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Social security: social relationship strength and connectedness influence how marmots respond to alarm calls

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A Correction to this article was published on 16 December 2019

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Abstract

Individuals vary in the number and types of social relationships they maintain. If beneficial, social relationships may reduce predation risk and thus increase an individual’s sense of security. We tested this hypothesis by studying the responses of female yellow-bellied marmots (Marmota flaviventer) to broadcast alarm calls from unfamiliar individuals. First, we quantified affiliative interactions of animals in the field to calculate a set of social network measures. Because attributes of sociality are often correlated, we used principal component analysis to reduce our social network metrics to two unrelated factors and used the social network measure that accounted for the most variance for each principal component in further analyses. We then quantified the change in time allocated to vigilance and foraging following alarm call playback from baseline levels to the first 30 s and the second 30 s period (i.e., 31–60 s) following playback. We expected that if marmots with strong affiliative relationships felt more secure, they would forage more and allocate less time to vigilance after their immediate vigilance response to the broadcast alarm calls. Using mixed effects models that controlled for variation explained by a number of biologically important covariates and permutation tests to test the significance of social network variables, we found that marmots with a higher incloseness allocated significantly more time to vigilance in both the first and second 30 s after hearing a novel alarm call. Additionally, and while not significant (the observed parameter estimate fell between the 90 and 95% CI), marmots with a higher outstrength increased foraging in the second 30 s after hearing a novel alarm call. If we assume that time allocated to foraging is a measure of security, then marmots with strong affiliative relationships reacted more to an alarm call from a novel individual and seemingly felt more secure than their counterparts. Our results, therefore, suggest that strong social relationships increase perceptions of security and illustrate an effect of social relationships on predation risk assessment.

Significance statement

In many species, including humans, there are benefits from maintaining good social relationships. These benefits include better health and greater longevity. We studied yellow-bellied marmots, a ground-dwelling squirrel that is notable because it has variable social relationships. Capitalizing on this social variation, we found that marmots that maintain strong affiliative relationships with other marmots may indeed forage more after hearing an artificially broadcast alarm call than marmots with weaker affiliative relationships. This result suggests that marmots that are more socially connected with others in their group may feel relatively more secure, possibly because they have others that can help them assess risk, and that a benefit of maintaining strong friendly social ties is that it permits animals to forage more. Thus, we suggest a new way that social relationships can be beneficial: they increase perceptions of security and this ultimately may facilitate foraging.

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Change history

  • 16 December 2019

    Unfortunately, there was an error in the R script which led to the incorrect labeling of two social network measures.

References

  • Archie EA, Altmann J, Alberts SC (2012) Social status predicts wound healing in wild baboons. P Natl Acad Sci USA 109:9017–9022

    CAS  Google Scholar 

  • Armitage KB (1965) Vernal behaviour of the yellow-bellied marmot (Marmota flaviventris). Anim Behav 13:59–68

    Google Scholar 

  • Armitage KB, Schwartz OA (2000) Social enhancement of fitness in yellow-bellied marmots. Proc Natl Acad Sci USA 97:12149–12152

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bachman GC (1993) The effect of body condition on the trade-off between vigilance and foraging in Belding’s ground squirrels. Anim Behav 46:233–244

    Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. http://lme4.r-forge.r-project.org/

  • Beauchamp G (2008) What is the magnitude of the group size effect on vigilance? Behav Ecol 19:1361–1368

    Google Scholar 

  • Bednekoff PA, Blumstein DT (2009) Peripheral obstructions influence marmot vigilance: integrating observational and experimental results. Behav Ecol 20:1111–1117

    Google Scholar 

  • Blumstein DT (2013) Yellow-bellied marmots: insights from an emergent view of sociality. Philos T Roy Soc B 368:20120349

    Google Scholar 

  • Blumstein DT, Armitage KB (1998) Life history consequences of social complexity: a comparative study of ground-dwelling sciurids. Behav Ecol 9:8–19

