Skip to main content
SpringerLink
Log in

Maternal Behavior and Physiological Stress Levels in Wild Chimpanzees (Pan troglodytes schweinfurthii)

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

Abstract

Individual differences in maternal behavior toward, and investment in, offspring can have lasting consequences, particularly among primate taxa characterized by prolonged periods of development over which mothers can exert substantial influence. Given the role of the neuroendocrine system in the expression of behavior, researchers are increasingly interested in understanding the hormonal correlates of maternal behavior. Here, we examined the relationship between maternal behavior and physiological stress levels, as quantified by fecal glucocorticoid metabolite (FGM) concentrations, in lactating chimpanzees, Pan troglodytes schweinfurthii, at Gombe National Park, Tanzania. After accounting for temporal variation in FGM concentrations, we found that mothers interacted socially (groomed and played) with and nursed their infants more on days when FGM concentrations were elevated compared to days when FGM concentrations were within the range expected given the time of year. However, the proportion of time mothers and infants spent in contact did not differ based on FGM concentrations. These results generally agree with the suggestion that elevated GC concentrations are related to maternal motivation and responsivity to infant cues and are the first evidence of a hormonal correlate of maternal behavior in a wild great ape.

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

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adamakos, H., Ryan, K., Ullman, D. G., Pascoe, J., Diaz, R., & Chessare, J. (1986). Maternal social support as a predictor of mother-child stress and stimulation. Child Abuse & Neglect, 10(4), 463–470.

    Article  CAS  Google Scholar 

  • Albers, E. M., Riksen-Walraven, J. M., Sweep, F. C. G. J., & de Weerth, C. (2008). Maternal behavior predicts infant cortisol recovery from a mild everyday stressor. Journal of Child Psychology and Psychiatry, 49(1), 97–103.

    Article  PubMed  Google Scholar 

  • Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–266.

    Article  CAS  PubMed  Google Scholar 

  • Bahr, N. I., Pryce, C. R., Döbeli, M., & Martin, R. D. (1998). Evidence from urinary cortisol that maternal behavior is related to stress in gorillas. Physiology & Behavior, 64(4), 429–437.

    Article  CAS  Google Scholar 

  • Bardi, M., Bode, A. E., Ramirez, S. M., & Brent, L. Y. (2005). Maternal care and development of stress responses in baboons. American Journal of Primatology, 66(3), 263–278.

    Article  PubMed  Google Scholar 

  • Bardi, M., French, J. A., Ramirez, S. M., & Brent, L. (2004). The role of the endocrine system in baboon maternal behavior. Biological Psychiatry, 55(7), 724–732.

    Article  CAS  PubMed  Google Scholar 

  • Bardi, M., & Huffman, M. A. (2002). Effects of maternal style on infant behavior in Japanese macaques (Macaca fuscata). Developmental Psychobiology, 41(4), 364–372.

    Article  PubMed  Google Scholar 

  • Bardi, M., Shimizu, K., Barrett, G. M., Borgognini-Tarli, S. M., & Huffman, M. A. (2003). Peripartum cortisol levels and mother-infant interactions in Japanese macaques. American Journal of Physical Anthropology, 120(3), 298–304.

    Article  PubMed  Google Scholar 

  • Bates, D., Maechler, M., Bolker, B., & Walker, S. (2014). lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7. http://CRAN.R-project.org/package=lme4.

  • Behringer, V., Clauss, W., Hachenburger, K., Kuchar, A., Möstl, E., & Selzer, D. (2009). Effect of giving birth on the cortisol level in a bonobo groups’ (Pan paniscus) saliva. Primates, 50(2), 190–193.

    Article  PubMed  Google Scholar 

  • Berman, C. M. (1990). Consistency in maternal behavior within families of free-ranging rhesus monkeys: An extension of the concept of maternal style. American Journal of Primatology, 22(3), 159–169.

    Article  Google Scholar 

  • Boesch, C. (1997). Evidence for dominant wild female chimpanzees investing more in sons. Animal Behaviour, 54, 811–815.

