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Allonursing in white-faced capuchins ( Cebus capucinus) provides evidence for cooperative care of infants

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Allonursing is a highly cooperative behaviour that may have important fitness consequences for the infant while the benefits to the allomother are less clear. To investigate the function of this behaviour, we compared patterns of allonursing and nursing exhibited by white-faced capuchin monkeys ( Cebus capucinus). We used a linear mixed model approach to analyse data collected on 21 infants from six social groups in Sector Santa Rosa, Costa Rica. Infants nursed at higher rates and for longer durations from their mothers than from allonurses. They also allonursed at higher rates from lactating and non-lactating parous females than from nulliparous females and at higher rates from maternally related female allonurses than other females. We found no observed effect of adult female rank or infant sex. We conclude that infant white-faced capuchins engage in allonursing as a means to acquire additional milk, and that participating allonurses may benefit from increased inclusive fitness.

Affiliations: 1: aDepartment of Anthropology, University of Calgary, AB, Canada; 2: bDepartment of Integrated Biosciences, University of Tokyo, Kashiwa, Chiba, Japan

10.1163/1568539X-00003308
/content/journals/10.1163/1568539x-00003308
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1. Alfaro J.W. , Silva J. , Rylands A.B. ( 2012). "How different are robust and gracile capuchin monkeys? An argument for the use of Sapajusand Cebus ". — Am. J. Primatol. Vol 74: 381- 393. http://dx.doi.org/10.1002/ajp.21998
2. Altmann J. ( 1974). "Observational study of behaviour: sampling methods". — Behaviour Vol 49: 227- 267. http://dx.doi.org/10.1163/156853974X00534
3. Appleby M.C. ( 1983). "The probability of linearity in hierarchies". — Anim. Behav. Vol 31: 600- 608. http://dx.doi.org/10.1016/S0003-3472(83)80084-0
4. Baldovino M.C. , Di Bitetti M.S. ( 2008). "Allonursing in tufted capuchin monkeys ( Cebus nigritus): milk or pacifier?"— Folia Primatol. Vol 79: 79- 92. http://dx.doi.org/10.1159/000108780
5. Bergstrom M.L. , Fedigan L.M. ( 2010). "Dominance among female white-faced capuchin monkeys ( Cebus capucinus): hierarchical linearity, nepotism, strength and stability". — Behaviour Vol 147: 899- 931. http://dx.doi.org/10.1163/000579510X497283
6. Bergstrom M.L. , Fedigan L.M. ( 2013). "Dominance style of female white-faced capuchins". — Am. J. Phys. Anthropol. Vol 150: 591- 601. http://dx.doi.org/10.1002/ajpa.22231
7. Birgersson B. , Ekvall J. , Temrin H. ( 1991). "Allosuckling in fallow deer, Dama dama ". — Anim. Behav. Vol 42: 326- 327. http://dx.doi.org/10.1016/S0003-3472(05)80567-6
8. Bisset G.W. ( 1974). "Milk ejection". — In: Handbook of physiology and endocrinology, Part 1( Knobil E. , Sawyer W.H. , eds). American Physiological Society, Washington, DC, p.  493- 526.
