Interchange between grooming and infant handling in female Tibetan macaques(Macaca thibetana)
|
摘要
In some non-human primates, infants function as a social tool that can bridge relationships among group members. Infants are a desired commodity for group members, and mothers control access to them. The biological market theory suggests that grooming is widespread and represents a commodity that can be exchanged for infant handling. As a limited resource, however, the extent to which infants are interchanged between mothers(females with an infant) and non-mothers(potential handlers,females without an infant) remains unclear. In this study, we collected behavioral data to investigate the relationship between grooming and infant handling in free-ranging Tibetan macaques(Macaca thibetana)at Mt. Huangshan, China. Our results showed that females with infants received more grooming than females without infants. After her infant was handled,mother females received more grooming than they did during daily grooming interactions. However, with the increasing number of infants within the social group, both the grooming that mothers received and the grooming that non-mothers invested for handling infants decreased. We also found that non-mothers invested more time in grooming to gain access to younger infants than older infants. Our results provide evidence that infants are social commodities for both mother and non-mother females. Mothers use infants for obtain grooming and non-mothers use grooming to gain access to infants. The current study implies a bidirectional and complex interchange pattern between grooming and infant handling to compensate for the dyadic grooming disparity in non-human primates.
In some non-human primates, infants function as a social tool that can bridge relationships among group members. Infants are a desired commodity for group members, and mothers control access to them. The biological market theory suggests that grooming is widespread and represents a commodity that can be exchanged for infant handling. As a limited resource, however, the extent to which infants are interchanged between mothers(females with an infant) and non-mothers(potential handlers,females without an infant) remains unclear. In this study, we collected behavioral data to investigate the relationship between grooming and infant handling in free-ranging Tibetan macaques(Macaca thibetana)at Mt. Huangshan, China. Our results showed that females with infants received more grooming than females without infants. After her infant was handled,mother females received more grooming than they did during daily grooming interactions. However, with the increasing number of infants within the social group, both the grooming that mothers received and the grooming that non-mothers invested for handling infants decreased. We also found that non-mothers invested more time in grooming to gain access to younger infants than older infants. Our results provide evidence that infants are social commodities for both mother and non-mother females. Mothers use infants for obtain grooming and non-mothers use grooming to gain access to infants. The current study implies a bidirectional and complex interchange pattern between grooming and infant handling to compensate for the dyadic grooming disparity in non-human primates.
In some non-human primates, infants function as a social tool that can bridge relationships among group members. Infants are a desired commodity for group members, and mothers control access to them. The biological market theory suggests that grooming is widespread and represents a commodity that can be exchanged for infant handling. As a limited resource, however, the extent to which infants are interchanged between mothers(females with an infant) and non-mothers(potential handlers,females without an infant) remains unclear. In this study, we collected behavioral data to investigate the relationship between grooming and infant handling in free-ranging Tibetan macaques(Macaca thibetana)at Mt. Huangshan, China. Our results showed that females with infants received more grooming than females without infants. After her infant was handled,mother females received more grooming than they did during daily grooming interactions. However, with the increasing number of infants within the social group, both the grooming that mothers received and the grooming that non-mothers invested for handling infants decreased. We also found that non-mothers invested more time in grooming to gain access to younger infants than older infants. Our results provide evidence that infants are social commodities for both mother and non-mother females. Mothers use infants for obtain grooming and non-mothers use grooming to gain access to infants. The current study implies a bidirectional and complex interchange pattern between grooming and infant handling to compensate for the dyadic grooming disparity in non-human primates.
引文
Altmann J.1974.Observational study of behaviour sampling methods.Behaviour,49(3):227-267.
Altmann J.2002.Baboon mothers and infants.African Journal of Ecology,40(4):417.
Barrett L,Henzi SP.2001.The utility of grooming in baboon troops.In:No?R,Van Hooff JARAM,Hammerstein P.,Eds Economics in Nature:Social Dilemmas,Mate Choice and Biological Markets.Cambridge:Cambridge University Press,119-145.
Berman CM,Ionica C,Li JH.2007.Supportive and tolerant relationships among male Tibetan macaques at Huangshan,China.Behaviour,144(6):631-661.
Berman CM,Ionica C,Li JH.2004.Dominance style among Macaca thibetana on Mt.Huangshan,China.International Journal of Primatology,25(6):1283-1312.
Castles DL,Whiten A,Aureli F.1999.Social anxiety,relationships and self-directed behaviour among wild female olive baboons.Animal Behaviour,58(6):1207-1215.
