Ocean acidification can mediate biodiversity shifts by changing biogenic habitat

Abstract

The effects of ocean acidification (OA) on the structure and complexity of coastal marine biogenic habitat have been broadly overlooked. Here we explore how declining pH and carbonate saturation may affect the structural complexity of four major biogenic habitats. Our analyses predict that indirect effects driven by OA on habitat-forming organisms could lead to lower species diversity in coral reefs, mussel beds and some macroalgal habitats, but increases in seagrass and other macroalgal habitats. Available in situ data support the prediction of decreased biodiversity in coral reefs, but not the prediction of seagrass bed gains. Thus, OA-driven habitat loss may exacerbate the direct negative effects of OA on coastal biodiversity; however, we lack evidence of the predicted biodiversity increase in systems where habitat-forming species could benefit from acidification. Overall, a combination of direct effects and community-mediated indirect effects will drive changes in the extent and structural complexity of biogenic habitat, which will have important ecosystem effects.

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: Observed and predicted relationships between pH, habitat structure and community richness in four focal habitats, based on published data.
Figure 2: Changes in habitat density along spatial gradients from high to low pH regimes, showing cases where alternative habitat types were reported.
Figure 3: Conceptual model showing potential effects of OA on relative performance on competing habitat-forming organisms.

References

  1. 1

    Gattuso, J.-P. et al. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349, aac4722 (2015).

    Article  Google Scholar 

  2. 2

    Kroeker, K. J. et al. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19, 1884–1896 (2013).

    Article  Google Scholar 

  3. 3

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

    Article  Google Scholar 

  4. 4

    Falkenberg, L. J., Russell, B. D. & Connell, S. D. Contrasting resource limitations of marine primary producers: implications for competitive interactions under enriched CO2 and nutrient regimes. Oecologia 172, 575–583 (2013).

    Article  Google Scholar 

  5. 5

    Le Quesne, W. J. F. & Pinnegar, J. K. The potential impacts of ocean acidification: scaling from physiology to fisheries. Fish Fish. 13, 333–344 (2012).

    Article  Google Scholar 

  6. 6

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

    CAS  Article  Google Scholar 

  7. 7

    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 

  8. 8

    Kroeker, K. J. et al. Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability. Ecol. Lett. 19, 771–779 (2016).

    Article  Google Scholar 

  9. 9

    Thomsen, J., Casties, I., Pansch, C., Körtzinger, A. & Melzner, F. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments. Glob. Change Biol. 19, 1017–1027 (2013).

    Article  Google Scholar 

  10. 10

    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. Proc. R. Soc. B 368, 20120442 (2013).

    Google Scholar 

  11. 11

    Nagelkerken, I., Russell, B. D., Gillanders, B. M. & Connell, S. D. Ocean acidification alters fish populations indirectly through habitat modification. Nat. Clim. Change 6, 89–93 (2015).

    Article  Google Scholar 

  12. 12

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

    CAS  Article  Google Scholar 

  13. 13

    Ghedini, G., Russell, B. D. & Connell, S. D. Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of multiple disturbances. Ecol. Lett. 18, 182–187 (2015).

    Article  Google Scholar 

  14. 14

    Harley, C. D. G. Climate change, keystone predation, and biodiversity loss. Science 334, 1124–1127 (2011).

    CAS  Article  Google Scholar 

  15. 15

    Munday, P. L., Cheal, A. J., Dixson, D. L., Rummer, J. L. & Fabricius, K. E. Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps. Nat. Clim. Change 4, 487–492 (2014).

    CAS  Article  Google Scholar 

  16. 16

    Garrard, S. L. et al. Indirect effects may buffer negative responses of seagrass invertebrate communities to ocean acidification. J. Exp. Mar. Biol. Ecol. 461, 31–38 (2014).

    Article  Google Scholar 

  17. 17

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

    Article  Google Scholar 

  18. 18

    Vizzini, S. et al. Trace element bias in the use of CO2 vents as analogues for low pH environments: implications for contamination levels in acidified oceans. Estuar. Coast. Shelf Sci. 134, 19–30 (2013).

    CAS  Article  Google Scholar 

  19. 19

    Sunday, J. M. et al. Evolution in an acidifying ocean. Trends Ecol. Evol. 29, 117–125 (2014).

    Article  Google Scholar 

  20. 20

    Harley, C. D. G. et al. The impacts of climate change in coastal marine systems: Climate change in coastal marine systems. Ecol. Lett. 9, 228–241 (2006).

    Article  Google Scholar 

  21. 21

    Dustan, P., Doherty, O. & Pardede, S. Digital reef rugosity estimates coral reef habitat complexity. PLoS ONE 8, e57386 (2013).