9. Boubli J.P. , Rylands A.B. , Farias I.P. , Alfaro M.E. , Alfaro L. ( 2012). " Cebusphylogenetic relationships: a preliminary reassessment of the diversity of the untufted capuchin monkeys". — Am. J. Primatol. Vol 74: 381- 393. http://dx.doi.org/10.1002/ajp.21998
10. Boyd R. , Richerson P.J. ( 1988). "The evolution of reciprocity in sizable groups". — J. Theor. Biol. Vol 132: 337- 356. http://dx.doi.org/10.1016/S0022-5193(88)80219-4
11. Burkart J.M. , Hrdy S.B. , van Schaik C.P. ( 2009). "Cooperative breeding and human cognitive evolution". — Evol. Anthropol. Vol 18: 175- 176. http://dx.doi.org/10.1002/evan.20222
12. Cameron E.Z. ( 1998). "Is suckling behaviour a useful predictor of milk intake? A review". — Anim. Behav. Vol 58: 521- 532. http://dx.doi.org/10.1006/anbe.1998.0793
13. Carnegie S.D. , Fedigan L.M. , Melin A.D. ( 2011). "Reproductive seasonality in female capuchins ( Cebus capucinus)". — Int. J. Primatol. Vol 32: 1076- 1090. http://dx.doi.org/10.1007/s10764-011-9523-x
14. Carnegie S.D. , Fedigan L.M. , Ziegler T.E. ( 2006). "Post-conceptive mating in white-faced capuchins, Cebus capucinus: hormonal and sociosexual patterns of cycling, noncycling, and pregnant females". — In: New perspectives in the study of mesoamerican primates: distribution, ecology, behavior, and conservation( Estrada A. , Garber P.A. , Pavelka M.S.M. , Luecke L. , eds). Springer, New York, NY, p.  387- 409. http://dx.doi.org/10.1007/0-387-25872-8_19
15. Carson K. , Wood-Gush D.G.M. ( 1983). "Equine behaviour: a review of the literature on social and dam–foal behaviour". — Appl. Anim. Ethol. Vol 10: 165- 178. http://dx.doi.org/10.1016/0304-3762(83)90138-4
16. Chapais B. ( 2001). "Primate nepotism: what is the explanatory value of kin selection". — Int. J. Primatol. Vol 22: 203- 229. http://dx.doi.org/10.1023/A:1005619430744
17. Clutton-Brock T.H. ( 2006). "Cooperative breeding in mammals". — In: Cooperation in primates and humans: mechanisms and evolution( Kappeler P.M. , van Schaik C.P. , eds). Springer, Berlin, p.  173- 190. http://dx.doi.org/10.1007/3-540-28277-7_10
18. Clutton-Brock T.H. ( 1991). The evolution of parental care. — Princeton University Press, Princeton, NJ.
19. Clutton-Brock T.H. , Albon S.D. , Guiness F.E. ( 1989). "Fitness costs of gestation and lactation in wild animals". — Nature Vol 337: 260- 262. http://dx.doi.org/10.1038/337260a0
20. Cortés-Ortiz L. , Mondragón E. , Cabotage J. ( 2010). "Isolation and characterization of microsatellite loci for the study of Mexican howler monkeys, their natural hybrids, and other Neotropical primates". — Conserv. Gen. Resourc. Vol 2: 21- 26. http://dx.doi.org/10.1007/s12686-009-9124-6
21. de Waal F.M.B. , Leimgruber K. , Greenberg A.R. ( 2008). "Giving is self-rewarding for monkeys". — Proc. Natl. Acad. Sci. USA Vol 105: 13685- 13689. http://dx.doi.org/10.1073/pnas.0807060105
22. Fedigan L.M. ( 2003). "Impact of male takeovers on infant deaths, births, and conceptions in Cebus capucinusat Santa Rosa, Costa Rica". — Int. J. Primatol. Vol 24: 723- 741. http://dx.doi.org/10.1023/A:1024620620454
23. Fedigan L.M. , Jack K. ( 2001). "Neotropical primates in a regenerating Costa Rican dry forest: a comparison of howler and capuchin population patterns". — Int. J. Primatol. Vol 22: 689- 713. http://dx.doi.org/10.1023/A:1012092115012
24. Festa-Bianchet M. ( 1988). "Nursing behaviour of bighorn sheep: correlates of ewe age, parasitism, lamb age, birthdate and sex". — Anim. Behav. Vol 36: 1445- 1454. http://dx.doi.org/10.1016/S0003-3472(88)80215-X
25. Fletcher I.C. ( 1971). "Relationships between frequency of suckling, lamb growth and post-partum oestrous behaviour in ewes". — Anim. Behav. Vol 19: 108- 111. http://dx.doi.org/10.1016/S0003-3472(71)80142-2
26. Fragaszy D.M. , Visalberghi E. , Fedigan L.M. ( 2004). The complete capuchin: the biology of the genus Cebus . — Cambridge University Press, Cambridge.
