Skip to main content Accessibility help
×
Hostname: page-component-848d4c4894-nr4z6 Total loading time: 0 Render date: 2024-05-01T07:10:24.724Z Has data issue: false hasContentIssue false

21 - Group-specific social dynamics affect urinary oxytocin levels in Taï male chimpanzees

Published online by Cambridge University Press:  25 November 2019

Christophe Boesch
Affiliation:
Max-Planck-Institut für Evolutionäre Anthropologie, Germany
Roman Wittig
Affiliation:
Max-Planck-Institut für Evolutionäre Anthropologie, Germany
Catherine Crockford
Affiliation:
Max-Planck-Institut für Evolutionäre Anthropologie, Germany
Linda Vigilant
Affiliation:
Max-Planck-Institut für Evolutionäre Anthropologie, Germany
Tobias Deschner
Affiliation:
Max-Planck-Institut für Evolutionäre Anthropologie, Germany
Fabian Leendertz
Affiliation:
Robert Koch-Institut, Germany
Get access

Summary

Examining variation in social behaviour and associated endocrine physiology across groups of the same species can help identify consistent hormone–behaviour interactions. We investigated differences in urinary oxytocin levels of individuals, of two neighbouring chimpanzee groups related to (a) socio-positive and -negative interaction frequencies, (b) within-group cooperation associated with between-group competition and (c) group-specific differences in urinary oxytocin reactivity of individuals in response to the same behavioural contexts. We found higher rates of cooperative group-level behaviours and larger relative party sizes in East Group males, while South Group males had higher non-directed aggression and copulation rates. Individuals of both groups showed consistent urinary oxytocin reactivity after the same behavioural contexts. However, East Group males had higher urinary oxytocin levels across contexts than South Group males, including higher baseline levels. Our results support the oxytocinergic system’s involvement in cooperation and gregariousness, and suggest an association between group-specific social dynamics and oxytocinergic profiles.

Type
Chapter
Information
The Chimpanzees of the Taï Forest
40 Years of Research
, pp. 339 - 365
Publisher: Cambridge University Press
Print publication year: 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227266. https://doi.org/10.1163/156853974X00534Google Scholar
Altmann, J. & Muruthi, P. (1988). Differences in daily life between semiprovisioned and wild-feeding baboons. American Journal of Primatology, 15, 213221. https://doi.org/10.1002/ajp.1350150304Google Scholar
Amico, J. A., Ulbrecht, J. S. & Robinson, A. G. (1987). Clearance studies of oxytocin in humans using radioimmunoassay measurements of the hormone in plasma and urine. The Journal of Clinical Endocrinology & Metabolism, 64, 340345. https://doi.org/10.1210/jcem-64–2–340CrossRefGoogle ScholarPubMed
Anacker, A. M. J. & Beery, A. K. (2013). Life in groups: the roles of oxytocin in mammalian sociality. Frontiers in Behavioral Neuroscience, 7, 185. https://doi.org/10.3389/fnbeh.2013.00185Google Scholar
Anderson, D. P., Nordheim, E. V., Boesch, C. & Moermond, T. C. (2002). Factors influencing fissionfusion grouping in chimpanzees in the Taï National Park, Côte d’Ivoire. In Boesch, C., Hohmann, G. & Marchant, L. F. (eds.), Behavioural Diversity in Chimpanzees and Bonobos (pp. 90101). Cambridge: Cambridge University Press.Google Scholar
Anestis, S. F. (2010). Hormones and social behavior in primates. Evolutionary Anthropology, 19, 6678. https://doi.org/10.1002/evan.20253Google Scholar
