笼养川金丝猴理毛行为功能
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摘要
<正>理毛行为(Grooming behavior)的定义是动物个体对自身或其同类个体体表(皮肤、毛发或羽毛等)进行的多种形式护理,包括对体表进行有规律的梳理,以及用舌头或嘴唇舔皮肤和毛发等(Veà et al., 1999)。在灵长类动物中,理毛行为大多表现为个体接触和探查自身或另一个体体表被毛,将毛发分开后从中拣出盐粒或皮肤寄生物放入口中咀嚼或直接用嘴咬食被毛下的盐粒或皮肤寄生物(李银华和李保国, 2002)。依据理毛接收对象的不同,可将
Grooming behavior is one of the social behaviors commonly found among primates. Such behavior is often associated with particle removal, with the groomers manually brushing away,or sometimes devouring, loose particles. However, the function of allogrooming and the associated particulate matter still remain controversial. In this study, we used all occurrence sampling to record autogrooming and allogrooming behaviors in captive Sichuan snub-nosed monkey(Rhinopithecus roxellana) in the Endangered Animal Breeding Center of the Beijing Wildlife Park from February to Match 2017. A total of 120 bouts of autogrooming and 259 bouts of allogrooming were recorded to test the hygienic functional hypothesis and the compensation hypothesis of allogrooming. The particulate matter on the hair and skin was checked for ectoparasite, flakes of skin or secretion of salt using microscopy. In addition, we manipulate salt and protein intake via offering the monkeys with drinking water of different concentrations of salts and fresh Populus leaves with high protein, in order to test the nutritional function of allogrooming and particle intake. Our results suggested that the grooming behaviors of the monkeys in general were consistent with the prediction of hygienic functional hypothesis, but in adult males,but not in adult females, were broadly in line with the prediction of compensation hypothesis. No association was noted between grooming and removal of parasites, and neither the functions of obtaining protein, or sodium chloride were confirmed. In conclusion, grooming behavior of captive Sichuan snub-nosed monkeys is more likely to be a semi-ritualized social behavior.
Grooming behavior is one of the social behaviors commonly found among primates. Such behavior is often associated with particle removal, with the groomers manually brushing away,or sometimes devouring, loose particles. However, the function of allogrooming and the associated particulate matter still remain controversial. In this study, we used all occurrence sampling to record autogrooming and allogrooming behaviors in captive Sichuan snub-nosed monkey(Rhinopithecus roxellana) in the Endangered Animal Breeding Center of the Beijing Wildlife Park from February to Match 2017. A total of 120 bouts of autogrooming and 259 bouts of allogrooming were recorded to test the hygienic functional hypothesis and the compensation hypothesis of allogrooming. The particulate matter on the hair and skin was checked for ectoparasite, flakes of skin or secretion of salt using microscopy. In addition, we manipulate salt and protein intake via offering the monkeys with drinking water of different concentrations of salts and fresh Populus leaves with high protein, in order to test the nutritional function of allogrooming and particle intake. Our results suggested that the grooming behaviors of the monkeys in general were consistent with the prediction of hygienic functional hypothesis, but in adult males,but not in adult females, were broadly in line with the prediction of compensation hypothesis. No association was noted between grooming and removal of parasites, and neither the functions of obtaining protein, or sodium chloride were confirmed. In conclusion, grooming behavior of captive Sichuan snub-nosed monkeys is more likely to be a semi-ritualized social behavior.
引文
Alexander R D.1974.The evolution of social behavior.Annual Review of Ecology and Systematics,5(1):325-383.
Altmann J.1974.Observational study of behavior:sampling methods.Behaviour,49(3):227-266.
Barton R.1985.Grooming site preferences in primates and their functional implications.International Journal of Primatology,6(5):519-532.
Boccia M L.1983.A functional analysis of social grooming patterns through direct comparison with self-grooming in rhesus monkeys.International Journal of Primatology,4(4):399-418.
Borries C.1992.Grooming site preferences in female langurs(Presbytis entellus).International Journal of Primatology,13(1):19-32.
Bolwing N.1957.Some observations on the habits of the chacma baboon,Papio ursinus.South African Journal of Science,53(10):255-260.
Chiarello A G.1995.Grooming in brown howler monkeys,Alouatta fusca.American Journal of Primatology,35(1):73-81.
