Skip to main content
Log in

Parturition and potential infanticide in free-ranging Alouatta guariba clamitans

  • News and Perspectives
  • Published:
Primates Aims and scope Submit manuscript

Abstract

Parturition is a key process of mammalian reproduction that is rarely documented in New World monkeys because it often occurs at night. However, diurnal births have been recorded in several species. In howler monkeys (Alouatta spp.) they have often been observed during prolonged resting periods. Similarly, infanticide is a behavior observed quite infrequently. Infanticide in howler monkeys is often inferred from infant deaths or disappearances after group takeovers by nonresident male(s). Here we report the first observation of parturition and birth-related behaviors in the brown howler monkey (Alouatta guariba clamitans) and the likely attack on the infant that caused its death. The mother was a multiparous female that lived in a ca. 3-ha Atlantic forest fragment in southern Brazil with nine group mates. The behavior (“all occurrences”) sampling method was used to record birth-related behaviors and social interactions. The parturition occurred during the day of 27 October 2013 during a feeding session. The female showed no sign of contraction or birth delivery posture. Parturition began apparently after matrix rupture and release of the amniotic fluid. Expulsion of the newborn occurred between 1 and 3 min later (the exact moment of delivery was not observed). Then, the female held and licked the newborn and began to ingest the placenta and the umbilical cord. The other group members continued feeding and had no interaction with the parturient during the preparturition and parturition events. The infant died ca. 35 days later as a consequence of injuries to his forehead and face, potentially caused by a conspecific bite. Because the adult and subadult males chased the female in the day that the infant’s wounds were detected, we believe that one of them might have been the aggressor. We discuss this putative case of infanticide in light of the potential motivation of each male.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Agoramoorthy G, Rudran R (1995) Infanticide by adult and subadult males in free-ranging red howler monkeys, Alouatta seniculus, in Venezuela. Ethology 99:75–88

    Article  Google Scholar 

  • Aguiar LM, Ludwing G, Hilst CLS, Malanski LS, Passos FC (2005) Tentativa de infanticídio por um macho dominante de Alouatta caraya (Humboldt) (Primates, Atelidae) em um infante extra-grupo devido a influência do observador. Rev Bras Zool 22:1201–1203

    Article  Google Scholar 

  • Beltrán ML, Stevenson PR (2012) Twins and infanticide in red howler monkeys inhabiting a fragment in western Orinoquia. Neotrop Primates 19:41–42

    Article  Google Scholar 

  • Bernis C, Varea C (2012) Hour of birth and birth assistance: from a primate to a medicalized pattern? Am J Hum Biol 24:14–21

    Article  PubMed  Google Scholar 

  • Bezerra EN, Porter LM (1999) Birth of Saguinus labiatus twins observed in their natural habitat. Neotrop Primates 7:27–28

    Google Scholar 

  • Bianchi RD, Mendes SL (2007) Ocelot (Leopardus pardalis) predation on primates in Caratinga Biological Station, southeast Brazil. Am J Primatol 69:1173–1178

    Article  Google Scholar 

  • Calegaro-Marques C, Bicca-Marques JC (1993) Allomaternal care in the black howler monkey (Alouatta caraya). Folia Primatol 61:104–109

    Article  CAS  PubMed  Google Scholar 

  • Camargo CC, Ferrari SF (2007) Observations of daytime births in two groups of red-handed howlers (Alouatta belzebul) on an island in the Tucuruí Reservoir in eastern Brazilian Amazonia. Am J Primatol 69:1075–1079

    Article  PubMed  Google Scholar 

  • Chism J, Olson DK, Rowell TE (1983) Diurnal births and perinatal behavior among wild patas monkeys: evidence of an adaptive pattern. Int J Primatol 4:167–184

    Article  Google Scholar 

  • Clarke MR (1983) Infant-killing and infant disappearance following male takeovers in a group of free-ranging howling monkeys (Alouatta palliata) in Costa Rica. Am J Primatol 5:241–247

    Article  Google Scholar 

  • Condit VK, Smith EO (1994) Yellow baboon labor and parturition at the Tana River National Primate Reserve, Kenya. Am J Primatol 33:51–55

    Article  Google Scholar 

  • Cristóbal-Azkarate J, Urbani B, Asensio N (2015) Interactions of howlers with other vertebrates: a review. In: Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology, and conservation. Springer, New York, pp 141–164

    Chapter  Google Scholar 

  • DeLuycker AM (2014) Observations of a daytime birthing event in wild titi monkeys (Callicebus oenanthe): implications of the male parental role. Primates 55:59–67

    Article  PubMed  Google Scholar 

  • Dias PAD (2005) Observation of parturition in the Mexican mantled howler monkeys (Alouatta palliata) on the island of Agaltepec, Veracruz State, Mexico. Am J Primatol 65:93–98

    Article  Google Scholar 

  • Ding W, Yang L, Xiao W (2013) Daytime birth and parturition assistant behavior in wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) Yunnan, China. Behav Process 94:5–8

    Article  Google Scholar 

  • Douglas PH (2014) Female sociality during the daytime birth of a wild bonobo at Luikotale, Democratic Republic of the Congo. Primates 55:533–542

    Article  PubMed  Google Scholar 

  • Duboscq J, Neumann C, Farajallahb DP, Engelhardt A (2008) Daytime birth of a baby crested black macaque (Macaca nigra) in the wild. Behav Process 79:81–84

    Article  Google Scholar 

  • Galetti M (1994) Infanticide in the brown howler monkey, Alouatta fusca. Neotrop Primates 2:6–7

