Environmental Biology of Fishes

, Volume 46, Issue 3, pp 225–242 | Cite as

The life history of the tropical shad Tenualosa toli from Sarawak: first evidence of protandry in the Clupeiformes?

  • Stephen J. M. Blaber
  • David A. Milton
  • Josephine Pang
  • Philip Wong
  • Ong Boon-Teck
  • Lolin Nyigo
  • David Lubim


Sharp declines in catches prompted a detailed study of the commercially and culturally important ‘terubok’ Tenualosa toli, which lives in the fast-flowing, turbid estuaries and adjacent shallow coastal waters of Sarawak. Its reproduction, diet, age and growth were investigated. An absence of small females and large males, together with histological data showing transitional gonads, suggest that T. toli is a protandrous hermaphrodite. Ageing based on otoliths indicates that individuals may not live more than about two years. Male fish spawn towards the end of their first year, change sex (transitional gonads were recorded in fish from 14 to 31 cm SL) and spawn as females in their second year. Spawning takes place in the middle reaches of estuaries and females deposit all their eggs at once. Fecundity is linearly related to fish length but shows significant seasonal and site variations. Hermaphroditism is discussed in relation to possible environmental and isolating mechanisms. T. toli is a zooplanktivore eating mainly calanoid copepods. Laser-ablation inductively-coupled plasma mass spectroscopy of trace elements across otoliths revealed that the species does not move into full seawater or freshwater, but completes its life cycle in estuarine and adjacent coastal waters. Therefore T. toli populations in each estuary and adjacent coastal waters may be relatively isolated from one another, and hence particularly susceptible to overfishing.