De Vries H.1995.An improved test of linearity in dominance hierarchies containing unknown or tied relationships.Animal Behaviour,50(5):1375-1389.
De Wall FBM,Yoshihara D.1983.Reconciliation and redirected affection in rhesus monkeys.Behaviour,85(3):224-241.
Dunayer ES,Berman CM.2017.Infant handling enhances social bonds in free-ranging rhesus macaques(Macaca mulatta).Behaviour,154(7-8):875-907.
Dunbar RIM.2010.The social role of touch in humans and primates:behavioural function and neurobiological mechanisms.Neuroscience&Biobehavioral Reviews,34(2):260-268.
Dunbar RIM.1984.Infant-use by male gelada in agonistic contexts:agonistic buffering,progeny protection or soliciting support?Primates,25(1):28-35.
Frank RE,Silk JB.2009.Grooming exchange between mothers and non-mothers:the price of natal attraction in wild baboons(Papio anubis).Behaviour,146(7):889-906.
Fruteau C,van de Waal E,van Damme E,No?R.2011.Infant access and handling in sooty mangabeys and vervet monkeys.Animal Behaviour,81(1):153-161.
Gammell MP,De Vries H,Jennings DJ,Carlin CM,Hayden TJ.2003.David’s score:A more appropriate dominance ranking method than Clutton-Brock et al.’s index.Animal Behaviour,66(3):601-605.
Gumert MD.2007a.Grooming and infant handling interchange in Macaca fascicularis:The relationship between infant supply and grooming payment.International Journal of Primatology,28(5):1059-1074.
Gumert MD.2007b.Payment for sex in a macaque mating market.Animal Behaviour,74(6):1655-1667.
Gumert MD,Ho MHR.2008.The trade balance of grooming and its coordination of reciprocation and tolerance in Indonesian long-tailed macaques(Macaca fascicularis).Primates,49(3):176-185.
Henzi SP,Barrett L.2002.Infants as a commodity in a baboon market.Animal Behaviour,63(5):915-921.
Hsu MJ,Lin S,Lin JF,Lin TJ,Agoramoorthy G.2016.Non-maternal infant handling in wild formosan macaques of mount longevity,Taiwan.Folia primatologica,86:491-505.
Jin T,Wang DZ,Pan WS,Yao M.2015.Nonmaternal infant handling in wild white-headed langurs(Trachypithecus leucocephalus).International Journal of Primatology,36(2):269-287.
Lehmann J,Korstjens AH,Dunbar RIM.2007.Group size,grooming and social cohesion in primates.Animal Behaviour,74(6):1617-1629.
Li JH.1999.The Tibetan Macaque Society:A Field Study.Hefei,Anhui University Press.(in Chinese)
Li JH,Yin H,Zhou L.2007.Non-reproductive copulation behavior among Tibetan macaques(Macaca thibetana)at Huangshan,China.Primates,48(1):64-72.
Maestripieri D.1994.Social structure,infant handling,and mothering styles in group-living old world monkeys.International Journal of Primatology,15(4):531-553.
Manson JH.1999.Infant handling in wild Cebus capucinus:Testing bonds between females?Animal Behaviour,57(4):911-921.
Nicolson NA.1987.Infants,mothers,and other females.In:Smuts BB,Cheney DL,Seyfarth RM,Wrangham RW,Struhsaker T(Eds).Primate Societies.Chicago:University of Chicago Press,330-342.
No?R,van Schaik CP,van Hooff JARAM.1991.The market effect:an explanation for pay-off asymmetries among collaborating animals.Ethology,87(1-2):97-118.
No?R,van Hooff JARAM,Hammerstein P.2001.Economics in Nature:Social Dilemmas,Mate Choice and Biological Markets.Cambridge:Cambridge University Press.
Seyfarth RM,Cheney DL.1984.Grooming,alliances and reciprocal altruism in vervet monkeys.Nature,308(5959):541-543.
Seyfarth RM.1977.A model of social grooming among adult female monkeys.Journal of Theoretical Biology,65(4):671-698.
Slater KY,Schaffner CM,Aureli F.2007.Embraces for infant handling in spider monkeys:evidence for a biological market?Animal Behaviour,74(3):455-461.
Stanford CB.1992.Costs and benefits of allomothering in wild capped langurs(Presbytis pileata).Behavioral Ecology and Sociobiology,30(1):29-34.
