Aquatic Ecology

, Volume 43, Issue 2, pp 539–547 | Cite as

Phototactic response and light sensitivity in an epigean and a hypogean population of a barb (Garra barreimiae, Cyprinidae)

Article

Abstract

We investigated the response of two populations of the barb Garra barreimiae to different light intensities (0.5–2000 lx) from a light source. Adults of both the surface (epigean) and cave (hypogean) G. barreimiae populations show photophobic behavior. A photophobic response in the cave form was seen only at higher light intensities because the cavefish are eyeless and rely on extra-retinal light receptors to detect light. In contrast, juveniles (surface and cave) showed photophilic behavior, and their preference for the photic zone of the test tank decreased with increasing age. We discuss the potential role played by photophobic behavior for the colonization of caves by previously surface-dwelling fishes.

Keywords

Cave colonization Cavefish Oman Phototaxis Scotophilia 

References

  1. Banister KE (1984) A subterranean population of Garra barreimiae (Teleostei: Cyprinidae) from Oman, with comments on the concept of regressive evolution. J Nat Hist 18:927–938CrossRefGoogle Scholar
  2. Banister KE (1987) Two new species of Garra (Teleostei-Cyprinidae) from the Arabian peninsula. Bull Br Mus Nat Hist (Zool) 52:59–70Google Scholar
  3. Banister KE (1992) Blind cave fishes. Aqua Geogr 2:65–73Google Scholar
  4. Barr TC (1968) Cave ecology and the evolution of troglobites. Evol Biol 2:35–102Google Scholar
  5. Barr TC, Holsinger JR (1985) Speciation in cave faunas. Annu Rev Ecol Syst 16:313–337CrossRefGoogle Scholar
  6. Breder CM, Rasquin P (1947) Comparative studies on the light sensitivity of blind characins from a series of Mexican caves. Bull Am Mus Nat Hist 89:325–351Google Scholar
  7. Büttiker W, Krupp F (1989) Fauna eines Sandmeeres—Zoologische Untersuchung in der Wahiba–Wüste, Oman. Natur Mus 119:241–261Google Scholar
  8. Camassa MM (2001) Responses to light in epigean and hypogean populations of Gambusia affinis (Cyprinodontiformes: Poeciliidae). Environ Biol Fish 62:115–118CrossRefGoogle Scholar
  9. Ercolini A, Berti R (1975) Light sensitivity experiments and morphology studies of the blind phreatic fish Phreatichthys andruzzii Vinciguerra from Somalia. Monit Zool Ital 6:29–43Google Scholar
  10. Ercolini A, Berti R (1978) Morphology and response to light of Barbopsis devecchii Caporiacco (Cyprinidae), microphthalmic phreatic fish from Somalia. Monit Zool Ital 10:299–314Google Scholar
  11. Feulner G (1998) Wadi fish of the UAE. Tribulus 8:16–22Google Scholar
  12. Fowler HW, Steinitz H (1956) Fishes from Cyprus, Iran, Iraq, Israel and Oman. Bull Res Counc Isr 5B:260–292Google Scholar
  13. Gertychowa R (1970) Studies on the ethology and space orientation of the blind cavefish Anoptichthys jordani Hubbs and Innes 1936 (Characidae). Fol Biol 18:9–69Google Scholar
  14. Hafeez MA, Quay WB (1970) The role of the pineal organ in the control of phototaxis and body coloration in rainbow trout (Salmo gairdneri, Richardson). J Comp Physiol A 68:403–416Google Scholar
  15. Hüppop K (1986) Oxygen consumption of Astyanax fasciatus (Characidae, Pisces): a comparison of epigean and hypogean populations. Environ Biol Fish 17:299–308CrossRefGoogle Scholar
  16. Hüppop K (1988) Phänomene und Bedeutung der Energieersparnis beim Höhlensalmler Astyanax fasciatus. PhD thesis. University of Hamburg, HamburgGoogle Scholar
  17. 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 159–188Google Scholar
  18. Jeffery WR (2001) Cavefish as a model system in evolutionary and developmental biology. Dev Biol 231:1–12PubMedCrossRefGoogle Scholar
  19. Jeffery WR (2005) Adaptive evolution of eye degeneration in the Mexican blind cavefish. J Hered 96:185–196PubMedCrossRefGoogle Scholar
