Ocean acidification causes ecosystem shifts via altered competitive interactions

Abstract

Ocean acidification represents a pervasive environmental change that is predicted to affect a wide range of species1,2, yet our understanding of the emergent ecosystem impacts is very limited. Many studies report detrimental effects of acidification on single species in lab studies, especially those with calcareous shells or skeletons3,4,5. Observational studies using naturally acidified ecosystems have shown profound shifts away from such calcareous species6,7,8, and there has been an assumption that direct impacts of acidification on sensitive species drive most ecosystem responses. We tested an alternative hypothesis that species interactions attenuate or amplify the direct effects of acidification on individual species9,10,11,12. Here, we show that altered competitive dynamics between calcareous species and fleshy seaweeds drive significant ecosystem shifts in acidified conditions. Although calcareous species recruited and grew at similar rates in ambient and low pH conditions during early successional stages, they were rapidly overgrown by fleshy seaweeds later in succession in low pH conditions. The altered competitive dynamics between calcareous species and fleshy seaweeds is probably the combined result of decreased growth rates of calcareous species, increased growth rates of fleshy seaweeds, and/or altered grazing rates13. Phase shifts towards ecosystems dominated by fleshy seaweed are common in many marine ecosystems14,15,16, and our results suggest that changes in the competitive balance between these groups represent a key leverage point through which the physiological responses of individual species to acidification could indirectly lead to profound ecosystem changes in an acidified ocean.

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: Community structure at 14 months.
Figure 2: Successional trajectories defined by the mean community structure (N = 3–6 tiles per time point) at 0, 1.5, 2.5, 3.5, 6, and 14 months in an nMDS plot estimated by zero-adjusted Brace–Curtis similarities between tiles.
Figure 3: Variation in community development.

References

  1. 1

    Feely, R. A. et al. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305, 362–366 (2004).

    CAS  Article  Google Scholar 

  2. 2

    Kroeker, K. J., Kordas, R. L., Crim, R. N. & Singh, G. G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419–1434 (2010).

    Article  Google Scholar 

  3. 3

    Kleypas, J. A. et al. Geochemical consequences of increased atmospheric CO2 on coral reefs. Science 284, 118–120 (1999).

    CAS  Article  Google Scholar 

  4. 4

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

    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

    Hall-Spencer, J. M. et al. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454, 96–99 (2008).

    CAS  Article  Google Scholar 

  7. 7

    Kroeker, K. J., Micheli, F., Gambi, M. C. & Martz, T. R. Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc. Natl Acad. Sci. USA 108, 14515–14520 (2011).

    CAS  Article  Google Scholar 

  8. 8

    Fabricius, K. E. et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Clim. Change 1, 1–5 (2011).

    Article  Google Scholar 

  9. 9

    Wootton, J. T., Pfister, C. A. & Forester, J. D. Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proc. Natl Acad. Sci. USA 105, 18848–18853 (2008).

    CAS  Article  Google Scholar 

  10. 10

    Sanford, E. Regulation of keystone predation by small changes in ocean temperature. Science 283, 2095–2097 (1999).

    CAS  Article  Google Scholar 

  11. 11

    Diaz-Pulido, G., Gouezo, M., Tilbrook, B., Dove, S. & Anthony, K. R. N. High CO2 enhances the competitive strength of seaweeds over corals. Ecol. Lett. 14, 156–162 (2011).

    Article  Google Scholar 

  12. 12

    Connell, S. D. & Russell, B. D. The direct effects of increasing CO2 and temperature on non-calcifying organisms: Increasing the potential for phase shifts in kelp forests. Proc. R. Soc. B 277, 1409–1415 (2010).

    Article  Google Scholar 

  13. 13

    Connell, J. H. & Slatyr, R. O. Mechanisms of succession in natural communities and their role in community stability and organization. Am. Nat. 111, 1119–1144 (1977).

    Article  Google Scholar 

  14. 14

    Hughes, T. P. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265, 1547–1551 (1994).

    CAS  Article  Google Scholar 

  15. 15

    Airoldi, L. & Beck, M. W. Loss, status and trends for coastal marine habitats of Europe. Oceanogr. Mar. Biol. Annu. Rev. 45, 345–405 (2007).

    Google Scholar 

  16. 16

    Connell, S. D. et al. Recovering a lost baseline: Missing kelp forests from a metropolitan coast. Mar. Ecol. Prog. Ser. 360, 63–72 (2008).

