Estuaries

, 17:26 | Cite as

Ontogeny and evolution of salinity tolerance in anadromous salmonids: Hormones and heterochrony

  • Stephen D. McCormick
Article

Abstract

Use of estuaries and oceans by salmonids varies greatly, from no use in nonanadromous species, to movement toward the sea soon after hatching and emergence in some Pacific salmon. This variation is accompanied by large differences in the ontogeny of salinity tolerance among salmonids. Some species acquire increased salinity tolerance early in development, whereas others develop this characteristic much later, indicating there is a heterochrony (change in timing) in the development of salinity tolerance in salmonids. The basic physiological mechanisms for ion regulation in seawater (such as increased gill chloride cells, gill Na+,K+-ATPase activity, membrane permeability, and drinking rate) are common to all salmonids. What determines the differences in salinity tolerance among the salmonids is not the basic mechanisms for salt secretion but the environmental and ontogenetic control of these mechanisms. In salmonids such as pink and chum salmon that enter seawater soon after emergence, acclimation to seawater may be controlled largely by internal (ontogenetic) information. In smolting salmonids that acquire increased salinity tolerance 1–2 yr after hatching, photoperiod is the dominant environmental cue. In nonsmolting species that migrate 2–3 yr after hatching, salinity itself may be the primary stimulus for salt secretory mechanisms. Physiological changes triggered by developmental and environmental cues are mediated by endocrine factors. Treatments with cortisol, growth hormone, and insulin-like growth factor I have been shown to increase seawater tolerance of salmonids, whereas prolactin is inhibitory. Differences in developmental patterns of endocrine activity (such as secretion, binding proteins, and receptors) are hypothesized to be responsible for the differences in timing (heterochrony) of increased salinity tolerance among and within salmonid species.

