Abstract
Experimental observations suggest that the gametogenic cycle of Mytilus edulis from Swansea Bay, South Wales (U.K.) is adversely modified by the combined effects of temperature, nutritive and sublethal metal-induced stress. During low temperature stress, oogenesis remained in the vegetative stage and vitellogenesis only commenced when temperatures were raised to ambient levels. Copper was the most toxic metal, although its uptake was slowest. A concentration of 0.05 mg l-1 of this metal proved lethal at ambient temperatures, although at low temperatures there was no mortality. Copper suppressed both the growth of young oocytes and vitellogenesis in larger oocytes. Zinc was less toxic than copper, although this also inhibited oocyte development and resulted in severe lysis of gametes. Cadmium was the least toxic of the three metals studied and suppressed gametogenesis only in the initial stages of gonad development. The low toxicity of cadmium to gametogenesis may be a result of its high solubility and its possible storage in the digestive gland.
Similar content being viewed by others
Literature Cited
Ansell, A. D., F. A. Loosemore and F. F. Lander: Studies on the hard shell clam Venus mercenaria in British waters. II. Seasonal cycle in condition and biochemical composition. J. appl. Ecol. 1, 83–95 (1964)
Baird, R. H.: Measurement of condition in mussels and oysters. J. Cons. perm. int. Explor. Mer 23, 249–257 (1958)
Baird, R. H.: Factors affecting the growth and condition of mussels (Mytilus edulis). Fishery Invest., Lond. (Ser. 2) 25, 1–33 (1966)
Baric, A. and M. Branica: Polarography of seawater. I. Ionic state of cadmium and zinc in seawater. J. polarogr. Soc. 13, 4–8 (1967)
Bayne, B. L.: Growth and the delay of metamorphosis of the larvae of Mytilus edulis (L.). Ophelia 2, 1–47 (1965).
Bayne, B. L.: Marine mussels: their ecology and physiology, 410 pp. Cambridge: University Press 1976
Bayne, B. L. and R. J. Thompson: Some physiological consequences of keeping Mytilus edulis in the laboratory. Helgoländer wiss. Meeresunters. 20, 526–552 (1970)
Bryan, G. W.: The effects of heavy metals (other than mercury) on marine and estuarine organisms. Proc. R. Soc. (Ser. B) 177, 389–410 (1971)
Caddy, J. F.: Maturation of gametes and spawning in Macoma balthica (L.). Can J. Zool. 45, 955–965 (1967)
Calabrese, A., R. S. Collier, D. A. Nelson and J. R. MacInnes: The toxicity of heavy metals to embryos of the American oyster Crassostrea virginica. Mar. Biol. 18, 162–166 (1973)
Calabrese, A., J. R. MacInnes, D. A. Nelson and J. E. Miller: Survival and growth of bivalve larvae under heavy-metal stress. Mar. Biol. 41, 179–184 (1977)
Calabrese, A. and D. A. Nelson: Inhibition of embryonic development of the hard clam Mercenaria mercenaria by heavy metals. Bull. envir. Contam. Toxicol 11, 92–97 (1974)
Classy d'Silva and T. W. Kureishy: Experimental studies on the accumulation of copper and zinc in the green mussel. Mar. Pollut. Bull. 9, 187–190 (1978)
Coe, W. R. and H. J. Turner, Jr.: Development of the gonads and gametes in the soft shell clam (Mya arenaria). J. Morph. 62, 91–111 (1938)
Daniel, R. J.: Seasonal changes in the chemical composition of the mussel (Mytilus edulis). Rep. Lancs. Sea-Fish. Labs 30, 74–84 (1921)
Fujiya, M.: Studies on the effects of copper dissolved in seawater on oysters. Bull. Jap. Soc. scient. Fish. 26, 462–468 (1960)
Gabbott, P. A. and B. L. Bayne: Biochemical effects of temperature and nutritive stress on Mytilus edulis L. J. mar. biol. Ass. U.K. 53, 269–286 (1973)
Giese, A. C.: Comparative physiology: annual reproductive cycles of marine invertebrates. A. Rev. Physiol. 21, 547–576 (1959)
Giese, A. C.: A new approach to the biochemical composition of the mollusc body. Oceanogr. mar. Biol. A. Rev. 7, 175–229 (1969)
Goldberg, E. D.: The mussel watch — a first step in global marine monitoring. Mar. Pollut. Bull. 6, p. 111 (1975)
Ingols, R. S.: Evaluation of toxicity. Sewage ind. Wastes 26, p. 27 (1955)
Kanwisher, J. W.: Freezing in intertidal animals. Biol. Bull. mar. biol. Lab., Woods Hole 109, 56–63 (1955)
Kanwisher, J. W.: Freezing in intertidal animals. In: Cryobiology, pp 487–494. Ed. by H. T. Merryman. New York: Academic Press 1966
Kinne, O.: Temperature: animals — invertebrates. In: Marine ecology. Vol. I. Environmental factors, Pt 1, pp 407–514. Ed. by O. Kinne, London: Wiley-Interscience 1970
Krauskopf, K. B.: Factors controlling the concentrations of thrteen rare metals in seawater. Geochim. cosmochim. Acta. 9, 1–32B (1956)
Loosanoff, V. L.: Gametogenesis and spawning of the European oyster O. edulis in waters off Maine. Biol. Bull. mar. biol. Lab., Woods Hole 122, 86–94 (1963)
Loosanoff, V. L.: Gonad development and discharge of spawn in oysters of Long Island Sound. Biol. Bull. mar. biol. Lab., Woods Hole 129, 546–561 (1965)
Loosanoff, V. L. and H. C. Davis: Delayed spawning of lamellibranchs by low temperature. J. mar. Res. 10, 197–202 (1951)
