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

in Behaviour
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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.

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

in Behaviour



AlfaroJ.W.SilvaJ.RylandsA.B. (2012). How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. — Am. J. Primatol. 74: 381-393.

AltmannJ. (1974). Observational study of behaviour: sampling methods. — Behaviour 49: 227-267.

ApplebyM.C. (1983). The probability of linearity in hierarchies. — Anim. Behav. 31: 600-608.

BaldovinoM.C.Di BitettiM.S. (2008). Allonursing in tufted capuchin monkeys (Cebus nigritus): milk or pacifier?Folia Primatol. 79: 79-92.

BergstromM.L.FediganL.M. (2010). Dominance among female white-faced capuchin monkeys (Cebus capucinus): hierarchical linearity, nepotism, strength and stability. — Behaviour 147: 899-931.

BergstromM.L.FediganL.M. (2013). Dominance style of female white-faced capuchins. — Am. J. Phys. Anthropol. 150: 591-601.

BirgerssonB.EkvallJ.TemrinH. (1991). Allosuckling in fallow deer, Dama dama. — Anim. Behav. 42: 326-327.

BissetG.W. (1974). Milk ejection. — In: Handbook of physiology and endocrinology Part 1 ( KnobilE.SawyerW.H. eds). American Physiological SocietyWashington, DC p.  493-526.

BoubliJ.P.RylandsA.B.FariasI.P.AlfaroM.E.AlfaroL. (2012). Cebus phylogenetic relationships: a preliminary reassessment of the diversity of the untufted capuchin monkeys. — Am. J. Primatol. 74: 381-393.

BoydR.RichersonP.J. (1988). The evolution of reciprocity in sizable groups. — J. Theor. Biol. 132: 337-356.

BurkartJ.M.HrdyS.B.van SchaikC.P. (2009). Cooperative breeding and human cognitive evolution. — Evol. Anthropol. 18: 175-176.

CameronE.Z. (1998). Is suckling behaviour a useful predictor of milk intake? A review. — Anim. Behav. 58: 521-532.

CarnegieS.D.FediganL.M.MelinA.D. (2011). Reproductive seasonality in female capuchins (Cebus capucinus). — Int. J. Primatol. 32: 1076-1090.

CarnegieS.D.FediganL.M.ZieglerT.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 ( EstradaA.GarberP.A.PavelkaM.S.M.LueckeL. eds). SpringerNew York, NY p.  387-409.

CarsonK.Wood-GushD.G.M. (1983). Equine behaviour: a review of the literature on social and dam–foal behaviour. — Appl. Anim. Ethol. 10: 165-178.

ChapaisB. (2001). Primate nepotism: what is the explanatory value of kin selection. — Int. J. Primatol. 22: 203-229.

Clutton-BrockT.H. (2006). Cooperative breeding in mammals. — In: Cooperation in primates and humans: mechanisms and evolution ( KappelerP.M.van SchaikC.P. eds). SpringerBerlin p.  173-190.

Clutton-BrockT.H. (1991). The evolution of parental care. — Princeton University PressPrinceton, NJ.

Clutton-BrockT.H.AlbonS.D.GuinessF.E. (1989). Fitness costs of gestation and lactation in wild animals. — Nature 337: 260-262.

Cortés-OrtizL.MondragónE.CabotageJ. (2010). Isolation and characterization of microsatellite loci for the study of Mexican howler monkeys, their natural hybrids, and other Neotropical primates. — Conserv. Gen. Resourc. 2: 21-26.

de WaalF.M.B.LeimgruberK.GreenbergA.R. (2008). Giving is self-rewarding for monkeys. — Proc. Natl. Acad. Sci. USA 105: 13685-13689.

FediganL.M. (2003). Impact of male takeovers on infant deaths, births, and conceptions in Cebus capucinus at Santa Rosa, Costa Rica. — Int. J. Primatol. 24: 723-741.

FediganL.M.JackK. (2001). Neotropical primates in a regenerating Costa Rican dry forest: a comparison of howler and capuchin population patterns. — Int. J. Primatol. 22: 689-713.

Festa-BianchetM. (1988). Nursing behaviour of bighorn sheep: correlates of ewe age, parasitism, lamb age, birthdate and sex. — Anim. Behav. 36: 1445-1454.

FletcherI.C. (1971). Relationships between frequency of suckling, lamb growth and post-partum oestrous behaviour in ewes. — Anim. Behav. 19: 108-111.

FragaszyD.M.VisalberghiE.FediganL.M. (2004). The complete capuchin: the biology of the genus Cebus. — Cambridge University PressCambridge.

FragaszyD.M.MitchellG. (1974). Infant socialization in primates. — J. Hum. Evol. 3: 563-574.

