Abstract
Most eucaryotic organisms classified as living in an extreme habitat are invertebrates. Here we report of a fish living in a Mexican cave (Cueva del Azufre) that is rich in highly toxic H2S. We compared the water chemistry and fish communities of the cave and several nearby surface streams. Our study revealed high concentrations of H2S in the cave and its outflow (El Azufre). The concentrations of H2S reach more than 300 μM inside the cave, which are acutely toxic for most fishes. In both sulfidic habitats, the diversity of fishes was heavily reduced, and Poecilia mexicana was the dominant species indicating that the presence of H2S has an all-or-none effect, permitting only few species to survive in sulfidic habitats. Compared to habitats without H2S, P. mexicana from the cave and the outflow have a significantly lower body condition. Although there are microhabitats with varying concentrations of H2S within the cave, we could not find a higher fish density in areas with lower concentrations of H2S. We discuss that P. mexicana is one of the few extremophile vertebrates. Our study supports the idea that extreme habitats lead to an impoverished species diversity.
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References
Abel DC, Koenig CC, Davis WP (1987) Emersion in the mangrove forest fish Rivulus marmoratus: a unique response to hydrogen sulfide. Environ Biol Fishes 18:67–72
Adelman IR, Smith LL Jr (1970) Effect of hydrogen sulfide on northern pike eggs and sac fry. Trans Am Fish Soc 99:501–509
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 141:275–280
Bagarinao T (1992) Sulfide as an environmental factor and toxicant: tolerance and adaptations of aquatic organisms. Aquat Toxicol 24:21–62
Bagarinao T, Lantin-Olaguer I (1999) The sulfide tolerance of milkfish and tilapia in relation to fish kills in farms and natural waters in the Philippines. Hydrobiologia 382:137–150
Bagarinao T, Vetter RD (1989) Sulfide tolerance and detoxification in shallow water marine fishes. Mar Biol 103:291–302
Bagarinao T, Vetter RD (1990) Oxidative detoxification of sulfide by mitochondria of the California killifish Fundulus parvipinnis and the speckled sanddap Citharichthys stignaeus. J Comp Physiol B 160:519–527
Barr TC, Holsinger JR (1985) Speciation in cave faunas. Annu Rev Ecol Syst 16:313–337
Begon ME, Harper JL, Townsend CR (1996) Ecology, 3rd edn. Blackwell Science, Oxford
Boston PJ, Spilde MN, Northup DE et al (2001) Cave biosignature suites: microbes, minerals, and mars. Astrobiology 1:25–55
Carrico RJ, Blumberg WE, Peisach J (1978) The reversible binding of oxygen to sulfhemoglobin. J Biol Chem 253:7212–7215
Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458
Colby PJ, Smith LL Jr (1967) Survival of walleye eggs and fry on paper fiber sludge deposits in the Rainy River, Minnesota. Trans Am Fish Soc 96:278–296
Dare MR, Hubert WA, Meyer JS (2001) Influence of stream flow on hydrogen sulfide concentrations and distributions of two trout species in a Rocky Mountains tailwater. N Am J Fish Manag 21:971–975
Geiger SP, Torres JJ, Crabtree RE (2000) Air breathing and gill ventilation frequencies in juvenile tarpon, Megalops atlanticus: responses to changes in dissolved oxygen, temperature, hydrogen sulfide, and pH. Environ Biol Fishes 59:181–190
Gordon MS, Rosen DE (1962) A cavernicolous form of the Poeciliid fish Poecilia sphenops from Tabasco, México. Copeia 360–368
Gough L, Shaver GR, Carroll J, Royer DL, Laundre JA (2000) Vascular plant species richness in Alaskan arctic tundra: the importance of soil pH. J Ecol 88:54–66
Grieshaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu Rev Physiol 60:33–53
Hochachka PW, Somero GN (1984) Biochemical adaptation. Princeton University Press, Princeton
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 Science, Amsterdam pp 159–188
Kramer DL (1987) Dissolved oxygen and fish behavior. Environ Biol Fishes 18:81–92
Kramer DL, Mehegan JP (1981) Aquatic surface respiration, an adaptive response to hypoxia in the guppy, Poecilia reticulata (Pisces: Poeciliidae). Environ Biol Fishes 6:299–313
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
Lovatt Evans C (1967) The toxicity of hydrogen sulphide and other sulphides. Q J Exp Physiol 52:231–248
Luther GW, et al (2004) The roles of anoxia, H2S, and storm events in fish kills of dead-end canals of Delaware inland bays. Estuaries 27:551–560
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton
Matthews WJ (1998) Patterns in freshwater fish ecology. Kluwer Academic Publisher, Boston
Mayland HJ (1984) Mittelamerika: Cichliden und Lebendgebärende. Landbuch, Hannover
McMullin ER, Bergquist DC, Fisher CR (2000) Metazoans in extreme environments: adaptations of hydrothermal vent and hydrocarbon fauna. Gravit Space Biol Bull 13:13–23