Aureli, F., Cords, M. & van Schaik, C. P. (2002). Conflict resolution following aggression in gregarious animals: A predictive framework. Animal Behaviour, 64, 325343. https://doi.org/10.1006/anbe.2002.3071CrossRefGoogle Scholar
Baayen, R. H. (2008). Analyzing Linguistic Data: A Practical Introduction to Statistics using R. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Bahr, N. I., Palme, R., Möhle, U., Hodges, J. K. & Heistermann, M. (2000). Comparative aspects of the metabolism and excretion of cortisol in three individual nonhuman primates. General and Comparative Endocrinology, 117, 427438. https://doi.org/10.1006/gcen.1999.7431CrossRefGoogle Scholar
Barr, D. J., Levy, R., Scheepers, C. & Tily, H. J. (2013). Random effects structure for confirmatory hypothesis testing: Keep it maximal. Journal of Memory and Language, 68, 255278. https://doi.org/10.1016/j.jml.2012.11.001CrossRefGoogle ScholarPubMed
Bates, D., Mächler, M., Bolker, B. & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(i01).CrossRefGoogle Scholar
Becker, J. B. (2002). Behavioral Endocrinology. Cambridge, MA: MIT Press.Google Scholar
Beehner, J. C. & Bergman, T. J. (2017). The next step for stress research in primates: To identify relationships between glucocorticoid secretion and fitness. Hormones and Behavior, 91, 6883. https://doi.org/10.1016/j.yhbeh.2017.03.003CrossRefGoogle ScholarPubMed
Boesch, C. (2003). Is culture a golden barrier between human and chimpanzee? Evolutionary Anthropology, 12, 8291. https://doi.org/10.1002/evan.10106CrossRefGoogle Scholar
Boesch, C. & Boesch-Achermann, H. (2000). The Chimpanzees of the Taï Forest: Behavioural Ecology and Evolution. Oxford: Oxford University Press.Google Scholar
Bosch, O. J., Meddle, S. L., Beiderbeck, D. I., Douglas, A. J. & Neumann, I. D. (2005). Brain oxytocin correlates with maternal aggression: Link to anxiety. Journal of Neuroscience, 25, 68076815. https://doi.org/10.1523/JNEUROSCI.1342–05.2005Google Scholar
Bretz, F., Hothorn, T. & Westfall, P. (2016). Multiple Comparisons Using R. London: CRC Press.CrossRefGoogle Scholar
Carter, C. S. (1998). Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology, 23, 779818. https://doi.org/10.1016/S0306–4530(98)00055–9CrossRefGoogle ScholarPubMed
Chang, S. W. C., Brent, L. J. N., Adams, G. K., Klein, J. T., Pearson, J. M., Watson, K. K., et al. (2013). Neuroethology of primate social behavior. Proceedings of the National Academy of Sciences of the United States of America, 110, 10,38710,394. https://doi.org/10.1073/Proceedings of the National Academy of Sciences of the United States of America.1301213110Google Scholar
Cheney, D. L. (1992). Intragroup cohesion and intergroup hostility: The relation between grooming distributions and intergroup competition among female primates. Behavioral Ecology, 3, 334345. https://doi.org/10.1093/beheco/3.4.334CrossRefGoogle Scholar
Cohen, J., Cohen, P., West, S. G. & Aiken, L. S. (2013). Statistical inference strategy in multiple regression/correlation. In Pituch, K. A. & Stevens, J. P. (eds.), Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences (pp. 182189). Abingdon: Routledge.CrossRefGoogle Scholar
Cords, M. (1992). Post-conflict reunions and reconciliation in long-tailed macaques. Animal Behaviour, 44, 5761. https://doi.org/10.1016/S0003–3472(05)80754–7Google Scholar
Crespi, B. J. (2016). Oxytocin, testosterone, and human social cognition: Oxytocin and social behavior. Biological Reviews, 91, 390408. https://doi.org/10.1111/brv.12175Google 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, 280(1755), 20122765. https://doi.org/10.1098/rspb.2012.2765Google Scholar
