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Shift from coral to macroalgae dominance on a volcanically acidified reef


Rising anthropogenic CO2 in the atmosphere is accompanied by an increase in oceanic CO2 and a concomitant decline in seawater pH (ref. 1). This phenomenon, known as ocean acidification (OA), has been experimentally shown to impact the biology and ecology of numerous animals and plants2, most notably those that precipitate calcium carbonate skeletons, such as reef-building corals3. Volcanically acidified water at Maug, Commonwealth of the Northern Mariana Islands (CNMI) is equivalent to near-future predictions for what coral reef ecosystems will experience worldwide due to OA. We provide the first chemical and ecological assessment of this unique site and show that acidification-related stress significantly influences the abundance and diversity of coral reef taxa, leading to the often-predicted shift from a coral to an algae-dominated state4,5. This study provides field evidence that acidification can lead to macroalgae dominance on reefs.

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Figure 1: Map showing the location of the study site at Maug.
Figure 2: Spatial extent of the acidified vent plume and location of sites as determined by interpolation of single-point bottle sample data (n = 33).
Figure 3: High-resolution photomosaic imagery of benthic cover at high- p CO 2 , mid- p CO 2 and control sites, showing the progression from coral-dominated to algae-dominated systems.
Figure 4: The influence of vent proximity on the cover of coral reef taxa.


  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

    Fabry, V. J., Seibel, B. A., Feely, R. A. & James, O. C. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 65, 414–432 (2008).

    CAS  Article  Google Scholar 

  3. 3

    Langdon, C. & Atkinson, M. Effect of elevated p CO 2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J. Geophys. Res. 110, C09S07 (2005).

    Google Scholar 

  4. 4

    Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).

    CAS  Article  Google Scholar 

  5. 5

    Connell, S. D., Kroeker, K. J., Fabricius, K. E., Kline, D. I. & Russell, B. D. The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Phil. Trans. R. Soc. B 368, 20120442 (2013).

    Article  Google Scholar 

  6. 6

    Reaka-Kudla, M. L. in Biodiversity II (eds Reaka-Kudla, M. L., Wilson, D. E. & Wilson, E. O.) Ch. 7, 83–108 (Joseph Henry Press, 1997).

    Google Scholar 

  7. 7

    Moberg, F. & Folke, C. Ecolgoical goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233 (1999).

    Article  Google Scholar 

  8. 8

    Enochs, I. C. et al. Ocean acidification enhances the bioerosion of a common coral reef sponge: Implications for the persistence of the Florida Reef Tract. Bull. Mar. Sci. 91, 271–291 (2015).

    Article  Google Scholar 

  9. 9

    Eyre, B. D., Andersson, A. J. & Cyronak, T. Benthic coral reef calcium carbonate dissolution in an acidifying ocean. Nature Clim. Change 4, 969–976 (2014).

    CAS  Article  Google Scholar 

  10. 10

    Johnson, M. D., Price, N. N. & Smith, J. E. Contrasting effects of ocean acidification on tropical fleshy and calcareous algae. PeerJ 2, e411 (2014).

    Article  Google Scholar 

  11. 11

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

    Article  Google Scholar 

  12. 12

    Kroeker, K. J., Micheli, F. & Gambi, M. C. Ocean acidification causes ecosystem shifts via altered competitive interactions. Nature Clim. Change 3, 156–159 (2012).

    Article  Google Scholar 

  13. 13

    Jokiel, P. L. et al. Ocean acidification and calcifying reef organisms: A mesocosm investigation. Coral Reefs 27, 473–483 (2008).

    Article  Google Scholar 

  14. 14

    Shaw, E. C., McNeil, B. I. & Tilbrook, B. Impacts of ocean acidification in naturally variable coral reef flat ecosystems. J. Geophys. Res. 117, C03038 (2012).

    Article  Google Scholar 

  15. 15

    Manzello, D. P. et al. Galápagos coral reef persistence after ENSO warming across an acidification gradient. Geophys. Res. Lett. 41, 9001–9008 (2015).

    Article  Google Scholar 

  16. 16

    Crook, E. D., Cohen, A. L., Rebolledo-Vieyra, M., Hernandez, L. & Paytan, A. Reduced calcification and lack of acclimatization by coral colonies growing in areas of persistent natural acidification. Proc. Natl Acad. Sci. USA 110, 11044–11049 (2013).

    CAS  Article  Google Scholar 

  17. 17

    Shamberger, K. E. F. et al. Diverse coral communities in naturally acidified waters of a Western Pacific reef. Geophys. Res. Lett. 41, 499–504 (2014).

    Article  Google Scholar 

  18. 18

    Martin, S. et al. Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol. Lett. 4, 689–692 (2008).

    Article  Google Scholar 

  19. 19

    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 

  20. 20

    Kroeker, K. J., Gambi, M. C. & Micheli, F. Community dynamics and ecosystem simplification in a high-CO2 ocean. Proc. Natl Acad. Sci. USA 110, 12721–12726 (2013).

    CAS  Article  Google Scholar 

  21. 21

    Kerfahi, D. et al. Shallow water marine sediment bacterial community shifts along a natural CO2 gradient in the Mediterranean Sea off Vulcano, Italy. Microb. Ecol. 67, 819–828 (2014).

    CAS  Article  Google Scholar 

  22. 22

    Milazzo, M. et al. Ocean acidification impairs vermetid reef recruitment. Sci. Rep. 4, 1–7 (2014).

    Google Scholar 

  23. 23

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

    CAS  Article  Google Scholar 

  24. 24

    Inoue, S., Kayanne, H., Yamamoto, S. & Kurihara, H. Spatial community shift from hard to soft corals in acidified water. Nature Clim. Change 3, 683–687 (2013).