27. Fragaszy D.M. , Mitchell G. ( 1974). "Infant socialization in primates". — J. Hum. Evol. Vol 3: 563- 574. http://dx.doi.org/10.1016/0047-2484(74)90017-7
28. Hamilton W.D. ( 1964). "The genetic evolution of social behavior". — J. Theor. Biol. Vol 7: 1- 51. http://dx.doi.org/10.1016/0022-5193(64)90038-4
29. Hayes L.D. ( 2000). "To nest communally or not to nest communally: a review of rodent communal nesting and nursing". — Anim. Behav. Vol 59: 677- 688. http://dx.doi.org/10.1006/anbe.1999.1390
30. Hewlett B.S. , Winn S. ( 2014). "Allomaternal nursing in humans". — Curr. Anthropol. Vol 55: 200- 229. http://dx.doi.org/10.1086/675657
31. Higgins L.V. , Costa D.P. , Huntley A.C. , Le Boeuf B.J. ( 1988). "Behavioral and physiological measurements of maternal investment in the Stellar sea lion, Eumetopias jubatus ". — Mar. Mamm. Sci. Vol 4: 44- 58. http://dx.doi.org/10.1111/j.1748-7692.1988.tb00181.x
32. Hinde K. ( 2007). "First-time macaque mothers bias milk composition in favor of sons". — Curr. Biol. Vol 17: 958- 959. http://dx.doi.org/10.1016/j.cub.2007.09.029
33. Hinde K. , Milligan L.A. ( 2011). "Primate milk: proximate mechanisms and ultimate perspectives". — Evol. Anthropol. Vol 20: 9- 23. http://dx.doi.org/10.1002/evan.20289
34. Hinde K. , Power M.L. , Oftedal O.T. ( 2009). "Rhesus macaque milk: magnitude, sources, and consequences of individuals variation over lactation". — Am. J. Phys. Anthropol. Vol 138: 148- 157. http://dx.doi.org/10.1002/ajpa.20911
35. Jack K.M. , Fedigan L.M. ( 2006). "Why be alpha male? Dominance and reproductive success in wild white-faced capuchins ( Cebus capucinus)". — In: New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation( Estrada A. , Garber P. , Pavelka M.S.M. , Luecke L. , eds). Springer, New York, NY, p.  367- 386. http://dx.doi.org/10.1007/0-387-25872-8_18
36. Kalinowski S.T. , Taper M.L. , Marshall T.C. ( 2007). "Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment". — Mol. Ecol. Vol 16: 1099- 1106. http://dx.doi.org/10.1111/j.1365-294X.2007.03089.x
37. Kapsalis E. ( 2004). "Matrilineal kinship and primate behavior". — In: Kinship and behavior in primates( Chapais B. , Berman C.M. , eds). Oxford University Press, London, p.  153- 176.
38. Kapsalis E. , Berman C.M. ( 1996). "Models of affiliative relationships among female rhesus monkeys ( Macaca mulatta). I. Criteria for kinship". — Behaviour Vol 133: 1209- 1234. http://dx.doi.org/10.1163/156853996X00378
39. Konig B. ( 1997). "Cooperative care of young in mammals". — Naturwissenschaften Vol 84: 95- 104. http://dx.doi.org/10.1007/s001140050356
40. Konig B. ( 1993). "Maternal investment of communally nursing female house mice ( Mus musculus domesticus)". — Behav. Proc. Vol 30: 61- 74. http://dx.doi.org/10.1016/0376-6357(93)90012-G
41. Kozlov A.P. , Petrov E.S. , Kashinsky W. , Nizhnikov M.E. , Spear N.E. ( 2003). "Oral compression activity on a surrogate nipple in the newborn rat: nutritive and nonnutritive suckling". — Dev. Psychobiol. Vol 43: 290- 303. http://dx.doi.org/10.1002/dev.10145
42. Lancaster J. ( 1971). "Play-mothering: the relations between juvenile females and young infants among free-ranging vervet monkeys ( Cercopithecus aethiops)". — Folia Primatol. Vol 15: 161- 182. http://dx.doi.org/10.1159/000155377
43. Lappan S. ( 2009). "The effects of lactation and infant care on adult energy budgets in wild siamangs ( Symphalangus syndactylus)". — Am. J. Phys. Anthropol. Vol 140: 290- 301. http://dx.doi.org/10.1002/ajpa.21069
44. MacLeod K.J. , Nielsen J.F. , Clutton-Brock T.H. ( 2013). "Factors predicting the frequency, likelihood and duration of allonursing in the cooperatively breeding meerkat". — Anim. Behav. Vol 86: 1059- 1067. http://dx.doi.org/10.1016/j.anbehav.2013.09.012
45. Maestripieri D. ( 1994). "Social structure, infant handling and mothering styles in group-living old world monkeys". — Int. J. Primatol. Vol 15: 531- 553. http://dx.doi.org/10.1007/BF02735970
