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Survival costs of fast exploration during juvenile life in a small mammal

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Abstract

Animal personality is considered to be subject to natural selection, and measuring its fitness consequences is an important step in the study of the evolution of this phenomenon. The evolutionary costs and benefits of certain personality traits are frequently assumed to fluctuate across different life history stages. However, little is still known about survival consequences of personality during juvenile life. We predicted survival costs of exploration tendency in juvenile European rabbits (Oryctolagus cuniculus), which we studied under quasi-natural conditions. In addition, consistencies between exploration and the animal’s behavioral responses in other contexts were tested. Early exploratory behavior was assessed in two annual cohorts, either observationally by quantifying the time course of exploring the area around the nursery burrow shortly after emergence above ground or experimentally by conducting open-field tests shortly before emergence. In both years, the study revealed consistent results: more exploratory individuals had a lower chance of survival until the end of the vegetation period, presumably due to a higher predation risk. Fast explorers, as assessed by their exploration of the burrow environment, were also less sociable and tended to be more aggressive toward conspecifics as subadults. Sociability was repeatable across time. Furthermore, fast explorers, as assessed by their open-field behavior, were bolder in a handling test before emergence. These consistencies across context and time suggest the existence of personality. In conclusion, the results provide evidence for survival costs of fast exploration during juvenile life. The findings are in line with predictions on personality-related life history variation.

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References

  • Adriaenssens B, Johnsson JI (2013) Natural selection, plasticity and the emergence of a behavioural syndrome in the wild. Ecol Lett 16:47–55

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-7. http://CRAN.R-project.org/package=lme4

  • Bergeron P, Montiglio PO, Réale D, Humphries MM, Gimenez O, Garant D (2013) Disruptive viability selection on adult exploratory behaviour in eastern chipmunks. J Evol Biol 26:766–774

    Article  CAS  PubMed  Google Scholar 

  • Bergmüller R (2010) Animal personalities and behavioural syndromes. In: Kappeler P (ed) Animal behaviour: evolution and mechanisms. Springer, Heidelberg, pp 587–621

    Chapter  Google Scholar 

  • Bergmüller R, Taborsky M (2007) Adaptive behavioural syndromes due to strategic niche specialization. BMC Ecol 7:12

    Article  PubMed Central  PubMed  Google Scholar 

  • Biro PA (2012) Do rapid assays predict repeatability in labile (behavioural) traits? Anim Behav 83:1295–1300

    Article  Google Scholar 

  • Boon AK, Réale D, Boutin S (2007) The interaction between personality, offspring fitness and food abundance in North American red squirrels. Ecol Lett 10:1094–1104

    Article  PubMed  Google Scholar 

  • Both C, Dingemanse N, Drent PJ, Tinbergen JM (2005) Pairs of extreme avian personalities have highest reproductive success. J Anim Ecol 74:667–674

    Article  Google Scholar 

  • Bremner-Harrison S, Prodohl PA, Elwood RW (2004) Behavioural trait assessment as a release criterion: boldness predicts early death in a reintroduction programme of captive-bred swift fox (Vulpes velox). Anim Conserv 7:313–320

    Article  Google Scholar 

  • Briffa M, Weiss AA (2010) Animal personality. Curr Biol 20:R912

    Article  CAS  PubMed  Google Scholar 

  • Broekhuizen S, Bouman E, Went W (1986) Variations in time of nursing in the brown hare (Lepus europaeus) and the European rabbit (Oryctolagus cuniculus). Mamm Rev 16:139–144

    Article  Google Scholar 

  • Charnov EL (1986) Life-history evolution in a ‘recruitment population’: why are adult mortality rates constant? Oikos 47:129–134

    Article  Google Scholar 

  • Cote J, Clobert J (2007) Social personalities influence natal dispersal in a lizard. Proc R Soc Lond B 274:383–390

    Article  CAS  Google Scholar 

  • Cote J, Dreiss A, Clobert J (2008) Social personality trait and fitness. Proc R Soc Lond B 275:2851–2858

    Article  CAS  Google Scholar 

  • Coureaud G, Fortun-Lamothe L, Rödel HG, Monclús R, Schaal B (2008) Development of social and feeding behaviour in young rabbits. In: Xiccato G, Trocino A, Lukefahr SD (eds) Proceedings of the 9th World Rabbit Congress. FIZZ, Brescia, Italy, pp 1131–1146

    Google Scholar 

  • Cowan DP (1987a) Patterns of mortality in a free-living rabbit (Oryctolagus cuniculus) population. Symp Zool Soc Lond 58:59–77

    Google Scholar 

  • Cowan DP (1987b) Aspects of the social organization of the European wild rabbit (Oryctolagus cuniculus). Ethology 75:197–210