    Article  PubMed  Google Scholar 

  • Carter, C. S., Altemus, M., & Chrousos, G. P. (2001). Neuroendocrine and emotional changes in the post-partum period. Progress in Brain Research, 133, 241–249.

    Article  CAS  PubMed  Google Scholar 

  • Clark, C. (1977). A preliminary report on weaning among chimpanzees of the Gombe National Park, Tanzania. In S. Chevalier-Skolinkoff & F. Poirer (Eds.), Primate biosocial development: Biological, social and ecological determinants (pp. 235–260). New York: Garland.

    Google Scholar 

  • Clutton-Brock, T. H. (1991). The evolution of parental care. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Crockford, C., Wittig, R. M., Langergraber, K., Ziegler, T. E., Zuberbühler, K., & Deschner, T. (2013). Urinary oxytocin and social bonding in related and unrelated wild chimpanzees. Proceedings of the Royal Society B: Biological Sciences, 280, 20122765.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cutrona, C., & Troutman, B. (1986). Social support, infant temperment, and parenting self-efficacy: A mediational model of postpartum depression. Child Development, 57, 1507–1518.

    Article  CAS  PubMed  Google Scholar 

  • Daly, M., & Wilson, M. (1995). Discriminative parental solicitude and the relevance of evolutionary models to the analysis of motivational systems. In M. Gazzaniga (Ed.), The Cognitive Neurosciences (pp. 1269–1286). Cambridge, MA: MIT Press.

  • de Weerth, C., & Buitelaar, J. (2005a). Cortisol awakening response in pregnant women. Psychoneuroendocrinology, 30(9), 902–907.

    Article  PubMed  Google Scholar 

  • de Weerth, C., & Buitelaar, J. (2005b). Physiological stress reactivity in human pregnancy–a review. Neuroscience & Biobehavioral Reviews, 29(2), 295–312.

    Article  Google Scholar 

  • de Weerth, C., Wiled, C., Jansen, L., & Buitelaar, J. (2007). Cardiovascular and cortisol responses to a psychological stressor during pregnancy. Acta Obstetricia et Gynecologica Scandinavica, 86(10), 1181–1192.

  • Emery Thompson, M. (2013). Reproductive ecology of female chimpanzees. American Journal of Primatology, 75(3), 222–237.

    Article  Google Scholar 

  • Emery Thompson, M., Muller, M. N., Kahlenberg, S. M., & Wrangham, R. W. (2010). Dynamics of social and energetic stress in wild female chimpanzees. Hormones and Behavior, 58(3), 440–449.

    Article  PubMed  Google Scholar 

  • Emery Thompson, M., Muller, M. N., & Wrangham, R. W. (2012). The energetics of lactation and the return to fecundity in wild chimpanzees. Behavioral Ecology, 23(6), 1234–1241.

    Article  Google Scholar 

  • Entringer, S., Buss, C., Shirtcliff, E., Cammack, A., Yim, I., Chicz-Demet, A., Sandman, C. A., & Wadhwa, P. D. (2009). Attenuation of maternal psychophysiological stress responses and the maternal cortisol awakening response over the course of human pregnancy. Stress, 13(3), 258–268.

  • Fairbanks, L. (1996). Individual differences in maternal style: Causes and consequences for mothers and offspring. Advances in the Study of Behavior, 2(1969), 579–611.

    Article  Google Scholar 

  • Fairbanks, L. A., & Hinde, K. (2013). Behavioral response of mothers and infants to variation in maternal condition: Adaptation, compensation, and resilience. In K. B. H. Clancy, K. Hinde, & J. N. Rutherford (Eds.), Building babies (pp. 281–302). New York: Springer Science+Business Media.

    Chapter  Google Scholar 

  • Fairbanks, L., & McGuire, M. (1988). Long-term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Developmental Psychobiology, 21(7), 711–724.

    Article  CAS  PubMed  Google Scholar 

  • Feldman, R., Singer, M., & Zagoory, O. (2010). Touch attenuates infants’ physiological reactivity to stress. Developmental Science, 13(2), 271–278.

    Article  PubMed  Google Scholar 

  • Fleming, A. S., Ruble, D., Krieger, H., & Wong, P. Y. (1997). Hormonal and experiential correlates of maternal responsiveness during pregnancy and the puerperium in human mothers. Hormones and Behavior, 31(2), 145–158.

    Article  CAS  PubMed  Google Scholar 

  • Fleming, A. S., Steiner, M., & Anderson, V. (1987). Hormonal and attitudinal correlates of maternal behaviour during the early post-partum period in first-time mothers. Journal of Reproductive and Infant Psychology, 5(4), 193–205.

    Article  Google Scholar 

  • Gesquiere, L. R., Khan, M., Shek, L., Wango, T. L., Emmanuel, O., Alberts, S. C., & Altmann, J. (2008). Coping with a challenging environment: Effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus). Hormones and Behavior, 54(3), 410–416.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Hamilton, W. D. (1967). Extraordinary sex ratios. Science, 156, 477–488.

    Article  CAS  PubMed  Google Scholar 

  • Hennessy, M. B., Kaiser, S., & Sachser, N. (2009). Social buffering of the stress response: Diversity, mechanisms, and functions. Frontiers in Neuroendocrinology, 30(4), 470–482.

    Article  CAS  PubMed  Google Scholar 

  • Hinde, K. (2009). Richer milk for sons but more milk for daughters: Sex-biased investment during lactation varies with maternal life history in rhesus macaques. American Journal of Human Biology, 21(4), 512–519.

    Article  PubMed  Google Scholar 

  • Jones, J. H., Wilson, M. L., Murray, C., & Pusey, A. E. (2010). Phenotypic quality influences fertility in Gombe chimpanzees. The Journal of Animal Ecology, 79(6), 1262–1269.

    Article  PubMed Central  PubMed  Google Scholar 

  • Krpan, K. M., Coombs, R., Zinga, D., Steiner, M., & Fleming, A. S. (2005). Experiential and hormonal correlates of maternal behavior in teen and adult mothers. Hormones and Behavior, 47(1), 112–122.

    Article  CAS  PubMed  Google Scholar 

  • Kuznetsova, A., Bruun Brockhoff, P., & Haubo Bojesen Christensen, R. (2014). lmerTest: Tests in Linear Mixed Effects Models. R package version 2.0-20. http://CRAN.R-project.org/package=lmerTest.

  • Lindstrom, J. (1999). Early development and fitness in birds and mammals. Trends in Ecology & Evolution, 14(9), 343–348.

    Article  Google Scholar 

  • Lonsdorf, E. V., Anderson, K. E., Stanton, M. A., Shender, M., Heintz, M. R., Goodall, J., & Murray, C. M. (2014a). Boys will be boys: Sex differences in wild infant chimpanzee social interactions. Animal Behaviour, 88, 79–83.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lonsdorf, E. V., Markham, A. C., Heintz, M. R., Anderson, K. E., Ciuk, D. J., Goodall, J., & Murray, C. M. (2014b). Sex differences in wild chimpanzee behavior emerge during infancy. PloS One, 9(6), e99099.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lyons, D. M., Parker, K. J., Katz, M., & Schatzberg, A. F. (2009). Developmental cascades linking stress inoculation, arousal regulation, and resilience. Frontiers in Behavioral Neuroscience, 3, 1–9.

    Article  Google Scholar 

  • Maestripieri, D. (1994). Infant abuse associated with psychosocial stress in a group-living pigtail macaque (Macaca nemestrina) mother. American Journal of Primatology, 32(1), 41–49.

    Article  Google Scholar 

  • Maestripieri, D. (2005). Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proceedings of the National Academy of Sciences of the USA, 102(27), 9726–9729.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maestripieri, D. (2007). Intergenerational transmission of maternal behavior in rhesus macaques and its underlying mechanisms. Developmental Psychobiology, 49(2), 165–171.

    Article  PubMed  Google Scholar 

  • Maestripieri, D. (2009). Maternal influences on offspring growth, reproduction, and behavior in Primates. In D. Maestripieri & J. M. Mateo (Eds.), Maternal effects in mammals (pp. 256–291). Chicago: The University of Chicago Press.