    CAS  Article  Google Scholar 

  22. 22

    Graham, N. A. J. et al. Dynamic fragility of oceanic coral reef ecosystems. Proc. Natl Acad. Sci. USA 103, 8425–8429 (2006).

    CAS  Article  Google Scholar 

  23. 23

    Gratwicke, B. & Speight, M. R. The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. J. Fish Biol. 66, 650–667 (2005).

    Article  Google Scholar 

  24. 24

    Jones, G. P., McCormick, M. I., Srinivasan, M. & Eagle, J. V. Coral decline threatens fish biodiversity in marine reserves. Proc. Natl Acad. Sci. USA 101, 8251–8253 (2004).

    CAS  Article  Google Scholar 

  25. 25

    Sadchatheeswaran, S., Branch, G. M. & Robinson, T. B. Changes in habitat complexity resulting from sequential invasions of a rocky shore: implications for community structure. Biol. Invasions 17, 1799–1816 (2015).

    Article  Google Scholar 

  26. 26

    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 

  27. 27

    Russell, B. D. et al. Future seagrass beds: can increased productivity lead to increased carbon storage? Mar. Pollut. Bull. 73, 463–469 (2013).

    CAS  Article  Google Scholar 

  28. 28

    Attrill, M., Strong, J. A. & Rowden, A. Are macroinvertebrate communities influenced by seagrass structural complexity? Ecography 23, 114–121 (2000).

    Article  Google Scholar 

  29. 29

    Heck, K. L. & Wetstone, G. S. Habitat complexity and invertebrate species richness and abundance in tropical seagrass meadows. 4, 135–142 (1977).

  30. 30

    Stoner, A. W. & Lewis, F. G. The influence of quantitative and qualitative aspects of habitat complexity in tropical sea-grass meadows. J. Exp. Mar. Biol. Ecol. 94, 19–40 (1985).

    Article  Google Scholar 

  31. 31

    Enochs, I. C. et al. Shift from coral to macroalgae dominance on a volcanically acidified reef. Nat. Clim. Change 5, 1083–1088 (2015).

    CAS  Article  Google Scholar 

  32. 32

    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 

  33. 33

    Linares, C. et al. Persistent natural acidification drives major distribution shifts in marine benthic ecosystems. Proc. R. Soc. B 282, 20150587 (2015).

    CAS  Article  Google Scholar 

  34. 34

    Burnaford, J. L. Evaluating the Relative Roles of Positive and Negative Interactions in Communities: Shade, Herbivory and Physiological Stress in the Rocky Intertidal Zone PhD thesis, Oregon State Univ. (2002).

  35. 35

    Lilley, S. A. & Schiel, D. R. Community effects following the deletion of a habitat-forming alga from rocky marine shores. Oecologia 148, 672–681 (2006).

    Article  Google Scholar 

  36. 36

    Torres, A. C., Veiga, P., Rubal, M. & Sousa-Pinto, I. The role of annual macroalgal morphology in driving its epifaunal assemblages. J. Exp. Mar. Biol. Ecol. 464, 96–106 (2015).

    Article  Google Scholar 

  37. 37

    Watt, C. A. & Scrosati, R. A. Bioengineer effects on understory species richness, diversity, and composition change along an environmental stress gradient: experimental and mensurative evidence. Estuar. Coast. Shelf Sci. 123, 10–18 (2013).

    Article  Google Scholar 

  38. 38

    Willis, T. J. & Anderson, M. J. Structure of cryptic reef fish assemblages: relationships with habitat characteristics and predator density. Mar. Ecol. Prog. Ser. 257, 209–221 (2003).

    Article  Google Scholar 

  39. 39

    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 

  40. 40

    Kelaher, B. P. Changes in habitat complexity negatively affect diverse gastropod assemblages in coralline algal turf. Oecologia 135, 431–441 (2003).

    CAS  Article  Google Scholar 

  41. 41

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

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This article emerged from a working group funded by the Peter Wall Institute for Advanced Studies. We are grateful to R. Bechmann for helpful discussions, and thank the US National Science Foundation, the National Science and Engineering Research Council of Canada, and several of our institutions for research support.

Author information

Affiliations

Authors

Contributions

All authors conceptualized and designed the paper; J.M.S., K.E.F., K.J.K., K.M.A., N.E.B., J.M.H.-S., M.M. and C.D.G.H. assembled the data; J.M.S. analysed the data, produced figures and drafted the paper; all authors contributed discussion, writing and interpretation.

Corresponding author

Correspondence to Jennifer M. Sunday.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 336 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sunday, J., Fabricius, K., Kroeker, K. et al. Ocean acidification can mediate biodiversity shifts by changing biogenic habitat. Nature Clim Change 7, 81–85 (2017). https://doi.org/10.1038/nclimate3161

Download citation

Further reading