Oxytocin reduces food sharing in capuchin monkeys by modulating social distance
In: BehaviourRecent evidence indicates that oxytocin plays an important role in promoting prosocial behaviour amongst humans and other species. We tested whether oxytocin affected cooperation and food-sharing in capuchin monkeys, a highly cooperative New World primate. Subjects received either 2IU oxytocin or an inert adjuvent intranasally prior to each session. Oxytocin influenced food sharing in capuchins in ways we did not anticipate. Recipients were less likely to passively acquire food from possessors when either individual had received OT than in the control, and also spent less time in proximity to their partner. Passive food sharing requires proximity, and oxytocin decreased the capuchins’ typical congregating behaviour, apparently resulting in decreased sharing. We propose that the likely mechanism for increased social distance is the known anxiolytic effect of oxytocin. Our results indicate a need to consider how oxytocin affects the context of interactions and interacts with modes of sociality unique to each species.
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Bales K., Perkeybile A., Conley O., Lee M., Guoynes C., Downing G., Yun C., Solomon M., Jacob S., Mendoza S. (2013). Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles. — Biol. Psychiatr. 74: 180-188.
-
Barazza J.A., McCullough M.E., Zak P.J. (2011). Oxytocin infusion increases charitable donations regardless of monetary resources. — Horm. Behav. 60: 148-151.
-
Barazza J.A., Zak P.J. (2009). Empathy toward strangers triggers oxytocin release and subsequent generosity. — Ann. NY Acad. Sci. 1167: 182-189.
-
Barazza J.A., Zak P.J. (2013). Oxytocin instantiates empathy and produces prosocial behaviours. — In: Oxytocin, vasopressin and related peptides in the regulation of behaviour ( Choleris E., Pfaff D.W., Kavaliers M., eds). Cambridge University Press, Cambridge, p. 331-342.
-
Barraza I., Grewal N., Ropacki S., Perez P., Gonzales A., Zak P.J. (2013). Effects of a 10-day oxytocin infusion in older adults on health and well-being. — Psychopharmacology 21: 85-92.
-
Bartz J.A., Zaki J., Bolger N., Hollander E., Ludwig N.N., Kolevzon A., Ochsner K.N. (2010a). Oxytocin selectively improves empathetic accuracy. — Psychol. Sci. 21: 1426-1428.
-
Bartz J.A., Zaki J., Ochsner K.N., Bolger N., Kolevzon A., Ludwig N., Lyndon J.E. (2010b). Effects of oxytocin on recollections of maternal care and closeness. — Proc. Natl. Acad. Sci. USA 107: 21371-21375.
-
Bartz J.A., Simeon D., Hamilton H., Kim S., Crystal S., Braun A., Vincens V., Hollander E. (2011a). Oxytocin can hinder trust and cooperation in borderline personality disorder. — Soc. Cogn. Affect. Neurosci. 6: 556-563.
-
Bartz J.A., Zaki J., Bolger N., Ochsner K.N. (2011b). Social effects of oxytocin in humans: context and person matter. — Trends Cogn. Sci. 15: 301-309.
-
Baumgartner T., Heinrichs M., Vonlanthen A., Fischbacher U., Fehr E. (2008). Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. — Neuron 58: 639-650.
-
Bisset G.W., Clark B.J., Lewis G.P. (1967). The mechanism of the inhibitory action of adrenaline on the mammary gland. — Br. J. Pharmacol. Chemother. 31: 550-559.
-
Blevins J.E., Ho J.M. (2013). Role of oxytocin signaling in the regulation of body weight. — Rev. Endocr. Metab. Disord. 14: 311-329.
-
Born J., Lange T., Kern W., McGregor G.P., Bickel U., Fehm H.L. (2002). Sniffing neuropeptides: a transnasal approach to the human brain. — Nature Neurosci. 5: 514-516.
-
Brosnan S.F. (2010). What do capuchin monkeys tell us about cooperation? — In: For the greater good of all: perspectives on individualism, society, and leadership, Vol. Jepson studies in leadership series ( Forsyth D.R., Hoyt C.L., eds). Palgrave Macmillan, New York, NY, p. 11-28.
-
Brosnan S.F. (2011). An evolutionary perspective on morality. — J. Econ. Behav. Org. 77: 23-30.
-
Brosnan S.F., Freeman C., de Waal F.B.M. (2006). Partner’s behavior, not reward distribution, determines success in an unequal cooperative task in capuchin monkeys. — Am. J. Primatol. 68: 713-724.
