Aquatic Ecology

, Volume 42, Issue 4, pp 685–692

Sperm production in an extremophile fish, the cave molly (Poecilia mexicana, Poeciliidae, Teleostei)

  • Courtney M. Franssen
  • Michael Tobler
  • Rüdiger Riesch
  • Francisco J. García de León
  • Ralph Tiedemann
  • Ingo Schlupp
  • Martin Plath
Article

Abstract

A prominent trade-off in life history theory and evolution balances the costs of reproduction with those of basic somatic needs. Hence, reproductive efforts may be reduced in environments where additional energy is required for somatic maintenance. Here, we investigated male sperm stores in Atlantic mollies (Poecilia mexicana) from a sulfidic cave and several sulfidic and non-sulfidic surface habitats. We found significant differences among populations in the number of sperm stripped per male, which was also correlated with differences in gonad weights. The largest sperm stores were detected in males from non-sulfidic surface creeks, while males from a partially sulfidic surface system had lower sperm counts, and males from completely sulfidic systems, surface as well as subterranean, had even fewer available sperm. We conclude that the extreme environmental conditions in sulfidic habitats appear to constrain male sperm production, since hydrogen sulfide as a naturally occurring toxin requires energy-demanding adaptations. Furthermore, we examined sperm counts of lab-reared cave and surface mollies in response to energy limitation. Males from stock populations were placed under high and low food treatments for a 2-week period and then stripped of sperm. Sperm counts of surface mollies tended to be reduced by low food availability, whereas sperm counts of cave mollies did not significantly vary between food treatments, which likely points towards a higher starvation resistance in cave mollies.