    Google Scholar 

  • Garber PA (1987) Foraging strategies among living primates. Ann Rev Anthropol 16:339–364

    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 

  • Honnebier MBOM, Nathanielsz PW (1994) Primate parturition and the role of the maternal circadian system. Eur J Obstet Gynecol Reprod Biol 55:193–203

    Article  CAS  PubMed  Google Scholar 

  • Jolly A (1972) Hour of birth in primates and man. Folia Primatol 18:108–121

    Article  CAS  PubMed  Google Scholar 

  • Kristal MB (1980) Placentophagia: a biobehavioral enigma (or De gustibus non disputandum est). Neurosci Biobehav Rev 4:141–150

    Article  CAS  PubMed  Google Scholar 

  • Kristal MB, Dipirro JM, Thompson AC (2012) Placentophagia in humans and nonhuman mammals: causes and consequences. Ecol Food Nutr 51:177–197

    Article  PubMed  Google Scholar 

  • Martin P, Bateson P (2007) Measuring behavior: an introductory guide. Cambridge University Press, Cambridge

    Google Scholar 

  • Miranda JMD, Bernardi IP, Abreu KC, Passos FC (2005) Predation on Alouatta guariba clamitans Cabrera (Primates, Atelidae) by Leopardus pardalis (Linnaeus) (Carnivora, Felidae). Rev Bras Zool 22:793–795

    Article  Google Scholar 

  • Moreno LI, Salas IC, Glander KE (1991) Breech delivery and birth-related behaviors in wild mantled howling monkeys. Am J Primatol 23:197–199

    Article  Google Scholar 

  • Nisbett RA, Glander KE (1996) Quantitative description of parturition in a wild mantled howling monkey: a case study of prenatal behaviors associated with a primiparous delivery. Brenesia 45–46:157–168

    Google Scholar 

  • Pan W, Gu T, Pan Y, Feng C, Long Y, Zhao Y, Meng H, Liang Z, Yao M (2014) Birth intervention and non-maternal infant-handling during parturition in a nonhuman primate. Primates 55:483–488

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Rimbach R, Pardo-Martinez A, Montes-Rojas A, Di Fiore A, Link A (2012) Interspecific infanticide and infant-directed aggression by spider monkeys (Ateles hybridus) in a fragmented forest in Colombia. Am J Primatol 74:990–997

    Article  PubMed Central  PubMed  Google Scholar 

  • Ruiz WIT, Diaz DMV, Amasifuen CF, Heymann EW (2004) Diurnal birth of a wild red titi monkey, Callicebus cupreus, at the Estación Biológica Quebrada Blanco. Neotrop Primates 12:15–16

    Google Scholar 

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

    Article  Google Scholar 

  • Sussman RW, Cheverud JM, Bartlett TQ (1995) Infant killing as an evolutionary strategy: reality or myth? Evol Anthropol 3:311–314

    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 

  • Turner SE, Fedigan LM, Nakamichi M, Matthews HD, McKenna K, Nobuhara H, Nobuhara T, Shimizu K (2010) Birth in free-ranging Macaca fuscata. Int J Primatol 31:15–37

    Article  Google Scholar 

  • Van Belle S, Bicca-Marques JC (2015) Insights into reproductive strategies and sexual selection in howler monkeys. In: Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology, and conservation. Springer, New York, pp 57–84

    Chapter  Google Scholar 

  • Van Belle S, Kulp AE, Thiessen-Bock R, Garcia M, Estrada A (2010) Observed infanticide following a male immigration event in black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. Primates 51:279–284

    Article  PubMed  Google Scholar 

  • van Schaik CP (2000) Infanticide by male primates: the sexual selection hypothesis revisited. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 27–60

    Chapter  Google Scholar 

  • Windfelder TL (2000) Observations on the birth and subsequent care of twin offspring by a lone pair of wild emperor tamarins (Saguinus imperator). Am J Primatol 52:107–113

    Article  CAS  PubMed  Google Scholar 

  • Yao M, Yin L, Zhang L, Liu L, Qin D, Pan W (2012) Parturitions in wild white-headed langurs (Trachypithecus leucocephalus) in the Nongguan Hills, China. Int J Primatol 33:888–904

    Article  Google Scholar 

  • Zunino GE, Chalukian SC, Rumiz DI (1985) Infanticidio y desaparición de infantes asociados al reemplazo de macho en grupos de Alouatta caraya. In: Mello MT (ed) A primatologia no Brasil, vol 2. Sociedade Brasileira de Primatologia, Brasília, pp 185–190

    Google Scholar 

Download references

Acknowledgments

We thank E.G. Fernandes, E.F. Vianna, D. Camaratta, and E. Chassot for their hospitality, collaboration, and logistical support during fieldwork. We also thank F. Sehn, H.M. Prates, S.F. Castro, M. Fiedler, P.D.S. Santos, and P.B.E. Silva for field assistance. We thank the Brazilian Higher Education Authority (CAPES) for supporting V.M. (PhD fellowship, #11189/13-4) and O.M.C. (PNPD postdoctoral fellowship, #2755/2010), the Irmão José Otão Foundation/PUCRS for supporting M.B.N. (undergraduate fellowship), and the Brazilian National Research Council (CNPq) for supporting J.C.B.-M. (research fellowships, #303154/2009-8 and 303306/2013-0).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Júlio César Bicca-Marques.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (WMV 189350 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martins, V., Chaves, Ó.M., Neves, M.B. et al. Parturition and potential infanticide in free-ranging Alouatta guariba clamitans . Primates 56, 119–125 (2015). https://doi.org/10.1007/s10329-015-0461-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-015-0461-7

Keywords

Navigation