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Lack of metabolic temperature compensation in the intertidal gastropods, Littorina saxatilis (Olivi) and L. obtusata (L.)

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Abstract

Two intertidal snails, Littorina saxatilis (Olivi, 1972) (upper eulittoral fringe/maritime zone) and Littorina obtusata (Linnaeus, 1758) (lower eulittoral) were collected from a boulder shore on Nobska Point, Cape Cod, Massachusetts, in July and acclimated for 15–20 days at 4 ° or 21 °C. Oxygen consumption rate (Vo2) was determined for 11–15 subsamples of individuals at 4 °, 11 ° and 21 °C with silver/platinum oxygen electrodes. Multiple factor analysis of variance (MFANOVA) of lo10 transformed values of whole animal Vo2 with log10 dry tissue weight (DTW) as a covariant revealed that increased test temperature induced a significant increase in Vo2 in both species (P<0.00001). In contrast, MFANOVA revealed that temperature acclimation did not affect Vo2 in either L. saxatilis (P= 0.35) or L. obtusata (P= 0.095). Thus, neither species displayed a capacity for the typical metabolic temperature compensation marked by an increase in Vo2 at any one test temperature in individuals acclimated to a lower temperature that is characteristic of most ectothermic animals. Lack of capacity for metabolic temperature acclimation has also been reported in other littorinid snail species, and may be characteristic of the group as a whole. Lack of capacity for respiratory temperature acclimation in these two species and other littorinids may reflect the extensive semi-diurnal temperature variation that they are exposed to in their eulittoral and eulittoral fringe/maritime zone habitats. In these habitats, any metabolic benefits derived from longer-term temperature compensation of metabolic rates are negated by extreme daily temperature fluctuations. Instead, littorinid species appear to have evolved mechanisms for immediate metabolic regulation which, in L. saxatilis and L. obtusata and other littorinids, appear to centre on a unique ability for near instantaneous suppression of metabolic rate and entrance into short-term metabolic diapause at temperatures above 20–35 °C, making typical seasonal respiratory compensation mechanisms characteristic of most ectotherms of little adaptive value to littorinid species.

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References

  • Aldridge, D. W., W. D. Russell-Hunter & R. F. McMahon, 1995. Effects of ambient temperature and of temperature acclimation on nitrogen excretion and differential catabolism of protein and nonprotein resources in the intertidal snails, Littorina saxatilis (Olivi) and L. obtusata (L.). Hydrobiologia 309 (Dev. Hydrobiol. 111): 101–109.

    CAS  Google Scholar 

  • Apley, M. L., 1970. Field studies on life history, gonadal cycle and reproductive periodicity in Melampus bidentatus (Pulmonata: Ellobiidae). Malacologia 10: 381–397.

    Google Scholar 

  • Bayne, B. L., R. J. Thompson & J. Widdows, 1973. Some effects of temperature and food on the rate of oxygen consumption of Mytilus edulis L. In W. Wieser (ed.), Effects of Temperature on Ectothermic Organisms. Springer-Verlag, New York (N.Y.); Berlin: 181–193.

    Google Scholar 

  • Boyden, C. R., 1972. The behavior, survival and respiration of the cockles, Cerastoderma edule and C. glaucum in air. J. mar. biol. Ass. U.K. 52: 661–680.

    Article  Google Scholar 

  • Cavanaugh, G. M., 1956. Formulae and methods V. of the marine Biological Laboratory Chemical Room. Marine Biological Laboratory, Woods Hole (Massachusetts), 87 pp.

    Google Scholar 

  • Cossins, A. R., 1981. The adaptation of membrane dynamic structure to temperature. In G. J. Morris & A. Clarke (eds), Effects of Low Temperatures on Biological Membranes. Academic Press, London: 83–106.

    Google Scholar 

  • Cossins, A. R. & K. Bowler, 1987. Temperature biology of animals. Chapman and Hall, London; New York (N.Y.), 339 pp.

    Google Scholar 

  • Cossins, A. R., K. Bowler & C. L. Prosser, 1981. Homeoviscous adaptations and its effects on membrane bound proteins. J. therm. Biol. 6: 183–187.

    Article  CAS  Google Scholar 

  • Griffiths, R. J., 1977a. Thermal stress and the biology of Actinia equina L. (Anthozoa). J. exp. mar. Biol. Ecol. 27: 141–154.

