Abstract
Animals often interact non‐randomly with conspecifics, and association preferences can differ across life‐history stages to maximize individuals' fitness. Mongolian gerbils (Meriones unguiculatus) are a social rodent that live in highly seasonal habitats and display seasonal fluctuations in population density, growth rate and the size of overlapped home ranges. Nevertheless, whether gerbils modify their social relationships at different life‐history stages remains unknown. Here, we used social network analysis to examine whether social associations differ between the sexes and between life‐history stages in a wild population of Mongolian gerbils. We quantified social attributes at both group level (assortativity) and individual level (social differentiation and degree, closeness and betweenness centrality); these attributes reflect individuals' social preferences and their potential influence on others in the network. We found that both male and female gerbils established fewer inter‐group social connections during the food‐hoarding season than during the breeding season, revealing constraints on sociality. Similarly, during the food‐hoarding season, degree centrality and social differentiation increased significantly whereas closeness and betweenness centrality decreased significantly. Together, these results suggest that gerbils have relatively more partners and preferred associations and decreased influence over others in the network during the food‐hoarding season. In addition, we found no significant difference in any of the social attribute between males and females, but there was a significant interaction effect between sex and season on degree, closeness and betweenness centrality. Our results demonstrate that Mongolian gerbils adjust their association strategies to adapt to the changes of life history. Such adjustments may balance the costs/benefits associated with survival and reproduction.
Keywords: centrality, inter‐group associations, life history, Meriones unguiculatus, social network analysis
Cite this article as:
Deng K, Liu W, Wang D (2017). Inter‐group associations in Mongolian gerbils: Quantitative evidence from social network analysis. Integrative Zoology 12, 446–56.
Contributor Information
Wei LIU, Email: liuwei@ioz.ac.cn.
Dehua WANG, Email: wangdh@ioz.ac.cn.
REFERENCES
- Ågren G, Zhou Q, Zhong W (1989a). Ecology and social‐behavior of Mongolian gerbils, Meriones‐unguiculatus, at Xilinhot, Inner‐Mongolia, China. Animal Behaviour 37, 11–27. [Google Scholar]
- Ågren G, Zhou Q, Zhong W (1989b). Territoriality, cooperation and resource priority – Hoarding in the Mongolian gerbil, Meriones‐unguiculatus . Animal Behaviour 37, 28–32. [Google Scholar]
- Arseneau‐Robar TJM, Taucher AL, Schnider AB, van Schaik CP, Willems EP (2017). Intra‐ and interindividual differences in the costs and benefits of inter-group aggression in female vervet monkeys. Animal Behaviour 123, 129–37. [Google Scholar]
- Bar Ziv E, 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 and Sociobiology 70, 901–12. [Google Scholar]
- Bates D, Maechler M, Bolker B (2013). Linear mixed‐effect models using S4 classes. R package; Available from URL: http://CRAN.R-project.org/package=lme4. [Google Scholar]
- Bejder L, Fletcher D, Brager S (1998). A method for testing association patterns of social animals. Animal Behaviour 56, 719–25. [DOI] [PubMed] [Google Scholar]
- Bulter RG (1980). Population size, social behaviour, and dispersal in house mice: A quantitative investigation. Animal Behaviour 28, 78–85. [Google Scholar]
- Cameron EZ, Setsaas TH, Linklater WL (2009). Social bonds between unrelated females increase reproductive success in feral horses. PNAS 106, 13850–53. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clark MM, Galef BG (2001). Socially induced infertility: familial effects on reproductive development of female Mongolian gerbils. Animal Behaviour 62, 897–903. [Google Scholar]
- Crockett CM, Eisenberg JF (1987). Howlers: variation in group size and demography In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RR, Struhsker TT, eds. Primate Societies. The University of Chicago Press, Chicago, IL. [Google Scholar]
- Croft DP, James R, Ward AJW, Botham MS, Mawdsley D, Krause J (2005). Assortative interactions and social networks in fish. Oecologia 143, 211–9. [DOI] [PubMed] [Google Scholar]
- Croft DP, Madden JR, Franks DW, James R (2011). Hypothesis testing in animal social networks. Trends in Ecology & Evolution 26, 502–7. [DOI] [PubMed] [Google Scholar]
- Csardi G, Nepusz T (2006). The IGRAPH software package for complex network research. International Journal of Complex Systems.