Key words

Estuaries Ecology Hermaphroditism Diet Age Growth Distribution 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Alheit, J. 1988. Reproductive biology of sprat (Sprattus sprattus): factors determining annual egg production. J. Cons. int. Explor. Mer 44: 162–168.Google Scholar
  2. Assis, C.A., P.R. Almeida, F. Moreira, J.L. Costa & M.J. Costa. 1992. Diet of the twaite shad, Alosa fallax (Lacepede) (Clupeidae) in the River Tagus estuary, Portugal. J. Fish Biol. 41: 1049–1050.Google Scholar
  3. Chan, S.T.H. & W.S.B. Yeung. 1983. Sex control and sex reversal in fish under natural conditions. pp. 171–222. In: W.S. Hoar, D.J. Randall & E.M. Donaldson (ed.) Fish Physiology, Volume 9, Reproduction, Academic Press, New York.Google Scholar
  4. Charles-Dominique, E. 1982. Expose synoptique des donnees biologiques sur l'ethmalose (Ethmalosa fimbriata Bowditch 1825). Rev. Hydrobiol. Trop. 15: 373–397.Google Scholar
  5. Conand, F. 1991. Biology and phenology of Amblygaster sirm. (Clupeidae) in New Caledonia, a sardine of the coral environment. Bull. Mar. Sci. 48: 137–149.Google Scholar
  6. Creed, R.P. 1985. Feeding, diet, and repeat spawning of blueback herring, Alosa aestivalis, from the Chowan River, North Carolina. U.S. Fish. Bull. 83: 711–716.Google Scholar
  7. Cyrus, D.P. & S.J.M. Blaber. 1984. The reproductive biology of Gerres in Natal estuaries. J. Fish Biol. 24: 491–504.Google Scholar
  8. De, D.K. & N.C. Datta. 1990. Studies on certain aspects of the morpho-histology of Indian shad hilsa, Tenualosa ilisha (Hamilton) in relation to food and feeding habits. Ind. J. Fish. 37: 189–198.Google Scholar
  9. De, D.K. 1980. Maturity, fecundity and spawning of post-monsoon run of hilsa, Hilsa ilisha (Hamilton) in the upper stretches of the Hooghly estuarine system. J. Inland Fish. Soc. India 12: 54–63.Google Scholar
  10. Dutrieux E. 1991. Study of the ecological functioning of the Mahakam delta (East Kalimantan, Indonesia). Est. Coast. Shelf Sci. 32: 415–420.Google Scholar
  11. Edmonds, J.S., R.C.J. Lenanton, N. Caputi & M. Morita. 1992. Trace elements in the otoliths of yellow-eye mullet (Aldrichetta forsteri) as an aid to stock identification. Fish. Res. 13: 39–51.Google Scholar
  12. Francis, R.I.C.C. 1988. Are growth parameters estimated from tagging and age-length data comparable? Can. J. Fish. Aquat. Sci. 45: 936–942.Google Scholar
  13. Ghiselin, M.T. 1969. The evolution of hermaphroditism among animals. Quart. Rev. Biol. 44: 189–208.Google Scholar
  14. Halder, D.D. 1971. Observations on the food of young Hilsa ilisha (Ham.) of the Hooghly estuarine system. J. Bombay. nat. Hist. Soc. 67: 578–583.Google Scholar
  15. Ingram, B.L. & D. Sloan. 1992. Strontium isotopic composition of estuarine sediments as paleosalinity-paleoclimate indicator. Science 255: 68–72.Google Scholar
  16. Jennings, S. & R.J.H. Beverton. 1991. Intraspecific variation in the life history tactics of Atlantic herring (Clupea harengus) stocks. ICES J. Mar. Sci. 48: 117–125.Google Scholar
  17. Jones, S. & P.M.G. Menon. 1951. Observations on the life-history of the Indian shad, Hilsa ilisha (Hamilton). Proc. Indian Acad. Sci. 23: 101–125.Google Scholar
  18. Kalish, J.M. 1989. Otolith microchemistry: validation of the effects of physiology, age and environment on otolith composition. J. Exp. mar. Biol. Ecol. 132: 151–178.Google Scholar
  19. Kalish, J.M. 1990. Use of otolith microchemistry to distinguish the progeny of sympatric anadromous and non-anadromous salmonids. U.S. Fish. Bull. 88: 657–666.Google Scholar
  20. Kawasaki, T. 1980. Fundamental relations among the selections of life-history in marine teleosts. Bull. Japan Soc. Sci. Fish. 46: 289–293.Google Scholar
  21. McDowall, R.M. 1988. Diadromy in fishes. Croom Helm, London. 308 pp.Google Scholar
  22. Mennesson-Boisneau, C., P. Boisneau & J-L. Bagliniere. 1986. Premieres observations sur les caracteristiques biologiques des adultes des grande alose (Alosa alosa L.) dans le cours moyen de la Loire. Acta Oecol. 7: 337–353.Google Scholar
  23. Milton, D.A., S.J.M. Blaber & N.J.F. Rawlinson. 1993. Age and growth of three species of tuna baitfish (genus Spratelloides) in the tropical Indo-Pacific. J. Fish Biol. 39: 849–866.Google Scholar
  24. Milton, D.A., S.J.M. Blaber & N.J.F. Rawlinson. 1993. Age and growth of three tropical clupeids from Kiribati, central south Pacific. J. Fish Biol. 43: 89–108.Google Scholar
  25. Moula, G., M.J. Rahman & M.A. Mazid. 1991. Observations on the maturity and spawning of Indian shad, Tenualosa ilisha (Hamilton) of the River Meghna, Bangladesh. J. Zool. Bangladesh 6: 109–117.Google Scholar
  26. Nelson, J.S. 1984. Fishes of the world. John Wiley & Sons, New York. 523 pp.Google Scholar
  27. Nigro, A.A. & J.J. Ney. 1982. Reproduction and early-life accommodations of landlocked alewives to a southern range extension. Trans. Amer. Fish. Soc. 111: 555–569.Google Scholar
  28. Pang, S.C. 1991. Stock assessment of the Hilsa toli fishery and its management implications in the batang Lupar estuary, Sarawak, Malaysia. M.Sc. Thesis, University of York, York. 113 pp.Google Scholar
  29. Pillay, S.R. & K.K. Rao. 1962. Observations on the biology and fishery of the hilsa, Hilsa ilisha (Ham.) of river Godavari. Proc. Indo-Pac. fish. Council 10: 37–61.Google Scholar
  30. Pillay, T.V.R. 1967. Estuarine fishes of the Indian Ocean coastal zone. pp. 647–657. In: G.H. Lauff (ed.) Estuaries, American Association for the Advancement of Science, Publication 83, Washington.Google Scholar
  31. Radtke, R.L. 1989. Strontium-calcium concentration ratios in fish otoliths as environmental indicators. Comp. Biochem. Physiol. 92A: 189–193.Google Scholar
  32. Radtke, R.L., D.W. Townsend, S.D. Folsom & M.A. Morrison. 1990. Strontium: calcium ratios in otoliths of herring larvae as indicators of environmental histories. Env. Biol. Fish. 27: 51–61.Google Scholar
  33. Rajyalakshmi, T. 1973. The population characteristics of the godavary hilsa over the years 1963–1967. Ind. J. Fish. 20: 78–94.Google Scholar
  34. Reinboth, R. 1980. Can sex inversion be environmentally induced? Biol. Reprod. 22: 49–59.Google Scholar
  35. Ross, R.M. 1990. The evolution of sex-change mechanisms in fishes. Env. Biol. Fish. 29: 81–93.Google Scholar
  36. Sadovy, Y. & K.P. Severin. 1994. Elemental patterns in red hind (Epinephelus guttatus) otoliths from Bermuda and Puerto Rico reflect growth rate, not temperature. Can. J. Fish. Aquat. Sci. 51: 133–141.Google Scholar
  37. Sadovy, Y. & D.Y. Shapiro. 1987. Criteria for the diagnosis of hermaphroditism in fish. Copeia 1987: 136–156.Google Scholar
  38. Sinis, A.I. & M.E. Kattoulas. 1986. Population structure of Alosa macedonica (Vinciguerra, 1921) (Pisces: Clupeidae) in Lake Volvi (Macedonia, Greece). Cybium 10: 91–101.Google Scholar
  39. Warner, R.T. 1988. Sex change in fishes: hypotheses, evidence and objections. Env. Biol. Fish. 22: 81–90.Google Scholar
  40. Whitehead, P.J.P. 1985. FAO species catalogue 7: clupeoid fishes of the world (Clupeoidei) UNDP, FAO, Rome. 303 pp.Google Scholar
  41. Williams, V.R. & T.A. Clarke. 1983. Reproduction, growth and other aspects of the biology of the gold-spot herring Herklotsichthys quadrimaculatus (Clupeidae), a recent introduction to Hawaii. U.S. Fish. Bull. 81: 587–597.Google Scholar
  42. Yamamoto, T. 1969. Sex differentiation. pp. 117–177. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Volume 3, Reproduction and growth, Academic Press, New York.Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • Stephen J. M. Blaber
    • 1
  • David A. Milton
    • 1
  • Josephine Pang
    • 2
  • Philip Wong
    • 2
  • Ong Boon-Teck
    • 2
  • Lolin Nyigo
    • 3
  • David Lubim
    • 3
  1. 1.CSIRO Division of FisheriesMarine LaboratoriesClevelandAustralia
  2. 2.Inland Fisheries BranchMinistry of Agriculture & Community DevelopmentKuching, SarawakMalaysia
  3. 3.PPES Santubong (Sdn Bhd), SEDCKuching, SarawakMalaysia

Personalised recommendations