Skip to main content

Comparative digestive enzyme ontogeny in two marine larval fishes: Pacific threadfin (Polydactylus sexfilis) and bluefin trevally (Caranx melampygus)

Abstract

The specific activity of digestive enzymes; aspartic and serine protease, collagenase, lipase, acid and alkaline amylase, acid and alkaline phosphatase, and chitinase was assayed throughout early development in two species of marine fishes: the Pacific threadfin (Polydactylus sexfilis) and bluefin trevally (Caranx melampygus). Specific enzyme activities were determined on whole larval extracts sampled at selected stages of development, from day 0 to day 30 post-hatching. Similar developmental patterns of enzyme specific activity were observed in the two species, although differences in timing, amplitude and effects of first feeding were noted. Amylase activity increased prior to first feeding, peaking at the middle of the larval period, and becoming nearly undetectable by the time of larval-to-juvenile metamorphosis. Serine protease, collagenase, lipase and alkaline (and acid for threadfin) phosphatase activities increased gradually, followed by sharp increases to a plateau during the second half of larval development. Aspartic protease and chitinase activities, in addition to acid phosphatase (for trevally), were low to undetectable in the first half of development, increasing through metamorphosis. In the trevally only, this group of enzymes exhibited high activity levels at the time of hatching, followed by a precipitous drop. Species-dependent differences in enzyme specific activity at first feeding may have been a result of differences in yolk utilization. These results, taken in the context of earlier reports, lead us to conclude that carbohydrate utilization may play a significant role in the earlier phases of development among some marine larvae, followed by a shift to protein and lipid utilization.

This is a preview of subscription content, access via your institution.

References

  • Bengtson, D.A., Léger, P. and Sorgeloos, P. 1991. Use of artemia as a food source for aquaculture. In: Artemia Biology. pp. 225–286. Edited by R.A. Browne, P. Sorgeloos & C.N.A. Trotman. CRC Press, Florida, USA.

    Google Scholar 

  • Bengtson, D.A., Borrus, D.N. Leibovitz, H.E. and Simpson, K.L. 1993. Studies on structure and function of the digestive system of Menidia beryllina (Pisces, atherinidae). In: Physical and Bio-chemical Aspects of Fish Development. pp. 199–208. Edited by B.T. Walther and H.J. Fyhn. Univ. Bergen.Norway.

  • Blaxter, J.H.S. and Hempel, G. 1966. Utilization of yolk by herring larvae. J. Marine Biol. Assoc. U.K. 46: 219–234.

    Google Scholar 

  • Brown, C.L. and Kim, B.G. 1995. Combined application of cortisol and triiodothyronine in marine finfish culture. Aquaculture 135(1–3): 79–86.

    Google Scholar 

  • Brown, C.L. and NÚñez, J.M. 1994. Hormone actions and applications in embryogenesis. In: Perspectives in Comparative Endocrinology. pp. 333–339. Edited by K.G. Davey, R.E. Peter and S.S. Tobe, National Research Council of Canada, Ottawa.

    Google Scholar 

  • Buddington, R.K. 1985. Digestive secretions of lake sturgeon, Acipenser fulvescens, during early development. J. Fish Biol. 26: 715–723.

    Google Scholar 

  • Buddington, R.K. and Doroshov, S.I. 1986. Development of digestive secretions in white sturgeon juveniles (Scipenser transmontanus). Comp. Biochem. Physiol. 83: 233–238.

    Google Scholar 

  • Cahu, C.L., Zambonino Infante, J.L., Peres, A., Quazuguel, P. and Le Gall, MM. 1998. Algal addition in sea bass (Dicentrarchus labrax) larvae rearing: Effect on digestive enzymes. Aquaculture 161: 179–489.

    Google Scholar 

  • Copeland, R.A. 1996. Structural components of enzymes. In: Enzymes, A practical introduction to structure, mechanism and data analysis. pp. 35–65. Wiley-VCH, New York.

