Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-19T21:58:40.700Z Has data issue: false hasContentIssue false

Metabolic rate of late Holocene freshwater fish: Evidence from δ13C values of otoliths

Published online by Cambridge University Press:  08 April 2016

Christopher M. Wurster
Affiliation:
Department of Earth Sciences, 204 Heroy Geology Laboratory Syracuse University, Syracuse, New York 13244
William P. Patterson
Affiliation:
Department of Earth Sciences, 204 Heroy Geology Laboratory Syracuse University, Syracuse, New York 13244

Abstract

We examine patterns of intra-otolith variation in δ13C values of fossil Aplodinotus grunniens (freshwater drum) otoliths recovered from an archeological site in northeast Tennessee. We find three repeatable patterns: an initial increase early in ontogeny followed by relatively stable δ13C values as the fish ages, an initial strong covariation between seasonal δ18O and δ13C values, and a decrease with age in the magnitude of seasonal change in δ13C values. These last two observations are illustrated by seasonal least-squares linear regressions between δ13C and δ18O values that tend to progressively decrease in r2 value and slope with fish age. These patterns are evaluated by using a mass balance model in which otolith δ13C values are derived from dissolved inorganic carbon of ambient water mixing with carbon derived from metabolic processes. The proportion of metabolically derived carbon is found to be the dominant factor controlling intra-otolith variation in δ13C values.

Thus, the difference between maximum and minimum δ13C values from a single otolith (δ13Cmax-min) is postulated to reflect the total change in metabolic rate over the lifetime of a fish. δ13Cmax-min values significantly and negatively covary with average δ18O(CaCO3) values, suggesting either a higher total change in metabolic rate over the lifetime of a fish in cooler climates characterized by shorter growing seasons, or a decrease in summer/winter precipitation ratio. A proxy for metabolic rate preserved in otoliths would facilitate the understanding of evolutionary history in physiological traits of fishes and improve our understanding of bioenergetics.

