Behavioral Ecology and Sociobiology

, Volume 67, Issue 5, pp 765–774 | Cite as

Behavioral type–environment correlations in the field: a study of three-spined stickleback

Original Paper

Abstract

Behavioral type–environment correlations occur when specific behavioral types of individuals are more common in certain environments. Behavioral type–environment correlations can be generated by several different mechanisms that are probably very common such as niche construction and phenotypic plasticity. Moreover, behavioral type–environment correlations have important ecological and evolutionary implications. However, few studies have examined behavioral type–environment correlations in natural populations. In this study, we asked whether some behavioral types of three-spined stickleback were more likely to occur in certain social environments (alone or in a shoal with other stickleback) or in certain microhabitats in a river (in the open or under cover). We found that individuals that were in shoals with other stickleback at the time of collection from the field emerged from a refuge more quickly compared to individuals that were found alone. In addition, fish that were alone in an open microhabitat explored more of a pool compared to fish that were alone in cover, but this difference did not occur among fish that were in shoals at the time of collection. Subsequent analyses of gut contents suggested that differences in microhabitat use were consistent over time. Our study provides some of the first evidence for behavioral type–environment correlations in a natural population of non-human animals.

Keywords

Personality Social environment Habitat selection Niche Refuge Exploratory behavior 

Notes

Acknowledgments

We thank RJH Pearish for assistance in the field and J Tompkins for assistance in identifying invertebrates. River’s Bend Retreat generously provided access to the Navarro River. KL Laskowski reviewed an early version of this manuscript. Comments from NJ Dingemanse and two anonymous reviewers greatly improved this manuscript.

Ethical standards

All experiments comply with the current laws of the United States and were approved by the University of Illinois Institutional Animal Care and Use Committee (Protocol number 09024).

