雄性短尾猴个体特征与临时配偶关系研究
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摘要
多雄多雌的灵长类社会群体中,性成熟的雄性和雌性形成临时性的配偶关系(Consortship)是极其显著特征,但这种关系对个体的交配和繁殖成功的作用缺少深入研究。本研究以栖息于安徽黄山的短尾猴YA1群为研究对象,采用全事件取样法(All occurrences recording)、目标动物取样法(Focal animal sampling)以及行为取样法(Behavioral sampling method)记录个体间的社会行为、雄性的配偶数量和临时配偶关系的持续时间,对雄性短尾猴临时配偶关系的基本特征与适应策略进行了初步探讨。研究期间,雄性个体的顺位发生替换,在替换前后,处于高顺位的雄性个体始终拥有最多的配偶数量以及形成临时配偶关系的持续时间最长,并且雄性个体的顺位与临时配偶关系呈正相关关系(顺位变化前:配偶数量,P=0.010;持续时间,P=0.014;顺位变化后:配偶数量,P=0.032;持续时间,P=0.035);雄性个体的年龄与临时配偶关系无显著相关性(配偶关系:P=0.150;持续时间:P=0.511);雄性个体在群体中生活的时间与临时配偶关系呈显著正相关(配偶数量:P=0.034;持续时间:P=0.023);雄性个体的社会关系与临时配偶关系呈显著正相关(顺位变化前:配偶数量,P=0.013;持续时间,P=0.001;顺位变化后:配偶数量,P<0.001;持续时间,P=0.003)。研究结果表明:雄性个体的顺位、在群体中生活时间以及社会关系对临时配偶的形成起主要作用,这为进一步阐明雄性行为策略与临时配偶关系提供新的科学依据。
In polygynandrous nonhuman primates,an adult male and an oestrous female often form a temporary sexual relationship. However,few studies have focused on how consortships affect polygynandrous males' mating behavior and reproductive success. In this study,we collected data on male-female social interactions,consort partners,and consortship durations in a group( YA1) of free-ranging Tibetan macaques( Macaca thibetana) at Mt. Huangshan,China using all occurrences and focal animal and behavioral sampling methods. We used our observations to discuss males' characteristics and their relationships to consortships. During the study period,male ranks within the group changed. Both before and after the male rank change,we found a positive correlation between a male's rank and his number of consort partners( before rank change P = 0. 010,after rank change P = 0. 032) and the duration of his consortships( before rank change P = 0. 014;after rank change P = 0. 035). We found no significant correlation between a male's age and the number of his consortship partners( P = 0. 150) or the duration of his consorts( P = 0. 511),but the length of his tenure in the group was positively correlated to both his number of his consort partners( P = 0. 034) and the duration of his consortships( P =0. 023). Both before and after the change of male rank,a male's social interactions positively correlated to his number of consort partners( before rank change P = 0. 013; after rank change P < 0. 001) and with duration of his consortships( before rank change P = 0. 001; after rank change P = 0. 003). Our data indicate that male rank,length of tenure in the group,and social interactions with females all influence males' consortship formations. Our study provides new scientific evidence for understanding male reproductive strategies and consortship behaviors.
In polygynandrous nonhuman primates,an adult male and an oestrous female often form a temporary sexual relationship. However,few studies have focused on how consortships affect polygynandrous males' mating behavior and reproductive success. In this study,we collected data on male-female social interactions,consort partners,and consortship durations in a group( YA1) of free-ranging Tibetan macaques( Macaca thibetana) at Mt. Huangshan,China using all occurrences and focal animal and behavioral sampling methods. We used our observations to discuss males' characteristics and their relationships to consortships. During the study period,male ranks within the group changed. Both before and after the male rank change,we found a positive correlation between a male's rank and his number of consort partners( before rank change P = 0. 010,after rank change P = 0. 032) and the duration of his consortships( before rank change P = 0. 014;after rank change P = 0. 035). We found no significant correlation between a male's age and the number of his consortship partners( P = 0. 150) or the duration of his consorts( P = 0. 511),but the length of his tenure in the group was positively correlated to both his number of his consort partners( P = 0. 034) and the duration of his consortships( P =0. 023). Both before and after the change of male rank,a male's social interactions positively correlated to his number of consort partners( before rank change P = 0. 013; after rank change P < 0. 001) and with duration of his consortships( before rank change P = 0. 001; after rank change P = 0. 003). Our data indicate that male rank,length of tenure in the group,and social interactions with females all influence males' consortship formations. Our study provides new scientific evidence for understanding male reproductive strategies and consortship behaviors.