HamiltonW.D. (1964). The genetic evolution of social behavior. — J. Theor. Biol. 7: 1-51.

HayesL.D. (2000). To nest communally or not to nest communally: a review of rodent communal nesting and nursing. — Anim. Behav. 59: 677-688.

HewlettB.S.WinnS. (2014). Allomaternal nursing in humans. — Curr. Anthropol. 55: 200-229.

HigginsL.V.CostaD.P.HuntleyA.C.Le BoeufB.J. (1988). Behavioral and physiological measurements of maternal investment in the Stellar sea lion, Eumetopias jubatus. — Mar. Mamm. Sci. 4: 44-58.

HindeK. (2007). First-time macaque mothers bias milk composition in favor of sons. — Curr. Biol. 17: 958-959.

HindeK.MilliganL.A. (2011). Primate milk: proximate mechanisms and ultimate perspectives. — Evol. Anthropol. 20: 9-23.

HindeK.PowerM.L.OftedalO.T. (2009). Rhesus macaque milk: magnitude, sources, and consequences of individuals variation over lactation. — Am. J. Phys. Anthropol. 138: 148-157.

JackK.M.FediganL.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 ( EstradaA.GarberP.PavelkaM.S.M.LueckeL. eds). SpringerNew York, NY p.  367-386.

KalinowskiS.T.TaperM.L.MarshallT.C. (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. — Mol. Ecol. 16: 1099-1106.

KapsalisE. (2004). Matrilineal kinship and primate behavior. — In: Kinship and behavior in primates ( ChapaisB.BermanC.M. eds). Oxford University PressLondon p.  153-176.

KapsalisE.BermanC.M. (1996). Models of affiliative relationships among female rhesus monkeys (Macaca mulatta). I. Criteria for kinship. — Behaviour 133: 1209-1234.

KonigB. (1997). Cooperative care of young in mammals. — Naturwissenschaften 84: 95-104.

KonigB. (1993). Maternal investment of communally nursing female house mice (Mus musculus domesticus). — Behav. Proc. 30: 61-74.

KozlovA.P.PetrovE.S.KashinskyW.NizhnikovM.E.SpearN.E. (2003). Oral compression activity on a surrogate nipple in the newborn rat: nutritive and nonnutritive suckling. — Dev. Psychobiol. 43: 290-303.

LancasterJ. (1971). Play-mothering: the relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops). — Folia Primatol. 15: 161-182.

LappanS. (2009). The effects of lactation and infant care on adult energy budgets in wild siamangs (Symphalangus syndactylus). — Am. J. Phys. Anthropol. 140: 290-301.

MacLeodK.J.NielsenJ.F.Clutton-BrockT.H. (2013). Factors predicting the frequency, likelihood and duration of allonursing in the cooperatively breeding meerkat. — Anim. Behav. 86: 1059-1067.

MaestripieriD. (1994). Social structure, infant handling and mothering styles in group-living old world monkeys. — Int. J. Primatol. 15: 531-553.

MaestripieriD. (2001). Is there mother-infant bonding in primates?Dev. Rev. 21: 93-120.

MansonJ.H. (1999). Infant handling in wild Cebus capucinus: testing bonds between females?Anim. Behav. 57: 911-921.

MarshallT.C.SlateJ.KruukL.E.B.PembertonJ.M. (1998). Statistical confidence for likelihood-based paternity inference in natural populations. — Mol. Ecol. 7: 639-655.

McCabeG.M.FediganL.M. (2007). Effects of reproductive status on energy intake, ingestion rates and dietary composition of female Cebus capucinus at Santa Rosa, Costa Rica. — Int. J. Primatol. 28: 837-851.

McKennaJ.T. (1979). The evolution of allomothering behavior among colobine monkeys: function and opportunism in evolution. — Am. Anthropol. 81: 818-840.

MillarJ.S. (1978). Energetics of reproduction in Peromyscus leucopus: the cost lactation. — Ecology 59: 1055-1061.

MunizL.VigilantL. (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. 8: 402-405.

MuroyamaY. (1994). Exchange of grooming for allomothering in female patas monkeys. — Behaviour 128: 103-119.

O’BrienT.G. (1988). Parasitic nursing behaviour in the wedge-capped capuchin monkey (Cebus olivaceus). — Am. J. Primatol. 16: 341-344.

O’BrienT.G.RobinsonJ.G. (1991). Allomaternal care by female wedge-capped capuchin monkeys: effects of age, rank and relatedness. — Behaviour 119: 30-50.

PackerC.LewisS.PuseyA. (1992). A comparative analysis of non-offspring nursing. — Anim. Behav. 43: 265-281.

