Letter | Published:

Ocean acidification causes ecosystem shifts via altered competitive interactions

Nature Climate Change volume 3, pages 156159 (2013) | Download Citation


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 optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. 1.

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

  2. 2.

    , , & Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419–1434 (2010).

  3. 3.

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

  4. 4.

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

  5. 5.

    & 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).

  6. 6.

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

  7. 7.

    , , & Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc. Natl Acad. Sci. USA 108, 14515–14520 (2011).

  8. 8.

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

  9. 9.

    , & 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).

  10. 10.

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

  11. 11.

    , , , & High CO2 enhances the competitive strength of seaweeds over corals. Ecol. Lett. 14, 156–162 (2011).

  12. 12.

    & 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).

  13. 13.

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

  14. 14.

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

  15. 15.

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

  16. 16.

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

  17. 17.

    & Anthropogenic carbon and ocean pH. Nature 425, 365 (2003).

  18. 18.

    , & Effects of ocean acidification on macroalgal communities. J. Exp. Mar. Biol. Ecol. 400, 278–287 (2011).

  19. 19.

    & Development and stability of the fouling community at Beaufort, North Carolina. Ecol. Monogr. 47, 425–446 (1977).

  20. 20.

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

  21. 21.

    , , , & Testing the effects of ocean acidification on algal metabolism: Considerations for experimental designs. J. Phycol. 45, 1236–1251 (2009).

  22. 22.

    , , & Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Glob. Change Biol. 15, 2153–2162 (2009).

  23. 23.

    , , , & Decreased abundance of crustose coralline algae due to ocean acidification. Nature Geosci. 1, 114–117 (2007).

  24. 24.

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

  25. 25.

    , , , & Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions. Ecol. Lett. 15, 338–346 (2012).

  26. 26.

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

  27. 27.

    , & Adaptive evolution of a key phytoplankton species to ocean acidification. Nature Geosci. 5, 346–351 (2012).

  28. 28.

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

  29. 29.

    , & Thresholds and the resilience of Caribbean coral reefs. Nature 450, 98–102 (2007).

  30. 30.

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

Download references


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


  1. Department of Biology, Stanford University, Hopkins Marine Station, 100 Oceanview Blvd., Pacific Grove, California 93950, USA

    • Kristy J. Kroeker
    •  & Fiorenza Micheli
  2. Laboratory of Functional and Evolutionary Ecology, Stazione Zoologica Anton Dohrn, Villa Dohrn Punta San Pietro, 80077 Ischia, Naples, Italy

    • Maria Cristina Gambi


  1. Search for Kristy J. Kroeker in:

  2. Search for Fiorenza Micheli in:

  3. Search for Maria Cristina Gambi in:


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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Kristy J. Kroeker.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Information

About this article

Publication history






Further reading