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

Abstract

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 (2,000 ppm; 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 (400 ppm), exposure of M. beryllina embryos to 1,000 ppm 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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Effect of increased CO2 on early life M. beryllina survival and length.
Figure 2: CO2 sensitivity of the egg versus early post-hatch stage in M. beryllina.
Figure 3: M. berylina larvae exposed to normal and elevated levels of CO2.

References

  1. 1

    Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. Ocean acidification: The other CO2 problem. Annu. Rev. Mar. Sci. 1, 169–192 (2009).

    Article  Google Scholar 

  2. 2

    Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).

    CAS  Article  Google Scholar 

  3. 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. 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, 414–432 (2008).

    CAS  Article  Google Scholar 

  5. 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, 17246–17251 (2010).

    CAS  Article  Google Scholar 

  6. 6

    Kurihara, H., Kato, S. & Ishimatsu, A. Effects of increased seawater p CO 2 on early development of the oyster Crassostrea gigas. Aquat. Biol. 1, 91–98 (2007).

    CAS  Article  Google Scholar 

  7. 7

    Ishimatsu, A., Hayashi, M. & Kikkawa, T. Fishes in high-CO2, acidified oceans. Mar. Ecol. Prog. Ser. 373, 295–302 (2008).

    CAS  Article  Google Scholar 

  8. 8

    Caldeira, K. & Wickett, M. E. Anthropogenic carbon and ocean pH. Nature 425, 365–365 (2003).

    CAS  Article  Google Scholar 

  9. 9

    Sissenwine, M. P. in Exploitation of Marine Communities (ed. May, R.) 59–94 (Springer, 1984).

    Google Scholar 

  10. 10

    Trippel, E. A. & Chambers, R. C. in Early Life History and Recruitment in Fish Populations (eds Chambers, R. C. & Trippel, E. A.) xxi–xxxii (Chapman & Hall, 1997).

    Google Scholar 

  11. 11

    www.esrl.noaa.gov/gmd/ccgg/trends/.

  12. 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, 1394–1397 (2009).

    CAS  Article  Google Scholar 

  13. 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, 497–500 (1997).

    CAS  Article  Google Scholar 

  14. 14

    Riebesell, U. et al. Reduced calcification of marine plankton in response to increased atmospheric CO2 . Nature 407, 364–367 (2000).

    CAS  Article  Google Scholar 

  15. 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, 41–46 (2008).

    CAS  Article  Google Scholar 

  16. 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, 285–294 (2008).

    CAS  Article  Google Scholar 

  17. 17

    Hayashi, M., Kita, J. & Ishimatsu, A. Acid–base responses to lethal aquatic hypercapnia in three marine fishes. Mar. Biol. 144, 153–160 (2004).

    CAS  Article  Google Scholar 

  18. 18

    Munday, P. L. et al. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc. Natl Acad. Sci. USA 106, 1848–1852 (2009).

    CAS  Article  Google Scholar 

  19. 19

    Munday, P. L. et al. Replenishment of fish populations is threatened by ocean acidification. Proc. Natl Acad. Sci. USA 107, 12930–12934 (2010).

    CAS  Article  Google Scholar 

  20. 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, 68–75 (2010).

    Article  Google Scholar 

  21. 21

    Checkley, D. M. et al. Elevated CO2 enhances otolith growth in young fish. Science 324, 1683–1683 (2009).

    CAS  Article  Google Scholar 

  22. 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, 211–221 (2011).

    Article  Google Scholar 

  23. 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).

    Google Scholar 

  24. 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, 55–66 (1988).

    Article  Google Scholar 

  25. 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, 119–134 (1994).

    Article  Google Scholar 

  26. 26

    Mangor-Jensen, A. Water balance in developing eggs of the cod Gadus morhua L. Fish Physiol. Biochem. 3, 17–24 (1987).

    CAS  Article  Google Scholar 

  27. 27

    Perry, S. F. & Gilmour, K. M. Acid–base balance and CO2 excretion in fish: Unanswered questions and emerging models. Respir. Physiol. Neurobiol. 154, 199–215 (2006).

    CAS  Article  Google Scholar 

  28. 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, 127–136 (1990).

    CAS  Article  Google Scholar 

  29. 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, 1490–1492 (2008).

    CAS  Article  Google Scholar 

  30. 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).

Download references

Acknowledgements

We acknowledge the assistance of L. Merlo, R. Anderson, R. Light and Y. Tang. This work was supported by grants from the New Tamarind Foundation and National Science Foundation Biological Oceanography (no 1129622).

Author information

Affiliations

Authors

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.

Corresponding author

Correspondence to Christopher J. Gobler.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 392 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Baumann, H., Talmage, S. & Gobler, C. Reduced early life growth and survival in a fish in direct response to increased carbon dioxide. Nature Clim Change 2, 38–41 (2012). https://doi.org/10.1038/nclimate1291

Download citation

Further reading