引文
Alberts S C,Buchan J C,Altmann J.2006.Sexual selection in wild baboons:from mating opportunities to paternity success.Animal Behaviour,72(5):1177-1196.
Altmann J.1974.Observational study of behavior:sampling methods.Behaviour,49(3):227-267.
Altmann S A.1962.A field study of the sociobiology of rhesus monkeys,Macaca mulatta.Ann N Y Acad Sci,102:338-435.
Balasubramaniam K N,Berman C M,Ogawa H,Li J H.2011.Using biological markets principles to examine patterns of grooming exchange in Macaca thibetana.Am J Primatol,73(12):1269-1279.
Berard J D,Nürnberg P,Epplen J T,Schmidtke J.1993.Male rank,reproductive behavior,and reproductive success in free-ranging rhesus macaques.Primates,34(4):481-489.
Bercovitch F B,Nürnberg P.1997.Genetic determination of paternity and variation in male reproductive success in two populations of rhesus macaques.Slectrophoresis,18(9):1701-1705.
Berman C M,Ionica C S,Li J H.2004.Dominance style among Macaca thibetana on Mt.Huangshan,China.International Journal of Primatology,25(6):1283-1312.
Brauch K,Hodges K,Engelhardt A,Fuhrmann K,Shaw E,Heistermann M.2008.Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques(Macaca sylvanus).Behavioral E-cology and Sociobiology,62(9):1453-1466.
De Marco A,Cozzolino R,Dessì-Fulgheri F,Thierry B.2011.Interactions between third parties and consortship partners in Tonkean Macaques(Macaca tonkeana).International Journal of Primatology,32(3):708-720.
De Waal F.1982.Chimpanzee Politics:Power and Sex Among Apes.Baltimore:Johns Hopkins University Press.
Dixson A F.1998.Primate Sexuality:Comparative Studies of the Prosimians,Monkeys,Apes,and Human Beings.Oxford:Oxford University Press.
Dixson A F,Anderson M J.2002.Sexual selection,seminal coagulation and copulatory plug formation in primates.Folia Primatologica,73(2-3):63-69.
Dubuc C,Muniz L,Heistermann M,Engelhardt A,Widdig A.2011.Testing the priority-of-access model in a seasonally breeding primate species.Behav Ecol Sociobiol,65(8):1615-1627.
Gu Z Y,Chen R,Sun B H,Wang X,Xia D P,Li J H.2017.Social bond strength and its influencing factors in adult female Tibetan macaques(Macaca thibetana).Acta Theriologica Sinica,37(4):363-370.(in Chinese)
Gammell M P,De Vries H,Jennings D J,Carlin C O M,Hayden T J.2003.David’s score:a more appropriate dominance ranking method than Clutton-Brock et al.’s index.Animal Behaviour,66(3):601-605.
Higham J P,Heistermann M,Maestripieri D.2011.The energetics of male-male endurance rivalry in free-ranging rhesus macaques,Macaca mulatta.Animal Behaviour,81(5):1001-1007.
Hill D A.1987.Social relationships between adult male and female rhesus macaques 1 sexual consortships.Primates,28(4):439-456.
Kokko H,Brooks R,Jennions M D,Morley J.2003.The evolution of mate choice and mating biases.Proc Biol Sci,270(1515):653-664.
Kulik L,Muniz L,Mundry R,Widdig A.2012.Patterns of interventions and the effect of coalitions and sociality on male fitness.Mol Ecol,21(3):699-714.
Li J H.1999.The Tibetan Macaque Society:A Field Study.Hefei:Anhui University Press.(in Chinese)
Li J H.2000.The cognition of rank in Tibetan macaques.Journal of Anhui University(Natural Science Edition),24(3):116-120.(in Chinese)
Li J H,Yin H B,Zhou L Z,Ge J Z.2004.Social behaviors and relationships among Thibetan macaques.Chinese Journal of Zoology,39(1):40-44.(in Chinese)
Li J H,Yin H B,Wang Q S.2005.Seasonality of reproduction and sexual activity in female Tibetan macaques Macaca thibetana at Huangshan,China.Acta Zoologica Sinica,51(3):365-375.