    Google Scholar 

  • Blumstein DT, Daniel JC (2004) Yellow-bellied marmots discriminate between the alarm calls of individuals and are more responsive to the calls from pups. Anim Behav 68:1257–1265

    Google Scholar 

  • Blumstein DT, Daniel JC (2007) Quantifying behavior the JWatcher way. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Blumstein DT, Récapet C (2009) The sound of arousal: the addition of novel non-linearities increases responsiveness in marmot alarm calls. Ethology 115:1074–1081

    Google Scholar 

  • Blumstein DT, Steinmetz J, Armitage KB, Daniel JC (1997) Alarm calling in yellow-bellied marmots: II. The importance of direct fitness. Anim Behav 53:173–184

    Google Scholar 

  • Blumstein DT, Verenyre L, Daniel JC (2004) Reliability and the adaptive utility of discrimination among alarm callers. Proc R Soc Lond B 271:1851–1857

    Google Scholar 

  • Blumstein DT, Patton ML, Saltzman W (2006) Faecal glucocorticoid metabolites and alarm calling in free-living yellow-bellied marmots. Biol Lett 2:29–32

    CAS  PubMed  Google Scholar 

  • Blumstein DT, Cooley L, Winternitz J, Daniel JC (2008a) Do yellow-bellied marmots respond to predator vocalizations? Behav Ecol Sociobiol 62:457–468

    Google Scholar 

  • Blumstein DT, Richardson DT, Cooley L, Winternitz J, Daniel JC (2008b) The structure, meaning and function of yellow-bellied marmot pup screams. Anim Behav 76:1055–1064

    Google Scholar 

  • Blumstein DT, Wey TW, Tang K (2009) A test of the social cohesion hypothesis: interactive female marmots remain at home. Proc R Soc Lond B 276:3007–3012

    Google Scholar 

  • Blumstein DT, Ebensperger LA, Hayes LD et al (2010) Towards an integrative understanding of social behavior: new models and new opportunities. Front Behav Neurosci 4:34

    PubMed  PubMed Central  Google Scholar 

  • Cañon Jones HA, Noble C, Damsgård B, Pearce GP (2011) Social network analysis of the behavioural interactions that influence the development of fin damage in Atlantic salmon parr (Salmo salar) held at different stocking densities. Appl Anim Behav Sci 133:117–126

    Google Scholar 

  • Caro T (2005) Antipredator defenses in birds and mammals. The University of Chicago Press, Chicago

    Google Scholar 

  • Chmura HE, Wey TW, Blumstein DT (2016) Assessing the sensitivity of foraging and vigilance to internal state and environmental variables in yellow-bellied marmots (Marmota flaviventris). Behav Ecol Sociobiol 70:1901–1910

    Google Scholar 

  • Christakis NA, Fowler JH (2007) The spread of obesity in a large social network over 32 years. New Engl J Med 357:370–379

    CAS  PubMed  Google Scholar 

  • Croft DP, Krause J, Darden SK, Ramnarine IW, Faria JJ, James R (2009) Behavioural trait assortment in a social network: patterns and implications. Behav Ecol Sociobiol 63:1495–1503

    Google Scholar 

  • Croft DP, Madden JR, Franks DW, James R (2011) Hypothesis testing in animal social networks. Trends Ecol Evol 26:502–507

    PubMed  Google Scholar 

  • Csárdi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 2006:1695

    Google Scholar 

  • Daura-Jorge FG, Cantor M, Ingram SN, Lusseau D, Simões-Lopes PC (2012) The structure of a bottlenose dolphin society is coupled to a unique foraging cooperation with artisanal fishermen. Biol Lett 8:702–705

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elgar MA (1989) Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev 64:13–33

    CAS  PubMed  Google Scholar 

  • Falls JB (1982) Individual recognition by sounds in birds. In: Kroodsma DE, Miller EH (eds) Acoustic communication in birds, vol 2. Academic Press, New York, pp 237–278