46. Maestripieri D. ( 2001). "Is there mother-infant bonding in primates?"— Dev. Rev. Vol 21: 93- 120. http://dx.doi.org/10.1006/drev.2000.0522
47. Manson J.H. ( 1999). "Infant handling in wild Cebus capucinus: testing bonds between females?"— Anim. Behav. Vol 57: 911- 921. http://dx.doi.org/10.1006/anbe.1998.1052
48. Marshall T.C. , Slate J. , Kruuk L.E.B. , Pemberton J.M. ( 1998). "Statistical confidence for likelihood-based paternity inference in natural populations". — Mol. Ecol. Vol 7: 639- 655. http://dx.doi.org/10.1046/j.1365-294x.1998.00374.x
49. McCabe G.M. , Fedigan L.M. ( 2007). "Effects of reproductive status on energy intake, ingestion rates and dietary composition of female Cebus capucinusat Santa Rosa, Costa Rica". — Int. J. Primatol. Vol 28: 837- 851. http://dx.doi.org/10.1007/s10764-007-9159-z
50. McKenna J.T. ( 1979). "The evolution of allomothering behavior among colobine monkeys: function and opportunism in evolution". — Am. Anthropol. Vol 81: 818- 840. http://dx.doi.org/10.1525/aa.1979.81.4.02a00040
51. Millar J.S. ( 1978). "Energetics of reproduction in Peromyscus leucopus: the cost lactation". — Ecology Vol 59: 1055- 1061. http://dx.doi.org/10.2307/1938558
52. Muniz L. , Vigilant L. ( 2008). "Isolation and characterization of microsatellite markers in the white-faced capuchin monkey ( Cebus capucinus) and cross-species amplification in other New World monkeys". — Mol. Ecol. Resourc. Vol 8: 402- 405. http://dx.doi.org/10.1111/j.1471-8286.2007.01971.x
53. Muroyama Y. ( 1994). "Exchange of grooming for allomothering in female patas monkeys". — Behaviour Vol 128: 103- 119. http://dx.doi.org/10.1163/156853994X00064
54. O’Brien T.G. ( 1988). "Parasitic nursing behaviour in the wedge-capped capuchin monkey ( Cebus olivaceus)". — Am. J. Primatol. Vol 16: 341- 344. http://dx.doi.org/10.1002/ajp.1350160406
55. O’Brien T.G. , Robinson J.G. ( 1991). "Allomaternal care by female wedge-capped capuchin monkeys: effects of age, rank and relatedness". — Behaviour Vol 119: 30- 50. http://dx.doi.org/10.1163/156853991X00355
56. Packer C. , Lewis S. , Pusey A. ( 1992). "A comparative analysis of non-offspring nursing". — Anim. Behav. Vol 43: 265- 281. http://dx.doi.org/10.1016/S0003-3472(05)80222-2
57. Paul A. , Kuester J. ( 1996). "The sociobiology of the Barbary macaque ( Macaca sylvanus): a summary of the Salem Project (abstract)". — Primate Rep. Vol 44: 35- 36.
58. Pereira M.E. , Klepper A. , Simons E.L. ( 1987). "Tactics of care for young infants by forest-living ruffed lemurs ( Varecia variegata variegata): ground nests, parking and biparental guarding". — Am. J. Primatol. Vol 13: 129- 144. http://dx.doi.org/10.1002/ajp.1350130204
59. Perry S. ( 1996). "Female–female social relationships in wild white-faced capuchin monkeys, Cebus capucinus ". — Am. J. Primatol. Vol 40: 167- 182. http://dx.doi.org/10.1002/(SICI)1098-2345(1996)40:2<167::AID-AJP4>3.0.CO;2-W
60. Perry S. ( 2012). "The behavior of wild white-faced capuchins: demography, life history, social relationships, and communication". — Adv. Stud. Behav. Vol 44: 135- 181. http://dx.doi.org/10.1016/B978-0-12-394288-3.00004-6
61. Perry S. , Manson J.H. , Muniz L. , Gros-Louis J. , Vigilant L. ( 2008). "Kin-biased social behaviour in wild adult female white-faced capuchins, Cebus capucinus ". — Anim. Behav. Vol 76: 187- 199. http://dx.doi.org/10.1016/j.anbehav.2008.01.020
62. Prentice A.M. , Prentice A. ( 1995). "Evolutionary and environmental influences on human lactation". — Proc. Nutr. Soc. Vol 54: 391- 400. http://dx.doi.org/10.1079/PNS19950008
63. Pusey A.E. , Packer C. ( 1994). "Non-offspring nursing in social carnivores: minimizing the costs". — Behav. Ecol. Vol 5: 362- 374. http://dx.doi.org/10.1093/beheco/5.4.362
64. Rendall D. ( 2004). "‘Recognizing’ kin: mechanisms, media, minds, modules and muddles". — In: Kinship and behavior in primates( Chapais B. , Berman C.M. , eds). Oxford University Press, Oxford, p.  295- 316.
