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 CaCO(3) 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 CO(2) concentration.

Figure 1. Partial cross section of a coccolithophore with coccolith layer.

Figure 2. Carbonate system in seawater.

Equilibrial concentrations of HCO³⁻, CO₃ ²⁻, and H⁺ in response to increasing aqueous CO₂ concentration. Parameter values are set at salinity S = 35, temperature T = 25°C, and pressure P = 1 atm according to Zeebe and Wolf-Gladrow : total dissolved inorganic carbon (DIC) = 2.1 mmol/kg, stoichiometric equilibrium constants K ₁* = [HCO³⁻][H⁺]/[CO₂] = 10^−5.86 and K ₂* = [CO₃ ²⁻][H⁺]/[HCO³⁻] = 10^−8.92. The CaCO₃ saturation state of seawater, Ω, is lower than 1 in the shaded region, in which CO₃ ²⁻ concentration in seawater is assumed to be 41.6 µmol/kg (see [49]).

Figure 3. Relationships between the acidification-sensitive parameters, morphological variables, and life history variables.

Arrows with solid lines indicate positive relationships and arrows with dotted lines indicate negative ones. Numbers in parentheses correspond to the equation numbers in the main text.

Figure 4. Dependence of optimal generation time on defense efficiency exponent (q).

Based on the optimal proportion coefficient (δ*) calculated by numerically solving αδ^β+akδ−a(1−k)/s = 0 (see Appendix S2 equation [B3-2]), univariate static optimization was conducted by numerically choosing T that maximizes at different q-values (i.e., 1−k≤q≤2(1−k)). Parameter values: a = 1.0, s = 1.0, α = 0.0001, P = 0.2, k = β = 2/3.

Figure 5. Optimal coccolith size as a function of dissolution factor (α) and dissolution exponent (β).

(A) A contour plot of C(T)* in a wider range of β. (B) Detailed relationships between α and C(T)* with βs close to 1. Common parameters: a = 0.1, s = 0.001, P = 1.0, k = q = 2/3.

Figure 6. Environmental dependence of the total CaCO₃ precipitated during a bloom of evolutionarily optimized coccolithophores.

The population-wise carbon fixation (W) is given as the sum of the CaCO₃ left during the bloom (W ₁) and the CaCO₃ carried over until the end of the bloom (W ₂). (A) Both W ₁ (solid line) and W ₂ (dashed line) decrease and then increase with increasing net production coefficient (a) with s = 0.001. (B) Both W ₁ (solid line) and W ₂ (dashed line) depend on calcification cost (s) with L-shaped convex curves with a = 1.0. Common parameters: k = β = 2/3, q = 2 (1−k), α = 0, P = 1.0, N ₀ = 1.0, τ = 1.0. These figures assume the situation in which seawater remains oversaturated in CaCO₃ (i.e., α = 0). Parameter dependencies in CaCO₃-undersaturated seawater (i.e., α>0) are given in Figures S4 and S5.