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.2010 Oct 15;5(10):e13436.
doi: 10.1371/journal.pone.0013436.

Increasing costs due to ocean acidification drives phytoplankton to be more heavily calcified: optimal growth strategy of coccolithophores

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Increasing costs due to ocean acidification drives phytoplankton to be more heavily calcified: optimal growth strategy of coccolithophores

Takahiro Irie et al. PLoS One..

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.

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Conflict of interest statement

Competing Interests:The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Partial cross section of a coccolithophore with coccolith layer.
Figure 2
Figure 2. Carbonate system in seawater.
Equilibrial concentrations of HCO3−, CO32−, and H+ in response to increasing aqueous CO2 concentration. Parameter values are set at salinityS = 35, temperatureT = 25°C, and pressureP = 1 atm according to Zeebe and Wolf-Gladrow : total dissolved inorganic carbon (DIC) = 2.1 mmol/kg, stoichiometric equilibrium constantsK1* = [HCO3−][H+]/[CO2] = 10−5.86 andK2* = [CO32−][H+]/[HCO3−] = 10−8.92. The CaCO3 saturation state of seawater, Ω, is lower than 1 in the shaded region, in which CO32− concentration in seawater is assumed to be 41.6 µmol/kg (see [49]).
Figure 3
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
Figure 4. Dependence of optimal generation time on defense efficiency exponent (q).
Based on the optimal proportion coefficient (δ*) calculated by numerically solving αδβ+akδ−a(1−k)/s = 0 (see Appendix S2 equation [B3-2]), univariate static optimization was conducted by numerically choosingT that maximizesformula image at differentq-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
Figure 5. Optimal coccolith size as a function of dissolution factor (α) and dissolution exponent (β).
(A) A contour plot ofC(T)* in a wider range of β. (B) Detailed relationships between α andC(T)* with βs close to 1. Common parameters:a = 0.1,s = 0.001,P = 1.0,k = q = 2/3.
Figure 6
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 (W1) and the CaCO3 carried over until the end of the bloom (W2). (A) BothW1 (solid line) andW2 (dashed line) decrease and then increase with increasing net production coefficient (a) withs = 0.001. (B) BothW1 (solid line) andW2 (dashed line) depend on calcification cost (s) with L-shaped convex curves witha = 1.0. Common parameters:k = β = 2/3,q = 2 (1−k), α = 0,P = 1.0,N0 = 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.
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