Advertisement

Environmental Biology of Fishes

, Volume 59, Issue 3, pp 309–317 | Cite as

Age, Growth, and Sexual Development in the Self-fertilizing Hermaphroditic Fish Rivulus marmoratus

  • Yoshitaka Sakakura
  • David L. G. Noakes
Article

Abstract

We studied age, growth, and sexual development in the early life intervals of the self-fertilizing mangrove killi-fish, Rivulus marmoratus. Newly hatched (day 0) individuals had sagittal otoliths of 60 μm radius, with about 30 increments. Sequential sampling until about day 60 after hatching yielded otoliths with the number of increments outside the 60 μm radius equal to the daily age of the fish. Alizarin complexone marking of otoliths also confirmed the increments were daily, and demonstrated the applicability of this technique to field studies for capture-mark-recapture, or age and growth estimates. Individuals fed a restricted amount of food formed fewer daily otolith growth increments than fish fed to satiation each day. Using histological analysis for identifying gonad morphogenesis, we found no correlation between gonadal development and external appearance (caudal ocellus, orange fin colouration) in young fish of known ages. The caudal ocellus was not present until 9 mm total length, and developed thereafter. Of 136 individuals examined, fish less than 17.2 mm total length (TL, n = 124) were females. Testicular tissue first appeared among individuals 17–18 mm TL (n = 3), while some individuals greater than 18 mm TL (n = 8) were functional hermaphrodites. The single male in our study was relatively of small body size (9.6 mm, day 37) with a distinct caudal ocellus, indicating that it is presumably a primary male.

