Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-18T08:41:26.122Z Has data issue: false hasContentIssue false

Comparison of oxygen consumption by Terebratalia transversa (Brachiopoda) and two species of pteriomorph bivalve molluscs: implications for surviving mass extinctions

Published online by Cambridge University Press:  08 February 2016

Loren A. Ballanti
Affiliation:
Department of Biology, University of Washington, Seattle, Washington 98195, United States of America. E-mail: oceanic@uw.edu
Alexa Tullis
Affiliation:
Department of Biology, University of Puget Sound, Tacoma, Washington 98416, United States of America
Peter D. Ward
Affiliation:
Department of Biology, University of Washington, Seattle, Washington 98195, United States of America

Abstract

The Permian/Triassic mass extinction marks a permanent phylogenetic shift in the composition of the sessile benthos, from one largely dominated by articulate brachiopods to one dominated by mollusks. Widespread evidence of oceanic hypoxia and anoxia at this time provides a possible selective kill mechanism that could help explain the large taxonomic losses in brachiopods compared to the morphologically and ecologically similar bivalve molluscs. Our study compared the oxygen consumption of an articulate brachiopod, Terebratalia transversa, with that of two pteriomorph bivalves, Glycymeris septentrionalis and Mytilus trossulus, under normoxia and hypoxia, as well as their tolerance to anoxia, to gain insight into the relative metabolic characteristics of each group. We found no significant difference in the oxygen consumption of the three species when normalized to the same dry-tissue mass. However, when calculated for animals of the same external linear dimensions, bivalve oxygen consumption was two to three times greater than that of brachiopods. Our results also showed no significant decrease in the oxygen consumption of the three species until measured at a partial pressure of oxygen ∼10% of normoxic values. Finally, T. transversa and M. trossulus showed no significant difference in their tolerance to complete anoxia, but both showed a much lower tolerance than another bivalve, Acila castrensis. Findings from this study suggest that oxygen limitation is unlikely to account for the observed selective extinction of brachiopods during the Permian/Triassic mass extinction. Results may provide valuable information for assessing hypotheses put forth to explain why articulate brachiopods continue to remain a relatively minor group in marine environments.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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

