Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Ocean acidification reduces demersal zooplankton that reside in tropical coral reefs

Abstract

The in situ effects of ocean acidification on zooplankton communities remain largely unexplored. Using natural volcanic CO2 seep sites around tropical coral communities, we show a threefold reduction in the biomass of demersal zooplankton in high-CO2 sites compared with sites with ambient CO2. Differences were consistent across two reefs and three expeditions. Abundances were reduced in most taxonomic groups. There were no regime shifts in zooplankton community composition and no differences in fatty acid composition between CO2 levels, suggesting that ocean acidification affects the food quantity but not the quality for nocturnal plankton feeders. Emergence trap data show that the observed reduction in demersal plankton may be partly attributable to altered habitat. Ocean acidification changes coral community composition from branching to massive bouldering coral species, and our data suggest that bouldering corals represent inferior daytime shelter for demersal zooplankton. Since zooplankton represent a major source of nutrients for corals, fish and other planktivores, this ecological feedback may represent an additional mechanism of how coral reefs will be affected by ocean acidification.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Differences in zooplankton biomass between control and high-CO2 sites, derived from horizontal net tows.
Figure 2: Abundance ratios (high-CO2/control) for selected zooplankton taxa.
Figure 3: Differences in communities of nocturnal reef-associated zooplankton between control and high-CO2 conditions at two reefs (Dobu and Upa-Upasina) across three expeditions.
Figure 4: Influences of CO2, reef, date and substratum on dominant zooplankton taxa from emergence traps.

Similar content being viewed by others

References

  1. Broecker, W. S. & Clark, E. Glacial-to-Holocene redistribution of carbonate ion in the deep sea. Science 294, 2152–2155 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  4. Feely, R. A., Doney, S. C. & Cooley, S. R. Ocean acidification: present conditions and future changes in a high-CO2 world. Oceanography 22, 36–47 (2009).

    Article  Google Scholar 

  5. Richardson, A. J. In hot water: Zooplankton and climate change. ICES J. Mar. Sci. 65, 279–295 (2008).

    Article  Google Scholar 

  6. Longhurst, A. R. Role of the marine biosphere in the global carbon cycle. Limnol. Oceanogr. 36, 1507–1526 (1991).

    Article  CAS  Google Scholar 

  7. Bucklin, A. et al. in Life in the World’s Ocean (ed. McIntyre, A. D.) 247–265 (Blackwell Publishing, 2010).

    Book  Google Scholar 

  8. Comeau, S., Gorsky, G., Jeffree, R., Teyssie, J. L. & Gattuso, J.-P. Impact of ocean acidification on a key Arctic pelagic mollusc (Limacina helicina). Biogeosciences 6, 1877–1882 (2009).

    Article  CAS  Google Scholar 

  9. O’Donnell, M. J. et al. Ocean acidification alters skeletogenesis and gene expression in larval sea urchins. Mar. Ecol. Prog. Ser. 398, 157–171 (2009).

    Article  Google Scholar 

  10. Sheppard Brennand, H., Soars, N., Dworjanyn, S. A., Davis, A. R. & Byrne, M. Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS ONE 5, e11372 (2010).

    Article  Google Scholar 

  11. Kurihara, H. & Ishimatsu, A. Effects of high CO2 seawater on the copepod Acartia tsuensis through all life stages and subsequent generations. Mar. Pollut. Bull. 56, 1086–1090 (2008).

    Article  CAS  Google Scholar 

  12. Weydmann, A., Søreide, J. E., Kwasniewski, S. & Widdicombe, S. Influence of CO2-induced acidification on the reproduction of a key Arctic copepod. J. Exp. Mar. Biol. Ecol. 428, 39–42 (2012).

    Article  CAS  Google Scholar 

  13. McConville, K. et al. Effects of elevated CO2 on the reproduction of two calanoid copepods. Mar. Pollut. Bull. 73, 428–434 (2013).

    Article  CAS  Google Scholar 

  14. Hildebrandt, N., Niehoff, B. & Sartoris, F. J. Long-term effects of elevated CO2 and temperature on the Arctic calanoid copepods Calanus glacialis and C. hyperboreus. Mar. Pollut. Bull. 80, 59–70 (2014).

    Article  CAS  Google Scholar 

  15. Gaylord, B. et al. Ocean acidification through the lens of ecological theory. Ecology 96, 3–15 (2015).

    Article  Google Scholar 

  16. Hamner, W. M. & Carleton, J. H. Copepod swarms: attributes and role in coral reef ecosystems. Limnol. Oceanogr. 24, 1–14 (1979).