Literature Cited

  1. Arnesen, A. M., M. Halvorsen, andK. J. Nilssen. 1992. Development of hypoosmoregulatory capacity in Arctic char (Salvelinus alpinus) reared under either continuous light or natural photoperiod.Canadian Journal of Fisheries and Aquatic Sciences 49:229–237.CrossRefGoogle Scholar
  2. Besner, M., andD. Pelletier. 1991. Adaptation of the brook trout,Salvelinus fontinalis, to direct transfer to sea water in spring and summer.Aquaculture 97:217–230.CrossRefGoogle Scholar
  3. Boeuf, G. 1993. Salmonid smolting: A pre-adaptation to the oceanic environment, p. 105–135.In J. C. Rankin and F. B. Jensen (eds.), Fish Ecophysiology, Chapman Press, London.Google Scholar
  4. Clarke, W. C., H. Lundqvist, andL.-O. Eriksson 1985. Accelerated photoperiod advances seasonal cycle of seawater adaptation in juvenile Baltic salmon,Salmo salar L.Journal of Fish Biology 26:29–35.CrossRefGoogle Scholar
  5. Clarke, W. C., J. E. Shelbourn, T. Ogasawara, andT. Hirano. 1989. Effect of initial daylength on growth, seawater adaptability and plasma growth hormone levels in underyearling coho, chinook, and chum salmon.Aquaculture 82:51–62.CrossRefGoogle Scholar
  6. Clarke, W. C., R. E. Withler, andJ. E. Shelbourn. 1994. Inheritance of smolting phenotypes in backcrosses of hybrid stream-type x ocean-type chinook salmon (Oncorhynchus tshawytscha).Estuaries 17:13–25.CrossRefGoogle Scholar
  7. Conte, F. P., H. H. Wagner, J. Fessler, andC. Gnose. 1966. Development of osmotic and ionic regulation in juvenile coho salmon (Oncorhynchus kisutch).Comparative Biochemistry and Physiology 18:1–15.CrossRefGoogle Scholar
  8. Conte, F. P., andH. H. Wagner. 1965. Development of osmotic and ionic regulation in juvenile steelhead trout,Salmo gairdneri.Comparative Biochemistry and Physiology 14:603–620.CrossRefGoogle Scholar
  9. Duston, J., R. L. Saunders, andD. E. Knox. 1991. Effects of increases in freshwater temperature on loss of smolt characteristics in Atlantic salmon (Salmo salar).Canadian Journal of Fisheries and Aquatic Sciences 48:164–169.CrossRefGoogle Scholar
  10. Evans, D. H. 1979. Fish, p. 305–390.In G. M. O. Maloiy (ed.), Osmotic and Ionic Regulation in Animals, Vol. 1. Academic Press, London.Google Scholar
  11. Grewe, P. M., N. Billington, andD. N. Hebert. 1990. Phylogenetic relationships among members ofSalvelinus inferred from mitochondrial DNA divergence.Canadian Journal of Fisheries and Aquatic Sciences 47:984–991.CrossRefGoogle Scholar
  12. Hoar, W. S. 1988. The physiology of smolting salmonids, p. 275–343.In W. S. Hoar and D. J. Randall (eds.), Fish Physiology, Vol. XIB. Academic Press, New York.Google Scholar
  13. Hutchings, J. A., andD. W. Morris. 1985. The influence of phylogeny, size and behaviour on patterns of covariation in salmonid life history.Oikos 45:118–124.CrossRefGoogle Scholar
  14. Jarvi, T. 1990. Cumulative acute physiological stress in Atlantic salmon smolts: The effect of osmotic imbalance and the presence of predators.Aquaculture 89:337–350.CrossRefGoogle Scholar
  15. Johnston, C. E., andR. L. Saunders. 1981. Parr-smolt transformation of yearling Atlantic salmon (Salmo salar) at several rearing temperatures.Canadian Journal of Fisheries and Aquatic Sciences 38:1189–1198.Google Scholar
  16. Karnaky, K. J. 1986. Structure and function of the chloride cell ofFundulus heteroclitus and other teleosts.American Zoologist 26:209–224.Google Scholar
  17. Kato, F. 1991. Life histories of masu and amago salmon (Oncorhynchus masou andOncorhynchus rhodurus), p. 447–520.In C. Groot and L. Margolis (eds.), Pacific Salmon Life Histories. University of British Columbia Press, Vancouver.Google Scholar
  18. Kendall, A. W., andR. J. Behnke. 1984. Salmonidae: Development and relationships, p. 142–149.In H. G. Moser (ed.), Ontogeny and Systematics of Fishes. American Society of Ichthyologists and Herpetologists. La Jolla, California.Google Scholar
  19. McCormick, S. D., W. W. Dickhoff, J. Duston, R. S. Nishioka, andH. A. Bern. 1991. Developmental differences in the responsiveness of gill Na+, K+-ATPase to cortisol in salmonids.General and Comparative Endocrinology 84:308–317.CrossRefGoogle Scholar
  20. McCormick, S. D., C. D. Moves, andJ. S. Ballantyne. 1989. Influence of salinity on the energetics of gill and kidney of Atlantic salmon (Salmo salar).Fish Physiology and Biochemistry 6:243–254.CrossRefGoogle Scholar
  21. McCormick, S. D., andR. J. Naiman. 1984a. Osmoregulation in the brook trout,Salvelinus fontinalis. II. Effects of size, age and photoperiod on seawater survival and ionic regulation.Comparative Biochemistry and Physiology 79A:17–28.Google Scholar
  22. McCormick, S. D., andR. J. Naiman. 1984b. Osmoregulation in the brook trout,Salvelinus fontinalis. I. Diel, photoperiod and growth related physiological changes in freshwater.Comparative Biochemistry and Physiology 79A:7–16.Google Scholar