    Article  Google Scholar 

  • Griffiths, R. J., 1977b. Temperature acclimation in Actinia equina L. (Anthozoa). J. exp. mar. Biol. Ecol. 28: 285–292.

    Article  Google Scholar 

  • Grainger, J. N. R., 1969. Factors affecting the body temperature of Patella. Verh. dt. zool. Ges. 1968: 479–487.

  • Hochachka, P. W. & G. N. Somero, 1984. Biochemical adaptation. Princeton University Press, Princeton (N.J.), 537 pp.

    Google Scholar 

  • Kennedy, V. S. & J. A. Mihursky, 1972. Effects of temperature on the respiratory metabolism of three Chesapeake Bay bivalves. Chesapeake Sci. 13: 1–22.

    Article  Google Scholar 

  • Lewis, J. B., 1963. Environmental and tissue temperatures of some tropical intertidal marine animals. Biol. Bull. 124: 277–284.

    Google Scholar 

  • Markel, R. P., 1971. Temperature relations in two species of tropical west American littorines. Ecology 52: 1126–1130.

    Article  Google Scholar 

  • McMahon, R. F., 1988. Respiratory response to periodic emergence in intertidal molluscs. Am. Zool. 28: 97–114.

    Google Scholar 

  • McMahon, R. F., 1990. Thermal tolerance, evaporative water loss, air-water oxygen consumption and zonation of intertidal prosobranchs: a new synthesis. Hydrobiologia 193 (Dev. hydrobiol. 56): 241–260.

    Article  Google Scholar 

  • McMahon, R. F., 1992. Respiratory response to temperature and hypoxia in intertidal gastropods from the Texas coast of the Gulf of Mexico. In J. Grahame, P. J. Mill & D. G. Reid (eds), Proceedings of the 3rd International Symposium on Littorinid Biology. Malacological Society of London, London: 45–59.

    Google Scholar 

  • McMahon, R. F. & W. D. Russell-Hunter, 1977. Temperature relations of aerial and aquatic respiration in six littoral snails in relation to their vertical zonation. Biol. Bull. 152: 182–198.

    PubMed  CAS  Google Scholar 

  • McMahon, R. F. & W. D. Russell-Hunter, 1978. Respiratory responses to low oxygen stress in marine littoral and sublittoral snails. Physiol. Zool. 51: 408–424.

    Google Scholar 

  • McMahon, R. F. & W. D. Russell-Hunter, 1981. The effects of physical variables and acclimation on survival and oxygen consumption in the high littoral salt-marsh snail, Melampus bidentatus Say. Biol. Bull. 161: 246–269.

    Google Scholar 

  • McMahon, R. F. & J. G. Wilson, 1981. Seasonal respiratory responses to temperature and hypoxia in relation to burrowing depth in three intertidal bivalves. J. therm. Biol. 6: 267–277.

    Article  Google Scholar 

  • Newell, R. C., 1979. Biology of intertidal animals, third edition. Marine Ecological Surveys Ltd., Faversham, Kent, U.K., 781 pp.

    Google Scholar 

  • Newell, R. C. & B. L. Bayne, 1973. A review on temperature and metabolic adaptation in intertidal marine invertebrates. Neth. J. Sea Res. 7: 421–433.

    Article  Google Scholar 

  • Newell, R. C. & L. H. Kofoed, 1977. Adjustment of the components of energy balance in the gastropod Crepidula fornicata in response to thermal acclimation. Mar. Biol. 44: 275–286.

    Article  Google Scholar 

  • Newell, R. C. & V. I. Pye, 1970a. The influence of thermal acclimation on the relation between oxygen consumption and temperature in Littorina littorea (L.) and Mytilus edulis L. Comp. Biochem. Physiol. 34: 367–383.

    Article  Google Scholar 

  • Newell, R. C. & V. I. Pye, 1970b. Seasonal changes in the effect of temperature on the oxygen consumption of the winkle, Littorina littorea (L.) and the mussel Mytilus edulis L. Comp. Biochem. Physiol. 34: 367–383.

    Article  Google Scholar 

  • Newell, R. C. & V. I. Pye, 1971. Quantitative aspects of the relationship between metabolism and temperature in the winkle Littorina littorea (L.). Comp. Biochem. Physiol. 38B: 635–650.

    Article  CAS  Google Scholar 

  • Newell, R. C. & A. Roy, 1973. A statistical model relating the oxygen consumption of a mollusk (Littorina littorea) to activity, body size, and environmental conditions. Physiol. Zool. 46: 253–275.