Lukas D,Clutton-Brock T H.2013.The evolution of social monogamy in mammals.Science,341(6145):526-530.
Newman M E J.2004.Analysis of weighted networks.Physical Review EStatistical Nonlinear&Soft Matter Physics,70(2):1-9.
NoёR,Sluijter A A.1990.Reproductive tactics of male savanna Baboons.Behaviour,113(1-2):117-170.
Rakhovskaya M V.2013.Correlates of male consortship rate in free-ranging rhesus macaques(Macaca mulatta).International Journal of Primatology,34(4):662-680.
Schroeder J,Nakagawa S,Rees M,Mannarelli M E,Burke T.2015.Reduced fitness in progeny from old parents in a natural population.Proc Natl Acad Sci USA,112(13):4021-4025.
Schülke O,Bhagavatula J,Vigilant L,Ostner J.2010.Social bonds enhance reproductive success in male macaques.Curr Biol,20(24):2207-2210.
Silk J B,Alberts S C,Altmann J.2006.Social relationships among adult female baboons(Papio cynocephalus)II.Variation in the quality and stability of social bonds.Behavioral Ecology and Sociobiology,61(2):197-204.
Soltis J.1999.Measuring male-female relationships during the mating season in wild Japanese macaques(Macaca fuscata yakui).Primates,40(3):453-467.
Tutin C E G.1979.Mating patterns and reproductive strategies in a community of wild Chimpanzees(Pan troglodytes schweinfurthii).Behavioral Ecology&Sociobiology,6(1):29-38.
Van Noordwijk M A.1985.Sexual behaviour of sumatran long-tailed macaques(Macaca fascictclaris).Z Tierpsychol,70(4):277-296.
Wang X,Sun L X,Sheeran L K,Sun B H,Zhang Q X,Zhang D,Xia D P,Li J H.2016.Social rank versus affiliation:Which is more closely related to leadership of group movements in Tibetan macaques(Macaca thibetana)?Am J Primatol,78(8):816-824.
Watts D P.2010.In Mind the Gap:Tracing the Origins of Human Universals.New York:Springer,109-139.
Weingrill T,Lycett J E,Barrett L,Hill R A,Henzi S P.2003.Male consortship behaviour in chacma baboons:the role of demographic factors and female conceptive probabilities.Behaviour,140(3):405-427.
Weingrill T,Lycett J E,Henzi S P.2000.Consortship and mating success in Chacma baboons(Papio cynocephalus ursinus).Ethology,106(11):1033-1044.
Wickings E J,Bossi T,Dixson A F.1993.Reproductive success in the mandrill,Mandrillus sphinx:correlations of male dominance and mating success with paternity,as determined by DNA fingerprinting.Journal of Zoology,231(4):563-574.
Widdig A,Bercovitch F B,Streich W J,Sauermann U,Nurnberg P,Krawczak M.2004.A longitudinal analysis of reproductive skew in male rhesus macaques.Proc Biol Sci,271(1541):819-826.
Xiong C P,Wang Q S.1991.A Comparative study on the male sexual behavior in Tibetan macaques and Japanese monkey.Acta Theriologica Sinica,11(1):13-22.(in Chinese)
Xia D P,Li J H,Garber P A,Matheson M D,Sun B H,Zhu Y.2013.Grooming reciprocity in male Tibetan macaques.Am J Primatol,75(10):1009-1020.
Zhang M,Li J H,Zhu Y,Wang X,Wang S.2010.Male mate choice in Tibetan macaques Macaca thibetana at Mt.Huangshan,China.Current Zoology,56(2):213-221.
Zhao Q K.1993.Sexual behavior of Tibetan macaques at Mt.Emei,China.Primates,34(4):431-444.
Ziv E B,Ilany A,Demartsev V,Barocas A,Geffen E,Koren L.2016.Individual,social,and sexual niche traits affect copulation success in a polygynandrous mating system.Behavioral Ecology&Sociobiology,70(6):901-912.
李进华.1999.野生短尾猴的社会.合肥:安徽大学出版社.
李进华.2000.短尾猴对顺位关系的认知.安徽大学学报:自然科学版,24(3):116-120.
李进华,尹华宝,周立志,葛继志.2004.短尾猴的社会行为与社会关系.动物学杂志,39(1):40-44.
顾志远,陈锐,孙丙华,王希,夏东坡,李进华.2017.成年雌性短尾猴的社会联系强度及影响因素.兽类学报,37(4):363-370.