  23. McCormick, S. D., R. J. Naiman, andE. T. Montgomery. 1985. Physiological smolt characteristics of anadromous and nonanadromous brook trout (Salvelinus fontinalis) and Atlantic salmon (Salmo salar).Canadian Journal of Fisheries and Aquatic Sciences 42:529–538.CrossRefGoogle Scholar
  24. McCormick, S. D., andR. L. Saunders. 1987. Preparatory physiological adaptations for marine life in salmonids: Osmoregulation, growth, and metabolism.American Fisheries Society Symposium 1:211–229.Google Scholar
  25. McCormick, S. D., R. L. Sauders, E. B. Henderson, andP. R. Harmon. 1987. Photoperiod control of parr-smolt transformation in Atlantic salmon (Salmo salar): Changes in salinity tolerance, gill Na+, K+-ATPase activity, and plasma thyroid hormones.Canadian Journal of Fisheries and Aquatic Sciences 45:1462–1468.CrossRefGoogle Scholar
  26. McKinney, M. L., andK. J. McNamara. 1991. Heterochrony. Plenum Press, New York.Google Scholar
  27. Montgomery, W. L., S. D. McCormick, R. J. Naiman, F. G. Whoriskey, andG. Black. 1990. Anadromous behaviour of brook charr (Salvelinus fontinalis) in the Moisie river, Quebec.Polish Archive of Hydrobiology 37:43–61.Google Scholar
  28. Naiman, R. J., S. D. McCormick, W. L. Montgomery, andR. Morin. 1987. Anadromous brook charr,Salvelinus fontinalis. Opportunities and constraints for population enhancement.Marine Fisheries Review 49:1–13.Google Scholar
  29. Norden, C. R.. 1961. Comparative osteology of representative salmonid fishes, with particular reference to the grayling (Thymallus arcticus) and its phylogeny.Journal of the Fisheries Research Board of Canada 18:679–791.Google Scholar
  30. Parry, G. 1960. The development of salinity tolerance in the salmon,Salmo salar (L.) and some related species.Journal of Experimental Biology 37:425–434.Google Scholar
  31. Randall, D. andC. Brauner. 1991. Effects of environmental factors on exercise in fish.The Journal of Experimental Biology 160:113–126.Google Scholar
  32. Rosenkilde, P. 1979. The thyroid hormones in amphibia, p. 437–491.In E. J. W. Barrington (ed.), Hormones and Evolution. Academic Press, New York.Google Scholar
  33. Rounsefell, G. A. 1958. Anadromy in North American salmonidae.Fishery Bulletin 58:171–185.Google Scholar
  34. Sakamoto, T., S. D. McCormick, andT. Hirano. 1993. Osmoregulatory actions of growth hormone and its mode of action in salmonids: A review.Fish Physiology and Biochemistry 11:155–164.CrossRefGoogle Scholar
  35. Salo, E. O.. 1991. Life history of chum salmon (Oncorhynchus kisutch), p. 231–309.In C. Groot and L. Margolis (eds.), Pacific Salmon Life Histories. University of British Columbia Press, Vancouver.Google Scholar
  36. Saunders, R. L., E. D. Henderson, andP. R. Harmon. 1985. Effects of photoperiod on juvenile growth and smolting of Atlantic salmon and subsequent survival and growth in sea cages.Aquaculture 45:55–66.CrossRefGoogle Scholar
  37. Scott, W. B., andE. J. Crossman. 1973. Freshwater fishes of Canada. Fisheries Research Board of Canada, Ottawa.Google Scholar
  38. Specker, J. L. 1982. Interrenal function and smoltification.Aquaculture 28:59–66.CrossRefGoogle Scholar
  39. Sullivan, C. V., W. W. Dickhoff, S. D. Brewer, andG. P. Johnston. 1983. Plasma thyroid-hormone concentrations and gill (Na+K+)-ATPase activities in postemergent pink salmon.Transactions of the American Fisheries Society 112:825–829.CrossRefGoogle Scholar
  40. Thorpe, J. E. 1982. Migration in salmonids, with special reference to juvenile movements in freshwater, p. 86–97.In E. L. Brannon and E. O. Salo (eds.), Proceedings of the Salmon and Trout Migratory Behavior Symposium. University of Washington, Seattle, Washington.Google Scholar
  41. Thorpe, J. E. 1994. Salmonid fishes and the estuarine environment.Estuaries 17:76–93.CrossRefGoogle Scholar
  42. Tytler, P., J. E. Thorpe, andW. M. Shearer. 1978. Ultrasonic tracking of the movements of Atlantic salmon smolts (Salmo salar L.) in the estuaries of two Scottish rivers.Journal of Fish Biology 12:575–586.CrossRefGoogle Scholar
  43. Wagner, H. H., F. P. Conte, andJ. L. Fessler. 1969. Development of osmotic and ionic regulation in two races of chinook salmonO. tshawytscha.Comparative Biochemistry and Physiology 29:325–341.CrossRefGoogle Scholar
  44. Wedemeyer, G. A., R. L. Saunders, andW. C. Clarke. 1980. Environmental factors affecting smoltification and early marine survival of anadromous salmonids.Marine Fisheries Review 42:1–14.Google Scholar
  45. Weisbart, M. 1968. Osmotic and ionic regulation in embryos, alevins, and fry of the five species of Pacific salmon.Canadian Journal of Zoology 46:385–397.CrossRefGoogle Scholar
  46. Wilson, M. V. H. 1977. Middle eocene freshwater fishes from British Columbia.Life Sciences Contributions of the Royal Ontario Museum 113:1–61.Google Scholar

Copyright information

© Estuarine Research Federation 1994

Authors and Affiliations

  • Stephen D. McCormick
    • 1
  1. 1.Anadromous Fish Research CenterUnited States Fish and Wildlife ServiceTurners Falls

Personalised recommendations