Skip to main content
SpringerLink
Log in

Catarrhine juvenile mortality in captivity, under seminatural conditions, and in the wild

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Juvenile mortality is an important problem in the development of captive populations. I compiled data from published literature on abortion, premature mortality, stillbirth, and death of unweaned young. Cumulative mortality incidences (CMI) during the first month in captive populations (CP) of Cercopithecoidea range between 13 and 51%, and CMI in the first year between 28 and 56%. Mortality rate during the first year ranges between <4 and 48% in free- ranging populations (FRP) and between 10 and 60% in wild populations (WP). Much of the juvenile mortality in CP appears to occur in the first month, whereas in FRP and WP mortality is more scattered throughout the juvenile period. High mortality rates occur in both CP and WP of nonhuman Hominoidea. Mortality rate during the first month in CP is between 12 and 36% for the Hylobatidae and between 18 and 31% for the Pongidae. If the entire juvenile period is considered, gorilla CP and WP have comparable CMI, while CMI is higher in WP than CP for chimpanzees. Most of the juvenile mortality in CP of chimpanzees occurs before the age of 1 year. Trauma, including infanticide and maternal inadequacy, seems to be a more important factor in infant mortality of Cercopithecoidea than infectious disease is. Relatively frequent reports of congenital, hereditary, and/or genetically determined malformations in the Cercopithecoidea may be related to the long use of animals in this group for laboratory purposes. Infectious disease is the most important cause of nonhuman hominoid juvenile mortality, followed by trauma and maternal disorders, particularly related aberrant maternal behavior. Cercopithecoid juvenile mortality risk factors most frequently mentioned in the literature are sex of the infant and rank of the mother: dominant females produce more female offspring, and juvenile males suffer higher mortality than females do. The female skewed sex ratio at birth in gorillas and chimpanzees could be explained by the local resource competition theory. Higher male mortality rates occur in nonhuman Hominoidea, except in two Hylobatesspp. and Pan paniscus,which have higher female mortality. Parity and rearing history of the mother are very important risk factors in nonhuman hominoid infant mortality.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adang, O. M. J., Wensing, J. A. B., and van Hooff, J. A. R. A. M. (1987). The Arnhem zoo colony of chimpanzees.Int. Zoo Yb. 27: 236–248.

    Google Scholar 

  • Adler, H. J. (1990). Mehrfacher Infantizid in einer Pavian Gruppe(Papio hamadryas) im zoologischen Garten Leipzig.Proc. Int. Symp. Erkrank. Zoo Wildtiere 32: 43–45.

    Google Scholar 

  • Agoramoorthy, G., Mohnot, S. M., Sommer, V., and Srivastava, A. (1988). Abortions in free-ranging hanuman langurs(Presbytis entellus)-A male induced strategy?Hum. Evol. 3(4): 297–308.

    Article  Google Scholar 

  • Altmann, J. (1980). Demography: Births, deaths and interbirth intervals. In Altmann, J. (ed.),Baboon Mothers and Infants, Harvard University Press, Cambridge, MA, pp. 32–41.

    Google Scholar 

  • Altmann, J., Altmann, S. A., and Hausfater, G. (1978). Primate infant's effect on mother's future reproduction.Science 201: 1028–2029.

    Article  PubMed  CAS  Google Scholar 

  • Anderson, M. P., Oosterhuis, J., Kennedy, S., and Benirschke, K. (1986). Pneumonia and meningoencephalitis due to Amoeba in a lowland gorilla.J Zoo Anim. Med. 17: 87–91.

    Google Scholar 

  • Andrews, E. A. (1974). Pulmonary pathology in stillborn non-human primates.J. Am. Vet. Med. Assoc. 164: 715–718.

    PubMed  CAS  Google Scholar 

  • Angst, W. (1978). Breeding statistics ofMacaca fascicularis. In Chivers (ed.),Recent Advances in Primatology, Vol. II, pp. 270–272.

  • Angst, W., and Thommen, D. (1977). New data and a discussion of infant killing in Old World monkeys and apes.Folia Primatol. 27: 198–229.

    PubMed  CAS  Google Scholar 

  • Barkley, E. H., Kenny, D., Lowenstine, L. J., and Foster, J. W. (1991). Mountain gorillas and measles: Ontogeny of a wildlife vaccination program.Proc. Annu. Meet. Am. Assoc. Zoo Vet. 1991, pp. 198–205.

  • Baumgartner, R., Ruber, A., Wunderlin, E., Dangel, P. H., and Giedion, A. (1990). Kasuistische Zusammenstellung von Erkrankungen bei Jungtieren der Flachlandgorilla.Proc. Int. Symp. Erkrank Zoo Wildtiere 32: 15–18.

    Google Scholar 

  • Beck, B. B., and Power, M. L. (1988). Correlates of sexual and maternal competence in captive gorillas.Zoo Biol. 7: 339–350.

    Article  Google Scholar 

  • Benirschke, K. (1983). Chorioamnionitis as cause of abortion in orang-utan(Pongo pygmaeus obeli).J. Zoo Anim. Med. 14: 56–60.

    Google Scholar 

  • Benirschke, K., Adams, F. D., Black, K. L., and Gluck, L. (1980a). Perinatal mortality in zoo animals. In Montali, R., and Migaki, G. (eds.),Comparative Pathology of Zoo Animals, Smithsonian Institution, Washington, DC, pp. 471–481.

    Google Scholar 

  • Benirschke, K, Bogart, M. H., and Adams, F. (1980b). The status of the pygmee chimpanzee(Pan paniscus) in the USA.Int. Zoo Yb. 20: 71–76.

    Google Scholar 

  • Berman, C. M. (1988). Maternal condition and offspring sex ratio in a group of free-ranging rhesus monkeys: An eleven-year study.Am. Nat. 131: 307–328.

    Article  Google Scholar 

  • Bourne, G. H. (1972). Breeding chimpanzees and other apes. In Beveridge, W. I. B. (ed.),Breeding Primates, Karger, Basel, pp. 24–33.

