Variation along the shy–bold continuum in extremophile fishes (Poecilia mexicana, Poecilia sulphuraria)

Abstract

One potential trade-off that bold individuals face is between increased predation risks and gains in resources. Individuals experiencing high predation and hungry individuals (or individuals with low body condition) are predicted to show increased boldness. We examined one behavioral trait previously reported to be associated with boldness (the time individual fish needed to emerge from shelter) in various populations of mollies (Poecilia spp.). Our study system included several southern Mexican surface streams with high piscine predation and high food availability, sulfidic surface streams with high avian predation, in which the inhabiting fish show reduced body condition, and a sulfidic cave, where predation and body condition are low. Our comparison revealed very short times to emerge from the start box in populations from non-sulfidic streams. In sulfidic habitats (whether surface or cave), it took individual Poecilia mexicana considerably longer to emerge from the start box, and the same difference was also found in an independent comparison between P. mexicana and the closely related, highly sulfide-adapted Poecilia sulphuraria. Fish reared under common garden conditions (in the absence of predators and hydrogen sulfide) showed intermediate boldness scores to the extremes observed in the field. Our data thus indicate that (a) boldness is shaped by environmental conditions/experiential effects, but is not heritable, (b) predation affects boldness in the predicted direction, but (c) low body condition leads to reduced boldness. Extremophile Poecilia spp. spend most of their time surfacing to survive under sulfidic and hypoxic conditions, which exposes them to increased levels of predations, but the fish forage on the bottom. Hence, in this system, increased boldness does not increase foraging success. We argue that energy limitation favors reducing energetically costly behaviors, and exploring novel environments may be just one of them.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Alvarez del Villar J (1948) Descripción de una nueva especie de Mollienisia capturada en Baños del Azufre, Tabasco (Pisces, Poeciliidae). An Esc Nac Cienc Biol 5:275–281

    Google Scholar 

  2. Bakker TCM (1986) Aggressiveness in sticklebacks (Gasterosteus aculeatus)—a behavior-genetic study. Behaviour 98:1–144

    Article  Google Scholar 

  3. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473

    PubMed  Article  CAS  Google Scholar 

  4. Brown C, Braithwaite VA (2004) Size matters: a test of boldness in eight populations of bishop, Brachyraphis episcopi. Anim Behav 68:1325–1329

    Article  Google Scholar 

  5. Brown C, Jones F, Braithwaite VA (2005) In situ examination of boldness–shyness traits in the tropical poeciliid, Brachyraphis episcopi. Anim Behav 70:1003–1009

    Article  Google Scholar 

  6. Brown C, Burgess F, Braithwaite VA (2007a) Heritable and experiential effects on boldness in a tropical poeciliid. Behav Ecol Sociobiol 62:237–243

    Article  Google Scholar 

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

    Google Scholar 

  8. Carrico R, Blumberg W, Peisach J (1978) The reversible binding of oxygen to sulfhemoglobin. J Biol Chem 253:7212–7215

    PubMed  CAS  Google Scholar 

  9. Chapman LJ, Chapman CA (1993) Desiccation, flooding, and the behavior of Poecilia gillii (Pisces: Poeciliidae). Ichthyol Explor Freshw 4:279–287

    Google Scholar 

  10. Coleman K, Wilson DS (1998) Shyness and boldness in pumpkinseed sunfish: individual differences are context-specific. Anim Behav 56:927–936

    PubMed  Article  Google Scholar 

  11. Dall SR, 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 

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

    Article  Google Scholar 

  13. 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 

  14. Dingemanse NJ, Wright J, Kazem AJN, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138

    PubMed  Article  Google Scholar 

  15. Dingemanse NJ, Van der Plas F, Wright J, Réale D, Schrama M, Roff DA, Van der Zee E, Barber I (2009) Individual experience and evolutionary history of predation affect expression of heritable variation in fish personality and morphology. Proc R Soc Lond B 276:1285–1293

    Google Scholar 

  16. Evans C (1967) The toxicity of hydrogen sulphide and other sulphides. Quart J Exp Physiol 52:231–248

    PubMed  CAS  Google Scholar 

  17. Fraser DF, Gilliam JF, Daley MJ, Le AN, Skalski GT (2001) Explaining leptokurtic movement distributions: intrapopulation variation in boldness and exploration. Am Nat 158:124–135

    PubMed  Article  CAS  Google Scholar 

  18. Godin J-GJ, Dugatkin LA (1999) Female mating preference for bold males in the guppy, Poecilia reticulata. Proc Natl Acad Sci U S A 93:10262–10267

