Reduced early life growth and survival in a fish in direct response to increased carbon dioxide

Journal name:
Nature Climate Change
Volume:
2,
Pages:
38–41
Year published:
DOI:
doi:10.1038/nclimate1291
Received
Accepted
Published online

Absorption of anthropogenic carbon dioxide by the world’s oceans is causing mankind’s ‘other CO2 problem’, ocean acidification1. Although this process will challenge marine organisms that synthesize calcareous exoskeletons or shells2, 3, 4, 5, 6, it is unclear how it will affect internally calcifying organisms, such as marine fish7. Adult fish tolerate short-term exposures to CO2 levels that exceed those predicted for the next 300 years (~2,000ppm; ref. 8), but potential effects of increased CO2 on growth and survival during the early life stages of fish remain poorly understood7. Here we show that the exposure of early life stages of a common estuarine fish (Menidia beryllina) to CO2 concentrations expected in the world’s oceans later this century caused severely reduced survival and growth rates. When compared with present-day CO2 levels (~400ppm), exposure of M. beryllina embryos to ~1,000ppm until one week post-hatch reduced average survival and length by 74% and 18%, respectively. The egg stage was significantly more vulnerable to high CO2-induced mortality than the post-hatch larval stage. These findings challenge the belief that ocean acidification will not affect fish populations, because even small changes in early life survival can generate large fluctuations in adult-fish abundance9, 10.

At a glance

Figures

  1. Effect of increased CO2 on early life M. beryllina survival and length.
    Figure 1: Effect of increased CO2 on early life M. beryllina survival and length.

    a, Survival was averaged across replicates (experiment 1, n=3; experiments 2, 3, n=4; experiment 4, n=6; experiment 5, n=5) for each experiment and CO2level. b, Weighted means (±1 s.e.m.) of standard length averaged across replicates per experiment and CO2 level. Pooled data in a and b were fitted with an exponential decay model (thick grey line) with 95% confidence intervals (thin grey lines). Experiment 1, red squares; experiment 2, blue down triangles; experiment 3, green diamonds; experiment 4, yellow circles; experiment 5, black up triangles. Points represent means±1 s.d.

  2. CO2 sensitivity of the egg versus early post-hatch stage in M. beryllina.
    Figure 2: CO2 sensitivity of the egg versus early post-hatch stage in M. beryllina.

    Bars depict average survival (±1 s.e.m.) 10 days after fertilization in control (410ppm), increased (780ppm) and ‘switch’, where CO2 concentration was increased only after eggs hatched (5 days post-fertilization), treatments. Precise CO2 levels and complete carbonate chemistry from experiments appear in Supplementary Tables S1–S5.

  3. M. berylina larvae exposed to normal and elevated levels of CO2.
    Figure 3: M. berylina larvae exposed to normal and elevated levels of CO2.

    ac, Larvae with curved or curled bodies were significantly more common at increased (b,c) when compared with control (a) CO2 levels. Scale bar=1mm.

