Skip to main content
Log in

The socioecology of infant handling in primates: Is the current model convincing?

  • Published:
Primates Aims and scope Submit manuscript

Abstract

A strong interest shown by females towards infants other than their own is one of the most consistent behavioral traits found in primates, including humans. Species differences exist, however, in the extent mothers allow other group members to interact with their offspring. Socioecological theory predicts that in species characterized by relaxed, egalitarian dominance relations mothers should allow extensive interactions between their infants and other individuals from the first weeks of life, while in species characterized by nepotistic and despotic dominance relations maternal tolerance of infant handling should be low. While this model received some support from a comparison between colobines and some cercopithecines, several other species, including the Barbary macaque, do not appear to fit easily into the framework. In fact, only about half of all well-studied species follow the predicted pattern, suggesting that other factors, associated with the costs and benefits of the behavior, must be invoked to explain the variation in mothering styles and infant handling found in primates.

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.

Similar content being viewed by others

References

  • Anderson, C. M. 1992. Male investment under changing conditions among chacma baboons at Suikerbosrand.Amer. J. Phys. Anthropol., 87: 479–496.

    Article  CAS  Google Scholar 

  • Aureli, F. 1992. Post-conflict behaviour among wild long-tailed macaques (Macaca fascicularis).Behav. Ecol. Sociobiol., 31: 329–337.

    Article  Google Scholar 

  • Aureli, F.;Das, M.;Veenema, H. C. 1997. Differential kinship effect on reconciliation in three species of macaques (Macaca fascicularis, M. fuscata, andM. sylvanus).J. Comp. Psychol., 111: 91–99.

    Article  PubMed  CAS  Google Scholar 

  • Berman, C. M. 1980. Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: a comparison with captive pairs.Anim. Behav., 28: 860–873.

    Article  Google Scholar 

  • Bernstein, I. S. 1976. Activity patterns in a sooty mangabey group.Folia Primatol. 26: 185–206.

    PubMed  CAS  Google Scholar 

  • Burton, F. D. 1972. The integration of biology and behavior in the socialization ofMacaca sylvana of Gibraltar. In:Primate Socialization,Poirier,F. E., (ed.), Random House, New York, pp. 29–62.

    Google Scholar 

  • Caldecott, J. O. 1986. Mating patterns, societies and the ecogeography of macaques.Anim. Behav., 34: 208–220.

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Chapais, B. 1992. The role of alliances in social inheritance of rank among female primates. In:Coalitions and Alliances in Humans and Other Mammals,Harcourt,A. H.;de Waal,F. B. M. (eds.), Oxford Univ. Press, Oxford, pp. 29–59.

    Google Scholar 

  • Clutton-Brock, T. H.;Harvey, P. H. 1984. Comparative approaches to investigating adaptation. In:Behavioural Ecology: An Evolutionary Approach (2nd ed.),Krebs, J. R.;Davies, N. B. (eds.), Blackwell Scientific, Oxford, pp. 7–29.

    Google Scholar 

  • Deag, J. M. 1973. Intergroup encounters in the wild Barbary macaqueMacaca sylvanus L. In:Comparative Ecology and Behaviour of Primates,Michael,R. P.;Crook,J. H. (eds.), Academic Press, London, pp. 315–373.

    Google Scholar 

  • Deag, J. M. 1974. A study of the social behaviour and ecology of the wild barbary macaque,Macaca sylvanus L. Ph. D. Diss., Univ. of Bristol, England.

    Google Scholar 

  • Deag, J. M. 1977. Aggression and submission in monkey societies.Anim. Behav., 25: 456–474.

    Google Scholar 

  • Deag, J. M. 1980. Interactions between males and unweaned Barbary macaques: testing the agonistic buffering hypothesis.Behaviour, 75: 54–81.

    Google Scholar 

  • Delson, E. 1980. Fossil macaques: phyletic relationships and a scenario of deployment. In:The Macaques: Studies in Ecology, Behavior and Evolution,Lindburg,D. G. (ed.), Van Nostrand Reinhold, New York, pp. 10–30.