Taub DM.1980.Testing the‘agonistic buffering’hypothesis.Behavioral Ecology and Sociobiology,6(3):187-197.
Tiddi B,Aureli F,Schino G.2010.Grooming for infant handling in tufted capuchin monkeys:a reappraisal of the primate infant market.Animal Behaviour,79(5):1115-1123.
Ueno M.2017.Development of studies on grooming reciprocity in primates.Japanese Journal of Animal Psychology,66(2):91-107.
Watts DP.2002.Reciprocity and interchange in the social relationships of wild male chimpanzees.Behaviour,139:343-370.
Wei W,Qi XG,Garber PA,Guo ST,Zhang P,Li BG.2013.Supply and demand determine the market value of access to infants in the golden snub-nosed monkey(Rhinopithecus roxellana).PLoS One,8(6):e65962.
Wei W,Qi XG,Guo ST,Zhao DP,Zhang P,Huang K,Li BG.2012.Market powers predict reciprocal grooming in golden snub-nosed monkeys(Rhinopithecus roxellana).PLoS One,7(5):e36802.
Wilkinson GS.1984.Reciprocal food sharing in the vampire bat.Nature,308(5955):181-184.
Xia DP,Li JH,Garber PA,Matheson MD,Sun BH,Zhu Y.2013.Grooming reciprocity in male Tibetan macaques.American Journal of Primatology,75(10):1009-1020.
Xia DP,Li JH,Garber PA,Sun LX,Zhu Y,Sun BH.2012.Grooming reciprocity in female Tibetan macaques Macaca thibetana.American journal of Primatology,74(6):568-572.
Yu Y,Xiang ZF,Yao H,Grueter CC,Li M.2013.Female snub-nosed monkeys exchange grooming for sex and infant handling.PLoS One,8(9):e74822.
Altmann J.2002.Baboon mothers and infants.African Journal of Ecology,40(4):417.
Barrett L,Henzi SP.2001.The utility of grooming in baboon troops.In:No?R,Van Hooff JARAM,Hammerstein P.,Eds Economics in Nature:Social Dilemmas,Mate Choice and Biological Markets.Cambridge:Cambridge University Press,119-145.
Berman CM,Ionica C,Li JH.2007.Supportive and tolerant relationships among male Tibetan macaques at Huangshan,China.Behaviour,144(6):631-661.
Berman CM,Ionica C,Li JH.2004.Dominance style among Macaca thibetana on Mt.Huangshan,China.International Journal of Primatology,25(6):1283-1312.
Castles DL,Whiten A,Aureli F.1999.Social anxiety,relationships and self-directed behaviour among wild female olive baboons.Animal Behaviour,58(6):1207-1215.
De Vries H.1995.An improved test of linearity in dominance hierarchies containing unknown or tied relationships.Animal Behaviour,50(5):1375-1389.
De Wall FBM,Yoshihara D.1983.Reconciliation and redirected affection in rhesus monkeys.Behaviour,85(3):224-241.
Dunayer ES,Berman CM.2017.Infant handling enhances social bonds in free-ranging rhesus macaques(Macaca mulatta).Behaviour,154(7-8):875-907.
Dunbar RIM.2010.The social role of touch in humans and primates:behavioural function and neurobiological mechanisms.Neuroscience&Biobehavioral Reviews,34(2):260-268.
Dunbar RIM.1984.Infant-use by male gelada in agonistic contexts:agonistic buffering,progeny protection or soliciting support?Primates,25(1):28-35.
Frank RE,Silk JB.2009.Grooming exchange between mothers and non-mothers:the price of natal attraction in wild baboons(Papio anubis).Behaviour,146(7):889-906.
Fruteau C,van de Waal E,van Damme E,No?R.2011.Infant access and handling in sooty mangabeys and vervet monkeys.Animal Behaviour,81(1):153-161.
Gammell MP,De Vries H,Jennings DJ,Carlin CM,Hayden TJ.2003.David’s score:A more appropriate dominance ranking method than Clutton-Brock et al.’s index.Animal Behaviour,66(3):601-605.
Gumert MD.2007a.Grooming and infant handling interchange in Macaca fascicularis:The relationship between infant supply and grooming payment.International Journal of Primatology,28(5):1059-1074.
Gumert MD.2007b.Payment for sex in a macaque mating market.Animal Behaviour,74(6):1655-1667.