熊成培,王岐山.1991.短尾猴和日本猴雄性性行为的比较研究.兽类学报,11(1):13-22.
Altmann J.1974.Observational study of behavior:sampling methods.Behaviour,49(3):227-267.
Altmann S A.1962.A field study of the sociobiology of rhesus monkeys,Macaca mulatta.Ann N Y Acad Sci,102:338-435.
Balasubramaniam K N,Berman C M,Ogawa H,Li J H.2011.Using biological markets principles to examine patterns of grooming exchange in Macaca thibetana.Am J Primatol,73(12):1269-1279.
Berard J D,Nürnberg P,Epplen J T,Schmidtke J.1993.Male rank,reproductive behavior,and reproductive success in free-ranging rhesus macaques.Primates,34(4):481-489.
Bercovitch F B,Nürnberg P.1997.Genetic determination of paternity and variation in male reproductive success in two populations of rhesus macaques.Slectrophoresis,18(9):1701-1705.
Berman C M,Ionica C S,Li J H.2004.Dominance style among Macaca thibetana on Mt.Huangshan,China.International Journal of Primatology,25(6):1283-1312.
Brauch K,Hodges K,Engelhardt A,Fuhrmann K,Shaw E,Heistermann M.2008.Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques(Macaca sylvanus).Behavioral E-cology and Sociobiology,62(9):1453-1466.
De Marco A,Cozzolino R,Dessì-Fulgheri F,Thierry B.2011.Interactions between third parties and consortship partners in Tonkean Macaques(Macaca tonkeana).International Journal of Primatology,32(3):708-720.
De Waal F.1982.Chimpanzee Politics:Power and Sex Among Apes.Baltimore:Johns Hopkins University Press.
Dixson A F.1998.Primate Sexuality:Comparative Studies of the Prosimians,Monkeys,Apes,and Human Beings.Oxford:Oxford University Press.
Dixson A F,Anderson M J.2002.Sexual selection,seminal coagulation and copulatory plug formation in primates.Folia Primatologica,73(2-3):63-69.
Dubuc C,Muniz L,Heistermann M,Engelhardt A,Widdig A.2011.Testing the priority-of-access model in a seasonally breeding primate species.Behav Ecol Sociobiol,65(8):1615-1627.
Gu Z Y,Chen R,Sun B H,Wang X,Xia D P,Li J H.2017.Social bond strength and its influencing factors in adult female Tibetan macaques(Macaca thibetana).Acta Theriologica Sinica,37(4):363-370.(in Chinese)
Gammell M P,De Vries H,Jennings D J,Carlin C O M,Hayden T J.2003.David’s score:a more appropriate dominance ranking method than Clutton-Brock et al.’s index.Animal Behaviour,66(3):601-605.
Higham J P,Heistermann M,Maestripieri D.2011.The energetics of male-male endurance rivalry in free-ranging rhesus macaques,Macaca mulatta.Animal Behaviour,81(5):1001-1007.
Hill D A.1987.Social relationships between adult male and female rhesus macaques 1 sexual consortships.Primates,28(4):439-456.
Kokko H,Brooks R,Jennions M D,Morley J.2003.The evolution of mate choice and mating biases.Proc Biol Sci,270(1515):653-664.
Kulik L,Muniz L,Mundry R,Widdig A.2012.Patterns of interventions and the effect of coalitions and sociality on male fitness.Mol Ecol,21(3):699-714.
Li J H.1999.The Tibetan Macaque Society:A Field Study.Hefei:Anhui University Press.(in Chinese)
Li J H.2000.The cognition of rank in Tibetan macaques.Journal of Anhui University(Natural Science Edition),24(3):116-120.(in Chinese)
Li J H,Yin H B,Zhou L Z,Ge J Z.2004.Social behaviors and relationships among Thibetan macaques.Chinese Journal of Zoology,39(1):40-44.(in Chinese)
Li J H,Yin H B,Wang Q S.2005.Seasonality of reproduction and sexual activity in female Tibetan macaques Macaca thibetana at Huangshan,China.Acta Zoologica Sinica,51(3):365-375.
Lukas D,Clutton-Brock T H.2013.The evolution of social monogamy in mammals.Science,341(6145):526-530.
Newman M E J.2004.Analysis of weighted networks.Physical Review EStatistical Nonlinear&Soft Matter Physics,70(2):1-9.
