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Behavioral Ecology and Sociobiology

, Volume 66, Issue 4, pp 547–559 | Cite as

The role of ecological context and predation risk-stimuli in revealing the true picture about the genetic basis of boldness evolution in fish

  • Thomas Klefoth
  • Christian Skov
  • Jens Krause
  • Robert Arlinghaus
Original Paper

Abstract

To showcase the importance of genotype × environment interactions and the presence of predation risk in the experimental assessment of boldness in fish, we investigated boldness in terms of feeding behavior and refuge use in two genetically different populations of juvenile carp (Cyprinus carpio) in two replicated experimental conditions in ponds and laboratory tanks. The populations were expected to exhibit genetic differences in boldness due to differential evolutionary adaptation to low-predation-risk pond aquaculture conditions. Boldness was measured in variants of open-field trials with and without implementation of additional predation risk-stimuli by angling on feeding spots. Without explicit implementation of risk, genotypes adapted to low-risk environments, i.e., domesticated mirror carp behaved consistently bolder than their less domesticated scaled conspecifics in the pond environment, but not in the laboratory environment. When we implemented artificial risk-stimuli by angling on previously safe feeding spots, boldness differences among genotypes also emerged in the laboratory environment, indicating strong genotype × environment effects on boldness behavior of carp. The expected genetic basis of boldness differences among genotypes was clearly supported in the pond environment, while the laboratory study revealed these patterns only under inclusion of explicit risk-stimuli. Our study thus underscores that boldness may involve both a basal component that is expressed independently of obvious predation risk (e.g., in open fields) and a component revealed in relation to explicit predation risk, and both dimensions may respond differently in behavioral tests.

Keywords

Genotype × environment interactions Cyprinus carpio Predation risk Common garden Angling 

Notes

Acknowledgements

We would like to thank Thilo Pagel and Tobias Rapp for their help during data collection; Jörn Gessner for providing laboratory and pond facilities; Georg Staaks, Klaus Kohlmann, Christian Wolter, Silva Uusi-Heikkila, Fiona Johnston, and Ashley Ward for the fruitful discussion; and the two anonymous reviewers for the very helpful comments on a former version of this manuscript. Funding was provided by the Deutsche Bundesstiftung Umwelt (DBU, No AZ 20007/924) through a scholarship to TK and through the project Adaptfish by the Gottfried-Wilhelm-Leibniz-Community to RA (www.adaptfish.igb-berlin.de) and the German Ministry for Education and Research for the project Besatzfisch to RA (www.besatz-fisch.de). Our study benefited from the input provided by Thomas Mehner and the participants of the workshop “Scientific Writing” held at IGB.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical note

Animal handling associated with this study was approved through an animal care permit (No G 0178/09) granted by the State Office of Health and Social Affairs in Berlin in accordance with the German Animal Protection Act.