    Chapter  Google Scholar 

  • Maestripieri, D. (2011). Emotions, stress, and maternal motivation in primates. American Journal of Primatology, 73(6), 516–529.

    Article  PubMed  Google Scholar 

  • Maestripieri, D., & Carroll, K. (1998). Risk factors for infant abuse and neglect in group-living rhesus monkeys. Psychological Science, 9(2), 143–145.

    Article  Google Scholar 

  • Maestripieri, D., Hoffman, C. L., Anderson, G. M., Carter, C. S., & Higley, J. D. (2009). Mother-infant interactions in free-ranging rhesus macaques: Relationships between physiological and behavioral variables. Physiology & Behavior, 96(4–5), 613–619.

    Article  CAS  Google Scholar 

  • Magiakou, M., Mastorakos, G., Webster, E., & Chrousos, G. (1997). The hypothalamic‐pituitary‐adrenal axis and the female reproductive system. Annals of the New York Academy of Sciences, 816, 42–46.

    Article  CAS  PubMed  Google Scholar 

  • Markham, A. C., Santymire, R. M., Lonsdorf, E. V., Heintz, M. R., Lipende, I., & Murray, C. M. (2014). Rank effects on social stress in lactating chimpanzees. Animal Behaviour, 87, 195–202.

    Article  PubMed Central  PubMed  Google Scholar 

  • Mastorakos, G., & Ilias, I. (2003). Maternal and fetal hypothalamic-pituitary-adrenal axes during pregnancy and postpartum. Annals of the New York Academy of Sciences, 997(1), 136–149.

    Article  CAS  PubMed  Google Scholar 

  • McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43(1), 2–15.

    Article  PubMed  Google Scholar 

  • Muller, M. N., & Wrangham, R. W. (2004). Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behavioral Ecology and Sociobiology, 55(4), 332–340.

    Article  Google Scholar 

  • Murray, C. M., Heintz, M. R., Lonsdorf, E. V., Parr, L. A., & Santymire, R. M. (2013). Validation of a field technique and characterization of fecal glucocorticoid metabolite analysis in wild chimpanzees (Pan troglodytes). American Journal of Primatology, 8(1), 57–64.

    Article  Google Scholar 

  • Murray, C. M., Lonsdorf, E. V., Stanton, M. A., Wellens, K. R., Miller, J. A., Goodall, J., & Pusey, A. E. (2014). Social exposure in wild chimpanzees: Mothers with sons are more gregarious than mothers with daughters. Proceedings of the National Academy of Sciences USA, 111(51), 18189–18194.

    Article  CAS  Google Scholar 

  • Nguyen, N., Gesquiere, L. R., Wango, E. O., Alberts, S. C., & Altmann, J. (2008). Late pregnancy glucocorticoid levels predict responsiveness in wild baboon mothers (Papio cynocephalus). Animal Behaviour, 75(5), 1747–1756.

  • Nishida, T. (1968). The social group of wild chimpanzees in the Mahali mountains. Primates, 9, 167–224.

    Article  Google Scholar 

  • Nishida, T., Corp, N., Hamai, M., Hasegawa, T., Hiraiwa-Hasegawa, M., Hosaka, K., Hunt, K. D., Itoh, N., Kawanaka, K., Matsumoto-Oda, A., Mitani, J., Nakamura, M., Norikoshi, K., Sakamaki, T., Turner, L., Uehara, S., & Zamma, K. (2003). Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. American Journal of Primatology, 59(3), 99–121.

  • Numan, M. (2007). Motivational systems and the neural circuitry of maternal behavior in the rat. Developmental Psychobiology, 49, 165–171.

    Article  Google Scholar 

  • Nyberg, C. H. (2013). Navigating transitions in hypothalamic– pituitary–adrenal function from pregnancy through lactation: Implications for maternal health and infant brain development. In Building babies: Primate development in proximate and ultimate perspective (pp. 133–154). Developments in primatology: Progress and Prospects. New York: Springer Science+Business Media.