- Drickamer LC, Gowaty PA, Wagner DM (2003). Free mutual mate preferences in house mice affect reproductive success and offspring performance. Animal Behaviour 65, 105–14. [DOI] [PubMed] [Google Scholar]
- Farine DR (2014). Measuring phenotypic assortment in animal social networks: weighted associations are more robust than binary edges. Animal Behaviour 89, 141–53. [Google Scholar]
- Farine DR, O'Hara RB (2013). Animal social network inference and permutations for ecologists in R using asnipe. Methods in Ecology and Evolution 4, 1187–94. [Google Scholar]
- Farine DR, Whitehead H (2015). Constructing, conducting and interpreting animal social network analysis. Journal of Animal Ecology 84, 1144–63. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Freeman LC (1979). Centrality in social networks conceptual clarification. Social Networks 1, 215–39. [Google Scholar]
- Ginsberg JR, Young TP (1992). Measuring association between individuals or groups in behavioral studies. Animal Behaviour 44, 377–9. [Google Scholar]
- Hirsch BT (2011). Within‐group spatial position in ring‐tailed coatis: balancing predation, feeding competition, and social competition. Behavioral Ecology and Sociobiology 65, 391–9. [Google Scholar]
- Holekamp KE, Smith JE, Strelioff CC, Van Horn RC, Watts HE (2012). Society, demography and genetic structure in the spotted hyena. Molecular Ecology 21, 613–32. [DOI] [PubMed] [Google Scholar]
- Kanngiesser P, Sueur C, Riedl K, Grossmann J, Call J (2011). Grooming network cohesion and the role of individuals in a captive chimpanzee group. American Journal of Primatology 73, 758–67. [DOI] [PubMed] [Google Scholar]
- Krause J, Lusseau D, James R (2009). Animal social networks: an introduction. Behavioral Ecology and Sociobiology 63, 967–73. [Google Scholar]
- Krause J, Ruxton GD (2002). Living in Groups. Oxford University Press, New York. [Google Scholar]
- Krebs CJ (2015). One hundred years of population ecology: Successes, failures and the road ahead. Integrative Zoology 10, 233–40. [DOI] [PubMed] [Google Scholar]
- Kuhn KM, Vander Wall SB (2008). Linking summer foraging to winter survival in yellow pine chipmunks (Tamias amoenus). Oecologia 157, 349–60. [DOI] [PubMed] [Google Scholar]
- Kurvers RHJM, Adamczyk VMAP, Kraus RHS et al. (2013). Contrasting context dependence of familiarity and kinship in animal social networks. Animal Behaviour 86, 993–1001. [Google Scholar]
- Kurvers RHJM, Krause J, Croft DP, Wilson ADM, Wolf M (2014). The evolutionary and ecological consequences of animal social networks: emerging issues. Trends in Ecology & Evolution 29, 326–35. [DOI] [PubMed] [Google Scholar]
- Leu ST, Farine DR, Wey TW, Sih A, Bull CM (2016). Environment modulates population social structure: experimental evidence from replicated social networks of wild lizards. Animal Behaviour 111, 23–31. [Google Scholar]
- Li GL, Hou XL, Wan XR, Zhang ZB (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, 76–84. [DOI] [PubMed] [Google Scholar]
- Li XS, Wang DH (2005). Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (Meriones unguiculatus): The roles of short photoperiod and cold. Journal of Comparative Physiology B‐Biochemical Systemic and Environmental Physiology 175, 593–600. [DOI] [PubMed] [Google Scholar]
- Liu W, Wan X, Zhong W (2007). Population dynamics of the Mongolian gerbils: seasonal patterns and interactions among density, reproduction and climate. Journal of Arid Environments 68, 383–97. [Google Scholar]
- Liu W, Wang GM, Wang YN, Zhong WQ, Wan XR (2009). Population ecology of wild Mongolian gerbils Meriones unguiculatus . Journal of Mammalogy 90, 832–40. [Google Scholar]
- Liu W, Wang GM, Wan XR, Zhong WQ (2011). Winter food availability limits winter survival of Mongolian gerbils (Meriones unguiculatus). Acta Theriologica 56, 219–27. [Google Scholar]
- Lusseau D, Newman MEJ (2004). Identifying the role that animals play in their social networks. Proceedings of the Royal Society B‐Biological Sciences 271, S477–81. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ma ST, Resendez SL, Aragona BJ (2014). Sex differences in the influence of social context, salient social stimulation and amphetamine on ultrasonic vocalizations in prairie voles. Integrative Zoology 9, 280–93. [DOI] [PubMed] [Google Scholar]