References

  1. Alados CL, Escos JM, Emlen JM (1996) Fractal structure of sequential behaviour patterns: an indicator of stress. Anim Behav 51:437–443CrossRefGoogle Scholar
  2. Allouche S, Gaudin P (2001) Effects of avian predation threat, water flow and cover on growth and habitat use by chub, Leuciscus cephalus, in an experimental stream. Oikos 94:481–492CrossRefGoogle Scholar
  3. Archard GA, Braithwaite VA (2011) Increased exposure to predators increases both exploration and activity level in Brachyrhaphis episcope. J Fish Biol 78:593–601PubMedCrossRefGoogle Scholar
  4. Balon EK (1995) Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquaculture 129:3–48CrossRefGoogle Scholar
  5. Balon EK (2004) About the oldest domesticates among fishes. J Fish Biol 65:1–27CrossRefGoogle Scholar
  6. Barthel BL, Cooke SJ, Suski CD, Philipp DP (2003) Effects of landing net mesh type on injury and mortality in a freshwater recreational fishery. Fish Res 63:275–282CrossRefGoogle Scholar
  7. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473PubMedCrossRefGoogle Scholar
  8. Bell AM, Stamps JA (2004) Development of behavioural differences between individuals and populations of sticklebacks, Gasterosteus aculeatus. Anim Behav 68:1339–1348CrossRefGoogle Scholar
  9. Berejikian BA (1995) The effects of hatchery and wild ancestry and experience on the relative ability of steelhead trout fry (Oncorhynchus mykiss) to avoid a benthic predator. Can J Fish Aquat Sci 52:2476–2482CrossRefGoogle Scholar
  10. Beukema JJ (1969) Angling experiments with carp (Cyprinus carpio L.) I. Differences between wild, domesticated and hybrid strains. Neth J Zool 19:596–609CrossRefGoogle Scholar
  11. Brown C, Jones F, Braithwaite VA (2005) In situ examination of boldness—shyness traits in the tropical poeciliid, Brachyraphis episcopi. Anim Behav 70:1003–1009CrossRefGoogle Scholar
  12. Brown C, Burgess F, Braithwaite VA (2007) Heritable and experiential effects on boldness in a tropical poeciliid. Behav Ecol Sociobiol 62:237–243CrossRefGoogle Scholar
  13. Brydges NM, Colegrave N, Heathcote RJP, Braithwaite VA (2008) Habitat stability and predation pressure affect temperament behaviours in populations of three-spined sticklebacks. J Anim Ecol 77:229–235PubMedCrossRefGoogle Scholar
  14. Budaev SV (1997) Alternative styles in the European wrasse, Symphodus ocellatus: boldness-related schooling tendency. Environ Biol Fish 49:71–78CrossRefGoogle Scholar
  15. Budaev SV, Zworykin DD, Mochek AD (1999) Consistency of individual differences in behaviour of the lion-headed cichlid, Steatocranus casuarius. Behav Process 48:49–55CrossRefGoogle Scholar
  16. Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator–prey systems: a review and prospectus. Ecoscience 5:338–352Google Scholar
  17. Conover DO (1998) Local adaptation in marine fishes: evidence and implications for stock enhancement. Am Nat 62:477–493Google Scholar
  18. Conrad JL, Sih A (2009) Behavioural type in newly emerged steelhead Oncorhynchus mykiss does not predict growth rate in a conventional hatchery rearing environment. J Fish Biol 75:1410–1426PubMedCrossRefGoogle Scholar
  19. Conrad JL, Weinersmith KL, Brodin T, Saltz JB, Sih A (2011) Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. J Fish Biol 78:395–435PubMedCrossRefGoogle Scholar
  20. Cousyn C, De Meester L, Colbourne JK, Brendonck L, Verschuren D, Volckaert F (2001) Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proc Natl Acad Sci USA 98:6256–6260PubMedCrossRefGoogle Scholar
  21. R Development Core Team (2009) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria 1:ISBN 3-900051-07-0Google Scholar
  22. Dingemanse NJ, Kazem AJN, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89PubMedCrossRefGoogle Scholar
