Cookies Policy
X

This site uses cookies. By continuing to browse the site you are agreeing to our use of cookies.

I accept this policy

Find out more here

Oxytocin reduces food sharing in capuchin monkeys by modulating social distance

No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.
The full text of this article is not currently available.

Brill’s MyBook program is exclusively available on BrillOnline Books and Journals. Students and scholars affiliated with an institution that has purchased a Brill E-Book on the BrillOnline platform automatically have access to the MyBook option for the title(s) acquired by the Library. Brill MyBook is a print-on-demand paperback copy which is sold at a favorably uniform low price.

Access this article

+ Tax (if applicable)
Add to Favorites
You must be logged in to use this functionality

image of Behaviour

Recent 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.

Affiliations: 1: aLanguage Research Center, Georgia State University, Atlanta, GA 30034, USA; 2: dThe Center for Neuroeconomic Studies, Claremont Graduate University, Claremont, CA 91711, USA

10.1163/1568539X-00003268
/content/journals/10.1163/1568539x-00003268
dcterms_title,pub_keyword,dcterms_description,pub_author
10
5
Loading
Loading

Full text loading...

/content/journals/10.1163/1568539x-00003268
Loading

Data & Media loading...

1. 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. Vol 74: 180- 188. http://dx.doi.org/10.1016/j.biopsych.2012.08.025
2. Barazza J.A. , McCullough M.E. , Zak P.J. ( 2011). "Oxytocin infusion increases charitable donations regardless of monetary resources". — Horm. Behav. Vol 60: 148- 151. http://dx.doi.org/10.1016/j.yhbeh.2011.04.008
3. Barazza J.A. , Zak P.J. ( 2009). "Empathy toward strangers triggers oxytocin release and subsequent generosity". — Ann. NY Acad. Sci. Vol 1167: 182- 189. http://dx.doi.org/10.1111/j.1749-6632.2009.04504.x
4. 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. http://dx.doi.org/10.1017/CBO9781139017855.022
5. 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 Vol 21: 85- 92.
6. 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. Vol 21: 1426- 1428. http://dx.doi.org/10.1177/0956797610383439
7. 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 Vol 107: 21371- 21375. http://dx.doi.org/10.1073/pnas.1012669107
8. 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. Vol 6: 556- 563. http://dx.doi.org/10.1093/scan/nsq085
9. Bartz J.A. , Zaki J. , Bolger N. , Ochsner K.N. ( 2011b). "Social effects of oxytocin in humans: context and person matter". — Trends Cogn. Sci. Vol 15: 301- 309.
10. Baumgartner T. , Heinrichs M. , Vonlanthen A. , Fischbacher U. , Fehr E. ( 2008). "Oxytocin shapes the neural circuitry of trust and trust adaptation in humans". — Neuron Vol 58: 639- 650. http://dx.doi.org/10.1016/j.neuron.2008.04.009
11. 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. Vol 31: 550- 559. http://dx.doi.org/10.1111/j.1476-5381.1967.tb00419.x
12. Blevins J.E. , Ho J.M. ( 2013). "Role of oxytocin signaling in the regulation of body weight". — Rev. Endocr. Metab. Disord. Vol 14: 311- 329. http://dx.doi.org/10.1007/s11154-013-9260-x
13. 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. Vol 5: 514- 516. http://dx.doi.org/10.1038/nn0602-849
14. 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 Vol. Jepson studies in leadership series( Forsyth D.R. , Hoyt C.L. , eds). Palgrave Macmillan, New York, NY, p.  11- 28.
15. Brosnan S.F. ( 2011). "An evolutionary perspective on morality". — J. Econ. Behav. Org. Vol 77: 23- 30. http://dx.doi.org/10.1016/j.jebo.2010.04.008
