Skip to main content

Parallel evolution leads to reduced shoaling behavior in two cave dwelling populations of Atlantic mollies (Poecilia mexicana, Poeciliidae, Teleostei)

Abstract

Shoaling behavior protects fishes from avian and piscine predation, but at the same time costs of group living arise due to several mechanisms including increased food competition. Most cave fishes live in an environment in which avian and piscine predators are lacking, and cave environments are often characterized by low food availability, leading to increased food competition. Altogether, this should favor the reduction of shoaling in cave fishes. We compared shoaling behavior (i.e. the tendency to associate with a stimulus shoal) among surface dwelling populations of the Atlantic molly, Poecilia mexicana, and two cave forms of that species. The first cave population of P. mexicana originated from the Cueva del Azufre and was previously recognized as the only cave form of a poeciliid fish. The second cave population examined came from a cave that was discovered only recently (Cueva Luna Azufre). In both cave forms shoaling behavior was reduced compared with surface dwelling mollies.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Agrillo C, Dadda M, Bisazza A (2006) Sexual harassment influences group choice in female mosquitofish. Ethology 112:592–598

    Article  Google Scholar 

  2. Brock VE, Riffenburgh RH (1960) Fish schooling: a possible factor in reducing predation. J Conseil 25:307–317

    Google Scholar 

  3. Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fisheries 4:280–288

    Article  Google Scholar 

  4. Burt de Perera T (2004a) Spatial parameters encoded in the spatial map of the blind Mexican cave fish, Astyanax fasciatus. Anim Behav 68:291–295

    Article  Google Scholar 

  5. Burt de Perera T (2004b) Fish can encode order in their spatial map. Proc R Soc Lond B 271:2131–2134

    Article  Google Scholar 

  6. Chapman MR, Kramer DL (1996) Guarded resources: the effect of intruder number on the tactics and success of defenders and intruders. Anim Behav 52:83–94

    Article  Google Scholar 

  7. Dadda M, Pilastro A, Bisazza A (2005) Male sexual harassment and female schooling behaviour in the eastern mosquitofish. Anim Behav 70:463–471

    Article  Google Scholar 

  8. Foster SA (1985) Group foraging by a coral reef fish: a mechanism for gaining access to defended resources. Anim Behav 33:779–782

    Article  Google Scholar 

  9. Futuyma DJ (2005) Evolution. Sinauer Associates, Sunderland, MA, USA

    Google Scholar 

  10. Godin J-GJ (1986) Antipredator function of shoaling in teleost fishes: a selective review. Naturaliste Can 113:241–250

    Google Scholar 

  11. Gordon MS, Rosen DE (1962) A cavernicolous form of the Poeciliid fish Poecilia sphenops from Tabasco, México. Copeia 2:360–368

    Article  Google Scholar 

  12. Gregson JNS, Burt de Perera T (2007) Shoaling in eyed and blind morphs of the characin Astyanax fasciatus under light and dark conditions. J Fish Biol 70:1615–1619

    Article  Google Scholar 

  13. Hassan ES (1989) Hydrodynamic imaging of the surroundings by the lateral line of the blind cave fish Anoptichthys jordani. In: Coombs S, Gorner P, Munz H (eds) The mechanosensory lateral line neurobiology and evolution. Springer-Verlag, New York, pp 217–228

    Google Scholar 

  14. van Havre N, FitzGerald GJ (1988) Shoaling and kin recognition in the threespine stickleback (Gasterosteus aculeatus L.). Biol Behav 13:190–201

    Google Scholar 

  15. Hose LD, Pisarovicz JA (1999) Cueva de Villa Luz, Tabasco, Mexico: reconnaissance study of an active sulfur spring cave. J Cave Karst Stud 61:13–21

    CAS  Google Scholar 

  16. Hüppop K (1986) Oxygen consumption of Astyanax fasciatus (Characidae, Pisces): a comparison of epigean and hypogean populations. Environ Biol Fish 17:299–308

    Article  Google Scholar 

  17. Hüppop K (1988) Phänomene und Bedeutung der Energieersparnis beim Höhlensalmler Astyanax fasciatus. PhD thesis, University of Hamburg

  18. Hüppop K (2000) How do cave animals cope with the food scarcity in caves? In: Wilkens H, Culver DC, Humphries WF (eds) Ecosystems of the world 30: Subterranean ecosystems. Elsevier, Amsterdam, pp 159–188

