ORIGINAL PAPERS

The cooperative food hoarding behaviors of Brandt's voles and their influencing factors

  • SONG Yiran ,
  • LI Guoliang ,
  • ZHANG Zhibin
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  • 1 State Key Laboratory of Integrated Management of Pest Insects and Rodent, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China;
    2 University of Chinese Academy of Science, Beijing 100049, China;
    3 CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China

Received date: 2021-03-31

  Revised date: 2021-05-24

  Online published: 2021-08-04

Abstract

Food hoarding is a crucial strategy to cope with the seasonal shortage of food resources in many social animals, but the underlying ecological mechanisms remain unclear. In this study, Brandt's voles were divided into kin group (from the same family) and non-kin group (from different families). We used video camera to record the cooperative food hoarding patterns of different groups and individuals in experimental boxes, and calculated the time of different behaviors. We used correlation analysis to study the association between cost and benefit for cooperative food hoarding individuals, and its influencing factors. We found, as compared to the non-kin group, Brandt's voles in the kin group spent more time on cooperative food hoarding behavior. However, cooperative food hoarding behavior differed greatly among individuals in the same kin group. There was a significant negative correlation between time of hoarding food and time of eating food by voles. Voles with more time of hoarding food showed a significant decrease in testicle index and testosterone content. Our study suggests that kinship is essential for maintaining cooperative food hoarding in voles, but the reproduction of cooperators who largely contributed to food hoarding was inhibited.

Cite this article

SONG Yiran , LI Guoliang , ZHANG Zhibin . The cooperative food hoarding behaviors of Brandt's voles and their influencing factors[J]. ACTA THERIOLOGICA SINICA, 2021 , 41(6) : 658 -666 . DOI: 10.16829/j.slxb.150546