    Google Scholar 

  • Brack, M., and Gatesman, T. J. (1989). Bilateral posterior parietal atrophy in an infant rhesus monkey(Macaca mulatto).J. Med. Primatol. 18: 43–54.

    PubMed  CAS  Google Scholar 

  • Brady, A. G. (1983). Knotted umbilical cord as a cause of death in aCercopithecus aethiops fetus.Lab. Anim. Sci. 33(4): 375–376.

    PubMed  CAS  Google Scholar 

  • Bryce, R. (1991). The epidemiology of preterm birth. In Kiely, M. K. (ed.),Reproductive and Perinatal Epidemiology, CRC Press, Boston, pp. 438–443.

    Google Scholar 

  • Burton, F. D., and Sawchuk, L. A. (1974). Demography ofMacaca sylvanus of Gibraltar.Primates 15(2-3): 271–278.

    Article  Google Scholar 

  • Busse, C. (1982). Social dominance and offspring mortality among female chacma baboons.Int. J. Primatol. 3: 267.

    Article  Google Scholar 

  • Caljan, V. G., Meisvili, N. V., and Vancatova, M. A. (1987). Infanticide and primate evolution. In Leonovicova, V., and Novak, V. J. A. (eds.),Behaviour as One of the Main Factors of Evolution, Praha, pp. 321–330.

  • Calle, P. P. (1985). Abruptio placentae in a lion-tailed macaque.J. Am. Vet. Med. Assoc. 187(11): 1275–1276.

    PubMed  CAS  Google Scholar 

  • Cheney, D. L., Lee, P. C., and Seyfarth, R. M. (1981). Behavioural correlates of non-random mortality among free-ranging female vervet monkeys.Behav. Ecol. Sociobiol. 9: 153–162.

    Article  Google Scholar 

  • Christie, R. J. (1969). An occurrence of monozygotic twinning and anencephaly inMacaca arctoides.Lab. Anim. Care 19(4): 531–532.

    PubMed  CAS  Google Scholar 

  • Clarke, M. R., and Baskin, G. B. (1987). Patterns of infant mortality in a rhesus monkey(Macaca mulatto) breeding colony.Am. J. Primatol. 12: 336.

    Google Scholar 

  • Corner, G. W., and Bartelmez, G. W. (1954). Early abnormal embryos of the rhesus monkey.Contrib. Embryol. 35: 1.

    Google Scholar 

  • Courtenay, J. (1988). Infant mortality in mother-reared captive chimpanzees at Taronga Zoo, Sydney.Zoo Biol. 7: 61–68.

    Article  Google Scholar 

  • Courtenay, J., and Santow, G. (1989). Mortality of wild and captive chimpanzees.Folia Primatol. 52: 167–177.

    PubMed  CAS  Google Scholar 

  • Cousins, D. (1974). A review of some complaints suffered by captive gorillas with notes on some causes of death in wild gorillas(Gorilla gorilla).Zool. Garten 44(4): 201–210.

    Google Scholar 

  • Cuspinera, A. J. (1982). Primaten—Zootiere von besonderen Rang.Zool. Garten 5/6: 351–356.

    Google Scholar 

  • Dazey, J., and Erwin, J. (1976). Infant mortality inMacaca nemestrina: Neonatal and post-neonatal mortality at the Regional Primate Center Field station, University of Washington, 1967–1974.Theriogenology 5(2): 267–277.

    Google Scholar 

  • Debyser, I. W. J. (1995). Prosimian juvenile mortality in zoos and primate centers.Int. J. Primatol. 16: 113–131.

    Google Scholar 

  • Debyser, I., and Zwart, P. (1991). Hydranencephaly in a hamadryas baboon(Papio hamadryas).Proc. Int. Symp. Erkrank Zoo Wildtiere 33: 325–331.

    Google Scholar 

  • Debyser, I., and Zwart, P. (1992). Syncytial giant cell hepatitis in a juvenile chimpanzee(Pan troglodytes).Proc. Int. Symp. Erkrank. Zoo Wildtiere 34: 287–289.

    Google Scholar 

  • Debyser, I. W. J., Soma, H., and Zwart, P. (1993). Partial hydatiform mole in a pregnant chimpanzee(Pan troglodytes).Zoo Biol. 12: 299–305.

    Article  Google Scholar 

  • Deputte, B. L. (1991). Reproductive parameters of captive grey-cheeked mangabeys(Cercocebus albigeinea).Folia Primatol. 57: 57–69.

    PubMed  CAS  Google Scholar 

  • Dittus, W. P. J. (1977). The social regulation of population density and age and sex distributions in the toque monkey(Macaca sinica).Behaviour 63: 281–322.

    Google Scholar 

  • Dittus, W. P. J. (1981). Primate population analysis. InTechniques for the Study of Primate Population Ecology, Subcommittee on Conservation of Natural Population, National Academy Press, Washington, DC, pp. 135–175.

    Google Scholar 

  • Drickamer, L. C. (1974). A ten-year summary of reproductive data for free-rangingMacaca mulatto.Folia Primatol. 21: 61–80.

    PubMed  CAS  Google Scholar 

  • Dunbar, R. I. M. (1982). Demographic and life history variables of a population of gelada baboons(Theropithecus gelada).J. Anim. Ecol. 49: 485–506.

    Google Scholar 

  • Dunbar, R. I. M., and Dunbar, E. P. (1974). Ecology and population dynamics ofColobus guereza in Ethiopia.Folia Primatol. 21: 188–208.

    PubMed  CAS  Google Scholar 

  • Dunbar, R. I. M., and Dunbar, E. P. (1977). Dominance and reproductive success among female gelada baboons.Nature 266: 351–353.

    Article  PubMed  CAS  Google Scholar 

  • Elze, K., Kronberger, H., and Seifert, S. (1969). Gestose mit tödichem Ausgang bei einem Orang-utan.Proc. Int. Symp. Erkrank. Zoo Wildtiere 11: 113–117.

    Google Scholar 

  • Enurah, L. U., Uche, E. M. I., and Nawathe, D. R. (1988). Fatal shigellosis in a chimpanzee(Pan troglodytes) in the Jos Zoo, Nigeria.J. Wildlife Dis. 24(1): 178–179.

