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Variation in oxygen consumption among ‘living fossils’ (Mollusca: Polyplacophora)

Published online by Cambridge University Press:  22 October 2012

Nicholas Carey*
Affiliation:
Queen's University Belfast, School of Biological Sciences, Lisburn Road, Belfast, BT9 7BL, Northern Ireland Queen's University Belfast Marine Laboratory, 12–13 The Strand, Portaferry, County Down, BT22 1PF, Northern Ireland
Alexander Galkin
Affiliation:
Queen's University Belfast, School of Biological Sciences, Lisburn Road, Belfast, BT9 7BL, Northern Ireland
Patrik Henriksson
Affiliation:
The University of British Columbia, Department of Zoology, 6270 University Boulevard, Vancouver, BC, V6T 1Z4, Canada CML, Institute of Environmental Sciences, Leiden University, PO Box 9518, 2300 RA, Leiden, The Netherlands
Jeffrey G. Richards
Affiliation:
The University of British Columbia, Department of Zoology, 6270 University Boulevard, Vancouver, BC, V6T 1Z4, Canada
Julia D. Sigwart
Affiliation:
Queen's University Belfast, School of Biological Sciences, Lisburn Road, Belfast, BT9 7BL, Northern Ireland Queen's University Belfast Marine Laboratory, 12–13 The Strand, Portaferry, County Down, BT22 1PF, Northern Ireland
*
Correspondence should be addressed to: N. Carey, Queen's University Belfast, Marine Laboratory, 12–13 The Strand, Portaferry, BT22 1PF, Northern Ireland email: ncarey02@qub.ac.uk

Abstract

Polyplacophoran molluscs (chitons) are phylogenetically ancient and morphologically constrained, yet multiple living species are often found co-occurring within widely overlapping ecological niches. This study used two sets of experiments to compare interspecific variation among co-occurring species in the North Atlantic (Ireland) and separately in the North Pacific (British Columbia, Canada) chiton faunas. A complementary review of historical literature on polyplacophoran physiology provides an overview of the high level of metabolic variability in this group of ‘living fossils’. Species examined in de novo experiments showed significant variation in oxygen consumption both under air-saturated water conditions (normoxia), and in response to decreasing oxygen availability (hypoxia). Some species demonstrate an ability to maintain constant oxygen uptake rates despite hypoxia (oxyregulators), while others oxyconform, with uptake rate dependent on ambient oxygen tension. These organisms are often amalgamated in studies of benthic communities, yet show obvious physiological difference that may impact their response or tolerance to environmental change.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

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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, Part A: Molecular and Integrative Physiology 137, 425–34.CrossRefGoogle ScholarPubMed
Barbosa, S.S., Byrne, M. and Kelaher, B.P. (2008) Bioerosion caused by foraging of the tropical chiton Acanthopleura gemmata at One Tree Reef, southern Great Barrier Reef. Coral Reefs 27, 635639.CrossRefGoogle Scholar
Bayne, B. (1971) Ventilation, the heart beat and oxygen uptake by Mytilus edulis L. in declining oxygen tension. Comparative Biochemistry and Physiology, Part A: Molecular and Integrative Physiology 40, 10651085.CrossRefGoogle Scholar
Bayne, B. (1973) The responses of three species of bivalve mollusc to declining oxygen tension at reduced salinity. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 45, 793806.CrossRefGoogle ScholarPubMed
Benson, B.B. and Krause, D. (1984) The concentration and isotopic fractionation of oxygen dissolved in freshwater and seawater in equilibrium with the atmosphere. Limnology and Oceanography 29, 620632.CrossRefGoogle Scholar