    Article  Google Scholar 

  19. Gordon MS, Rosen DE (1962) A cavernicolous form of the Poeciliid fish Poecilia sphenops from Tabasco, México. Copeia 1962:360–368

    Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  21. Gosling SD, John OP (1999) Personality dimensions in non-human animals: a cross-species review. Curr Dir Psychol Sci 8:69–75

    Article  Google Scholar 

  22. Ip YK, Kuah SSL, Chew SF (2004) Strategies adopted by the mudskipper Boleophthalmus boddaerti to survive sulfide exposure in normoxia or hypoxia. Physiol Biochem Zool 77:824–837

    PubMed  Article  CAS  Google Scholar 

  23. Johnsson JI, Sernland E, Blixt M (2001) Sex-specific aggression and antipredator behaviour in young brown trout. Ethology 107:587–599

    Article  Google Scholar 

  24. Kilgour R (1975) Open-field test as an assessment of temperament of dairy cows. Anim Behav 23:615–624

    Article  Google Scholar 

  25. Körner KE, Schlupp I, Plath M, Loew ER (2006) Spectral sensitivity of mollies: comparing surface- and cave-dwelling Atlantic mollies, Poecilia mexicana. J Fish Biol 69:54–65

    Article  Google Scholar 

  26. Kramer DL (1983) The evolutionary ecology of respiratory modes in fishes: an analysis based on the costs of breathing. Environ Biol Fish 9:145–158

    Article  Google Scholar 

  27. Kramer DL, Manley D, Bourgeois R (1983) The effect of respiratory mode and oxygen concentration on the risk of aerial predation in fishes. Can J Zool 61:653–665

    Article  Google Scholar 

  28. Lopez P, Hawlena D, Polo V, Amo L, Martin J (2006) Sources of individual shy–bold variations in antipredator behaviour of male Iberian rock lizards. Anim Behav 69:1–9

    Article  Google Scholar 

  29. Magnhagen C (2007) Social influence on the correlation between behaviours in young-of-the-year perch. Behav Ecol Sociobiol 61:525–531

    Article  Google Scholar 

  30. Magurran AE, Macías Garcia C (2000) Sex differences in behaviour as an indirect consequence of mating system. J Fish Biol 57:839–857

    Article  Google Scholar 

  31. McCune S (1995) The impact of paternity and early socialization on the development of cats’ behaviour to people and novel objects. Appl Anim Behav Sci 45:109–124

    Article  Google Scholar 

  32. Miller RR (1975) Five new species of Mexican poeciliid fishes of the genera Poecilia, Gambusia, and Poeciliopsis. Occ Pap Mus Zool Univ Mich 672:1–44

    Google Scholar 

  33. Miller RR (2005) Freshwater fishes of Mexico. University of Chicago Press, Chicago

    Google Scholar 

  34. National Research Council (1979) Hydrogen sulfide. University Park, Baltimore

    Google Scholar 

  35. Nicholls P (1975) The effect of sulphide on cytochrome aa3. Isosteric and allosteric shifts of the reduced alpha-peak. Biochem Biophys Acta 396:24–35

    PubMed  Article  CAS  Google Scholar 

  36. van Oers K, Drent PJ, de Goede P, van Nordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc Lond B 271:65–73

    Article  Google Scholar 

  37. Park C, Nagel R, Blumberg W, Peisach J, Maliozzo R (1986) Sulfhemoglobin: properties of partially sulfurated tetramers. J Biol Chem 261:8805–8810

    PubMed  CAS  Google Scholar 

  38. Parzefall J (1974) Rückbildung aggressiver Verhaltensweisen bei einer Höhlenform von Poecilia sphenops (Pisces, Poeciliidae). Z Tierpsychol 35:66–84

    PubMed  CAS  Google Scholar 

  39. Parzefall J (1979) Zur Genetik und biologischen Bedeutung des Aggressionsverhaltens von Poecilia sphenops (Pisces, Poeciliidae). Z Tierpsychol 50:399–422

    Google Scholar 

  40. Parzefall J (1993) Schooling behaviour in population-hybrids of Astyanax fasciatus and Poecilia mexicana (Pisces, Characidae and Poeciliidae). In: Schröder H, Bauer J, Schartl M (eds) Trends in ichthyology: an international perspective. Blackwell Scientific, Oxford, pp 297–303

    Google Scholar 

  41. Peters N, Peters G, Parzefall J, Wilkens H (1973) Über degenerative und konstruktive Merkmale bei einer phylogenetisch jungen Höhlenform von Poecilia sphenops (Pisces, Poeciliidae). Int Rev Gesamten Hydrobiol 58:417–436

    Article  Google Scholar 

  42. Plath M (2008) Male mating behavior and costs of sexual harassment for females in cavernicolous and extremophile populations of Atlantic mollies (Poecilia mexicana). Behaviour 145:73–98

