Impact of dissolved CO2 on calcification in two large, benthic foraminiferal species

PLOS ONE RESEARCH ARTICLE Impact of dissolved CO2 on calcification in two large, benthic foraminiferal species Linda Karoline Dämmer ID1*, Angelina Ivkić1¤, Lennart de Nooijer1, Willem Renema2,3, Alice E. Webb1, Gert-Jan Reichart1,4 1 Department of Ocean Systems, NIOZ Royal Netherlands Institute for Sea Research, Texel, The Netherlands, 2 Marine Biodiversity, Naturalis Biodiversity Center, Leiden, The Netherlands, 3 Department of Ecosystem & Landscape Dynamics, Institute for Biodiversity & Ecosystem Dynamics (IBED), University of Amsterdam, Amsterdam, The Netherlands, 4 Department of Earth Sciences, Faculty of Geosciences, Utrecht University, Utrecht, The Netherlands a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 ¤ Current address: Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, University of Vienna, Vienna, Austria * Abstract OPEN ACCESS Citation: Dämmer LK, Ivkić A, de Nooijer L, Renema W, Webb AE, Reichart G-J (2023) Impact of dissolved CO2 on calcification in two large, benthic foraminiferal species. PLoS ONE 18(8): e0289122. https://doi.org/10.1371/journal. pone.0289122 Editor: Fabrizio Frontalini, Universita degli Studi di Urbino Carlo Bo, ITALY Received: February 12, 2023 Accepted: July 12, 2023 Published: August 16, 2023 Copyright: © 2023 Dämmer et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Rising atmospheric CO2 shifts the marine inorganic carbonate system and decreases seawater pH, a process often abbreviated to ‘ocean acidification’. Since acidification decreases the saturation state for crystalline calcium carbonate (e.g., calcite and aragonite), rising dissolved CO2 levels will either increase the energy demand for calcification or reduce the total amount of CaCO3 precipitated. Here we report growth of two large benthic photosymbiontbearing foraminifera, Heterostegina depressa and Amphistegina lessonii, cultured at four different ocean acidification scenarios (400, 700, 1000 and 2200 ppm atmospheric pCO2). Using the alkalinity anomaly technique, we calculated the amount of calcium carbonate precipitated during the incubation and found that both species produced the most carbonate at intermediate CO2 levels. The chamber addition rates for each of the conditions were also determined and matched the changes in alkalinity. These results were complemented by micro-CT scanning of selected specimens to visualize the effect of CO2 on growth. The increased chamber addition rates at elevated CO2 concentrations suggest that both foraminifera species can take advantage of the increased availability of the inorganic carbon, despite a lower saturation state. This adds to the growing number of reports showing the variable response of foraminifera to elevated CO2 concentrations, which is likely a consequence of differences in calcification mechanisms. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was carried out under the program of the Netherlands Earth System Science Centre (NESSC), financially supported by the Ministry of Education, Culture and Science (OCW) gravitational grant 024.002.001. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Introduction With globally rising atmospheric CO2 levels, the marine carbonate system is steadily changing, approximately 25% of the CO2 added to the atmosphere since the industrial revolution has been taken up in the upper layers of the ocean [1]. This uptake has decreased pH by ~0.1 units [2–5] and shifted the speciation of dissolved inorganic carbon (DIC) by decreasing the carbonate ion concentration ([CO32-]) and increasing the bicarbonate ion concentration ([HCO3-]). As a consequence, the saturation state with respect to aragonite and calcite has been steadily PLOS ONE | https://doi.org/10.1371/journal.pone.0289122 August 16, 2023 1 / 19 PLOS ONE Competing interests: The authors have declared that no competing interests exist. Impact of dissolved CO2 on calcification in two large, benthic foraminiferal species declining and is widely believed to hamper marine calcification, for example by increasing the energy costs for maintaining high internal saturation states [6, 7]. However, the addition of CO2 to seawater also elevates the total concentration of DIC, which may be beneficial to calcification provided that the organism is capable of manipulating the ratio between the different inorganic carbon species. This may be achieved, for example, by actively increasing the pH during calcification and hence converting the (extra) HCO3- into CO32-, thereby increasing saturation state [8, 9]. Differences in the ability to manipulate their internal pH, may explain the observed variable responses of organisms to ocean acidification [10, 11]. Other parameters that may determine the reaction of foraminifera to ocean acidification may include increased carbon uptake by the symbionts (if present) and increased energy allocation to maintain the intracellular-extracellular ion balance [12]. Foraminifera are amongst the ocean’s most important calcifiers, with planktonic species estimated to produce up to 50% of all calcium carbonate in the open ocean [13]. In tropical regions, large benthic foraminifera can contribute up to 54% of the sediment [14–16] and approximately 80% of foraminiferal derived carbonate in reefs stems from large benthic foraminifera [16]. Since both planktonic and benthic foraminifera play a significant role in the global calcium carbonate production, it is essential to quantify and understand their response to changes in marine inorganic carbon chemistry. Since calcification produces CO2, the net impact of ocean acidification on calcification rates may either provide a positive or negative feedback to atmospheric CO2. Among the larger benthic foraminifera the responses to ocean acidification are mixed [17], with reports showing a reduction in calcification [18–24] or standing stocks [25, 26], but also an increase in chamber addition rates or no response to experimentally-induced ocean acidification [20, 27, 28]. Whereas the response in growth rates by low Mg-foraminifera to changes in pCO2 seems to be less variable [29], the overall mixed responses of foraminiferal calcification may well indicate differences in biomineralization strategies between genetically distant groups [30]. This could be related to the presence of photosynthetic symbionts in most large benthic foraminifera and their absence in most smaller, benthic foraminifera. Although some of these species have kleptoplasts [31, 32], photosynthesis by these intact algal plastids is unlikely to have an equally large impact on calcification as algal symbionts (...truncated)