Mid Pleistocene foraminiferal mass extinction coupled with phytoplankton evolution

Understanding the interaction between climate and biotic evolution is crucial for deciphering the sensitivity of life. An enigmatic mass extinction occurred in the deep oceans during the Mid Pleistocene, with a loss of over 100 species (20%) of sea floor calcareous foraminifera. An evolutionarily conservative group, benthic foraminifera often comprise >50% of eukaryote biomass on the deep-ocean floor. Here we test extinction hypotheses (temperature, corrosiveness and productivity) in the Tasman Sea, using geochemistry and micropalaeontology, and find evidence from several globally distributed sites that the extinction was caused by a change in phytoplankton food source. Coccolithophore evolution may have enhanced the seasonal ‘bloom’ nature of primary productivity and fundamentally shifted it towards a more intra-annually variable state at ∼0.8 Ma. Our results highlight intra-annual variability as a potential new consideration for Mid Pleistocene global biogeochemical climate models, and imply that deep-sea biota may be sensitive to future changes in productivity

Experimental set-up.

<p>For each treatment (in triplicate; T = 18.9±0.1°C), the target A_T (total alkalinity in µmol kg⁻¹), pH_T and Ω_a (saturation state of the seawater with respect to aragonite) are indicated. pH_T was controlled by bubbling ambient or high-CO₂ air. A_T was decreased in T4 by HCl addition and increased in T5 by NaHCO₃ addition. In T4, calcium concentrations have been increased above ambient levels by CaCl₂ addition. See text for more details.</p

Larval developmental parameters at the end of the incubation period in the five treatments (72 h; T1 to T5).

<p>Proportion of embryos that developed to viable D-veliger (±SD; upper left plot), average shell area and length of D-veliger larvae (±SD; upper right and lower left plot, respectively) as well as the amount of calcium incorporated (±SE; lower right plot) are shown. Different letters on bars indicate significant differences in the median values (Kruskal-Wallis and post-hoc Dunn's multiple comparison tests, p<0.05).</p

Relationships between larval developmental parameters and conditions of the carbonate chemistry in the five treatments.

<p>Relationships between the average (±SD) shell length and area of D-veliger larvae as well as the amount of calcium incorporated at the end of the 72 h incubation period, and the average (±SD) conditions of the carbonate chemistry in the five treatments are shown; pH_T: pH on the total scale (left plots), Ω_a: saturation state with respect to aragonite (middle plots) and [CO₃²⁻]: carbonate ion concentration (right plots). On the right plots, the dotted lines refer to the carbonate ion concentration at the aragonite saturation level (see text for details).</p

Environmental parameters and carbonate chemistry for the five different treatments during the course of the experiment (mean ± SD).

<p>The partial pressure of CO₂ (pCO₂), dissolved inorganic carbon concentration (<i>C</i>_T) as well as the saturation state of seawater with respect to aragonite and calcite (Ω_a and Ω_c respectively) were computed from pH_T and total alkalinity (<i>A</i>_T).</p><p>*: Ω_a and Ω_c were increased by addition of calcium (CaCl₂-2H₂O; ×2.6 <i>in situ</i> Ca²⁺ concentrations).</p

Proteins (Homolgous Protein Groups) down-regulated in <i>Emilania huxleyi</i> NZEH under high CO₂.

a<p>Identifications are associated with either UniProtKB accession, <i>Emiliania huxleyi</i> genome protein ID or BUDAPEST consensus sequence. Further information can be found in <b><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0061868#pone.0061868.s002" target="_blank">Data S2</a>;</b> BUDAPEST sequence files can be found in <b><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0061868#pone.0061868.s001" target="_blank">Data S1</a></b>.</p>b<p>Ratio of protein identified between the two CO₂ treatments for each replicate incubation, whereby 114∶113 is the first replicate, 116∶115 is the second and 118∶117 the third. Reporter ions 114, 116 and 118 were applied to peptides extracted from the high CO₂ treatments and 113, 115, 117 to the current day treatment.</p>c<p>“Range” (<i>G</i>−<i>CI</i>)–(<i>G</i>+<i>CI</i>) as defined in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0061868#s2" target="_blank">Materials and Methods</a>.</p

Example of coccoliths derived at the end of the experiment (<i>t2</i>).

<p>Panel A: typical coccoliths from 395 p.p.m.v. CO₂ treatment; B: coccoliths from the lower pH (∼7.6) and 1340 p.p.m.v. CO₂ treatment which are typically larger and are slighly less calcified but possess no signs of dissolution or malformation.</p

Morphometric analysis of detached coccoliths obtained at the end of the experiment (<i>t2</i>) from monoclonal cultures of <i>Emiliania huxleyi</i> NZEH bubbled with 395 and 1340 p.p.m.v. CO_2.

<p>Morphometric analysis of detached coccoliths obtained at the end of the experiment (<i>t2</i>) from monoclonal cultures of <i>Emiliania huxleyi</i> NZEH bubbled with 395 and 1340 p.p.m.v. CO_2.</p

Physiological parameters of <i>Emiliania huxleyi</i> NZEH grown under 395 and 1340 p.p.m.v. CO₂ at <i>t1</i> and <i>2</i>.

*, **, ***<p>Significant results from t-tests comparing results from different <i>p</i>CO₂ treatments at the same time point (i.e. 395 v 1340 p.p.m.v. CO₂ at <i>t1</i>; 395 v. 1340 p.p.m.v. CO₂ at <i>t2</i>) are designated as follows: ^* p≤0.05; ^** p≤0.01; ^*** p≤0.001.</p>a, b,<p>Significant results from t-tests comparing results from the same <i>p</i>CO₂ treatment at different time points (e.g. 395 <i>t1</i> v 395 p.p.m.v. CO₂<i>t2</i>) are defined according to: ^a p≤0.05; ^b p≤0.01.</p

Comparison of <i>Emiliania huxleyi</i> NZEH coccosphere sizes at 395 and 1340 p.p.m.v. CO₂.

<p>* p≤0.05; ** p≤0.01; *** p≤0.001. A point with no star indicates differences were non-significant. Arrows indicate inoculations into media with different <i>p</i>CO₂ conditions, as outlined in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0061868#s2" target="_blank">Materials and Methods</a>. Open circles represent cells grown under under 395 p.p.m.v. CO₂ that were harvested after 12–13 generations (<i>t2</i> = day 8). Solid circles indicate cells grown under 1340 p.p.m.v. CO₂. In order to ensure suitable biomass for proteomics, these were harvested after 9–12 generations (<i>t2</i> = day 9 or 10) because of their lower growth rates.</p