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

Atekwana, E. A., and Krishnamurthy, R. V. 1998. Seasonal variations of dissolved inorganic carbon and δ13C of surface waters: application of a modified gas evolution technique. Journal of Hydrology 205:265278.Google Scholar
Boisclair, D., and Leggett, W. C. 1989. The importance of activity in bioenergetics model applied to actively foraging fishes. Canadian Journal of Fisheries and Aquatic Sciences 46:18591867.Google Scholar
Calow, P. 1985. Adaptive aspects of energy allocation. Pp. 1331in Tytler, P. and Calow, P., eds. Fish energetics: new perspectives. Johns Hopkins University Press, Baltimore.Google Scholar
Campana, S. E. 1999. Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Marine Ecology Progress Series 188:263297.Google Scholar
Campana, S. E., and Neilson, J. D. 1985. Microstructure of fish otoliths. Canadian Journal of Fisheries and Aquatic Sciences 39:10141032.Google Scholar
Casselman, J. M. 1987. Determination of age and growth. Pp. 209242in Weatherley, A. H. and Gill, H. S., eds. The biology of fish growth. Academic Press, London.Google Scholar
Casteel, R. W. 1976. Fish remains in archeology and paleoenvironmental studies. Academic Press, New York.Google Scholar
Dansgaard, W. 1964. Stable isotopes in precipitation. Tellus 16:436468.Google Scholar
Degens, E. T. 1978. Why do organisms calcify? Chemical Geology 25:257269.CrossRefGoogle Scholar
Degens, E. T., Deuser, W. G., and Haedrich, R. L. 1969. Molecular structure and composition of fish otoliths. Marine Biology 2:105113.CrossRefGoogle Scholar
DeNiro, M. J., and Epstein, S. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42:495506.Google Scholar
Dettman, D. L., Reische, A. K., and Lohmann, K. C. 1999. Controls on the stable isotope composition of seasonal growth bands in aragonitic fresh-water bivalves (Unionidae). Geochimica et Cosmochimica Acta 63:10491057.Google Scholar
Dreves, D. P., Timmons, T. J., and Henson, J. 1996. Age, growth, and food of freshwater drum, Aplodinotus grunniens (Sciaenidae), in Kentucky Lake, Kentucky/Tennessee. Transactions of the Kentucky Academy of Science 57:2226.Google Scholar
Elliott, J. M. 1979. Energetics of freshwater teleosts. Symposia of the Zoological Society of London 44:2961.Google Scholar
Fry, B. 1999. Using stable isotopes to monitor watershed influences on aquatic trophodynamics. Canadian Journal of Fisheries and Aquatic Sciences 56:21672171.Google Scholar
Fry, B., and Sherr, E. B. 1984. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contributions in Marine Science 27:1347.Google Scholar
Gauldie, R. W. 1996. Biological factors controlling the carbon isotope record in fish otoliths: principles and evidence. Comparative Biochemistry and Physiology B 115B:201208.Google Scholar
Hanson, P. C., Johnson, T. B., Schindler, D. E., and Kitchell, J. F. 1997. Fish bioenergetics 3.0. University of Wisconsin, Sea Grant Institute, Technical Report WISCU-T-97-001, Madison.Google Scholar
Hartman, K. J., and Brandt, S. B. 1995a. Comparative energetics and the development of bioenergetics models for sympatric estuarine piscivores. Canadian Journal of Fisheries and Aquatic Sciences 52:16471666.CrossRefGoogle Scholar
Hartman, K. J., and Brandt, S. B. 1995b. Predatory demand and impact of striped bass, bluefish, and weakfish in the Chesapeake Bay: applications of bioenergetics models. Canadian Journal of Fisheries and Aquatic Sciences 52:16671687.Google Scholar
Harvey, C. J., Hanson, P. C., Essington, T. E., Brown, P. B., and Kitchell, J. F. 2002. Using bioenergetics models to predict stable isotope ratios in fishes. Canadian Journal of Fisheries and Aquatic Sciences 59:115124.Google Scholar
He, J., and Stewart, D. J. 1998. Ontogeny of energetic relationships and potential effects of tissue turnover: a comparative modeling study on lake trout. Canadian Journal of Fisheries and Aquatic Sciences 55:25182532.Google Scholar
Hughes, G. M., and Al-Kadhomiy, N. K. 1988. Changes in scaling of respiratory systems during the development of fishes. Journal of the Marine Biological Association of the United Kingdom 68:489498.Google Scholar
Junger, M., and Planas, D. 1994. Quantitative use of stable carbon isotope analysis to determine the trophic base of invertebrate communities in a boreal forest lotic system. Canadian Journal of Fisheries and Aquatic Sciences 51:5261.Google Scholar
Kalish, J. M. 1991a. 13C and 18O isotopic disequilibria in fish otoliths: metabolic and kinetic effects. Marine Ecology Progress Series 75:191203.Google Scholar
Kalish, J. M. 1991b. Oxygen and carbon stable isotopes in the otoliths of wild and laboratory-reared Australian salmon Arripis trutta. Marine Biology 110:3747.Google Scholar
Kitchell, J. F., Stewart, D. J., and Weininger, D. 1977. Applications of a bioenergetics model to yellow perch (Perca flavescens) and walleye (Stizostedion vitreum vitreum). Journal of the Fisheries Research Board of Canada 34:19221935.Google Scholar
LaBaugh, J. W., Rosenberry, D. O., and Winter, T. C. 1995. Groundwater contribution to the water and chemical budgets of Williams Lake, Minnesota, 1980–1991. Canadian Journal of Fisheries and Aquatic Sciences 52:754767.Google Scholar
Liem, K. F. 1980. Acquisition of energy by teleosts: adaptive mechanisms and evolutionary patterns. Pp. 299334in Ali, M. A., ed. Environmental physiology of fishes. Plenum, New York.CrossRefGoogle Scholar
McConnaughey, T. A., Burdett, J., Whelan, J. F., and Paull, C. K. 1997. Carbon isotopes in biological carbonates: respiration and photosynthesis. Geochimica et Cosmochimica Acta 61:611622.CrossRefGoogle Scholar
McInerny, M. C., and Held, J. W. 1995. First-year growth of seven co-occurring fish species of navigation pool 9 of the Mississippi River. Journal of Freshwater Ecology 10:3341.Google Scholar