    Article  Google Scholar 

  17. Christou, E. D. & Verriopoulos, G. C. Analysis of the biological cycle of Acartia clausi (Copepoda) in a meso-oligotrophic coastal area of the eastern Mediterranean Sea using time-series analysis. Mar. Biol. 115, 643–651 (1993).

    Article  Google Scholar 

  18. González, J. G. Critical thermal maxima and upper lethal temperatures for the calanoid copepods Acartia tonsa and A. clausi. Mar. Biol. 27, 219–223 (1974).

    Article  Google Scholar 

  19. Cervetto, G., Gaudy, R. & Pagano, M. Influence of salinity on the distribution of Acartia tonsa (Copepoda, Calanoida). J. Exp. Mar. Biol. Ecol. 239, 33–45 (1999).

    Article  Google Scholar 

  20. Fabricius, K. E. et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Change 1, 165–169 (2011).

    Article  CAS  Google Scholar 

  21. Andersson, A. J. & Gledhill, D. Ocean acidification and coral reefs: Effects on breakdown, dissolution, and net ecosystem calcification. Annu. Rev. Mar. Sci. 5, 321–348 (2011).

    Article  Google Scholar 

  22. Enochs, I. C. et al. Shift from coral to macroalgae dominance on a volcanically acidified reef. Nat. Clim. Change 5, 1–9 (2015).

    Article  Google Scholar 

  23. Alldredge, A. L. & King, J. M. Distribution, abundance, and substrate preferences of demersal reef zooplankton at Lizard Island Lagoon, Great Barrier Reef. Mar. Biol. 41, 317–333 (1977).

    Article  Google Scholar 

  24. Carleton, J. H. Zooplankton and coral reefs: an overview. South Pacific Underw. Med. Soc. 23, 102–107 (1993).

    Google Scholar 

  25. Fabricius, K. E., Kluibenschedl, A., Harrington, L., Noonan, S. & De’ath, G. In situ changes of tropical crustose coralline algae along carbon dioxide gradients. Sci. Rep. 5, 9537 (2015).

    Article  CAS  Google Scholar 

  26. Kurihara, H., Shimode, S. & Shirayama, Y. Sub-lethal effects of elevated concentration of CO2 on planktonic copepods and sea urchins. J. Oceanogr. 60, 743–750 (2004).

    Article  CAS  Google Scholar 

  27. Isari, S., Zervoudaki, S., Saiz, E., Pelejero, C. & Peters, J. Copepod vital rates under CO2-induced acidification: a calanoid species and a cyclopoid species under short-term exposures. J. Plankton Res. 37, 912–922 (2015).

    Article  CAS  Google Scholar 

  28. Fabricius, K. E., De’ath, G., Noonan, S. & Uthicke, S. Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc. R. Soc. Lond. B 281, 20132479 (2014).

    Article  CAS  Google Scholar 

  29. Rossoll, D. et al. Ocean acidification-induced food quality deterioration constrains trophic transfer. PLoS ONE 7, 2–7 (2012).

    Article  Google Scholar 

  30. Johnson, V. R. Responses of marine benthic microalgae to elevated CO2 . Mar. Biol. 160, 1813–1824 (2013).

    Article  CAS  Google Scholar 

  31. 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).

    Article  CAS  Google Scholar 

  32. Kim, H., Spivack, A. J. & Menden-Deuer, S. pH alters the swimming behaviors of the raphidophyte Heterosigma akashiwo: implications for bloom formation in an acidified ocean. Harmful Algae 26, 1–11 (2013).

    Article  CAS  Google Scholar 

  33. Genin, A., Jaffe, J. S., Reef, R., Richter, C. & Franks, P. J. S. Swimming against the flow: a mechanism of zooplankton aggregation. Science 308, 860–862 (2005).

    Article  CAS  Google Scholar 

  34. Hamner, W. M., Jones, M. S., Carleton, J. H., Hauri, I. R. & Williams, D. M. Zooplankton, planktivorous fish, and water currents on a windward reef face: Great Barrier Reef, Australia. Bull. Mar. Sci. 42, 459–479 (1988).

    Google Scholar 

  35. Ferrier-Pagès, C., Hoogenboom, M. & Houlbrèque, F. Coral Reefs: An Ecosystem in Transition (Springer Science, 2011); http://dx.doi.org/10.1007/978-94-007-0114-4

    Google Scholar 

  36. Houlbrèque, F. & Ferrier-Pagès, C. Heterotrophy in tropical scleractinian corals. Biol. Rev. 84, 1–17 (2009).

    Article  Google Scholar 

  37. Edmunds, P. J. Zooplanktivory ameliorates the effects of ocean acidification on the reef coral Porites spp. Limnol. Oceanogr. 56, 2402–2410 (2011).