    Google Scholar 

  • Cousin, J.C.B. and Baudin-Laurencin, F. 1985. Morphogenese de l'appareil digestif et de la vessie gazeuse du turbot, Scophthalmus maximus. Aquacul. 47: 305–319.

    Google Scholar 

  • Cousin, J.C.B., Baudin-Laurencin, F. and Gabaudan, J. 1987. Ontogeny of enzymatic activities in fed and fasting turbot, Scophthalmus maximus L. J. Fish Biol. 30: 15–33.

    Google Scholar 

  • Dabrowski, K. and Glogowski,J. 1977. The role of exogenic proteolytic enzymes in digestion process in fish. Hydrobiol. 54: 129–134.

    Google Scholar 

  • Dabrowski, K. and Culver, D. 1991. The physiology of larval fish: Digestive tract and formulation of starter diets. Aquacul. Magazine. 2: 49–61.

    Google Scholar 

  • Danilowicz, B.S. and Brown, C.L. 1992. Rearing methods for two damslefish species: Dascyllus albisella (Gill) and D. aruanus (L.). Aquaculture. 106: 141–149.

    Google Scholar 

  • Divakaran, S., Kim, B.G. and Ostrowski, A.C. 1999. Digestive enzymes present in Pacific threadfin Polydactylus sexfilis (Bloch and Schneider 1801) and bluefin travelly Caranx melampyrus (Cuvier 1833). Aquacult Res. 30: 781–787.

    Google Scholar 

  • DLNR-DAR. 1963–1968. Life history study of the moi, Polydactylus sexfilis. Reef and inshore game fish management research, Job no. 14. Job completion report. Project No. F-5–R-11 through F-5–R-17.

  • Erlanger, B.F., Kokowsky, N. and Cohen, W. 1961. The preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys. 95: 271–278.

    Google Scholar 

  • Fauconneau, B. 1984. The measurement of whole body protein synthesis in larval and juvenile carp (Cyprinus carpio). Comp. Biochem. Physiol. 78: 845–850.

    Google Scholar 

  • Fukusho, K., Okauchi, M., Nuraini, S., Tsujigado, A. and Watanabe, T. 1984. Food value of rotifer Brachionus plicatilis, cultured with Tetraselmis tetrathele for larvae of red seabream Pagrus major. Bull. Japan. Soc. Sci. Fish. 50: 1439–1444.

    Google Scholar 

  • Gawlicka, A., Teh, S.J., Hung, S.S.O., Hinton, D.E. and de la Noüe, J. 1995. Histological and histochemical changes in the digestive tract of white sturgeon larvae during ontogeny. Fish Physiol. Biochem. 14: 357–371.

    Google Scholar 

  • Gawlicka, A., Parent, B., Horn, M.H., Ross, N., Opstad, I. and Torrissen, O.J. 2000. Activity of digestive enzymes in yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus): indication of readiness for first feeding. Aquaculture 184: 303–314.

    Google Scholar 

  • Govoni, J.J., Boehlert, G.W. and Watanabe, Y. 1986. The physiology of digestion in fish larvae. Env. Biol. Fish. 16: 59–77.

    Google Scholar 

  • Hackman, R.H. and Goldberg, M. 1964. New substrates for use with chitinases. Analytical Biochem. 8: 397–410.

    Google Scholar 

  • Hofer, R. and Burkle, O. 1986. Daily consumption, gut passage rate and protein utilization in whitefish larvae (Coregonus sp.). Arch. Hydrobiol. Beih. Ergebn. Limnol. 22: 189–196.

    Google Scholar 

  • Kanayama, R.K. 1973. Life history aspects of the moi Polydactylus sexifilis (Cuvier and Valenciennes) in Hawaii. pp. 50. DLNR Honolulu, Hawaii.

