Behavioral Ecology and Sociobiology

, Volume 60, Issue 6, pp 794–802

Reduction of the association preference for conspecifics in cave-dwelling Atlantic mollies, Poecilia mexicana

  • Rüdiger Riesch
  • Ingo Schlupp
  • Michael Tobler
  • Martin Plath
Original Article

Abstract

Cave animals are widely recognised as model organisms to study regressive evolutionary processes like the reduction of eyes. In this paper, we report on the regressive evolution of species discrimination in the cave molly, Poecilia mexicana, which, unlike other cave fishes, still has functional eyes. This allowed us to examine the response to both visual and non-visual cues involved in species discrimination. When surface-dwelling females were given a chance to associate with either a conspecific or a swordtail (Xiphophorus hellerii) female, they strongly preferred the conspecific female both when multiple cues and when solely visual cues were available to the female. No association preference was observed when only non-visual cues were provided. In contrast, cave-dwelling females showed no preference under all testing conditions, suggesting that species recognition mechanisms have been reduced. We discuss the role of species discrimination in relation to habitat differences.

Keywords

Cave fish Poeciliidae Xiphophorus Shoaling Species recognition 

References

  1. Allan JR, Pitcher TJ (1986) Species segregation during predator evasion in cyprinid fish shoals. Freshw Biol 16:653–659CrossRefGoogle Scholar
  2. Barnard CJ, Thompson DBA, Stephens H (1982) Time budgets, feeding efficiency and flock dynamics in mixed species flocks of lapwings, golden plovers and gulls. Behaviour 80:44–69CrossRefGoogle Scholar
  3. Burt de Perera T (2004a) Spatial parameters encoded in the spatial map of the blind Mexican cave fish, Astyanax fasciatus. Anim Behav 68:291–295CrossRefGoogle Scholar
  4. Burt de Perera T (2004b) Fish can encode order in their spatial map. Proc R Soc Lond B 271:2131–2134CrossRefGoogle Scholar
  5. Bisazza A, Marin G (1995) Sexual selection and sexual size dimorphism in the eastern mosquitofish Gambusia holbrooki (Pisces, Poeciliidae). Ethol Ecol Evol 7:169–183CrossRefGoogle Scholar
  6. Brown C, Warburton K (1997) Predator recognition and anti-predator responses in the rainbowfish Melanotaenia eachamensis. Behav Ecol Sociobiol 41:61–68CrossRefGoogle Scholar
  7. Couldridge VCK, Alexander GJ (2002) Color patterns and species recognition in four closely related species of Lake Malawi cichlid. Behav Ecol 13(1):59–64CrossRefGoogle Scholar
  8. Crapon de Caprona M-D, Ryan MJ (1990) Conspecific mate recognition in swordtails, Xiphophorus nigrensis and X. pygmaeus: olfactory and visual cues. Anim Behav 29:290–296CrossRefGoogle Scholar
  9. Godin J-GJ (1986) Antipredator function of shoaling in teleost fishes: a selective review. Nat Can 113:241–250Google Scholar
  10. Gordon MS, Rosen DE (1962) A cavernicolous form of the Poeciliid fish Poecilia sphenops from Tabasco, Mexico. Copeia 1962:360–368CrossRefGoogle Scholar
  11. Greig-Smith PW (1981) The role of alarm responses in the formation of mixed-species flocks of heathland birds. Behav Ecol Sociobiol 8:7–10CrossRefGoogle Scholar
  12. Hankison SJ, Morris MR (2003) Avoiding a compromise between sexual selection and species recognition: female swordtail fish assess multiple species-specific cues. Behav Ecol 14:282–287CrossRefGoogle Scholar
  13. Jeffery WR (2001) Cavefish as a model system in evolutionary and developmental biology. Dev Biol 231:1–12PubMedCrossRefGoogle Scholar
  14. Jeffery WR (2005) Adaptive evolution of eye degeneration in the Mexican blind cavefish. J Heredity 96:185–196CrossRefGoogle Scholar
  15. Jordan R, Kellogg K, Juanes F, Stauffer J Jr (2003) Evaluation of female mate choice cues in a group of Lake Malawi Mbuna (Cichlidae). Copeia 2003:181–186CrossRefGoogle Scholar
  16. Kiester RA (1979) Conspecifics as cues: a mechanism for habitat selection in the Panamanian grass anole (Anolis auratus). Behav Ecol Sociobiol 5:323–330CrossRefGoogle Scholar
  17. Kodric-Brown A, Strecker U (2001) Responses of Cyprinodon maya and C. labiosus females to visual and olfactory cues of conspecific and heterospecific males. Biol J Linn Soc 74:541–548CrossRefGoogle Scholar
  18. 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 (In press)Google Scholar
