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Aquatic biochronologies and climate change

Nature Climate Change volume 2, pages 849–857 (2012)Cite this article

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Abstract

Historical evidence provides essential context for models predicting the biological impacts of climate change. Such long-term data sets are relatively common for terrestrial taxa and environments, but sparse for aquatic systems. Aquatic biochronologies — generated from information recorded in the hard parts of fish, molluscs and corals that are archived in their millions worldwide — can provide valuable long-term ecological insights into marine and freshwater environments. These resources are, however, at present under-utilized in the measurement and prediction of ecological responses to climate change, despite their potential to provide unprecedented levels of spatial and temporal detail in aquatic environments.

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Figure 1: Examples of aquatic hard parts illustrating time-dependent structures and the biochronological data available.
Figure 2: The relationship among fish length, otolith increment width and age in estuary perch (Macquaria colonorum) from eastern Victoria, Australia.

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References

  1. Ozgul, A. et al. The dynamics of phenotypic change and the shrinking sheep of St. Kilda. Science 325, 464–467 (2009).

    CAS  Google Scholar 

  2. Penuelas, J., Filella, I. & Comas, P. Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region. Glob. Change Biol. 8, 531–544 (2002).

    Google Scholar 

  3. Jackson, J. B. C. et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–638 (2001).

    CAS  Google Scholar 

  4. Pyke, G. H. & Ehrlich, P. R. Biological collections and ecological/environmental research: A review, some observations and a look to the future. Biol. Rev. 85, 247–266 (2010).

    Google Scholar 

  5. Thackeray, S. J. et al. Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob. Change Biol. 16, 3304–3313 (2010).

    Google Scholar 

  6. Southward, A. J. et al. Long-term oceanographic and ecological research in the western English Channel. Adv. Mar. Biol. 47, 1–105 (2005).

    Google Scholar 

  7. Field, D. B., Baumgartner, T. R., Charles, C. D., Ferreira-Bartrina, V. & Ohman, M. D. Planktonic foraminifera of the California Current reflect 20th-century warming. Science 311, 63–66 (2006).

    CAS  Google Scholar 

  8. Richardson, A. J. & Poloczanska, E. S. Ocean science under-resourced, under threat. Science 320, 1294–1295 (2008).

    CAS  Google Scholar 

  9. Brander, K., Bruno, J., Hobday, A. & Schoeman, D. The value of attribution. Nature Clim. Change 1, 70–71 (2011).

    Google Scholar 

  10. Brown, C. J. et al. Quantitative approaches in climate change ecology. Glob. Change Biol. 17, 3697–3713 (2011).

    Google Scholar 

  11. Campana, S. E. Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J. Fish Biol. 59, 197–242 (2001).

    Google Scholar 

  12. Kalish, J. M. Pre-bomb and post-bomb radiocarbon in fish otoliths. Earth Planet. Sci. Lett. 114, 549–554 (1993).

    CAS  Google Scholar 

  13. Knutson, D. W., Buddemeier, R. W. & Smith, S. V. Coral chronometers: Seasonal growth bands in reef corals. Science 177, 270–272 (1972).

    CAS  Google Scholar 

  14. Pannella, G. & MacClintock, C. Biological and environmental rhythms reflected in molluscan shell growth. Mem. J. Paleontol. 42, 64–80 (1968).

    Google Scholar 

  15. Campana, S. E. & Thorrold, S. R. Otoliths, increments, and elements: Keys to a comprehensive understanding of fish populations? Can. J. Fish. Aquat. Sci. 58, 30–38 (2001).

    Google Scholar 

  16. Morrongiello, J. R., Robertson, S. & Thresher, R. Australian Otolith Collections http://www.otolithcollections.net (2011).

    Google Scholar 

  17. Andrus, C. F. T. Shell midden sclerochronology. Quat. Sci. Rev. 30, 2892–2905 (2011).

    Google Scholar 

  18. Roark, E. B., Guilderson, T. P., Dunbar, R. B., Fallon, S. J. & Mucciarone, D. A. Extreme longevity in proteinaceous deep-sea corals. Proc. Natl Acad. Sci. USA 106, 5204–5208 (2009).