-
Brosnan S.F., Houser D., Leimgruber K., Xiao E., Chen T., de Waal F.B.M. (2010). Competing demands of prosociality and equity in monkeys. — Evol. Hum. Behav. 31: 279-288.
-
Burkart J., Fehr E., Efferson C., van Schaik C.P. (2007). Other-regarding preferences in a non-human primate: common marmosets provision food altruistically. — Proc. Natl. Acad. Sci. USA 104: 19762-19766.
-
Carter C.S., Grippo A.J., Pournajafi-Nazarloo H., Ruscio M.G., Porges S.W. (2008). Oxytocin, vasopressin and sociality. — Prog. Brain Res. 170: 331-336.
-
Carter C.S., Keverne E.B. (2002). The neurobiology of social affiliation and pair bonding. — In: Hormones, brain and behavior ( Pfaff D., ed.). Academic Press, San Diego, CA, p. 299-337.
-
Chang S.W.C., Barter J.W., Ebitz R.B., Watson K.K., Platt M.L. (2012). Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus monkeys. — Proc. Natl. Acad. Sci. USA 109: 959-964.
-
Cronin K.A., Schroeder K.K.E., Rothwell E.S., Silk J.B., Snowdon C. (2009). Cooperatively breeding cottontop tamarins (Saguinus oedipus) do not donate rewards to their long-term mates. — J. Comp. Psychol. 123: 231-241.
-
Cronin K.A., Schroeder K.K.E., Snowdon C. (2010). Prosocial behaviour emerges independent of reciprocity in cottontop tamarins. — Proc. Roy. Soc. Lond. B: Biol. Sci. 277: 3845-3851.
-
De Dreu C.K.W., Greer L.L., Handgraaf M.J.J., Shalvi S., Van Kleef G.A., Baas M., Ten Velden F., Van Dijk E., Feith S. (2010). The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. — Science 328: 1408-1411.
-
De Dreu C.K.W., Greer L.L., Handgraaf M.J.J., Shalvi S., Van Kleef G.A. (2012). Oxytocin modulates selection of allies in intergroup conflict. — Proc. Roy. Soc. Lond. B: Biol. Sci. 279: 1150-1154.
-
de Waal F.B.M. (1997). Bonobo: the forgotten ape. — University of California Press, Berkeley, CA.
-
de Waal F.B.M. (2008). Putting the altruism back into altruism: the evolution of empathy. — Annu. Rev. Psychol. 59: 279-300.
-
de Waal F.B.M., Berger M.L. (2000). Payment for labour in monkeys. — Nature 404: 563.
-
de Waal F.B.M., Davis J.M. (2002). Capuchin cognitive ecology: cooperation based on projected returns. — Neuropsychologia 1492: 1-8.
-
de Waal F.B.M., Leimgruber K., Greenberg A. (2008). Giving is self-rewarding for monkeys. — Proc. Natl. Acad. Sci. USA 105: 13685-13689.
-
Donaldson Z., Young L.J. (2008). Oxytocin, vasopressin, and the neurogenetics of sociality. — Science 322: 900-904.
-
Ebitz R.B., Watson K.K., Platt M.L. (2013). Oxytocin blunts social vigilance in the rhesus macaque. — Proc. Natl. Acad. Sci. USA 110: 11630-11635.
-
Evans T.A., Beran M.J., Chan B., Klein E.D., Menzel C.R. (2008). An efficient computerized testing method for the capuchin monkey (Cebus apella): adaptation of the LRC-CTS to a socially housed nonhuman primate species. — Behav. Res. Methods 40: 590-596.
-
Feistner A.T.C., McGrew W.C. (1989). Food-sharing in primates: a critical review. — In: Perspectives in primate biology, Vol. 3 ( Seth P.K., Seth S., eds). Today & Tomorrow’s Printers and Publishers, New Delhi, p. 21-36.
-
Flack J., de Waal F.B.M. (2000). ‘Any animal whatever’: Darwinian building blocks of morality in monkeys and apes. — J. Consciousness Stud. 7: 1-29.
-
Fragaszy D.M., Visalberghi E., Fedigan L.M. (2004). The complete capuchin: the biology of the genus Cebus. — Cambridge University Press, Cambridge.
-
Gamer M., Zurowski B., Büchel C. (2010). Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. — Proc. Natl. Acad. Sci. USA 107: 9400-9405.
-
Gimpl G., Fahrenholz F. (2001). The oxytocin receptor system: structure, function and regulation. — Physiol. Rev. 81: 629-683.