    CAS  Google Scholar 

  • Erwin, J. (1977). Infant mortality inMacaca fascicularis: Neonatal and post-neonatal mortality at the Regional Primate Research Center field station, University of Washington, 1967–1976.Theriogenology (6): 357–367.

  • Fa, J. E. (ed.) (1977).Use of Time and Resources by Provisioned Troops of Monkeys: Social Behaviour, Time and Energy in the Barbary Macaque (Macaca Sylvanus) at Gibraltar, Karger, Basel, pp. 191–192.

    Google Scholar 

  • Fairbanks, L. A., and McGuire, M. T. (1984). Determinants of fecundity and reproductive success in captive vervet monkeys.Am. J. Primatol. 7: 27–38.

    Article  Google Scholar 

  • Fedigan, L. M., Fedigan, L., Chapman, C., and McGuire, M. T. (1984). A demographic model of colonization by a population of St. Kitts vervets.Folia Primatol. 42: 194–202.

    Google Scholar 

  • Fedigan, L. M., Fedigan, L., Gouzoules, S., Gouzoules, H., and Koyama, N. (1986). Life time reproductive success in female Japanese macaques.Folia Primatol. 47: 143–157.

    PubMed  CAS  Google Scholar 

  • Fossey, D. (1982). Reproduction among free-living mountain gorillas.Am. J. Primatol. 1:97–104.

    Article  Google Scholar 

  • Foster, J. W. (1992). Mountain gorilla conservation: a study in human values.J. Am. Vet. Med. Assoc. 200(5): 629–633.

    PubMed  CAS  Google Scholar 

  • Fritz, J., and Fritz, P. (1982). Great ape hand rearing with a goal of normalcy and a reproductive continuum.Proc. Am. Assoc. Zoo Vet, pp. 27–31.

  • Fukuda, F. (1988). Influence of artificial food supply on population parameters and dispersal in the Hakone T troop of Japanese macaques.Primates 29(4): 477–492.

    Article  Google Scholar 

  • Furuya, Y. (1966). On the malformation that occurred in the Gagyusan troop of wild Japanese monkeys.Primates 7(4): 488–492.

    Article  Google Scholar 

  • Gaertner, D. J., Lytton, B., and Morgenstern, S. (1991). Perineal urinary bladder diverticulum resulting in partial urinary obstruction in a rhesus monkey.J. Am. Vet. Med. Assoc. 199(12): 1772–1774.

    PubMed  CAS  Google Scholar 

  • Galat, G., and Galat-Luong, A. G. (1977). Demographie et regime alimentaire d'une troupe deCercopithecus aethiops sabaeus.Terre Vie 31: 557–577.

    Google Scholar 

  • Galdikas, B. M. F. (1981). Orang-utan reproduction in the wild. In Graham, C. E. (ed.),Reproductive Biology of the Great Apes, Academic Press, New York, pp. 281–300.

    Google Scholar 

  • Gardin, J. F., Jerome, C. P., Jayo, M. J., and Weaver, D. S. (1989). Maternal factors affecting reproduction in a breeding colony of cynomolgus macaques(Macaca fascicularis).Lab. Anim. Sci. 39(3): 205–212.

    PubMed  CAS  Google Scholar 

  • Göltenboth, R., and Klös, H. G. (1977). Übersicht uber die Todesursachen und das Krankheitsgeschehen im Primatenbestand des zoologischen Gartens Berlin von 1957-1976.Proc. Int. Symp. Erkrank. Zoo Wildtiere 19: 273–279.

    Google Scholar 

  • Goodall, J. (1983). Population dynamics during a 15-year period in one community of free-living chimpanzees in the Gombe National Park, Tanzania. Z.Tierpsychol. 61: 1–60.

    Google Scholar 

  • Goosen, C, Schrams, A., Brinkhof, H., Schonk, J., and van Hoek, L. A. (1983). Housing conditions and breeding success of chimpanzees at the Primate Center TNO.Zoo Biol. 2: 295–302.

    Article  Google Scholar 

  • Gouzoules, H., Gouzoules, S., and Fedigan, L. (1982). Behavioural dominance and reproductive success in female Japanese monkeys(Macaca fuscata).Anim. Behav. 30: 1138–1150.

    Article  Google Scholar 

  • Grassé, P. P. (1955).Traité de Zoologie. Anatomie, Systématique, Biologie des mammifères, Masson et Cie, Paris, Tome XVII, Fase. II, pp. 1854–2206.

    Google Scholar 

  • Gust, D. A., Busse, C. D., and Gordon, T. P. (1990). Reproductive performance in the Sooty Mangabey(Cercocebus torquatus atys).Am. J. Primatol. 22: 241–250.

    Article  Google Scholar 

  • Hamai, M., Nishida, T., Takasaki, H., and Turner, L. A. (1992). New records of within-group infanticide and cannibalism in wild chimpanzees.Primates 33(2): 151–162.

    Article  Google Scholar 

  • Hamilton, W. J., Busse, G., and Smith, K. S. (1982). Adoption of infant orphan chacma baboons.Anim. Behav. 30: 29–34.

    Article  Google Scholar 

  • Hänichen, T., Wiesner, H., and Rietschel, W. (1983). Beitrag zur physiologischen und pathologischen Gravidität und perinatale Probleme beim Orang-utan(Pongo pygmaeus).Proc. Int. Symp. Erkrank. Zoo Wildtiere 25: 357–362.

    Google Scholar 

  • Harcourt, A. H. (1987). Dominance and fertility among female primates.J. Zool. 213: 471–487.

    Google Scholar 

  • Harcourt, A. H., Fossey, D., and Sabater-Pi, J. (1981). Demography ofGorilla gorilla.J. Zool. 195: 215–233.

    Article  Google Scholar 

  • Harley, D. (1988). Patterns of reproduction and mortality in two captive colonies of Hanuman langur monkeys(Presbytis entellus).Am. J. Primatol. 15: 103–114.

