Does Encapsulation Protect Embryos from the Effects of Ocean Acidification? The Example of Crepidula fornicata

Abstract

Early life history stages of marine organisms are generally thought to be more sensitive to environmental stress than adults. Although most marine invertebrates are broadcast spawners, some species are brooders and/or protect their embryos in egg or capsules. Brooding and encapsulation strategies are typically assumed to confer greater safety and protection to embryos, although little is known about the physico-chemical conditions within egg capsules. In the context of ocean acidification, the protective role of encapsulation remains to be investigated. To address this issue, we conducted experiments on the gastropod Crepidula fornicata. This species broods its embryos within capsules located under the female and veliger larvae are released directly into the water column. C. fornicata adults were reared at the current level of CO2 partial pressure (pCO2) (390 μatm) and at elevated levels (750 and 1400 μatm) before and after fertilization and until larval release, such that larval development occurred entirely at a given pCO2. The pCO2 effects on shell morphology, the frequency of abnormalities and mineralization level were investigated on released larvae. Shell length decreased by 6% and shell surface area by 11% at elevated pCO2 (1400 μatm). The percentage of abnormalities was 1.5- to 4-fold higher at 750 μatm and 1400 μatm pCO2, respectively, than at 390 μatm. The intensity of birefringence, used as a proxy for the mineralization level of the larval shell, also decreased with increasing pCO2. These negative results are likely explained by increased intracapsular acidosis due to elevated pCO2 in extracapsular seawater. The encapsulation of C. fornicata embryos did not protect them against the deleterious effects of a predicted pCO2 increase. Nevertheless, C. fornicata larvae seemed less affected than other mollusk species. Further studies are needed to identify the critical points of the life cycle in this species in light of future ocean acidification.

Slow shell building, a possible trait for resistance to the effects of acute ocean acidification

“…In the absence of evidence for other explanatory physiological mechanisms, we suggest that the lack of acute negative response to low Ω ar coupled to significantly slower PDI calcification rate provides further support for a kinetic‐energetic constraint on rapidly calcifying PDI bivalve larvae (Waldbusser et al a ,b). Furthermore, slower development (and thus slower calcification) may be a mechanism by which brooding indirectly provides increased resiliency to ocean acidification in marine invertebrates as seen in recent studies (Noisette et al ; Lucey et al ). The slower calcification rate during O. lurida PDI development coupled to a lack of acute response does not provide an absolute proof of a trait for resiliency to OA; however our results suggest the possibility of slow shell building as an example of exaptation (Gould and Vrba ).…”

“…In contrast, brooding species of oysters develop far more slowly during PDI formation (days instead of hours) (Hopkins ; Baker ). If the rapid rate of calcification is central to larval bivalve sensitivity to ocean acidification (as in Waldbusser et al ), slow shell development in brooding oysters may provide one possible mechanism for the recent findings of increased resistance of brooded invertebrate larvae to global change (Noisette et al ; Lucey et al ). Indeed, the limited studies to date however suggest brooded larvae maybe more resilient to acidification than broadcast spawned larvae, with important caveats seen in negative carry over effects from the swimming veliger stage to adult stages (Hettinger et al ).In general however, studies have generally focused on post‐release larvae in brooding oyster species and have not removed possible maternal effects during brooding.…”

Resilience of Atlantic Slippersnail Crepidula fornicata Larvae in the Face of Severe Coastal Acidification

“…To better 99 understand the response of C. fornicata larvae to OA, this study first characterized a suite of phenotypic 100 traits in response to three pH treatments (pH 8.0, 7.6, 7.5) coupled with transcriptomic responses of 101 larvae that had been reared at the different pH levels for 4 days, starting within 12 hours of hatching. in combination with previously reported phenotypes of reduced shell growth rates in C. fornicata larvae 106 (Noisette et al, 2014). The impact of acidification on time to competence for metamorphosis was also 107 quantified; we predicted that time to competence would be prolonged even if growth rates were 108 unaffected, as the onset of competence relates to processes of differentiation rather than growth 109 (Pechenik et al, 1996); delayed time to competence has previously been noted in other marine 110 mollusks, eastern oyster and bay scallop (Talmage and Gobler, 2010).…”

“…However, 308 complex interactions were observed between OA and diet (Maboloc and Chan, 2017). In a study 309 exposing C. fornicata to OA treatments (pH 7.82, pH 7.56) over the entire course of development, from fertilization to hatching, larvae from reduced pH treatments were smaller at hatching than those 311 under control conditions (Noisette et al, 2014), suggesting that OA impacted the reproductive or 312 development process or that maternal effects were passed onto offspring. These two studies highlight 313 the importance of considering other factors in addition to OA, such as pre-hatching events and diet, in…”

“…In contrast to adult C. fornicata, early life stages have been shown to be 92 relatively more negatively affected by environmental stressors. For instance, C. fornicata larvae under 93 reduced pH exhibited decreased shell growth, their shells had more abnormalities, and their 94 mineralization rates decreased (Noisette et al, 2014). A study on C. fornicata's congener, C. onyx, 95 found no effect of reduced pH on larval mortality, but did similarly document reduced growth rates 96 and increasingly porous shells (Maboloc and Chan, 2017).…”