  • Obel, C., Hedegaard, M., Henriksen, T. B., Secher, N. J., Olsen, J., & Levine, S. (2005). Stress and salivary cortisol during pregnancy. Psychoneuroendocrinology, 30(7), 647–656.

    Article  CAS  PubMed  Google Scholar 

  • Pusey, A. (1990). Behavioural changes at adolescence in chimpanzees. Behaviour, 115(3), 203–246.

    Article  Google Scholar 

  • Pusey, A. E. (1983). Mother-offspring relationships in chimpanzees after weaning. Animal Behaviour, 31(2), 363–377.

    Article  Google Scholar 

  • Pusey, A. E.,Oehlert, G. W., Williams, J., and Goodall, J. 2005. Influence of ecological and social factors on body mass of wild chimpanzees. International Journal of Primatology 26, 3–31.

  • R Development Core Team. (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna Austria. http://www.R-project.org/.

  • Rees, S. L., Panesar, S., Steiner, M., & Fleming, A. S. (2004). The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Hormones and Behavior, 46(4), 411–419.

    Article  CAS  PubMed  Google Scholar 

  • Romero, L. M. (2004). Physiological stress in ecology: Lessons from biomedical research. Trends in Ecology & Evolution, 19(5), 249–255.

    Article  Google Scholar 

  • Romero, L. M., Dickens, M. J., & Cyr, N. E. (2009). The Reactive Scope Model – A new model integrating homeostasis, allostasis, and stress. Hormones and Behavior, 55(3), 375–389.

    Article  PubMed  Google Scholar 

  • Saltzman, W., & Abbott, D. (2009). Effects of elevated circulating cortisol concentrations on maternal behavior in common marmoset monkeys (Callithrix jacchus). Psychoneuroendocrinology, 34(8), 1222–1234.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Saltzman, W., & Maestripieri, D. (2011). The neuroendocrinology of primate maternal behavior. Progress in Neuropsychopharmacology and Biological Psychiatry, 35(5), 1192–1204.

    Article  CAS  Google Scholar 

  • Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308(5722), 648–652.

    Article  CAS  PubMed  Google Scholar 

  • Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and perparative actions. Endocrine Reviews, 21(1), 55–89.

    CAS  PubMed  Google Scholar 

  • Schino, G., Speranza, L., & Troisi, A. (2001). Early maternal rejection and later social anxiety in juvenile and adult Japanese macaques. Developmental Psychobiology, 38, 186–190.

    Article  CAS  PubMed  Google Scholar 

  • Shumway, R. H., & Stoffer, D. S. (2011). Time series analyses and its applications (3rd ed.). London: Springer Science+Business Media.

    Book  Google Scholar 

  • Sloboda, D., Moss, T. J., Newnham, J., & Challis, J. R. (2005). Fetal HPA activation, preterm birth, and postnatal programming. In M. Power & J. Schulkin (Eds.), Birth, distress, and disease: Placenta-brain interactions. Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Smith, A., & Wang, Z. (2012). Salubrious effects of oxytocin on social stress-induced deficits. Hormones and Behavior, 61(3), 320–330.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smith, R., Wickings, E. J., Bowman, M. E., Belleoud, A., Dubreuil, G., Davies, J. J., & Madsen, G. (1999). Corticotropin-releasing hormone in chimpanzee and gorilla pregnancies. The Journal of Clinical Endocrinology and Metabolism, 84(8), 2820–2825.

    Article  CAS  PubMed  Google Scholar 

  • Sullivan, E., & Hinde, K. (2011). Cortisol concentrations in the milk of rhesus monkey mothers are associated with confident temperament in sons, but not daughters. Developmental Psychobiology, 53(1), 96–104.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Surbeck, M., Deschner, T., Weltring, A., & Hohmann, G. (2012). Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus). Hormones and Behavior, 62(1), 27–35.

    Article  CAS  PubMed  Google Scholar 

  • Tamashiro, K. L. K., Nguyen, M. M. N., & Sakai, R. R. (2005). Social stress: From rodents to primates. Frontiers in Neuroendocrinology, 26(1), 27–40.