    Article  Google Scholar 

  • Harlow, H. F. (1964).Early Social Deprivation and Later Social Behavior in the Monkey, Williams and Wilkens, Baltimore, pp. 154–173.

    Google Scholar 

  • Harvey, P. H., and Clutton-Brock, T. H. (1985). Life history variation in primates.Evolution 39(3): 559–581.

    Article  Google Scholar 

  • Hauser, M. D. (1988). Variation in maternal responsiveness in free-ranging vervet monkeys: A response to infant mortality risk?Am. Nat. 131: 537–587.

    Article  Google Scholar 

  • Heldstab, A., and Thommen, D. R. (1984). Neonatale Mortalität bei Javaneraffen(Macaca irus) im zoologischen Garten Basel.Int. Symp. Erkrank. Zoo Wildtiere 26: 103–110.

    Google Scholar 

  • Heldstab, A., Rüeldi, D., Sonnabend, W., and Deinhardt, F. (1981). Spontaneous generalizedHerpesvirus hominis infection of a lowland gorilla(Gorilla gorilla gorilla).J. Med. Primatol. 10: 129–135.

    PubMed  CAS  Google Scholar 

  • Hiraiwa, M. (1981). Maternal and alloparental care in a troop of free-ranging Japanese monkeys.Primates 22(3): 309–329.

    Article  Google Scholar 

  • Hiraiwa-Hasegawa, M., Hasegawa, T., and Nishida, T. (1984). Demographic study of a large-sized unit group of chimpanzees in the Mahale mountains, Tanzania: A preliminary report.Primates 25(4): 401–413.

    Article  Google Scholar 

  • Hird, D. W., Hendrickson, R. V., and Hendrickx, A. G. (1975). Infant mortality inMacaca mulatto: Neonatal and post-neonatal mortality at the California Primate Research Center, 1968-1972.J. Med. Primatol. 4: 8–22.

    Google Scholar 

  • Hochbaum, M., Wilson, J. G., and Gavan, J. A. (1975). Bericht uber die Aufzucht eines durch Zange entbundenen Orang-utans.Pongo pygmaeus. Zool. Garten 45(4/6): 427–435.

    Google Scholar 

  • Hoopes, P. J., McKay, D. W., Daisley, G. W., Kennedy, S., and Bush, M. (1978). Suppurative arthritis in an infant orangutan.J. Am. Vet. Med. Assoc. 173(9): 1145–1147.

    PubMed  CAS  Google Scholar 

  • Horrocks, J. A. (1986). Life-history characteristics of a wild population of vervets(Cercopithecus aethiops sabaeus) in Barbados, West Indies.Int. J. Primatol. 7: 31–47.

    Google Scholar 

  • Hrdy, S. B., and Hrdy, D. B. (1976). Hierarchical relations among female Hanuman langurs (Primates, Colobinae,Presbytis entellus).Science 193: 913–915.

    Article  PubMed  CAS  Google Scholar 

  • Ikeda, H. (1982). Population changes and ranging behaviour of wild Japanese monkeys at Mt. Kawaradake in Kyushu, Japan,Primates 23: 338–347.

    Article  Google Scholar 

  • Itoigawa, N., Tanaka, T., Ukai, N., Fujii, H., Kurokawa, T., Koyama, A., Watanabe, A. A., and Imakawa, S. (1992). Demography and reproductive parameters of a free-ranging group of Japanese macaques(Macaca fuscata) at Katsuyama.Primates 33(1): 49–68.

    Article  Google Scholar 

  • Johnson, L. D., Petto, A. J., Boy, D. S., Sehgal, P. K., and Beland, M. E. (1986). The effect of perinatal and juvenile mortality in colony-born production at the New England Regional Primate Center. In Benirschke, K. (ed.),Primates, the Road to Self-Sustaining Populations, Springer Verlag, New York, pp. 771–779.

    Google Scholar 

  • Jolly, A. (1973). Primate birth hour.Int. Zoo Yb. 13: 391–397.

    Google Scholar 

  • Joy, J. E. (1971). Pregnancy toxaemia in a multiparous chimpanzee at Dallas zoo.Int. Zoo Yb. 11: 239–241.

    Google Scholar 

  • Kalter, S. S. (1989). Infectious diseases of noń-human primates in a zoo setting.Zoo Biol. Suppl. 1: 61–76.

    Google Scholar 

  • Kaplan, J. R., Anthony, M., and Wood, L. (1981). Domestic breeding of Patas monkeys.Lab. Anim. Sci. 31(4): 409–412.

    PubMed  CAS  Google Scholar 

  • Kempske, S. (1985).Macaca silenus: Survey of North American and European zoo practices. InThe Lion-Tailed Macaque: Status and Conservation, VII, Alan R. Liss, New York, pp. 221–235.

    Google Scholar 

  • King, N. E., and Mitchell, G. (1987). Breeding primates in zoos. In Mitchell, G. M., and Erwin, J. (eds.),Comparative Primate Biology, Vol. II. Behavior, Cognition and Motivation, Alan R. Liss, New York, pp. 219–261.

    Google Scholar 

  • Kingsley, S. R., and Martin, R. D. (1979). A case of placenta praevia in an orang-utan.Vet. Rec. 104: 56–57.

    PubMed  CAS  Google Scholar 

  • Kollias, G. V., and Kawakami, T. G. (1981). Factors contributing to the successful captive reproduction of white-handed gibbons(Hylobates lar). Proc. Am. Assoc. Zoo Vet. 45–47.

  • Koyama, N., Norikoshi, K., and Mano, T. (1975). Population dynamics of Japanese monkeys at Arashiyama. In Kondo, S., Kawai, N., and Ehara, A. (eds.),Contemporary Primatology. 5th Int. Congr. Primatol, Karger, Basel, pp. 411–417.

    Google Scholar 

  • Koyama, N. K., Takahata, Y., Huffman, M. A., Norikoshi, K., and Suzuki, H. (1992). Reproductive parameters of female Japanese macaques(Macaca fuscata): Thirty years data from the Arashiyama troops, Japan.Primates 33(1): 33–47.

    Article  Google Scholar 

  • Krylova, R. I. (1986). Comparative pathology of sacred baboons.Vestn. Akad. Med. Nauk. SSSR 0(3): 19–22.

    CAS  Google Scholar 

  • Kuhlman, S. M., Rubin, L. F., and Quander, R. V. (1992). Choroidal colomboma in a cynomolgus monkey.Prog. Vet. Comp. Ophthalmol. 2(2): 95–101.

    Google Scholar 

  • Lernen, R., Lernen, S., Morrish, R., and Tooley, W. (1974). Marasmus and shigellosis in two infant gorillas.J. Med. Primatol. 3: 365–369.

    Google Scholar 

  • Lindburg, D. G. (1980). Status and captive reproduction of the lion-tailed macaque(Macaca silenus).Int. Zoo Yb. 20: 60–64.

    Google Scholar 

  • Lindburg, D. G., Berkson, J. M., and Nightenhelser, L. K. (1984). Primate breeding in zoos: A ten-year summary. In Ryder, O. A., and Byrd, M. L. (eds.),One Medicine, Springer-Verlag, Berlin, pp. 163–170.

    Google Scholar 

  • Lindburg, D. G., Lyles, A. M., and Czekala, N. M. (1989). Status and reproductive potential of lion-tailed macaques in captivity.Zoo Biol. Suppl. 1: 5–16.

    Article  Google Scholar 

  • Lyles, A. M., and Dobson, A. P. (1988). Dynamics of provisioned and unprovisioned primate populations. InEcology and Behaviour of Food-Enhanced Primate Groups, Alan R. Liss, New York, pp. 167–198.

    Google Scholar 

  • Mace, G. M. (1988). The genetic and demographic status of the western lowland gorilla(gorilla g. gorilla) in captivity.J. Zool. 216: 629–654.

    Google Scholar 

  • Mace, G. M. (1990). Birth sex ratio and infant mortality rates in captive western lowland gorillas.Folia Primatol. 55: 156–165.

    Google Scholar 

  • Malik, I., Seth, P. K., and Southwick, C. H. (1984). Population growth of free-ranging rhesus monkeys at Tuglaqabad.Am. J. Primatol. 7: 311–321.

    Article  Google Scholar 

  • Mallinson, J. J. C. (1984). The breeding of great apes at the Yersey Wildlife Preservation Trust and a look into the future.Zoo Biol. 3: 1–11.

    Article  Google Scholar 

  • Maple, T. L., and Stone, W. W. (1980). Environmental variables and great ape husbandry.Am. J. Primatol. Suppl. 1: 67–76.

    Google Scholar 

  • Maruhasi, T. (1982). An ecological study of troop fissions of Japanese monkeys(Macaca fuscata) on Yakusima Island, Japan.Primates 23: 317–337.

    Article  Google Scholar 

  • Masure, A. M., and Bouliere, F. (1971). Surpeuplement, fecondité, mortalité et aggressivité dans une population dePapio papio.Terre Vie 25: 491–505.

    Google Scholar 

  • Meiss, L., Goosen, C, Schrama, A. G. L. A., and Schonk, J. (1990). Control data on pre- and postneonatal survival of captive chimpanzees.J. Med. Primatol. 19: 479–484.

    PubMed  CAS  Google Scholar 

  • Melnick, D. (1981).Microevolution in a Population of Himalayan Rhesus Monkeys (Macaca mulatta), Ph.D. dissertation, Yale University, New Haven, CT.

    Google Scholar 

  • Menard, N., Vallet, D., and Gauthier-Hion, A. (1985). Demographie et réproduction deMacaca sylvanus dans different habitats en Algerie.Folia Primatol. 44: 65–81.

    PubMed  CAS  Google Scholar 

  • Minezawa, M., Nozawa, K., Gotoh, S., Yoshiro, S., Hamada, Y., Inagaki, H., and Nigi, H. (1990). A cytogenetic study on congenital limb malformations in the Japanese monkey(Macaca fuscata).Primates 31(4): 571–577.

    Article  Google Scholar 

  • Mooney, M., Siegel, M., and Gest, T. (1985). Prenatal stress and increased fluctuating symmetry in the parietal bones of neonatal rats.Am. J. Phys. Anthropol. 68: 131–134.

    Article  PubMed  CAS  Google Scholar 

  • Moor-Jankowski, J., and Mahoney, C. J. (1989). Chimpanzees in captivity: Humane handling and breeding within the confines imposed by medical research and testing.J. Med. Primatol. 18: 1–26.

    Article  PubMed  CAS  Google Scholar 

  • Mori, A. (1979). Analysis of population changes by measurement of body weight in the Koshima troup of Japanese monkeys.Primates 20: 371–397.

    Article  Google Scholar 

  • Murphy, M. F. (1982). Breeding statistics of western lowland gorilla(Gorilla g. gorilla).Int. Zoo Yb. 22: 180–185.

    Google Scholar 

  • Murphy, J. P., Markovits, J. E., Wesley, I., and Roberts, J. A. (1990). Listeriosis causing stillbirths and neonatal septicemia in outdoor housed macaques.Lab. Anim. Sci. 40(5): 547.

    Google Scholar 

  • Nadler, R. (1974). Determinants of variability in maternal behavior of captive female gorillas.Proc. Symp. 5th Congr. Int. Primatol. Soc. pp. 207–216.

  • Nadler, R. (1981). Laboratory research on sexual behavior of the great apes. In Graham, C. E. (ed.),Reproductive Biology of the Great Apes, Comparative and Biomedical Perspectives, Academic Press, New York, pp. 191–238.

    Google Scholar 

  • Nakamichi, M., Fujii, H., and Koyama, T. (1983). Development of a congenitally malformed Japanese monkey in a free-ranging group during the first four years of life.Am. J. Primatol. 5: 205–210.

    Article  Google Scholar 

  • Neugebauer, W. (1980). The status and management of the pygmee chimpanzee(Pan paniscus) in European zoos.Int. Zoo Yb. 20: 64–70.