De Waal F.1989.Peacemaking among Primates.Cambridge:Harvard U-niversity Press,90-91.
Dixson A F,Scruton D M,Herbert J.1975.Behaviour of the talapoin monkey(Miopithecus talapoin)studied in groups,in the laboratory.Journal of Zoology,176(2):177-210.
Fruteau C,Voelkl B,Van Damme E,Noё.2009.Supply and demand determine the market value of food providers in wild vervet monkeys.Proceedings of the National Academy of Sciences,106(29):12007-12012.
Ghiglieri M P.1984.The Chimpanzees of Kibale Forest:A field Study of Ecology and Social Structure.New York:Columbia University Press,1-226.
Goosen C.1974.Immediate effects of allogrooming in adult stump-tailed macaques Macaca Arctoides.Behaviour,48(1):75-88.
Griffen D R.1982.Animal Mind-Human Mind.Berlin:Springer-Verlag,81-105.
Gumert M D.2007.Payment for sex in a macaque mating market.Animal Behaviour,74(6):1655-1667.
Hinde R A.1983.Primate Social Relationships.Oxford:Blackwell,182-190.
Idani G I.1991.Social relationships between immigrant and resident bonobo(Pan paniscus)females at Wamba.Folia Primatologica,57(2):83-95.
Jablonski N G.1998.The Natural History of the Doucs and Snub-nosed Monkeys.Singapore:World Scientific Publishing,279-300.
Morris D.1967.Primate Ethology.London:Weidenfeld&Nicolson,7-68.
Onishi K,Yamada K,Nakamichi M.2013.Grooming-related feeding motivates macaques to groom and affects grooming reciprocity and episode duration in Japanese macaques(Macaca fuscata).Behavioural Processes,92(1):125-130.
Pérez A P,VeàJ J.1999.Does allogrooming serve a hygienic function in Cercocebus torquatus lunulatus?American Journal of Primatology,49(3):223-242.
Pérez A P,VeàJ J.2000.Functional implications of allogrooming in Cercocebus torquatus.International Journal of Primatology,21(2):255-267.
Schino G,Maestripieri D,Scucchi S,Turillazzi P G.1990.Social tension in familiar and unfamiliar pairs of long-tailed macaques.Behaviour,113(3):264-272.
Schino G,Ventura R,Troisi A.2003.Grooming among female Japanese macaques:distinguishing between reciprocation and interchange.Behavioral Ecology,14(6):887-891.
Seyfarth R M.1977.A model of social grooming among adult female monkeys.Journal of Theoretical Biology,65(4):671-698.
Seyfarth R M,Cheney D L.1984.Grooming,alliances and reciprocal altruism in vervet monkeys.Nature,308(5959):541-543.
Smith C C.1977.Feeding Behaviour and Social Organization in Howling Monkeys.London:Academic Press,97-126.
Smuts B B.1985.Sex and Friendship in Baboons.New York:Aldine Publishing Company,1-580.
Tanaka I,Takefushi H.1993.Elimination of external parasites(lice)is the primary function of grooming in free-ranging Japanese macaques.Anthropological Science,101(2):187-193.
Taub D M,King F A.1986.Current Perspectives in Social Dynamics.New York:Van Nostrand Reinhold,505-519.
Terry R L.1970.Primate grooming as a tension reduction mechanism.The Journal of Psychology,76(1):129-136.
VeàJ J,Pérez A P,Baldellou M,Alea V.1999.Cost-benefit analysis of allogrooming behaviour in Cercocebus torquatus lunulatus.Behaviour,136(2):243-256.
Ventura R,Majolo B,Koyama N F,Hardie S,Schino G.2006.Reciprocation and interchange in wild Japanese macaques:grooming,cofeeding,and agonistic support.American Journal of Primatology,68(12):1138-1149.
Wei W,Qi X G,Guo S T,et al.2012.Market powers predict reciprocal grooming in golden snub-nosed monkeys(Rhinopithecus roxellana).PLoS ONE,7(5):e36802.
World Health Organization.2012.Guideline:Sodium intake for adults and children.Geneva:World Health Organization(WHO),18.