Das, M., Penke, Z. & van Hooff, J. A. R. A. M. (1998). Postconflict affiliation and stress-related behavior of long-tailed macaque aggressors. International Journal of Primatology, 19, 5371. https://doi.org/10.1023/A:1020354826422Google Scholar
De Dreu, C. K. W. (2012). Oxytocin modulates cooperation within and competition between groups: An integrative review and research agenda. Hormones and Behavior, 61, 419428. https://doi.org/10.1016/j.yhbeh.2011.12.009CrossRefGoogle ScholarPubMed
De Dreu, C. K. W., Greer, L. L., Handgraaf, M. J. J., Shalvi, S., Van Kleef, G. A., Baas, M., et al. (2010). The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science, 328(5984), 14081411. https://doi.org/10.1126/science.1189047Google Scholar
de Jong, T. R., Beiderbeck, D. I. & Neumann, I. D. (2014). Measuring virgin female aggression in the Female Intruder Test (FIT): Effects of oxytocin, estrous cycle, and anxiety. PLoS ONE, 9(3), e91701. https://doi.org/10.1371/journal.pone.0091701Google Scholar
de Jong, T.R. & Neumann, I.D. (2017). Oxytocin and Aggression. Berlin: Springer. https://doi.org/10.1007/7854_2017_13CrossRefGoogle Scholar
de Waal, F. B. M. (1982). Chimpanzee Politics: Power and Sex Among Apes. Baltimore: Johns Hopkins University Press.Google Scholar
Deschner, T. & Boesch, C. (2007). Can the patterns of sexual swelling cycles in female Taï chimpanzees be explained by the cost-of-sexual-attraction hypothesis? International Journal of Primatology, 28, 389406. https://doi.org/10.1007/s10764-007–9120–1Google Scholar
Dobson, A. J. & Barnett, A. (2008). An Introduction to Generalized Linear Models. London: CRC Press.CrossRefGoogle Scholar
Donaldson, Z. R. & Young, L. J. (2008). Oxytocin, vasopressin, and the neurogenetics of sociality. Science, 322(5903), 900904. https://doi.org/10.1126/science.1158668CrossRefGoogle ScholarPubMed
Eckstein, M., Scheele, D., Weber, K., Stoffel-Wagner, B., Maier, W. & Hurlemann, R. (2014). Oxytocin facilitates the sensation of social stress: Oxytocin and social stress. Human Brain Mapping, 35, 47414750. https://doi.org/10.1002/hbm.22508CrossRefGoogle ScholarPubMed
Engh, A. L., Beehner, J. C., Bergman, T. J., Whitten, P. L., Hoffmeier, R. R., Seyfarth, R. M., et al. (2006). Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proceedings of the Royal Society B, 273(1587), 707712. https://doi.org/10.1098/rspb.2005.3378Google Scholar
Ferris, C. F., Foote, K. B., Meltser, H. M., Plenby, M. G., Smith, K. L. & Insel, T. R. (1992). Oxytocin in the amygdala facilitates maternal aggression. Annals of the New York Academy of Sciences, 652, 456457. https://doi.org/10.1111/j.1749–6632.1992.tb34382.xCrossRefGoogle ScholarPubMed
Field, A. (2009). Discovering Statistics using SPSS. New York: Sage.Google Scholar
Finkenwirth, C., Martins, E., Deschner, T. & Burkart, J.M. (2016). Oxytocin is associated with infant-care behavior and motivation in cooperatively breeding marmoset monkeys. Hormones and Behavior, 80, 1018. https://doi.org/10.1016/j.yhbeh.2016.01.008Google Scholar
Forstmeier, W. & Schielzeth, H. (2011). Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner’s curse. Behavioral Ecology and Sociobiology, 65, 4755. https://doi.org/10.1007/s00265-010–1038–5Google Scholar
Fox, J. & Weisberg, S. (2011). An R Companion to Applied Regression. New York: Sage.Google Scholar
French, J. A., Cavanaugh, J., Mustoe, A. C., Carp, S. B. & Womack, S. L. (2018). Social monogamy in nonhuman primates: Phylogeny, phenotype, and physiology. The Journal of Sex Research, 55, 410434. https://doi.org/10.1080/00224499.2017.1339774CrossRefGoogle ScholarPubMed