References

  1. Adriaenssens B, Johnsson JI (2011) Shy trout grow faster: exploring links between personality and fitness-related traits in the wild. Behav Ecol 22:135–143CrossRefGoogle Scholar
  2. Bakker TCM (1986) Aggressiveness in sticklebacks (Gasterosteus aculeatus L.): a behaviour–genetic study. Behaviour 98:1–144CrossRefGoogle Scholar
  3. Bateson P (1988) The active role of behaviour in evolution. In: Ho MW, Fox SW (eds) Evolutionary processes and metaphors. Wiley, New York, pp 191–207Google Scholar
  4. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783CrossRefGoogle Scholar
  5. Bell AM, Dingemanse NJ, Hankison SJ, Langenhof MBW, Rollins K (2011) Early exposure to nonlethal predation risk by size-selective predators increases somatic growth and decreases size at adulthood in threespined sticklebacks. J Evol Biol 24:943–953CrossRefPubMedGoogle Scholar
  6. Bentzen P, McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair. Can J Zool 62:2280–2286CrossRefGoogle Scholar
  7. Bergmüller R, Taborsky M (2010) Animal personality due to social niche specialisation. Trends Ecol Evol 25:504–511CrossRefPubMedGoogle Scholar
  8. Biro PA, Dingemanse NJ (2009) Sampling bias resulting from animal personality. Trends Ecol Evol 24:66–67CrossRefPubMedGoogle Scholar
  9. Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28CrossRefPubMedGoogle Scholar
  10. Bolnick DI, Caldera EJ, Matthews B (2008) Evidence for asymmetric migration load in a pair of ecologically divergent stickleback populations. Biol J Linn Soc 94:273–287CrossRefGoogle Scholar
  11. Boon AK, Réale D, Boutin S (2008) Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurus hudsonicus. Oikos 117:1321–1328CrossRefGoogle Scholar
  12. Brown CR, Brown MB (2000) Heritable basis for choice of group size in a colonial bird. Proc Natl Acad Sci U S A 97:14825–14830CrossRefPubMedGoogle Scholar
  13. Brown C, Jones F, Braithwaite V (2005) In situ examination of boldness-shyness traits in the tropical poeciliid, Brachyraphis episcopi. Anim Behav 70:1003–1009CrossRefGoogle 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. Chapman BB, Hulthén K, Blomqvist DR, Hansson LA, Nilsson JÅ, Brodersen J, Anders Nilsson P, Skov C, Brönmark C (2011) To boldly go: individual differences in boldness influence migratory tendency. Ecol Lett 14:871–876CrossRefPubMedGoogle Scholar
  16. Cote J, Clobert J (2007) Social personalities influence natal dispersal in a lizard. Proc R Soc Lond B 274:383–390CrossRefGoogle Scholar
  17. Cote J, Fogarty S, Weinersmith K, Brodin T, Sih A (2010) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc R Soc Lond B 277:1571–1579CrossRefGoogle Scholar
  18. Cote J, Fogarty S, Brodin T, Weinersmith K, Sih A (2011) Personality-dependent dispersal in the invasive mosquitofish: group composition matters. Proc R Soc Lond B 278:1670–1678CrossRefGoogle Scholar
  19. Day T, McPhail JD (1996) The effect of behavioural and morphological plasticity on foraging efficiency in the threespine stickleback (Gasterosteus sp.). Oecologia 108:380–388Google Scholar
  20. Dewitt TJ, Sih A, Hucko JA (1999) Trait compensation and cospecialization in a freshwater snail: size, shape and antipredator behaviour. Anim Behav 58:397–407CrossRefPubMedGoogle Scholar
  21. Dill LM (1987) Animal decision making and its ecological consequences: the future of aquatic ecology and behaviour. Can J Zool 65:803–811CrossRefGoogle Scholar
  22. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed- effect modelling approaches. J Anim Ecol 82:39–54CrossRefPubMedGoogle Scholar
  23. Dingemanse NJ, Both C, van Noordwijk AJ, Rutten AL, Drent PJ (2003) Natal dispersal and personalities in great tits (Parus major). Proc R Soc Lond B 270:741–747CrossRefGoogle Scholar
  24. Dingemanse NJ, Kazem AJN, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89CrossRefPubMedGoogle Scholar
  25. Donohue K, Polisetty CR, Wender NJ (2005) Genetic basis and consequences of niche construction: plasticity-induced genetic constraints on the evolution of seed dispersal in Arabidopsis thaliana. Am Nat 165:537–550CrossRefPubMedGoogle Scholar
  26. Duckworth RA, Badyaev AV (2007) Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci U S A 104:15017–15022CrossRefPubMedGoogle Scholar
  27. Edelaar P, Siepielski AM, Clobert J (2008) Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology. Evolution 62:2462–2472CrossRefPubMedGoogle Scholar
  28. Ehlinger TJ (1990) Habitat choice and phenotype-limited feeding efficiency in bluegill: individual differences and trophic polymorphism. Ecology 71:886–896CrossRefGoogle Scholar
  29. Fowler-Finn KD, Hebets EA (2011) The degree of response to increased predation risk corresponds to male secondary sexual traits. Behav Ecol 22:268–275CrossRefGoogle Scholar
  30. Godin J-GJ, Crossman SL (1994) Hunger-dependent predator inspection and foraging behaviours in the threespine stickleback (Gasterosteus aculeatus) under predation risk. Behav Ecol Sociobiol 34:359–366CrossRefGoogle Scholar