    Article  Google Scholar 

  17. 17

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

    CAS  Article  Google Scholar 

  18. 18

    Porzio, L., Buia, M. C. & Hall-Spencer, J. M. Effects of ocean acidification on macroalgal communities. J. Exp. Mar. Biol. Ecol. 400, 278–287 (2011).

    CAS  Article  Google Scholar 

  19. 19

    Sutherland, J. P. & Karlson, R. H. Development and stability of the fouling community at Beaufort, North Carolina. Ecol. Monogr. 47, 425–446 (1977).

    Article  Google Scholar 

  20. 20

    Farrell, T. M. Models and mechanisms of succession: An example from a rocky intertidal community. Ecol. Monogr. 61, 95–113 (1991).

    Article  Google Scholar 

  21. 21

    Hurd, C. L., Hepburn, C., Currie, K. I., Raven, J. A. & Hunter, K. A. Testing the effects of ocean acidification on algal metabolism: Considerations for experimental designs. J. Phycol. 45, 1236–1251 (2009).

    CAS  Article  Google Scholar 

  22. 22

    Russell, B. D., Thompson, J-A.I., Falkenberg, L. J. & Connell, S. D. Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Glob. Change Biol. 15, 2153–2162 (2009).

    Article  Google Scholar 

  23. 23

    Kuffner, I. B., Andersson, A. J., Jokiel, P. L., Rodgers, K. S. & Mackenzie, F. T. Decreased abundance of crustose coralline algae due to ocean acidification. Nature Geosci. 1, 114–117 (2007).

    Article  Google Scholar 

  24. 24

    Steneck, R. S. The ecology of coralline algal crusts: Convergent patterns and adaptive strategies. Annu. Rev. Ecol. Syst. 17, 273–303 (1986).

    Article  Google Scholar 

  25. 25

    Doropoulos, C., Ward, S., Diaz-Pulido, G., Hoegh-Guldberg, O. & Mumby, P. J. Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions. Ecol. Lett. 15, 338–346 (2012).

    Article  Google Scholar 

  26. 26

    Hofmann, G. E. et al. High-frequency dynamics of ocean pH: A multi-ecosystem comparison. PLoS ONE e28983 (2011).

    CAS  Article  Google Scholar 

  27. 27

    Lohbeck, K. T., Riebesell, U. & Reusch, T. B. H. Adaptive evolution of a key phytoplankton species to ocean acidification. Nature Geosci. 5, 346–351 (2012).

    CAS  Article  Google Scholar 

  28. 28

    Hughes, T. P. et al. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr. Biol. 17, 360–365 (2007).

    CAS  Article  Google Scholar 

  29. 29

    Mumby, P. J., Hastings, A. & Edwards, H. J. Thresholds and the resilience of Caribbean coral reefs. Nature 450, 98–102 (2007).

    CAS  Article  Google Scholar 

  30. 30

    Bates, D. & Maechler, M. lme4: Linear mixed-effects models using S4 classes. R Package Version 0.999375-32 (2009).

Download references

Acknowledgements

We thank E. Sanford and S. Palumbi for comments that improved earlier versions of this manuscript. We are grateful to the staff from the Ischia benthic ecology group of the Stazione Zoologica Anton Dohrn, and especially M. C. Buia and L. Porzio for field/lab assistance and advice regarding algae, and to M. Lorenti, B. Iacono and Capt. V. Rando for their field assistance. A. Haupt was instrumental in the field. A. Callea (molluscs), G. Innocenti (crustaceans/echinoderms) and J. F. Sartone (algae) helped in classifications. This research was supported by a National Science Foundation GRF (K.J.K.), Stanford University Chambers Fellowship (F.M.), and the Stazione Zoologica Anton Dohrn.

Author information

Affiliations

Authors

Contributions

K.J.K., F.M. and M.C.G. designed experiments, K.J.K. and M.C.G. performed field experiments, K.J.K. analysed data and wrote the paper with contributions from F.M. and M.C.G.

Corresponding author

Correspondence to Kristy J. Kroeker.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 621 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kroeker, K., Micheli, F. & Gambi, M. Ocean acidification causes ecosystem shifts via altered competitive interactions. Nature Clim Change 3, 156–159 (2013). https://doi.org/10.1038/nclimate1680

Download citation

Further reading