Bishop, G. (2003) The ecology of the rocky shores of Sherkin Island: a twenty year perspective. Cork, Ireland: Sherkin Island Marine Station Publications.Google Scholar
Boero, F., Bouillon, J., Gravili, C., Miglietta, M., Parsons, T. and Piraino, S. (2008) Gelatinous plankton: irregularities rule the world (sometimes). Marine Ecology Progress Series 356, 299310.CrossRefGoogle Scholar
Bolnick, D.I., Amarasekare, P., Araújo, M.S., Bürger, R., Levine, J.M., Novak, M., Rudolf, V.H.W., Schreiber, S.J., Urban, M.C. and Vasseur, D.A. (2011) Why intraspecific trait variation matters in community ecology. Trends in Ecology and Evolution 26, 183192.CrossRefGoogle ScholarPubMed
Boyle, P.R. (1970) Aspects of the ecology of a littoral chiton, Sypharochiton pelliserpentis (Mollusca: Polyplacophora). New Zealand Journal of Marine and Freshwater Research 4, 364384.CrossRefGoogle Scholar
Brewer, P.G. and Peltzer, E.T. (2009) Limits to marine life. Science 324, 347348.CrossRefGoogle ScholarPubMed
Bridges, C.R. and Brand, A.R. (1980) Oxygen consumption and oxygen-independence in marine crustaceans. Marine Ecology Progress Series 2, 133141.CrossRefGoogle Scholar
Brodersen, K.P., Pedersen, O., Lindegaard, C. and Hamburger, K. (2004) Chironomids (Diptera) and oxy-regulatory capacity: an experimental approach to paleolimnological interpretation. Limnology and Oceanography 49, 15491559.Google Scholar
Chelazzi, G., Focardi, S. and Deneubourg, J.-L. (1988) Analysis of movement patterns and orientation mechanisms in intertidal chitons and gastropods. In Chelazzi, G. and Vannini, M. (eds) Behavioural adaptation to intertidal life. New York: Plenum Press, pp.173184.CrossRefGoogle Scholar
De Fur, P. and Mangum, C.P. (1979) The effects of environmental variables on the heart rates of invertebrates. Comparative Biochemistry and Physiology, Part A: Molecular and Integrative Physiology 62, 283294.CrossRefGoogle Scholar
Dethier, M.N. and Duggins, D.O. (1984) An indirect commensalism between marine herbivores and the importance of competitive hierarchies. American Naturalist 124, 205219.CrossRefGoogle Scholar
Dethier, M.N. and Duggins, D.O. (1988) Variation in strong interactions in the intertidal zone along a geographical gradient: a Washington–Alaska comparison. Marine Ecology Progress Series 50, 97105.CrossRefGoogle Scholar
de Zwaan, A., Cortesi, P., Thillart, G., Roos, J. and Storey, K.B. (1991) Differential sensitivities to hypoxia by two anoxia-tolerant marine molluscs: a biochemical analysis. Marine Biology 111, 343351.CrossRefGoogle Scholar
Duke, J.T. and Ultsch, G.R. (1990) Metabolic oxygen regulation and conformity during submergence in the salamanders Siren lacertina, Amphiuma means, and Amphiuma tridactylum, and a comparison with other giant salamanders. Oecologia 84, 1623.CrossRefGoogle Scholar
Eberlee, J. and Storey, K.B. (1988) Tissue-specific biochemical responses during anoxia and recovery in the channelled whelk. Journal of Experimental Marine Biology and Ecology 121, 165176.CrossRefGoogle Scholar
Eernisse, D.J., Clark, R.N. and Draeger, A. (2007) Polyplacophora. In Carlton, J.T. (ed.) The Light and Smith Manual: intertidal invertebrates from central California to Oregon. Berkeley, CA: University of California Press, pp. 701713.Google Scholar
Eernisse, D.J. and Reynolds, P.D. (1994) Polyplacophora. In Harrison, F.W. and Kohn, A.J. (eds) Microscopic anatomy of invertebrates, Volume 5, Mollusca. New York: Wiley, pp. 56110.Google Scholar
Fisher, T.R. (1976) Oxygen uptake of the solitary tunicate Styela plicata. Biological Bulletin. Marine Biological Laboratory, Woods Hole 151, 297305.CrossRefGoogle ScholarPubMed
