P. A. D. (2005). Observation of parturition in the Mexican mantled howler monkeys (Alouatta palliata) on the Island of Agaltepec, Veracruz State, Mexico. American Journal of Primatology, 65, 93–98.

    Article  Google Scholar 

  • Duboscq, J. Neumann, C. Perwitasari-Farajallah, D. & Engelhardt, A. (2008). Daytime birth of a baby crested black macaque (Macaca nigra) in the wild. Behavioral Processes, 79, 81–84.

    Article  Google Scholar 

  • Fairbanks, L. A. (1990). Reciprocal benefits of allomothering for female vervet monkeys. Animal Behavior, 40, 553–562.

    Article  Google Scholar 

  • Fraser, D. Phillips, P. A. & Thompson, B. K. (1997). Farrowing behaviour and stillbirth in two environments: an evaluation of the restraint-stillbirth hypothesis. Applied Animal Behaviour Science, 55, 51–66.

    Article  Google Scholar 

  • Goodall, J. & Athumani, J. (1980). An observed birth in a free-living chimpanzee (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. Primates, 21, 545–549.

    Article  Google Scholar 

  • Gorzitze, A. B. (1996). Birth-related behaviors in wild proboscis monkeys (Nasalis larvatus). Primates, 37, 75–78.

    Article  Google Scholar 

  • Gouzoules, H. T. (1974). Group responses to parturition in Macaca arctoides. Primates, 15, 287–292.

    Article  Google Scholar 

  • Hammerschmidt, K. & Ansorge, V. (1989). Birth of a Barbary macaque (Macaca sylvanus): acoustic and behavioural features. Folia Primatologica (Basel), 52, 78–87.

    Article  CAS  Google Scholar 

  • Hannah, M. E. Hannah, W. J. Hewson, S. A. Hodnett, E. D. Saigal, S. & Willan, A. R. (2000). Planned caesarean section versus planned vaginal birth for breech presentation at term: a randomized multicentre trial. Lancet, 356, 1375–1383.

    Article  CAS  PubMed  Google Scholar 

  • Hrdy, S. B. (2009). Mothers and others. The evolutionary origins of mutual understanding. Cambridge, Massachusetts: The Belknap Press of Harvard University Press.

    Google Scholar 

  • Itoigawa, N. & Tanaka, T. (1963). Parturition and neonate’s behavior in Japanese monkey (Macaca fuscata). The Annual of Animal Psychology (Dobutsu shinrigaku nenpo), 13, 71–81.

    Google Scholar 

  • Jolly, A. (1972). Hour of birth in primates and man. Folia Primatologica (Basel), 18, 108–121.

    Article  CAS  Google Scholar 

  • Kanazawa, T., & Nakamichi, M. (1991). Parturition behavior during the last 3 hours prior to delivery in captive Japanese macaques. In A. Ehara, T. Kimura, O. Takenaka & M. Iwamoto (Eds.), Primatology today: Proceedings of the XIIIth Congress of the International Primatological Society, Nagoya and Kyoto 18–24 July 1990 (pp. 423–426). Amsterdam: Elsevier.

  • Kemps, A. & Timmermans, P. (1982). Parturition behaviour in pluriparous Java-macaques. Primates, 23, 75–88.

    Article  Google Scholar 

  • Kinnaird, M. F. (1990). Pregnancy, gestation and parturition in free-ranging Tana River crested mangabeys (Cercocebus galeritus galeritus). American Journal of Primatology, 22, 285–289.

    Article  Google Scholar 

  • Kristal, M. B. (1991). Enhancement of opioid-mediated analgesia: a solution to the enigma of placentophagia. Neuroscience & Biobehavioral Reviews, 15, 425–435.

    Article  CAS  Google Scholar 

  • Kumar, A. Solanki, G. S. & Sharma, K. B. (2005). Observations on parturition and allomothering in wild capped langur (Trachypithecus pileatus). Primates, 46, 215–217.

    Article  PubMed  Google Scholar 

  • Malmkvist, J. Gade, M. & Damm, B. I. (2007). Parturient behaviour in farmed mink (Mustela vison) in relation to early kit mortality. Applied Animal Behaviour Science, 107, 120–132.

    Article  Google Scholar 

  • Moreno, L. Salas, I. C. & Glander, K. E. (1991). Breech delivery and birth-related behaviors in wild mantled howling monkeys. American Journal of Primatology, 23, 197–199.

