, Volume 94, Issue 12, pp 991–996 | Cite as

Survival in an extreme habitat: the roles of behaviour and energy limitation

  • Martin Plath
  • Michael Tobler
  • Rüdiger Riesch
  • Francisco J. García de León
  • Olav Giere
  • Ingo Schlupp
Original Paper


Extreme habitats challenge animals with highly adverse conditions, like extreme temperatures or toxic substances. In this paper, we report of a fish (Poecilia mexicana) inhabiting a limestone cave in Mexico. Several springs inside the cave are rich in toxic H2S. We demonstrate that a behavioural adaptation, aquatic surface respiration (ASR), allows for the survival of P. mexicana in this extreme, sulphidic habitat. Without the possibility to perform ASR, the survival rate of P. mexicana was low even at comparatively low H2S concentrations. Furthermore, we show that food limitation affects the survival of P. mexicana pointing to energetically costly physiological adaptations to detoxify H2S.


Aquatic surface respiration Cave fish Extremophile Hypoxia Hydrogen sulphide 



We thank L. Fromhage (Hamburg) and H.-U. Reyer (Zürich) for critically reading earlier drafts of the manuscript. D. McLennan and two anonymous reviewers provided very helpful comments. The Mexican Government kindly issued research permits (291002-613-1577, DGOPA/5864/260704/-2408 and 16986/191/205/-8101). Financial support came from the DFG (SCHL 344/15-1, PL 470/1-1, PL 470/1-2) and the University of Oklahoma as well as the German Ichthyological Association (to M.T. and M.P.), the Basler Foundation for Biological Research, the Janggen-Poehn-Foundation, the Roche Research Foundation and the Wolfermann-Nägeli-Foundation (to M.T.). We are deeply indebted to the people of Tapijulapa for their hospitality, especially the hotel Maison de la Sierra.