    Google Scholar 

  • de Waal, F. B. M. 1989. Dominance “style” and primate social organization. In:Comparative Socioecology: The Behavioural Ecology of Humans and Other Mammals,Standen,V.;Foley,R. A. (eds.), Blackwell Scientific, Oxford, pp. 243–263.

    Google Scholar 

  • de Waal, F. B. M.;Luttrell, L. M. 1989. Toward a comparative socioecology of the genusMacaca: different dominance styles in rhesus and stumptail monkeys.Amer. J. Primatol., 19: 83–109.

    Article  Google Scholar 

  • Edwards, C. P. 1993. Behavioral sex differences in children of diverse cultures: the case of nurturance to infants. In:Juvenile Primates: Life History, Development, and Behavior,Pereira,M. E.;Fairbanks,L. A., (eds.), Oxford Univ. Press, New York, pp. 327–338.

    Google Scholar 

  • Estrada, A.;Estrada, R. 1984. Female-infant interactions among free-ranging stumptail macaques (Macaca arctoides).Primates, 25: 48–61.

    Article  Google Scholar 

  • Fa, J. E. 1994. Herbivore intake/habitat productivity correlations can help ascertain re-introduction potential for the Barbary macaque.Biodiversity Conserv., 3: 309–317.

    Article  Google Scholar 

  • Fa, J. E.;Southwick, C. H. (eds.). 1988.Ecology and Behavior of Food-enhanced Primate Groups. Alan R. Liss, New York.

    Google Scholar 

  • Fairbanks, L. A. 1990. Reciprocal benefits of allomothering for female vervet monkeys.Anim. Behav., 40: 553–562.

    Article  Google Scholar 

  • Garber, P. A.;Leigh, S. R. 1997. Ontogenetic variation in small-bodied New World primates: implications for patterns of reproduction and infant care.Folia Primatol., 68: 1–22.

    PubMed  CAS  Google Scholar 

  • Gould, L. 1992. Alloparental care in free-rangingLemur catta at Berenty Reserve, Madagascar.Folia Primatol., 58: 72–83.

    Google Scholar 

  • Hauser, M. D.;Fairbanks, L. A. 1988. Mother-offspring conflict in vervet monkeys: variation in response to ecological conditions.Anim. Behav. 36: 802–813.

    Article  Google Scholar 

  • Heinz, U. 1995. Konkurrenz zwischen adulten Berberaffenweibchen. Diploma thesis, Univ. of Innsbruck, Austria.

    Google Scholar 

  • Heinz, U.;Paul, A. 1996. Food competition and social relationships in female Barbary macaques (M. sylvanus) at Affenberg Salem.Primate Report, 44: 18.

    Google Scholar 

  • Higley, J. D.;Suomi, S. J. 1986. Parental behaviour in non-human primates. In:Parental Behaviour,Sluckin,W.;Herbert,M. (eds.), Blackwell, Oxford, pp. 152–207.

    Google Scholar 

  • Hill, D. A. 1999. Effects of provisioning on the social behaviour of Japanese and rhesus macaques: implications for socioecology.Primates, 40: 187–198.

    Google Scholar 

  • Hinde, R. A.;Atkinson, S. 1970. Assessing the roles of social partners in maintaining mutual proximity, as exemplified by mother-infant relations in monkeys.Anim. Behav., 18: 169–176.

    Article  Google Scholar 

  • Hrdy, S. B. 1976. Care and exploitation of nonhuman primate infants by conspecifics other than the mother. In:Advances in the Study of Behavior, Vol. 6,Rosenblatt,L.;Hinde,R. A.;Shaw,R.;Beer,C. (eds.), Academic Press, New York, pp. 101–158.

    Google Scholar 

  • Jay, P. 1965. Field studies. In:Behavior in Nonhuman Primates, Vol. 2,Schrier,A. M.;Harlow,H. F.;Stollnitz,F. (eds.), Academic Press, New York, pp. 525–591.