- Makagon MM, McCowan B, Mench JA (2012). How can social network analysis contribute to social behavior research in applied ethology? Applied Animal Behaviour Science 138, 152–61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maldonado‐Chaparro AA, Hubbard L, Blumstein DT (2015). Group size affects social relationships in yellow‐bellied marmots (Marmota flaviventris). Behavioral Ecology 26, 909–15. [Google Scholar]
- Mitani JC, Watts DP, Amsler SJ (2010). Lethal inter-group aggression leads to territorial expansion in wild chimpanzees. Current Biology 20, R507–8. [DOI] [PubMed] [Google Scholar]
- Montague MJ, Disotell TR, 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, 169–87. [Google Scholar]
- Morrison SF, Pelchat G, Donahue A, Hik DS (2009). Influence of food hoarding behavior on the over‐winter survival of pikas in strongly seasonal environments. Oecologia 159, 107–16. [DOI] [PubMed] [Google Scholar]
- Nichols HJ, Cant MA, Sanderson JL (2015). Adjustment of costly extra‐group paternity according to inbreeding risk in a cooperative mammal. Behavioral Ecology 26, 1486–94. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Owen MA, Swaisgood RR, Blumstein DT (2017). Contextual influences on animal decision‐making: Significance for behavior‐based wildlife conservation and management. Integrative Zoology 12, 32–48. [DOI] [PubMed] [Google Scholar]
- Pinter‐Wollman N, Hobson EA, Smith JE et al. (2014). The dynamics of animal social networks: analytical, conceptual, and theoretical advances. Behavioral Ecology 25, 242–55. [Google Scholar]
- R Core Team (2015). R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing; Available from: http://www.R-project.org. [Google Scholar]
- Royle NJ, Pike TW, Heeb P, Richner H, Kolliker M (2012). Offspring social network structure predicts fitness in families. Proceedings of the Royal Society B‐Biological Sciences 279, 4914–22. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruckstuhl KE (2007). Sexual segregation in vertebrates: Proximate and ultimate causes. Integrative and Comparative Biology 47, 245–57. [DOI] [PubMed] [Google Scholar]
- Silk JB, Beehner JC, Bergman TJ et al. (2009). The benefits of social capital: Close social bonds among female baboons enhance offspring survival. Proceedings of the Royal Society B‐Biological Sciences 276, 3099–104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silk JB, Beehner JC, Bergman TJ et al. (2010). Strong and consistent social bonds enhance the longevity of female baboons. Current Biology 20, 1359–61. [DOI] [PubMed] [Google Scholar]
- Smith JE, Van Horn RC, Powning KS et al. (2010). Evolutionary forces favoring intragroup coalitions among spotted hyenas and other animals. Behavioral Ecology 21, 284–303. [Google Scholar]
- Vessey SH, Vessey KB (2007). Linking behavior, life history and food supply with the population dynamics of white‐footed mice (Peromyscus leucopus). Integrative Zoology 2, 123–30. [DOI] [PubMed] [Google Scholar]
- Walker FM, Taylor AC, Sunnucks P (2008). Female dispersal and male kinship‐based association in southern hairy‐nosed wombats (Lasiorhinus latifrons). Molecular Ecology 17, 1361–74. [DOI] [PubMed] [Google Scholar]
- Wang Y, Liu W, Wang G, Wan X, Zhong W (2011). Home‐range sizes of social groups of Mongolian gerbils Meriones unguiculatus . Journal of Arid Environments 75, 132–7. [Google Scholar]
- Wey T, Blumstein DT, Shen W, Jordán F (2008). Social network analysis of animal behaviour: a promising tool for the study of sociality. Animal Behaviour 75, 333–44. [Google Scholar]
- Wey TW, Blumstein DT (2010). Social cohesion in yellow‐bellied marmots is established through age and kin structuring. Animal Behaviour 79, 1343–52. [Google Scholar]
- Wey TW, Blumstein DT (2012). Social attributes and associated performance measures in marmots: bigger male bullies and weakly affiliating females have higher annual reproductive success. Behavioral Ecology and Sociobiology 66, 1075–85. [Google Scholar]
- Wey TW, Burger JR, Ebensperger LA, Hayes LD (2013). Reproductive correlates of social network variation in plurally breeding degus (Octodon degus). Animal Behaviour 85, 1407–14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whitehead H (2008). Analyzing Animal Societies: Quantitative Methods for Vertebrate Social Analysis. Chicago: University of Chicago Press. [Google Scholar]
- Wolff JO (2007). Social biology of rodents. Integrative Zoology 2, 193–204. [DOI] [PubMed] [Google Scholar]