References

  1. Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. Ocean acidification: The other CO2 problem. Annu. Rev. Mar. Sci. 1, 169192 (2009).
  2. Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681686 (2005).
  3. Kleypas, J. A. et al. Impacts of Ocean Acidification on Coral Reefs and Other Marine Calcifiers: A Guide for Future Research (Report of a workshop held 18–20 April 2005, St. Petersburg, FL, Sponsored by NSF, NOAA, and the US Geological Survey, 2006).
  4. Fabry, V. J., Seibel, B. A., Feely, R. A. & Orr, J. C. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Res. 65, 414432 (2008).
  5. Talmage, S. C. & Gobler, C. J. Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proc. Natl Acad. Sci. USA 107, 1724617251 (2010).
  6. Kurihara, H., Kato, S. & Ishimatsu, A. Effects of increased seawater pCO2 on early development of the oyster Crassostrea gigas. Aquat. Biol. 1, 9198 (2007).
  7. Ishimatsu, A., Hayashi, M. & Kikkawa, T. Fishes in high-CO2, acidified oceans. Mar. Ecol. Prog. Ser. 373, 295302 (2008).
  8. Caldeira, K. & Wickett, M. E. Anthropogenic carbon and ocean pH. Nature 425, 365365 (2003).
  9. Sissenwine, M. P. in Exploitation of Marine Communities (ed. May, R.) 5994 (Springer, 1984).
  10. Trippel, E. A. & Chambers, R. C. in Early Life History and Recruitment in Fish Populations (eds Chambers, R. C. & Trippel, E. A.) xxixxxii (Chapman & Hall, 1997).
  11. www.esrl.noaa.gov/gmd/ccgg/trends/.
  12. Tripati, A. K., Roberts, C. D. & Eagle, R. A. Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science 326, 13941397 (2009).
  13. Spero, H. J., Bijma, J., Lea, D. W. & Bemis, B. E. Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes. Nature 390, 497500 (1997).
  14. Riebesell, U. et al. Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407, 364367 (2000).
  15. Kurihara, H., Matsui, M., Furukawa, H., Hayashi, M. & Ishimatsu, A. Long-term effects of predicted future seawater CO2 conditions on the survival and growth of the marine shrimp Palaemon pacificus. J. Exp. Mar. Biol. Ecol. 367, 4146 (2008).
  16. Dupont, S., Havenhand, J., Thorndyke, W., Peck, L. & Thorndyke, M. C. Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar. Ecol. Prog. Ser. 373, 285294 (2008).
  17. Hayashi, M., Kita, J. & Ishimatsu, A. Acid–base responses to lethal aquatic hypercapnia in three marine fishes. Mar. Biol. 144, 153160 (2004).
  18. Munday, P. L. et al. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc. Natl Acad. Sci. USA 106, 18481852 (2009).
  19. Munday, P. L. et al. Replenishment of fish populations is threatened by ocean acidification. Proc. Natl Acad. Sci. USA 107, 1293012934 (2010).
  20. Dixson, D. L., Munday, P. L. & Jones, G. P. Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol. Lett. 13, 6875 (2010).
  21. Checkley, D. M. et al. Elevated CO2 enhances otolith growth in young fish. Science 324, 16831683 (2009).
  22. Munday, P. L., Gagliano, M., Donelson, J. M., Dixson, D. L. & Thorrold, S. R. Ocean acidification does not affect the early life history development of a tropical marine fish. Mar. Ecol. Prog. Ser. 423, 211221 (2011).
  23. Riebesell, U., Fabry, V. J., Hansson, L. & Gattuso, J. P. in Guide to Best Practices for Ocean Acidification Research and Data Reporting (Publications Office of the European Union, 2010).
  24. Anderson, J. T. A review of size dependent survival during pre-recruit stages of fishes in relation to recruitment. J. Northw. Atl. Fish. Sci. 8, 5566 (1988).
  25. Leggett, W. C. & Deblois, E. Recruitment in marine fishes: Is it regulated by starvation and predation in the egg and larval stages? Neth. J. Sea Res. 32, 119134 (1994).
  26. Mangor-Jensen, A. Water balance in developing eggs of the cod Gadus morhua L. Fish Physiol. Biochem. 3, 1724 (1987).
  27. Perry, S. F. & Gilmour, K. M. Acid–base balance and CO2 excretion in fish: Unanswered questions and emerging models. Respir. Physiol. Neurobiol. 154, 199215 (2006).
  28. Hemmer, M. J., Middaugh, D. P. & Moore, J. C. Effects of temperature and salinity on Menidia beryllina embryos exposed to terbufos. Dis. Aquat. Org. 8, 127136 (1990).
  29. Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D. & Hales, B. Evidence for upwelling of corrosive ‘acidified’ water onto the continental shelf. Science 320, 14901492 (2008).
  30. Salisbury, J., Green, M., Hunt, C. & Campbell, J. Coastal acidification by rivers: A threat to shellfish? EOS Trans. AGU 89 http://dx.doi.org/10.1029/2008EO500001 (2008).

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Author information

Affiliations

  1. School of Marine & Atmospheric Sciences, Stony Brook University, Stony Brook, NY 11794, USA

    • Hannes Baumann,
    • Stephanie C. Talmage &
    • Christopher J. Gobler

Contributions

H.B., S.C.T. and C.J.G. designed the experiments, conducted the experiments, generated the data, analysed samples, analysed the data and wrote the manuscript.

Competing financial interests

The authors declare no competing financial interests.

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