    Article  Google Scholar 

  • Nakamichi, M. Imakawa, S. Kojima, Y. & Natsume, A. (1992). Parturition in a free-ranging Japanese monkey. Primates, 33, 413–418.

    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). American Journal of Primatology, 42, 225–234.

    Google Scholar 

  • Nakamichi, M. Yamada, K. Ohtsuka, N. Imakawa, S. Yasuda, J. & Shizawa, Y. (2004). Case reports on parturition and maternal behavior in a free-ranging group of Japanese monkeys at Katsuyama. Primate Research, 20, 31–43.

    Article  Google Scholar 

  • Nash, L. T. (1974). Parturition in a feral baboon (Papio anubis). Primates, 15, 279–285.

    Article  Google Scholar 

  • Negayama, K. Negayama, T. & Kondo, K. (1986). Behavior of Japanese monkey (Macaca fuscata) mothers and neonates at parturition. International Journal of Primatology, 7, 365–378.

    Article  Google Scholar 

  • Nigi, H. (1982). Nihonzaru no Seino Seiri (Reproductive physiology in Japanese monkeys). Tokyo: Doubutsu-sha.

    Google Scholar 

  • Nowak, R. Porter, R. H. Lévy, F. Orgeur, P. & Schaal, B. (2000). Role of mother-young interactions in the survival of offspring in domestic mammals. Reviews of Reproduction, 5, 153–163.

    Article  CAS  PubMed  Google Scholar 

  • Peker, S. Kowalewski, M. M. Pavé, R. E. & Zunino, G. E. (2009). Births in wild black and gold howler monkeys (Alouatta caraya) in northern Argentina. American Journal of Primatology, 71, 261–265.

    Article  PubMed  Google Scholar 

  • Price, E. C. (1990). Parturition and perinatal behaviour in captive cotton-top tamarins (Saguinus oedipus). Primates, 31, 523–535.

    Article  Google Scholar 

  • Pusey, A. Murray, C. Wallauer, W. Wilson, M. Wroblewski, E. & Goodall, J. (2008). Severe aggression among female Pan troglodytes schweinfurthii at Gombe National Park, Tanzania. International Journal of Primatology, 29, 949–973.

    Article  Google Scholar 

  • Ramakrishnan, U. & Coss, R. G. (2001). Strategies used by bonnet macaques (Macaca radiata) to reduce predation risk while sleeping. Primates, 42(3), 193–206.

    Article  Google Scholar 

  • Ratnayeke, A. P. & Dittus, W. P. J. (1989). Observation of a birth among wild Toque macaques (Macaca sinica). International Journal of Primatology, 10, 235–242.

    Article  Google Scholar 

  • Rawlins, R. G. (1979). Parturient and postpartum behavior of a free-ranging rhesus monkey (Macaca mulatta). Journal of Mammalogy, 60(2), 432–433.

    Article  Google Scholar 

  • Rosenberg, K. & Trevathan, W. (2002). Birth, obstetrics and human evolution. BJOG: An International Journal of Obstetrics and Gynaecology, 109, 1199–1206.

    Article  Google Scholar 

  • Rosenberg, K. R. (1992). The evolution of modern human childbirth. Yearbook of Physical Anthropology, 35, 89–124.

    Article  Google Scholar 

  • Sekulic, R. (1982). Birth in free-ranging howler monkeys Alouatta seniculus. Primates, 23, 580–582.

    Article  Google Scholar 

  • Stewart, K. J. (1984). Parturition in wild gorillas: behaviour of mothers, neonates, and others. Folia Primatologica (Basel), 42, 62–69.

    Article  Google Scholar 

  • Sunderland, N. Heffernan, S. Thomson, S. & Hennessy, A. (2008). Maternal parity affects neonatal survival rate in a colony of captive bred baboons (Papio hamadryas). Journal of Medical Primatology, 37, 223–228.

    Article  PubMed  Google Scholar 

  • Suzuki, M. T. Ono, T. Kohno, M. & Ogawa, H. (1990). Hour of delivery in cynomolgus monkeys under indoor individually-caged conditions. Primates, 31, 251–255.

    Article  Google Scholar 

  • Takahata, Y. Koyama, N. Miyamoto, N. & Okamoto, M. (2001). Daytime deliveries observed for the ring-tailed lemurs of the Berenty Reserve, Madagascar. Primates, 42, 267–271.