Yu Y,Xiang Z F,Yao H,et al.2013.Female snub-nosed monkeys exchange grooming for sex and infant handling.PLoS ONE,8(9):e74822.
朱紫瑞.2008.秦岭川金丝猴(Rhinopithecus roxellana)成年雌性相互理毛的时间匹配性以及理毛策略的研究.西安:西北大学硕士学位论文.
李保国,张鹏,渡边邦夫,谈家伦.2002.川金丝猴的相互理毛行为是否具有卫生功能.动物学报,48(6):707-715.
李银华,李保国.2004.灵长类相互理毛的影响因素,功能及其利益分析.人类学学报,23(4):334-342.
李静宜,和昱辰,申立泉,杨国祥,白文妹,刘耘,肖运才,余辉亮,杨敬元,姚辉,李翔.2016.神农架金丝猴对食物味道偏好性初探.养殖与饲料,(4):8-10.
宋葆华,李法曾,贺新强,樊守金,倪陈凯.1999.107种植物叶蛋白产量及其蛋白质含量比较.植物资源与环境,8(4):53-55.
张德军,黎大勇,胡杰,任宝平,袁晓霞,和鑫明,李艳红,李明.2014.滇金丝猴雌性个体间的理毛行为.兽类学报,34(1):38-45.
贺晓冬,苗世光,窦晶晶,申双和.2014.北京城市气候图系统的初步建立.南京大学学报(自然科学版),50(6):759-771.
黄帅.2014.人工饲养环境下川金丝猴营养代谢、应激及免疫生理状态的非损伤研究.南京:南京农业大学硕士学位论文..
梁冰,戚汉君,张树义,任宝平.2001.笼养川金丝猴不同年龄阶段的发育特征.动物学报,47(4):381-387.
彭廉宾.2000.树叶的饲用价值.饲料与畜牧,(4):27-29.
Altmann J.1974.Observational study of behavior:sampling methods.Behaviour,49(3):227-266.
Barton R.1985.Grooming site preferences in primates and their functional implications.International Journal of Primatology,6(5):519-532.
Boccia M L.1983.A functional analysis of social grooming patterns through direct comparison with self-grooming in rhesus monkeys.International Journal of Primatology,4(4):399-418.
Borries C.1992.Grooming site preferences in female langurs(Presbytis entellus).International Journal of Primatology,13(1):19-32.
Bolwing N.1957.Some observations on the habits of the chacma baboon,Papio ursinus.South African Journal of Science,53(10):255-260.
Chiarello A G.1995.Grooming in brown howler monkeys,Alouatta fusca.American Journal of Primatology,35(1):73-81.
De Waal F.1989.Peacemaking among Primates.Cambridge:Harvard U-niversity Press,90-91.
Dixson A F,Scruton D M,Herbert J.1975.Behaviour of the talapoin monkey(Miopithecus talapoin)studied in groups,in the laboratory.Journal of Zoology,176(2):177-210.
Fruteau C,Voelkl B,Van Damme E,Noё.2009.Supply and demand determine the market value of food providers in wild vervet monkeys.Proceedings of the National Academy of Sciences,106(29):12007-12012.
Ghiglieri M P.1984.The Chimpanzees of Kibale Forest:A field Study of Ecology and Social Structure.New York:Columbia University Press,1-226.
Goosen C.1974.Immediate effects of allogrooming in adult stump-tailed macaques Macaca Arctoides.Behaviour,48(1):75-88.
Griffen D R.1982.Animal Mind-Human Mind.Berlin:Springer-Verlag,81-105.
Gumert M D.2007.Payment for sex in a macaque mating market.Animal Behaviour,74(6):1655-1667.
Hinde R A.1983.Primate Social Relationships.Oxford:Blackwell,182-190.
Idani G I.1991.Social relationships between immigrant and resident bonobo(Pan paniscus)females at Wamba.Folia Primatologica,57(2):83-95.
Jablonski N G.1998.The Natural History of the Doucs and Snub-nosed Monkeys.Singapore:World Scientific Publishing,279-300.
Morris D.1967.Primate Ethology.London:Weidenfeld&Nicolson,7-68.
Onishi K,Yamada K,Nakamichi M.2013.Grooming-related feeding motivates macaques to groom and affects grooming reciprocity and episode duration in Japanese macaques(Macaca fuscata).Behavioural Processes,92(1):125-130.