Gachter, S. & Herrmann, B. (2009). Reciprocity, culture and human cooperation: Previous insights and a new cross-cultural experiment. Philosophical Transactions of the Royal Society B, 364(1518), 791806. https://doi.org/10.1098/rstb.2008.0275Google Scholar
Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, MA: The Belknap Press of Harvard University Press.Google Scholar
Goodson, J. L. (2013). Deconstructing sociality, social evolution and relevant nonapeptide functions. Psychoneuroendocrinology, 38, 465478. https://doi.org/10.1016/j.psyneuen.2012.12.005Google Scholar
Goodson, J. L., Schrock, S. E., Klatt, J. D., Kabelik, D. & Kingsbury, M. A. (2009). Mesotocin and nonapeptide receptors promote estrildid flocking behavior. Science, 325(5942), 862866. https://doi.org/10.1126/science.1174929CrossRefGoogle ScholarPubMed
Grewen, K. M., Girdler, S. S., Amico, J. & Light, K. C. (2005). Effects of partner support on resting oxytocin, cortisol, norepinephrine, and blood pressure before and after warm partner contact: Psychosomatic Medicine, 67, 531538. https://doi.org/10.1097/01.psy.0000170341.88395.47Google Scholar
Grillon, C., Krimsky, M., Charney, D. R., Vytal, K., Ernst, M. & Cornwell, B. (2013). Oxytocin increases anxiety to unpredictable threat. Molecular Psychiatry, 18, 958960. https://doi.org/10.1038/mp.2012.156CrossRefGoogle ScholarPubMed
Grueter, C. C. (2013). No effect of inter-group conflict on within-group harmony in non-human primates. Communicative & Integrative Biology, 6(6), e26801. https://doi.org/10.4161/cib.26801Google Scholar
Gurven, M., Zanolini, A. & Schniter, E. (2008). Culture sometimes matters: Intra-cultural variation in pro-social behavior among Tsimane Amerindians. Journal of Economic Behavior & Organization, 67, 587607. https://doi.org/10.1016/j.jebo.2007.09.005Google Scholar
Hamilton, W. D. (1972). Altruism and related phenomena, mainly in social insects. Annual Review of Ecology and Systematics, 3, 193232.CrossRefGoogle Scholar
Hamilton, W. D. (1975). Innate social aptitudes of man: An approach from evolutionary genetics. Biosocial Anthropology, 53, 133155.Google Scholar
Heinrichs, M., Baumgartner, T., Kirschbaum, C. & Ehlert, U. (2003). Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biological Psychiatry, 54, 13891398. https://doi.org/10.1016/S0006–3223(03)00465–7CrossRefGoogle ScholarPubMed
Henrich, J., Boyd, R., Bowles, S., Camerer, C., Fehr, E., Gintis, H., et al. (2005). ‘Economic man’ in cross-cultural perspective: Behavioral experiments in 15 small-scale societies. Behavioral and Brain Sciences, 28, 795815. https://doi.org/10.1017/S0140525X05000142Google Scholar
Hobaiter, C., Samuni, L., Mullins, C., Akankwasa, W. J. & Zuberbühler, K. (2017). Variation in hunting behaviour in neighbouring chimpanzee communities in the Budongo forest, Uganda. PLoS ONE, 12(6), e0178065. https://doi.org/10.1371/journal.pone.0178065Google Scholar
Insel, T. R. & Young, L. J. (2001). The neurobiology of attachment. Nature Reviews Neuroscience, 2, 129136. https://doi.org/10.1038/35053579Google Scholar
Kaburu, S. S. K., Inoue, S. & Newton-Fisher, N. E. (2013). Death of the alpha: Within-community lethal violence among chimpanzees of the Mahale Mountains National Park: Coalitional lethal violence in chimpanzees. American Journal of Primatology, 75, 789797. https://doi.org/10.1002/ajp.22135Google Scholar
Kaburu, S. S. K. & Newton-Fisher, N. E. (2015). Trading or coercion? Variation in male mating strategies between two communities of East African chimpanzees. Behavioral Ecology and Sociobiology, 69, 10391052. https://doi.org/10.1007/s00265-015–1917–xGoogle Scholar