  31. Griffiths SW, Magurran AE (1999) Schooling decisions in guppies (Poecilia reticulata) are based on familiarity rather than kin recognition by phenotype matching. Behav Ecol Sociobiol 45:437–443CrossRefGoogle Scholar
  32. Hedrick AV (2000) Crickets with extravagant mating songs compensate for predation risk with extra caution. Proc R Soc Lond B 267:671–675CrossRefGoogle Scholar
  33. Hensley NM, Cook T, Lang M, Petelle MB, Blumstein DT (2012) Personality and habitat segregation in giant sea anemones (Condylactis gigantea). J Exp Mar Biol Ecol 426–427:1–4CrossRefGoogle Scholar
  34. Holt RD, Barfield M (2008) Habitat selection and niche conservatism. Isr J Ecol Evol 54:295–309CrossRefGoogle Scholar
  35. Jaenike J, Holt RD (1991) Genetic variation for habitat preference: evidence and explanations. Am Nat 137:s67–s90CrossRefGoogle Scholar
  36. Killen SS, Marras S, McKenzie DJ (2011) Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass. J Anim Ecol 80:1024–1033CrossRefPubMedGoogle Scholar
  37. Kobler A, Klefoth T, Mehner T, Arlinghaus R (2009) Coexistence of behavioural types in an aquatic top predator: a response to resource limitation? Oecologia 161:837–847CrossRefPubMedGoogle Scholar
  38. Krause J, Ruxton GD (2002) Living in groups. New York, OxfordGoogle Scholar
  39. Krause J, Loader SP, McDermott J, Ruxton GD (1998) Refuge use by fish as a function of body length-related metabolic expenditure and predation risks. Proc R Soc Lond B 265:2373–2379CrossRefGoogle Scholar
  40. Larson GL (1976) Social behavior and feeding ability of two phenotypes of Gasterosteus aculeatus in relation to their spatial and trophic segregation in a temperate lake. Can J Zool 54:107–121CrossRefGoogle Scholar
  41. Levene H (1953) Genetic equilibrium when more than one ecological niche is available. Am Nat 87:331–333CrossRefGoogle Scholar
  42. López P, Hawlena D, Polo V, Amo L, Martín J (2005) Sources of individual shy-bold variations in antipredator behaviour of male Iberian rock lizards. Anim Behav 69:1–9CrossRefGoogle Scholar
  43. Martin JGA, Réale D (2008) Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. Anim Behav 75:309–318CrossRefGoogle Scholar
  44. Martin JGA, Nussey DH, Wilson AJ, Réale D (2011) Measuring individual differences in reaction norms in field and experimental studies: a power analysis of random regression models. Methods Ecol Evol 2:362–374CrossRefGoogle Scholar
  45. McGlothlin JW, Moore AJ, Wolf JB, Brodie ED III (2010) Interacting phenotypes and the evolutionary process III. Social evolution. Evolution 64:2558–2574CrossRefPubMedGoogle Scholar
  46. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  47. Odling-Smee FJ, Laland KN, Feldman MW (1996) Niche construction. Am Nat 147:641–648CrossRefGoogle Scholar
  48. Peluc SI, Sillett TS, Rotenberry JT, Ghalambor CK (2008) Adaptive phenotypic plasticity in an island songbird exposed to a novel predation risk. Behav Ecol 19:830–835CrossRefGoogle Scholar
  49. Peuhkuri N, Ranta E, Juvonen S-K, Lindström K (1995) Schooling affects growth in the three-spined stickleback, Gasterosteus aculeatus. J Fish Biol 46:221–226CrossRefGoogle Scholar
  50. Pike T, Samanta M, Lindström J, Royle NJ (2008) Behavioural phenotype affects social interactions in an animal network. Proc R Soc Lond B 275:2515–2520CrossRefGoogle Scholar
  51. Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) Behaviour of teleost fishes, 2nd edn. Chapman and Hall, London, pp 363–440CrossRefGoogle Scholar
  52. Plomin R, DeFries JC, Loehlin JC (1977) Genotype–environment interaction and correlation in the analysis of human behavior. Psychol Bull 84:309–322CrossRefPubMedGoogle Scholar
  53. Poulin R (1999) Parasitism and shoal size in juvenile sticklebacks: conflicting selection pressures from different ectoparasites? Ethology 105:959–968CrossRefGoogle Scholar
  54. Ranta E, Lindström K (1990) Assortative schooling in three-spined sticklebacks. Ann Zool Fenn 27:67–75Google Scholar
  55. Ravigné V, Olivieri I, Dieckmann U (2003) Implications of habitat choice for protected polymorphisms. Evol Ecol Res 5:1–20Google Scholar
  56. Ravigné V, Dieckmann U, Olivieri I (2009) Live where you thrive: joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. Am Nat 174:E141–E169CrossRefPubMedGoogle Scholar
  57. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318CrossRefPubMedGoogle Scholar
  58. Réale D, Dingemanse NJ, Kazem AJN, Wright J (eds) (2010) Evolutionary and ecological approaches to the study of personality [Theme issue]. Philos T Roy Soc B 365:3937–4106Google Scholar
  59. Rice WR (1987) Speciation via habitat specialization: the evolution of reproductive isolation as a correlated character. Evol Ecol 1:301–314CrossRefGoogle Scholar
  60. Rödel HG, Monclús R, von Holst D (2006) Behavioral styles in European rabbits: social interactions and responses to experimental stressors. Physiol Behav 89:180–188CrossRefPubMedGoogle Scholar