    Google Scholar 

  • Kuester, J.;Paul, A. 1986. Male-infant relationships in semifree-ranging Barbary macaques (Macaca sylvanus) of Affenberg Salem/FRG: testing the “male care” hypothesis.Amer. J. Primatol., 10: 315–327.

    Article  Google Scholar 

  • Kuester, J.;Paul, A. 1992. Influence of male competition and female mate choice on male mating success in Barbary macaques (Macaca sylvanus).Behaviour, 120: 192–217.

    Google Scholar 

  • Kuester, J.;Paul, A.;Arnemann, J. 1994. Kinship, familiarity and mating avoidance in Barbary macaques,Macaca sylvanus.Anim. Behav., 48: 1183–1194.

    Article  Google Scholar 

  • Kumar, A.;Kurup G. U. 1981. Infant development in the lion-tailed macaque,Macaca silenus (Linnaeus) the first eight weeks.Primates, 22: 512–522.

    Article  Google Scholar 

  • Lahiri, R. K.;Southwick, C. H. 1966. Paternal care inMacaca sylvana.Folia Primatol., 4: 257–264.

    PubMed  CAS  Google Scholar 

  • Lancaster, J. 1971. Play-mothering: the relation between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops).Folia Primatol., 15: 161–182.

    Google Scholar 

  • Maestripieri, D. 1994a. Social structure, infant handling, and mothering styles in group-living Old World monkeys.Int. J. Primatol., 15: 531–553.

    Google Scholar 

  • Maestripieri, D. 1994b. Mother-infant relationships in three species of macaques (Macaca mulatta, M. nemestrina, andM. arctoides), II. The social environment.Behaviour, 131: 97–113.

    Google Scholar 

  • Matsoo-Smith, E.;Watt, S. L.;Allen, J. S.;Lambert, D. M. 1997. Genetic relatedness and alloparental behaviour in a captive group of spider monkeys (Ateles geoffroyi).Folia Primatol., 68: 26–30.

    Google Scholar 

  • Matsumura, S. 1997. Mothers in a wild group of moor macaques (Macaca maurus) are more attractive to other group members when holding their infants.Folia Primatol., 68: 77–85.

    Article  PubMed  CAS  Google Scholar 

  • McKenna, J. J. 1979. Aspects of infant socialization, attachment, and maternal caregiving patterns among primates: a cross-disciplinary review.Yrbk. Phys. Anthropol., 22: 250–286.

    Google Scholar 

  • McKenna, J. J. 1987. Parental supplements and surrogates among primates: cross-species and cross-cultural comparisons. In:Parenting Across the Life Span: Biosocial Dimensions,Lancaster,J.;Altmann,J.;Rossi,A. (eds.), Aldine de Gruyter, New York, pp. 143–184.

    Google Scholar 

  • Mehlman, P. 1986. Male intergroup mobility in a wild population of the Barbary macaque (Macaca sylvanus), Ghomaran Rif Mountains, Morocco,Amer. J. Primatol., 10: 67–81.

    Article  Google Scholar 

  • Mehlman, P. T.;Parkhill, R. S. 1988. Intergroup interactions in wild Barbary macaques (Macaca sylvanus), Ghomaran Rif Mountains, Morocco,Amer. J. Primatol., 15: 31–44.

    Article  Google Scholar 

  • Ménard, N.;Scheffrahn, W.;Vallet, D. 1994. Paternity certainty, relatedness and parental investment: a test in a natural population of Barbary macaques (Macaca sylvanus).Folia Primatol., 62: 204–205.

    Article  Google Scholar 

  • Ménard, N.;Scheffrahn, W.;Vallet, D.;Reber, C. 1992. Application of blood protein electrophoresis and DNA fingerprinting to the analysis of paternity and social characteristics of wild Barbary macaques. InPaternity in Primates: Genetic Tests and Theories,Martin,R. D.;Dixson,A. F.;Wickings,E. J. (eds.), Karger, Basel, pp. 155–174.

