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Repeatability and reproductive consequences of boldness in female gray seals

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Abstract

Wild animals show consistent individual variation in behavior across time and/or contexts, now referred to as animal personality. While this variability may have important ecological and evolutionary implications, how and why variation in animal personality is maintained in a natural population remains unclear. In this study, we assessed the influence of environmental and biological sources of variation on behavioral responses measured along the shy-bold continuum in a long-lived, iteroparous marine mammal, the gray seal (Halichoerus grypus). Between 2008 and 2016, 469 females from the Sable Island, Nova Scotia breeding colony of gray seals were given a boldness score in response to a human approach, designed to stimulate maternal defense of offspring. Using generalized linear mixed-effects models (GLMM) in a Bayesian framework, we show that boldness is highly repeatable between and within years. There were age differences in boldness, with younger females being less bold than older, more experienced females providing some support for the life history trade-off hypothesis. We further used GLMMs to assess sources of variation on offspring weaning mass. We found that young females that were bolder produced heavier pups than shyer counterparts, and that pups produced by bolder females were on average ~ 2 kg heavier than pups of shy females. These results provide further evidence that personality influences life history strategies, and illustrates the evolutionary potential of animal personality in response to selection.

Significance statement

Consistent individual differences in behavior influence various aspects of ecology including species interactions, species distributions, and life history strategies. However, how and why this individual variation is maintained in a natural population remains uncertain. In this study, we assessed the influence of boldness, specifically maternal defense of offspring, on a component of reproductive success in a long-lived marine mammal. We showed highly repeatable behavioral differences, and found that boldness varied with age, with younger individuals being less bold than older individuals. Younger individuals that were bolder produced heavier offspring than shyer counterparts. Our study contributes to an under-represented group of animals, wild marine mammals, in the personality literature, and further prompts the investigation into the proximate and ultimate factors influencing personality in an ecologically important marine predator.

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References

  • Ambs SM, Boness DJ, Bowen WD, Perry EA, Fleischer RC (1999) Proximate factors associated with high levels of extraconsort fertilization in polygynous grey seals. Anim Behav 58:527–535

    Article  PubMed  CAS  Google Scholar 

  • Baker JR (1984) Mortality and morbidity in grey seal pups (Halichoerus grypus). Studies on its causes, effects of environment, the nature and sources of infectious agents and the immunological status of pups. J Zool 203:23–48

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Beekman M, Jordan LA (2017) Does the field of animal personality provide any new insights for behavioral ecology? Behav Ecol 28:617–623

    Article  Google Scholar 

  • Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783

    Article  PubMed  PubMed Central  Google Scholar 

  • Bergmüller R, Taborsky M (2010) Animal personality due to social niche specialization. Trends Ecol Evol 25:504–511

    Article  PubMed  Google Scholar 

  • Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368

    Article  PubMed  Google Scholar 

  • Bishop AM, Joseph O, Moss S, Pomeroy PP, Twiss SD (2016) Cannibalism by a male grey seal (Halichoerus grypus) in the North Sea. Aquat Mamm 42:137–143

    Article  Google Scholar 

  • Boake CRB (1989) Repeatability: its role in evolutionary studies of mating behaviour. Evol Ecol 3:173–182

    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 

  • Boness DJ, Anderson SS, Cox CR (1982) Function of female aggression during the pupping and mating season of grey seals, Halichoerus grypus (Fabricius). Can J Zool 60:2270–2278

    Article  Google Scholar 

  • Boness DJ, Bowen WD, Iverson SJ (1995) Does male harassment of females contribute to reproductive synchrony in the grey seal by affecting maternal performance? Behav Ecol Sociobiol 36:1–10

    Article  Google Scholar 

  • Bowen WD, McMillan J, Mohn R (2003) Sustained exponential growth of grey seals at Sable Island, Nova Scotia. ICES J Mar Sci 60:1265–1274

    Article  Google Scholar 

  • Bowen WD, Iverson SJ, McMillan JI, Boness DJ (2006) Reproductive performance in grey seals: age-related improvement and senescence in a capital breeder. J Anim Ecol 75:1340–1351

    Article  PubMed  CAS  Google Scholar 

  • Bowen WD, McMillan JI, Blanchard W (2007) Reduced population growth of grey seals at Sable Island: evidence from pup production and age of primiparity. Mar Mam Sci 23:48–64