    Article  Google Scholar 

  • Timmermans, P. J. A. & Vossen, J. M. H. (1996). The influence of repeated motherhood on periparturitional behavior in cynomolgus macaques (Macaca fascicularis). International Journal of Primatology, 17, 277–296.

    Article  Google Scholar 

  • Trevathan, W. R. (1987). Human birth: An evolutionary perspective. New York: Aldine de Gruyter.

    Google Scholar 

  • Trevathan, W. R. (1988). Fetal emergence patterns in evolutionary perspective. AA, 90, 674–681.

    Google Scholar 

  • Tunde-Byass, M. O. & Hannah, M. E. (2003). Breech vaginal delivery at or near term. Seminars in Perinatology, 27, 34–45.

    Article  PubMed  Google Scholar 

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

  • Windfelder, T. L. (2000). Observations on the birth and subsequent care of twin offspring by a lone pair of wild emperor tamarins (Saguinus imperator). American Journal of Primatology, 52, 107–113.

    Article  CAS  PubMed  Google Scholar 

  • Wittman, A. B. & Wall, L. L. (2007). The evolutionary origins of obstructed labour: bipedalism, encephalization, and the human obstetric dilemma. Obstetrical & Gynecological Survey, 62, 739–748.

    Article  Google Scholar 

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Acknowledgments

S. E. Turner thanks the Nobuhara and Nakahashi families for their hospitality and permission to conduct research at the Awajishima Monkey Center and the following for providing funding: LSB Leakey Foundation, Animal Behavior Society, Izaak Walton Killam Memorial Scholarship, Province of Alberta Graduate Scholarship, Queen Elizabeth II Scholarships, University of Calgary, University of Calgary Department of Anthropology, and National Science and Engineering Research Council of Canada (Postgraduate Scholarship B). L. M. Fedigan’s research is supported by an NSERC Discovery Grant and the Canada Research Chair’s Program. K. Shimizu thanks Mr. Takumi Kunieda for his work on compiling the video footage of Mff1549’s parturition. Cake’s parturition was also documented by Mr. Tatsuya Okada of NTV; we thank him for access to his footage for comparison to our own. We thank C. Walsh, A. Jacob, M. Irwin, K. Tombak, the Chapman Lab discussion group at McGill University, and 1 anonymous reviewer for helpful comments on manuscript drafts; Dr. J. Ha for the customized behavioral data collection Palm program; and Ms. T. Nosal for assistance with Japanese translation. S. E. Turner thanks N. Turner, C. Holmes, and J. Glass for the privilege of witnessing natural human labor and birth and Prof. F. and Mrs. H Taniguchi, Mr. K. and Mrs. K. Okada and family, Dr. C. Chapman, Dr. M. Huffman, Dr. P. Asquith, and Ms. Y. Kamata for supporting the research.

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Authors and Affiliations

  1. Department of Anthropology, University of Calgary, Calgary, AB, Canada, T2N 1N4

    Sarah E. Turner & Linda M. Fedigan

  2. Laboratory of Ethological Studies, Faculty of Human Sciences, Osaka University, 1-2 Yamada-Oka, Suita, Osaka, 565-0871, Japan

    Masayuki Nakamichi

  3. Department of Geography, Planning and Environment, Concordia University, Montreal, Quebec, H3G 1M8, Canada

    H. Damon Matthews

  4. Department of Government, London School of Economics and Political Science, Houghton Street, London, WC2A 2AE, UK

    Katie McKenna

  5. Awajishima Monkey Center, Awaji Island, 289 Hatada, Sumoto, Hyogo, 656-2533, Japan

    Hisami Nobuhara & Toshikazu Nobuhara

  6. Department of Zoology, Okayama University of Science, 1-1 Ridaicho, Kitaku, Okayama, 700-0005, Japan

    Keiko Shimizu

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  1. Sarah E. Turner
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  2. Linda M. Fedigan
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  3. Masayuki Nakamichi
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Correspondence to Sarah E. Turner.

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Turner, S.E., Fedigan, L.M., Nakamichi, M. et al. Birth in Free-ranging Macaca fuscata . Int J Primatol 31, 15–37 (2010). https://doi.org/10.1007/s10764-009-9376-8

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