    Google Scholar 

  • Ménard, N.;Vallet, D. 1993. Population dynamics ofMacaca sylvanus in Algeria: an 8-year study.Amer. J. Primatol., 30: 101–118.

    Article  Google Scholar 

  • Ménard, N.;Vallet, D. 1996. Demography and ecology of Barbary macaques (Macaca sylvarnus) in two different habitats. In:Evolution and Ecology of Macaque Societies,Fa,J. E.;Lindburg,D. G. (eds.), Cambridge Univ. Press, Cambridge, pp. 106–131.

    Google Scholar 

  • Mitani, J. C.;Watts, D. 1997. The evolution of non-maternal caretaking among anthropoid primates: do helpers help?Behav. Ecol. Sociobiol., 40: 213–220.

    Article  Google Scholar 

  • Mitchell, C. L.;Boinski, S.;van Schaik, C. P. 1991. Competitive regimes and female bonding in two species of squirrel monkeys (Saimiri oerstedi andS. sciureus).Behav. Ecol. Sociobiol., 28: 55–60.

    Article  Google Scholar 

  • Moore, J. 1992. Dispersal, nepotism, and primate social behavior.Int. J. Primatol., 13: 361–378.

    Article  Google Scholar 

  • Morales, J. C.;Melnick, D. J. 1998. Phylogenetic relationships of the macaques (Cercopithecidae,Macaca), as revealed by high resolution restriction site mapping of mitochondrial ribosomal genes.J. Human Evol., 34: 1–23.

    Article  CAS  Google Scholar 

  • Muroyama, Y.;Thierry, B. 1996. Fatal attack on an infant by an adult female Tonkean macaque.Int. J. Primatol., 17: 219–227.

    Google Scholar 

  • Nicolson, N. 1987. Infants, mothers, and other females. In:Primate Societies,Smuts,B. B.;Cheney,D. L.;Seyfarth,R. M.;Wrangham,R. W.;Struhsaker,T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 330–342.

    Google Scholar 

  • O'Brien, T. G.;Robinson, J. G. 1991. Allomaternal care by female wedge-capped capuchin monkeys: effects of age, rank, and relatedness.Behaviour, 119: 30–50.

    Google Scholar 

  • Ogawa, H. 1995. Bridging behavior and other affiliative interactions among male Tibetan macaques (Macaca thibetana).Int. J. Primatol., 16: 707–729.

    Google Scholar 

  • Packer, C.;Lewis, S.;Pusey, A. 1992. A comparative analysis of non-offspring nursing.Anim. Behav., 43: 265–281.

    Article  Google Scholar 

  • Paul, A. 1984. Zur Sozialstruktur und Sozialisation semi-freilebender Berberaffen (Macaca sylvanus L. 1758). Ph.D. diss., Univ. of Kiel, Kiel.

    Google Scholar 

  • Paul, A.;Kuester, J. 1985. Intergoup transfer and incest avoidance in semifree-ranging Barbary macaques (Macaca sylvanus), at Salem (FRG).Amer. J. Primatol., 8: 317–322.

    Article  Google Scholar 

  • Paul, A.;Kuester, J. 1987. Dominance, kinship and reproductive value in female Barbary macaques (Macaca sylvanus) at Affenberg Salem.Behav. Ecol. Sociobiol. 21: 323–331.

    Article  Google Scholar 

  • Paul, A.;Kuester, J. 1988. Life-history patterns of Barbary macaques (Macaca sylvanus) at Affenberg Salem. In:Ecology and Behavior of Food-enhanced Primate Groups,Fa,J. E.;Southwick,C. H. (eds.), Alan R. Liss, New York, pp. 199–228.

    Google Scholar 

  • Paul, A.;Kuester, J. 1996. Infant handling by female Barbary macaques (Macaca sylvanus) at Affenberg Salem: testing functional and evolutionary hypotheses.Behav. Ecol. Sociobiol., 39: 133–145.

