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Variability in individual rates of aggression in wild gray seals: fine-scale analysis reveals importance of social and spatial stability

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Abstract

Aggressive interactions are costly for individuals in time, energy, or physical damage, and in polygynous mating systems, there is high variability in the rates and intensity of aggression across individuals and within breeding seasons. However, examinations into the drivers of this variability are often conducted in isolation, in non-wild systems, or the predictor variables in question, for example, dominance, are averaged across large spatial, social, or temporal scales. The aim of this study was to adopt a fine spatial and temporal scale approach to investigate the factors associated with inter-individual variation in aggression in wild, breeding male gray seals within three consecutive breeding seasons. To do this, we fit models examining if the daily frequency of aggression and probability of escalated aggression for males was best explained by factors such as dominance score, proximity to competitors or females, local social stability, and the occurrence of stochastic environmental events. Stability of neighbor identities was the strongest correlate of reduced male aggression. Dominance status did not correlate with aggression at the daily scale, with the exception of one period after a natural disturbance to the breeding colony where dominant males had relatively reduced rates of aggression. These findings emphasize the importance of local social stability in explaining inter-individual variation in aggression in a wild population and suggest that factors associated with aggression are context dependent in relation to the natural environment. Furthermore, we highlight the utility of a fine temporal scale and incorporating spatial parameters when investigating variability in aggression in wild systems.

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References

  • Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–265

    Article  CAS  PubMed  Google Scholar 

  • Anderson SS, Fedak MA (1985) Grey seal males: energetic and behavioural links between size and sexual success. Anim Behav 33:829–838

    Article  Google Scholar 

  • Anderson SS, Harwood J (1985) Time budgets and topography: how energy reserves and terrain determine the breeding behaviour of grey seals. Anim Behav 33:1343–1348

    Article  Google Scholar 

  • Anderson SS, Burton RW, Summers CF (1975) Behaviour of grey seals (Halichoerus grypus) during a breeding season at North Rona. J Zool 177:179–195

    Article  Google Scholar 

  • Ang TZ, Manica A (2010) Benefits and costs of dominance in the angelfish Centropyge bicolor. Ethology 9:855–865

    Google Scholar 

  • Arnott G, Elwood RW (2009) Assessment of fighting ability in animal contests. Anim Behav 77:991–1004

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42, http://CRAN.R-project.org/package=lme4

  • Bee MA (2003) A test of the ‘dear enemy effect’ in the strawberry dart-poison frog (Dendrobates pumilio). Behav Ecol Sociobiol 54:601–610

    Article  Google Scholar 

  • Bishop AB, Lidstone-Scott R, Pomeroy PP, Twiss SD (2014) Body Slap: an innovative aggressive display by breeding male gray seals (Halichoerus grypus). Mar Mammal Sci 30:579–593

    Article  Google Scholar 

  • Bishop AB, Denton P, Pomeroy PP, Twiss SD (2015a) Good vibrations by the beach boys: seismic magnitude is an honest indicator of male grey seal size. Anim Behav 100:74–82

    Article  Google Scholar 

  • Bishop AB, Pomeroy PP, Twiss SD (2015b) Breeding male grey seals exhibit similar activity budgets across varying exposures to human activity. Mar Ecol-Prog Ser 527:247–259

    Article  Google Scholar 

  • Bohórquez-Herrera J, Hernández-Camacho CJ, Aurioles-Gamboa D, Cruz-Escalona VH (2014) Plasticity in the agonistic behaviour of male California sea lions, Zalophus californianus. Anim Behav 89:31–38

    Article  Google Scholar 

  • Boness DJ (1984) Activity budget of male gray seals, Halichoerus grypus. J Mammal 65:291–297

    Article  Google Scholar 

  • Boness DJ, James H (1979) Reproductive behaviour of the grey seal (Halichoerus grypus) on Sable Island, Nova Scotia. J Zool 188:477–500

    Article  Google Scholar 

  • Booksmythe I, Jennions MD, Backwell PRY (2010) Investigating the ‘dear enemy’ phenomenon in the territory defence of the fiddler crab, Uca mjoebergi. Anim Behav 79:419–423

    Article  Google Scholar 

  • Boyd R, Silk JB (1983) A method for assigning cardinal dominance ranks. Anim Behav 31:45–58

    Article  Google Scholar 

  • Briffa M, Elwood RW (2004) Use of energy reserves in fighting hermit crabs. Proc R Soc Lond B 271:373–379

    Article  Google Scholar 

  • Carlini AR, Poljak S, Daneri GA, Márquez MEI, Negrete J (2006) The dynamics of male harem dominance in southern elephant seals (Mirounga leonina) at the South Shetland Islands. Polar Biol 29:796–805

    Article  Google Scholar 

  • Casey C, Reichmuth C, Fregosi S, Charrier I, Mathevon N (2013) The acoustic signature of the male northern elephant seal: individual variation supports recognition during competitive interactions. J Acoust Soc Am 134:3988

    Article  Google Scholar 

  • Cross HB, Blumstein DT, Rosell F (2013) Do marmots display a ‘dear enemy phenomenon’ in response to anal gland secretions? J Zool 289:189–195

    Article  Google Scholar 

  • David HA (1987) Ranking from unbalanced paired-comparison data. Biometrika 74:432–436

    Article  Google Scholar 

  • De Vries H, Stevens JMG, Vervaecke H (2006) Measuring and testing the steepness of dominance hierarchies. Anim Behav 71:585–592

    Article  Google Scholar 

  • Drews C (1993) The concept and definition of dominance in animal behaviour. Behaviour 125:283–313

    Article  Google Scholar 

  • Francis RC (1988) On the relationship between aggression and social dominance. Ethology 3:223–237

    Google Scholar 

  • Gammell MP, De Vries H, Jennings DJ, Carlin CM, Hayden TJ (2003) David’s score: a more appropriate dominance ranking method than Clutton-Brock et al.’s index. Anim Behav 66:601–605

    Article  Google Scholar 

  • Ganem G, Nevo E (1996) Ecophysiological constraints associated with aggression, and evolution toward pacifism in Spalax ehrenbergi. Behav Ecol Sociobiol 38:245–252

    Article  Google Scholar 

  • Gerber LR, González-Suárez M, Hernández-Camacho CJ, Young JK, Sabo JL (2010) The cost of male aggression and polygyny in California sea lions (Zalophus californianus). PLoS-ONE 5, e12230

    Article  PubMed Central  PubMed  Google Scholar 

  • Getty T (1987) Dear enemies and the prisoner’s dilemma: why should territorial neighbors form defensive coalitions? Am Zool 27:327–336

    Google Scholar 

  • Goessmann C, Hemelrijk C, Huber R (2000) The formation and maintenance of crayfish hierarchies: behavioural and self-structuring properties. Behav Ecol Sociobiol 48:418–428

    Article  Google Scholar 

  • Graham ME, Herberholz J (2009) Stability of dominance relationships in crayfish depends on social context. Anim Behav 77:195–199

    Article  Google Scholar 

  • Haley MP, Deutsch CJ, Le Boeuf BJ (1994) Size, dominance and copulatory success in male northern elephant seals, Mirounga angustirostris. Anim Behav 48:1249–1260

    Article  Google Scholar 

  • Heitor F, do Mar Oom M, Vicente L (2006) Social relationships in a herd of Sorraia horses: part 1. Correlates of social dominance and contexts of aggression. Behav Process 73:170–177

    Article  Google Scholar 

  • Hemelrijk CK (2000) Towards the integration of social dominance and spatial structure. Anim Behav 59:1035–1048

    Article  PubMed  Google Scholar 

  • Herberholz J, McCurdy C, Edwards DH (2007) Direct benefits of social dominance in juvenile crayfish. Biol Bull 213:21–27

    Article  PubMed  Google Scholar 

  • Husak JF, Fox SF (2003a) Adult male collard lizards, Crotaphytus collaris, increase aggression towards displaced neighbours. Anim Behav 65:391–396

    Article  Google Scholar 

  • Husak JF, Fox SF (2003b) Spatial organization and the dear enemy phenomenon in adult female collared lizards, Crotaphytus collaris. J Herpetol 37:211–215

    Article  Google Scholar 

  • Insley SJ, Phillips AV, Charrier I (2003) A review of social recognition in pinnipeds. Aquat Mamm 29:181–201

    Article  Google Scholar 

  • Jaeger RG (1981) Dear enemy recognition and the costs of aggression between salamanders. Am Nat 117:962–974

    Article  Google Scholar 

  • James HMC (2013) Individual differences in maternal behaviour in the grey seal (Halichoerus grypus) and the impact of disturbance at Donna Nook. Durham Theses, Durham University, http://etheses.dur.ac.uk/7305

  • Killen SS, Marras S, Metcalfe NB, McKenzie DJ, Domenici P (2013) Environmental stressors alter relationships between physiology and behaviour. Trends Ecol Evol 28:651–658

