Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T13:33:10.810Z Has data issue: false hasContentIssue false

Does size matter? The effects of body size and declining oxygen tension on oxygen uptake in gastropods

Published online by Cambridge University Press:  03 November 2011

Islay D. Marsden*
Affiliation:
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand
Sandra E. Shumway
Affiliation:
Department of Marine Sciences, University of Connecticut, 1080 Shennecossett Road, Groton, CT 06340
Dianna K. Padilla
Affiliation:
Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY 11794-5245
*
Correspondence should be addressed to: I. Marsden, School of Biological Sciences, University of Canterbury, Christchurch, New Zealand email: islay.marsden@canterbury.ac.nz

Abstract

Metabolic rate is one of the most frequently measured physiological variables and the relationship between oxygen uptake and body mass is one of the most controversial issues in biology. The present study used closed chamber respirometry to compare the oxygen uptake of 32 species of benthic British gastropod molluscs of a wide size-range (from less than 0.001 g to greater than 10 g dry tissue weight). We investigated the effects of body size on the respiratory rate at 10°C to explore the evolutionary and phylogenetically determined patterns of metabolic scaling both among different gastropods groups, and within siphonate and asiphonate caenogastropods. Resting oxygen uptake (O2) increased with body mass (W) with a slope value of 0.6 using both ordinary least squares (OLS) and standard major axis (SMA) where N = 488, over a 6 fold range of body mass. The slopes b of the regression lines relating oxygen uptake to body mass were similar for all heterobranch molluscs and most caenogastropods. Highest mass-specific rates for oxygen consumption were found for the smallest littorinid species. Trophic mode significantly affected the amount of oxygen consumed with higher oxygen uptake in herbivores than other groups, including detritivores and predators. All of the gastropods reduced their oxygen consumption when exposed to declining oxygen conditions; however, about a third of the species exhibited partial regulation at higher oxygen partial pressures. When exposed to 20% normal saturation levels, smaller gastropods respired at approximately 25% of their rates in fully saturated seawater whereas larger species (above 0.1 g dry tissue weight) respired at approximately 35% of the values recorded at full saturation. Our study suggests that a scaling exponent relating O2 to body mass of 0.6 is typical and may be ‘universal’ for gastropods. It is below the 0.75 scaling exponent which has been proposed for ectothermic invertebrates. It is concluded that size does matter in determining the metabolic patterns of gastropods and that the quantity of oxygen consumed and the energy balance of gastropods is affected by activity, food type and exposure to declining oxygen conditions.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alexander, J.E. and McMahon, R.F. (2004) Respiratory response to temperature and hypoxia in the zebra mussel Dreissena polymorpha. Comparative Biochemistry and Physiology A 137, 425434.Google Scholar
Anderson, K.J. and Jetz, W. (2005) The broad-scale ecology of energy expenditure of endotherms. Ecology Letters 8, 310318.CrossRefGoogle Scholar
Angilletta, M.J. and Dunham, A.E. (2003) The temperature–size rule in ectotherms: simple evolutionary explanations may not be general. American Naturalist 162, 332342.Google Scholar
Bayne, B.L. (1971a) Oxygen consumption by three species of lamellibranch mollusk in declining ambient oxygen tension. Comparative Biochemistry and Physiology 40A, 955970.CrossRefGoogle Scholar
