Increasing Costs Due to Ocean Acidification Drives Phytoplankton to Be More Heavily Calcified: Optimal Growth Strategy of Coccolithophores

Takahiro Irie,Helen S Findlay,Piero Calosi,Kazuhiro Bessho,Zoe Finkel

doi:10.1371/journal.pone.0013436

Takahiro Irie, Helen S Findlay + Show 3 more

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https://doi.org/10.1371/journal.pone.0013436

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Abstract

Ocean acidification is potentially one of the greatest threats to marine ecosystems and global carbon cycling. Amongst calcifying organisms, coccolithophores have received special attention because their calcite precipitation plays a significant role in alkalinity flux to the deep ocean (i.e., inorganic carbon pump). Currently, empirical effort is devoted to evaluating the plastic responses to acidification, but evolutionary considerations are missing from this approach. We thus constructed an optimality model to evaluate the evolutionary response of coccolithophorid life history, assuming that their exoskeleton (coccolith) serves to reduce the instantaneous mortality rates. Our model predicted that natural selection favors constructing more heavily calcified exoskeleton in response to increased acidification-driven costs. This counter-intuitive response occurs because the fitness benefit of choosing a better-defended, slower growth strategy in more acidic conditions, outweighs that of accelerating the cell cycle, as this occurs by producing less calcified exoskeleton. Contrary to the widely held belief, the evolutionarily optimized population can precipitate larger amounts of CaCO3 during the bloom in more acidified seawater, depending on parameter values. These findings suggest that ocean acidification may enhance the calcification rates of marine organisms as an adaptive response, possibly accompanied by higher carbon fixation ability. Our theory also provides a compelling explanation for the multispecific fossil time-series record from ∼200 years ago to present, in which mean coccolith size has increased along with rising atmospheric CO2 concentration.

Highlights

Scientists predict that increasing atmospheric CO2 partial pressure, elevated by anthropogenic emissions of CO2, causes an increase in aqueous CO2 [CO2(aq)] and hydrogen ion concentrations [H+] in seawater, and a decrease in carbonate ion concentration [CO322]
We provide a theoretical model on the growth schedule of coccolith-bearing coccolithophores in the asexual reproduction phase, aiming to predict how natural selection alters their phenotypes as ocean acidification progresses and to evaluate the resultant change in carbon fixation ability
The most important finding from our calculation is that natural selection favors having more heavily calcified exoskeleton in response to increased acidification-driven costs in bloom-forming coccolithophores

Summary

Introduction

Scientists predict that increasing atmospheric CO2 partial pressure (pCO2), elevated by anthropogenic emissions of CO2, causes an increase in aqueous CO2 [CO2(aq)] and hydrogen ion concentrations [H+] in seawater, and a decrease in carbonate ion concentration [CO322] (this effect has been termed ocean acidification [1]). The carbonate undersaturation expected to arise from continued ocean acidification is considered to reduce precipitation of calcium carbonate in marine organisms that build calcareous exoskeletons [2]. Negative effects on higher-level ecological processes are possibly buffered by phenotypic plasticity [25], which has evolved as (pre)adaptation to existing spatial and/or temporal heterogeneities of environmental conditions. If this adaptation is possible, the effect of ocean acidification should first appear in morphological/life-history traits prior to the local extinctions and distribution change in the focal species

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