    Article  Google Scholar 

  • Paul, A.;Kuester, J.;Arnemann, J. 1992. DNA fingerprinting reveals that infant care by male Barbary macaques (Macaca sylvanus) is not paternal investment.Folia Primatol. 58: 93–98.

    PubMed  CAS  Google Scholar 

  • Paul, A.;Kuester, J.;Arnemann, J. 1996. The sociobiology of male-infant interactions in Barbary macaques,Macaca sylvanus.Anim. Behav., 51: 155–170.

    Article  Google Scholar 

  • Paul, A.;Thommen, D. 1984. Timing of birth, female reproductive success and infant sex ratio in semi-free-ranging Barbary macaques (Macaca sylvanus).Folia Primatol., 42: 2–16.

    Google Scholar 

  • Preuschoft, S.;Beckmann, F. 1995. “Smiling” and “Laughter” in lion-tailed macaques (Macaca silenus): a preliminary analysis of their bared-teeth displays. In: “Laughter” and “Smiling” in Macaques. Ph.D. thesis byPreuschoft, S., Univ. of Utrecht, Utrecht, pp. 111–136.

    Google Scholar 

  • Preuschoft, S.; Paul, A. in press. Dominance, egalitarianism, and stalemate: an experimental approach to male-male competition in, Barbary macaques. In:Primate Males,Kappeler, P. M. (ed.), Cambridge Univ. Press, Cambridge.

  • Preuschoft, S.;Paul, A.;Kuester, J. 1998. Dominance styles of female and male Barbary macaques (Macaca sylvanus).Behaviour, 135: 731–755.

    Google Scholar 

  • Prud'Homme, J.;Chapais, B. 1993. Rank relations among sisters in semi-free-ranging Barbary macaques (Macaca sylvanus).Int. J. Primatol., 14: 405–420.

    Article  Google Scholar 

  • Rosenblum, L. A. 1971. Infant attachment in monkeys. In:The Origins of Human Social Relations,Schaffer,H. R. (ed.), Academic Press, New York, pp. 85–113.

    Google Scholar 

  • Rosenblum, L. A.;Kaufman, I. C. 1967. Laboratory observations of early mother-infant relations in pigtail and bonnet macaques. In:Social Communication among Primates,Altmann,S. A. (ed.), Univ. of Chicago Press, Chicago, pp. 33–41.

    Google Scholar 

  • Ross, C.;MacLarnon, A. 1995. Ecological and social correlates of maternal expenditure on infant growth in haplorhine primates. In:Motherhood in Human and Nonhuman Primates,Price,C. R.;Martin,R. D.;Skuse,D. (eds.), Karger, Basel, pp. 37–46.

    Google Scholar 

  • Rowell, T.E.;Hinde, R. A.;Spencer-Booth, Y. 1964. “Aunt”-infant interaction in captive rhesus monkeys.Anim. Behav., 12: 219–226.

    Article  Google Scholar 

  • Serio-Silva, J. C.;Rodriguez-Luna, E. 1994. Howler monkey (Alouatta palliata) behavior during the first weeks of life. In:Current Primatology, Vol. 2: Social Development, Learning and Behaviour,Roeder,J. J.;Thierry,B.;Anderson,J. R.;Herrenschmidt,N. (eds.), ULP Press, Strasbourg, pp. 309–313.

    Google Scholar 

  • Silk, J. B. 1980. Kidnapping and female competition among captive bonnet macaques.Primates, 21: 100–110.

    Article  Google Scholar 

  • Simonds, P. E. 1965. The bonnet macaque in South India. In:Primate Behavior: Field Studies of Monkeys and Apes,DeVore,I. (ed.), Holt, Rinehart & Winston, New York, pp. 175–196.

    Google Scholar 

  • Simonds, P. E. 1974. Sex differences in bonnet macaque networks and social structure.Archives of Sexual Behav., 3: 151–166.

    Article  CAS  Google Scholar 

  • Skamel, U. 1994. Zur Struktur und Funktion zwischengeschlechtlicher Beziehungen bei Berberaffen (Macaca sylvanus L. 1758) außerhalb der Paarungszeit. Diploma thesis, Univ. of Goettingen, Germany.