    Google Scholar 

  • Kawai, S.I. 1972. Studies on the digestive enzymes of fishes with special reference to carbohydrases. PhD. dissertation. pp. 44. Depart. of Fisheries, Faculty of Agriculture, Kyoto University.

    Google Scholar 

  • Kawai, S.I. and Ikeda, S. 1971. Studies on digestive enzymes of fishes. I. Carbohydtases in digestive organs of several fishes. Bull. Japan. Soc. Sci. Fish. 37: 333–337.

    Google Scholar 

  • Kim, B.G. and Brown, C.L. 1997. Interaction of cortisol and thyroid hormone in the larval development of the pacific threadfin. Am. Zool. 37: 468–479.

    Google Scholar 

  • Kim, B.G. 1999. Developmental biology of larval moi, Polydactylus sexfilis, and implications for aquaculture. PhD. Thesis, University of Hawaii. 186 pp.

  • Laurence, G.C. 1977. A bioenergetic model for the analysis of feeding and survival potential of winter flounder, Pseudopleuronectes americanus, larvae during the period from hatching to metamorphosis. Fish. Bull. NMFS/NOAA 75(3): 529–546.

    Google Scholar 

  • Loewe, H. and Eckmann, R. 1988. The ontogeny of the alimentary tract of coregonid larvae: Normal development. J. Fish Biol. 33: 841–850.

    Google Scholar 

  • Martinez, I., Moyaano, F.J., Fernandez-Diaz, C. and Yufera, M. 1999. Digestive enzymes activity during larval development of the Senegal sole (Solea senegalensis). Fish Physiol Biochem. 21: 317–323.

    Google Scholar 

  • Masui, Y., Takemoto, T., Sakakibara, S., Hori, H. and Nagai, Y. 1977. Synthetic substrates for vertebrate collagenase. Biochem Medicine. 17: 215–221.

    Google Scholar 

  • Miwa, A., Yamano, K. and Inui, Y. 1992. Thyroid hormone stimulates gastric development in flounder larvae during metamorphosis. J. Exp. Zool. 261: 424–430.

    Google Scholar 

  • Moyano, F.J. Diaz, M., Alarcon, F.J. and Sarasquete, M.C. 1996. Characterization of digestive enzyme activity during larval development of gilthead seabream (Sparus aurata). Fish Physiol. Biochem. 15: 121–130.

    Google Scholar 

  • Munilla-Moran, R. and Stark, J.R. 1989. Protein digestion in early turbot larvae, Scophthalmus maximus (L.). Aquaculture 81: 315–327.

    Google Scholar 

  • Munilla-Moran, R., Stark, J.R. and Barbour, A. 1990. The role of exogenous enzymes in digestion in cultured turbot larvae (Scophthalmus maximus L.). Aquaculture 88: 337–350.

    Google Scholar 

  • O'Connell, C.P. 1981. Development of organ systems in the northern anchovy, Engraulis mordax, and other teleosts. Am. Zool. 21: 429–226.

    Google Scholar 

  • Oozeki, Y. and Bailey, K.M. 1995. Ontogenetic development of digestive enzyme activities in larval walleye pollock, Theragta chalcogramma. Marine Biol. 122: 177–186.

    Google Scholar 

  • Ostrowski, A.C. and Molnar A. 1998. Pacific threadfin, Polydactylus sexfilis (moi), Hatchery manual. Center for Tropical and Subtropical Aquaculture. Publication no. 132, Oceanic Institute, Waimanalo, HI 96795, 96 pp.

    Google Scholar 

  • Potts, G.W. 1980. The predatory behavior of Caranx melampyrus in the channel environment of Aldabra Atoll. J. Zool. Soc. London. 192: 323–350.

    Google Scholar 

  • Rinderknecht, H., Wilding, P. and Haverback, B.J. 1967. A new method for the determination α-amylase. Experientia 23: 805.