Literature Cited

Bayne, B. L., and Livingstone, D. R. 1977. Responses of Mytilus edulis L. to low oxygen tension: acclimation of the rate of oxygen consumption. Journal of Comparative Physiology B 144:129142.CrossRefGoogle Scholar
Bayne, B. L., Bayne, C. J., Carefoot, T. C., and Thomson, R. J. 1976. The physiological ecology of Mytilus californianus Conrad. 1. Metabolism and energy balance. Oecologia 22:229250.CrossRefGoogle ScholarPubMed
Curry, G. B., and Ansell, A. D. 1986. Tissue mass in living brachiopods. Biostratigraphie du Paléozoïque 4:231241.Google Scholar
Curry, G. B., Ansell, A. D., James, M., and Peck, L. 1989. Physiological constraints on living and fossil brachiopods. Transactions of the Royal Society of Edinburgh: Earth Sciences 80:255262.CrossRefGoogle Scholar
de Zwaan, A., and Eertman, R. H. M. 1996. Anoxic or aerial survival of bivalves and other euryoxic invertebrates as a useful response to environmental stress—a comprehensive review. Comparative Biochemistry and Physiology C 113:299312.Google Scholar
de Zwaan, A., Babarro, J. M. F., Monari, M., and Cattani, O. 2002. Anoxic survival potential of bivalves: (arte)facts. Comparative Biochemistry and Physiology 131:615624.CrossRefGoogle ScholarPubMed
Diaz, R. J., and Rosenberg, R. 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioral responses of benthic macrofauna. Oceanography and Marine Biology: An Annual Review 33:245303.Google Scholar
Dries, R. R., and Theede, H. 1974. Sauerstoffmangelresistanz mariner Bodenvertebraten aus der Westlichen Ostsee. Marine Biology 25:327333.CrossRefGoogle Scholar
Erwin, D. H. 2006. Extinction: how life on earth nearly ended 250 million years ago. Princeton University Press, Princeton.Google Scholar
Finks, R. M. 2006. Are hypercalcified demosponges a key to the end-Permian mass extinction? Geological Society of America, Abstracts with Programs 38 (7):538.Google Scholar
Fraiser, M. L., and Bottjer, D. J. 2005. Restructuring in benthic level-bottom shallow marine communities due to prolonged environmental stress following the end-Permian mass extinction. Comptes Rendus Palevol 4:515523.CrossRefGoogle Scholar
Gould, S. J., and Calloway, C. B. 1980. Clams and brachiopods––ships that pass in the night. Paleobiology 6:383396.CrossRefGoogle Scholar
Grice, K., Cao, C., Love, G. D., Böttcher, M. E., Twitchett, R. J., Grosjean, E., Summons, R. E.Turgeon, S. C., Dunning, W., and Jin, Y. 2005. Photic zone euxinia during the Permian-Triassic superanoxic event. Science 307:706709.CrossRefGoogle ScholarPubMed
Hammen, C. S. 1977. Brachiopod metabolism and enzymes. Integrative and Comparative Biology 17:141147.Google Scholar
Harper, D. A. T., and Jia-Yu, R. 2001. Palaeozoic brachiopod extinctions, survival, and recovery: patterns within the rhynchonelliformeans. Geological Journal 36:317328.CrossRefGoogle Scholar
Henriksson, R. 1969. Influence of pollution on the bottom fauna of the sound (Öresund). Oikos 20:507523.CrossRefGoogle Scholar
Isozaki, Y. 1997. Permo-Triassic boundary superanoxia and stratified superocean: records from the lost deep sea. Science 272:235238.CrossRefGoogle Scholar
James, M. A., Ansell, A. D., Collins, M. J., Curry, G. B., Peck, L. S., and Rhodes, M. C. 1992. Biology of living brachiopods. Advances in Marine Biology 28:175387.CrossRefGoogle Scholar
Knoll, A. H., Bambach, R. K., Canfield, D. E., and Grotzinger, J. P. 1996. Comparative Earth history and Late Permian mass extinction. Science 273:452457.CrossRefGoogle ScholarPubMed
Knoll, A. H., Bambach, R. K., Payne, J. L., Pruss, S., and Fischer, W. W. 2007. Paleophysiology and end-Permian mass extinction. Earth and Planetary Science Letters 256:295313.CrossRefGoogle Scholar
Kozloff, E. N. 1983. Seashore life of the northern Pacific Coast. University of Washington Press, Seattle.Google Scholar
Kump, L. R., Pavlov, A., and Arthur, M. A. 2005. Massive release of hydrogen sulfide to the surface ocean and atmosphere during intervals of oceanic anoxia. Geology 33:397400.CrossRefGoogle Scholar
LaBarbera, M. 1978. Brachiopod orientation to water movement: functional morphology. Lethaia 11:6779.CrossRefGoogle Scholar
LaBarbera, M. 1986. Brachiopod lophophores: functional diversity and scaling. InRacheboeuf, P. R. and Emig, C., eds. Les brachiopods fossils et actuels. Biostratigraphie du Paléozoïque 4:314321.Google Scholar