    Article  Google Scholar 

  • Bowen WD, den Heyer CE, McMillan JI, Iverson SJ (2015) Offspring size at weaning affects survival to recruitment and reproductive performance of primiparous grey seals. Ecol Evol 5:1412–1424

    Article  PubMed  PubMed Central  Google Scholar 

  • Breed GA, Jonsen ID, Myers RA, Bowen WD, Leonard ML (2009) Sex-specific, seasonal foraging tactics of adult grey seals (Halichoerus grypus) revealed by state-space analysis. Ecology 90:3209–3221

    Article  PubMed  Google Scholar 

  • Bridger D, Bonner SJ, Briffa M (2015) Individual quality and personality: bolder males are less fecund in the hermit crab Pagurus bernhardus. Proc R Soc B 282:20142492

    Article  PubMed  Google Scholar 

  • Brown C, Jones F, Braithwaite VA (2007) Correlations between boldness and body mass in natural populations of the poeciliid Brachyrhaphis episcopi. J Fish Biol 71:1590–1601

    Article  Google Scholar 

  • Campioni L, Delgado MM, Penteriani V (2015) Pattern of repeatability in the movement behaviour of a long-lived territorial species, the eagle owl. J Zool 298:191–197

    Article  Google Scholar 

  • Carere C, Locurto C (2011) Interaction between animal personality and animal cognition. Curr Zool 57:491–498

    Article  Google Scholar 

  • Carter AJ, Heinsohn R, Goldizen AW, Biro PA (2012) Boldness, trappability and sampling bias in wild lizards. Anim Behav 83:1051–1058

    Article  Google Scholar 

  • Carter AJ, Feene WE, Marshall HH, Cowlishaw G, Heinsohn R (2013) Animal personality: what are behavioural ecologists measuring? Biol Rev 88:465–475

    Article  PubMed  Google Scholar 

  • Catling PM, Freedman B, Lucas Z (1984) Vegetation and phytogeography of Sable Island, Nova Scotia. Proc N S Inst Sci 24:181–248

    Google Scholar 

  • Christensen, RHB (2015) Ordinal–regression models for ordinal data. R package version 2015.6–28, http://www.cran.r-project.org/package=ordinal/

  • Christenson TE, Le Boeuf BJ (1978) Aggression in the female northern elephant seal, Mirounga angustirostris. Behaviour 64:158–172

    Article  PubMed  CAS  Google Scholar 

  • Coulson JC, Hickling G (1964) The breeding biology of the grey seal, Halichoerus grypus (Fab.), on the Farne Islands, Northumberland. J Anim Ecol 33:485–512

    Article  Google Scholar 

  • Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739

    Article  Google Scholar 

  • Delgado MM, Penteriani V (2008) Behavioural states help translate dispersal movements into spatial distribution patterns of floaters. Am Nat 172:475–485

    Article  Google Scholar 

  • Dingemanse NJ, de Goede P (2004) The relation between dominance and exploratory behaviour is context-dependent in wild great tits. Behav Ecol 15:1023–1030

    Article  Google Scholar 

  • Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184

    Article  Google Scholar 

  • Dohm MR (2002) Repeatability estimates do not always set an upper limit to heritability. Funct Ecol 16:273–280

    Article  Google Scholar 

  • Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86

    Article  PubMed  CAS  Google Scholar 

  • Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22

    Article  Google Scholar 

  • Hall AJ, McConnell BJ, Barker RJ (2001) Factors affecting first-year survival in grey seals and their implications for life history strategy. J Anim Ecol 70:138–149

    Article  Google Scholar 

  • Hammill MO, den Heyer CE, Bowen WD (2014) Grey seal popul trends in Canadian waters, 1960–2014. Department of Fisheries and Ocean, Canadian Science Advisory Secretariat, Research Document 2014/037.iv + 44p, Ottawa, Ontario, Canada

  • Harcourt R (1992) Maternal aggression in the South American fur seal in Peru. Can J Zool 70:320–325

    Article  Google Scholar 

  • Iverson SJ, Bowen WD, Boness DJ, Oftedal OT (1993) The effect of maternal size and milk output on pup growth in grey seals (Halichoerus grypus). Physiol Zool 66:61–88

    Article  Google Scholar 

  • Jungwirth A, Wedell N, Bshary R, Milinski M (2017) Animal personalities—an empty placeholder feigning understanding. Behav Ecol 28:629–630