    Google Scholar 

  • Farine DR (2017) A guide to null models for animal social network analysis. Meth Ecol Evol. https://doi.org/10.1111/2041-210X.12772

    PubMed  PubMed Central  Google Scholar 

  • Fuong H, Maldonado-Chaparro A, Blumstein DT (2015) Are social attributes associated with alarm calling propensity? Behav Ecol 26:587–592

    Google Scholar 

  • Gould L, Fedigan LM, Rose LM (1997) Why be vigilant? The case of the alpha animal. Int J Primatol 18:401–414

    Google Scholar 

  • Halekoh U, Højsgaard S (2017) Package ‘pbkrtest’, cran. r-project.org/web/packages/pbkrtest/pbkrtest.pdf

  • Heathcote RJP, Darden SK, Franks DW, Ramnarine IW, Croft DP (2017) Fear of predation drives stable and differentiated social relationships in guppies. Sci Rep 7:41679

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hofmann HA, Beery AK, Blumstein DT, Couzin ID, Earley RL, Hayes LD, Hurd PL, Lacey EA, Phelps SM, Solomon NG, Taborsky M, Young LJ, Rubenstein DR (2014) An evolutionary framework for studying mechanisms of social behaviour. Trends Ecol Evol 29:581–589

    PubMed  Google Scholar 

  • Ioannou CC, Ramnarine IW, Torney CJ (2017) High-predation habitats affect the social dynamics of collective exploration in a shoaling fish. Sci Adv 3:e1602682

    PubMed  PubMed Central  Google Scholar 

  • Kern JM, Radford AN (2016) Social-bond strength influences vocally mediated recruitment to mobbing. Biol Lett 12:20160648

    PubMed  PubMed Central  Google Scholar 

  • Krams I (1998) Dominance-specific vigilance in the great tit. J Avian Biol 29:55–60

    Google Scholar 

  • Lea AJ, Blumstein DT (2011) Age and sex influence marmot antipredator behavior during periods of heightened risk. Behav Ecol Sociobiol 65:1525–1533

    PubMed  PubMed Central  Google Scholar 

  • Lea AJ, Blumstein DT, Wey TW, Martin JGA (2010) Heritable victimization and the benefits of agonistic relationships. P Natl Acad Sci USA 107:21587–21592

    CAS  Google Scholar 

  • Lehmann J, Ross C (2011) Baboon (Papio anubis) social complexity—a network approach. Am J Primatol 73:775–789

    PubMed  Google Scholar 

  • Li C, Monclus R, Maul TL, Jiang Z, Blumstein DT (2011) Quantifying human disturbance on antipredator behaviour and flush initiation distance in yellow-bellied marmots. Appl Anim Behav Sci 129:146–152

    Google Scholar 

  • Micheletta J, Waller BM, Panggur MR, Neumann C, Duboscq J, Agil M, Engelhardt A (2012) Social bonds affect anti-predator behavior in a tolerant species of macaque, Macaca nigra. P Natl Acad Sci USA 279:4042–4050

    Google Scholar 

  • Monclús R, Anderson AM, Blumstein DT (2015) Do yellow-bellied marmots perceive enhanced predation risk when they are farther from safety?: an experimental study. Ethology 121:831–839

    Google Scholar 

  • Moody J, White DR (2003) Structural cohesion and embeddedness: a hierarchical concept of social groups. Am Sociol Rev 68:103–127

    Google Scholar 

  • Pollard KA (2011) Making the most of alarm signals: the adaptive value of individual discrimination in an alarm context. Behav Ecol 22:93–100

    Google Scholar 

  • R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org

    Google Scholar 

  • Revelle W (2015) Psych: procedures for personality and psychological research. http://cran.r-project.org/web/packages/psych/index.html