-
Ho J.M., Blevins J.E. (2013). Coming full circle: contributions of central and peripheral oxytocin actions to energy balance. — Endocrinology 154: 589-596.
-
Horner V., Carter J.D., Suchak M., de Waal F.B.M. (2011). Spontaneous prosocial choice by chimpanzees. — Proc. Natl. Acad. Sci. USA 108: 13847-13851.
-
Insel T. (1997). A neurobiological basis of social attachment. — Am. J. Psychiatr. 154: 726-735.
-
Jaeggi A.V., van Schaik C.P. (2011). The evolution of food sharing in primates. — Behav. Ecol. Sociobiol. 65: 2125-2140.
-
Jaeggi A.V., Burkart J.M., Van Schaik C.P. (2010). On the psychology of cooperation in humans and other primates: combining the natural history and experimental evidence of prosociality. — Phil. Trans. Roy. Soc. Lond. B 365: 2723-2735.
-
Jensen K., Hare B., Call J., Tomasello M. (2006). What’s in it for me? Self-regard precludes altruism and spite in chimpanzees. — Proc. Roy. Soc. Lond. B: Biol. Sci. 273: 1013-1021.
-
Kirsch P., Esslinger C., Chen Q., Mier D., Lis S., Siddhanti S., Gruppe H., Mattay V.S., Gallhofer B., Meyer-Lindenberg A. (2005). Oxytocin modulates neural circuitry for social cognition and fear in humans. — J. Neurosci. 25: 11489-11493.
-
Kosfeld M., Heinrichs M., Zak P.J., Fischbacher U., Fehr E. (2005). Oxytocin increases trust in humans. — Nature 435: 673-676.
-
Lakshminarayanan V., Santos L.R. (2008). Capuchin monkeys are sensitive to others’ welfare. — Curr. Biol. 18: R999-R1000.
-
Lee A.G., Cool D.R., Grunwald W.C., Neal D.E., Buckmaster C.L., Cheng M.Y., Hyde S.A., Lyons D.M., Parker K.J. (2011). A novel form of oxytocin in New World monkeys. — Biol. Lett. 7: 584-587.
-
Lim M.M., Young L.J. (2006). Neuropeptidergic regulation of affiliative behavior and social bonding in animals. — Horm. Behav. 50: 506-517.
-
Maestripieri D., Schino G., Aureli F., Troisi A. (1992). A modest proposal: displacement activities as an indicator of emotions in primates. — Anim. Behav. 44: 967-979.
-
Meaney M.J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. — Annu. Rev. Neurosci. 24: 1161-1192.
-
Mendres K.A., de Waal F.B.M. (2000). Capuchins do cooperate: the advantage of an intuitive task. — Anim. Behav. 60: 523-529.
-
Morhenn V.B., Park J.W., Piper E., Zak P.J. (2008). Monetary sacrifice among strangers is mediated by endogenous oxytocin release after physical contact. — Evol. Hum. Behav. 29: 375-383.
-
Ott V., Finlayson G., Lehnert H., Heitmann B., Heinrichs M., Born J., Hallschmid M. (2013). Oxytocin reduces reward-driven food intake in humans. — Diabetes 62: 3418-3425.
-
Parker K.J., Buckmaster C.L., Schatzberg A.F., Lyons D.M. (2005). Intranasal oxytocin administration attenuates the ACTH stress response in monkeys. — Psychoneuroendocrinology 30: 924-929.
-
Perry S., Manson J.H., Dower G., Wikbert E. (2003). White-faced capuchins cooperate to rescue a groupmate from a Boa constrictor. — Folia Primatol. 74: 109-111.
-
Perry S., Rose L. (1994). Begging and transfer of coati meat by white-faced capuchin monkeys, Cebus capucinus. — Primates 35: 409-415.
-
Petersson M., Uvnäs-Moberg K., Erhardt S., Engberg G. (1998). Oxytocin increases locus coeruleus alpha 2-adrenoreceptor responsiveness in rats. — Neurosci. Lett. 255: 115-118.
-
Petrovic P., Kalisch R., Singer T., Dolan R.J. (2008). Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. — J. Neurosci. 28: 6607-6615.
-
Rand D.G., Green J.D., Nowak M.A. (2012). Spontaneous giving and calculated greed. — Nature 489: 427-430.
-
Ross H.E., Freeman S.M., Spiegel L.L., Ren X., Terwilliger E.F., Young L.J. (2009). Variation in oxytocin receptor density in the nucleaus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. — J. Neurosci. 4: 1312-1318.