  19. Krause J, Godin J-GJ (1994) Shoal choice in the banded killifish (Fundulus diaphanous, Teleostei, Cyprinodontidae): effects of predation risk, fish size, species composition and size of shoals. Ethology 98:105–116Google Scholar
  20. Kyriacou CP, Hall JC (1982) The function of courtship song rhythms in Drosophila. Anim Behav 30:784–801CrossRefGoogle Scholar
  21. Landeau L, Terborgh J (1986) Oddity and the ‘confusion effect’ in predation. Anim Behav 34:1372–1380CrossRefGoogle Scholar
  22. McLennan DA, Ryan MJ (1997) Responses to conspecific and heterospecific olfactory cues in the swordtail Xiphophorus cortezi. Anim Behav 54:1077–1088PubMedCrossRefGoogle Scholar
  23. McLennan DA, Ryan MJ (1999) Interspecific recognition and discrimination based upon olfactory cues in northern swordtails. Evolution 53(3):880–888CrossRefGoogle Scholar
  24. McRobert SP, Bradner J (1998) The influence of body coloration on shoaling preferences in fish. Anim Behav 56:611–615PubMedCrossRefGoogle Scholar
  25. Magurran AE (1990) The adaptive significance of schooling as an anti-predator defense in fish. Ann Zool Fennici 27:51–66Google Scholar
  26. Magurran AE, Seghers BH, Shaw PW, Carvalho GR (1995) The behavioural diversity and evolution of guppy, Poecilia reticulata populations in Trinidad. Adv Study Behav 24:155–202CrossRefGoogle Scholar
  27. Möller D (2001) Aspekte zur Populationsgenetik des eingeschlechtlichen Amazonenkärpflings Poecilia formosa (GIRARD 1859) unter Berücksichtigung der genetischen parentalen Art, dem Breitflossenkärpfling Poecilia latipinna (LESUEUR 1821) und dem Atlantikkärpfling Poecilia mexicana (STEINDACHNER 1863). Ph.D. thesis, University of HamburgGoogle Scholar
  28. Morgan MJ and Godin J-GJ (1985) Antipredator Benefits of Schooling Behaviour in a Cyprinodontid Fish, the Banded Killifish (Fundulus diaphanus). Z Tierpsychol 70:236–246Google Scholar
  29. Parzefall J (1969) Zur vergleichenden Ethologie verschiedener Mollienesia-Arten einschlieβlich einer Höhlenform von Mollienesia sphenops. Behaviour 33:1–37PubMedCrossRefGoogle Scholar
  30. Parzefall J (1970) Morphologische Untersuchungen an einer Höhlenform von Mollienesia sphenops (Pisces, Poeciliidae). Z Morphol Tiere 68:323–342CrossRefGoogle Scholar
  31. Parzefall J (1974) Rückbildung aggressiver Verhaltensweisen bei einer Höhlenform von Mollienesia sphenops (Pisces, Poeciliidae). Z Tierpsychol 35:66–84PubMedGoogle Scholar
  32. Parzefall J (1979) Zur Genetik und biologischen Bedeutung des Aggressionsverhaltens von Poecilia sphenops (Pisces, Poeciliidae). Z Tierpsychol 50:399–422Google Scholar
  33. 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 297–303Google Scholar
  34. Parzefall J (2001) A review on morphological and behavioural changes in the cave molly Poecilia mexicana from Tabasco, Mexico. Environ Biol Fisches 50:263–275CrossRefGoogle Scholar
  35. Parzefall J, Gagelmann U, Schartl M (1997) Aggressive behaviour and optomotor response in different populations of Poecilia mexicana (Pisces, Poeciliidae). Mem Biospeol 24:63–69Google Scholar
  36. Persaud KN, Galef BG (2003) Female Japanese quail aggregate to avoid sexual harassment by conspecific males: a possible cause of conspecific cueing. Anim Behav 65:89–94CrossRefGoogle Scholar
  37. 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 58:417–436CrossRefGoogle Scholar
  38. Petrie M (1994) Improved growth and survival of offspring of peacock with more elaborate trains. Nature 371:598–599CrossRefGoogle Scholar
  39. Pilastro A, Benetton S, Bisazza A (2003) Female aggregation and male competition reduce the costs of sexual harassment in mosquitofish. Anim Behav 65:1151–1159CrossRefGoogle Scholar
  40. 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 363–437Google Scholar
  41. Plath M, Parzefall J, Schlupp I (2003a) The role of sexual harassment in cave and surface dwelling populations of the Atlantic molly, Poecilia mexicana (Poeciliidae, Teleostei). Behav Ecol Sociobiol 54:303–309CrossRefGoogle Scholar
  42. Plath M, Körner KE, Parzefall J, Schlupp I (2003b) Persistence of a visually mediated mating preference in the cave molly, Poecilia mexicana (Poeciliidae, Teleostei). Subterran Biol 1:93–97Google Scholar