    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 

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

    Article  Google Scholar 

  • Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc Lond B 271:847–852

    Article  Google Scholar 

  • Dingemanse NJ, Dochtermann NA, Nakagawa S (2012) Defining behavioural syndromes and the role of ‘syndrome deviation’ in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548

    Article  Google Scholar 

  • Eccard JA, Rödel HG (2011) Optimizing temperament through litter size in short-lived, iteroparous mammals in seasonal environments. Dev Psychobiol 53:585–591

    Article  PubMed  Google Scholar 

  • Edgington ES, Onghena P (2007) Randomization Tests. CRC Press, Taylor & Francis Group, Boca Raton

    Google Scholar 

  • Ellis L (1995) Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol 16:257–333

    Article  Google Scholar 

  • Faraway JJ (2005) Linear models with R. Chapman & Hall, Boca Raton

    Google Scholar 

  • Gramsbergen A, Westerga J (1992) Locomotor development in undernourished rats. Behav Brain Res 48:57–64

    Article  CAS  PubMed  Google Scholar 

  • Greenwood PJ (1980) Mating systems, philopatry, and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google Scholar 

  • Guenther A, Finkemeier MA, Trillmich F (2014) The ontogeny of personality in the wild guinea pig. Anim Behav 90:131–139

    Article  Google Scholar 

  • Hamilton WD (1971) The geometry of the selfish herd. J Theor Biol 31:295–311

    Article  CAS  PubMed  Google Scholar 

  • Hennessy MB (1997) Hypothalamic-pituitary-adrenal responses to brief social separation. Neurosci Biobehav Rev 21:11–29

    Article  CAS  PubMed  Google Scholar 

  • Hudson R, Trillmich F (2008) Sibling competition and cooperation in mammals: challenges, developments and prospects. Behav Ecol Sociobiol 62:299–307

    Article  Google Scholar 

  • Hudson R, Bilkó Á, Altbäcker V (1996) Nursing, weaning and the development of independent feeding in the rabbit (Oryctolagus cuniculus). Z Säugetierkd 61:39–48

    Google Scholar 

  • Kenward RE (2001) A manual for wildlife radio tagging. Academic Press, London

    Google Scholar 

  • Kight CR, David M, Dall SRX (2013) The evolution of animal personality variation. In: Kehrer-Sawatzki H (ed) Encyclopedia of Life Sciences (eLS). Wiley online citable reviews. http://www.els.net/WileyCDA/

  • Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935

    Article  CAS  PubMed  Google Scholar 

  • Krause J, Ruxton GD (2002) Living in groups. Oxford Univ. Press, Oxford

    Google Scholar 

  • Künkele J (1992) Infanticide in wild rabbits (Oryctolagus cuniculus). J Mammal 73:317–320

    Article  Google Scholar 

  • Künkele J, von Holst D (1996) Natal dispersal in the European wild rabbit. Anim Behav 51:1047–1059

    Article  Google Scholar 

  • Le Galliard JF, Paquet M, Cisel M, Montes-Poloni L (2013) Personality and the pace-of-life syndrome: variation and selection on exploration, metabolism and locomotor performances. Funct Ecol 27:136–144

    Article  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Article  Google Scholar 

  • Magee L (1990) R 2 measures based on Wald and likelihood ratio joint significance tests. Am Stat 44:250–253

    Google Scholar 

  • Meijsser FM, Kersten AMP, Wiepkema PR, Metz JHM (1989) An analysis of the open-field performance of sub-adult rabbits. Appl Anim Behav Sci 24:147–155

    Article  Google Scholar 

  • Mendl M (1988) The effects of litter size variation on mother-offspring relationships and behavioural and physical development in several mammalian species (principally rodents). J Zool 215:15–34

    Article  Google Scholar 

  • Metzgar LH (1967) An experimental comparison of screech owl predation on resident and transient white fooded mice (Peromyscus leucopus). J Mammal 48:387–391

    Article  Google Scholar 

  • Møller AP, Saino N (2004) Immune response and survival. Oikos 104:299–304

    Article  Google Scholar 

  • Monclús R, Rödel HG (2008) Different forms of vigilance in response to the presence of predators and conspecifics in a group-living mammal, the European rabbit. Ethology 114:287–297

    Article  Google Scholar 

  • Monclús R, Tiulim J, Blumstein DT (2011) Older mothers follow conservative strategies under predator pressure: the adaptive role of maternal glucocorticoids in yellow-bellied marmots. Horm Behav 60:660–665

    Article  PubMed  Google Scholar 

  • Muciño E, Bautista A, Jímenez I, Martínez-Gómez M, Hudson RJ (2009) Differential development of body equilibrium among littermates in the newborn rabbit. Dev Psychobiol 51:24–33

    Article  PubMed  Google Scholar 

  • Murray DL (2002) Differential body condition and vulnerability to predation in snowshoe hares. J Anim Ecol 71:614–625

    Article  Google Scholar 

  • Nagelkerke NJD (1991) A note on a general definition of the coefficient of determination. Biometrika 78:691–692

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Nettle D (2006) The evolution of personality variation in humans and other animals. Am Psychol 61:622–631

    Article  PubMed  Google Scholar 

  • Niemelä PT, Dingemanse NJ (2014) Artificial environments and the study of ‘adaptive’ personalities. Trends Ecol Evol 29:245–247

    Article  PubMed  Google Scholar 

  • Oli MK, Dobson FS (2003) The relative importance of life-history variables to population growth rate in mammals: Cole’s prediction revisited. Am Nat 161:422–440

    Article  PubMed  Google Scholar 

  • Palomares F (2001) Comparison of 3 methods to estimate rabbit abundance in a Mediterranean environment. Wildlife Soc B 29:578–585

    Google Scholar 

  • Petrovan SO, Barrio IC, Ward AI, Wheeler PM (2011) Farming for pests? Local and landscape-scale effects of grassland management on rabbit densities. Eur J Wildlife Res 57:27–34

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, Berlin

    Book  Google Scholar 

  • Prager G, Stefanski V, Hudson R, Rödel HG (2010) Family matters: maternal and litter-size effects on immune parameters in young laboratory rats. Brain Behav Immun 24:1371–1378

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing. www.R-project.org, Vienna, Austria

  • Réale D (2007) What do we really know about selection on personality? Eur J Personality 21:618–620

    Google Scholar 

  • Réale D, Festa-Bianchet M (2003) Predator-induced natural selection on temperament in bighorn ewes. Anim Behav 65:463–470

    Article  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 

  • Réale D, Martin J, Coltman DW, Poissant J, Festa-Bianchet M (2009) Male personality, life-history strategies and reproductive success in a promiscuous mammal. J Evol Biol 22:1599–1607

    Article  PubMed  Google Scholar 

  • Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio PO (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc B 365:4051–4063

  • Reddiex B, Hickling GJ, Norbury GL, Frampton CM (2002) Effects of predation and rabbit haemorrhagic disease on population dynamics of rabbits (Oryctolagus cuniculus) in North Canterbury, New Zealand. Wildl Res 29:627–633

    Article  Google Scholar 

  • Richardson B, Wood DH (1982) Experimental ecological studies on a subalpine rabbit population. I. Mortality factors acting on emergent kittens. Aust Wildlife Res 9:443–450

  • Rödel HG, Meyer S (2011) Early development influences ontogeny of personality types in young laboratory rats. Dev Psychobiol 53:601–613

    Article  PubMed  Google Scholar 

  • Rödel HG, Monclús R (2011) Long-term consequences of early development on personality traits: a study in European rabbits. Behav Ecol 22:1123–1130

    Article  Google Scholar 

  • Rödel HG, Bora A, Kaetzke P, Khaschei M, Hutzelmeyer H, von Holst D (2004) Over-winter survival in subadult European rabbits: weather effects, density dependence, and the impact of individual characteristics. Oecologia 140:566–576

    Article  PubMed  Google Scholar 

  • Rödel HG, Prager G, Stefanski V, von Holst D, Hudson R (2008a) Separating maternal and litter-size effects on early postnatal growth in two species of altricial small mammals. Physiol Behav 93:826–834

    Article  PubMed  Google Scholar 

  • Rödel HG, Starkloff A, Bautista A, Friedrich AC, von Holst D (2008b) Infanticide and maternal offspring defence in European rabbits under natural breeding conditions. Ethology 114:22–31

    Article  Google Scholar 

  • Rödel HG, Starkloff A, Bruchner B, von Holst D (2008c) Social environment and reproduction in female European rabbits (Oryctolagus cuniculus): benefits of the presence of litter sisters. J Comp Psychol 122:73–83

    Article  PubMed  Google Scholar 

  • Rödel HG, von Holst D, Kraus C (2009) Family legacies: short- and long-term fitness consequences of early-life conditions in female European rabbits. J Anim Ecol 78:789–797

    Article  PubMed  Google Scholar 

  • Rödel HG, Dausmann KH, Starkloff A, Schubert M, von Holst D, Hudson R (2012) Diurnal nursing pattern of wild-type European rabbits under natural breeding conditions. Mamm Biol 77:441–446

    Google Scholar 

  • Rosvall KA (2008) Sexual selection on aggressiveness in females: evidence from an experimental test with tree swallows. Anim Behav 75:1603–1610

    Article  Google Scholar 

  • Schradin C, Anzenberger G (2003) Mothers, not fathers, determine the delayed onset of male carrying in Goeldi’s monkey (Callimico goeldii). J Hum Evol 45:389–399

    Article  PubMed  Google Scholar 

  • Schuett W, Dall SRX, Royle NJ (2011) Pairs of zebra finches with similar ‘personalities’ make better parents. Anim Behav 81:609–618

    Article  Google Scholar 

  • Seltmann MW, Ruf T, Rödel HG (2009) Effects of body mass and huddling on resting metabolic rates of post-weaned European rabbits under different simulated weather conditions. Funct Ecol 23:1070–1080

    Article  Google Scholar 

  • Sibly RM, Collett D, Promislow DEL, Peacock DJ, Harvey PH (2009) Mortality rates of mammals. J Zool 243:1–12

    Article  Google Scholar 

  • Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  PubMed  Google Scholar 

  • Sinn DL, Apiolaza LA, Moltschaniwskyj NA (2006) Heritability and fitness-related consequences of squid personality traits. J Exp Biol 9:1437–1447

    Google Scholar 

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

    Article  Google Scholar 

  • Stamps J, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325

    Article  PubMed  Google Scholar 

  • Surridge AK, Bell DJ, Ibrahim KM, Hewitt GM (1999) Population structure and genetic variation of European wild rabbits (Oryctolagus cuniculus) in East Anglia. Heredity 82:479–487

    Article  PubMed  Google Scholar 

  • Tablado Z, Revilla E, Palomares F (2009) Breeding like rabbits: Global patterns of variability and determinants of European wild rabbit reproduction. Ecography 32:310–320

    Article  Google Scholar 

  • Verbeek MEM, Boon A, Drent PJ (1996) Exploration, aggressive behaviour and dominance in pair-wise confrontations of juvenile male great tits. Behaviour 133:945–963

    Article  Google Scholar 

  • von Holst D (2001) Social stress in wild mammals in their natural habitat. In: Broom DM (ed) Coping with challenge: welfare in animals including humans. Dahlem University Press, Berlin, pp 317–335

    Google Scholar 

  • von Holst D, Hutzelmeyer H, Kaetzke P, Khaschei M, Rödel HG, Schrutka H (2002) Social rank, fecundity and lifetime reproductive success in wild European rabbits (Oryctolagus cuniculus). Behav Ecol Sociobiol 51:245–254

    Article  Google Scholar 

  • Wallage-Drees JM (1989) A field study on seasonal changes in the circadian activity of rabbits. Z Säugetierkd 54:22–30

    Google Scholar 

  • Wilson ADM, Godin J-GJ (2009) Boldness and behavioral syndromes in the bluegill sunfish, Lepomis macrochirus. Behav Ecol 20:231–237

    Article  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  CAS  PubMed  Google Scholar 

  • Yoder JM, Marschall EA, Swanson DA (2004) The costs of dispersal: predation as a function of movement and site familiarity in ruffed grouse. Behav Ecol 15:469–476

    Article  Google Scholar 

  • Zarrow MX, Denenberg VH, Anderson CO (1965) Rabbit: frequency of suckling in the pup. Science 159:1835–1836

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

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Acknowledgments

We are grateful to Dietrich von Holst for his support and helpful discussions and to Tanja Dycta, Dominika Zielińska and Anett Starkloff for their help with the data collection. We also thank Niels Dingemanse, Pierre-Olivier Montiglio, and Isabella Clegg for their constructive comments. The study was partly supported by the German Research Foundation (RO2431/2-1).

Ethical standards

The studies, which were carried out in Germany, were conducted in accordance with the German law on animal welfare and the institutional guidelines of animal care and were approved by the institutional animal welfare officer of the University of Bayreuth. Permission for the studies on European rabbits was granted by the Government of Middle Franconia, Germany (211-3894a).

Conflicts of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Laboratoire d’Ethologie Expérimentale et Comparée E.A. 4443 (LEEC), Université Paris 13, Sorbonne Paris Cité, 93430, Villetaneuse, France

    Heiko G. Rödel

  2. Department of Animal Physiology, University of Bayreuth, Bayreuth, Germany

    Manuela Zapka, Stefan Talke, Tina Kornatz, Barbara Bruchner & Christine Hedler

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  1. Heiko G. Rödel
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  2. Manuela Zapka
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  3. Stefan Talke
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  4. Tina Kornatz
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  6. Christine Hedler
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Correspondence to Heiko G. Rödel.

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Communicated by N. Dingemanse

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Rödel, H.G., Zapka, M., Talke, S. et al. Survival costs of fast exploration during juvenile life in a small mammal. Behav Ecol Sociobiol 69, 205–217 (2015). https://doi.org/10.1007/s00265-014-1833-5

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