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Physiological advantages of dwarfing in surviving extinctions in high-CO2 oceans

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Abstract

Excessive CO2 in the present-day ocean–atmosphere system is causing ocean acidification, and is likely to cause a severe biodiversity decline in the future1, mirroring effects in many past mass extinctions2,3,4. Fossil records demonstrate that organisms surviving such events were often smaller than those before5,6, a phenomenon called the Lilliput effect7. Here, we show that two gastropod species adapted to acidified seawater at shallow-water CO2 seeps were smaller than those found in normal pH conditions and had higher mass-specific energy consumption but significantly lower whole-animal metabolic energy demand. These physiological changes allowed the animals to maintain calcification and to partially repair shell dissolution. These observations of the long-term chronic effects of increased CO2 levels forewarn of changes we can expect in marine ecosystems as CO2 emissions continue to rise unchecked, and support the hypothesis that ocean acidification contributed to past extinction events. The ability to adapt through dwarfing can confer physiological advantages as the rate of CO2 emissions continues to increase.

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Figure 1: Shells of the investigated species.
Figure 2: Shell dissolution, apical truncation and repairing calcification process in Nassarius corniculus living at CO2 seeps.
Figure 3: Gross calcification and metabolic oxygen consumption in N. corniculus and C. neritea across normal and acidified sites.

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Acknowledgements

We thank F. Houlbreque, J-F. Comanducci and F. Oberhänsli for their help during radiotracer experiments. We also thank H. Graham, D. Small and C. Bertolini for assisting in the field. The International Atomic Energy Agency is grateful to the Government of the Principality of Monaco for the support provided to its Environment Laboratories. This work contributes to the EU ‘Mediterranean Sea acidification under a changing climate’ project (MedSeA; grant agreement 265103) and the NERC UK Ocean Acidification Research Programme (Grant no. NE/H02543X/1). S.P.S.R. was funded by a NERC UK Ocean Acidification Research Programme AVA fellowship. This is UMR ENTROPIE scientific contribution n. 028.

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V.G. and R.R-M. designed the study and wrote the paper in collaboration with M.M., A.F., R.J.T., S.P.S.R. and J.M.H-S.; V.G. and D.P. performed scanning electronic microscopy analyses; R.R-M. performed gastropod radiotracer incorporation; S.P.S.R. and M.M. performed metabolic rate experiments; A.F. performed statistical analysis; M.M., D.S. and L.B. helped during sampling. J.M.H-S. conceived the overall seep project. All authors read and commented on the manuscript.

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Correspondence to Vittorio Garilli or Riccardo Rodolfo-Metalpa.

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The authors declare no competing financial interests.

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Garilli, V., Rodolfo-Metalpa, R., Scuderi, D. et al. Physiological advantages of dwarfing in surviving extinctions in high-CO2 oceans. Nature Clim Change 5, 678–682 (2015). https://doi.org/10.1038/nclimate2616

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