    CAS  Google Scholar 

  19. Tracey, D. M. & Horn, P. L. Background and review of ageing orange roughy (Hoplostethus atlanticus, Trachichthyidae) from New Zealand and elsewhere. NZ J. Mar. Freshwat. Res. 33, 67–86 (1999).

    Google Scholar 

  20. Kilada, R. W., Campana, S. E. & Roddick, D. Validated age, growth, and mortality estimates of the ocean quahog (Arctica islandica) in the western Atlantic. ICES J. Mar. Sci. 64, 31–38 (2007).

    Google Scholar 

  21. Druffel, E. R. M. Geochemistry of corals: Proxies of past ocean chemistry, ocean circulation, and climate. Proc. Natl Acad. Sci. USA 94, 8354–8361 (1997).

    CAS  Google Scholar 

  22. Lough, J. M. & Cooper, T. F. New insights from coral growth band studies in an era of rapid environmental change. Earth Sci. Rev. 108, 170–184 (2011).

    CAS  Google Scholar 

  23. Fritts, H. C. & Swetnam, T. W. Dendroecology: A tool for evaluating variations in past and present forest environments. Adv. Ecol. Res. 19, 111–188 (1989).

    Google Scholar 

  24. Gergis, J. L. & Fowler, A. M. A history of ENSO events since AD 1525: Implications for future climate change. Climatic Change 92, 343–387 (2009).

    Google Scholar 

  25. Cook, E. R. & Kairiukstis, L. A. Methods of Dendrochronology: Applications in the Environmental Sciences (Kluwer Academic, 1990).

    Google Scholar 

  26. Fritts, H. C. Tree Rings and Climate (Academic, 1976).

    Google Scholar 

  27. Lapointe-Garant, M. P. et al. Use of tree rings to study the effect of climate change on trembling aspen in Quebec. Glob. Change Biol. 16, 2039–2051 (2010).

    Google Scholar 

  28. Campana, S. E. How reliable are growth back-calculations based on otoliths? Can. J. Fish. Aquat. Sci. 47, 2219–2227 (1990).

    Google Scholar 

  29. Casselman, J. M. Growth and relative size of calcified structures of fish. Trans. Am. Fish. Soc. 119, 673–688 (1990).

    Google Scholar 

  30. Guyette, R. P. & Rabeni, C. F. Climate response among growth increments of fish and trees. Oecologia 104, 272–279 (1995).

    Google Scholar 

  31. Morrongiello, J. R., Crook, D. A., King, A. J., Ramsey, D. S. L. & Brown, P. Impacts of drought and predicted effects of climate change on fish growth in temperate Australian lakes. Glob. Change Biol. 17, 745–755 (2011).

    Google Scholar 

  32. Rowell, K. et al. Diverting the Colorado River leads to a dramatic life history shift in an endangered marine fish. Biol. Conserv. 141, 1138–1148 (2008).

    Google Scholar 

  33. Kendall, N. W., Rich, H. B., Jensen, L. R. & Quinn, T. P. Climate effects on inter-annual variation in growth of the freshwater mussel (Anodonta beringiana) in an Alaskan lake. Freshwat. Biol. 55, 2339–2346 (2010).

    Google Scholar 

  34. Black, B. A. et al. Winter and summer upwelling modes and their biological importance in the California Current ecosystem. Glob. Change Biol. 17, 2536–2545 (2011).

    Google Scholar 

  35. Carilli, J. E., Norris, R. D., Black, B., Walsh, S. M. & McField, M. Century-scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold. Glob. Change Biol. 16, 1247–1257 (2010).

    Google Scholar 

  36. Ostazeski, J. J. & Spangler, G. R. Use of biochronology to examine interactions of freshwater drum, walleye and yellow perch in the Red Lakes of Minnesota. Environ. Biol. Fish. 61, 381–393 (2001).

    Google Scholar 

  37. De'ath, G., Lough, J. M. & Fabricius, K. E. Declining coral calcification on the Great Barrier Reef. Science 323, 116–119 (2009).

    CAS  Google Scholar 

  38. Neuheimer, A. B., Thresher, R. E., Lyle, J. M. & Semmens, J. M. Tolerance limit for fish growth exceeded by warming waters. Nature Clim. Change 1, 110–113 (2011).