  • Smith JE, Monclús R, Wantuck D, Florant GL, Blumstein DT (2012) Fecal glucocorticoid metabolites in wild yellow-bellied marmots: experimental validation, individual differences and ecological correlates. Gen Comp Endocrinol 178:417–426

    CAS  PubMed  Google Scholar 

  • Taborsky M, Hofmann HA, Beery AK, Blumstein DT, Hayes LD, Lacey EA, Martins EP, Phelps SM, Solomon NG, Rubenstein DR (2015) Taxon matters: promoting integrative studies of social behavior. Trends Neurosci 38:189–191

    CAS  PubMed  Google Scholar 

  • Voelkl B, Firth JA, Sheldon BC (2016) Nonlethal predator effects on the turn-over of wild bird flocks. Sci Rep 6:33476

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waite TA (1987) Vigilance in the white-breasted nuthatch: effects of dominance and sociality. Auk 104:429–434

    Google Scholar 

  • Wasserman S, Faust K (1994) Social network analysis: methods and applications. Cambridge University Press, Cambridge

    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. Behav Ecol Sociobiol 66:1075–1085

    Google Scholar 

  • Wey T, Blumstein DT, Shen W, Jordan F (2008) Social network analysis of animal behavior: a promising tool for the study of sociality. Anim Behav 75:333–344

    Google Scholar 

  • Whitehead H (1995) Investigating structure and temporal scale in social organizations using identified individuals. Behav Ecol 6:199–208

    Google Scholar 

  • Wickham H (2009) ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York

    Google Scholar 

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Acknowledgements

We thank all the marmoteers who helped collect these data, and especially Janice Daniel, Jamie Winternitz, Charlotte Récapet, and Louise Cooley for help with playbacks; Amanda Lea for help organizing playback results; and five very constructive anonymous reviewers for comments on previous versions of the manuscript. We also thank Mason Porter, Noa Pinter-Wollman, Adriana Maldonado-Chaparro, and Nicole A. Thompson for many thoughtful discussions on social network analysis.

Funding

DTB was supported by the National Geographic Society, UCLA (Faculty Senate and the Division of Life Sciences), a Rocky Mountain Biological Laboratory research fellowship, and by the NSF (IDBR-0754247, and DEB-1119660 and 1557130 to DTB, as well as DBI 0242960, 0731346, and 1226713 to the Rocky Mountain Biological Laboratory). HF was a NSF-REU fellow and a UCLA Whitcome fellow, and manuscript writing was partially supported by the NSF (NYCEP IGERT 0966166).

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California, 621 Young Drive South, Los Angeles, CA, 90095-1606, USA

    Daniel T. Blumstein, Holly Fuong & Elizabeth Palmer

  2. The Rocky Mountain Biological Laboratory, Box 519, Crested Butte, CO, 81224, USA

    Daniel T. Blumstein

  3. Department of Ecology, Evolution, and Environmental Biology, Columbia University, 1200 Amsterdam Avenue, New York, NY, 10027, USA

    Holly Fuong

  4. New York Consortium in Evolutionary Primatology, New York, NY, USA

    Holly Fuong

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  1. Daniel T. Blumstein
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Correspondence to Daniel T. Blumstein.

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Ethical approval

The research was in compliance with ethical guidelines and the current laws of the USA. Marmots were studied under protocols approved by the UCLA and the RMBL Animal Use and Care Committees and under permits issued annually by the Colorado Division of Wildlife.

Conflict of interest

The authors declare that they have no conflict of interest.

Data availability statement

The datasets during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Additional information

Communicated by D. P. Croft

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Blumstein, D.T., Fuong, H. & Palmer, E. Social security: social relationship strength and connectedness influence how marmots respond to alarm calls. Behav Ecol Sociobiol 71, 145 (2017). https://doi.org/10.1007/s00265-017-2374-5

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  • DOI: https://doi.org/10.1007/s00265-017-2374-5

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