PaulA.KuesterJ. (1996). The sociobiology of the Barbary macaque (Macaca sylvanus): a summary of the Salem Project (abstract). — Primate Rep. 44: 35-36.

PereiraM.E.KlepperA.SimonsE.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. 13: 129-144.

PerryS. (1996). Female–female social relationships in wild white-faced capuchin monkeys, Cebus capucinus. — Am. J. Primatol. 40: 167-182.

PerryS. (2012). The behavior of wild white-faced capuchins: demography, life history, social relationships, and communication. — Adv. Stud. Behav. 44: 135-181.

PerryS.MansonJ.H.MunizL.Gros-LouisJ.VigilantL. (2008). Kin-biased social behaviour in wild adult female white-faced capuchins, Cebus capucinus. — Anim. Behav. 76: 187-199.

PrenticeA.M.PrenticeA. (1995). Evolutionary and environmental influences on human lactation. — Proc. Nutr. Soc. 54: 391-400.

PuseyA.E.PackerC. (1994). Non-offspring nursing in social carnivores: minimizing the costs. — Behav. Ecol. 5: 362-374.

RendallD. (2004). ‘Recognizing’ kin: mechanisms, media, minds, modules and muddles. — In: Kinship and behavior in primates ( ChapaisB.BermanC.M. eds). Oxford University PressOxford p.  295-316.

RoodJ.P. (1980). Mating relationships and breeding suppression in the dwarf mongoose. — Anim. Behav. 28: 143-150.

RoseL.M. (1998). Behavioural ecology of white-faced capuchins (Cebus capucinus) in Costa Rica. — Doctoral dissertation Washington University St. Louis MO.

RoulinA. (2002). Why do lactating females nurse alien offspring? A review of hypotheses and empirical evidence. — Anim. Behav. 63: 201-208.

SaylerA.SalmonM. (1969). Communal nursing in mice: influence of multiple mothers on the growth of the young. — Science 164: 1309-1310.

SeyfarthR.M. (1977). A model of social grooming among adult female monkeys. — J. Theor. Biol. 65: 671-698.

SolomonN.G.FrenchJ.A. (1997). Cooperative breeding in mammals. — Cambridge University PressCambridge.

TanakaI. (1992). Three phases of lactation in free-ranging Japanese macaques. — Anim. Behav. 44: 129-139.

TardifS.D.PowerM.OftedalO.T.PowerR.A.LayneD.G. (2001). Lactation, maternal behavior, and infant growth in common marmoset monkeys (Callithrix jacchus): effects of maternal size and litter size. — Behav. Ecol. Sociobiol. 51: 17-25.

TorreyS.WidowskiT. (2007). Relationship between growth and non-nutritive massage in suckling pigs. — Appl. Anim. Behav. Sci. 107: 32-44.

van SchaikC.P.BurkartJ.M. (2010). Mind the gap: cooperative breeding and the evolution of our unique features. — In: Mind the gap. Tracing the origins of human universals ( KappelerP.M.SilkJ. eds). SpringerBerlin p.  477-496.

VaseyN. (2007). The breeding system of wild ruffed lemurs (Varecia rubra): a preliminary report. — Primates 48: 41-54.

WaltersJ.R. (1987). Kin recognition in non-human primates. — In: Kin recognition in animals ( FletcherD.J.C.MichenerC.D. eds). John Wiley and SonsNew York p.  359-393.

WeaverA.C. (1999). The role of attachment in the development of reconciliation. — Doctoral dissertation Emory University Atlanta GA.

WikbergE.C.JackK.M.CamposF.A.FediganL.M.SatoA.BergstromM.L.HiwatashiT.KawamuraS. (2014). The effect of male parallel dispersal on group composition in white-faced capuchins (Cebus capucinus). — Anim. Behav. 96: 9-17.

WilkinsonG.S. (1987). Altruism and cooperation in bats. — In: Recent advances in the study of bats ( FentonM.B.RaceyP.RaynerJ.M.V. eds). Cambridge University PressCambridge p.  299-323.


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    Mean rate (bouts/h ± SE) of nursing (dark grey) and allonursing (light grey) bouts across infant age (months).

  • View in gallery

    Mean duration (s ± SE) of nursing (dark grey) and allonursing (light grey) bouts across infant age (months).

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    Mean rate (bouts/h ± SE) and the mean duration (s ± SE) of allonursing behaviour for nulliparous non-lactating, parous non-lactating and parous lactating females.

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    Mean rate (bouts/h ± SE) and the mean duration (s ± SE) of allonursing behaviour for maternally unrelated and related infant–allonurse dyads.


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