    Google Scholar 

  • Newell-Morris, L. L., Fahrenbruch, C. E., and Sackett, G. P. (1989). Prenatal psychological stress, dermatoglyphic asymmetry and pregnancy outcome in the pigtailed macaque(Macaca nemestrina).Biol. Neonate 56: 61–75.

    Article  PubMed  CAS  Google Scholar 

  • Newman, L. M. (1974).Reproduction in the Indian Langur Monkey (Presbytis entellus) Under Laboratory Conditions, Master's thesis, University of California, Davis.

    Google Scholar 

  • Nowak, R. M., and Paradiso, J. L. (eds.) (1983).Walker's Mammals of the World, 4th ed., John Hopkins University Press, Baltimore, Vol. 1, pp. 393–479.

    Google Scholar 

  • Ocholi, R. A., Enurah, L. U., and Odeyemi, P. S. (1987). Fatal case of salmonellosis(Salmonella pullorum) in a chimpanzee(Pan troglodytes) in the Jos Zoo.J. Wildlife Dis. 23(4): 669–670.

    CAS  Google Scholar 

  • Ohsawa, H. (1979). Herd dynamics. In Kawai (ed.),Ecological and Sociological Studies of Gelada Baboons, Contributions to Primatology, Karger, Basel, Vol. 16, pp. 47–80.

    Google Scholar 

  • Olney, P. J. S. (ed.) (1982). Species of wild animals bred in captivity and multiple generations births in 1980.Int. Zoo Yb. 22: 409–416.

    Google Scholar 

  • Olney, P. J. S. (ed.) (1983). Species of wild animals bred in captivity and multiple generations births 1981.Int. Zoo Yb. 23: 311–318.

    Google Scholar 

  • Olney, P. J. S. (ed.) (1986a). Species of wild animals bred in captivity and multiple generations births 1982/1983.Int. Zoo. Yb. 24/25: 511–524.

    Google Scholar 

  • Olney, P. J. S. (ed.) (1986b). Species of wild animals bred in captivity and multiple generations births 1984.Int. Zoo Yb. 26: 471–480.

    Google Scholar 

  • Olney, P. J. S. (ed.) (1987). Species of wild animals bred in captivity and multiple generations births 1985.Int. Zoo Yb. 27: 399–408.

    Google Scholar 

  • Olney, P. J. S. (ed.) (1988). Species of wild animals bred in captivity and multiple generations births 1986.Int. Zoo Yb. 28: 449–459.

    Google Scholar 

  • Olney, P. J. S. (ed.) (1989). Species of wild animals bred in captivity and multiple generations births 1987.Int. Zoo Yb. 29: 310–320.

    Google Scholar 

  • Olney, P. J. S. (ed.) (1990). Species of wild animals bred in captivity and multiple generations births 1988/89.Int. Zoo Yb. 30: 427–443.

    Google Scholar 

  • Packer, C. (1979). Inter-troop transfer and inbreeding avoidance inPapio anubis.Anim. Behav. 27: 1–36.

    Article  Google Scholar 

  • Padovan, D., and Cantrell, C. (1983). Causes of death of infant rhesus and squirrel monkeys.J. Am. Vet. Med. Assoc. 183(11): 1182–1184.

    PubMed  CAS  Google Scholar 

  • Paul, A., and Kuester, J. (1987). Sex ratio adjustment in seasonally breeding primate species: Evidence from the Barbary macaque population at Affenberg Salem.Ethology 74: 117–132.

    Article  Google Scholar 

  • Rails, K., and Ballou, J. (1982). Effects of inbreeding on infant mortality in captive primates.Int. J. Primatol. 3(4): 491–505.

    Article  Google Scholar 

  • Randall, P., Taylor, P., and Banks, D. R. (1983). Pregnancy and stillbirth in a lowland gorilla(Gorilla g. gorilla).Int. Zoo Yb. 23: 183–185.

    Google Scholar 

  • Ratterree, M. S., and Baskin, G. B. (1992). Congenital hypotrichosis in a Rhesus monkey.Lab. Anim. Sci. 42(4): 410–412.

    PubMed  CAS  Google Scholar 

  • Rawlins, R. G., and Kessler, M. J. (1983). Congenital hereditary anomalies in the rhesus monkeys(Macaca mulatto) of Cayo Santiago.Teratology 28: 169–174.

    Article  PubMed  CAS  Google Scholar 

  • Rawlins, R. G., and Kessler, M. J. (1986). Demography of the free-ranging Cayo Santiago macaques (1976-1983). InThe Cayo Santiago Macaques, State University Press, New York.

    Google Scholar 

  • Redman, H. C., and Schneider, R. (1979). An epidemiological study of neonatal and postneonatal mortality inMacaca radiata at the California Primate Research Center (1966-1973),J. Med. Primatol. 8: 1–17.

    PubMed  CAS  Google Scholar 

  • Rhine, R. J., Wasser, S. K., and Noton (1988). Eight-year study of social and ecological correlates of mortality among immature baboons of Nikumi National Park, Tanzania.Am. J. Primatol. 16: 199–212.

    Article  Google Scholar 

  • Richard, A. F. (ed.) (1985).Primates in Nature, W. H. Freeman, New York, Chap. VI.

    Google Scholar 

  • Richig, J. W., Sullivan, D. J., Plocharski, E. J., Keselica, M. C., Pisacreta, D., and Katz, R. (1988). Pulmonic stenosis in a male cynomolgus monkey(Macaca fascicularis).Lab Anim. Sci. 38(4): 510.

    Google Scholar 

  • Rijksen, H. D. (ed.) (1978). III. Complexes of behaviour. InA Field Study on the Sumatrean Orang-utan, H. Veenman & Zonen, Wageningen, pp. 239–249.

    Google Scholar 

  • Ritscher, D., and Linke, K. (1982). Wiederholter Kaiserschnitt bei einem Silbergibbon(Hylobates moloch) und veterinär-medizische Probleme bei der Aufzucht der beiden Jungtiere,proc. Int. Symp. Erkrank. Zoo Wildtiere 24: 107–111.