mangrove killifish gonads histology otolith colouration 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Abel, D.C., C.C. Koenig & W.P. Davis. 1987. Emersion in the mangrove forest fish Rivulus marmoratus: a unique response to hydrogen sulfide. Env. Biol. Fish. 18: 67–72.Google Scholar
  2. Ali, M.A., M.A. Klyne, E.H. Park & S.H. Lee. 1988. Structural changes in retinal pigmented epithelium of Rivulus marmoratus Poey embryos during development. Anatom. Embryol. 177: 451–458.Google Scholar
  3. Campana, S.E. 1983. Feeding periodicity and the production of daily growth increments in otoliths of steelhead trout (Salmo gairdneri) and starry flounder (Paralichthys stellatus). Can. J. Zool. 61: 1591–1597.Google Scholar
  4. Campana, S.E. & J.D. Neilson. 1985. Microstructure of fish otoliths. Can. J. Fish. Aquat. Sci. 42: 1014–1032.Google Scholar
  5. Cole, K.S. & D.L.G. Noakes. 1997. Gonadal development and sexual allocation in mangrove killifish, Rivulus marmoratus (Pisces: Atherinomorpha). Copeia 1997: 596–600.Google Scholar
  6. Couch, J.A. 1995. Invading and metastasizing cardiac hemangioendothelial neoplasms in a cohort of the fish Rivulus marmoratus: unusually high prevalence, histopathology, and possible etiologies. Cancer Res. 55: 2438–2447.Google Scholar
  7. Davis, W.P. 1988. Reproductive and developmental responses in the self-fertilizing fish, Rivulus marmoratus, induced by the plasticizer, di-n-butylphthalate. Env. Biol. Fish. 21: 81–90.Google Scholar
  8. Davis, W.P., D.S. Taylor & B.J. Turner. 1990. Field observations of the ecology and habits of mangrove rivulus (Rivulus marmoratus) in Belize and Florida. Ichthyol. Explor. Freshwater 1: 123–134.Google Scholar
  9. Green, R.F. & D.L.G. Noakes. 1995. Is a little bit of sex as good as a lot? J. Theoret. Biol. 174: 87–96.Google Scholar
  10. Harrington Jr., R.W. 1961. Oviparous hermaphroditic fish with internal self-fertilization. Science 134: 1749–1750.Google Scholar
  11. Harrington Jr., R.W. 1967. Environmentally controlled induction of primary male gonochrists from eggs of the self-fertilizing hermaphroditic fish, Rivulus marmoratus Poey. Biol. Bull. 132: 174–199.Google Scholar
  12. Harrington Jr., R.W. 1968. Delimitation of the thermolabile phenocritical period of sex determination and differentiation in the ontogeny of the normally hermaphroditic fish Rivulus marmoratus Poey. Physiological Zoology 41: 447–460.Google Scholar
  13. Harrington Jr., R.W. 1971. How ecological and genetic factors interact to determine when self-fertilizing hermaphrodites of Rivulus marmoratus change into functional secondary males, with reappraisal of the models of intersexuality among fishes. Copeia 1971: 339–432.Google Scholar
  14. Harrington Jr., R.W. 1975. Sex determination and differentiation among uniparental homozygotes of the hermaphroditic fish Rivulus marmoratus (Cyprinodontidae: Atheriniformes). pp. 249–262. In: R. Reinboth (ed.) Intersexuality in the Animal Kingdom, Springer Verlag, New York.Google Scholar
  15. Harrington Jr., R.W. & K.D. Kallman. 1968. The homozygosity of clones of the self-fertilizing hermaphroditic fish, Rivulus marmoratus Poey (Cyprinodontidae, Atheriniformes). Amer. Nat. 102: 337–343.Google Scholar
  16. Harrington Jr., R.W. & L.R. Rivas. 1958. The discovery in Florida of the cyprinodont fish, Rivulus marmoratus, with a redescription and ecological notes. Copeia 1958: 125–130.Google Scholar
  17. Keene, J.L., D.L.G. Noakes, R.D. Moccia & C.G. Soto. 1998. The efficiency of clove oil as an anaesthetic for rainbow trout, Oncorhynchus mykiss (Walbaum). Aquacult. Res. 29: 89–101.Google Scholar
  18. King, J.A.C., D.C. Abel, D.R. Dibona & J.L.C. Ashcraft. 1988. Effects of salinity on chloride cell ultrastructure and density in the euryhaline cyprinodontid fish Rivulus marmoratus. Amer. Zool. 28: 100A.Google Scholar
  19. King, J.A.C., D.C. Abel & D.R. Dibona. 1989. Effects of salinity on chloride cells in the euryhaline cyprinodontid fish Rivulus marmoratus. Cell Tiss. Res. 257: 367–378.Google Scholar
  20. Koenig, C.C. & M.P. Chasar. 1984. Usefulness of the hermaphroditic marine fish, Rinlus marmoratus, in carcinogenicity testing. Nat. Cancer Inst. Monogr. 65: 15–33.Google Scholar
  21. Lin, H.C. & W.A. Dunson. 1993. The effect of salinity on the acute toxicity of cadmium to the tropical, estuarine, hermaphroditic fish, Rivulus marmoratus: a comparison of cadmium, copper, and zinc tolerance with Fundulus heteroclitus. Arch. Env. Contami. Toxicol. 25: 41–47.Google Scholar
  22. Lubinski, B.A., W.P. Davis, D.S. Taylor & B.J. Turner. 1995. Outcrossing in a natural population of a self-fertilizing hermaphroditic fish. J. Hered. 86: 469–473.Google Scholar
  23. Masuda, R. & K. Tsukamoto. 1998. The ontogeny of schooling behaviour in the striped jack. J. Fish Biol. 52: 483–493.Google Scholar
  24. Masuda, R., T. Takeuchi, K. Tsukamoto, Y. Ishizaki, M. Kanematsu & K. Imaizumi. 1998. Critical involvement of dietary docosahexaenoic acid in the ontogeny of schooling behavior in the yellowtail. J. Fish Biol. 53: 471–484.Google Scholar
  25. Molony, B.W. 1996. Episodes of starvation are recorded in the otoliths of juvenile Ambassis vachelli (Chandidae), a tropical estuarine fish. Mar. Biol. 125: 439–446.Google Scholar
  26. Mugiya, Y. 1987. Effects of photoperiods on the formation of otolith increments in the embryonic and larval rainbow trout Salmo gairdneri. Bull. Japan. Soc. Sci. Fish. 53: 1979–1984.Google Scholar
  27. Noakes, D.L.G. & J.-G.J. Godin. 1988. Ontogeny of behavior and concurrent developmental changes in sensory systems in teleost fishes. pp. 345–395. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Volume XI, Part B, Academic Press, San Diego.Google Scholar