  23. Gerlai R, Csányi V (1990) Genotype-environment interaction and the correlation structure of behavioral elements in paradise fish (Macropodus opercularis). Physiol Behav 47:343–356PubMedCrossRefGoogle Scholar
  24. Ghalambor CK, Reznick DN, Walker JA (2004) Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the trinidadian guppy (Poecilia reticulata). Am Nat 164:38–50PubMedCrossRefGoogle Scholar
  25. Girvan JR, Braithwaite VA (1998) Population differences in spatial learning in three-spined sticklebacks. Proc R Soc Lond B 265:913–918CrossRefGoogle Scholar
  26. Gotthard K, Nylin S, Wiklund C (1994) Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99:281–289CrossRefGoogle Scholar
  27. Herczeg G, Gonda A, Merilä J (2009) Predation mediated population divergence in complex behaviour of nine-spined stickleback (Pungitius pungitius). J Evol Biol 22:544–552PubMedCrossRefGoogle Scholar
  28. Huntingford FA (2004) Implications of domestication and rearing conditions for the behaviour of cultivated fishes. J Fish Biol 65:122–142CrossRefGoogle Scholar
  29. Huntingford FA, Adams C (2005) Behavioural syndromes in farmed fish: implications for production and welfare. Behaviour 142:1207–1221CrossRefGoogle Scholar
  30. Huntingford FA, Wright PJ (1992) Inherited population differences in avoidance conditioning in three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 122:264–273CrossRefGoogle Scholar
  31. Johnsson JI (1993) Big and brave: size selection affects foraging under risk of predation in juvenile rainbow trout, Oncorhynchus mykiss. Anim Behav 45:1219–1225CrossRefGoogle Scholar
  32. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  33. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  34. Kirpichnikov VS, Billard R (1999) Genetics and breeding of common carp. INRA, ParisGoogle Scholar
  35. Klefoth T, Kobler A, Arlinghaus R (2008) The impact of catch-and-release angling on short-term behaviour and habitat choice of northern pike (Esox lucius L.). Hydrobiologia 601:99–110CrossRefGoogle Scholar
  36. Klefoth T, Kobler A, Arlinghaus R (2011) Behavioural and fitness consequences of direct and indirect non-lethal disturbances in a catch-and-release northern pike (Esox lucius) fishery. Knowl Managt Aquatic Ecosyst 403: doi: 10.1051/kmae/2011072
  37. Lewin WC, Okun N, Mehner T (2004) Determinants of the distribution of juvenile fish in the littoral area of a shallow lake. Freshw Biol 49:410–424CrossRefGoogle Scholar
  38. Magnhagen C (2006) Risk-taking behaviour in foraging young-of-the-year perch varies with population size structure. Oecologia 147:734–743PubMedCrossRefGoogle Scholar
  39. Magurran AE, Seghers BH, Carvalho GR, Shaw PW (1992) Behavioural consequences of an artificial introduction of guppies (Poecilia reticulata) in Trinidad: evidence for the evolution of anti-predator behaviour in the wild. Proc R Soc Lond B 248:117–122CrossRefGoogle Scholar
  40. Matsuzaki SS, Mabuchi K, Takamura N, Nishida M, Washitani I (2009) Behavioural and morphological differences between feral and domesticated strains of common carp Cyprinus carpio. J Fish Biol 75:1206–1220PubMedCrossRefGoogle Scholar
  41. Nuismer SL, Gandon S (2008) Moving beyond common-garden and transplant designs: insights into causes of local adaptation in species interactions. Am Nat 171:658–668PubMedCrossRefGoogle Scholar
  42. O'Steen S, Cullum AJ, Bennett AF (2002) Rapid evolution of escape ability in Trinidadian guppies (Poecilia reticulata). Evolution 56:776–784PubMedGoogle Scholar
  43. Probst E (1953) Die Beschuppung des Karpfens. Münchener Beiträge zur Abwasser-, Fischerei- und Flussbiologie 1:150–227Google Scholar
  44. Raat AJP (1985) Analysis of angling vulnerability of common carp, Cyprinus carpio L., in catch-and-release angling in ponds. Aquac Fish Manag 16:171–187Google Scholar