    Google Scholar 

  • Newell, R. C., L. G. Johnson & L. H. Kofoed, 1977. Adjustment of the components of energy balance in response to temperature change in Ostrea edulis. Oecologia 30: 97–110.

    Article  Google Scholar 

  • Precht, H., J. Christophersen, H. Hensel & W. Larcher, 1973. Temperature and life. Springer-Verlag, New York (N.Y.); Berlin, 779 pp.

    Google Scholar 

  • Prosser, C. L. & J. E. Heath, 1991. Temperature. In C. L. Prosser (ed.), Environmental and metabolic animal physiology. Wiley-Liss, New York (N.Y.); Chichester, Brisbane; Singapore: 109–165.

    Google Scholar 

  • Reid, D. G., 1989. The comparative morphology, phylogeny and evolution of the gastropod family, Littorinidae. Phil. Trans. r. Soc., Lond. B 324: 1–110.

    Google Scholar 

  • Reid, D. G., 1990. A cladistic phylogeny of the genus Littorina (Gastropoda): implications for evolution of reproductive strategies and for classification. Hydrobiologia. 193 (Dev. Hydrobiol. 56): 1–19.

    Article  Google Scholar 

  • Russell-Hunter, W. D. & M. L. Apley, 1965. A condition of temporary hyperthermia in a marine littoral snail. Biol. Bull. 129: 408–409.

    Google Scholar 

  • Russell-Hunter, W. D., R. F. McMahon & D. W. Aldridge, 1980. Lack of respiratory response to temperature acclimation in two littorinid snails. Biol. Bull. 159: 452.

    Google Scholar 

  • Shirley, T. C., G. J. Denoux & W. B. Stickle, 1978. Seasonal respiration in the marsh periwinkle, Littorina irrorata. Biol. Bull. 154: 322–334.

    Google Scholar 

  • Shumway, S. E. & R. K. Koehn, 1982. Oxygen consumption in the American oyster Crassostrea virginica. Mar. Ecol. Prog. Ser. 9: 59–68.

    Google Scholar 

  • Southward, A. J., 1958. Note on the temperature tolerances of some intertidal animals in relation to environmental temperatures and geographical distribution. J. mar. biol. Ass. U.K. 37: 49–66.

    Article  Google Scholar 

  • Underwood, A. J., 1979. The ecology of intertidal gastropods. Adv. mar. Biol. 16: 111–210.

    Article  Google Scholar 

  • Vermeij, G. J., 1971a. Temperature relationships of some tropical Pacific gastropods. Mar. Biol. 10: 308–314.

    Article  Google Scholar 

  • Vermeij, G. J., 1971b. Substratum relationships of some tropical Pacific intertidal gastropods. Mar. Biol. 10: 315–320.

    Article  Google Scholar 

  • Vernberg, F. J., 1969. Acclimation of intertidal crabs. Am. Zool. 9: 333–341.

    Google Scholar 

  • Vernberg, W. B. & F. J. Vernberg, 1972. Environmental physiology of marine animals. Springer-Verlag, New York (N.Y.); Berlin, 346 pp.

    Google Scholar 

  • Wolcott, T. G., 1973. Physiological ecology and intertidal zonation in limpets (Acmaea): a critical look at ‘limiting factors’. Biol. Bull. 145: 389–422.

    Google Scholar 

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Author notes

  1. W. D. Russell-Hunter

    Present address: Department of Biology, North Carolina Agricultural and Technical State University, 27411, Greensboro, North Carolina, USA

Authors and Affiliations

  1. Marine Biological Laboratory, 02543, Woods Hole, Massachusetts, USA

    Robert F. McMahon, W. D. Russell-Hunter & David W. Aldridge

  2. Section of Comparative Physiology, Department of Biology, The University of Texas at Arlington, Box 19498, 76019-0498, Arlington, Texas, USA

    Robert F. McMahon

  3. Department of Biology, Syracuse University, 13210, Syracuse, New York, USA

    W. D. Russell-Hunter

  4. 711 Howard Street, 21601-3934, Easton, Maryland, USA

    David W. Aldridge

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McMahon, R.F., Russell-Hunter, W.D. & Aldridge, D.W. Lack of metabolic temperature compensation in the intertidal gastropods, Littorina saxatilis (Olivi) and L. obtusata (L.). Hydrobiologia 309, 89–100 (1995). https://doi.org/10.1007/BF00014475

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