  28. Park, E.H. & D.S. Kim. 1984. Hepatocarcinogenicity of diethylnitrosamine to the self-fertilizing hermaphroditic fish Rivulus marmoratus (Teleostomi: Cyprinodontidae). J. Nat. Cancer Inst. (Japan) 73: 871–876.Google Scholar
  29. Park, E.H. & S.H. Lee. 1988. Scale growth and squamation chronology for the laboratory-reared hermaphroditic fish Rivulus marmoratus (Cyprinodontidae). Japan. J. Ichthyol. 34: 476–482.Google Scholar
  30. Park, E.H., H.H. Chang, W.N. Joo, H.S. Chung & H.S. Kwak. 1994. Assessment of the estuarine hermaphroditic fish Rivulus marmoratus as a useful euryhaline species for acute toxicity tests as shown using cadmium. Can. J. Fish. Aquat. Sci. 51: 280–285.Google Scholar
  31. Payan, P., G. Borelli, G. Boeuf & N. Mayer-Gostan. 1998. Relationship between otolith and somatic growth: consequence of starvation on acid-base balance in plasma and endolymph in the rainbow trout Oncorhynchus mykiss. Fish Physiol. Biochem. 19: 35–41.Google Scholar
  32. Radtke, R.L. & J.M. Dean. 1982. Increment formation in the otoliths of embryos, larvae, and juveniles of the mummichog, Fundulus heteroclitus. U.S. Fish. Bull. 80: 201–215.Google Scholar
  33. Ritchie, S.A. & W.P. Davis. 1986. Evidence for embryonic diapause in Rivulus marmoratus: laboratory and field observations. J. Amer. Killifish Ass. 19: 103–108.Google Scholar
  34. Sakakura, Y. & K. Tsukamoto. 1997. Age composition in the schools of juvenile yellowtail, Seriola quinqueradiata, associated with drifting seaweeds in the East China Sea. Fish. Sci. 63: 37–41.Google Scholar
  35. Sakakura, Y. & K. Tsukamoto. 1999. Ontogeny of aggressive behaviour in schools of yellowtail Seriola quinqueradiata. Env. Biol. Fish. 56: 231–242.Google Scholar
  36. Secor, D.H., J.M. Dean & S.E. Campana (ed.). 1995. Recent developments in fish otolith research. University of South Carolina Press, Columbia. 735 pp.Google Scholar
  37. Sokal, R.R. & F.J. Rohlf. 1995. Analysis of frequencies. pp. 685–793. In: R.R. Sokal & F.J. Rohlf (ed.) Biometry, W.H. Freeman and Company, New York.Google Scholar
  38. Soto, C.G., J.F. Leatherland & D.L.G. Noakes. 1992. Gonadal histology in the self-fertilizing hermaphroditic fish Rivulus marmoratus (Pisces, Cyprinodontidae). Can. J. Zool. 70: 2338–2347.Google Scholar
  39. Soto, C.G. & D.L.G. Noakes. 1994. Colouration and gender in the hermaphroditic fish Rivulus marmoratus Poey (Teleostei: Rivulidae). Ichthyol. Explor. Freshwaters 5: 79–90.Google Scholar
  40. Swain, D.P. & C.C. Lindsey. 1986a. Influence of reproductive history of parents on meristic variation in offspring in the cyprinodont fish Rivulus marmoratus. Can. J. Zool. 64: 1456–1459.Google Scholar
  41. Swain, D.P. & C.C. Lindsey. 1986b. Meristic variation in a clone of the cyprinodont fish Rivulus marmoratus related to temperature history of the parents and of the embryos. Can. J. Zool. 64: 1444–1455.Google Scholar
  42. Taylor, D.S. 1992. Diet of the killifish Rivulus marmoratus collected from land crab burrows, with further ecological notes. Env. Biol. Fish. 33: 389–393.Google Scholar
  43. Taylor, D.S., W.P. Davis & B.J. Turner. 1995. Rivulus marmoratus: ecology of distributional patterns in Florida and the Central Indian River Lagoon. Bull. Mar. Sci. 57: 202–207.Google Scholar
  44. Turner, B.J., J.F. Elders, Jr. & T.F. Laughlin. 1991. Repetitive DNA sequences and the divergence of fish populations: some hopeful beginnings. J. Fish Biol. 39: 131–142.Google Scholar
  45. Turner, B.J., W.P. Davis & D.S. Taylor. 1992a. Abundant males in populations of a selfing hermaphrodite fish, Rivulus marmoratus, from some Belize cays. J. Fish Biol. 40: 307–310.Google Scholar
  46. Turner, B.J., J.F. Elder, Jr., T.F. Laughlin, W.P. Davis & D.S. Taylor. 1992b. Extreme clonal diversity and divergence in populations of a selfing hermaphroditic fish. Proc. Nat. Acad. Sci. 89: 10643–10647.Google Scholar
  47. Tsukamoto, K. 1985. Mass-marking of ayu eggs and larvae by tetracycline-tagging of otoliths. Bull. Japan. Soc. Sci. Fish. 51: 903–911.Google Scholar
  48. Tsukamoto, K. 1988. Otolith tagging of ayu embryo with fluorescent substances. Bull. Japan. Soc. Sci. Fish. 54: 1289–1295.Google Scholar
  49. Tsukamoto, K. & T. Kajihara. 1987. Age determination of ayu with otolith. Bull. Japan. Soc. Sci. Fish. 53: 1985–1997.Google Scholar
  50. Tsukamoto, K., Y. Seki, T. Oba, M. Oya & M. Iwahashi. 1989a. Application of otolith to migration study of salmonids. Physiol. Ecol. Japan 1: 119–140.Google Scholar
  51. Tsukamoto, K., H. Kuwada, J. Hirokawa, M. Oya, S. Sekiya, H. Fujimoto & K. Imaizumi. 1989b. Size-dependent mortality of red sea bream, Pagrus major, juveniles released with fluorescent otolith-tags in News Bay, Japan. J. Fish Biol. 35: 59–69.Google Scholar
  52. Tzeng, W.N. & S.Y. Yu. 1992. Effects of starvation on the formation of daily growth increments in the otoliths of milkfish, Chanos chanos (Forssk al), larvae. J. Fish Biol. 40: 39–48.Google Scholar
  53. Umezawa, A. & K. Tsukamoto. 1991. Factors influencing otolith increment formation in Japanese eel, Anguilla japonica T&S., elvers. J. Fish Biol. 39: 211–223.Google Scholar
  54. Warner, R.R. 1978. The evolution of hermaphroditism and unisexuality in aquatic and terrestrial vertebrates. pp. 77–101. In: E.S. Reese & F.J. Lighter (ed.) Contrasts in Behavior, Wiley, New York.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Yoshitaka Sakakura
    • 1
  • David L. G. Noakes
    • 1
  1. 1.Department of Zoology and Axelrod Institute of IchthyologyUniversity of GuelphGuelphCanada

Personalised recommendations