    Article  PubMed  Google Scholar 

  • Kokko H (2013) Dyadic contests: modelling fights between two individuals. In: Hardy ICW, Briffa M (eds) Animal contests. Cambridge University Press, Cambridge, pp 5–32

    Chapter  Google Scholar 

  • Kovacs KM, Lavigne DM (1986) Growth of grey seal (Halichoerus grypus) neonates: differential maternal investment in the sexes. Can J Zool 64:1937–1943

    Article  Google Scholar 

  • Lachish S, Goldizen AW (2004) Responses to neighbours and non-neighbours in the buff-banded rail (Gallirallus philippensis): no dear-enemy relationships. Aust J Zool 52:369–378

    Article  Google Scholar 

  • Lawson JM (1993) A descriptive and quantitative comparison of the communication of gray seals, Halichoerus grypus, at three sites in the North Atlantic Ocean. PhD thesis, Memorial University, St. John’s, Newfoundland, http://collections.mun.ca/PDFs/theses/Lawson_JohnWarren2.pdf

  • Leiser JK (2003) When are neighbours ‘dear enemies’ and when are they not? The responses of territorial male variegated pupfish, Cyprinodon variegatus, to neighbours, strangers and heterospecifics. Anim Behav 65:453–462

    Article  Google Scholar 

  • Lidgard DC, Boness DJ, Bowen WD, McMillan JI, Fleischer RC (2004) The rate of fertilization in male mating tactics of the polygynous grey seal. Mol Ecol 13:3543–3548

    Article  CAS  PubMed  Google Scholar 

  • Lidgard DC, Boness DJ, Bowen WD, McMillan JI (2005) State-dependent male mating tactics in the grey seal: the importance of body size. Behav Ecol 16:541–549

  • Maynard Smith J (1974) The theory of games and the evolution of animal conflicts. J Theor Biol 47:209–221

    Article  Google Scholar 

  • Maynard Smith J, Price GR (1973) The logic of animal conflict. Nature 246:15–18

    Article  Google Scholar 

  • McCulloch S, Boness DJ (2000) Mother-pup vocal recognition in the grey seal (Halichoerus grypus) Sable Island, Nova Scotia. Can J Zool 251:449–455

    Google Scholar 

  • McCulloch S, Pomeroy PP, Slater PJB (1999) Individually distinctive pup vocalizations fail to prevent allo-suckling in grey seals. Can J Zool 77:716–723

    Article  Google Scholar 

  • Miller EH, Boness DJ (1979) Remarks on display functions of the snout of the grey seal, Halichoerus grypus (Fab.), with comparative notes. Can J Zool 57:140–148

  • Monclús R, Saavedra I, de Miguel J (2014) Context-dependent responses to neighbours and strangers in wild European rabbits (Oryctolagus cuniculus). Behav Process 106:17–21

  • Neumann C, Duboscq J, Dubuc C, Ginting A, Irwan AM, Agil M, Widdig A, Englehardt A (2011) Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating. Anim Behav 82:911–921

    Article  Google Scholar 

  • Ostner J, Heistermann M, Schulke O (2008) Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Horm Behav 54:613–619

    Article  PubMed  Google Scholar 

  • Pomeroy PP, Anderson SS, Twiss SD, McConnell BJ (1994) Dispersion and site fidelity of breeding female grey seals (Halichoerus grypus) on North Rona, Scotl. J Zool 233:429–447

  • Pomeroy PP, Twiss SD, Redman P (2000) Philopatry, site fidelity and local kin associations within grey seal breeding colonies. Ethology 10:899–919

    Article  Google Scholar 

  • Pomeroy PP, Redman PR, Ruddell SJS, Duck CD, Twiss SD (2005) Breeding site choice fails to explain interannual associations of female grey seals. Behav Ecol Sociobiol 57:546–556

    Article  Google Scholar 

  • Pörschmann U, Trillmich F, Mueller B, Wolf JBW (2010) Male reproductive success and its behavioural correlates in a polygynous mammal, the Galápagos sea lion (Zalophus wollebaeki). Mol Ecol 19:2574–2586

    PubMed  Google Scholar 

  • Redman P, Pomeroy PP, Twiss SD (2001) Grey seal maternal attendance patterns are affected by water availability on North Rona, Scotland. Can J Zool 79:1073–1079

    Article  Google Scholar 

  • Richards SA (2008) Dealing with overdispersed count data in applied ecology. J Appl Ecol 45:218–227

    Article  Google Scholar 

  • Robinson KJ, Twiss S, Hazon N, Moss S, Lonergan M, Pomeroy PP (2015) Conspecific recognition and aggression reduction to familiars in newly weaned, socially plastic mammals. Behav Ecol and Sociobiol (published online doi:10.1007/s00265-015-1952-7)