References

Agren G, Zhou Q, Zhong W. 1989. Ecology and social-behavior of Mongolian gerbils, Meriones unguiculatus, at Xilinhot, InnerMongolia, China. Animal Behaviour, 37 (1):11-27.
Andreoni J, Harbaugh W, Vesterlund L. 2003. The carrot or the stick:Rewards, punishments, and cooperation. American Economic Review, 93 (3):893-902.
Balducci M G, Van der Niet T, Johnson S D. 2020. Diel scent and nectar rhythms of an African orchid in relation to bimodal activity patterns of hawkmoth pollinators. Annals of Botany, 126 (7):1155-1164.
Beekman M, Oldroyd B P. 2003. Different policing rates of eggs laid by queenright and queenless anarchistic honey-bee workers (Apis mellifera L.). Behavioral Ecology and Sociobiology, 54 (5):480-484.
Bergmuller R, Taborsky M. 2010. Animal personality due to social niche specialization. Trends in Ecology and Evolution, 25 (9):504-511.
Bresgunova O A. 2016. Cooperative breeding in corvids (Passeriformes, Corvidae). Biology Bulletin, 43 (7):693-706.
Briga M, Pen I, Wright J. 2012. Care for kin:within-group relatedness and allomaternal care are positively correlated and conserved throughout the mammalian phylogeny. Biology Letters, 8(4):533-536.
Carter A J, English S, Clutton-Brock T H. 2014. Cooperative personalities and social niche specialization in female meerkats. Journal of Evolutionary Biology, 27 (5):815-825.
Chaby L E, Sheriff M J, Hirrlinger A M, Braithwaite V A. 2015. Does early stress prepare individuals for a stressful future? Stress during adolescence improves foraging under threat. Animal Behaviour, 105:37-45.
Connor R. 2007. Invested, extracted and byproduct benefits:A modified scheme for the evolution of cooperation. Behavioural Processes, 76 (2):109-113.
Cressman R, Wu J, Li C, Tao Y. 2013. Game experiments on cooperation through reward and punishment. Biological Theory, 8 (2):158-166.
Darby N A, McGhee K E. 2019. Boldness is affected by recent experience with predation cues and body size in mosquitofish. Behavioral Processes, 164:143-149.
Deng K, Liu W, Wang D H. 2016. A review on social behavior-kinship linkage mechanisms in population regulation of small mammals. Chinese Journal of Ecology, 35 (3):825-833. (in Chinese)
Ebensperger L A. 2001. A review of the evolutionary causes of rodent group-living. Acta Theriologica, 46 (2):115-144.
Grinsted L, Bacon J P. 2014. Animal behaviour:task differentiation by personality in spider groups. Current Biology, 24 (16):R749-R750.
Hamilton W D. 1963. The evolution of altruistic behavior. American Naturalist, 97 (896):354-356.
Hamilton W D. 1964. The genetical evolution of social behavior. Journal of Theoretical Biology, 7 (1):1-52.
Hughes W O H, Oldroyd B P, Beekman M, Francis LW, Ratnieks F L W. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science, 320 (5880):1213-1216.
Jiang J, Moore J A M, Priyadarshi A, Classen A T. 2017. Plant-mycorrhizal interactions mediate plant community coexistence by altering resource demand. Ecology, 98 (1):187-197.
Kilgour R J, Faure P A, Brigham R M. 2013. Evidence of social preferences in big brown bats (Eptesicus fuscus). Canadian Journal of Zoology, 91 (10):756-760.
Li G, Hou X, Wan X, Zhang Z. 2016. Sheep grazing causes shift in sex ratio and cohort structure of Brandt's vole:Implication of their adaptation to food shortage. Integrative Zoology, 11 (1):76-84.
Lou Y, Shi M, Fang Y, Swenson J E, Lyu N, Sun Y. 2017. Male vigilance and presence are important for foraging by female Chinese grouse in the pre-incubation period. Wildlife Biology, SP1:1-6.
Lu J Q, Xiao Z S, Cheng J R, Zhang Z B. 2004. Scatter-hoarding behavior of rodents. Acta Theriologica Sinica, 24 (3):267-272. (in Chinese)
Lu J Q, Zhang Z B. 2005. Food hoarding behavior of Chinese whitebellied rat (Niviventor confucianus). Acta Theriologica Sinica, 25(3):248-253. (in Chinese)
Montague M J, Disotell T R, Di Fiore A. 2014. Population genetics, dispersal, and kinship among wild squirrel monkeys (Saimiri sciureus macrodon):Preferential association between closely related females and its implications for insect prey capture success. International Journal of Primatology, 35:169-187.
Nowak M. 2006. Five rules for the evolution of cooperation. Science, 314 (5805):1560-1563.