Bayne, B.L. (1971b) Ventilation, the heart beat and oxygen uptake by Mytilus edulis L. in declining oxygen tension. Comparative Biochemistry and Physiology 40A, 10651085.CrossRefGoogle Scholar
Bayne, B.L. and Scullard, C. (1978) Rates of oxygen consumption by Thais (Nucella) lapillus. Journal of Experimental Marine Biology and Ecology 32, 97111.CrossRefGoogle Scholar
Bayne, B.L., Thompson, R.J. and Widdows, J. (1976) Physiology 1. In Bayne, B.L. (ed.) Marine mussels: their ecology and physiology. London: Cambridge University Press, pp. 121202.Google Scholar
Bougrier, S., Geairon, P., Deslouspaol, J.M., Bacher, C. and Jonquieres, G. (1995) Allometric relationships and effects of temperature on clearance and oxygen-consumption rates of Crassostrea gigas (Thunberg). Aquaculture 134, 143154.CrossRefGoogle Scholar
Branch, G.M. and Newell, R.C. (1978) A comparative study of metabolic energy expenditure in the limpets Patella cochlear, P. oculus and P. granularis . Marine Biology 49, 351361.CrossRefGoogle Scholar
Bricelj, V.M. and Shumway, S.E. (1991) Physiology: energy acquisition and utilization. In Shumway, S.E. (ed.) Scallops: biology, ecology and aquaculture. Amsterdam: Elsevier Science Publishers, pp. 305346.Google Scholar
Bridges, C.R. and Butler, P.J. (1989) Techniques in comparative respiratory physiology: an experimental approach. New York: Cambridge University Press.Google Scholar
Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M. and West, G.B. (2004) Toward a metabolic theory of ecology. Ecology 85, 17711789.Google Scholar
Bruce, J.R., Coleman, J.S. and Jones, N.S. (eds) (1963) Marine fauna of the Isle of Man and its surrounding seas. Liverpool: Liverpool University Press.Google Scholar
Burrows, M.T. and Hughes, R.N. (1991) Variation in foraging behaviour among individuals and populations of dogwhelks, Nucella lapillus: natural constraints on energy intake. Journal of Animal Ecology 60, 497514.Google Scholar
Crisp, M. (1978) Effects of feeding on the behaviour of Nassarius species. Journal of the Marine Biological Association of the United Kingdom 58, 659669.Google Scholar
Crisp, M., Davenport, J. and Shumway, S.E. (1978) Effects of feeding and chemical stimulation on oxygen uptake of Nassarius reticulatus (Gastropoda: Prosobranchia). Journal of the Marine Biological Association of the United Kingdom 51, 378399.Google Scholar
Davies, P.S. (1966) Physiological ecology of Patella. 1. The effect of body size and temperature on metabolic rate. Journal of the Marine Biological Association of the United Kingdom 46, 646658.Google Scholar
Dickens, F. and Neil, E. (eds) (1964) Oxygen in the animal organism. Oxford: Pergamon Press Ltd.Google Scholar
Dolnik, V.R. (2002) Standard metabolic rate in vertebrate animals: causes of differences between poikilothermic and homeothermic classes. Zoolichesky Zhurnal 8, 643654.Google Scholar
Eales, N.B. (1967) The littoral fauna of the British Isles: a handbook for collectors. Cambridge: Cambridge University Press, 306 pp.Google Scholar
Elgar, M.A. and Harvey, P.H. (1987) Basal metabolic rates in mammals: allometry, phylogeny and ecology. Functional Ecology 1, 2536.Google Scholar
Fretter, V. and Graham, A. (1962) British prosobranch molluscs. London: The Ray Society and Adlard and Son Ltd.Google Scholar
Gillooly, J.F., Brown, J.H., West, G.B., Savage, V.M. and Charnov, E.L. (2001) Effects of size and temperature on metabolic rate. Science 293, 22482251.Google Scholar
Ginzburg, L. and Dalmuth, J. (2008) The space–lifetime hypothesis: viewing organisms in four dimensions, literally. American Naturalist 171, 125131.CrossRefGoogle ScholarPubMed