    Google Scholar 

  39. Cooper, T. F., O'Leary, R. A. & Lough, J. M. Growth of Western Australian corals in the Anthropocene. Science 335, 593–596 (2012).

    CAS  Google Scholar 

  40. Thresher, R. E., Koslow, J. A., Morison, A. K. & Smith, D. C. Depth-mediated reversal of the effects of climate change on long-term growth rates of exploited marine fish. Proc. Natl Acad. Sci. USA 104, 7461–7465 (2007).

    CAS  Google Scholar 

  41. Black, B. A. Climate-driven synchrony across tree, bivalve, and rockfish growth-increment chronologies of the northeast Pacific. Mar. Ecol. Prog. Ser. 378, 37–46 (2009).

    Google Scholar 

  42. Francis, R. I. C. C. & Horn, P. L. Transition zone in otoliths of orange roughy (Hoplostethus atlanticus) and its relationship to the onset of maturity. Mar. Biol. 129, 681–687 (1997).

    Google Scholar 

  43. Hale, R. & Swearer, S. E. Otolith microstructural and microchemical changes associated with settlement in the diadromous fish Galaxias maculatus. Mar. Ecol. Prog. Ser. 354, 229–234 (2008).

    Google Scholar 

  44. Jorgensen, T. Long-term changes in age at sexual maturity of northeast Arctic cod (Gadus morhua L.). ICES J. Mar. Sci. 46, 235–248 (1990).

    Google Scholar 

  45. Barbee, N. C. et al. Large-scale variation in life history traits of the widespread diadromous fish, Galaxias maculatus, reflects geographic differences in local environmental conditions. Mar. Freshwat. Res. 62, 790–800 (2011).

    Google Scholar 

  46. Chan, K. S., Zhang, T. Y. & Bailey, K. M. Otolith biochronology reveals factors underlying dynamics in marine fish larvae. Mar. Ecol. Prog. Ser. 412, 1–10 (2010).

    Google Scholar 

  47. Sinclair, A. F., Swain, D. P. & Hanson, J. M. Measuring changes in the direction and magnitude of size-selective mortality in a commercial fish population. Can. J. Fish. Aquat. Sci. 59, 361–371 (2002).

    Google Scholar 

  48. Campana, S. E. Chemistry and composition of fish otoliths: Pathways, mechanisms and applications. Mar. Ecol. Prog. Ser. 188, 263–297 (1999).

    CAS  Google Scholar 

  49. Radtke, R. L., Showers, W., Moksness, E. & Lenz, P. Environmental information stored in otoliths: Insights from stable isotopes. Mar. Biol. 127, 161–170 (1996).

    Google Scholar 

  50. Lowenstam, H. A. & Weiner, S. On Biomineralization (Oxford Univ. Press, 1989).

    Google Scholar 

  51. Kalish, J. M. Otolith microchemistry: Validation of the effects of physiology, age and environment on otolith composition. J. Exp. Mar. Biol. Ecol. 132, 151–178 (1989).

    CAS  Google Scholar 

  52. Jones, J. B. & Campana, S. E. Stable oxygen isotope reconstruction of ambient temperature during the collapse of a cod (Gadus morhua) fishery. Ecol. Appl. 19, 1500–1514 (2009).

    Google Scholar 

  53. Gillanders, B. M. Otolith chemistry to determine movements of diadromous and freshwater fish. Aquat. Living Resour. 18, 291–300 (2005).

    CAS  Google Scholar 

  54. Crook, D. A., Macdonald, J. I. & Raadik, T. A. Evidence of diadromous movements in a coastal population of southern smelts (Retropinninae: Retropinna) from Victoria, Australia. Mar. Freshwat. Res. 59, 638–646 (2008).

    CAS  Google Scholar 

  55. Hoie, H., Folkvord, A. & Otterlei, E. Effect of somatic and otolith growth rate on stable isotopic composition of early juvenile cod (Gadus morhua L.) otoliths. J. Exp. Mar. Biol. Ecol. 289, 41–58 (2003).