  45. Rapp T, Cooke SJ, Arlinghaus R (2008) Exploitation of specialised fisheries resources: the importance of hook size in recreational angling for large common carp (Cyprinus carpio L.). Fish Res 94:79–83CrossRefGoogle Scholar
  46. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318PubMedCrossRefGoogle Scholar
  47. Reznick DA, Bryga H, Endler JA (1990) Experimentally induced life-history evolution in a natural population. Nature 346:357–359CrossRefGoogle Scholar
  48. Sæther BE (1988) Pattern of covariation between life-history traits of European birds. Nature 331:616–617PubMedCrossRefGoogle Scholar
  49. Seghers BH (1974) Schooling behavior in the guppy (Poecilia reticulata): an evolutionary response to predation. Evolution 28:486–489CrossRefGoogle Scholar
  50. Skov C, Brodersen J, Bronmark C, Hansson L, Hertonsson P, Nilsson PA (2005) Evaluation of PIT-tagging in cyprinids. J Fish Biol 67:1195–1201CrossRefGoogle Scholar
  51. Sneddon LU (2003) The bold and the shy: individual differences in rainbow trout. J Fish Biol 62:971–975CrossRefGoogle Scholar
  52. Stamps JA, Groothuis TGG (2010) Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Phil Trans R Soc B 365:4029–4041PubMedCrossRefGoogle Scholar
  53. Steffens W (1980) Der Karpfen, Cyprinus carpio: Neue Brehm Bücherei, 5th edn. A. Ziemsen Verlag, Wittenberg LutherstadtGoogle Scholar
  54. Stoks R, McPeek MA, Mitchell JL (2003) Evolution of prey behavior in response to changes in predation regime: damselflies in fish and dragonfly lakes. Evolution 57:574–585PubMedGoogle Scholar
  55. Sundström LF, Petersson E, Höjesjö J, Johnsson JI, Järvi T (2004) Hatchery selection promotes boldness in newly hatched brown trout (Salmo trutta): implications for dominance. Behav Ecol 15:192–198CrossRefGoogle Scholar
  56. Toms CN, Echevarria DJ, Jouandot DJ (2010) A methodological review of personality-related studies in fish: focus on the shy-bold axis of behaviour. Int J Comp Psychol 23:1–25Google Scholar
  57. van de Pol M, Wright J (2009) A simple method for distinguishing within-versus between-subject effects using mixed models. Anim Behav 77:753–758CrossRefGoogle Scholar
  58. Walling CA, Dawnay N, Kazem AJN, Wright J (2004) Predator inspection behaviour in three-spined sticklebacks (Gasterosteus aculeatus): body size, local predation pressure and cooperation. Behav Ecol Sociobiol 56:164–170CrossRefGoogle Scholar
  59. Wilson ADM, Godin JGJ (2009) Boldness and behavioral syndromes in the bluegill sunfish, Lepomis macrochirus. Behav Ecol 20:231–237CrossRefGoogle Scholar
  60. Wilson ADM, McLaughlin RL (2007) Behavioural syndromes in brook charr, Salvelinus fontinalis: prey-search in the field corresponds with space use in novel laboratory situations. Anim Behav 74:689–698CrossRefGoogle Scholar
  61. Wilson ADM, Stevens ED (2005) Consistency in context-specific measures of shyness and boldness in rainbow trout, Oncorhynchus mykiss. Ethol 111:849–862CrossRefGoogle Scholar
  62. Wisenden BD (2000) Olfactory assessment of predation risk in the aquatic environment. Phil Trans R Soc B 355:1205–1208PubMedCrossRefGoogle Scholar
  63. Zydlewski GB, Haro A, Whalen KG, McCormick SD (2001) Performance of stationary and portable passive transponder detection systems for monitoring of fish movements. J Fish Biol 58:1471–1475CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Thomas Klefoth
    • 1
  • Christian Skov
    • 2
  • Jens Krause
    • 1
    • 3
  • Robert Arlinghaus
    • 1
    • 3
  1. 1.Department of Biology and Ecology of FishesLeibniz-Institute of Freshwater Ecology and Inland FisheriesBerlinGermany
  2. 2.National Institute of Aquatic Resources (DTU-Aqua)Technical University of DenmarkSilkeborgDenmark
  3. 3.Department for Crop and Animal Sciences, Faculty of Agriculture and HorticultureHumboldt-Universität zu BerlinBerlinGermany

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