García, H.E. and Gordon, L.I. (1992) Oxygen solubility in seawater: better fitting equations. Limnology and Oceanography 37, 13071312.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Hagerman, L. (1998) Physiological flexibility: a necessity for life in anoxic and sulphidic habitats. Hydrobiologia 375–76, 241–254.Google Scholar
Hayward, P.J. and Ryland, J.S. (1996) Handbook of the marine fauna of North-West Europe. Oxford: Oxford University Press.Google Scholar
Herreid, C.F. (1980) Hypoxia in invertebrates. Comparative Biochemistry and Physiology, Part A: Molecular and Integrative Physiology 67, 311320.CrossRefGoogle Scholar
Hetherington, R. and Reid, R.G.B. (2003) Malacological insights into the marine ecology and changing climate of the late Pleistocene—early Holocene Queen Charlotte Islands archipelago, western Canada, and implications for early peoples. Canadian Journal of Zoology 81, 626661.CrossRefGoogle Scholar
Horn, P.L. (1982) Adaptations of the chiton Sypharochiton pelliserpentis to rocky and estuarine habitats. New Zealand Journal of Marine and Freshwater Research 16, 253261.CrossRefGoogle Scholar
Horn, P.L. (1985) Respiration in air and water of the chiton Chiton pelliserpentis from high and low zones of a sheltered shore. New Zealand Journal of Marine and Freshwater Research 19, 1119.CrossRefGoogle Scholar
Kaas, P. and Van Belle, R.A. (1985) Monograph of living chitons: Volume 1. Order Neoloricata: Lepidopleurina. Leiden, The Netherlands: Brill.Google Scholar
Katsanevakis, S., Xanthopoulos, J., Protopapas, N. and Verriopoulos, G. (2007) Oxygen consumption of the semi-terrestrial crab Pachygrapsus marmoratus in relation to body mass and temperature: an information theory approach. Marine Biology 151, 343352.CrossRefGoogle Scholar
Keeling, R.F., Koertzinger, A. and Gruber, N. (2010) Ocean deoxygenation in a warming world. Annual Review of Marine Science 2, 199229.CrossRefGoogle Scholar
Kelly, R.P. and Eernisse, D.J. (2008) Reconstructing a radiation: the chiton genus Mopalia in the North Pacific. Invertebrate Systematics 22, 1728.CrossRefGoogle Scholar
Kincannon, E.A. (1975) The relations between body weight and habitat temperature and the respiratory rate of Tonicella lineata (Wood, 1815) (Mollusca: Polyplacophora). Veliger 18 (Supplement), 8793.Google Scholar
Larade, K. and Storey, K.B. (2002) A profile of the metabolic responses to anoxia in marine invertebrates. In Storey, K.B. and Storey, J.M. (eds) Cell and molecular response to stress. Volume 3: sensing, signaling and cell adaptation. Amsterdam: Elsevier, pp. 2746.CrossRefGoogle Scholar
Lebsack, C.S. (1975) Effect of temperature and salinity on the oxygen consumption of the chiton Mopalia lignosa. Veliger 18 (Supplement), 9497.Google Scholar
Lencioni, V., Bernabò, P., Vanin, S., Di Muro, P. and Beltramini, M. (2008) Respiration rate and oxy-regulatory capacity in cold stenothermal chironomids. Journal of Insect Physiology 54, 13371342.CrossRefGoogle ScholarPubMed
Littler, M.M., Littler, D.S. and Taylor, P.R. (1995) Selective herbivore increases biomass of its prey: a chiton–coralline reef-building association. Ecology 76, 16661681.CrossRefGoogle Scholar
Livingstone, D.R. (1991) Organic xenobiotic metabolism in marine invertebrates. In Gilles, R. (ed.) Advances in comparative and environmental physiology. Volume 7. Berlin: Springer, pp. 45185.CrossRefGoogle Scholar
Mangum, C.P. and Van Winkle, W. (1973) Responses of aquatic invertebrates to declining oxygen conditions. American Zoologist 13, 529541.CrossRefGoogle Scholar
Marshall, D. and McQuaid, C. (1993) Effects of hypoxia and hyposalinity on the heartbeat of the intertidal limpets Patella granvlaris (prosobranchia) and Siphonaria capensis (pulmonata). Comparative Biochemistry and Physiology, Part A: Molecular and Integrative Physiology 106, 6568.CrossRefGoogle Scholar
