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

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.

Environmental controls on coccolithophore calcification

“…At the level of the organism, modelling by Irie et al (2010) suggested that an increase in coccolith mass (as reported by several but not all investigators: see above and Fukuda et al 2011, Krug et al 2011, Langer 2011, Richier et al 2011) was, counter-intuitively, the optimal evolutionary response to decreasing ocean CO 3 2− . It must be emphasised that this conclusion rests on the untested assumption that increased mass decreases mortality.…”

High levels of solar radiation offset impacts of ocean acidification on calcifying and non-calcifying strains of Emiliania huxleyi

“…Elevated CO 2 increases the costs of calcification (Irie et al 2010, Raven 2011, Raven & Crawfurd 2012, thereby lowering available energy and reducing calcification at low light levels.…”

“…The decreased calcification rate under OA is partially caused by increasing energy costs of calcification (Irie et al 2010, Raven 2011, Raven & Crawfurd 2012, which is required to sustain a sufficient supply of CO 3 2− in the coccolith-forming vesicle, and net H + efflux (Raven 2011). Therefore, based on the documented knowledge on the effects of OA and/or light intensity on E. huxleyi, we hypothesize that increased levels of supplied energy with high levels of solar radiation may offset the negative effects of OA on calcification of E. huxleyi.…”

The biological pump in a high CO<sub>2 world

“…Ocean acidification makes calcification more difficult, but increased pCO 2 appears to facilitate primary production for this group with variable outcome for the growth success of the species (Zondervan 2007, Iglesias-Rodriguez et al 2008, Bach et al 2011). Inclusion of other factors for an evaluation of the competitiveness of coccolithophores in the future ocean (Irie et al 2010, Xu et al 2011 makes predictions even less robust at present. The degree of water column stability exerts an additional strong selective pressure on phytoplankton composition (Falkowski & Oliver 2007).…”