NoёR,Sluijter A A.1990.Reproductive tactics of male savanna Baboons.Behaviour,113(1-2):117-170.
Rakhovskaya M V.2013.Correlates of male consortship rate in free-ranging rhesus macaques(Macaca mulatta).International Journal of Primatology,34(4):662-680.
Schroeder J,Nakagawa S,Rees M,Mannarelli M E,Burke T.2015.Reduced fitness in progeny from old parents in a natural population.Proc Natl Acad Sci USA,112(13):4021-4025.
Schülke O,Bhagavatula J,Vigilant L,Ostner J.2010.Social bonds enhance reproductive success in male macaques.Curr Biol,20(24):2207-2210.
Silk J B,Alberts S C,Altmann J.2006.Social relationships among adult female baboons(Papio cynocephalus)II.Variation in the quality and stability of social bonds.Behavioral Ecology and Sociobiology,61(2):197-204.
Soltis J.1999.Measuring male-female relationships during the mating season in wild Japanese macaques(Macaca fuscata yakui).Primates,40(3):453-467.
Tutin C E G.1979.Mating patterns and reproductive strategies in a community of wild Chimpanzees(Pan troglodytes schweinfurthii).Behavioral Ecology&Sociobiology,6(1):29-38.
Van Noordwijk M A.1985.Sexual behaviour of sumatran long-tailed macaques(Macaca fascictclaris).Z Tierpsychol,70(4):277-296.
Wang X,Sun L X,Sheeran L K,Sun B H,Zhang Q X,Zhang D,Xia D P,Li J H.2016.Social rank versus affiliation:Which is more closely related to leadership of group movements in Tibetan macaques(Macaca thibetana)?Am J Primatol,78(8):816-824.
Watts D P.2010.In Mind the Gap:Tracing the Origins of Human Universals.New York:Springer,109-139.
Weingrill T,Lycett J E,Barrett L,Hill R A,Henzi S P.2003.Male consortship behaviour in chacma baboons:the role of demographic factors and female conceptive probabilities.Behaviour,140(3):405-427.
Weingrill T,Lycett J E,Henzi S P.2000.Consortship and mating success in Chacma baboons(Papio cynocephalus ursinus).Ethology,106(11):1033-1044.
Wickings E J,Bossi T,Dixson A F.1993.Reproductive success in the mandrill,Mandrillus sphinx:correlations of male dominance and mating success with paternity,as determined by DNA fingerprinting.Journal of Zoology,231(4):563-574.
Widdig A,Bercovitch F B,Streich W J,Sauermann U,Nurnberg P,Krawczak M.2004.A longitudinal analysis of reproductive skew in male rhesus macaques.Proc Biol Sci,271(1541):819-826.
Xiong C P,Wang Q S.1991.A Comparative study on the male sexual behavior in Tibetan macaques and Japanese monkey.Acta Theriologica Sinica,11(1):13-22.(in Chinese)
Xia D P,Li J H,Garber P A,Matheson M D,Sun B H,Zhu Y.2013.Grooming reciprocity in male Tibetan macaques.Am J Primatol,75(10):1009-1020.
Zhang M,Li J H,Zhu Y,Wang X,Wang S.2010.Male mate choice in Tibetan macaques Macaca thibetana at Mt.Huangshan,China.Current Zoology,56(2):213-221.
Zhao Q K.1993.Sexual behavior of Tibetan macaques at Mt.Emei,China.Primates,34(4):431-444.
Ziv E B,Ilany A,Demartsev V,Barocas A,Geffen E,Koren L.2016.Individual,social,and sexual niche traits affect copulation success in a polygynandrous mating system.Behavioral Ecology&Sociobiology,70(6):901-912.
李进华.1999.野生短尾猴的社会.合肥:安徽大学出版社.
李进华.2000.短尾猴对顺位关系的认知.安徽大学学报:自然科学版,24(3):116-120.
李进华,尹华宝,周立志,葛继志.2004.短尾猴的社会行为与社会关系.动物学杂志,39(1):40-44.
顾志远,陈锐,孙丙华,王希,夏东坡,李进华.2017.成年雌性短尾猴的社会联系强度及影响因素.兽类学报,37(4):363-370.
熊成培,王岐山.1991.短尾猴和日本猴雄性性行为的比较研究.兽类学报,11(1):13-22.