    Article  Google Scholar 

  • Kovacs KM (1987) Maternal behaviour and early behavioural ontogeny of grey seals (Halichoerus grypus) on the Isle of May, UK. J Zool 213:697–715

    Article  Google Scholar 

  • Lang SLC, Iverson SJ, Bowen WD (2009) Repeatability in lactation performance and the consequences for maternal reproductive success in grey seals. Ecology 90:2513–2523

    Article  PubMed  CAS  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

    Article  Google Scholar 

  • Lidgard DC, Bowen WD, Boness DJ (2012) Longitudinal changes and consistency in male physical and behavioural traits have implications for mating success in the grey seal (Halichoerus grypus). Can J Zool 90:849–860

    Article  Google Scholar 

  • Maillet Z, Halliday W, Blouin-Demers G (2015) Exploratory and defensive behaviours change with sex and body size in eastern garter snakes (Thamnophis sirtalis). J Ethol 33:47–54

    Article  Google Scholar 

  • Mansfield AW, Beck B (1977) The grey seal in eastern Canada. Tech Rept Fish Mar Serv Canada 706:1–81

    Google Scholar 

  • Mayer M, Shine R, Brown GP (2016) Bigger babies are bolder: effects of body size on personality of hatchling snakes. Behaviour 153:313–323

    Article  Google Scholar 

  • Mellish JAE, Iverson SJ, Bowen WD (1999) Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics. Physiol Biochem Zool 72:677–690

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Noren DP, Crocker DE, Williams TM, Costa DP (2003) Energy reserve utilization in northern elephant seal (Mirounga angustirostris) pups during the postweaning fast: size does matter. J Comp Physiol B 173:443–454

    Article  PubMed  CAS  Google Scholar 

  • Noren SR, Boness DJ, Iverson SJ, McMillan J, Bowen WD (2008) Body condition at weaning affects the duration of the postweaning fast in grey seal pups (Halichoerus grypus). Physiol Biochem Zool 81:269–277

    Article  PubMed  Google Scholar 

  • Patrick SC, Weimerskirch H (2014) Senescence rates and late adulthood reproductive success are strongly influenced by personality in a long-lived seabird. Proc R Soc Lond B 282:20141649

    Article  Google Scholar 

  • Patrick SC, Charmantier A, Weimerskirch H (2013) Differences in boldness are repeatable and heritable in a long-lived marine predator. Ecol Evol 3:4291–4299

    Article  PubMed  PubMed Central  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, Scotland. J Zool 233:429–447

    Article  Google Scholar 

  • Pomeroy PP, Fedak MA, Rothery P, Anderson S (1999) Consequences of maternal size for reproductive expenditure and pupping success of grey seals at North Rona, Scotland. J Anim Ecol 68:235–253

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/

    Google Scholar 

  • Réale D, Gallant BY, Leblanc M, Festa-Bianchet M (2000) Consistency of temperament in bighorn ewes and correlates with behaviour and life history. Anim Behav 60:589–597

    Article  PubMed  Google Scholar 

  • Réale D, Reader SM, Sol D, Mcdougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    Article  PubMed  Google Scholar 

  • Roche DG, Careau V, Binning SA (2016) Demystifying animal ‘personality’ (or not): why individual variation matters to experimental biologists. J Exp Biol 219:3832–3843

    Article  PubMed  Google Scholar 

  • Schuett W, Tregenza T, Dall SRX (2010) Sexual selection and animal personality. Biol Rev 85:217–246

    Article  PubMed  Google Scholar 

  • Sih A (2017) Insights for behavioral ecology from behavioral syndromes: a comment on Beekman and Jordan. Behav Ecol 28:627–628

    Article  Google Scholar 

  • Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioural syndromes: an integrative overview. Q Rev Biol 79:241–277

    Article  PubMed  Google Scholar 

  • Sloan Wilson D (1998) Adaptive individual differences within single populations. Phil Trans R Soc B 353:199–205

    Article  Google Scholar 

  • Sloan Wilson D, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442–446

    Article  PubMed  CAS  Google Scholar 

  • Smith BR, Blumstein DT (2008) Fitness consequence of personality: a meta-analysis. Behav Ecol 19:448–455

    Article  Google Scholar 

  • Stamps JA, Groothuis TGG (2010) Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Phil Trans R Soc B 365:4029–4041

    Article  PubMed  Google Scholar 

  • Stamps JA, Briffa M, Biro PA (2012) Unpredictable animals: individual differences in intraindividual variability. Anim Behav 83:1325–1334

    Article  Google Scholar 

  • Turbill C, Ruf T (2010) Senescence is more important in the natural lives of long- than short-lived mammals. PLoS One 5:e12019

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Twiss SD, Franklin J (2010) Individually consistent behavioural patterns in wild, breeding male grey seals (Halichoerus grypus). Aquat Mamm 36:234–238

    Article  Google Scholar 

  • Twiss SD, Cairns C, Culloch RM, Richards SA, Pomeroy PP (2012) Variation in female grey seal (Halichoerus grypus) reproductive performance correlates to proactive-reactive behavioural types. PLoS One 7:e49598

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de Villemereuil P, Gimenez O, Doligez B (2013) Comparing parent-offspring regression with frequentist and Bayesian animal models to estimate heritability in wild populations: a simulation study for Gaussian and binary traits. Methods Ecol Evol 4:260–275

    Article  Google Scholar 

  • Weitzman J, den Heyer C, Bowen WD (2016) Factors influencing and consequences of breeding dispersal and habitat choice in female grey seals (Halichoerus grypus) on Sable Island, Nova Scotia. Oecologia 183:367

    Article  PubMed  Google Scholar 

  • Wilson ADM, Krause J (2012) Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav Ecol 23:1316–1323

    Article  Google Scholar 

  • Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461

    Article  PubMed  Google Scholar 

  • Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584

    Article  PubMed  CAS  Google Scholar 

  • Worthy GAJ, Lavigne DM (1987) Mass loss, metabolic rate, and energy utilization by harp and grey seal during the postweaning fast. Physiol Zool 60:352–364

    Article  Google Scholar 

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Acknowledgments

We thank C. Abraham, S. Armsworthy, D. Austin, J. Badger, L. Baker, C. Beck, D. Boness, W. Blanchard, G. Breed, S. Budge, M. Cooper, B. Farmer, M. Hammill, S. Heaslip, S. Insley, W. Joyce, H. Koopman, E. Leadon, P. LeBlanc, R. Lewis, S. McCullough, C. McEwan, J. McMillan, B. Nowak, P. O’Laughlin, D. Parker, L. Rea, R. Ronconi, H. Smith, S. Smith, T. Schulz, J. Tremblay, K. Trzcinski, S. Tucker, D. Tully, P. Varkey, K. Whoriskey, M. Wilson, and S. Wong for assistance with the field work. We are also grateful for infrastructure support provided on Sable Island by Environment Canada and Parks Canada. We thank the reviewers for their insightful comments, which helped to improve our manuscript.

Funding

This work was supported by the Department of Fisheries and Oceans, Canada, a Research Network Grant (NETGP 375118-08), Discovery Grants to WDB (grant number 36762-2012), and to DWC (grant number 146522) from the Natural Sciences and Engineering Research Council of Canada. CMB has been funded by scholarship from Alberta Innovates Technology Futures.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada

    Christine M. Bubac & David W. Coltman

  2. Population Ecology Division, Bedford Institute of Oceanography, Dartmouth, Nova Scotia, Canada

    W. Don Bowen, Shelley L. C. Lang & Cornelia E. den Heyer

  3. Biology Department, Dalhousie University, Halifax, Nova Scotia, Canada

    W. Don Bowen & Damian C. Lidgard

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  1. Christine M. Bubac
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  2. David W. Coltman
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  3. W. Don Bowen
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  4. Damian C. Lidgard
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  5. Shelley L. C. Lang
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  6. Cornelia E. den Heyer
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Correspondence to Christine M. Bubac.

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The authors declare that they have no conflict of interest.

Animal welfare and ethical approval

All procedures on gray seals used in this study complied with the guidelines for animal use as provided by the Canadian Council on Animal Care, and were approved by the Animal Care Committees of the University of Alberta and the Department of Fisheries and Oceans, Canada.

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Communicated by L. Rendell

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Bubac, C.M., Coltman, D.W., Don Bowen, W. et al. Repeatability and reproductive consequences of boldness in female gray seals. Behav Ecol Sociobiol 72, 100 (2018). https://doi.org/10.1007/s00265-018-2515-5

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