Keywords

Cave fish Energy limitation Hydrogen sulfide Spermatogenesis Testes weight 

References

  1. Aspbury AS, Gabor CR (2004) Differential sperm priming by male sailfin mollies (Poecilia latipinna): effects of female and male size. Ethology 110:193–202CrossRefGoogle Scholar
  2. Bagarinao T (1992) Sulfide as an environmental factor and toxicant: tolerance and adaptations of aquatic organisms. Aquat Toxicol 24:21–62CrossRefGoogle Scholar
  3. Bagarinao T, Vetter RD (1989) Sulfide tolerance and detoxification in shallow water marine fishes. Mar Biol 103:291–302CrossRefGoogle Scholar
  4. Bagarinao T, Vetter R (1990) Oxidative detoxification of sulfide by mitochrondria of the California killifish Fundulus parvipinnis and the speckled sanddap Citharichthys stignaeus. J Comp Physiol B 160:519–527CrossRefGoogle Scholar
  5. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368PubMedCrossRefGoogle Scholar
  6. Bell G, Koufopanou V (1986) The cost of reproduction. In: Dawkins R, Ridley M (eds) Oxford surveys in evolutionary biology, vol 3. Oxford University Press, Oxford, pp 83–131Google Scholar
  7. Birkhead TR (1991) Sperm depletion in the Bengalese finch, Lonchura striata. Behav Ecol 2(4):267–275CrossRefGoogle Scholar
  8. Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic Press, LondonGoogle Scholar
  9. Bozynski CC, Liley NR (2003) The effect of female presence on spermiation, and of male sexual activity on ‘ready’ sperm in the male guppy. Anim Behav 65:53–58CrossRefGoogle Scholar
  10. Carrico RJ, Blumberg WE, Peisach J (1978) The reversible binding of oxygen to sulfhemoglobin. J Biol Chem 253:7212–7215PubMedGoogle Scholar
  11. Celentano E, Defeo O (2006) Habitat harshness and morphodynamics: life history traits of the mole crab Emerita brasiliensis in Uruguayan sandy beaches. Mar Biol 149:1453–1461CrossRefGoogle Scholar
  12. Evans CL (1967) The toxicity of hydrogen sulphide and other sulphides. Quart J Exp Physiol 52:231–248PubMedGoogle Scholar
  13. Gordon MS, Rosen DE (1962) A cavernicolous form of the poeciliid fish Poecilia sphenops from Tabasco, Mexico. Copeia 1962:360–368CrossRefGoogle Scholar
  14. Grieshaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu Rev Physiol 60:33–53PubMedCrossRefGoogle Scholar
  15. Hervant F, Mathieu J, Durand J (2001) Behavioural physiological and metabolic responses to long-term starvation and refeeding in a blind cave-dwelling (Proteus anguinus) and surface-dwelling (Euproctus asper) salamander. J Exp Biol 204:269–281PubMedGoogle Scholar
  16. 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, vol 30: subterranean ecosystems. Elsevier, Amsterdam, pp 159–188Google Scholar
  17. Kramer DL (1987) Dissolved oxygen and fish behavior. Environ Biol Fish 18:81–92CrossRefGoogle Scholar
  18. 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
  19. McMullin E, Bergquist D, Fisher C (2000) Metazoans in extreme environments: adaptations of hydrothermal vent and hydrocarbon fauna. Grav Space Biol Bull 13:13–23Google Scholar
  20. Nakatsuru K, Kramer DL (1982) Is sperm cheap? Limited male-fertility and female choice in the lemon tetra (Pisces, Characidae). Science 216:753–755PubMedCrossRefGoogle Scholar
  21. Nicholls P (1975) The effect of sulphide on cytochrome aa3. Isosteric and allosteric shifts of the reduced alpha-peak. Biochim Biophys Acta 396:24–35PubMedCrossRefGoogle Scholar
  22. 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
  23. 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
  24. 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 55:596–601CrossRefGoogle Scholar
  25. 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 58:144–151CrossRefGoogle Scholar
  26. Plath M, Seggel U, Burmeister H, Heubel KU, Schlupp I (2006a) Choosy males from the underground: male mate choice in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae, Teleostei). Naturwissenschaften 93:103–109PubMedCrossRefGoogle Scholar
  27. Plath M, Brümmer A, Parzefall J, Schlupp I (2006b) Size-dependent male mating behaviour and sexual harassment in a population of Atlantic mollies (Poecilia mexicana) from a sulphur creek. Acta Etholog 9:15–21CrossRefGoogle Scholar
  28. 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 sulphide. Mol Ecol 16:967–976PubMedCrossRefGoogle Scholar
  29. Plath M, Tobler M, Riesch R, García de León FJ, Giere O, Schlupp I (in press) Survival in an extreme habitat: the role of behaviour and energy limitation. NaturwissenschaftenGoogle Scholar
  30. Poulson TL (1963) Cave adaptations in Amblyopsid fishes. Am Mid Nat 79:257–290CrossRefGoogle Scholar
  31. Schlupp I, Plath M (2005) Male mate choice and sperm allocation in a sexual/asexual mating complex of Poecilia (Poeciliidae, Teleostei). Biol Lett 1:169–171PubMedCrossRefGoogle Scholar
  32. Sibly RM, Calow P (1989) A life-cycle theory of responses to stress. Biol J Linn Soc 37:101–116CrossRefGoogle Scholar
  33. Smith C, Reichard M (2005) Females solicit sneakers to improve fertilization success in the bitterling fish (Rhodeus sericeus). Proc Roy Soc Lond B: Biol Sci 272:1683–1688CrossRefGoogle Scholar
  34. Smith Jr LL, 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 105:442–449CrossRefGoogle Scholar
  35. 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 26:2247–2250PubMedCrossRefGoogle Scholar
  36. Stallones RA et al (1979) Hydrogen sulfide. University Park Press, BaltimoreGoogle Scholar
  37. Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268CrossRefGoogle Scholar
  38. Theede H (1973) Comparative studies on the influence of oxygen deficiency and hydrogen sulphide on marine bottom invertebrates. Neth J Sea Res 7:245–252Google Scholar
  39. Tobler M, Schlupp I, Heubel KU, Riesch R, García de León FJ, Giere O, Plath M (2006) Hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10:577–585PubMedCrossRefGoogle Scholar
  40. Toft G, Guillette LJ (2005) Decreased sperm count and sexual behavior in mosquitofish exposed to water from a pesticide-contaminated lake. Ecotoxicol Environ Safety 60(1):15–20PubMedCrossRefGoogle Scholar
  41. Townsend CR, Begon ME, Harper JL (2003) Essentials of ecology, 2nd edn. Blackwell Publishing, OxfordGoogle Scholar
  42. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine Publishing Company, Chicago, USA, pp 136–179Google Scholar
  43. 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
  44. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17(7):313–320CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Courtney M. Franssen
    • 1
  • Michael Tobler
    • 1
    • 2
  • Rüdiger Riesch
    • 1
  • Francisco J. García de León
    • 3
  • Ralph Tiedemann
    • 4
  • Ingo Schlupp
    • 1
  • Martin Plath
    • 1
    • 4
  1. 1.Department of ZoologyUniversity of OklahomaNormanUSA
  2. 2.Zoologisches InstitutUniversität ZürichZurichSwitzerland
  3. 3.Centro de Investigaciones Biológicas del Noroeste, S.CLa PazMexico
  4. 4.Unit of Evolutionary Biology and Systematic Zoology, Institute of Biochemistry and BiologyUniversity of PotsdamPotsdamGermany

Personalised recommendations