Keebaugh, A. C. & Young, L. J. (2011). Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults. Hormones and Behavior, 60, 498504. https://doi.org/10.1016/j.yhbeh.2011.07.018Google Scholar
Kendrick, K. M., da Costa, A. P., Hinton, M. R. & Keverne, E. B. (1992). A simple method for fostering lambs using anoestrous ewes with artificially induced lactation and maternal behaviour. Applied Animal Behaviour Science, 34, 345357. https://doi.org/10.1016/S0168–1591(05)80094–2Google Scholar
Koyama, N. F., Ronkainen, K. & Aureli, F. (2017). Durability and flexibility of chimpanzee grooming patterns during a period of dominance instability. American Journal of Primatology, 79(11), e22713. https://doi.org/10.1002/ajp.22713CrossRefGoogle ScholarPubMed
Laland, K. & Janik, V. (2006). The animal cultures debate. Trends in Ecology & Evolution, 21, 542547. https://doi.org/10.1016/j.tree.2006.06.005Google Scholar
Lamba, S. & Mace, R. (2011). Demography and ecology drive variation in cooperation across human populations. Proceedings of the National Academy of Sciences of the United States of America, 108, 14,42614,430. https://doi.org/10.1073/Proceedings of the National Academy of Sciences of the United States of America.1105186108Google Scholar
Langergraber, K. E., Boesch, C., Inoue, E., Inoue-Murayama, M., Mitani, J. C., Nishida, T., et al. (2011). Genetic and ‘cultural’ similarity in wild chimpanzees. Proceedings of the Royal Society B, 278(1704), 408416. https://doi.org/10.1098/rspb.2010.1112CrossRefGoogle ScholarPubMed
Lukas, M., Toth, I., Reber, S. O., Slattery, D. A., Veenema, A. H. & Neumann, I. D. (2011). The neuropeptide oxytocin facilitates pro-social behavior and prevents social avoidance in rats and mice. Neuropsychopharmacology, 36, 21592168. https://doi.org/10.1038/npp.2011.95CrossRefGoogle ScholarPubMed
Luncz, L. V. & Boesch, C. (2015). The extent of cultural variation between adjacent chimpanzee (Pan troglodytes verus) communities; A microecological approach. American Journal of Physical Anthropology, 156, 6775. https://doi.org/10.1002/ajpa.22628Google Scholar
Luncz, L. V., Mundry, R. & Boesch, C. (2012). Evidence for cultural differences between neighboring chimpanzee communities. Current Biology, 22, 922926. https://doi.org/10.1016/j.cub.2012.03.031Google Scholar
Madden, J. R. & Clutton-Brock, T. H. (2011). Experimental peripheral administration of oxytocin elevates a suite of cooperative behaviours in a wild social mammal. Proceedings of the Royal Society B, 278(1709), 11891194. https://doi.org/10.1098/rspb.2010.1675Google Scholar
Majolo, B., de Bortoli Vizioli, A. & Lehmann, J. (2016). The effect of intergroup competition on intragroup affiliation in primates. Animal Behaviour, 114, 1319.Google Scholar
Markham, A. C., Gesquiere, L. R., Alberts, S. C. & Altmann, J. (2015). Optimal group size in a highly social mammal. Proceedings of the National Academy of Sciences of the United States of America, 112, 14,88214,887. https://doi.org/10.1073/Proceedings of the National Academy of Sciences of the United States of America.1517794112Google Scholar
Marler, P. & Tamura, M. (1962). Song ‘dialects’ in three populations of white-crowned sparrows. The Condor, 64, 368377. https://doi.org/10.2307/1365545Google Scholar
McCullagh, P. & Nelder, J. A. (1989). Generalized Linear Models. London: Chapman and Hall.CrossRefGoogle Scholar
McEwen, B. S. & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43, 215. https://doi.org/10.1016/S0018-506X(02)00024–7Google Scholar