    Google Scholar 

  19. Jankowska M, Thinès G (1982) Étude comparative de la densité de groupes de poissons cavernicoles et épigés (Characidae, Cyprinidae, Clariidae). Behav Proces 7:289–294

    Google Scholar 

  20. Keenleyside MHA (1979) Diversity and adaptation in fish behaviour. Springer-Verlag, Berlin

    Google Scholar 

  21. 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 

  22. Krause J (1993) The influence of hunger on shoal size choice by three-spined sticklebacks, Gasterosteus aculeatus. J Fish Biol 43:775–780

    Article  Google Scholar 

  23. Krause J, Godin J-GJ (1994) Influence of parasitism on the shoaling behaviour of banded killifish, Fundulus diaphanus. Can J Zool 72:1775–1779

    Article  Google Scholar 

  24. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford

    Google Scholar 

  25. Krause J, Hartmann N, Pritchard VL (1999) The influence of nutritional state on shoal choice in zebrafish, Danio rerio. Anim Behav 57:771–775

    PubMed  Article  Google Scholar 

  26. Laland KN, Williams K (1997) Shoaling generates social learning of foraging information in guppies. Anim Behav 53:1161–1169

    PubMed  Article  Google Scholar 

  27. Langecker TG, Wilkens H, Parzefall J (1996) Studies on the trophic structure of an energy rich Mexican cave (Cueva de las Sardinas) containing sulfurous water. Mem Biospeol 23:121–125

    Google Scholar 

  28. Magurran AE (1990) The adaptive significance of schooling as an antipredator defence in fish. Ann Zool Fenn 27:51–66

    Google Scholar 

  29. Magurran AE, Pitcher TJ (1987) Provenance, shoal size and the sociobiology of predator evasion behaviour in minnow shoals. Proc Roy Soc Lond B 229:439–445

    Article  Google Scholar 

  30. Magurran AE, Seghers BH (1990) Population differences in the schooling behaviour of newborn guppies, Poecilia reticulata. Ethology 84:334–342

    Google Scholar 

  31. Magurran AE, Seghers BH (1991) Variation in schooling and aggression amongst guppy (Poecilia reticulata) populations in Trinidad. Behaviour 118:214–234

    Article  Google Scholar 

  32. Magurran AE, Oulton W, Pitcher TJ (1985) Vigilant behaviour and shoal size in minnows. Z Tierpsychol 67:167–178

    Google Scholar 

  33. Magurran AE, Seghers BH, Carvalho GR, Shaw PW (1992) Behavioural consequences of an artificial introduction of guppies (Poecilia reticulata) in N. Trinidad: evidence for the evolution of antipredator behaviour in the wild. Proc Roy Soc Lond B 248:260–277

    Google Scholar 

  34. Magurran AE, Seghers BH, Carvalho GR, Shaw PW (1993) Evolution of adaptive variation in antipredator behaviour. In: Huntingford FA, Torricelli P (eds) Behavioural ecology of fishes. Harwood Academic Publishers, Switzerland, pp 29–44

    Google Scholar 

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

    Google Scholar 

  36. Montgomery JC, Coombs S, Baker CF (2001) The mechanosensory lateral line system of the hypogean form of Astyanax fasciatus. Environ Biol Fish 62:87–96

    Article  Google Scholar 

  37. Neill SR, Cullen JM (1973) Experiments on whether schooling by their prey affects the hunting behaviour of cephalopods and fish predators. J Zool Lond 172:549–569

    Article  Google Scholar 

  38. Partridge BL, Pitcher TJ (1980) The sensory basis for fish schools: relative roles of lateral line and vision. J Comp Physiol A 135:315–325

    Article  Google Scholar 

  39. Parzefall J (1993a) 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. Blackwell Science, Oxford, pp 297–303

    Google Scholar 

  40. Parzefall J (1993b) Behavioural ecology of cave-dwelling fishes. In: Pitcher TJ (ed) Behaviour of teleost fishes, second edition. Chapman and Hall, London, pp 573–608

    Google Scholar 

  41. Parzefall J (2001) A review on morphological and behavioural changes in the cave molly Poecilia mexicana from Tabasco, Mexico. Environ Biol Fish 50:263–275

    Article  Google Scholar 

  42. Parzefall J, Kraus C, Tobler M, Plath M (2007) Photophilic behaviour in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae). J Fish Biol 71:1225–1231

    Google Scholar 

  43. 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 Ges Hydrobiol 58:417–436