McAllen, R., Taylor, A.C. and Davenport, J. (1999) The effects of temperature and oxygen partial pressure on the rate of oxygen consumption of the high-shore rock pool copepod Tigriopus brevicornis. Comparative Biochemistry and Physiology, Part A: Molecular and Integrative Physiology 123, 195202.CrossRefGoogle Scholar
McMahon, B.R., Burggren, W.W., Pinder, A.W. and Wheatly, M.G. (1991) Air exposure and physiological compensation in a tropical intertidal chiton, Chiton stokesii (Mollusca: Polyplacophora). Physiological Zoology 64, 728747.CrossRefGoogle Scholar
Murdoch, R.C. and Shumway, S.E. (1980) Oxygen consumption in six species of chitons in relation to their position on the shore. Ophelia 19, 127144.CrossRefGoogle Scholar
Nagabhushanam, R. and Murti, K.G. (1972) The influence of body size, salinity and temperature on the respiration of Chiton granoradiatus. Marathwada University Journal of Science, Section B, Biological Sciences 11, 7982.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, 253275.CrossRefGoogle Scholar
Nichols, A.R. (1900) Marine Mollusca of Ireland. Dublin: Royal Irish Academy.Google Scholar
Ortiz, M. and Wolff, M. (2002) Application of loop analysis to benthic systems in northern Chile for the elaboration of sustainable management strategies. Marine Ecology Progress Series 242, 1527.CrossRefGoogle Scholar
Padilla, D.K. and Allen, B.J. (2000) Paradigm lost: reconsidering functional form and group hypotheses in marine ecology. Journal of Experimental Marine Biology and Ecology 250, 207221.CrossRefGoogle ScholarPubMed
Paine, R.T. (1992) Food-web analysis through field measurement of per capita interaction strength. Nature 355, 7375.CrossRefGoogle Scholar
Pannunzio, T.M. and Storey, K.B. (1998) Antioxidant defenses and lipid peroxidation during anoxia stress and aerobic recovery in the marine gastropod Littorina littorea. Journal of Experimental Marine Biology and Ecology 221, 277292.CrossRefGoogle Scholar
Pauly, D., Graham, W., Libralato, S., Morissette, L. and Deng Palomares, M.L. (2009) Jellyfish in ecosystems, online databases, and ecosystem models. Hydrobiologia 616, 6785.CrossRefGoogle Scholar
Petersen, J.A. and Johansen, K. (1973) Gas exchange in the giant sea cradle Cryptochiton stelleri (Middendorff). Journal of Experimental Marine Biology and Ecology 12, 2743.CrossRefGoogle Scholar
Poloczanska, E.S., Smith, S., Fauconnet, L., Healy, J., Tibbetts, I.R., Burrows, M.T. and Richardson, A.J. (2011) Little change in the distribution of rocky shore faunal communities on the Australian east coast after 50 years of rapid warming. Journal of Experimental Marine Biology and Ecology 400, 145154.CrossRefGoogle Scholar
Poppe, G. and Goto, Y. (1991) European seashells. Volume 1 (Polyplacophora, Caudofoveata, Solenogastra, Gastropoda). Wiesbaden, Germany: Verlag Christa Hemmen.Google Scholar
R Core Development Team (2012) R: a language and environment for statistical computing. An introduction to R notes on R a programming environment for data analysis and graphics R core team version. Vienna: R Foundation for Statistical Computing.Google Scholar
Robbins, B.A. (1975) Aerial and aquatic respiration in the chitons Nuttallina californica and Tonicella lineata. Veliger 18 (Supplement), 98102.Google Scholar
Rostal, D.C. and Simpson, L. (1988) The influence of salinity on the distribution of two Oregon chiton species (Katharina tunicata Wood and Mopalia hindsii Reeve). Veliger 31, 120126.Google Scholar