65. Rood J.P. ( 1980). "Mating relationships and breeding suppression in the dwarf mongoose". — Anim. Behav. Vol 28: 143- 150. http://dx.doi.org/10.1016/S0003-3472(80)80019-4
66. Rose L.M. ( 1998). Behavioural ecology of white-faced capuchins ( Cebus capucinus) in Costa Rica. — Doctoral dissertation, Washington University, St. Louis, MO.
67. Roulin A. ( 2002). "Why do lactating females nurse alien offspring? A review of hypotheses and empirical evidence". — Anim. Behav. Vol 63: 201- 208. http://dx.doi.org/10.1006/anbe.2001.1895
68. Sayler A. , Salmon M. ( 1969). "Communal nursing in mice: influence of multiple mothers on the growth of the young". — Science Vol 164: 1309- 1310. http://dx.doi.org/10.1126/science.164.3885.1309
69. Seyfarth R.M. ( 1977). "A model of social grooming among adult female monkeys". — J. Theor. Biol. Vol 65: 671- 698. http://dx.doi.org/10.1016/0022-5193(77)90015-7
70. Solomon N.G. , French J.A. ( 1997). Cooperative breeding in mammals. — Cambridge University Press, Cambridge.
71. Tanaka I. ( 1992). "Three phases of lactation in free-ranging Japanese macaques". — Anim. Behav. Vol 44: 129- 139. http://dx.doi.org/10.1016/S0003-3472(05)80762-6
72. Tardif S.D. , Power M. , Oftedal O.T. , Power R.A. , Layne D.G. ( 2001). "Lactation, maternal behavior, and infant growth in common marmoset monkeys ( Callithrix jacchus): effects of maternal size and litter size". — Behav. Ecol. Sociobiol. Vol 51: 17- 25. http://dx.doi.org/10.1007/s002650100400
73. Torrey S. , Widowski T. ( 2007). "Relationship between growth and non-nutritive massage in suckling pigs". — Appl. Anim. Behav. Sci. Vol 107: 32- 44. http://dx.doi.org/10.1016/j.applanim.2006.08.001
74. van Schaik C.P. , Burkart J.M. ( 2010). "Mind the gap: cooperative breeding and the evolution of our unique features". — In: Mind the gap. Tracing the origins of human universals( Kappeler P.M. , Silk J. , eds). Springer, Berlin, p.  477- 496.
75. Vasey N. ( 2007). "The breeding system of wild ruffed lemurs ( Varecia rubra): a preliminary report". — Primates Vol 48: 41- 54. http://dx.doi.org/10.1007/s10329-006-0010-5
76. Walters J.R. ( 1987). "Kin recognition in non-human primates". — In: Kin recognition in animals( Fletcher D.J.C. , Michener C.D. , eds). John Wiley and Sons, New York, p.  359- 393.
77. Weaver A.C. ( 1999). The role of attachment in the development of reconciliation. — Doctoral dissertation, Emory University, Atlanta, GA.
78. Wikberg E.C. , Jack K.M. , Campos F.A. , Fedigan L.M. , Sato A. , Bergstrom M.L. , Hiwatashi T. , Kawamura S. ( 2014). "The effect of male parallel dispersal on group composition in white-faced capuchins ( Cebus capucinus)". — Anim. Behav. Vol 96: 9- 17. http://dx.doi.org/10.1016/j.anbehav.2014.07.016
79. Wilkinson G.S. ( 1987). "Altruism and cooperation in bats". — In: Recent advances in the study of bats( Fenton M.B. , Racey P. , Rayner J.M.V. , eds). Cambridge University Press, Cambridge, p.  299- 323.
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