    Google Scholar 

  • Roberts, M. S. (1978). The annual reproductive cycle of captiveMacaca sylvana.Folia Primatol. 29: 229–235.

    PubMed  CAS  Google Scholar 

  • Rowel, T. E. (1972).Social Behavior of Monkeys, Penguin Books, Kingsport Press, Kingsport, TN.

    Google Scholar 

  • Rüedi, D., and Heldstab, A. (1978). Herpes-virus Sepsis bei einem 13 Tage alten Flachland Gorilla(Gorilla gorilla gorilla) in zoologischen Garten Basel.Proc. Int. Symp. Erkrank. Zoo Wildtiere 20: 279–283.

    Google Scholar 

  • Sakakibara, I., and Honjo, S. (1990). Spontaneously occurring congenital polycystic kidney in a cynomologus monkey(Macaca fascicularis).J. Med. Primatol 19(5): 501–506.

    PubMed  CAS  Google Scholar 

  • Savage, A. (1987). Collaboration between research institutions and zoos for primate conservation.Int. Zoo Yb. 27: 140–148.

    Google Scholar 

  • Scanlan, R. M., Maclin, R., Ripp, C, and Suomi, S. J. (1985). Sex, birthweight and neonatal mortality in rhesus monkeys(Macaca mulatto).Am. J. Primatol. 8: 363.

    Google Scholar 

  • Schneider, H. E., and Gensch, W. (1974). Aborti beim Weisshandgibbon(Hylobates lar).Proc. Int. Symp. Erkrank. Zoo Wildtiere 16: 261–263.

    Google Scholar 

  • Seal, U. S., and Flesness, N. R. (1986). Captive chimpanzee populations—past, present and future. In Benirschke, K. (ed.),Primates, the Road to Self-Sustaining Populations, Springer Verlag, New York, pp. 47–55.

    Google Scholar 

  • Seal, U. S., Flesness, N., and Foose, T. (1985). Neonatal and infant mortality in captive-born great apes. In Graham, C. E., and Bowen, J. A. (eds.),Clinical Management of Infant Great Apes, Alan R. Liss, New York, pp. 193–203.

    Google Scholar 

  • Seifert, S. (1970). Uber eine Schwangerschaft und die Frühgeburt eines toten Jungen bei einem Orang-utan(Pongo pygmaeus) im Leipziger Zoo.Zool. Garten 38(6): 310–321.

    Google Scholar 

  • Sesline, D. H., Simpson, J., and Hendrickson, R. V. (1983). Neonatal deaths in Bonnet monkeys born to dams with rudimentary papillae mammae.Lab. Anim. Sci. 33(5): 467–468.

    PubMed  CAS  Google Scholar 

  • Sigg, H., Stolba, A., Abegglen, J. J., and Dasser, V. (1982). Life history of Hamadryas baboons: Physical development, infant mortality, reproductive parameters and family relationships.Primates 23(4): 473–487.

    Article  Google Scholar 

  • Silk, J. B., Clark-Wheatley, C. B., Rodman, P. S., and Samuels, A. (1981). Differential reproductive success and facultative adjustment of sex ratios among female bonnet macaques(Macaca radiata).Anim. Behav. 29: 1106–1120.

    Article  Google Scholar 

  • Simpson, M. J. A., and Simpson, A. E. (1982). Birth sex ratios and social rank in rhesus monkey mothers.Nature 300: 440–441.

    Article  PubMed  CAS  Google Scholar 

  • Small, M. F. (1982). Reproductive failure in macaques.Am. J. Primatol. 2: 137–147.

    Article  Google Scholar 

  • Small, M. F., and Rodman, P. S. (1981). Primigravidity and infant loss in bonnet macaques.J. Med. Primatol. 10: 164–169.

    PubMed  CAS  Google Scholar 

  • Smith, D. G. (1982). A comparison of the demographic structure and growth of free ranging and captive groups of rhesus monkeys(Macaca mulatto).Primates 23: 24–30.

    Article  Google Scholar 

  • Smith, N. R., and Damit, M. (1982). Fatal bronchopneumonia in a young orangutan caused byPseudomonas pseudomallei.Vet. Rec. 110: 251.

    PubMed  Google Scholar 

  • Smuts, B. B., and Nicolson, N. (1989). Reproduction in wild female olive baboons.Am. J. Primatol. 19: 229–246.

    Article  Google Scholar 

  • Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, Th. T. (eds.) (1987).Primate Societies, University of Chicago Press, Chicago.

    Google Scholar 

  • Snook, S. S., and King, N. W. (1989). Familial infantile cortical hyperostosis (Caffey's disease) in rhesus monkeys(Macaca mulatto).Vet. Pathol. 26(3): 274–277.

    Article  PubMed  CAS  Google Scholar 

  • Southwick, C. H., and Siddiqi, M. F. (1976). Demographic characteristics of semi-protected rhesus monkeys groups in India.Yearb. Phys. Anthropol. 20: 242–252.

    Google Scholar 

  • Strauss, G., Cario, W. R., Struhrberg, E., and Dathe, R. (1988). Klinik einer letalen Staphylokokken-Infektion beim Orang-utan.Proc. Int. Symp. Erkrank. Zoo Wildtiere 30: 377–380.

    Google Scholar 

  • Strum, S. G., and Western, J. D. (1982). Variations in fecundity with age and environment in olive baboons(Papio anubis).Am. J. Primatol. 3: 61–76.

    Article  Google Scholar 

  • Sugiyama, Y., and Ohsawa, H. (1982a). Population dynamics of Japanese monkeys at Ryozenyama. III. Female desertion of the troup.Primates 23: 31–44.

    Article  Google Scholar 

  • Sugiyama, Y., and Ohsawa, H. (1982b). Population dynamics of Japanese monkeys with special reference to the effect of artificial feeding.Folia Primatol. 39: 238–263.

    PubMed  CAS  Google Scholar 

  • Struhsaker, T. T., and Leland, L. (1987). Infanticide by adult males. In Smuts, B., Cheney, D. L., and Seyfarth, R. M. (eds.),Primate Societies, University of Chicago Press, Chicago, pp. 92–97.