    Google Scholar 

  • Small, M. F. 1990. Alloparental behaviour in Barbary macaques,Macaca sylvanus, Anim. Behav., 39: 297–306.

    Article  Google Scholar 

  • Stanford, C. B. 1992. Costs and benefits of allomothering in, wild capped langurs (Presbytis pileata).Behav. Ecol. Sociobiol., 30: 29–34.

    Article  Google Scholar 

  • Sterck, E. H. M.;Watts, D. P.;van Schaik, C. P. 1997. The evolution of female social relationships in nonhuman primates.Behav. Ecol. Sociobiol., 41: 291–309.

    Article  Google Scholar 

  • Swartz, K. B.;Rosenblum, L. A. 1981. The social context of parental behavior: a perspective on primate socialization. In:Parental Care in Mammals,Gubernick,D. J.;Klopfer,P. H. (eds.), Plenum Press, New York, pp 417–454.

    Google Scholar 

  • Taub, D. M. 1978. Aspects of the biology of the wild Barbary macaque (Primates, Cercopithecinae,Macaca sylvanus L., 1758): biogeography, the mating system and male-infant associations. Ph.D. diss., Univ. of California, Davis.

    Google Scholar 

  • Taub, D. M. (ed.). 1984. Male caretaking behavior, among wild Barbary macaques (Macaca sylvanus). In:Primate Paternalism, Van Nostrand Reinhold, New York, pp. 20–55.

    Google Scholar 

  • Thierry, B. 1990. Feedback loop between kinship and dominance: the macaque model.J. Theor. Biol., 145: 511–521.

    Article  PubMed  CAS  Google Scholar 

  • Thierry, B.;Anderson, J. R.;Demaria, C.;Desportes, C.;Petit, O. 1994. Tonkean macaque behaviour from the perspective of the evolution of Sulawesi macaques. In:Current Primatology, Vol. 2, Social Development, Learning and Behaviour,Roeder,J. J.;Thierry,B.;Anderson,J. R.;Herrenschmidt,N. (eds.), ULP Press, Strasbourg, pp. 103–117.

    Google Scholar 

  • van Schaik, C. P. 1989. The ecology of social relationships amongst female primates. In:Comparative Socioecology: The Behavioural Ecology of Humans and Other Mammals,Standen,V.;Foley,R. A. (eds.), Blackwell Sci., Oxford, pp. 195–218.

    Google Scholar 

  • Vogel, C. 1984. Patterns of infant-transfer within two troops of common langurs (Presbytis entellus) near Jodhpur: testing hypotheses concerning the benefits and risks. In:Current Primate Researches,Roonwal,M. L.;Mohnot,S. M.;Rathore,N. S. (eds.), Jodhpur Univ. Press, Jodhpur, India, pp. 361–379.

    Google Scholar 

  • Wasser, S. K.;Barash, D. P. 1981. The selfish ‘allomother’: a comment onScollay andDeBold (1980).Ethol. Sociobiol. 2: 91–93.

    Article  Google Scholar 

  • Whitten, P. L. 1987. Infants and adult males. In:Primate Societies,Smuts,B. B.;Cheney,D. L.;Seyfarth,R. M.;Wrangham,R. W.;Struhsaker,T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 343–357.

    Google Scholar 

  • Williams, L.;Gibson, S.;McDaniel, M.;Bazzel, J.;Barnes, S.;Abee, C. 1994. Allomaternal interactions in the Bolivian squirrel monkey (Saimiri boliviensis boliviensis).Amer. J. Primatol., 34: 145–156.

    Article  Google Scholar 

  • Wilson, E. O. 1975.Sociobiology: The New Synthesis. Belknap Press of Harvard Univ. Press, Cambridge, Massachusetts.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

About this article

Cite this article

Paul, A. The socioecology of infant handling in primates: Is the current model convincing?. Primates 40, 33–46 (1999). https://doi.org/10.1007/BF02557700

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02557700

Key Words

Navigation