    Article  Google Scholar 

  44. Pilastro A, Benetton S, Bisazza A (2003) Female aggregation and male competition reduce costs of sexual harassment in the mosquitofish Gambusia holbrooki. Anim Behav 65:1161–1167

    Article  Google Scholar 

  45. Pisarowicz J (2005) Return to Tabasco. Assoc Mexican Cave Stud Newslett 28:27–57

    Google Scholar 

  46. Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) Behaviour of teleost fishes, second edition. Chapman and Hall, London, pp 363–437

    Google Scholar 

  47. Pitcher TJ, Maggurran AE, Winfield I (1982) Fish in larger shoals find food faster. Behav Ecol Sociobiol 10:149–151

    Article  Google Scholar 

  48. 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 

  49. 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 

  50. 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 

  51. 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 

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

    Article  Google Scholar 

  53. Plath M, Tobler M, Riesch R, García de León FJ, Giere O, Schlupp I (2007c) Survival in an extreme habitat: the roles of behaviour and energy limitation. Naturwissenschaften (in press)

  54. Poulson TL, White WB (1969) The cave environment. Science 165:971–981

    PubMed  Article  CAS  Google Scholar 

  55. Poulson TL, Lavoie KH (2000) The trophic basis of subterranean ecosystems. In: Wilkens H, Culver DC, Humphries WF (eds) Ecosystems of the world 30: Subterranean ecosystems. Elsevier, Amsterdam, pp 231–249

    Google Scholar 

  56. Proudlove GS (2006) Subterranean fishes of the world. International Society for Subterranean Biology, Moulis, France

    Google Scholar 

  57. Pulliam HR, Caraco T (1984) Living in groups: is there an optimal group size. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Scientific, Oxford, pp 122–147

    Google Scholar 

  58. Ranta E, Rita H, Lindström K (1993) Competition versus cooperation: success of individuals foraging alone and in groups. Am Nat 142:42–58

    Article  PubMed  CAS  Google Scholar 

  59. Reebs SG, Saulnier N (1997) The effect of hunger on shoal choice in golden shiners (Pisces: Cyprinidae, Notemigonus crysoleucas). Ethology 103:642–652

    Article  Google Scholar 

  60. Riesch R, Schlupp I, Tobler M, Plath M (2006) Reduction of the association preference for conspecifics in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana. Behav Ecol Sociobiol 60:794–802

    Article  Google Scholar 

  61. Romero A, Green SM (2005) The end of regressive evolution: examining and interpreting the evidence from cave fishes. J Fish Biol 67:3–32

    Article  Google Scholar 

  62. Seghers BH (1974) Schooling behaviour in the guppy Poecilia reticulata: an evolutionary response to predation. Evolution 28:486–489

    Article  Google Scholar 

  63. Tobler M, Schlupp I (2007) Influence of black spot disease on shoaling behaviour in female western mosquitofish, Gambusia affinis (Poeciliidae, Teleostei). Environ Biol Fish (in press)

  64. Tobler M, Schlupp I, Plath M (2007a) Predation of a cavefish (Poecilia mexicana, Poeciliidae) by a giant water bug (Belostoma, Belostomatidae) in a Mexican sulfur cave. Ecol Entomol (in press)

  65. Tobler M, Riesch R, García de León FJ, Schlupp I, Plath M (2007b) A new and morphologically distinct population of cavernicolous Poecilia mexicana (Poeciliidae: Teleostei). Environ Biol Fish (in press)

  66. 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(6):577–585

    PubMed  Article  CAS  Google Scholar 

  67. Timmermann M, Schlupp I, Plath M (2004) Shoaling behaviour in a surface- and a cave-dwelling population of a barb, Garra barreimiae (Cyprinidae, Teleostei). Acta Ethol 7:59–64

    Article  Google Scholar 

  68. Walters LH, Walters VW (1965) Laboratory observations on a cavernicolous poeciliid from Tabasco, Mexico. Copeia 1965:214–233

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to the people of Tapijulapa for their hospitality during the field work preceding this study. The Mexican government (DGOPA/16988/191205/-8101) and Texas Parks and Wildlife (SPR-0305–045) kindly issued permits to collect fish. Two anonymous reviewers provided helpful comments. Financial support came from the DFG (PL 470/1–1, PL 470/1–2).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Martin Plath.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Plath, M., Schlupp, I. 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 (2008). https://doi.org/10.1007/s10641-007-9291-9

Download citation

Keywords

  • Cave fish
  • Cave molly
  • Food competition
  • Group living
  • Predator avoidance