Glazier, D.S. (2005) Beyond the ‘3/4-power law’: variation in the intra- and interspecific scaling of metabolic rate in animals. Biological Reviews 80, 611662.CrossRefGoogle ScholarPubMed
Glazier, D.S. (2006) The 3/4-power law is not universal: evolution of isometric, ontogenetic metabolic scaling in pelagic animals. BioScience 56, 325332.Google Scholar
Gosner, K.L. (1971) Guide to identification of marine estuarine invertebrates. New York: Wiley-Interscience, John Wiley and Sons, Inc.Google Scholar
Guralnick, R. and Smith, K. (1999) Historical and biomechanical analysis of integration and dissociation in molluscan feeding, with special emphasis on the true limpets (Patellogastropoda: Gastropoda). Journal of Morphology 241, 175195.Google Scholar
Haure, J., Penisson, C., Bougrier, S. and Baud, J.P. (1998) Influence of temperature on clearance and oxygen consumption rates of the flat oyster Ostrea edulis: determination of allometric coefficients. Aquaculture 169, 211224.Google Scholar
Hemmingson, A.M. (1960) Energy metabolism as related to body size and respiratory surfaces and its evolution. Report from Steno Memorial Hospital, Copenhagen 9, 7110.Google Scholar
Hochachka, P.W. (2002) Biochemical adaptation mechanism and process in physiological evolution. Oxford: Oxford University Press.CrossRefGoogle Scholar
Hochachka, P.W., Darveau, C.A., Andrews, R.D. and Suarez, R.K. (2003) Allometric cascade: a model for resolving body mass effects on metabolism. Comparative Biochemistry and Physiology A 134, 675691.Google Scholar
Holker, F. (2003) The metabolic rate of roach in relation to body size and temperature. Journal of Fish Biology 62, 565579.Google Scholar
Holmes, S.P., Miller, N. and Weber, A. (2002) The respiration and hypoxic tolerance of Nucula nitidosa and N. nucleus: factors responsible for determining their distribution? Journal of the Marine Biological Association of the United Kingdom 82, 971981.Google Scholar
Howson, C.M. and Picton, B.E. (1997) The species directory of the marine fauna and flora of the British Isles and surrounding seas. Ross-on-Wye: Marine Conservation Society, 507 pp.Google Scholar
Hughes, G.M. (1963) Comparative physiology of vertebrate respiration. Cambridge, MA: Harvard University Press.Google Scholar
Innes, A.J., Marsden, I.D. and Wong, P.P.S. (1984) Bimodal respiration of intertidal pulmonates. Comparative Biochemistry and Physiology 77A, 441445.CrossRefGoogle Scholar
Kemp, P. and Bertness, M.D. (1984) Snail shape and growth rates: evidence for plastic shell allometry in Littorina littorea. Proceedings of the National Academy of Sciences of the United States of America 81, 811813.Google Scholar
Kinne, O. (1970) Temperature—invertebrates. In Kinne, O. (ed.) Marine ecology 1. Environmental factors. London: Wiley-Interscience, pp. 407514.Google Scholar
Kleiber, M. (1932) Body size and metabolism. Hilgardia 6, 315353.Google Scholar
Lewis, J.R. (1961) The littoral zone on a rocky shore—a biological or physical entity? Oikos 12, 380–301.Google Scholar
Lewis, J.B. (1971) Comparative respiration of some tropical intertidal gastropods. Journal of Experimental Marine Biology and Ecology 6, 101108.Google Scholar
Lighton, J.R.B. and Felden, L.J. (1995) Mass scaling for metabolic rates in ticks: a valid case of low metabolic rates in sit-and -wait strategies. Physiological Zoology 68, 4362.Google Scholar
Lindberg, D.R. and Ponder, W.F. (2001) The influence of classification on the evolutionary interpretation of structure—a reevaluation of the evolutionary interpretation of the pallial cavity of gastropod molluscs. Organisms Diversity and Evolution 1, 273299.Google Scholar
Lindstedt, S.L. and Schaeffer, P.J. (2002) Use of allometry in predicting anatomical and physiological parameters of mammals. Laboratory Animals 36, 119.Google Scholar