    CAS  Article  Google Scholar 

  25. 25

    Marubini, F., Barnett, H., Langdon, C. & Atkinson, M. J. Dependence of calcification on light and carbonate ion concentration for the hermatypic coral Porites compressa. Mar. Ecol. Prog. Ser. 220, 153–162 (2001).

    CAS  Article  Google Scholar 

  26. 26

    Baker, A. C., Glynn, P. W. & Riegl, B. Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuar. Coast. Shelf Sci. 80, 435–471 (2008).

    Article  Google Scholar 

  27. 27

    Hurd, C. L. Water motion, marine macroalgal physiology, and production. J. Phycol. 36, 453–472 (2000).

    CAS  Article  Google Scholar 

  28. 28

    Iguchi, A. et al. Effects of acidified seawater on coral calcification and symbiotic algae on the massive coral Porites australiensis. Mar. Environ. Res. 73, 32–36 (2012).

    CAS  Article  Google Scholar 

  29. 29

    van Woesik, R., Sakai, K., Ganase, A. & Loya, Y. Revisiting the winners and the losers a decade after coral bleaching. Mar. Ecol. Prog. Ser. 434, 67–76 (2011).

    Article  Google Scholar 

  30. 30

    Johnson, V. R., Russell, B. D., Fabricius, K. E., Brownlee, C. & Hall-Spencer, J. M. Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients. Glob. Change Biol. 18, 2792–2803 (2012).

    Article  Google Scholar 

  31. 31

    McCook, L. J. Macroalgae, nutrients and phase shifts on coral reefs scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18, 357–367 (1999).

    Article  Google Scholar 

  32. 32

    Albright, R., Mason, B., Miller, M. & Langdon, C. Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc. Natl Acad. Sci. USA 107, 20400–20404 (2010).

    CAS  Article  Google Scholar 

  33. 33

    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 

  34. 34

    Sasaki, H., Kataoka, H., Murakami, A. & Kawai, H. Inorganic ion compositions in brown algae, with special reference to sulfuric acid ion accumulations. Hydrobiologia 512, 255–262 (2004).

    CAS  Article  Google Scholar 

  35. 35

    Disalvo, L. H., Randall, J. E. & Cea, A. Stomach contents and feeding observations of some Easter Island fishes. Atoll Res. Bull. 548, 1–22 (2007).

    Article  Google Scholar 

  36. 36

    Program developed for CO2 system calculations (ORNL/CDIAC, 1998)

  37. 37

    Mehrbach, C., Culberson, C. H., Hawley, J. E. & Pytkowicz, R. M. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol. Oceanogr. 18, 897–907 (1973).

    CAS  Article  Google Scholar 

  38. 38

    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).

    CAS  Article  Google Scholar 

  39. 39

    Dickson, A. G. Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K. Deep-Sea Res. 37, 755–766 (1990).

    CAS  Article  Google Scholar 

  40. 40

    Manzello, D. et al. Remote monitoring of chlorophyll fluorescence in two reef corals during the 2005 bleaching event at Lee Stocking Island, Bahamas. Coral Reefs 28, 209–214 (2009).

    Article  Google Scholar 

  41. 41

    Gintert, B. et al. in Proc. 11th Int Coral Reef Symp. 577–581 (Nova Southeastern Univ., 2008).

    Google Scholar 

  42. 42

    Kohler, K. E. & Gill, S. M. Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comp. Geosci. 32, 1259–1269 (2006).

    Article  Google Scholar 

  43. 43

    Newcombe, R. G. Two-sided confidence intervals for the single proportion: Comparison of seven methods. Stat. Med. 17, 857–872 (1998).

    CAS  Article  Google Scholar 

  44. 44

    Helmle, K., Kohler, K. & Dodge, R. The Coral X-Radiograph Densitometry System: Coral XDS (Nova Southeastern Univ., 2015);

    Google Scholar 

  45. 45

    Sokal, R. R. & Rohlf, F. J. Biometry (WH Freeman, 1981).

    Google Scholar 

  46. 46

    IBM SPSS Statistics for Windows (2013);

  47. 47

    GraphPad Prism (2012);

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Funding was provided by NOAA’s CRCP and OAP. We are grateful for the support and guidance of F. Rabauliman and F. Castro at BECQ/DCRM, M. Pangelinan and T. Miller at DFW, as well as J. Morgan, J. Tomczuk and D. Okano at NOAA. The crews of the Hi’Ialakai and Super Emerald provided logistic support. F. Forrestal and T. Dearg provided assistance with developing the manuscript.

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I.C.E., D.P.M., E.M.D., G.K., R.O., L.J., C.Y., J.I., S.J., D.B., R.C. and N.N.P. assisted in study design and project planning. I.C.E., E.M.D., G.K., R.O., L.J., C.Y., J.I., C.B.E., M.D.F., S.J., D.B. and S.J.C. collected the data presented herein. I.C.E., D.P.M., E.M.D., G.K., R.O., L.J., J.I., C.B.E., M.D.F., L.V., S.J., D.B., S.J.C., R.C., T.B., Y.E. and N.N.P. worked on data analysis. I.C.E., D.P.M., E.M.D., G.K., R.O., L.J., C.Y., C.B.E., M.D.F., L.V. and N.N.P. contributed to manuscript preparation.

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Correspondence to I. C. Enochs.

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Enochs, I., Manzello, D., Donham, E. et al. Shift from coral to macroalgae dominance on a volcanically acidified reef. Nature Clim Change 5, 1083–1088 (2015).

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