  20. Kane TC, Richardson RC (1985) Regressive evolution: a historical perspective. Nat Speleol Soc Bull 47:71–77Google Scholar
  21. Kosswig C (1960) Zur Phylogenese sogenannter Anpassungsmerkmale bei Höhlentieren. Int Rev Ges Hydrobiol 45:493–512Google Scholar
  22. Krupp F, Schneider W (1988) Die Süßwasserfauna des Vorderen Orients. Anpassungsstrategien und Besiedlungsgeschichte einer zoogeographischen Übergangszone. Nat Mus 118:193–212Google Scholar
  23. Langecker TG (1989) Studies on the light reaction of epigean and cave populations of Astyanax fasciatus (Characidae, Pisces). Mem Biospeol 16:169–176Google Scholar
  24. Langecker TG (1990) Der Einfluss des Lichts bei der Evolution von Höhlenfischen. PhD thesis. University of Hamburg, HamburgGoogle Scholar
  25. Langecker TG (1992) Light sensitivity of cave vertebrates—behavioral and morphological aspects. In: Camachio AI (ed) The natural history of Biospeleology. Monografias del Museo Nacional de Ciencias Naturales, Madrid, pp 295–326Google Scholar
  26. Ludwig W (1942) Zur evolutorischen Erklärung der Höhlentiermerkmale durch Allelelimination. Biol Zentralbl 62:447–482Google Scholar
  27. Lüling KH (1954) Untersuchungen am Blindfisch Anoptichthys jordani Hubbs & Innes (Characidae). II. Beobachtungen und Experimente an Anoptichthys jordani zur Prüfung der Einstellung zum Futter, zum Licht und zur Wasserturbulenz. Zool Jahrb Abt Zool Physiol 65:9–42Google Scholar
  28. McCauley DW, Hixon E, Jeffery WR (2004) Evolution of pigment cell regression in the cavefish Astyanax: a late step in melanogenesis. Evol Dev 6:209–218PubMedCrossRefGoogle Scholar
  29. Mitchell RW, Russell WH, Elliott WR (1977) Mexican eyeless characin fishes, genus Astyanax: Environment, distribution and evolution. Spec Publ Mus Tex Tech Univ 12:1–89Google Scholar
  30. Parzefall J (1993) Behavioural ecology of cave-dwelling fishes. In: Pitcher TJ (ed) Behaviour of teleost fishes, 2nd edn. Chapman & Hall, London, pp 573–608Google Scholar
  31. Parzefall J, Kraus C, Tobler M, Plath M (2007) Photophilic behaviour in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae). J Fish Biol 71:1225–1231CrossRefGoogle Scholar
  32. Pati AK (2007) Circadian rhythms in hypogean fishes with special reference to the cave loach, Nemacheilus evezardi. In: Sébert P, Onyango DW, Kapoor BG (eds) Fish life in special environments. Science Publishers, Enfield, pp 83–130Google Scholar
  33. Pati AK, Agrawal A (2002) Studies on the behavioural ecology and physiology of a hypogean loach, Nemacheilus evezardi, from the Kotsumsar Cave, India. Curr Sci 83:1112–1116Google Scholar
  34. 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 16:967–976PubMedCrossRefGoogle Scholar
  35. Plath M, Tobler M, Riesch R, García de León FJ, Giere O, Schlupp I (2007b) Survival in an extreme habitat: the roles of behaviour and energy limitation. Naturwissenschaften 94:991–996PubMedCrossRefGoogle Scholar
  36. Poulson TL (1963) Cave adaptation in amblyopsid fishes. Am Midl Nat 70:257–290CrossRefGoogle Scholar
  37. Poulson TL (1964) Animals in aquatic environments: animals in caves. In: Bill DB (ed) Handbook of physiology, section 4: adaptation to the environment. Williams & Wilkins, Baltimore, pp 749–771Google Scholar
  38. 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 231–249Google Scholar
  39. Poulson TL, White WB (1969) The cave environment. Science 165:971–981PubMedCrossRefGoogle Scholar
  40. Pradhan RK, Pati AK, Agarwal SM (1989) Meal scheduling modulation of circadian rhythm of phototactic behaviour in cave dwelling fish. Chronobiol Int 6:245–249PubMedCrossRefGoogle Scholar
  41. Proudlove GS (2006) Subterranean fishes of the world. International Society for Subterranean Biology, MoulisGoogle Scholar