    Article  Google Scholar 

  43. Plath M, Schlupp I (2008) Parallel evolution leads to reduced shoaling behavior in two cave-dwelling populations of Atlantic mollies (Poecilia mexicana, Poeciliidae, Teleostei). Environ Biol Fish 82:289–297

    Article  Google Scholar 

  44. Plath M, Strecker U (2008) Behavioral diversification in a young species flock of pupfish (Cyprinodon spp., Cyprinodontidae, Teleostei): shoaling and aggressive behavior. Behav Ecol Sociobiol 62:1727–1737

    Article  Google Scholar 

  45. Plath M, Tobler M (2009) The evolutionary ecology of the cave molly (Poecilia mexicana) from the Cueva del Azufre system. In: Trajano E, Bichuette ME, Kapoor BG (eds) The biology of subterranean fishes (in press)

  46. Plath M, Parzefall J, Schlupp I (2003) The role of sexual harassment in cave- and surface-dwelling populations of the Atlantic molly, Poecilia mexicana (Poeciliidae, Teleostei). Behav Ecol Sociobiol 54:303–309

    Article  Google Scholar 

  47. Plath M, Parzefall J, Körner KE, Schlupp I (2004) Sexual selection in darkness? Female mating preferences in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae, Teleostei). Behav Ecol Sociobiol 55:596–601

    Article  Google Scholar 

  48. Plath M, Heubel KU, García de León FJ, Schlupp I (2005) Cave molly females (Poecilia mexicana, Poeciliidae, Teleostei) like well-fed males. Behav Ecol Sociobiol 58:144–151

    Article  Google Scholar 

  49. Plath M, Hauswaldt JS, Moll K, Tobler M, García de León FJ, Schlupp I, Tiedemann R (2007a) Local adaptation and pronounced genetic differentiation in an extremophile fish, Poecilia mexicana, from a Mexican cave with toxic hydrogen sulfide. Mol Ecol 16:967–976

    PubMed  Article  CAS  Google Scholar 

  50. Plath M, Tobler M, Riesch RW, García de León FJ, Giere O, Schlupp I (2007b) Survival in an extreme habitat: the roles of behaviour and energy limitation. Naturwissenschaften 94:991–996

    PubMed  Article  CAS  Google Scholar 

  51. Plath M, Makowicz AM, Schlupp I, Tobler M (2007c) Sexual harassment in live-bearing fishes: comparing courting and non-courting species. Behav Ecol 18:680–688

    Article  Google Scholar 

  52. Ptacek MB, Breden F (1998) Phylogenetic relationships among the mollies (Poeciliidae: Poecilia: Mollienesia group) based on mitochondrial DNA sequences. J Fish Biol 53:64–81

    Article  Google Scholar 

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

    Article  Google Scholar 

  54. 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

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  56. Reaney LT, Backwell PRY (2007) Risk-taking behavior predicts aggression and mating success in a fiddler crab. Behav Ecol 18:521–525

    Article  Google Scholar 

  57. Riesch R, Tobler M, Schlupp I, Plath M (2009) Offspring number in a livebearing fish (Poecilia mexicana, Poeciliidae): reduced fecundity and reduced plasticity in a population of cave mollies. Environ Biol Fishes 84:89–94

    Article  Google Scholar 

  58. Rochette R, Tetreault F, Himmelman JH (2001) Aggregation of whelks, Buccinium undatum, near feeding predators—the role of reproductive requirement. Anim Behav 61:31–41

    PubMed  Article  Google Scholar 

  59. Schartl M, Meyer MK, Wilde B (2006) Description of Priapella chamulae sp. n.—a new poeciliid fish from the upper Río Grijalva system, Tabasco, Mexico (Teleostei: Cyprinodontiformes: Poeciliidae). Zool Abh Dresden 55:59–67

    Google Scholar 

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

    PubMed  Article  Google Scholar 

  61. Sinn DL, Apiolaza LA, Moltschaniwskyj NA (2006) Heritability and fitness-related consequences of squid personality traits. J Evol Biol 19:1437–1447

    PubMed  Article  CAS  Google Scholar 

  62. Stein MB, Chartier MJ, Lizak MV, Jang L (2001) Familial aggregation of anxiety-related quantitative traits in generalized social phobia—clues to understand “disorder” heritability? Am J Med Genet 105:79–83

    PubMed  Article  CAS  Google Scholar 

  63. Svartberg K, Tapper I, Temrin H, Radesater T, Thorman S (2005) Consistency of personality in dogs. Anim Behav 69:283–291