Mitani, J. C., Watts, D. P. & Lwanga, J. S. (2002). Ecological and social correlates of chimpanzee party size and composition. In Boesch, C., Hohmann, G. & Marchant, L. (eds.), Behavioural Diversity in Chimpanzees and Bonobos (pp. 102111). Cambridge: Cambridge University Press.Google Scholar
Muller, M. N. (2002). Agonistic relations among Kanyawara chimpanzees. In Boesch, C., Hohmann, G. & Marchant, L. (eds.), Behavioural Diversity in Chimpanzees and Bonobos (pp. 112124). Cambridge:Cambridge University Press. https://doi.org/10.1017/CBO9780511606397.012CrossRefGoogle Scholar
Muller, M. N., Thompson, M. E. & Wrangham, R. W. (2006). Male chimpanzees prefer mating with old females. Current Biology, 16, 22342238. https://doi.org/10.1016/j.cub.2006.09.042Google Scholar
Muller, M. N. & Wrangham, R. W. (2004). Dominance, aggression and testosterone in wild chimpanzees: A test of the ‘challenge hypothesis’. Animal Behaviour, 67, 113123. https://doi.org/10.1016/j.anbehav.2003.03.013Google Scholar
Nettle, D., Colléony, A. & Cockerill, M. (2011). Variation in cooperative behaviour within a single city. PLoS ONE, 6(10), e26922. https://doi.org/10.1371/journal.pone.0026922CrossRefGoogle ScholarPubMed
Nettle, D., Pepper, G. V., Jobling, R. & Schroeder, K. B. (2014). Being there: A brief visit to a neighbourhood induces the social attitudes of that neighbourhood. PeerJ, 2, e236. https://doi.org/10.7717/peerj.236Google Scholar
Neumann, I. D. & Landgraf, R. (2012). Balance of brain oxytocin and vasopressin: Implications for anxiety, depression, and social behaviors. Trends in Neurosciences, 35, 649659. https://doi.org/10.1016/j.tins.2012.08.004Google Scholar
Nishida, T., Kano, T., Goodall, J., McGrew, W. C. & Nakamura, M. (1999). Ethogram and ethnography of Mahale chimpanzees. Anthropological Science, 107, 141188.Google Scholar
Preis, A., Samuni, L., Mielke, A., Deschner, T., Crockford, C. & Wittig, R. M. (2018). Urinary oxytocin levels in relation to post-conflict affiliations in wild male chimpanzees (Pan troglodytes verus). Hormones and Behavior, 105, 2840. https://doi.org/10.1016/j.yhbeh.2018.07.009Google Scholar
Pride, R. E. (2005). Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta). Behavioral Ecology, 16, 550560. https://doi.org/10.1093/beheco/ari025CrossRefGoogle Scholar
R Core Team. (2016). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Radke, S., Volman, I., Kokal, I., Roelofs, K., de Bruijn, E. R. A. & Toni, I. (2017). Oxytocin reduces amygdala responses during threat approach. Psychoneuroendocrinology,79, 160166. https://doi.org/10.1016/j.psyneuen.2017.02.028Google Scholar
Raouf, S. A., Smith, L. C., Brown, M. B., Wingfield, J. C. & Brown, C. R. (2006). Glucocorticoid hormone levels increase with group size and parasite load in cliff swallows. Animal Behaviour, 71, 3948. https://doi.org/10.1016/j.anbehav.2005.03.027Google Scholar
Reeve, H. K. & Holldobler, B. (2007). The emergence of a superorganism through intergroup competition. Proceedings of the National Academy of Sciences of the United States of America, 104, 97369740. https://doi.org/10.1073/Proceedings of the National Academy of Sciences of the United States of America.0703466104CrossRefGoogle ScholarPubMed
Romero, T., Onishi, K. & Hasegawa, T. (2016). The role of oxytocin on peaceful associations and sociality in mammals. Behaviour, 153, 10531071. https://doi.org/10.1163/1568539X–00003358Google Scholar
Ross, H. E., Cole, C. D., Smith, Y., Neumann, I. D., Landgraf, R., Murphy, A. Z., et al. (2009). Characterization of the oxytocin system regulating affiliative behavior in female prairie voles. Neuroscience, 162, 892903. https://doi.org/10.1016/j.neuroscience.2009.05.055CrossRefGoogle ScholarPubMed