16. 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. Vol 68: 713- 724. http://dx.doi.org/10.1002/ajp.20261
17. 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. Vol 31: 279- 288. http://dx.doi.org/10.1016/j.evolhumbehav.2010.02.003
18. 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 Vol 104: 19762- 19766. http://dx.doi.org/10.1073/pnas.0710310104
19. Carter C.S. , Grippo A.J. , Pournajafi-Nazarloo H. , Ruscio M.G. , Porges S.W. ( 2008). "Oxytocin, vasopressin and sociality". — Prog. Brain Res. Vol 170: 331- 336.
20. 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. http://dx.doi.org/10.1016/B978-012532104-4/50006-8
21. 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 Vol 109: 959- 964. http://dx.doi.org/10.1073/pnas.1114621109
22. 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. Vol 123: 231- 241. http://dx.doi.org/10.1037/a0015094
23. 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. Vol 277: 3845- 3851. http://dx.doi.org/10.1098/rspb.2010.0879
24. 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 Vol 328: 1408- 1411. http://dx.doi.org/10.1126/science.1189047
25. 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. Vol 279: 1150- 1154. http://dx.doi.org/10.1098/rspb.2011.1444
26. de Waal F.B.M. ( 1997). Bonobo: the forgotten ape. — University of California Press, Berkeley, CA.
27. de Waal F.B.M. ( 2008). "Putting the altruism back into altruism: the evolution of empathy". — Annu. Rev. Psychol. Vol 59: 279- 300. http://dx.doi.org/10.1146/annurev.psych.59.103006.093625
28. de Waal F.B.M. , Berger M.L. ( 2000). "Payment for labour in monkeys". — Nature Vol 404: 563. http://dx.doi.org/10.1038/35007138
29. de Waal F.B.M. , Davis J.M. ( 2002). "Capuchin cognitive ecology: cooperation based on projected returns". — Neuropsychologia Vol 1492: 1- 8.
30. de Waal F.B.M. , Leimgruber K. , Greenberg A. ( 2008). "Giving is self-rewarding for monkeys". — Proc. Natl. Acad. Sci. USA Vol 105: 13685- 13689. http://dx.doi.org/10.1073/pnas.0807060105
31. Donaldson Z. , Young L.J. ( 2008). "Oxytocin, vasopressin, and the neurogenetics of sociality". — Science Vol 322: 900- 904. http://dx.doi.org/10.1126/science.1158668
32. Ebitz R.B. , Watson K.K. , Platt M.L. ( 2013). "Oxytocin blunts social vigilance in the rhesus macaque". — Proc. Natl. Acad. Sci. USA Vol 110: 11630- 11635. http://dx.doi.org/10.1073/pnas.1305230110
33. 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 Vol 40: 590- 596. http://dx.doi.org/10.3758/BRM.40.2.590
34. Feistner A.T.C. , McGrew W.C. ( 1989). "Food-sharing in primates: a critical review". — In: Perspectives in primate biology, Vol Vol. 3( Seth P.K. , Seth S. , eds). Today & Tomorrow’s Printers and Publishers, New Delhi, p.  21- 36.
35. Flack J. , de Waal F.B.M. ( 2000). "‘Any animal whatever’: Darwinian building blocks of morality in monkeys and apes". — J. Consciousness Stud. Vol 7: 1- 29.
36. Fragaszy D.M. , Visalberghi E. , Fedigan L.M. ( 2004). The complete capuchin: the biology of the genus Cebus . — Cambridge University Press, Cambridge.
37. 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 Vol 107: 9400- 9405. http://dx.doi.org/10.1073/pnas.1000985107
38. Gimpl G. , Fahrenholz F. ( 2001). "The oxytocin receptor system: structure, function and regulation". — Physiol. Rev. Vol 81: 629- 683.
39. Ho J.M. , Blevins J.E. ( 2013). "Coming full circle: contributions of central and peripheral oxytocin actions to energy balance". — Endocrinology Vol 154: 589- 596. http://dx.doi.org/10.1210/en.2012-1751
40. Horner V. , Carter J.D. , Suchak M. , de Waal F.B.M. ( 2011). "Spontaneous prosocial choice by chimpanzees". — Proc. Natl. Acad. Sci. USA Vol 108: 13847- 13851. http://dx.doi.org/10.1073/pnas.1111088108
41. Insel T. ( 1997). "A neurobiological basis of social attachment". — Am. J. Psychiatr. Vol 154: 726- 735. http://dx.doi.org/10.1176/ajp.154.6.726
42. Jaeggi A.V. , van Schaik C.P. ( 2011). "The evolution of food sharing in primates". — Behav. Ecol. Sociobiol. Vol 65: 2125- 2140. http://dx.doi.org/10.1007/s00265-011-1221-3
43. 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 Vol 365: 2723- 2735. http://dx.doi.org/10.1098/rstb.2010.0118
44. 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. Vol 273: 1013- 1021. http://dx.doi.org/10.1098/rspb.2005.3417
45. 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. Vol 25: 11489- 11493. http://dx.doi.org/10.1523/JNEUROSCI.3984-05.2005
46. Kosfeld M. , Heinrichs M. , Zak P.J. , Fischbacher U. , Fehr E. ( 2005). "Oxytocin increases trust in humans". — Nature Vol 435: 673- 676. http://dx.doi.org/10.1038/nature03701
47. Lakshminarayanan V. , Santos L.R. ( 2008). "Capuchin monkeys are sensitive to others’ welfare". — Curr. Biol. Vol 18: R999- R1000. http://dx.doi.org/10.1016/j.cub.2008.08.057
48. 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. Vol 7: 584- 587. http://dx.doi.org/10.1098/rsbl.2011.0107
49. Lim M.M. , Young L.J. ( 2006). "Neuropeptidergic regulation of affiliative behavior and social bonding in animals". — Horm. Behav. Vol 50: 506- 517. http://dx.doi.org/10.1016/j.yhbeh.2006.06.028
50. Maestripieri D. , Schino G. , Aureli F. , Troisi A. ( 1992). "A modest proposal: displacement activities as an indicator of emotions in primates". — Anim. Behav. Vol 44: 967- 979. http://dx.doi.org/10.1016/S0003-3472(05)80592-5
51. Meaney M.J. ( 2001). "Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations". — Annu. Rev. Neurosci. Vol 24: 1161- 1192. http://dx.doi.org/10.1146/annurev.neuro.24.1.1161
52. Mendres K.A. , de Waal F.B.M. ( 2000). "Capuchins do cooperate: the advantage of an intuitive task". — Anim. Behav. Vol 60: 523- 529. http://dx.doi.org/10.1006/anbe.2000.1512
53. 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. Vol 29: 375- 383. http://dx.doi.org/10.1016/j.evolhumbehav.2008.04.004
54. Ott V. , Finlayson G. , Lehnert H. , Heitmann B. , Heinrichs M. , Born J. , Hallschmid M. ( 2013). "Oxytocin reduces reward-driven food intake in humans". — Diabetes Vol 62: 3418- 3425. http://dx.doi.org/10.2337/db13-0663
55. Parker K.J. , Buckmaster C.L. , Schatzberg A.F. , Lyons D.M. ( 2005). "Intranasal oxytocin administration attenuates the ACTH stress response in monkeys". — Psychoneuroendocrinology Vol 30: 924- 929. http://dx.doi.org/10.1016/j.psyneuen.2005.04.002
56. Perry S. , Manson J.H. , Dower G. , Wikbert E. ( 2003). "White-faced capuchins cooperate to rescue a groupmate from a Boa constrictor ". — Folia Primatol. Vol 74: 109- 111. http://dx.doi.org/10.1159/000070008
57. Perry S. , Rose L. ( 1994). "Begging and transfer of coati meat by white-faced capuchin monkeys, Cebus capucinus ". — Primates Vol 35: 409- 415. http://dx.doi.org/10.1007/BF02381950
58. Petersson M. , Uvnäs-Moberg K. , Erhardt S. , Engberg G. ( 1998). "Oxytocin increases locus coeruleus alpha 2-adrenoreceptor responsiveness in rats". — Neurosci. Lett. Vol 255: 115- 118. http://dx.doi.org/10.1016/S0304-3940(98)00729-0