    Google Scholar 

  56. Cuveliers, E. L., Bolle, L. J., Volckaert, F. A. M. & Maes, G. E. Influence of DNA isolation from historical otoliths on nuclear-mitochondrial marker amplification and age determination in an overexploited fish, the common sole (Solea solea L.). Mol. Ecol. Resour. 9, 725–732 (2009).

    CAS  Google Scholar 

  57. Nielsen, E. E. & Hansen, M. M. Waking the dead: The value of population genetic analyses of historical samples. Fish. Fish. 9, 450–461 (2008).

    Google Scholar 

  58. Morison, A. K., Robertson, S. G. & Smith, D. C. An integrated system for production fish aging: Image analysis and quality assurance. North Am. J. Fish Manage. 18, 587–598 (1998).

    Google Scholar 

  59. Black, B. A., Boehlert, G. W. & Yoklavich, M. M. Using tree-ring crossdating techniques to validate annual growth increments in long-lived fishes. Can. J. Fish. Aquat. Sci. 62, 2277–2284 (2005).

    Google Scholar 

  60. Helama, S., Schone, B. R., Black, B. A. & Dunca, E. Constructing long-term proxy series for aquatic environments with absolute dating control using a sclerochronological approach: Introduction and advanced applications. Mar. Freshwat. Res. 57, 591–599 (2006).

    Google Scholar 

  61. Campana, S. E. & Neilson, J. D. Microstructure of fish otoliths. Can. J. Fish. Aquat. Sci. 42, 1014–1032 (1985).

    Google Scholar 

  62. Punt, A. E., Walker, T. I., Taylor, B. L. & Pribac, F. Standardization of catch and effort data in a spatially-structured shark fishery. Fish Res. 45, 129–145 (2000).

    Google Scholar 

  63. Branch, T. A. et al. Fleet dynamics and fishermen behavior: Lessons for fisheries managers. Can. J. Fish. Aquat. Sci. 63, 1647–1668 (2006).

    Google Scholar 

  64. Ricker, W. E. Effects of size-selective mortality and sampling bias on estimates of growth, mortality, production and yield. J. Fish. Res. Board Can. 26, 479–541 (1969).

    Google Scholar 

  65. Francis, R. I. C. C. Back-calculation of fish length: A critical review. J. Fish Biol. 36, 883–904 (1990).

    Google Scholar 

  66. Wootton, R. J. Ecology of Teleost Fishes (Kluwer Academic, 1998).

    Google Scholar 

  67. Newman, S. J., Williams, D. M. & Russ, G. R. Age validation, growth and mortality rates of the tropical snappers (Pisces: Lutjanidae) Lutjanus adetii (Castelnau, 1873) and L. quinquelineatus (Bloch, 1790) from the central Great Barrier Reef, Australia. Mar. Freshwat. Res. 47, 575–584 (1996).

    Google Scholar 

  68. Morrissey, M. B. Exploiting natural history variation: Looking to fishes for quantitative genetic models of natural populations. Ecol. Freshwat. Fish 20, 328–345 (2011).

    Google Scholar 

  69. Weisberg, S., Spangler, G. & Richmond, L. S. Mixed effects models for fish growth. Can. J. Fish. Aquat. Sci. 67, 269–277 (2010).

    Google Scholar 

  70. Nussey, D. H., Wilson, A. J. & Brommer, J. E. The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20, 831–844 (2007).

    CAS  Google Scholar 

  71. Nussey, D. H., Clutton-Brock, T. H., Elston, D. A., Albon, S. D. & Kruuk, L. E. B. Phenotypic plasticity in a maternal trait in red deer. J. Anim. Ecol. 74, 387–396 (2005).

    Google Scholar 

  72. Kearney, M. & Porter, W. Mechanistic niche modelling: Combining physiological and spatial data to predict species' ranges. Ecol. Lett. 12, 334–350 (2009).

    Google Scholar 

  73. Harley, C. D. G. Climate change, keystone predation, and biodiversity loss. Science 334, 1124–1127 (2011).

    CAS  Google Scholar 

  74. Cook, E. R., Briffa, K. R., Meko, D. M., Graybill, D. A. & Funkhouser, G. The segment length curse in long tree-ring chronology development for palaeoclimatic studies. Holocene 5, 229–237 (1995).