    Article  Google Scholar 

  64. Tobler M (2008) Divergence in trophic ecology characterises colonisation of extreme habitats. Biol J Linn Soc 95:517–528

    Article  Google Scholar 

  65. Tobler M, Schlupp I, Heubel KU, Riesch R, García de León FJ, Giere O, Plath M (2006) Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10:577–585

    PubMed  Article  CAS  Google Scholar 

  66. Tobler M, Schlupp I, Plath M (2007) Predation of a cavefish (Poecilia mexicana, Poeciliidae) by a giant water bug (Belostoma, Belostomatidae) in a Mexican sulfur cave. Ecol Entomol 32:492–495

    Article  Google Scholar 

  67. Tobler M, DeWitt TJ, Schlupp I, García de León FJ, Herrmann R, Feulner PGD, Tiedemann R, Plath M (2008a) Toxic hydrogen sulfide and dark caves: phenotypic and genetic divergence across two abiotic environmental gradients in Poecilia mexicana. Evolution 62:2643–2659

    PubMed  Article  Google Scholar 

  68. Tobler M, Riesch R, García de León FJ, Schlupp I, Plath M (2008b) Two endemic and endangered fishes, Poecilia sulphuraria (Alvarez, 1948) and Gambusia eurystoma Miller, 1975 (Poeciliidae, Teleostei) as only survivors in a small sulphidic habitat. J Fish Biol 72:523–533

    Article  Google Scholar 

  69. Tobler M, Franssen C, Plath M (2008c) Male-biased predation of a cave fish by a giant water bug. Naturwissenschaften 95:775–779

    PubMed  Article  CAS  Google Scholar 

  70. Yoshida M, Nagamine M, Uematsu K (2005) Comparison of behavioral responses to a novel environment between three teleosts, bluegill Lepomis macrochirus, crucian carp Carassius langsdorfii, and goldfish Carassius auratus. Fish Sci 71:314–319

    Article  CAS  Google Scholar 

  71. Ward A, Thomas P, Hart P, Krause J (2004) Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 55:561–568

    Article  Google Scholar 

  72. Weber JM, Kramer DL (1983) Effects of hypoxia and surface access on growth, mortality, and behavior of juvenile guppies, Poecilia reticulata. Can J Fish Aquat Sci 40:1583–1588

    Google Scholar 

  73. Webster MM, Ward AJW, Hart PJB (2009) Individual boldness affects interspecific interactions in sticklebacks. Behav Ecol Sociobiol 63:511–520

    Article  Google Scholar 

  74. 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 74:689–698

    Article  Google Scholar 

  75. Wilson DS, Coleman K, Clark AB, Biederman L (1993) The shy–bold continuum in pumkinseed sunfish (Lepomis gibbosus): an ecological study of a psychological trait. J Comp Psychol 107:250–260

    Article  Google Scholar 

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

    Google Scholar 

  77. Winemiller KO (1989) Development of dermal lip protuberances for aquatic surface respiration in South American characid fishes. Copeia 1989:382–390

    Article  Google Scholar 

  78. Wright D, Rimmer LB, Pritchard VL, Krause J, Butlin RK (2003) Inter- and intra-population variations in shoaling and boldness in the zebrafish (Danio rerio). Naturwissenschaften 90:374–377

    PubMed  Article  CAS  Google Scholar 

  79. Yerkes RM (1939) The life history and personality of the chimpanzee. Am Nat 73:97–112

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank A. Böttger, N. Bunzel (both University of Potsdam), and J. Horstkotte (University of Hamburg) for their help in the field. We thank G. Rosenthal for commenting on a previous manuscript draft. G. Rosenthal and J.B. Johnson kindly provided information about boldness in Xiphophorus spp. The Mexican Government (Permiso de Pesca de Fomento No. DGOPA.06192.240608.-1562), Semarnat (No. SGPA/DGVS/04148/08 and SGPA/DGVS/04751/08), as well as the Municipal of Tacotalpa (SM/1133/208) kindly provided permits for the work at the Cueva del Azufre and the Baños del Azufre areas. Financial support came from the DFG (PL 470/1-2, to M.P.) and from NSF (#105095200).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Rüdiger Riesch.

Additional information

Communicated by T. Bakker

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Riesch, R., Duwe, V., Herrmann, N. et al. Variation along the shy–bold continuum in extremophile fishes (Poecilia mexicana, Poecilia sulphuraria). Behav Ecol Sociobiol 63, 1515–1526 (2009). https://doi.org/10.1007/s00265-009-0780-z

Download citation

Keywords

  • Boldness
  • Extremophiles
  • Hydrogen sulfide
  • Poeciliidae
  • Predator regimes