Ross, H. E. & Young, L. J. (2009). Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Frontiers in Neuroendocrinology, 30, 534547. https://doi.org/10.1016/j.yfrne.2009.05.004Google Scholar
Samuni, L., Preis, A., Mundry, R., Deschner, T., Crockford, C. & Wittig, R. M. (2017). Oxytocin reactivity during intergroup conflict in wild chimpanzees. Proceedings of the National Academy of Sciences of the United States of America, 114, 268273. https://doi.org/10.1073/Proceedings of the National Academy of Sciences of the United States of America.1616812114Google Scholar
Sapolsky, R. M. (1983). Endocrine aspects of social instability in the olive baboon (Papio anubis). American Journal of Primatology, 5, 365379. https://doi.org/10.1002/ajp.1350050406Google Scholar
Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308(5722), 648652. https://doi.org/10.1126/science.1106477Google Scholar
Sapolsky, R. M. (2011). Physiological and pathophysiological implications of social stress in mammals. In Terjung, R. (ed.), Comprehensive Physiology. Hoboken, NJ: John Wiley & Sons, Inc. https://doi.org/10.1002/cphy.cp070423Google Scholar
Sapolsky, R. M. (2006). Social cultures among nonhuman primates. Current Anthropology, 47, 641656. https://doi.org/10.1086/504162Google Scholar
Sapolsky, R. M., Romero, L. M. & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21, 5589. https://doi.org/10.1210/edrv.21.1.0389Google Scholar
Sapolsky, R. M. & Share, L. J. (2004). A Pacific culture among wild baboons: Its emergence and transmission. PLoS Biology, 2(4), e106. https://doi.org/10.1371/journal.pbio.0020106CrossRefGoogle ScholarPubMed
Schielzeth, H. (2010). Simple means to improve the interpretability of regression coefficients: Interpretation of regression coefficients. Methods in Ecology and Evolution, 1, 103113. https://doi.org/10.1111/j.2041-210X.2010.00012.xGoogle Scholar
Schielzeth, H. & Forstmeier, W. (2009). Conclusions beyond support: Overconfident estimates in mixed models. Behavioral Ecology, 20, 416420. https://doi.org/10.1093/beheco/arn145Google Scholar
Seltzer, L. J., Ziegler, T. E. & Pollak, S. D. (2010). Social vocalizations can release oxytocin in humans. Proceedings of the Royal Society B, 277(1694), 26612666. https://doi.org/10.1098/rspb.2010.0567CrossRefGoogle ScholarPubMed
Shamay-Tsoory, S. G. & Abu-Akel, A. (2016). The social salience hypothesis of oxytocin. Biological Psychiatry, 79, 194202. https://doi.org/10.1016/j.biopsych.2015.07.020CrossRefGoogle ScholarPubMed
Smith, A. S. & Wang, Z. (2014). Hypothalamic oxytocin mediates social buffering of the stress response. Biological Psychiatry, 76, 281288. https://doi.org/10.1016/j.biopsych.2013.09.017CrossRefGoogle ScholarPubMed
Snowdon, C. T., Pieper, B. A., Boe, C. Y., Cronin, K. A., Kurian, A. V. & Ziegler, T. E. (2010). Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins. Hormones and Behavior, 58, 614618. https://doi.org/10.1016/j.yhbeh.2010.06.014Google Scholar
Striepens, N., Scheele, D., Kendrick, K. M., Becker, B., Schafer, L., Schwalba, K., et al. (2012). Oxytocin facilitates protective responses to aversive social stimuli in males. Proceedings of the National Academy of Sciences of the United States of America, 109, 18,14418,149. https://doi.org/10.1073/Proceedings of the National Academy of Sciences of the United States of America.1208852109Google Scholar
Tooby, J. & Cosmides, L. (1988). The evolution of war and its cognitive foundations. Institute for Evolutionary Studies Technical Report, 88(1), 115.Google Scholar
