Environmental Biology of Fishes

, Volume 46, Issue 3, pp 281–288

Both-ways sex change in monogamous coral gobies, Gobiodon spp.

  • Yasuhiro Nakashima
  • Tetsuo Kuwamura
  • Yutaka Yogo
Article

Synopsis

We confirmed both-ways sex change in the coral-dwelling gobies Gobiodon micropus, G. oculolineatus, G. quinquestrigatus and G. rivulatus rivulatus by mate-removal experiment in the field and by the aquarium experiment of keeping two consexual fish in a coral. Eight species of Gobiodon were found in Acropora corals on the reef flat of Sesoko Island, Okinawa, southern Japan. The 4 species mentioned above bred in monogamous pairs composed of a male and a female matched by size, and the male took care of eggs deposited on the coral branch. In G. quinquestrigatus and G. rivulatus rivulatus males were larger than females in newly formed pairs, and females grew faster than their mates until breeding. The growth-rate advantage in females seems to be the major factor in the evolution of female to male sex change. The gobies strongly depended on host corals, but they moved between the corals after mate loss or coral death to form new pairs. This provides opportunities for the evolution of male to female sex change; the ability to change sex in both directions reduces the frequency of risky movement between host corals to form new pairs. These conditions are very similar to those reported in the both-ways sex change of another coral-dwelling goby Paragobiodon echinocephalus.