Mangum, C. and van Winkle, W. (1973) Responses of aquatic invertebrates to declining oxygen conditions. American Zoologist 13, 529541.Google Scholar
Marsden, I.D. (1999) Respiration and feeding of the surf clam Paphies donacina from New Zealand. Hydrobiologia 405, 179188.Google Scholar
Martínez del Rio, C. (2008) Metabolic theory or metabolic models. Trends in Ecology and Evolution 23, 256260.Google Scholar
Morton, B. (2006) Diet and predation exhibited by Cominella eburnean (Gastropoda: Caenogastropoda: Neogastropoda) in Princess Royal Harbour, Albany, Western Australia, with a review of attack strategies in Buccinidae. Molluscan Research 26, 3950.Google Scholar
Morton, J.E. (1979) Molluscs. 5th edition. London: Hutchinson and Co. Ltd.Google Scholar
Nakaya, F., Saito, Y. and Motokawa, T. (2003) Switching of metabolic-rate scaling between allometry and isometry in colonial ascidians. Proceedings of the Royal Society of London 270, 11051113.Google Scholar
Newell, R.C. (1979) Biology of intertidal animals. Faversham, Kent: Marine Ecological Surveys.Google Scholar
Newell, R.C. and Pye, V.I. (1971) Variations in the relationship between oxygen consumption, body size and summated tissue metabolism in the winkle Littorina littorea. Journal of the Marine Biological Association of the United Kingdom 51, 315338.Google Scholar
Newell, R.C., Johnston, L.G. and Kofoed, L.H. (1977) Effects of environmental temperature and hypoxia on the oxygen uptake of the suspension-feeding gastropod Crepidula fornicata. Comparative Biochemistry and Physiology 59A, 175182.Google Scholar
Newell, R.C. and Roy, A. (1973) A statistical model relating the oxygen consumption of a mollusk (Littorina littorea) to activity, body size and environmental conditions. Physiological Zoology 46, 252275.CrossRefGoogle Scholar
Niklas, K.J., Cobb, E.D. and Spatz, H.C. (2009) Predicting the allometry of leaf surface area and dry mass. American Journal of Botany 96, 531536.Google Scholar
O'Connor, M.P., Kemp, S.J., Agosta, S.J., Hansen, F., Sieg, A.E., Wallace, B.P., McNair, J.N. and Dunham, A.E. (2007) Reconsidering the mechanistic basis of the metabolic theory of ecology. Oikos 116, 10581072.Google Scholar
Peck, M.A., Buckley, J. and Bengtson, D.A. (2005) Effects of temperature, body size and feeding on rates of metabolism in young-of-the-year haddock. Journal of Fish Biology 66, 911923.Google Scholar
Peters, R.H. (1983) The ecological implications of body size. Cambridge: Cambridge University Press Google Scholar
Peters, R.H., Cabana, G., Choulik, O., Cohen, T., Griesbach, S. and McCanny, S.J. (1996) General models for trophic fluxes in animals based on their body size. Ecoscience 3, 365377.Google Scholar
Phillipson, J. (1981) Bioenergetic options and phylogeny. In Townsend, C.R. and Callow, P. (eds) Physiological ecology: an evolutionary approach to resource use. Oxford: Blackwell Scientific, pp. 2045.Google Scholar
Ponder, W.F. and Lindberg, D.R. (1997) Towards phylogeny of gastropod molluscs: an analysis using morphological characters. Zoological Journal of the Linnean Society 119, 83265.Google Scholar
Ponder, W.F. and Lindberg, D.L. (2008) Phylogeny and evolution of the Mollusca. Berkeley, CA: University of California Press.Google Scholar
Pörtner, H.O. (2002) Environmental and functional limits to muscular exercise and body size in marine invertebrate athletes. Comparative Biochemistry and Physiology A 133, 303321.Google Scholar
Savage, V.M., Gillooly, J.F., Woodruff, W.H., West, G.B., Allen, A.P., Enquist, B.J. and Brown, J.H. (2004) The predominance of quarter-power scaling in biology. Functional Ecology 18, 257282.Google Scholar
Schmidt-Nielsen, K. (1984) Scaling. Why is animal size so important? Cambridge: Cambridge University Press.Google Scholar