Lubet, P.: Recherches sur le cycle sexuel et l'émission des gamètes chez les mytiledes et les pectinides (mollusque bivalves). Revue Trav. Inst. (scient. tech.) Pêch. marit. 23, 396–545 (1959)
Martin, J. M., F. M. Pittz and D. J. Reish: Studies on the Mytilus edulis community in Alamitos Bay, California. V. The effects of heavy metals on byssal thread production. Veliger 18, 183–188 (1975)
Mount D. I.: Chronic toxicity of copper in fathead minnow (Primephales promelas Rafinesque). Wat. Res. 2, 215–223 (1968)
Orton, J. H.: Sea temperature breeding and distribution in marine animals. J. mar. biol. Ass. U.K. 12, 339–366 (1920)
Pedan, J. D., J. M. Crothers, C. E. Waterfall and J. Beasley: Heavy metals in Somerset marine organisms. Mar. Pollut. Bull. 4, 7–9 (1973)
Phillips, D. J. H.: The common mussel Mutilus edulis as an indicator of pollution by zinc, cadmium, lead and copper. I. Effects of environmental variables on uptake of metals. Mar. Biol. 38, 59–69 (1976a)
Phillips, D. J. H.: The common mussel Mytilus edulis as an indicator of pollution by zinc, cadmium, lead and copper. II. Relationship of metals in the mussel to those discharged by industry. Mar. Biol. 38, 71–80 (1976b)
Piro, A.: Physiochemical states of some trace metals in seawater which are of interest from the radio-contamination standpoint. Revue int. Océanogr. méd. 20, 133–149 (1970)
Preston, A. and D. F. Jefferies: Aquatic aspects in chronic and acute contamination situations. In: Environmental contamination by radio-active materials, pp 183–211. Vienna: International Atomic Energy Agency 1969
Preston, E. M.: The importance of ingestion of chromium 51 accumulated by Crassostrea virginica. J. exp. mar. Biol. Ecol. 6, 47–54 (1971)
Pringle, B. H., D. E. Hossong, E. L. Katz and S. J. Mulanka: Trace metal accumulation by estuarine molluscs. J. sanit. Engng Div. Am. Soc. civ. Engrs 94, 455–475 (1968)
Quick, J. A.: A preliminary investigation. The effect of elevated temperature on the american oysger Crassostrea virginica (Gmelin). Prof. Pap. Ser. Dep. nat. Resour. mar. Res. Lab. Fla 15, 1–190 (1971)
Raven, Chr. P.: Oogenesis: the storage of developmental information, 226 pp. New York: Pergamon Press 1961
Romeril, M. G.: The uptake and distribution of 65Zn in oysters. Mar. Biol. 9, 347–354 (1971)
Sastry, A. N.: The relationships among food, temperature and gonad development of the bay scallop Aequipecten irradians Lamarck. Physiol. Zoöl. 44, 44–53 (1968)
Sastry, A. N.: Environmental regulation of oocyte growth in the bay scallop Aequipecten irradians Lamarck. Experientia 26, 1371–1372 (1970)
Sastry, A. N. and N. J. Blake: Regulation of gonad development in the bay scallop Aequipecten irradians Lamarck. Biol. Bull. mar. biol. Lab., Woods Hole 140, 274–283 (1971)
Schulz-Baldes, M.: Lead uptake from sea water and food, and lead loss in the common mussel Mytilus edulis. Mar. Biol. 25, 177–193 (1974)
Scott, D. M. and C. W. Major: The effect of copper (II) on survival, respiration and heart rate in the common blue mussel, Mytilus edulis. Biol. Bull. mar. biol. Lab., Woods Hole, 143, 679–688 (1972)
Shuster, C. N. and B. H. Pringle: Trace metal accumulation by the American eastern oyster Crassostrea virginica. Proc. natn. Shellfish. Ass. 79, 91–103 (1969)
Thompson, R. H., N. A. Ratcliff and B. L. Bayne: Effects of starvation on structure and function in the digestive gland of the mussel (Mytilus edulis). J. mar. biol. Ass. U.K. 54, 699–712 (1974)
Viarengo A., M. Pertica., G. Mancinelli., G. Zanicchi and M. Oruneso: Rapid induction of copper binding proteins in the gills of metal exposed mussels. Comp. Biochem. Physiol. 67c, 215–218 (1980)
Vivian, C. M. G.: The distribution of certein trace metals in seawater and sediments in relation to local sources, Swansea Bay and adjacent points in the Bristol Channel, 212 pp. Ph. D. thesis, University of Wales 1976
Walne, P. R.: The seasonal variation of meat and glycogen content of seven populations of oysters, Ostrea edulis and a review of the literature. Fishery Invest., Lond. (Ser. 2) 26, 1–35 (1970)
Widdows, J.: Effect of temperature and food on the heart beat, ventilation rate and oxygen uptake of Mytilus edulis. Mar. Biol. 20, 269–276 (1973)
Widdows, J.: Physiological adaptation of Mytilus edulis L. to fluctuating temperatures. J. comp. Physiol. 105, 115–128 (1976)
Yoshida, M.: Some observations on the maturation of the sea urchin, Diadema setosum. Annotnes zool. jap. 25, 265–271 (1952)
Author information
Authors and Affiliations
Additional information
Communicated by J. Mauchline, Oban
Rights and permissions
About this article
Cite this article
Myint, U.M., Tyler, P.A. Effects of temperature, nutritive and metal stressors on the reproductive biology of Mytilus edulis . Marine Biology 67, 209–223 (1982). https://doi.org/10.1007/BF00401287
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00401287