    Google Scholar 

  75. McMahon, S. M. et al. Improving assessment and modelling of climate change impacts on global terrestrial biodiversity. Trends Ecol. Evol. 26, 249–259 (2011).

    Google Scholar 

  76. Anchukaitis, K. J. et al. Forward modeling of regional scale tree-ring patterns in the southeastern United States and the recent influence of summer drought. Geophys. Res. Lett. 33, L04705 (2006).

    Google Scholar 

  77. Hoeke, R. K., Jokiel, P. L., Buddemeier, R. W. & Brainard, R. E. Projected changes to growth and mortality of Hawaiian corals over the next 100 years. PLoS One 6, e18038 (2011).

    CAS  Google Scholar 

  78. Buckley, L. B. et al. Can mechanism inform species' distribution models? Ecol. Lett. 13, 1041–1054 (2010).

    Google Scholar 

  79. Harley, C. D. G. et al. The impacts of climate change in coastal marine systems. Ecol. Lett. 9, 228–241 (2006).

    Google Scholar 

  80. Chen, P. Y., Welsh, C. & Hamann, A. Geographic variation in growth response of Douglas fir to interannual climate variability and projected climate change. Glob. Change Biol. 16, 3374–3385 (2010).

    Google Scholar 

  81. Matta, M. E., Black, B. A. & Wilderbuer, T. K. Climate-driven synchrony in otolith growth-increment chronologies for three Bering Sea flatfish species. Mar. Ecol. Prog. Ser. 413, 137–145 (2010).

    Google Scholar 

  82. Rypel, A. L., Haag, W. R. & Findlay, R. H. Pervasive hydrologic effects on freshwater mussels and riparian trees in southeastern floodplain systems. Wetlands 29, 497–504 (2009).

    Google Scholar 

  83. Stocks, J., Stewart, J., Gray, C. A. & West, R. J. Using otolith increment widths to infer spatial, temporal and gender variation in the growth of sand whiting Sillago ciliata. Fisheries Manage. Ecol. 18, 121–131 (2011).

    Google Scholar 

  84. Pereira, D. L., Bingham, C., Spangler, G. R., Conner, D. J. & Cunningham, P. K. in Recent Developments in Fish Otolith Research (eds Secor, D. H., Dean, J. M. & Campana, S. E.) 177–196 (Univ. South Carolina Press, 1995).

    Google Scholar 

  85. LeBreton, G. T. O. & Beamish, F. H. Interannual growth variation in fish and tree rings. Can. J. Fish. Aquat. Sci. 57, 2345–2356 (2000).

    Google Scholar 

  86. Weisberg, S. Using hard-part increment data to estimate age and environmental effects. Can. J. Fish. Aquat. Sci. 50, 1229–1237 (1993).

    Google Scholar 

  87. Walsh, C. T., Gray, C. A., West, R. J., van der Meulen, D. E. & Williams, L. F. G. Growth, episodic recruitment and age truncation in populations of a catadromous percichthyid, Macquaria colonorum. Mar. Freshwat. Res. 61, 397–407 (2010).

    CAS  Google Scholar 

  88. Sharpe, D. M. T. & Hendry, A. P. Life history change in commercially exploited fish stocks: An analysis of trends across studies. Evol. Appl. 2, 260–275 (2009).

    Google Scholar 

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Acknowledgements

We thank A. Hobday and G. Tuck for helpful comments on earlier versions of this manuscript. This project was funded by CSIRO's Wealth from Oceans Flagship and J.R.M. was supported by a CSIRO OCE Postdoctoral Fellowship.

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  1. Commonwealth Scientific and Industrial Research Organisation (CSIRO), Wealth from Oceans Flagship, GPO Box 1538, Hobart, 7001, Tasmania, Australia

    John R. Morrongiello, Ronald E. Thresher & David C. Smith

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Morrongiello, J., Thresher, R. & Smith, D. Aquatic biochronologies and climate change. Nature Clim Change 2, 849–857 (2012). https://doi.org/10.1038/nclimate1616

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