Miller RR (1976) Geographical distribution of Central American freshwater fishes. In: Thorson TB (eds) Investigations of the ichthyofauna of Nicaraguan Lakes—a monumental work on Nicaraguan Fishes. The school of life sciences, University of Nebraska Lincoln, Lincoln, Nebraska pp 125–155
Miller RR (2005) Freshwater fishes of Mexico. Chicago University Press, Chicago
Nicholls P (1975) The effect of sulphide on cytochrome aa3. Isosteric and allosteric shifts of the reduced alpha-peak. Biochim Biophys Acta 396:24–35
Oseid DM, Smith Jr LL (1974) Chronic toxicity of hydrogen sulfide to Gammarus pseudolimneatus. Trans Am Fish Soc 103:819–822
Parzefall J (1969) Zur vergleichenden Ethologie verschiedener Mollienesia-Arten einschliesslich einer Höhlenform von M. sphenops. Behaviour 33:1–37
Parzefall J (1993) Behavioural ecology of cave-dwelling fishes. In: Pitcher TJ (eds Behaviour of teleost fishes, 2nd edn. Chapman & Hall, London pp 573–608
Parzefall J (2001) A review of morphological and behavioural changes in the cave molly, Poecilia mexicana, from Tabasco, Mexico. Environ Biol Fishes 62:263–275
Peek AS, Feldmann RA, Lutz RA, Vrijenhoek RC (1998) Conspeciation of chemoautotrophic bacteria and deep sea clams. Proc Natl Acad Sci USA 95:9962–9966
Plath M, Körner K, Parzefall J, Schlupp I (2003a) Persistence of a visually mediated mating preference in the cave molly, Poecilia mexicana (Poeciliidae, Teleostei). Subterr Biol 1:93–97
Plath M, Parzefall J, Schlupp I (2003b) 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
Plath M, Parzefall J, Körner K, 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
Plath M, Heubel KU, García de León F, Schlupp I (2005) Cave molly females like well-fed males. Behav Ecol Sociobiol 58:144–151
Plath M, Seggel U, Burmeister H, Heubel KU, Schlupp I (2006) Choosy males from the underground: male mate choice in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae, Teleostei). Naturwissenschaften 93:103–109
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 Science, Amsterdam pp 231–249
Poulson TL, White WB (1969) The cave environment. Science 165:971–981
Price ARG (2002) Simultaneous ‘hotspots’ and ‘coldspots’ of marine biodiversity and implications for global conservation. Mar Ecol Prog Ser 241:23–27
Sarrazin J, Juniper SK (1999) Biological characteristics of a hydrothermal edifice mosaic community. Mar Ecol Prog Ser 185:1–19
Smith LL Jr, Oseid DM, Kimball GL, El-Kandelgy SM (1976) Toxicity of hydrogen sulfide to various life history stages of the bluegill (Lepomis macrochirus). Trans Am Fish Soc 105:442–449
Smith L, Kruszynah H, Smith RP (1977) The effect of methemoglobin on the inhibition of cytochrome c oxidase by cyanide, sulfide or azide. Biochem Pharmacol 26:2247–2250
Stallones RA, et al (1979) Hydrogen sulfide. University Park Press, Baltimore
Stawikowski R, Werner U (1998) Die Buntbarsche Amerikas, Band I. Eugen Ulmer, Stuttgart
Theede H (1973) Comparative studies on the influence of oxygen deficiency and hydrogen sulphide on marine bottom invertebrates. Neth J Sea Res 7:245–252
Torrans EL, Clemens HP (1982) Physiological and biochemical effects of acute exposure of fish to hydrogen sulfide. Comp Biochem Physiol 71C:183–190
Townsend CR, Begon ME, Harper JL (2003) Essentials of ecology, 2nd edn. Blackwell Publishing, Oxford
Tsurumi M (2003) Diversity at hydrothermal vents. Glob Ecol Biogeogr 12:181–190
Van Dover CL (2000) The ecology of deep-sea hydrothermal vents. Princeton University Press, Princeton
Acknowledgments
We are grateful to the people of Tapijulapa for their hospitality during our visits. J. Parzefall, M. Schartl, K.E. Körner, and D. Lamatsch provided help during our field trips. J. Parzefall furthermore provided very valuable information. L. Krumholz helped in the lab and provided the infrastructure for sulfide measurements. M. Chumchal provided information on mercury concentrations in mollies. C. Franssen and six anonymous reviewers improved previous versions of the manuscript with their valuable comments. The Mexican Government kindly issued permits to conduct this research (Permiso de pesca de fomento numbers—291002-613-1577, DGOPA/5864/260704/-2408, and DGOPA/16988/191205/-8101). Financial support came from the DFG (SCHL 344/5-3,15-1; PL 470/1-1) and the German Ichthyological Association (to M.T. and M.P.) as well as the Basler Foundation for Biological Research, the Janggen-Poehn-Foundation, the Roche Research Foundation, and the Wolfermann-Nägeli-Foundation (to M.T.). N. Tobler kindly provided the sketch of the collection sites (Fig. 1).
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Tobler, M., Schlupp, I., Heubel, K.U. et al. Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10, 577–585 (2006). https://doi.org/10.1007/s00792-006-0531-2
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DOI: https://doi.org/10.1007/s00792-006-0531-2