  61. Rutter M, Dunn J, Plomin R, Simonoff E, Pickles A, Maughan B, Ormel J, Meyer J, Eaves L (1997) Integrating nature and nurture: implications of person–environment correlations and interactions for developmental psychopathology. Dev Psychopathol 9:335–364CrossRefPubMedGoogle Scholar
  62. Saltz JB (2011) Natural genetic variation in social enviornment choice: context-dependent gene–environment correlation in Drosophila melanogaster. Evolution 65:2325–2334CrossRefPubMedGoogle Scholar
  63. Saltz JB, Foley BR (2011) Natural genetic variation in social niche construction: social effects of aggression drive disruptive sexual selection in Drosophila melanogaster. Am Nat 177:645–654CrossRefPubMedGoogle Scholar
  64. Schluter D, McPhail JD (1992) Ecological character displacement and speciation in sticklebacks. Am Nat 140:85–108CrossRefPubMedGoogle Scholar
  65. Sharpe PB, van Horne B (1998) Influence of habitat on behavior of Townsend’s ground squirrels (Spermophilus townsendii). J Mammal 79:906–918CrossRefGoogle Scholar
  66. Sih A (1987) Prey refuges and predator–prey stability. Theor Popul Biol 31:1–12CrossRefGoogle Scholar
  67. Sih A, Bell AM (2008) Insights for behavioral ecology from behavioral syndromes. Adv Stud Behav 38:1–56CrossRefGoogle Scholar
  68. Sih A, Watters J (2005) The mix matters: behavioural types and group dynamics in water striders. Behaviour 142:1417–1431CrossRefGoogle Scholar
  69. Skúlason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trends Ecol Evol 10:366–370CrossRefPubMedGoogle Scholar
  70. Skúlason S, Snorrason SS, Ota D, Noakes DLG (1993) Genetically based differences in foraging behaviour among sympatric morphs of arctic charr (Pisces: Salmonidae). Anim Behav 45:1179–1192CrossRefGoogle Scholar
  71. Stamps JA, Groothuis TGG (2010a) Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Philos T Roy Soc B 365:4029–4041CrossRefGoogle Scholar
  72. Stamps JA, Groothuis TGG (2010b) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325CrossRefPubMedGoogle Scholar
  73. Svanbäck R, Bolnick DI (2007) Intraspecific competition drives increased resource use diversity within a natural population. Proc R Soc Lond B 274:839–844CrossRefGoogle Scholar
  74. Tuttle MD, Ryan MJ (1982) The role of synchronized calling, ambient light, and ambient noise, in anti-bat-predator behavior of a treefrog. Behav Ecol Sociobiol 11:125–131CrossRefGoogle Scholar
  75. 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
  76. Van Valen L (1965) Morphological variation and width of ecological niche. Am Nat 99:377–390CrossRefGoogle Scholar
  77. Verbeek MEM, Drent PJ, Wiepkema PR (1994) Consistent individual differences in early exploratory behaviour of male great tits. Anim Behav 48:1113–1121CrossRefGoogle Scholar
  78. Via S (1999) Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53:1446–1457CrossRefGoogle Scholar
  79. Walsh RN, Cummings RA (1976) The open-field test: a critical review. Psychol Bull 83:482–504CrossRefPubMedGoogle Scholar
  80. Ward AJW, Botham MS, Hoare DJ, James R, Broom M, Godin J-GJ, Krause J (2002) Association patterns and shoal fidelity in the three-spined stickleback. Proc R Soc Lond B 269:2451–2455CrossRefGoogle Scholar
  81. Ward AJW, Thomas P, Hart PJB, Krause J (2004) Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 55:561–568CrossRefGoogle Scholar
  82. Ward AJW, Holbrook RI, Krause J, Hart PJB (2005) Social recognition in sticklebacks: the role of direct experience and habitat cues. Behav Ecol Sociobiol 57:575–583CrossRefGoogle Scholar
  83. Wark AR, Greenwood AK, Taylor EM, Yoshida K, Peichel CL (2011) Heritable differences in schooling behavior among threespine stickleback populations revealed by a novel assay. PLoS One 6:e18316CrossRefPubMedGoogle Scholar
  84. Webster MM, Ward AJW, Hart PJB (2007) Boldness is influenced by social context in threespine sticklebacks. Behaviour 144:351–371CrossRefGoogle Scholar
  85. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  86. Wilson DS, Coleman K, Clark AB, Biederman L (1993) Shy-bold continuum in pumpkinseed sunfish: an ecological study of a psychological trait. J Comp Psychol 107:250–260CrossRefGoogle Scholar
  87. Wilson ADM, Godin J-GJ, Ward AJW (2010) Boldness and reproductive fitness correlates in the eastern mosquitofish, Gambusia holbrooki. Ethology 116:96–104CrossRefGoogle Scholar
  88. Wolf JB, Brodie ED III, Moore AJ (1999) Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am Nat 153:254–266CrossRefGoogle Scholar
  89. Wootton RJ (1973) Fecundity of the three-spined stickleback, Gasterosteus aculeatus (L.). J Fish Biol 5:683–688CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Simon Pearish
    • 1
  • Lauren Hostert
    • 1
  • Alison M. Bell
    • 1
  1. 1.School of Integrative BiologyUniversity of Illinois, UrbanaUrbanaUSA

Personalised recommendations