59. Petrovic P. , Kalisch R. , Singer T. , Dolan R.J. ( 2008). "Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity". — J. Neurosci. Vol 28: 6607- 6615. http://dx.doi.org/10.1523/JNEUROSCI.4572-07.2008
60. Rand D.G. , Green J.D. , Nowak M.A. ( 2012). "Spontaneous giving and calculated greed". — Nature Vol 489: 427- 430. http://dx.doi.org/10.1038/nature11467
61. 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. Vol 4: 1312- 1318. http://dx.doi.org/10.1523/JNEUROSCI.5039-08.2009
62. Saito A. , Nakamura K. ( 2011). "Oxytocin changes primate paternal tolerance to offspring in food transfer". — J. Comp. Physiol. A Vol 197: 329- 337. http://dx.doi.org/10.1007/s00359-010-0617-2
63. 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 Vol 437: 1357- 1359. http://dx.doi.org/10.1038/nature04243
64. 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. Vol 57: 255- 262. http://dx.doi.org/10.1016/j.yhbeh.2009.12.004
65. 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. Vol 457: 303- 309. http://dx.doi.org/10.1016/0006-8993(88)90700-7
66. Stevens J.R. ( 2010). "Donor payoffs and other-regarding preferences in cotton-top tamarins ( Saguinus oedipus)". — Anim. Cogn. Vol 13: 663- 670. http://dx.doi.org/10.1007/s10071-010-0309-x
67. 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. Vol 3: 3440. http://dx.doi.org/10.1038/srep03440
68. 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.
69. 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.
70. Troisi A. ( 2002). "Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects". — Stress Vol 5: 47- 54. http://dx.doi.org/10.1080/102538902900012378
71. van Anders S. , Goodson I. , Kingsbury M. ( 2013). "Beyond “oxytocin = good”: neural complexities and the flipside of social bonds". — Arch. Sex. Behav. Vol 42: 1115- 1118. http://dx.doi.org/10.1007/s10508-013-0134-9
72. 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. Vol 114: 297- 301. http://dx.doi.org/10.1037/0735-7036.114.3.297
73. 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 Vol 28: 901- 918.
74. 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. Vol 280: 20122765.
75. Young L.J. , Wang Z. ( 2004). "The neurobiology of pair bonding". — Nature Neurosci. Vol 7: 1048- 1054. http://dx.doi.org/10.1038/nn1327
76. Zak P.J. ( 2011). "The physiology of moral sentiments". — J. Econ. Behav. Org. Vol 77: 53- 65. http://dx.doi.org/10.1016/j.jebo.2009.11.009
77. Zak P.J. ( 2012). The moral molecule: the source of love and prosperity. — Dutton, Boston, MA.
78. Zak P.J. , Barraza J.A. ( 2013). "The neurobiology of collective action". — Front. Neurosci. Vol 7: 211. http://dx.doi.org/10.3389/fnins.2013.00211
79. Zak P.J. , Kurzban R. , Matzner W.T. ( 2005). "The neurobiology of trust". — Ann. NY Acad. Sci. Vol 1032: 224- 227. http://dx.doi.org/10.1196/annals.1314.025
80. Zak P.J. , Stanton A.A. , Ahmadi S. ( 2007). "Oxytocin increases generosity in humans". — PLOS One Vol 2: e1128. http://dx.doi.org/10.1371/journal.pone.0001128
http://brill.metastore.ingenta.com/content/journals/10.1163/1568539x-00003268
Loading

Article metrics loading...

/content/journals/10.1163/1568539x-00003268
2015-05-29
2018-09-22

Sign-in

Can't access your account?
  • Tools

  • Add to Favorites
  • Printable version
  • Email this page
  • Subscribe to ToC alert
  • Get permissions
  • Recommend to your library

    You must fill out fields marked with: *

    Librarian details
    Your details
    Why are you recommending this title?
    Select reason:
     
    Behaviour — Recommend this title to your library
  • Export citations
  • Key

  • Full access
  • Open Access
  • Partial/No accessInformation