Seibel, B.A. (2007) On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the Class Cephalopoda (Mollusca). Journal of Experimental Biology 210, 111.Google Scholar
Shumway, S.E. (1981) Factors affecting oxygen consumption in the marine pulmonate Amphibola crenata (Gmelin, 1791). Biological Bulletin. Marine Biological Laboratory, Woods Hole 160, 332347.Google Scholar
Shumway, S.E. (1982) Oxygen consumption in oysters: an overview. Marine Biology Letters 3, 123.Google Scholar
Shumway, S.E., Lesser, M.P. and Crisp, D.J. (1993) Specific dynamic action demonstrated in the herbivorous marine periwinkles, Littorina littorea L and Littorina obtusata L (Mollusca, Gastropoda). Comparative Biochemistry and Physiology A 106, 391395.Google Scholar
Shumway, S.E. and Marsden, I.D. (1982) The combined effects of temperature, salinity, and declining oxygen-tension on oxygen-consumption in the marine pulmonate Amphibola crenata (Gmelin, 1791). Journal of Experimental Maine Biology and Ecology 6, 133146.Google Scholar
Sims, D.W. (1996) The effect of body size on the standard metabolic rate of the lesser spotted dogfish. Journal of Fish Biology 48, 542544.CrossRefGoogle Scholar
Snedecor, G.W. and Cochran, G. (1989) Statistical methods. Ames, IA: Iowa State University Press.Google Scholar
Sokal, R.R. and Rohlf, F.J. (1981) Biometry. San Francisco, CA: W.H. Freeman.Google Scholar
Spicer, J.I. and Stromberg, J.O. (2003) Developmental changes in the responses of O2 uptake and ventilation to acutely declining O2 tensions in larval krill Meganictiphanes norvegica. Journal of Experimental Marine Biology and Ecology 295, 207218.CrossRefGoogle Scholar
Suarez, R.K., Darveau, C.A. and Childress, J.J. (2004) Metabolic scaling: a many-splendoured thing. Comparative Biochemistry and Physiology B 139, 531541.Google Scholar
Toulmond, A. (1967a) Etude de la consommation d'oxygène en fonction du poids dans l'air et dans l'eau, chez quatre espèces du genre Littorina (Gasteropoda, Prosobranchia). Comptes Rendus Hebdomadaires de Séances de l'Académie des Sciences Série D, Sciences Naturelles 264, 636638.Google Scholar
Toulmond, A. (1967b) Consommation d'oxygène dans l'air et dans l'eau chez quatre Gastéropodes du genre Littorina. Journal of Physiology—Paris 59, 303304.Google Scholar
West, G.B., Brown, J.H. and Enquist, B.J. (1997) A general model for the origin of allometric scaling laws in biology. Science 276, 122126.CrossRefGoogle ScholarPubMed
West, G.B., Brown, J.H. and Enquist, B.J. (1999) The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284, 16771679.CrossRefGoogle ScholarPubMed
West, G.B., Woodruff, W.H. and Brown, J.H. (2002) Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals. Proceedings of the National Academy of Sciences of the United States of America 99, (Supplement 1) 24732478.Google Scholar
Wilmer, P., Stone, G. and Johnston, I. (2005) Environmental physiology of animals. London: Blackwell Publishing.Google Scholar
Wilson, B., Wilson, C. and Baker, P. (1994) Australian marine shells—prosobranch gastropods. Volume 2. Perth, Western Australia: Odyssey Publishing.Google Scholar
Withers, P.C. (1992) Comparative animal physiology. Fort Worth, TX: Brooks/Cole Publishing.Google Scholar
Wood, S.C. and Lenfant, C. (1979) Evolution of respiratory processes: a comparative approach. New York: Marcel Dekker Inc.Google Scholar
Yonge, C.M. (1960) General characters of Mollusca. In Moore, R.C. (ed.) Treatise on invertebrate palaeontology. Lawrence, KS: University of Kansas Press and the Geological Society of America, pp. 13136.Google Scholar
Zeuthen, E. (1949) Body size and metabolic rate in the animal kingdom. Carlsberg Laboratory Series 26, 15161.Google Scholar