Sassaman, C. and Mangum, C.P. (1972) Adaptations to environmental oxygen levels in infaunal and epifaunal sea anemones. Biological Bulletin. Marine Biological Laboratory, Woods Hole 143, 657678.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Shumway, S.E., Scott, T.M. and Shick, J.M. (1993) The effects of anoxia and hydrogen sulphide on survival, activity and metabolic rate in the coot clam, Mulinia lateralis (Say). Journal of Experimental Marine Biology and Ecology 71, 135146.CrossRefGoogle Scholar
Sigwart, J.D. (2008) Gross anatomy and positional homology of gills, gonopores, and nephridiopores in ‘basal’ living chitons (Polyplacophora: Lepidopleurina). American Malacological Bulletin 25, 4349.CrossRefGoogle Scholar
Sigwart, J.D., Schwabe, E., Saito, H., Samadi, S. and Giribet, G. (2011) Evolution in the deep sea: a combined analysis of the earliest diverging living chitons (Mollusca: Polyplacophora: Lepidopleurida). Invertebrate Systematics 24, 560572.CrossRefGoogle Scholar
Sirenko, B.I. (1993) Revision of the system of the order Chitonida (Mollusca: Polyplacophora) on the basis of correlation between the type of gills arrangement and the shape of the chorion processes. Ruthenica 3, 93117.Google Scholar
Sirenko, B.I. (2006) New outlook on the system of chitons (Mollusca: Polyplacophora). Venus 65, 2749.Google Scholar
Slieker, F.J.A. (2000) Chitons of the world. Ancona, Italy: L'Informatore Piceno Edito.Google Scholar
Spicer, J.I., Dando, C.L. and Maltby, L. (2002) Anaerobic capacity of a crustacean sensitive to low environmental oxygen tensions, the freshwater amphipod Gammarus pulex (L.). Hydrobiologia 477, 189194.CrossRefGoogle Scholar
Steneck, R.S. and Watling, L. (1982) Feeding capabilities and limitation of herbivorous molluscs: a functional group approach. Marine Biology 68, 299319.CrossRefGoogle Scholar
Stickle, W.B. and Sabourin, T.D. (1979) Effects of salinity on the respiration and heart rate of the common mussel, Mytilus edulis L., and the black chiton, Katharina tunicata (Wood). Journal of Experimental Marine Biology and Ecology 41, 257268.CrossRefGoogle Scholar
Strahl, J., Dringen, R., Schmidt, M.M., Hardenberg, S. and Abele, D. (2011) Metabolic and physiological responses in tissues of the long-lived bivalve Arctica islandica to oxygen deficiency. Comparative Biochemistry and Physiology, Part A: Molecular and Integrative Physiology 158, 513519.CrossRefGoogle ScholarPubMed
Tang, P.S. (1933) On the rate of oxygen consumption by tissues and lower organisms as a function of oxygen tension. Quarterly Review of Biology 8, 260274.CrossRefGoogle Scholar
Taylor, A.C. and Brand, A.R. (1975) Effects of hypoxia and body size on the oxygen consumption of the bivalve Arctica islandica (L.). Journal of Experimental Marine Biology and Ecology 19, 187196.CrossRefGoogle Scholar
Taylor, A.C. and Moore, P.G. (1995) The burrows and physiological adaptations to a burrowing lifestyle of Natatolana borealis (Isopoda: Cirolanidae). Marine Biology 123, 805814.CrossRefGoogle Scholar
Truchot, J.P. and Duhamel-Jouve, A. (1980) Oxygen and carbon dioxide in the marine intertidal environment: diurnal and tidal changes in rockpools. Respiration Physiology 39, 241254.CrossRefGoogle ScholarPubMed
Warwick, R.M. (1993) Environmental impact studies on marine communities: pragmatical considerations. Australian Journal of Ecology 18, 6380.CrossRefGoogle 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
Yonge, C. (1939) Memoirs: on the mantle cavity and its contained organs in the Loricata (Placophora). Quarterly Journal of Microscopical Science 81, 367390.Google Scholar
Wilson, J.G. and Davis, J.P. (1984) The effect of environmental variables on the oxygen consumption of the protobranch bivalve Nucula turgida (Leckenby and Marshall). Journal of Molluscan Studies 50, 7377.CrossRefGoogle Scholar