Pérez A P,VeàJ J.1999.Does allogrooming serve a hygienic function in Cercocebus torquatus lunulatus?American Journal of Primatology,49(3):223-242.
Pérez A P,VeàJ J.2000.Functional implications of allogrooming in Cercocebus torquatus.International Journal of Primatology,21(2):255-267.
Schino G,Maestripieri D,Scucchi S,Turillazzi P G.1990.Social tension in familiar and unfamiliar pairs of long-tailed macaques.Behaviour,113(3):264-272.
Schino G,Ventura R,Troisi A.2003.Grooming among female Japanese macaques:distinguishing between reciprocation and interchange.Behavioral Ecology,14(6):887-891.
Seyfarth R M.1977.A model of social grooming among adult female monkeys.Journal of Theoretical Biology,65(4):671-698.
Seyfarth R M,Cheney D L.1984.Grooming,alliances and reciprocal altruism in vervet monkeys.Nature,308(5959):541-543.
Smith C C.1977.Feeding Behaviour and Social Organization in Howling Monkeys.London:Academic Press,97-126.
Smuts B B.1985.Sex and Friendship in Baboons.New York:Aldine Publishing Company,1-580.
Tanaka I,Takefushi H.1993.Elimination of external parasites(lice)is the primary function of grooming in free-ranging Japanese macaques.Anthropological Science,101(2):187-193.
Taub D M,King F A.1986.Current Perspectives in Social Dynamics.New York:Van Nostrand Reinhold,505-519.
Terry R L.1970.Primate grooming as a tension reduction mechanism.The Journal of Psychology,76(1):129-136.
VeàJ J,Pérez A P,Baldellou M,Alea V.1999.Cost-benefit analysis of allogrooming behaviour in Cercocebus torquatus lunulatus.Behaviour,136(2):243-256.
Ventura R,Majolo B,Koyama N F,Hardie S,Schino G.2006.Reciprocation and interchange in wild Japanese macaques:grooming,cofeeding,and agonistic support.American Journal of Primatology,68(12):1138-1149.
Wei W,Qi X G,Guo S T,et al.2012.Market powers predict reciprocal grooming in golden snub-nosed monkeys(Rhinopithecus roxellana).PLoS ONE,7(5):e36802.
World Health Organization.2012.Guideline:Sodium intake for adults and children.Geneva:World Health Organization(WHO),18.
Yu Y,Xiang Z F,Yao H,et al.2013.Female snub-nosed monkeys exchange grooming for sex and infant handling.PLoS ONE,8(9):e74822.
朱紫瑞.2008.秦岭川金丝猴(Rhinopithecus roxellana)成年雌性相互理毛的时间匹配性以及理毛策略的研究.西安:西北大学硕士学位论文.
李保国,张鹏,渡边邦夫,谈家伦.2002.川金丝猴的相互理毛行为是否具有卫生功能.动物学报,48(6):707-715.
李银华,李保国.2004.灵长类相互理毛的影响因素,功能及其利益分析.人类学学报,23(4):334-342.
李静宜,和昱辰,申立泉,杨国祥,白文妹,刘耘,肖运才,余辉亮,杨敬元,姚辉,李翔.2016.神农架金丝猴对食物味道偏好性初探.养殖与饲料,(4):8-10.
宋葆华,李法曾,贺新强,樊守金,倪陈凯.1999.107种植物叶蛋白产量及其蛋白质含量比较.植物资源与环境,8(4):53-55.
张德军,黎大勇,胡杰,任宝平,袁晓霞,和鑫明,李艳红,李明.2014.滇金丝猴雌性个体间的理毛行为.兽类学报,34(1):38-45.
贺晓冬,苗世光,窦晶晶,申双和.2014.北京城市气候图系统的初步建立.南京大学学报(自然科学版),50(6):759-771.
黄帅.2014.人工饲养环境下川金丝猴营养代谢、应激及免疫生理状态的非损伤研究.南京:南京农业大学硕士学位论文..
梁冰,戚汉君,张树义,任宝平.2001.笼养川金丝猴不同年龄阶段的发育特征.动物学报,47(4):381-387.
彭廉宾.2000.树叶的饲用价值.饲料与畜牧,(4):27-29.