Abstract
Direct intervention in infant delivery by non-parturient individuals is a rare phenomenon in nonhuman primates. In contrast, birth assistance by other individuals, or the practice of midwifery, is universal among human societies and generally believed to be a behavior unique to our species. It has been proposed that the enlarged head of the human fetus and the relatively narrow birth canal constrained by bipedalism has made human parturition more difficult than in nonhuman primates, and these anatomic challenges have led to the rotation of the fetus in the birth canal and an occiput anterior (i.e., backward-facing) orientation of emergence. These characteristics have hindered the mother’s ability to self-assist the delivery of the infant, therefore necessitating assistance by other individuals or midwives for successful birth. Here we report the first high-definition video recordings of birth intervention behavior in a wild nonhuman primate, the white-headed langur (Trachypithecus leucocephalus). We observed that while a primiparous female gave birth to an infant in an occiput posterior (i.e., forward-facing) orientation, a multiparous female intervened in the delivery by manually pulling the infant out of the birth canal and cared for it in the following hours. Our finding shows extensive social interactions throughout parturition, and presents an unequivocal case of non-maternal intervention with infant birth in a nonhuman primate.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abegglen H, Abegglen J-J (1976) Field observation of a birth in hamadryas baboons. Folia Primatol 26:54–56
Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge
Borries C, Lu A, Ossi-Lupo K, Larney E, Koenig A (2011) Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques. Am J Phys Anthropol 144:286–299
Brain C (1992) Deaths in a desert baboon troop. Int J Primatol 13:593–599
Cowlishaw G (1999) Ecological and social determinants of spacing behaviour in desert baboon groups. Behav Ecol Sociobiol 45:67–77
Ding W, Yang L, Xiao W (2013) Daytime birth and parturition assistant behaviour in wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) Yunnan, China. Behav Process 94:5–8
Hirata S, Fuwa K, Sugama K, Kusunoki K, Takeshita H (2011) Mechanism of birth in chimpanzees: humans are not unique among primates. Biol Lett 7:686–688
Hrdy S (1978a) Allomaternal care and abuse of infants among Hanuman langurs. In: Chivers DJ, Herbert WJ (eds) Recent advances in primatology. Academic Press, London, pp 169–172
Hrdy S (1978b) Intergroup infant kidnapping in Hanuman langur. Folia Primatol 34:259–277
Hrdy S (2009) Mothers and others. Harvard University Press, Cambridge, pp 73–79
Itani J (1959) Paternal care in the wild Japanese monkey, Macaca fuscata. Primates 2:61–93
Jin T, Wang DZ, Zhao Q, Yin LJ, Qin DG et al (2009a) Reproductive parameters of wild Trachypithecus leucocephalus: seasonality, infant mortality and interbirth interval. Am J Primatol 71:558–566
Jin T, Wang DZ, Zhao Q, Yin LJ, Qin DG et al (2009b) Social organization of white-headed langurs (Trachypithecus leucocephalus) in the Nongguan Karst Hills, Guangxi, China. Am J Primatol 71:206–213
Jin T, Wang D, Pan W, Yao M (2014) Non-maternal infant handling in wild white-headed langurs (Trachypithecus leucocephalus). Int J Primatol (under review)
Jolly A (1972) Hour of birth in primates and man. Folia Primatol 18:108–121
Koyama N, Nakamichi M, Oda R, Miyamoto N, Takahata Y (2001) A ten-year summary of reproductive parameters for ring-tailed lemurs at Berenty, Madagascar. Primates 42:1–14
Kumar A, Solanki GS, Sharma BK (2005) Observations on parturition and allomothering in wild capped langur (Trachypithecus pileatus). Primates 46:215–217
Maestripieri D (1993) Infant kidnapping among group-living rhesus macaques: why donʼt mothers rescue their infants? Primates 34:211–216
Maestripieri D (1994) Social structure, infant handling, and mothering styles in group-living old world monkeys. Int J Primatol 15:531–553
Maestripieri D, Schino G, Aureli F, Troisi A (1992) A modest proposal: displacement activities as an indicator of emotions in primates. Anim Behav 44:967–979
McKenna JJ (1979) The evolution of allomothering behavior among colobine monkeys: function and opportunism in evolution. Am Anthropol 81:818–840
Peker S, Kowalewski MM, Pavé RE, Zunino GE (2009) Births in wild black and gold howler monkeys (Alouatta caraya) in northern Argentina. Am J Primatol 71:261–265
Poindron P, Lévy F, Keller M (2007) Maternal responsiveness and maternal selectivity in domestic sheep and goats: the two facets of maternal attachment. Dev Psychobiol 49:54–70
Rosenberg KR (1992) The evolution of modern human childbirth. Am J Phys Anthropol 35:89–124
Rosenberg KR, Trevathan WR (2002) Birth, obstetrics and human evolution. Br J Obstet Gynaecol 109:1199–1206
Saltzman W, Maestripieri D (2011) The neuroendocrinology of primate maternal behavior. Prog Neuropsychopharmacol Biol Psychiatry 35:1192–1204
Shopland JM, Altmann J (1987) Fatal intragroup kidnapping in yellow baboons. Am J Primatol 13:61–65
Silk JB (1980) Kidnapping and female competition among captive bonnet macaques. Primates 21:100–110
Stoller MK (1995) The obstetric pelvis and mechanism of labor in nonhuman primates (Ph.D. thesis) University of Chicago, Chicago
Trevathan WR (1988) Fetal emergence patterns in evolutionary perspective. Am Anthropol 90:674–681
Trevathan WR (2011) Human birth: an evolutionary perspective. Aldine Transaction, Chicago
Troisi A (2002) Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. Stress 5:47–54
Turner SE, Fedigan LM, Nakamichi M, Matthews HD, McKenna K et al (2010) Birth in free-ranging Macaca fuscata. Int J Primatol 31:15–37
Yao M, Yin L, Zhang L, Liu L, Qin D et al (2012) Parturitions in wild white-headed langurs (Trachypithecus leucocephalus) in the Nongguan Hills, China. Int J Primatol 33:888–904
Yin L, Jin T, Watanabe K, Qin D, Wang D et al (2013) Male attacks on infants and infant mortality during male takeovers in wild white-headed langurs (Trachypithecus leucocephalus). Integr Zool 8:365–377
Zhao Q, Borries C, Pan WS (2011) Male takeover, infanticide, and female countertactics in white-headed leaf monkeys (Trachypithecus leucocephalus). Behav Ecol Sociobiol 65:1535–1547
Acknowledgments
We are grateful to Xiangdong Zhang, Chao Zhang, Wenkui You, Xinyang Li, Meiying Huang, Yanping Yang, Meijiao Wei, Jiajia Tan, and Jintong Lu for their assistance with video recordings and field observations. We thank Dr. Sarah Hrdy and two anonymous reviewers for their valuable comments on the early versions of the manuscript. The project was supported by Natural Science Foundation of China (Grant No. 31272329) to M. Yao and the research grants of Peking University to W. Pan and M. Yao. W. Pan designed and carried out the long-term study. T. Gu, Y. Pan, C. Feng, Y. Long, Y. Zhao, H. Meng and Z. Liang conducted video recordings and helped with individual identification. M. Yao analyzed data and wrote the paper. This study complied with protocols approved by the Guangxi Forestry Administration of China and adhered to the legal requirements of China.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Pan, W., Gu, T., Pan, Y. et al. Birth intervention and non-maternal infant-handling during parturition in a nonhuman primate. Primates 55, 483–488 (2014). https://doi.org/10.1007/s10329-014-0427-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-014-0427-1