Nolf, D. 1995. Studies on fossil otoliths: the state of the art. Pp. 513544in Secor, D. H., Dean, J. M., and Campana, S. E., eds. Recent developments in fish otolith research. University of South Carolina, Columbia.Google Scholar
Panella, G. 1980. Growth patterns in fish sagittae. Pp. 519560in Rhodes, D. C. and Lutz, R. A., eds. Skeletal growth of aquatic organisms. Plenum, New York.Google Scholar
Patterson, W. P. 1998. North American continental seasonality during the last millennium: high-resolution analysis of sagittal otoliths. Palaeogeography, Palaeoclimatology, Palaeoecology, 138:271303.CrossRefGoogle Scholar
Patterson, W. P. 1999. Oldest isotopically characterized fish otoliths provide insight to Jurassic continental climate of Europe. Geology 27:199202.Google Scholar
Patterson, W. P., Smith, G. R., and Lohmann, K. C. 1993. Continental paleothermometry and seasonality using the isotopic composition of aragonitic otoliths of freshwater fishes. In Swart, P., Lohmann, K. C., McKenzie, J., and Savin, S., eds. Continental climate change from isotopic records American Geophysical Union Monograph 78:191202.Google Scholar
Patterson, W. P., and Smith, G. R. 2002. Uses of fishes in analysis of paleolimnology. Pp. 173187in Smol, J. P., Birks, J. J. B., and Last, W. M., eds. Tracking environmental change using lake sediments, Vol. 4. Zoological Indicators. Kluwer Academic, Dordrecht.Google Scholar
Post, J. R., and Lee, J. A. 1996. Metabolic ontogeny of teleost fishes. Canadian Journal of Fisheries and Aquatic Sciences 53:910923.Google Scholar
Quay, P. D., Emerson, S. R., Quay, B. M., and Devol, A. H. 1986. The carbon cycle for Lake Washington: a stable isotope study. Limnology and Oceanography 31:596611.Google Scholar
Rand, P. S., Stewart, D. J., Seelbach, P. W., Jones, M. L., and Wedge, L. R. 1993. Modeling steelhead population energetics in Lakes Michigan and Ontario. Transactions of the American Fisheries Society 122:9771001.Google Scholar
Romanek, C. S., Grossman, E. L., and Morse, J. W. 1992. Carbon isotopic fractionation in synthetic aragonite and calcite: effects of temperature and precipitation rate. Geochimica et Cosmochimica Acta 56:419430.Google Scholar
Rozanski, K., Araguas-Araguas, L., and Gonfiantini, R. 1993. Isotopic patterns in modern global precipitation. In Swart, P. K., Lohmann, K. C., McKenzie, J., and Savin, S., eds. Climatic change in continental isotopic records. American Geophysical Union Monograph 78:136.Google Scholar
Schaeffer, J. S., Haas, R. C., Diana, J. S., and Breck, J. E. 1999. Field test of two energetic models for yellow perch. Transactions of the American Fisheries Society 128:414435.Google Scholar
Schwarcz, H. P., Gao, Y., Campana, S., Browne, D., Knyf, M., and Brand, U. 1998. Stable carbon isotope variations in otoliths of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 55:17981806.Google Scholar
Stewart, D. J., Weininger, D., Rottiers, D. V., and Edsall, T. A. 1983. An energetics model for lake trout, Salvelinus namaycusch: application to the Lake Michigan population. Canadian Journal of Fisheries and Aquatic Sciences 40:16471666.Google Scholar
Thorrold, S. R., Campana, S. E., Jones, C. M., and Swart, P. K. 1997. Factors determining 13C and 18O fractionation in aragonitic otoliths of marine fish. Geochimica et Cosmochimica Acta 61:29092919.Google Scholar
Tieszen, L. L., Boutton, T. W., Tesdahl, K. G., and Slade, N. A. 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:3237.Google Scholar
Ursin, E. 1979. Principles of growth in fishes. Symposia of the Zoological Society of London 44:6387.Google Scholar
Vannote, R. L., Minshall, G. W., Cummins, K. W., Sedell, J. R., and Cushing, C. E. 1980. The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences 37:130137.Google Scholar
Veinott, G. I., and Cornett, R. J. 1998. Carbon isotopic disequilibrium in the shell of the freshwater mussel Elliptio complanata. Applied Geochemistry 13:4957.CrossRefGoogle Scholar
von Bertalanffy, L. 1938. A quantitative theory of organic growth (inquiries on growth laws, II). Human Biology 10:181213.Google Scholar
von Grafenstein, U., Erlernkeuser, H., and Trimborn, P. 1999. Oxygen and carbon isotopes in modern fresh-water ostracod valves: assessing vital offsets and autecological effects of interest for palaeoclimate studies. Palaeogeography Palaeoclimatology Palaeoecology 148:133152.Google Scholar
Wahl, D. H., Bruner, K., and Nielson, L. A. 1988. Trophic ecology of freshwater drum in large rivers. Journal of Freshwater Ecology 4:483491.Google Scholar
Wang, X., and Veizer, J. 2000. Respiration/photosynthesis balance of terrestrial aquatic ecosystems, Ottawa area, Canada. Geochimica et Cosmochimica Acta 64:37773786.Google Scholar
Weidman, C. R., and Millner, R. 2000. High-resolution stable isotope records from North Atlantic cod. Fisheries Research 46:327342.Google Scholar
Whitledge, G. W., and Rabeni, C. F. 1997. Energy sources and ecological role of crayfishes in an Ozark stream: insights from stable isotopes and gut analysis. Canadian Journal of Fisheries and Aquatic Sciences 54:25552563.Google Scholar
Wurster, C. M., and Patterson, W. P. 2001. Late Holocene climate change for the eastern interior United States: evidence from high-resolution sagittal otolith stable isotope ratios of oxygen. Palaeogeography Palaeoclimatology Palaeoecology 170:81100.Google Scholar
Wurster, C. M., Patterson, W. P., and Cheatham, M. M. 1999. Advances in micromilling techniques: a new apparatus for acquiring high-resolution oxygen and carbon stable isotope values and major/minor elemental ratios from accretionary carbonate. Computers and Geosciences 25:11551162.Google Scholar
Yoshioka, T., Wada, E., and Hayashi, H. 1994. A stable isotope study on seasonal food web dynamics in a eutrophic lake. Ecology 75:835846.Google Scholar