  1. Affonso EG, Rantin FT (2005) Respiratory responses of the air-breathing fish Hoplosternum littorale to hypoxia and hydrogen-sulfide. Comp Biochem Physiol C Toxicol Pharmacol 141:275–280PubMedCrossRefGoogle Scholar
  2. Bagarinao T (1992) Sulfide as an environmental factor and toxicant—tolerance and adaptations in aquatic organisms. Aquat Toxicol 24:21–62CrossRefGoogle Scholar
  3. Bagarinao T, Vetter RD (1989) Sulphide tolerance and detoxification in shallow-water marine fishes. Mar Biol 103:291–302CrossRefGoogle Scholar
  4. Brauner CJ, Ballantyne CL, Randall DJ, Val AL (1995) Air breathing in the armoured catfish (Hoplosternum littorale) as an adaptation to hypoxic, acidic, and hydrogen sulphide rich waters. Can J Zool 73:739–744CrossRefGoogle Scholar
  5. Chapman LJ, Chapman CA (1993) Desiccation, flooding and the behavior of Poecilia gilii (Pisces: Poeciliidae). Ichthyol Explor Freshw 4:279–287Google Scholar
  6. Chapman LJ, Kaufman LS, Chapman CA, McKenzie FE (1995) Hypoxia tolerance in twelve species of East African cichlids: potential for low oxygen refugia in Lake Victoria. Conserv Biol 9:1274–1288CrossRefGoogle Scholar
  7. Gordon MS, Rosen DE (1962) A cavernicolous form of the Poeciliid fish Poecilia sphenops from Tabasco, México. Copeia 1962:360–368CrossRefGoogle Scholar
  8. Grieshaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulphide. Ann Rev Physiol 60:33–53CrossRefGoogle Scholar
  9. Jorgensen BB (1984) The microbial sulfur cycle. In: Krumbein, W (eds) Microbial geochemistry. Blackwell, Oxford, pp 91–124Google Scholar
  10. Kramer DL (1983) The evolutionary ecology of respiratory mode in fishes: an analysis based on the cost of breathing. Environ Biol Fish 9:145–158CrossRefGoogle Scholar
  11. Kramer DL, McClure M (1982) Aquatic surface respiration, a widespread adaptation to hypoxia in tropical freshwater fishes. Environ Biol Fish 7:47–55CrossRefGoogle Scholar
  12. Kramer DL, Mehegan JP (1981) Aquatic surface respiration, an adaptive response to hypoxia in the guppy, Poecilia reticulata (Pisces, Poeciliidae). Environ Biol Fish 6:299–313CrossRefGoogle Scholar
  13. 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 23:121–125Google Scholar
  14. McMullin ER, Bergquist DC, Fisher CR (2000) Metazoans in extreme environments: adaptations of hydrothermal vent and hydrocarbon fauna. Gravit Space Biol Bull 13:13–23PubMedGoogle Scholar
  15. Parzefall J (2001) A review of morphological and behavioural changes in the cave molly, Poecilia mexicana, from Tabasco, Mexico. Environ Biol Fish 62:263–275CrossRefGoogle Scholar
  16. 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 54:303–309CrossRefGoogle Scholar
  17. 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
  18. Plath M, Hauswaldt JS, Moll K, Tobler M, García de León FJ, Schlupp I, Tiedemann R (2007) Local adaptation and pronounced genetic differentiation in an extremophile fish, Poecilia mexicana, inhabiting a Mexican cave with toxic hydrogen sulfide. Mol Ecol 16:967–976PubMedCrossRefGoogle Scholar
  19. 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
  20. Sarbu SM, Kane TC, Kinkle BK (1996) A chemoautotrophically based cave ecosystem. Science 272:1953–1955PubMedCrossRefGoogle Scholar
  21. Smith LL, Oseid DM, Adelmann IR, Broderius SJ (1976) Effect of hydrogen sulphide on fish and invertebrates. Part I: acute and chronic toxicity studies. Ecol Res Ser EPA-600/3-76-062a:1–109Google Scholar
  22. Timmerman CM, Chapman LJ (2003) The effect of gestational state on oxygen consumption and response to hypoxia in the sailfin molly (Poecilia latipinna). Environ Biol Fish 68:293–299CrossRefGoogle Scholar
  23. Timmerman CM, Chapman LJ (2004a) Behavioral and physiological compensation for chronic hypoxia in the live-bearing sailfin molly (Poecilia latipinna). Physiol Biochem Zool 77:601–610CrossRefGoogle Scholar
  24. Timmerman CM, Chapman LJ (2004b) Hypoxia and interdemic variation in Poecilia latipinna. J Fish Biol 65:635–650CrossRefGoogle Scholar
  25. Tobler M, Schlupp I, Heubel KU, Riesch R, García de León FJ, Giere O, Plath M (2006) Life on the edge: Hydrogen sulphide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10:577–585PubMedCrossRefGoogle Scholar
  26. Torrans EL, Clemens HP (1982) Physiological and biochemical effects of acute exposure of fish to hydrogen sulphide. Comp Biochem Physiol C 71:183–190PubMedCrossRefGoogle Scholar
  27. Townsend CR, Begon ME, Harper JL (2003) Essentials of ecology, 2nd edn. Blackwell, OxfordGoogle Scholar
  28. Van Dover CL (2000) The ecology of deep-sea hydrothermal vents. Princeton Univ. Press, PrincetonGoogle Scholar
  29. Weber JM, Kramer DL (1983) Effects of hypoxia and surface access on growth, mortality and behavior of juvenile guppies Poecilia reticulata. Can J Fish Aqua Sci 40:1583–1588Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Martin Plath
    • 1
    • 2
    • 5
  • Michael Tobler
    • 3
    • 5
  • Rüdiger Riesch
    • 2
    • 5
  • Francisco J. García de León
    • 4
  • Olav Giere
    • 2
  • Ingo Schlupp
    • 2
    • 3
    • 5
  1. 1.Unit of Evolutionary Biology and Systematic Zoology, Institute of Biochemistry and BiologyUniversity of PotsdamPotsdamGermany
  2. 2.University of Hamburg, Biozentrum GrindelHamburgGermany
  3. 3.Universität Zürich, Zoologisches InstitutZürichSwitzerland
  4. 4.Centro de Investigaciones Biológicas del NoroesteBaja California SurMéxico
  5. 5.Department of ZoologyUniversity of OklahomaNormanUSA

Personalised recommendations