  42. Romero A (1985) Ontogenetic change in phototactic responses of surface and cave populations of Astyanax fasciatus (Pisces: Characidae). Copeia 1985:1004–1011CrossRefGoogle Scholar
  43. Romero A, Green SM (2005) The end of regressive evolution: examining and interpreting the evidence from cavefishes. J Fish Biol 67:3–32CrossRefGoogle Scholar
  44. Steven DM (1963) The dermal light sense. Biol Rev 38:204–240PubMedCrossRefGoogle Scholar
  45. Strecker U, Bernatchez L, Wilkens H (2003) Genetic divergence between cave and surface populations of Astyanax in Mexico (Characidae, Teleostei). Mol Ecol 12:699–710PubMedCrossRefGoogle Scholar
  46. Tabata M, Minh-Nyo M, Oguri M (1989) Thresholds of retinal and extraretinal photoreceptors measured by photobehavioral response in catfish, Silurus asotus. J Comp Physiol A 164:797–803CrossRefGoogle Scholar
  47. Thinès G (1954) Etude comparative de la photosensibilité des poissons aveugles Caecobarbus geertsii Boulenger et Anoptichthys jordani Hubbs and Innes. Ann Soc R Zool Belg 85:35–58Google Scholar
  48. Thinès G (1958) Beobachtungen über die Phototaxis und die Thermotaxis des blinden Höhlenfisches Caecobarbus geertsii (Cyprinidae). Experientia 14:381PubMedCrossRefGoogle Scholar
  49. Thinès G, Kähling J (1957) Beobachtungen über die Farbempfindlichkeit des Höhlenfisches Anoptichthys jordani Hubbs and Innes (Characidae). Z Biol 109:150–160PubMedGoogle Scholar
  50. 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 7:59–64CrossRefGoogle Scholar
  51. 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 10:577–585PubMedCrossRefGoogle Scholar
  52. Tobler M, Schlupp I, García de León FJ, Glaubrecht M, Plath M (2007) Extreme habitats as refuge from parasite infections? Evidence from an extremophile fish. Acta Oecol 31:270–275CrossRefGoogle Scholar
  53. Underwood H, Groos G (1982) Vertebrate circadian rhythms: retinal and extraretinal photoreception. Experientia 38:1013–1021PubMedCrossRefGoogle Scholar
  54. Vawter AT, Fong DW, Culver DC (1987) Negative phototaxis in surface and cave populations of the amphipod Gammarus minus. Stygologia 3:83–88Google Scholar
  55. Waltham A, Brown RD, Middleton TC (1985) Karst and caves in the Jabal Akhdar, Oman. Cave Sci 12:69–79Google Scholar
  56. Weber A, Proudlove GS, Parzefall J, Wilkens H, Nalbant TT (1998) Morphology, systematic diversity, distribution and ecology of stygobitic fishes. In: Juberthie C, Decu V (eds) Encyclopaedia Biospeologica, vol 2. Société de Biospéologie, Moulis, Bucarest, pp 835–1373Google Scholar
  57. Weissenbacher A, Sattmann H, Christ M, Scattolin G, Ahnelt H (2002) Auf der Spur der blinden Höhlenfische. Aquaristik-Fachmagazin 34:66–72Google Scholar
  58. Wilkens H (1988) Evolution and genetics of epigean and cave Astyanax fasciatus (Characidae, Pisces). Evol Biol 23:271–367Google Scholar
  59. Wilkens H (2001) Convergent adaptations to cave life in the Rhamdia laticauda catfish group (Pimelodidae, Teleostei). Environ Biol Fish 62:251–261CrossRefGoogle Scholar
  60. 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
  61. Yoshizawa M, Jeffery WR (2008) Shadow response in the blind cavefish Astyanax reveals conservation of a functional pineal eye. J Exp Biol 211:292–299PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Biozentrum Grindel und Zoologisches Museum der Universität HamburgHamburgGermany
  2. 2.Department of ZoologyUniversity of OklahomaNormanUSA
  3. 3.Unit of Evolutionary Biology and Systematic Zoology, Institute of Biochemistry and BiologyUniversity of PotsdamPotsdamGermany
  4. 4.Unit of Animal Ecology, Institute of Biochemistry and BiologyUniversity of PotsdamPotsdamGermany

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