Key words

Hermaphroditism Protandry Protogyny Growth-rate advantage Inter-group movement Monogamy Parental care Gobiidae 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Charnov, E.L. 1982. The theory of sex allocation Princeton University Press, Princeton. 355 pp.Google Scholar
  2. Cole, K.S. 1983. Protogynous hermaphroditism in a temperature zone territorial marine goby, Coryphopterus nicholsi. Copeia 1983: 809–812.Google Scholar
  3. Cole, K.S. 1988. Predicting the potential for sex-change on the basis of ovarian structure in gobiid fishes. Copeia 1988: 1082–1086.Google Scholar
  4. Cole, K.S. 1990. Patterns of gonad structure in hermaphroditic gobies (Teleostei: Gobiidae). Env. Biol. Fish. 28: 125–142.Google Scholar
  5. Cole, K.S. & D.R. Robertson. 1988. Protogyny in the Caribbean reef goby, Coryphopterus personatus: gonad ontogeny and social influences on sex-change. Bull. Mar. Sci. 42: 317–333.Google Scholar
  6. Fishelson, L. 1989. Bisexuality and pedogenesis in gobies (Gobiidae: Teleostei) and other fish, or why so many little fish in tropical seas? Senckenbergiana Marit. 20: 147–169.Google Scholar
  7. Fricke, H.W. & S. Fricke. 1977. Monogamy and sex change by aggressive dominance in coral reef fish. Nature 266: 830–832.Google Scholar
  8. Ghiselin, M.T. 1969. The evolution of hermaphroditism among animals. Quart. Rev. Biol. 44: 189–208.Google Scholar
  9. Hiatt, R.W. & D.W. Strasburg. 1960. Ecological relationships of the fish fauna on coral reefs of the Marshall Islands. Ecol. Monogr. 30: 65–127.Google Scholar
  10. Hioki, S. & K. Suzuki. 1993. Sex succession from male to female in three protogynous angelfishes belonging to the genus Centropyge. Advance abstracts for the 26th annual meeting, Ichthyol. Soc. Japan, Tokyo: 25 (in Japanese).Google Scholar
  11. Iwasa, Y. 1991. Sex change evolution and cost of reproduction. Behav. Ecol. 2: 56–68.Google Scholar
  12. Kobayashi, K. & K. Suzuki. 1992. Hermaphroditism and sexual function in Cirrhitichthys aureus and the other Japanese hawkfishes (Cirrhitidae: Teleostei). Japan. J. Ichthyol. 38: 397–410 (in Japanese).Google Scholar
  13. Kuwamura, T. 1976. Seasonal occurrence of fishes in the interstice of shrub corals on the rocky reef of Sirahama, Japan. Nankiseibutu 18: 15–22 (in Japanese).Google Scholar
  14. Kuwamura, T., Y. Nakashima & Y. Yogo. 1994a. Sex change in either direction by growth-rate advantage in the monogamous coral goby Paragobiodon echinocephalus. Behav. Ecol. 5: 434–438.Google Scholar
  15. Kuwamura, T., Y. Yogo & Y. Nakashima. 1994b. Population dynamics of goby Paragobiodon echinocephalus and host coral Stylophora pistillata. Mar. Ecol. Prog. Ser. 103: 17–23.Google Scholar
  16. Kuwamura, T., Y. Yogo & Y. Nakashima. 1993. Size-assortative monogamy and paternal egg care in a coral goby Paragobiodon echinocephalus. Ethology 95: 65–75.Google Scholar
  17. Lassig, B.R. 1977. Socioecological strategies adopted by obligate coral-dwelling fishes. Proc. 3rd Int. Coral Reef Symp. 1: 565–570.Google Scholar
  18. Nakashima, Y., T. Kuwamura & Y. Yogo. 1995. Why be a both-ways sex changer? Ethology (in press).Google Scholar
  19. Nakazono, A. & T. Kuwamura(ed.). 1987. Sex change in fishes. Tokai University Press, Tokyo. 284 pp. (in Japanese).Google Scholar
  20. Nishihira, M. 1991. Field guide to hermatypic corals of Japan. Tokai University Press, Tokyo. 264 pp. (in Japanese).Google Scholar
  21. Robertson, D.R. 1972. Social control of sex reversal in a coralreef fish. Science 177: 1007–1009.Google Scholar
  22. Robertson, D.R. & G. Justines. 1982. Protogynous hermaphroditism in four Caribbean reef gobies. Env. Biol. Fish. 7: 137–142.Google Scholar
  23. Ross, R.M. 1990. The evolution of sex-change mechanisms in fishes. Env. Biol. Fish. 29: 81–93.Google Scholar
  24. Sawada, Y. & R. Arai. 1973. Three species of coral gobies (the genus Gobiodon) from the Ryukyu Islands, Japan. Bull. Nat. Mus. Tokyo 16: 585–603.Google Scholar
  25. Shapiro, D.Y. 1987. Differentiation and evolution of sex change in fishes. BioSci. 37: 490–497.Google Scholar
  26. St. Mary, C.M. 1993. Novel sexual patterns in two simultaneously hermaphrodite gobies, Lythrypnus dalli and Lythrypnus zebra. Copeia 1993: 1062–1072.Google Scholar
  27. St. Mary, C.M. 1994. Sex allocation in a simultaneous hermaphrodite, the blue-banded goby (Lythrypnus dalli): the effects of body size and behavioral gender and the consequences for reproduction. Behav. Ecol. 5: 304–313.Google Scholar
  28. Sunobe, T. & A. Nakazono. 1990. Polygynous mating system of Trimma okinawae (Pisces: Gobiidae) at Kagoshima, Japan with a note on sex change. Ethology 84: 133–143.Google Scholar
  29. Sunobe, T. & A. Nakazono. 1993. Sex change in both directions by alteration of social dominance in Trimma okinawae (Pisces: Gobiidae). Ethology 94: 339–345.Google Scholar
  30. Tanaka, H., K. Hirose, K. Nogami, K. Hattori & N. Ishibashi. 1990. Sexual maturation and sex reversal in red spotted grouper, Epinephelus akaara. Bull. Nall. Res. Inst. Aquaculture 17: 1–15 (in Japanese).Google Scholar
  31. Tyler, J.C. 1971. Habitat preferences of the fishes that dwell in shrub corals on the Great Barrier Reef. Proc. Acad. Nat. Sci. USA 123: 1–26.Google Scholar
  32. Warner, R.R. 1975. The adaptive significance of sequential hermaphroditism in animals. Amer. Nat. 109: 61–82.Google Scholar
  33. Warner, R.R. 1978. The evolution of hermaphoroditism and uni-sexuality in aquatic and terrestrial vertebrates. pp. 77–101. In: E.S. Reese & F.J. Lighter (ed.) Contrasts in Behavior, John Wiley, New York.Google Scholar
  34. Warner, R.R. 1984. Mating behavior and hermaphroditism in coral reef fishes, Amer. Scientist 72: 128–136.Google Scholar
  35. Warner, R.R. 1988a. Sex change in fishes: hypotheses, evidence, and objections. Env. Biol. Fish. 22: 81–90.Google Scholar
  36. Warner, R.R. 1988b. Sex change and the size-advantage model. Trends Ecol. Evol. 3: 133–136.Google Scholar
  37. Yamamoto, T. 1980. Embryonic development in Paragobiodon lacunicola and the spawning sites of Gobiodon spp. and Paragobiodon spp. (Pisces: Gobiidae). Biol. Mag. Okinawa 18: 17–24.Google Scholar
  38. Yoshino, T. & T.Yamamoto. 1988. Gobiodon spp. pp. 254–255 and Plate 246. In: H. Masuda, K. Amaoka, C. Araga, T. Ueno & T. Yoshino (ed.). The Fishes of the Japanese Archipelago, Tokai University Press, Tokyo (in Japanese).Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • Yasuhiro Nakashima
    • 1
  • Tetsuo Kuwamura
    • 2
  • Yutaka Yogo
    • 3
  1. 1.Department of Zoology, Faculty of ScienceKyoto UniversityKyotoJapan
  2. 2.Biological Laboratory, Faculty of Liberal ArtsChukyo UniversityYagoto, NagoyaJapan
  3. 3.Showa Women's High SchoolHita, OitaJapan

Personalised recommendations