Oyegbile T O, Marler C A. 2005. Winning fights elevates testosterone levels in California mice and enhances future ability to win fights. Hormones and Behavior, 48 (3):259-267.
Paeke C, Pusey A E. 1982. Cooperation and competition within coalitions of male lions:Kin selection or game theory? Nature, 294:740-742.
Randall J A, Rogovin K A, Shier D M. 2000. Antipredator behavior of a social desert rodent:footdrumming and alarm calling in the great gerbil, Rhombomys opiums. Behavioral Ecology and Sociobiology, 48 (2):110-118.
Rasmussen J E, Belk M C. 2017. Predation environment affects boldness temperament of neotropical livebearers. Ecology and Evolution, 7 (9):3059-3066.
Ronce O, Gandon S, Rousset F. 2000. Kin selection and natal dispersal in an age-structured population. Theoretical Population Biology, 58 (2):143-159.
Smith C C, Reichman O J. 1984. The evolution of food caching by birds and mammals. Annual Review of Ecology and Systematics, 15:329-351.
Song W T, Wang Y, Zhang X Q, Zhang W J, Zheng S S, Gexigeduren, Chen W, Wan X R. 2017. Influence of group size and foraging distance on vigilance frequency of Brandt's vole (Lasiopodomys brandtii) in food storing period. Chinese Journal of Zoology, 52(5):754-760. (in Chinese)
Tamura N, Shibasaki E. 1996. Fate of walnut seeds, Juglans airanthifolia, hoarded by Japanese squirrels, Sciurus lis. Journal of Forest Research, 1:219-222.
Trivers R L. 1971. The evolution of reciprocal altruism. The Quarterly Review of Biology, 46 (1):35-57.
Van Der Merwe M, Brown J S. 2008. Mapping the landscape of fear of the cape ground squirrel (Xerus inauris). Journal of Mammalogy, 89 (5):1162-1169.
Vander Wall S B. 1990. Food Hoarding in Animals. Chicago:University of Chicago Press.
Wan X R, Wang M J, Wang G H, Zhong W Q. 2002. Food-storing preference of Microtus brandti. Chinese Journal of Ecology, 21(1):68-69. (in Chinese)
Wan X R, Zhang X J, Liu W, Wang G H, Wang M J, Zhong W Q. 2007. Social hierarchy and its seasonal changes of marked Lasiopodomys brandtii population. Chinese Journal of Ecology, 26 (3):359-362. (in Chinese)
Wan X R, Zhong W Q. 2000. Comparison the two estimators of food-storing-territory of communal over-winter nest of Brandt's vole. Chinese Journal of Ecology, 19 (4):75-76. (in Chinese)
Wang D W, Cong L, Wang Y, Liu X H. 2010. Population parameters and physiological characteristics of Brandt's vole (Lasiopodomys brandtii) in breeding and non-breeding seasons. Acta Ecology Sinica, 30 (13):3562-3568. (in Chinese)
Wang D, Zhang J, Zhang Z. 2012. Effect of testosterone and melatonin on social dominance and agonistic behavior in male Tscheskia triton. Behavioural Processes, 89 (3):271-277.
Wright C M, Keiser C N, Pruitt J N. 2015. Personality and morphology shape task participation, collective foraging and escape behaviour in the social spider Stegodyphus dumicola. Animal Behaviour, 105:47-54.
Wynne-Edwards V C. 1962. Animal Dispersion in Relation to Social Behaviour. New York:Hafner Publishing Company, 653-660.
Zhang H, Wang Z, Zeng Q, Chang G, Wang Z. 2015. Mutualistic and predatory interactions are driven by rodent body size and seed traits in a rodent-seed system in warm-temperate forest in northern China. Wildlife Research, 42 (2):149-157.
Zhang Z, Yan C, Zhang H. 2021. Mutualism between antagonists:its ecological and evolutionary implications. Integrative Zoology, 19:84-96.
王大伟, 丛林, 王宇, 刘晓辉. 2010.繁殖季节和非繁殖季节布氏田鼠种群参数和生理特点的差异.生态学报, 30 (13):3562-3568.
邓可, 刘伟, 王德华. 2016.小型哺乳动物种群调节中社会行为与亲缘结构联动机制研究进展.生态学杂志, 35 (3):825-833.
刘鹤玲. 2005.从竞争进化到合作进化:达尔文自然选择学说的新发展.科学技术与辩证法, 22 (1):38-40.
宋文韬, 王也, 张小倩, 张文杰, 郑思思, 格希格都仁, 陈卫, 宛新荣. 2017.集群数量和采食距离对储草期布氏田鼠警戒频次的影响.动物学杂志, 52 (5):754-760.
宛新荣, 钟文勤. 2000.布氏田鼠越冬集群贮草面积的两种估算方法比较.生态学杂志, 19 (4):75-76.
宛新荣, 王梦军, 王广和, 钟文勤. 2002.布氏田鼠对主要贮草种类的选储嗜好.生态学杂志, 21 (1):68-69.
宛新荣, 张新阶, 刘伟, 王广和, 王梦军, 钟文勤. 2007.布氏田鼠标志种群的社群等级及其季节变化.生态学杂志, 26 (3):359-362.
施大钊, 海淑珍, 金晓明, 刘小龙. 1997.越冬前布氏田鼠储草行为与储草种类选择的研究.草地学报, 5 (1):20-26.
蒋志刚. 1996a.动物保护食物贮藏的行为策略.动物学杂志, 31(5):52-55.
蒋志刚. 1996b.动物贮食行为及其生态意义.动物学杂志, 31(3):47-49.
路纪琪, 肖治术, 程瑾瑞, 张知彬. 2004.啮齿动物的分散贮食行为.兽类学报, 24 (3):267-272.
路纪琪, 张知彬. 2005.围栏条件下社鼠的食物贮藏行为.兽类学报, 25 (3):248-253.
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