Abstract
Rising atmospheric CO2 reduces seawater pH causing ocean acidification (OA). Understanding how resilient marine organisms respond to OA may help predict how community dynamics will shift as CO2 continues rising. The common slipper shell snail Crepidula fornicata is a marine gastropod native to eastern North America that has been a successful invader along the western European coastline and elsewhere. It has also been previously shown to be resilient to global change stressors. To examine the mechanisms underlying C. fornicata’s resilience to OA, we conducted two controlled laboratory experiments. First, we examined several phenotypes and genome-wide gene expression of C. fornicata in response to pH treatments (7.5, 7.6, and 8.0) throughout the larval stage and then tested how conditions experienced as larvae influenced juvenile stages (i.e., carry-over effects). Second, we examined genome-wide gene expression patterns of C. fornicata larvae in response to acute (4, 10, 24, and 48 h) pH treatment (7.5 and 8.0). Both C. fornicata larvae and juveniles exhibited resilience to OA and their gene expression responses highlight the role of transcriptome plasticity in this resilience. Larvae did not exhibit reduced growth under OA until they were at least 8 days old. These phenotypic effects were preceded by broad transcriptomic changes, which likely served as an acclimation mechanism for combating reduced pH conditions frequently experienced in littoral zones. Larvae reared in reduced pH conditions also took longer to become competent to metamorphose. In addition, while juvenile sizes at metamorphosis reflected larval rearing pH conditions, no carry-over effects on juvenile growth rates were observed. Transcriptomic analyses suggest increased metabolism under OA, which may indicate compensation in reduced pH environments. Transcriptomic analyses through time suggest that these energetic burdens experienced under OA eventually dissipate, allowing C. fornicata to reduce metabolic demands and acclimate to reduced pH. Carry-over effects from larval OA conditions were observed in juveniles; however, these effects were larger for more severe OA conditions and larvae reared in those conditions also demonstrated less transcriptome elasticity. This study highlights the importance of assessing the effects of OA across life history stages and demonstrates how transcriptomic plasticity may allow highly resilient organisms, like C. fornicata, to acclimate to reduced pH environments.
Highlights
Rising atmospheric carbon dioxide (CO2) concentrations, resulting from anthropogenic emissions, are causing substantial increases in the acidity of the world’s oceans (Bigg et al, 2003; IPCC, 2013)
These reduced juvenile shell lengths were due to reduced larval shell lengths observed from day 8 onward (Supplementary Figure 1A) and significant differences in juvenile shell length growth rates were not observed after multiple test correction (P = 0.0479; Tukey’s Honest Significant Difference (HSD) > 0.05; Figure 4A)
These reductions were not immediately apparent and only became evident after 8 days of exposure for tissue growth and after 11 days of exposure for shell length increases (Figure 2). These results are in line with previous studies on C. fornicata’s congener Crepidula onyx, which did not exhibit immediate growth rate reductions and slower larval growth was only observed after 14 days of rearing at reduced pH (7.3 and 7.7; Maboloc and Chan, 2017)
Summary
Rising atmospheric carbon dioxide (CO2) concentrations, resulting from anthropogenic emissions, are causing substantial increases in the acidity of the world’s oceans (Bigg et al, 2003; IPCC, 2013). This process, known as ocean acidification (OA), involves carbonic acid formed by the hydrolysis of atmospheric CO2 in seawater dissociating into bicarbonate [HCO3−] and hydrogen ions [H+], lowering seawater pH (Orr et al, 2005). The negative effects of OA on marine mollusk physiology have been well documented [Vargas et al, 2013; Dineshram et al, 2015; Waldbusser et al, 2016; Maboloc and Chan, 2017; reviewed in Strader et al (2020)]. While the physiological and molecular responses to OA have been widely studied (reviewed in Strader et al (2020)], how these responses vary across life history stages remain less explored
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