Gumert MD,Ho MHR.2008.The trade balance of grooming and its coordination of reciprocation and tolerance in Indonesian long-tailed macaques(Macaca fascicularis).Primates,49(3):176-185.
Henzi SP,Barrett L.2002.Infants as a commodity in a baboon market.Animal Behaviour,63(5):915-921.
Hsu MJ,Lin S,Lin JF,Lin TJ,Agoramoorthy G.2016.Non-maternal infant handling in wild formosan macaques of mount longevity,Taiwan.Folia primatologica,86:491-505.
Jin T,Wang DZ,Pan WS,Yao M.2015.Nonmaternal infant handling in wild white-headed langurs(Trachypithecus leucocephalus).International Journal of Primatology,36(2):269-287.
Lehmann J,Korstjens AH,Dunbar RIM.2007.Group size,grooming and social cohesion in primates.Animal Behaviour,74(6):1617-1629.
Li JH.1999.The Tibetan Macaque Society:A Field Study.Hefei,Anhui University Press.(in Chinese)
Li JH,Yin H,Zhou L.2007.Non-reproductive copulation behavior among Tibetan macaques(Macaca thibetana)at Huangshan,China.Primates,48(1):64-72.
Maestripieri D.1994.Social structure,infant handling,and mothering styles in group-living old world monkeys.International Journal of Primatology,15(4):531-553.
Manson JH.1999.Infant handling in wild Cebus capucinus:Testing bonds between females?Animal Behaviour,57(4):911-921.
Nicolson NA.1987.Infants,mothers,and other females.In:Smuts BB,Cheney DL,Seyfarth RM,Wrangham RW,Struhsaker T(Eds).Primate Societies.Chicago:University of Chicago Press,330-342.
No?R,van Schaik CP,van Hooff JARAM.1991.The market effect:an explanation for pay-off asymmetries among collaborating animals.Ethology,87(1-2):97-118.
No?R,van Hooff JARAM,Hammerstein P.2001.Economics in Nature:Social Dilemmas,Mate Choice and Biological Markets.Cambridge:Cambridge University Press.
Seyfarth RM,Cheney DL.1984.Grooming,alliances and reciprocal altruism in vervet monkeys.Nature,308(5959):541-543.
Seyfarth RM.1977.A model of social grooming among adult female monkeys.Journal of Theoretical Biology,65(4):671-698.
Slater KY,Schaffner CM,Aureli F.2007.Embraces for infant handling in spider monkeys:evidence for a biological market?Animal Behaviour,74(3):455-461.
Stanford CB.1992.Costs and benefits of allomothering in wild capped langurs(Presbytis pileata).Behavioral Ecology and Sociobiology,30(1):29-34.
Taub DM.1980.Testing the‘agonistic buffering’hypothesis.Behavioral Ecology and Sociobiology,6(3):187-197.
Tiddi B,Aureli F,Schino G.2010.Grooming for infant handling in tufted capuchin monkeys:a reappraisal of the primate infant market.Animal Behaviour,79(5):1115-1123.
Ueno M.2017.Development of studies on grooming reciprocity in primates.Japanese Journal of Animal Psychology,66(2):91-107.
Watts DP.2002.Reciprocity and interchange in the social relationships of wild male chimpanzees.Behaviour,139:343-370.
Wei W,Qi XG,Garber PA,Guo ST,Zhang P,Li BG.2013.Supply and demand determine the market value of access to infants in the golden snub-nosed monkey(Rhinopithecus roxellana).PLoS One,8(6):e65962.
Wei W,Qi XG,Guo ST,Zhao DP,Zhang P,Huang K,Li BG.2012.Market powers predict reciprocal grooming in golden snub-nosed monkeys(Rhinopithecus roxellana).PLoS One,7(5):e36802.
Wilkinson GS.1984.Reciprocal food sharing in the vampire bat.Nature,308(5955):181-184.
Xia DP,Li JH,Garber PA,Matheson MD,Sun BH,Zhu Y.2013.Grooming reciprocity in male Tibetan macaques.American Journal of Primatology,75(10):1009-1020.
Xia DP,Li JH,Garber PA,Sun LX,Zhu Y,Sun BH.2012.Grooming reciprocity in female Tibetan macaques Macaca thibetana.American journal of Primatology,74(6):568-572.
Yu Y,Xiang ZF,Yao H,Grueter CC,Li M.2013.Female snub-nosed monkeys exchange grooming for sex and infant handling.PLoS One,8(9):e74822.