  43. Plath M, Parzefall J, Körner KE, Schlupp I (2004a) Sexual selection in darkness? Female mating preferences in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae, Teleostei). Behav Ecol Sociobiol 55:596–601CrossRefGoogle Scholar
  44. Plath M, Brümmer A, Schlupp I (2004b) Sexual harassment in a live-bearing fish (Poecilia mexicana): influence of population-specific male mating behaviour. Acta Ethol 7:65–72CrossRefGoogle Scholar
  45. Plath M, Heubel KU, García de León FJ, Schlupp I (2005) Cave molly females (Poecilia mexicana) like well-fed males. Behav Ecol Sociobiol 58:144–151CrossRefGoogle Scholar
  46. Plath M, Seggel U, Burmeister H, Heubel KU, Schlupp I (2006) Choosy males from the underground: male mating preferences in surface- and cave-dwelling Atlantic mollies (Poecilia mexicana). Naturwissenschaften 93:103–109PubMedCrossRefGoogle Scholar
  47. Ratcliffe LM, Grant PR (1983) Species recognition in Darwin’s finches (Geospiza, Gould). I. Discrimination by morphological cues. Anim Behav 31:1139–1153CrossRefGoogle Scholar
  48. Reed JM, Dobson AP (1993) Behavioural constraints and conservation biology: conspecific attraction and recruitment. Trends Ecol Evol 8:253–256CrossRefGoogle Scholar
  49. Riesch R, Arndt M, Plath M (2005) Non-visual localisation of a conspecific male by surface- and cave-dwelling Atlantic molly females (Poecilia mexicana, Poeciliidae, Teleostei). Nat Croat 14:1–58Google Scholar
  50. Riesch R, Schlupp I, Plath M (2006) Influence of male competition on male mating behaviour in the cave molly, Poecilia mexicana. J Ethol 24:27–31CrossRefGoogle Scholar
  51. Ryan MJ, Rand AS (1993) Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47:647–657CrossRefGoogle Scholar
  52. Schlupp I, Ryan MJ (1996) Mixed-species shoals and the maintenance of a sexual–asexual mating system in mollies. Anim Behav 52:885–890CrossRefGoogle Scholar
  53. Seehausen O, Van Alphen JJM, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811CrossRefGoogle Scholar
  54. Sherman PW, Reeve HK, Pfennig DW (1997) Recognition systems. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 4th edn. Blackwell, London, pp 69–96Google Scholar
  55. Stamps JA (1988) Conspecific attraction and aggregation in territorial species. Am Nat 131:329–347CrossRefGoogle Scholar
  56. Theodorakis CW (1989) Size segregation and the effects of oddity on predation risk in minnow schools. Anim Behav 38:496–502CrossRefGoogle Scholar
  57. Tobler M, Schlupp I, Heubel KU, Riesch R, Garcia de Leon FJ, Giere O, Plath M (2006) Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles (in press) DOI 10.1007/s00792-006-0531-2
  58. Turner GF, Pitcher TJ (1986) Attack abatement: a model for group protection by combined avoidance and dilution. Am Nat 128:228–240CrossRefGoogle Scholar
  59. Weber A, Proudlove GS, Parzefall J, Wilkens H, Nalbant TT (1998) Pisces (Teleostei): Morphology, systematic diversity, distribution and ecology of stygobitic fishes. In: Juberthie C, Decu V (eds) Encyclopaedia Biospeologica, Tome II. Société de Biospéologie, Moulis, Bucarest, pp 835–1373Google Scholar
  60. Wilkens H (1988) Evolution and genetics of epigean and cave Astyanax fasciatus (Characidae, Pisces). Evol Biol 23:271–367Google Scholar
  61. Wilkens H, Strecker U (2003) Convergent evolution of the cavefish Astyanax (Characidae, Teleostei): genetic evidence from reduced eye-size and pigmentation. Biol J Linn Soc 80:545–554CrossRefGoogle Scholar
  62. Wolf N (1985) Odd fish abandon mixed-species groups when threatened. Behav Ecol Sociobiol 17:47–52CrossRefGoogle Scholar
  63. Yamamoto Y, Jeffery WR (2000) Central role for the lens in cavefish eye degeneration. Science 289:631–633PubMedCrossRefGoogle Scholar
  64. Yamamoto Y, Stock DW, Jeffery WR (2004) Hedgehog signalling controls eye degeneration in blind cavefish. Nature 431:844–847PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Rüdiger Riesch
    • 1
    • 2
  • Ingo Schlupp
    • 1
    • 3
  • Michael Tobler
    • 1
    • 3
  • Martin Plath
    • 1
    • 2
    • 4
  1. 1.Department of ZoologyUniversity of OklahomaNormanUSA
  2. 2.Biozentrum GrindelUniversität HamburgHamburgGermany
  3. 3.Zoologisches InstitutUniversität ZürichZürichSwitzerland
  4. 4.Unit of Evolutionary Biology and Systematic Zoology, Department of Biochemistry and BiologyUniversity of PotsdamPotsdamGermany

Personalised recommendations