Exposure to CO2 influences metabolism, calcification, and gene expression of the thecosome pteropodLimacina retroversa

Abstract

Thecosomatous pteropods, a group of aragonite shell-bearing zooplankton, are becoming an important sentinel organism for understanding the influence of ocean acidification on pelagic organisms. These animals show vulnerability to changing carbonate chemistry conditions, are geographically widespread, and are both biogeochemically and trophically important. The objective of this study was to determine how increasing duration and severity of CO treatment influence the physiology of the thecosome , integrating both gene expression and organism-level (respiration and calcification) metrics. We exposed pteropods to over-saturated, near-saturated or under-saturated conditions and sampled individuals at 1, 3, 7, 14 and 21 days of exposure to test for the effect of duration. We found that calcification was affected by borderline and under-saturated conditions by week two, while respiration appeared to be more strongly influenced by an interaction between severity and duration of exposure, showing complex changes by one week of exposure. The organismal metrics were corroborated by specific gene expression responses, with increased expression of biomineralization-associated genes in the medium and high treatments throughout and complex changes in metabolic genes corresponding to both captivity and CO treatment. Genes associated with other physiological processes such as lipid metabolism, neural function and ion pumping had complex responses, influenced by both duration and severity. Beyond these responses, our findings detail the captivity effects for these pelagic organisms, providing information to contextualize the conclusions of previous studies, and emphasizing a need for better culturing protocols.

Systematic Review and Meta-Analysis Toward Synthesis of Thresholds of Ocean Acidification Impacts on Calcifying Pteropods and Interactions With Warming

“…While juveniles showed reduced calcification at low ar (Comeau et al, 2010a;Bednaršek et al, 2017), an increase in calcification was seen in the less sensitive adults of L. retroversa (Maas et al, 2018). Experimentally derived LOE ranged from ar = 1.25 for 3 days (Comeau et al, 2010a) to ar = 1.02 for 1-3-week duration (Maas et al, 2018), which coincides with a significant calcification decline also in Heliconoides inflatus (Moya et al, 2016). These duration-dependent thresholds were validated with a field-derived changepoint of ar = 1.02 (SE = 0.07; Bednaršek et al, 2017).…”

“…This implies variable control over calcification processes, likely because calcification is energetically expensive when sustained at low ar gradients (Lischka et al, 2011;Bednaršek et al, 2017). While juveniles showed reduced calcification at low ar (Comeau et al, 2010a;Bednaršek et al, 2017), an increase in calcification was seen in the less sensitive adults of L. retroversa (Maas et al, 2018). Experimentally derived LOE ranged from ar = 1.25 for 3 days (Comeau et al, 2010a) to ar = 1.02 for 1-3-week duration (Maas et al, 2018), which coincides with a significant calcification decline also in Heliconoides inflatus (Moya et al, 2016).…”

“…We also recognized some additional caveats from the experimental studies that need to be considered; for example, experimental datasets were skewed toward shorter experiments, which made inferences of chronic effects less certain, or insufficient feeding that might have generated more acute responses that would have otherwise occurred in their natural environment. Finally, an insufficient number of experiments have explicitly tested multiple stressor effects on pteropods (e.g., Riebesell, 2012, 2017;Manno et al, 2012;Maas et al, 2018), making the stated thresholds only representative of ar in a single stressor future ocean. Approaches such as regional-specific habitat suitability indices that consider multiple stressors may represent a useful complementary approach.…”

The carbonic anhydrase activity of sinking and suspended particles in the North Pacific Ocean

“…Our measured pteropod CA activity is comparable to that of diatoms (1–2 × 10 −7 CA/POC; Table ), despite not using the enzyme for photosynthesis or in a traditional carbon‐concentrating mechanism (Hopkinson et al ). Instead, pteropods, like corals, most likely use CA for biomineralization (Tambutte et al ; Maas et al ). Because of the longevity of CA we have documented here, it is possible that CA produced by pteropods could still be active after the pteropods have died and are sinking through the water column, where corrosive carbonic acid will start to dissolve their aragonite shells.…”

Assessing annual variability in the shell thickness of the pteropod <i>Heliconoides inflatus</i> in the Cariaco Basin using micro-CT scanning

“…Manno et al, 2017). The impact of predicted future conditions on live specimens has been assessed using wide variety of parameters, including calcification (Comeau et al, 2009(Comeau et al, , 2010Maas et al, 2018;Moya et al, 2016), shell degradation (Bednaršek et al, 2012b;Bergan et al, 2017;Lischka and Riebesell, 2012), metabolic rates (Maas et al, 2011;Seibel et al, 2012), respiration (Comeau et al, 2010;Maas et al, 2018;Moya et al, 2016), and gene expression patterns (Koh et al, 2015;Maas et al, 2015Maas et al, , 2018Moya et al, 2016;Thabet et al, 2017). Generally, previous studies have found that as the aragonite saturation state decreases, pteropod calcification rates decrease (Comeau et al, 2010(Comeau et al, , 2009Lischka and Riebesell, 2012).…”