  • Rosenthal CM, Bennett NC, Jarvis JUM (1992) The changes in the dominance hierarchy over time of a complete field-captured colony of Cryptomys hottentotus hottentotus. J Zool 228:205–226

    Article  Google Scholar 

  • Ruddell SJS, Twiss SD, Pomeroy PP (2007) Measuring opportunity for sociality: quantifying social stability in a colonially breeding phocid. Anim Behav 74:1357–1368

    Article  Google Scholar 

  • Stewart JE, Pomeroy PP, Duck CD, Twiss SD (2014) Finescale ecological niche modelling provides evidence that lactating gray seals (Halichoerus grypus) prefer access to fresh water in order to drink. Mar Mamm Sci 30:1456–1472

    Article  Google Scholar 

  • Tierney AJ, Andrews K, Happer KR, White MKM (2013) Dear enemies and nasty neighbors in crayfish: effects of social status and sex on responses to familiar and unfamiliar conspecifics. Behav Process 99:47–51

    Article  CAS  Google Scholar 

  • Twiss SD (1991) Behavioural and energetic determinants of individual mating and success in male grey seals (Halichoerus grypus). PhD thesis, University of Glasgow, Glasgow

  • Twiss SD, Pomeroy PP, Anderson SS (1994) Dispersion and site fidelity of breeding male grey seals (Halichoerus grypus) on North Rona, Scotland. J Zool 233:683–693

    Article  Google Scholar 

  • Twiss SD, Anderson SS, Monaghan P (1998) Limited intra-specific variation in male grey seal (Halichoerus grypus) dominance relationships in relation to variation in male mating success and female availability. J Zool 246:259–267

    Article  Google Scholar 

  • Twiss SD, Caudron A, Pomeroy PP, Thomas CJ, Mills JP (2000) Finescale topographical correlates of behavioural investment in offspring by female grey seals, Halichoerus grypus. Anim Behav 59:327–338

    Article  PubMed  Google Scholar 

  • Twiss SD, Wright NC, Dunstone N, Redman P, Moss S, Pomeroy PP (2002) Behavioral evidence of thermal stress from overheating in UK breeding gray seals. Mar Mamm Sci 18:455–468

    Article  Google Scholar 

  • Twiss SD, Poland VF, Graves JA, Pomeroy PP (2006) Finding fathers: spatio-temporal analysis of paternity assignment in grey seals (Halichoerus grypus). Mol Ecol 15:1939–1953

    Article  CAS  PubMed  Google Scholar 

  • Twiss SD, Thomas C, Poland V, Graves JA, Pomeroy P (2007) The impact of climatic variation on the opportunity for sexual selection. Biol Lett 3:12–15

    Article  PubMed Central  PubMed  Google Scholar 

  • Wolf JBW, Kauermann G, Trillmich F (2005) Males in the shade: habitat use and sexual segregation in the Galápagos sea lion (Zalophus californianus wollebaeki). Behav Ecol Sociobiol 59:293–302

    Article  Google Scholar 

  • Worthington-Wilmer J, Overall AJ, Pomeroy PP, Twiss SD, Amos W (2000) Patterns of paternal relatedness in British grey seal colonies. Mol Ecol 9:283–292

    Article  Google Scholar 

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Acknowledgments

This work was supported by the Durham Doctoral Studentship. We would like to thank the assistance and support of the Lincolnshire Wildlife Trust, specifically Rob Lidstone-Scott and Lizzie Lemon, for logistical assistance. We also thank James Stewart for assistance in data collection. Finally, thank you to the editor and the two anonymous reviewers whose comments and suggestions improved this manuscript.

Ethical Approval

This study was observational in nature, and all work complies with the current UK laws of animal welfare. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Funding

This study was funded by a Durham Doctoral Studentship awarded to author AB.

Conflict of Interest

Author AB declares she has no conflict of interest. Author PP declares that he has no conflict of interest. Author ST declares that he has no conflict of interest.

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Correspondence to Amanda M. Bishop.

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Communicated by V. M. Janik

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Bishop, A.M., Pomeroy, P. & Twiss, S.D. Variability in individual rates of aggression in wild gray seals: fine-scale analysis reveals importance of social and spatial stability. Behav Ecol Sociobiol 69, 1663–1675 (2015). https://doi.org/10.1007/s00265-015-1978-x

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  • DOI: https://doi.org/10.1007/s00265-015-1978-x

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