-
Saito A., Nakamura K. (2011). Oxytocin changes primate paternal tolerance to offspring in food transfer. — J. Comp. Physiol. A 197: 329-337.
-
Silk J.B., Brosnan S.F., Vonk J., Henrich J., Povinelli D.J., Richardson A.S., Lambeth S., Mascaro J., Schapiro S. (2005). Chimpanzees are indifferent to the welfare of unrelated group members. — Nature 437: 1357-1359.
-
Smith A.S., Agmo A., Birnie A.K., French J.A. (2010). Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callitrhix penicillata. — Horm. Behav. 57: 255-262.
-
Song S.L., Crowley W.R., Grosvenor C.E. (1988). Evidence for involvement of an adrenal catecholamine in the β-adrenergic inhibition of oxytocin release in lactating rats. — Brain Res. 457: 303-309.
-
Stevens J.R. (2010). Donor payoffs and other-regarding preferences in cotton-top tamarins (Saguinus oedipus). — Anim. Cogn. 13: 663-670.
-
Striepens N., Kendrick K.M., Hanking V., Landgraf R., Wullner U., Maier W., Hurlemann R. (2013). Elevated cerebrospinal fluid and blood concentrations of oxytocin following its intranasal administration in humans. — Sci. Rep. 3: 3440.
-
Taylor S.E., Gonzaga G. (2007). Affiliative responses to stress: a social neuroscience model. — In: Social neuroscience: integrating biological and psychological explanations of social behavior ( Harmon-Jones E., Winkielman P., eds). Guilford, New York, NY, p. 454-473.
-
Terris B., Beavin L., Schloss J., Zak P.J. (2013). Oxytocin release during rituals and its effect on in-group and out-group behavior. — Poster presented at the Society for Neuroscience Conference 2013, San Diego, CA, No. 378.15.
-
Troisi A. (2002). Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. — Stress 5: 47-54.
-
van Anders S., Goodson I., Kingsbury M. (2013). Beyond “oxytocin = good”: neural complexities and the flipside of social bonds. — Arch. Sex. Behav. 42: 1115-1118.
-
Visalberghi E., Quarantotti B.P., Tranchida F. (2000). Solving a copoeration task without taking into account the partner’s behaviour: the case of capuchin monkeys (Cebus apella). — J. Comp. Psychol. 114: 297-301.
-
Winslow J., Noble P., Lyons C., Sterk S., Insel T. (2003). Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. — Neuropsychopharmacology 28: 901-918.
-
Wittig R., Crockford C., Deschner T., Langergraber K.E., Ziegler T.E., Zuberbühler K. (2014). Urinary oxytocin and social bonding in related and unrelated wild chimpanzees. — Proc. Roy. Soc. Lond. B: Biol. Sci. 280: 20122765.
-
Young L.J., Wang Z. (2004). The neurobiology of pair bonding. — Nature Neurosci. 7: 1048-1054.
-
Zak P.J. (2011). The physiology of moral sentiments. — J. Econ. Behav. Org. 77: 53-65.
-
Zak P.J. (2012). The moral molecule: the source of love and prosperity. — Dutton, Boston, MA.
-
Zak P.J., Barraza J.A. (2013). The neurobiology of collective action. — Front. Neurosci. 7: 211.
-
Zak P.J., Kurzban R., Matzner W.T. (2005). The neurobiology of trust. — Ann. NY Acad. Sci. 1032: 224-227.
-
Zak P.J., Stanton A.A., Ahmadi S. (2007). Oxytocin increases generosity in humans. — PLOS One 2: e1128.
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Oxytocin reduces food sharing in capuchin monkeys by modulating social distance
In: BehaviourRecent evidence indicates that oxytocin plays an important role in promoting prosocial behaviour amongst humans and other species. We tested whether oxytocin affected cooperation and food-sharing in capuchin monkeys, a highly cooperative New World primate. Subjects received either 2IU oxytocin or an inert adjuvent intranasally prior to each session. Oxytocin influenced food sharing in capuchins in ways we did not anticipate. Recipients were less likely to passively acquire food from possessors when either individual had received OT than in the control, and also spent less time in proximity to their partner. Passive food sharing requires proximity, and oxytocin decreased the capuchins’ typical congregating behaviour, apparently resulting in decreased sharing. We propose that the likely mechanism for increased social distance is the known anxiolytic effect of oxytocin. Our results indicate a need to consider how oxytocin affects the context of interactions and interacts with modes of sociality unique to each species.
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 730 | 129 | 23 |
| Full Text Views | 203 | 23 | 4 |
| PDF Views & Downloads | 81 | 29 | 9 |