    Google Scholar 

  • Segner, H., Rösch, R. Schmidt, H. and von Poeppinghausen, K.J. 1989. Digestive enzymes in larval Coregonus lavaretus L. J. Fish Biol. 35: 249–263.

    Google Scholar 

  • Segner, H. and Witt, U. 1990. Weaning experiments with turbot (Scophthalmus maximus): Electron microscopic study of liver. Marine Biol. 105: 353–361.

    Google Scholar 

  • Siebenaller, J.F. 1984. Aanlysis of the biochemical consequences of ontogenetic vertical migration in a deep-living teleost fish. Physiol. Zool. 57: 598–608.

    Google Scholar 

  • Snell, F.D. and Snell, C.T. 1971. Colorimetric methods of analysis. Vol IV. AAA Van Nostrand Reinhold Co. NY. 351 pp.

    Google Scholar 

  • Specker, J.L. 1988. Preadaptive role of thyroid hormones in larval and juvenile salmon: Growth, the gut, and evolutionary considerations. Am. Zool. 28: 337–350.

    Google Scholar 

  • Stroband, H.W.J., v.d.Meer, H. and Timmermans, L.P.M. 1979. Regional functional differentiation in the gut of grass carp, Ctenopharngodon idella (Val.). J. exp. Zool. 218: 149–156.

    Google Scholar 

  • Stroband, H.W.J. and Kroon, A.G. 1981. The development of the stomach in Clarias lazera and the intestinal absorption of protein macromolecules. Cell Tissue Res. 215: 397–415.

    Google Scholar 

  • Tanaka, M. 1971. Studies on the structure and function of the digestive system in teleost larvae. III. Development of the digestive system during postlarval stage. Japan. J. Ichthyol. 18: 164–174.

    Google Scholar 

  • Tanaka, M. 1973. Studies on the structure and function of the digestive system of teleost larvae. PhD. dissertation. pp. 136 Depart. of Fisheries, Faculty of Agriculture, Kyoto University.

    Google Scholar 

  • Tanaka, M., Kawai, S., Seikai, T. and Burke, J.S. 1996. Development of the digestive organ system in Japanese flounder in relation to metamorphosis and settlement. Mar. Fresh. Behav. Physiol. 28: 19–31.

    Google Scholar 

  • Theilacker, G.H. and Kimball, A.S. 1984. Comparative quality of rotifers and copepodes as foods for larval fishes. CalCOFI Rep. 25: 80–86.

    Google Scholar 

  • Walford, J., Lim, T.M. and Lam, T.J. 1991. Replacing live foods with microencapsulated diets in the rearing of seabass (Lates calcarifer) larvae: Do the larvae ingest and digest proteinmembrane microcapsules? Aquaculture 92: 225–235.

    Google Scholar 

  • Walford, J. and Lam, T.J. 1993. Development of digestive tract and proteolytic enzyme activity in seabass (Lates calcarifer) larvae and juveniles. Aquaculture 109: 187–205.

    Google Scholar 

  • Watanabe, Y. 1984. Morphological and functional changes in rectal epithelium cells of pond smelt during postembryonic development. Bull. Japan. Soc. Sci. Fish. 50: 805–814.

    Google Scholar 

  • Watanabe, Y. 1985. Histological changes in the liver and intestine of freshwater body larvae during short-term starvation. Bull. Japan. Soc. Sci. Fish. 51: 707–709.

    Google Scholar 

Download references

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kim, B.G., Divakaran, S., Brown, C.L. et al. Comparative digestive enzyme ontogeny in two marine larval fishes: Pacific threadfin (Polydactylus sexfilis) and bluefin trevally (Caranx melampygus). Fish Physiology and Biochemistry 24, 225–241 (2001). https://doi.org/10.1023/A:1014054431627

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1014054431627

  • larval Pacific threadfin (Polydactylus sexfilis)
  • larval bluefin trevally (Caranx melampygus)
  • digestive enzyme
  • first feeding