    Google Scholar 

  • Tanaka, T., Tokuda, K., and Kotera, S. (1970). Effects of infant loss on the interbirth interval of Japanese monkeys.Primates 11: 113–117.

    Article  Google Scholar 

  • Teas, J. T., Richie, L., Tayler, H. G., Siddiqi, M. F., and Southwick, C. H. (1981). Natural regulation of rhesus monkey populations in Kathmandu, Nepal.Folia Primatol. 35: 117–123.

    PubMed  CAS  Google Scholar 

  • Teleki, G., Hunt, E. E., and Pfifferling, J. H. (1976). Demographic observations (1963-1973) on the Chimpanzees of Gombe National Park, Tanzania.J. Hum. Evol. 5: 559–598.

    Article  Google Scholar 

  • Tigges, J., Gordon, T. P., McClure, H. M., Elmer, C. H., and Peters, A. (1988). Survival rate and life span of rhesus monkeys at the Yerkes regional primate research center.Am. J. Primatol. 15: 263–273.

    Article  Google Scholar 

  • Uemura, E., Houser, W. D., and Capp, C. J. (1979). Strongyloidiasis in an infant orangutan(Pongo pygmaeus).J. Med. Primatol. 8: 282–288.

    PubMed  CAS  Google Scholar 

  • van Schaik, C. P., and van Noordwijk, M. A. (1983). Social stress and the sex ratio of neonates and infants among non-human primates.Neth. J. Zool. 33(3): 249–265.

    Google Scholar 

  • van Schaik, C. P., and van Noordwijk, M. A. (1985). Interannual variability in fruit abundance and the reproductive seasonality in Sumatran long-tailed macaques(Macaca fascicularis).J. Zool. London 206: 533–549.

    Article  Google Scholar 

  • van Schaik, C. P., and de Visser, J. A. G. M. (1990). Fragile sons or harassed daughters? Sex differences in mortality among juvenile primates.Folia Primatol. 55: 10–23.

    PubMed  Google Scholar 

  • van Vreeswijk, W., and Koning, H. (1978). Breeding of macaques and chimpanzees at the Dutch Primate Center. In Chivers (ed.),Recent Advances in Primatology, Vol. II, pp. 279–287.

  • vanWagenen, G. (1972). Vital statistics from a breeding colony. Reproduction and pregnancy outcome inMacaca mulatto. J. Med. Primatol. 1: 3–28.

    Google Scholar 

  • Vetesi, F., Balsai, A., and Kemenes, F. (1972). Abortion in Gray's monkey(Cercopithecus mona) withListeria monocytogenes.Acta Microbiol. Acad. Sci Hung. 19: 441–443.

    PubMed  CAS  Google Scholar 

  • Watanabe, K., and Mori, A. (1992). Characteristic features of the reproduction of Koshima monkeys,Macaca fuscata fuscata: A summary of thirty-four years of observations.Primates 33(1): 1–32.

    Article  CAS  Google Scholar 

  • Watts, D. P. (1989). Infanticide in mountain gorillas: New cases and a reconsideration of the evidence.Ethology 81: 1–189.

    Article  Google Scholar 

  • Watts, D. P. (1990). Mountain gorilla life histories, reproductive competition, and sociosexual behavior and some implications for captive husbandry.Zoo Biol. 9: 185–200.

    Article  Google Scholar 

  • Whitten, P. I. (1983). Diet and dominance among female vervet monkeys(Cercopithecus aethiops).Am. J. Primatol. 5: 139–160.

    Article  Google Scholar 

  • Wilson, J. G. (1972). Abnormalities of intra-uterine development in non-human primates.Acta Endocr. Copenhagen Suppl. 166: 261–292.

    CAS  Google Scholar 

  • Wilson, J. G. (1978). Developmental abnormalities in non-human primates. In Benirschke, K., Garner, F. M., Jones, T. G., and Kozma, C. (eds.),Pathology of Laboratory Animals, Springer Verlag, München, pp. 1818–1946.

    Google Scholar 

  • Wilson, J. G., and Gavan, J. A. (1967). Congenital malformations in non-human primates: Spontaneous and experimentally induced.Anat. Rec. 158: 99–110.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, M. E., Gordon, T. P., and Berstein, I. S. (1978). Timing of births and reproductive success in rhesus monkey social groups.J. Med. Primatol. 7: 202–212.

    PubMed  CAS  Google Scholar 

  • Winkler, P., Loch, H., and Vogel, C. (1984). Life history of hanuman langurs(Presbytis entellus). Reproductive parameters, infant mortality and troop development.Folia Primatol. 43: 1–23.

    Article  PubMed  CAS  Google Scholar 

  • Wittstatt, U. (1990). Strongyloidiasis—pathologisch-anatomische und histologische Befunde bei zwei Weisshandgibbons(Hylobates lar) und einem Kappengibbon(Hylobates lar pileatus).Proc. Int. Symp. Erkrank Zoo Wildtiere 32: 35–40.

    Google Scholar 

  • Wundersee, W. (1974). Gestose bei einem Orang-utan(Pongo pygmaeus). Zool. Garten 44(3): 168–171.

    Google Scholar 

  • Young, R., and Reed, T. (1980). Maternal age and dermatoglyphic asymmetry in man: Another look.Hum. Hered. 30: 145–148.

    Article  PubMed  CAS  Google Scholar 

  • Zwart, P. (1969). Hepatitis infectiosa bei einem Schimpansen.Proc. Int. Symp. Erkrank. Zoo Wildtiere 11: 77–80.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Veterinary Medicine, Department of Pathology, Division of Laboratory and Exotic Animals, Utrecht, The Netherlands

    I. W. J. Debyser

Authors
  1. I. W. J. Debyser
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Debyser, I.W.J. Catarrhine juvenile mortality in captivity, under seminatural conditions, and in the wild. International Journal of Primatology 16, 935–969 (1995). https://doi.org/10.1007/BF02696111

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02696111

Key Words

Search

Navigation