Trainor, B. C., Takahashi, E. Y., Silva, A. L., Crean, K. K. & Hostetler, C. (2010). Sex differences in hormonal responses to social conflict in the monogamous California mouse. Hormones and Behavior, 58, 506512. https://doi.org/10.1016/j.yhbeh.2010.04.008Google Scholar
Uehara, S. (1982). Seasonal changes in the techniques employed by wild chimpanzees in the Mahale Mountains, Tanzania, to feed on termites (Pseudacanthotermes spiniger). Folia Primatologica, 37,4476. https://doi.org/10.1159/000156020Google Scholar
Uvnäs-Moberg, K. (1998). Oxytocin may mediate the benefits of positive social interaction and emotions. Psychoneuroendocrinology, 23, 819835. https://doi.org/10.1016/S0306–4530(98)00056–0Google Scholar
Van Parijs, S. M., Hastie, G. D. & Thompson, P. M. (2000). Individual and geographical variation in display behaviour of male harbour seals in Scotland. Animal Behaviour, 59, 559568. https://doi.org/10.1006/anbe.1999.1307CrossRefGoogle Scholar
van Schaik, C. P. (2003). Orangutan cultures and the evolution of material culture. Science, 299(5603), 102105. https://doi.org/10.1126/science.1078004Google Scholar
Weilgart, L. & Whitehead, H. (1997). Group-specific dialects and geographical variation in coda repertoire in South Pacific sperm whales. Behavioral Ecology and Sociobiology, 40, 277285. https://doi.org/10.1007/s002650050343Google Scholar
Whiten, A., Goodall, J., McGrew, W., Nishida, T., Reynolds, V., Sugiyama, Y., et al. (1999). Cultures in chimpanzee. Nature, 399, 682685. https://doi.org/10.1038/21415Google Scholar
Williams, J. M., Oehlert, G. W., Carlis, J. V. & Pusey, A. E. (2004). Why do male chimpanzees defend a group range? Animal Behaviour, 68, 523532. https://doi.org/10.1016/j.anbehav.2003.09.015Google Scholar
Williams, J. R., Insel, T. R., Harbaugh, C. R. & Carter, C. S. (1994). Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). Journal of Neuroendocrinology, 6, 247250. https://doi.org/10.1111/j.1365–2826.1994.tb00579.xGoogle Scholar
Wittig, R. M. & Boesch, C. (2003a). ‘Decision-making’ in conflicts of wild chimpanzees (Pan troglodytes): An extension of the Relational Model. Behavioral Ecology and Sociobiology, 54, 491504. https://doi.org/10.1007/s00265-003–0654–8Google Scholar
Wittig, R. M. & Boesch, C. (2003b). The choice of post-conflict interactions in wild chimpanzees (Pan troglodytes). Behaviour, 140, 15271559. https://doi.org/10.1163/156853903771980701Google Scholar
Wittig, R. M. & Boesch, C. (2005). How to repair relationships – Reconciliation in wild chimpanzees (Pan troglodytes). Ethology, 111, 736763. https://doi.org/10.1111/j.1439–0310.2005.01093.xGoogle Scholar
Wittig, R. M., Crockford, C., Deschner, T., Langergraber, K. E., Ziegler, T. E. & Zuberbühler, K. (2014). Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees. Proceedings of the Royal Society B, 281(1778), 20133096. https://doi.org/10.1098/rspb.2013.3096Google Scholar
Wittiger, L. & Boesch, C. (2013). Female gregariousness in Western Chimpanzees (Pan troglodytes verus) is influenced by resource aggregation and the number of females in estrus. Behavioral Ecology and Sociobiology, 67, 10971111.CrossRefGoogle Scholar
Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262300. https://doi.org/10.1163/156853980X00447Google Scholar
Wrangham, R. W. (2002). The cost of sexual attraction: is there a trade-off in female Pan between sex appeal and received coercion. In Boesch, C., Hohmann, G. & Marchant, L. (eds.), Behavioural Diversity in Chimpanzees and Bonobos (pp. 204–12). Cambridge: Cambridge University Press.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×