    Article  PubMed  Google Scholar 

  • Taylor, C. A., Guterman, N. B., Lee, S. J., & Rathouz, P. J. (2009). Intimate partner violence, maternal stress, nativity, and risk for maternal maltreatment of young children. American Journal of Public Health, 99(1), 175–183.

    Article  PubMed Central  PubMed  Google Scholar 

  • Trivers, R. (1974). Parent-offspring conflict. Americal Zoologist, 14, 249–264.

    Google Scholar 

  • Trivers, R., & Willard, D. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science, 179, 90–92.

    Article  CAS  PubMed  Google Scholar 

  • Troisi, A. (2002). Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. Stress, 5(1), 47–54.

    Article  PubMed  Google Scholar 

  • van de Rijt-Plooij, H., & Plooij, F. (1987). Growing independence, conflict and learning in mother-infant relations in free-ranging chimpanzees. Behaviour, 101(1), 1–86.

    Article  Google Scholar 

  • Walker, C. D. (2010). Maternal touch and feed as critical regulators of behavioral and stress responses in the offspring. Developmental Psychobiology, 52(7), 638–650.

    Article  PubMed  Google Scholar 

  • Windle, R. J., Kershaw, Y. M., Shanks, N., Wood, S. A., Lightman, S. L., & Ingram, C. D. (2004). Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. The Journal of Neuroscience, 24(12), 2974–2982.

    Article  CAS  PubMed  Google Scholar 

  • Wingfield, J. C. (2005). The concept of allostasis: Coping with a capricious environment. Journal of Mammalogy, 86(2), 248–254.

    Article  Google Scholar 

  • Wroblewski, E. E., Murray, C. M., Keele, B. F., Schumacher-Stankey, J. C., Hahn, B. H., & Pusey, A. E. (2009). Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Animal Behaviour, 77(4), 873–885.

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Tanzania National Parks, the Tanzania Wildlife Research Institute, and the Tanzanian Commission for Science and Technology for granting us permission to work in Gombe National Park. We also thank the Jane Goodall Institute for funding long-term research and the Gombe Stream Research Centre staff including J. Mazogo, M. Yahaya, S. Mpindu, B. Daniel, and C. Mpongo for maintaining data collection. This work was supported by grants from the National Institutes of Health (R00HD057992), the Leo S. Guthman Foundation, the National Geographic Society, and grants to M. Heintz (NSFGRF, Leakey Foundation, Werner-Gren, Foundation, and Field Museum African Council). Finally, we thank V. Fiorentio, S. Reji, and K. Anderson for data management; D. Armstrong for lab assistance; all of the assistants who participated in data entry; C. Markham for helpful discussions; and two anonymous reviewers for their comments on the manuscript.

Author information

Authors and Affiliations

  1. Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC, 20052, USA

    Margaret A. Stanton & Carson M. Murray

  2. Department of Conservation and Science, Lincoln Park Zoo, Chicago, Illinois, 60614, USA

    Matthew R. Heintz & Rachel M. Santymire

  3. Committee on Evolutionary Biology, University of Chicago, Chicago, Illinois, 60637, USA

    Matthew R. Heintz & Rachel M. Santymire

  4. Department of Psychology, Franklin and Marshall College, Lancaster, Pennsylvania, 17604, USA

    Elizabeth V. Lonsdorf

  5. Gombe Stream Research Centre, Gombe, Tanzania

    Iddi Lipende

Authors
  1. Margaret A. Stanton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew R. Heintz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elizabeth V. Lonsdorf
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rachel M. Santymire
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Iddi Lipende
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Carson M. Murray
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Margaret A. Stanton.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stanton, M.A., Heintz, M.R., Lonsdorf, E.V. et al. Maternal Behavior and Physiological Stress Levels in Wild Chimpanzees (Pan troglodytes schweinfurthii). Int J Primatol 36, 473–488 (2015). https://doi.org/10.1007/s10764-015-9836-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-015-9836-2

Keywords

Search

Navigation