Martin, R. E. 1996. Secular increase in nutrient levels through the Phanerozoic: implications for productivity, biomass, and diversity of the marine biosphere. Palaios 11:209219.CrossRefGoogle Scholar
Nilsson, H., and Rosenberg, R. 1994. Hypoxic responses of two marine benthic communities. Marine Ecology Progress Series 115:209217.CrossRefGoogle Scholar
Oeschger, R. 1990. Long term anaerobiosis in subtidal marine invertebrates from the western Baltic Sea: Halicryptus spinulosus (Priapulida), Astarte borealis and Arctica islandica (Bivalvia). Marine Ecology Progress Series 59:133143.CrossRefGoogle Scholar
Peck, L. S. 1992. Body volumes and internal space constraints in articulate brachiopods. Lethaia 25:383390.CrossRefGoogle Scholar
Peck, L. S. 1993. The tissue of articulate brachiopods and their value to predators. Philosophical Transactions of the Royal Society of London 339:1732.Google Scholar
Peck, L. S. 2001. Physiology. InCarlson, S. and Sandy, M., eds. Brachiopods ancient and modern: a tribute to G. Arthur Cooper. Paleontology Society Papers 7:89104. Yale University, New Haven, Conn.CrossRefGoogle Scholar
Peck, L. S. 2008. Brachiopods and climate change. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 98:451456.CrossRefGoogle Scholar
Peck, L. S., and Conway, L. Z. 2000. The myth of metabolic cold adaptation: oxygen consumption in stenothermal Antarctic bivalves. InHarper, E. M., Taylor, J. D., and Crame, J. A., eds. The evolutionary biology of the Bivalvia. Geological Society of London Special Publication 177:441450.CrossRefGoogle Scholar
Peck, L. S., and Holmes, L. J. 1989. Seasonal and ontogenetic changes in tissue size in the Antarctic brachiopod Liothyrella uva (Broderip, 1833). Journal of Experimental Marine Biology and Ecology 134:2536.CrossRefGoogle Scholar
Peck, L. S., Morris, D. J., and Clarke, A. 1986. The caeca of punctate brachiopods: a respiring tissue not a respiratory organ. Lethaia 19:232.CrossRefGoogle Scholar
Peck, L. S., Clarke, A., and Holmes, L. J. 1987. Size, shape and the distribution of organic matter in the Recent Antarctic brachiopod Liothyrella uva. Lethaia 20:3340.CrossRefGoogle Scholar
Pennington, J. T., Tamburri, M. N., and Barry, J. P. 1999. Development, temperature tolerance, and settlement preference of embryos and larvae of the articulate brachiopod Laqueus californianus. Biological Bulletin 196:245256.CrossRefGoogle ScholarPubMed
Rampino, M. R., and Caldeira, K. 2005. Major perturbations of ocean chemistry and a ‘Strangelove Ocean' after the end-Permian mass extinction. Terra Nova 17:554559.CrossRefGoogle Scholar
Rhodes, M. C., and Thayer, C. W. 1991. Mass extinctions: ecological selectivity and primary production. Geology 19:877880.2.3.CO;2>CrossRefGoogle Scholar
Rhodes, M. C., and Thompson, R. J. 1993. Comparative physiology of suspension-feeding in living brachiopods and bivalves: evolutionary implications. Paleobiology 19:322334.CrossRefGoogle Scholar
Rosenberg, R., Hellman, B., and Johansson, B. 1991. Hypoxic tolerance of marine benthic fauna. Marine Ecology Progress Series 79:127131.CrossRefGoogle Scholar
Rudwick, M. J. S. 1970. Living and fossil brachiopods. Hutchinson University Library, London, 199pp.Google Scholar
Seed, R. 1992. Systematics evolution and distribution of mussels belonging to the genus Mytilus: an overview. American Malacological Bulletin 9 (2):123137.Google Scholar
Sepkoski, J. J. Jr., 1984. A kinetic model of Phanerozoic taxonomic diversity. III. Post-Paleozoic families and mass extinctions. Paleobiology 10:246267.CrossRefGoogle Scholar
Sepkoski, J. J. Jr., 2002. A compendium of fossil marine animal genera. Bulletins of American Paleontology 363:1560.Google Scholar
Shumway, S. E. 1982. Oxygen consumption in brachiopods and the possible role of punctae. Journal of Experimental Marine Biology and Ecology 58:207220.CrossRefGoogle Scholar
Shumway, S. E., and Koehn, R. K. 1982. Oxygen consumption in the American oyster Crassostrea virginica. Marine Ecology Progress Series 9:5968.CrossRefGoogle Scholar
Sobral, P., and Widdows, J. 1997. Influences of hypoxia and anoxia on the physiological responses of the clam Ruditapes decussatus from southern Portugal. Marine Biology 127:455461.CrossRefGoogle Scholar
Stanley, S. M. 1972. Functional morphology and evolution of byssally attached bivalve mollusks. Journal of Paleontology 46:165212.Google Scholar
Steele-Petrović, H. M. 1979. The physiological differences between articulate brachiopods and filter-feeding bivalves as a factor in the evolution of marine bottom-level communities. Paleontology 22:101134.Google Scholar
Stickle, W. B., Kapper, M. A., Liu, L., Gnaiger, E., and Wang, S. Y. 1989. Metabolic adaptations of several species of crustaceans and molluscs to hypoxia: tolerance and microcalorimetric studies. Biological Bulletin 177:303312.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
Thayer, C. W. 1975. Strength of pedicle attachment in articulate brachiopods. Palaeontology 1:388399.Google Scholar
Thayer, C. W. 1981. Ecology of living brachiopods. InBroadhead, T. W., ed. Lophophorates: notes for a short course. University of Tennessee Studies in Geological Sciences 5:110126.Google Scholar
Thayer, C. W. 1986a. Respiration and the function of brachiopod punctae. Lethaia 19:2331.CrossRefGoogle Scholar
Thayer, C. W. 1986b. Are brachiopods better than bivalves? Mechanisms of turbidity tolerance and their interaction with feeding in articulates. Paleobiology 12:161174.CrossRefGoogle Scholar
Theede, H. 1973. Comparative studies on the influence of oxygen deficiency and hydrogen sulphide on marine bottom invertebrates. Netherlands Journal of Sea Research 7:244252.CrossRefGoogle Scholar
Tomašových, A., and Zuschin, M. 2008. Comparative ecology and taphonomy of shallow- to deep-water bivalve- and brachiopod assemblages from the modern Red Sea and Gulf of Aden. Geological Society of America Abstracts with Programs 40 (6):102.Google Scholar
Tomašových, A., Carlson, S. J., and LaBarbera, M. 2008. Ontogenetic niche shift in the brachiopod Terebratalia transversa: relationship between the loss of rotation ability and allometric growth. Palaeontology 51:14711496.CrossRefGoogle Scholar
Tunnicliffe, V. 1981. High species diversity and abundance of the epibenthic community in an oxygen-deficient basin. Nature 294:354356.CrossRefGoogle Scholar
Tunnicliffe, V., and Wilson, K. 1988. Brachiopod populations: distribution in fjords of British Columbia (Canada) and tolerance of low oxygen conditions. Marine Ecology Progress Series 47:117128.CrossRefGoogle Scholar
Vahl, O. 1973. Pumping and oxygen cunsumption [sic] rates of Mytilus edulis L. of different sizes. Ophelia 12:4552.CrossRefGoogle Scholar
Vaquer-Sunyer, R., and Duarte, C. M. 2008. Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences USA 105:1545215457.CrossRefGoogle ScholarPubMed
Wang, W. X., and Widdows, J. 1993. Metabolic responses of the common mussel Mytilus edulis to hypoxia and anoxia. Marine Ecology Progress Series 95:205214.CrossRefGoogle Scholar
Wang, W. X., Widdows, J., and Page, D. S. 1992. Effects of organic toxicants on the anoxic energy metabolism of the mussel Mytilus edulis. Marine Environmental Research 34:327331.CrossRefGoogle Scholar
Wignall, P. B. 2001. Large igneous provinces and mass extinctions. Earth-Science Reviews 53:133.CrossRefGoogle Scholar
Wignall, P. B. 2007. The end-Permian mass extinction—how bad did it get? Geobiology 5:303309.CrossRefGoogle Scholar
Wignall, P. B., and Hallam, A. 1996. Facies change and the end-Permian mass extinction in S.E. Sichuan, China. Palaios 11:587596.CrossRefGoogle Scholar
Wignall, P. B., and Twitchett, R. J. 1996. Oceanic anoxia and the end Permian mass extinction. Science 272:11551158.CrossRefGoogle ScholarPubMed
Wignall, P. B., and Twitchett, R. J. 2002. Extent, duration, and nature of the Permian-Triassic superanoxic event. Geological Society of America Special Paper 356:395413.Google Scholar
Wignall, P. B., Hallam, A., Lai, X., and Yang, F. 1995. Palaeoenvironmental changes across the Permian/Triassic boundary at Shangsi (N. Sichuan, China). Historical Biology 10:175189.CrossRefGoogle Scholar
Wignall, P. B., Morante, R., and Newton, R. 1998. The Permo-Triassic transition in Spitsbergen: δ13Corg. chemostratigraphy, Fe and S geochemistry, facies, fauna and trace fossils. Geological Magazine 135:4762.CrossRefGoogle Scholar