    Article  CAS  Google Scholar 

  38. Towle, E. K., Enochs, I. C. & Langdon, C. Threatened Caribbean coral is able to mitigate the adverse effects of ocean acidification on calcification by increasing feeding rate. PLoS ONE e0123394 (2015).

  39. Johannes, R. E. & Tepley, L. Examination of feeding of the reef coral Porites lobata in situ using time lapse photography. Proc. 2nd Coral Reef Symp. Vol. 19, 127–131 (The Great Barrier Reef Committee, 1974).

    Google Scholar 

  40. Wellington, G. M. An experimental analysis of the effects of light and zooplankton on coral zonation. Oecologia 52, 311–320 (1982).

    Article  Google Scholar 

  41. Palardy, J. E., Rodrigues, L. J. & Grottoli, A. G. The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. J. Exp. Mar. Bio. Ecol. 367, 180–188 (2008).

    Article  CAS  Google Scholar 

  42. Barnett, T. P. et al. Penetration of human-induced warming into the world’s oceans. Science 309, 284–287 (2005).

    Article  CAS  Google Scholar 

  43. Hays, G. C., Richardson, A. J. & Robinson, C. Climate change and marine plankton. Trends Ecol. Evol. 20, 337–344 (2005).

    Article  Google Scholar 

  44. Whitney, F. A., Freeland, H. J. & Robert, M. Persistently declining oxygen levels in the interior waters of the eastern subarctic Pacific. Prog. Oceanogr. 75, 179–199 (2007).

    Article  Google Scholar 

  45. Maas, A. E., Frazar, S. L., Outram, D. M., Seibel, B. A. & Wishner, K. F. Fine-scale vertical distribution of macroplankton and micronekton in the Eastern Tropical North Pacific in association with an oxygen minimum zone. J. Plankton Res. 36, 1557–1575 (2014).

    Article  Google Scholar 

  46. Roemmich, D. & McGowan, J. Climatic warming and the decline of zooplankton in the California current. Science 267, 1324 (1995).

    Article  CAS  Google Scholar 

  47. Kattner, G. & Fricke, H. S. G. Simple gas-liquid chromatographic method for the simultaneous determination of fatty acid and alcohols in wax esters of marine organisms. J. Chromatogr. A 361, 263–268 (1986).

    Article  CAS  Google Scholar 

  48. Hagen, W. in ICES Zooplankton Methodology Manual (eds Harris, R., Wiebe, P., Lenz, J., Skjoldal, H. & Huntley, M.) 113–119 (Academic, 2000).

    Google Scholar 

  49. Lewis, E. & Wallace, D. ORNL/CDIAC-105 Carbon Dioxide Information Analysis Center (US Department of Energy, 1998).

    Google Scholar 

  50. Dickson, A. G. & Millero, F. J. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res. 34, 1733–1743 (1987).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank crew members of the M/V Chertan for help in the field, in particular O. Daniel and R. Luke, along with other members of the Hamamas Team. We also thank the community of Upa-Upasina and Dobu Island for permission to study zooplankton in their reef. Additional thanks to S. Noonan from the Australian Institute of Marine Science for logistical support, and H. Auel and P. Wencke from Bremen University for laboratory help and advice for the biochemical analysis. This project was funded in part by the Erasmus Mundus funded joint doctoral programme MARES (FPA 2011-0016), the Great Barrier Reef Foundation’s ‘Resilient Coral Reefs Successfully Adapting to Climate Change’ programme in collaboration with the Australian Government, the BIOACID Phase II Programme of the German Science Ministry BMBF (Grant 03F0655B), and the Australian Institute of Marine Science.

Author information

Authors and Affiliations

Authors

Contributions

J.N.S., K.E.F., C.R. and A.C. designed the experiment. J.N.S. and K.E.F. carried out the fieldwork. J.N.S. performed the laboratory work. G.D., J.N.S. and K.E.F. carried out the statistical analysis. All authors contributed to writing the manuscript.

Corresponding author

Correspondence to Joy N. Smith.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 267 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Smith, J., De’ath, G., Richter, C. et al. Ocean acidification reduces demersal zooplankton that reside in tropical coral reefs. Nature Clim Change 6, 1124–1129 (2016). https://doi.org/10.1038/nclimate3122

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate3122

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing