Morphological responses of a temperate intertidal foraminifer, Haynesina sp., to coastal acidification

Abstract

Coastal acidification could have widespread impact on marine organisms, affecting the ability of calcifying organisms to build shells and skeletons through calcium carbonate precipitation. As an abundant group of calcifying organisms, some protists within the phylum Foraminifera demonstrate potential success under elevated partial pressure of carbon dioxide (pCO₂) due to their ability to modulate intracellular pH. However, little is known about their responses under more extreme acidification conditions that are already seen in certain coastal environments. Here we exposed specimens of Haynesina sp., which belongs to a genus that is prevalent in temperate intertidal salt marshes, to moderate (pCO₂ = 2386.05+/-97.14 μatm) and high acidification (pCO₂ = 4797.64+/-157.82 μatm) conditions through the duration of 28 days. We demonstrate that although this species is capable of withstanding moderate levels of coastal acidification with little impact on overall test thickness, it can experience precipitation deficiency and even dissolution of the calcareous test under highly elevated pCO₂. Interestingly, such a deficit was primarily seen among live foraminifera, as compared to dead specimens, throughout the four-week experiment. This study suggests that a combination of environmental stress and the physiological process of test formation (i.e., calcite precipitation) could induce thinning of the test surface. Therefore, with the acceleration of coastal acidification due to anthropogenic production of CO₂, benthic foraminifera and other calcifying organisms among coastal ecosystems could reach a tipping point that leads to thinning and dissolution of their calcareous tests, which in turn, will impair their ecological function as a carbon sink.

Keywords: Haynesina; calcification; foraminifera; ocean acidification; pCO2.

Figure 1

(A) Schematic representation of the experimental setup for pCO₂ manipulation. Components of the diagram are as follows: ① the Apex controller system, ② wires connecting pH probe to APEX controller, ③ pH probe, ④ water pumps with Venturi injector, ⑤ solenoids controlling gas flow for the elevated pCO₂ treatments, ⑥ wires connecting the apex controller to the solenoids, ⑦ gas tubing connecting the CO₂ gas supply to the treatment tanks, ⑧ CO₂ gas supply. (B) A foraminifera test with labels showing the 8 newest chambers. (C) An example of isolated exteriorly facing test areas from each chamber for test-thickness analysis. Created with BioRender.com.

Figure 2

(A) Plot showing the number of chambers against the proloculus diameter. Each point represents a foraminifer. Color represents the assignment of two life stages, microsphere or megalosphere, based on the diameter of proloculus. Symbol shape represents different treatment groups, including untreated. (B) Comparison of the number of chambers and the test diameter between two life stages. p-values are based on one-way ANOVA accounting for different life stages (Materials and Methods). (C) Box and whisker plot showing distribution of the number of chambers in live and not-live foraminifera between the two life stages. The “not-live” specimens include both untreated and dead treated samples. p-values are based on two-way ANOVA accounting for life stages and live vs. not-live treatment groups (Materials and Methods).

Figure 3

(A,B) Distribution of normalized test thickness across the highly- (red), moderately- (gold), and no- (Blue) elevated pCO₂ conditions among the live (A) and dead (B) specimens. (C–E) Distribution of the normalized test thickness between the live (green) and dead (gray) foraminifera at the highly elevated pCO₂ (C), moderately elevated pCO₂ (D), and no elevated pCO₂ (E) treatments. Only microspheric foraminifera were used in this analysis (Materials and Methods). Untreated specimens were not included in this comparison. The η² values are effect sizes derived from two-way ANOVA (Materials and Methods).

Figure 4

(A–C) Comparison of test thicknesses between live and dead treated specimens within each of the 8 newest chambers under the highly elevated pCO₂ (A), moderately elevated pCO₂ (B), and no elevated pCO₂ (C) treatment conditions. The color of each chamber represents the effect size (η²) of the live vs. dead factor in a two-way ANOVA that accounts for variations among individual foraminifera. (D) Box and whisker plot showing the median, the first and third quartiles, and the minimum and maximum of effect sizes across all 8 chambers for each treatment. Only microspheric foraminifera were used in this analysis (Materials and Methods). The total number of specimens in each treatment group is documented in Supplementary Table S3.

Figure 5

(A) Schematic of chamber formation in foraminifera. Components are as follows: ① the system of reactions dictating that increased CO₂ results in increased proton concentration, ② vacuolar ATPases facilitate the export of protons by collecting them into vacuoles, as reported by Ujiié et al. (2023), ③ proton vacuoles are moved throughout the cytoplasm to coordinate exocytosis, ④ protons are released through exocytosis, ⑤ protons diffuse outward and around the test, lowering pH in the microenvironment surrounding the actively growing foraminifera cell (Toyofuku et al., 2017), ⑥ The proton-depleted environment allows for calcium carbonate precipitation. (B) Carbon chemistry during foraminiferal test formation. ⑦ Foraminifera promote calcification through proton export, ⑧ test surface dissolution driven by acidification. (C) Calcite saturation state predicted based on tri-weekly experimental measurements acquired from this study. Each dot represents a measurement data point. Red represents the highly elevated pCO₂ treatment, gold represents the moderately elevated pCO₂ treatment, and blue represents the no elevated pCO₂ treatment. The black horizontal line represents a calcite saturation of 1. Dashed lines represent the mean calcite saturation values of each treatment. Arrows on the right indicate the effect of calcite saturation state on the dissolution or precipitation of calcareous tests. Created with BioRender.com.