Complex Responses of Intertidal Molluscan Embryos to a Warming and Acidifying Ocean in the Presence of UV Radiation

Davis, Andrew R.; Coleman, Daniel; Broad, Allison; Byrne, Maria; Dworjanyn, Symon A.; Przeslawski, Rachel

doi:10.1371/journal.pone.0055939

Cited by 36 publications

(37 citation statements)

References 45 publications

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“…The prevailing additive nature of their joint effects implies that warming tended to compensate for the negative effects of UV‐B radiation. For instance, we found that warming alleviated the negative effect of UV‐B radiation on marine organisms' fitness and the performance of marine larvae (Figure ), as warming generally enhanced metabolic processes that were suppressed by UV‐B (Davis et al, ; Li, Gao, Villafane, & Helbling, ; Moresino & Helbling, ; Vidussi et al, ). The compensatory effects of warming on the negative effects of elevated UV‐B radiation could be partly explained by temperature‐dependent photoenzymatic repair (PER), which is an enzyme‐mediated process and therefore tends to increase with increasing temperature (Langenbacher et al, ).…”

Section: Discussionmentioning

confidence: 90%

Increasing temperature within thermal limits compensates negative ultraviolet‐B radiation effects in terrestrial and aquatic organisms

Jin

Overmans

Duarte

et al. 2019

Global Ecol Biogeogr

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Aim The interactive effects of increased temperature and ultraviolet‐B (UV‐B) radiation on terrestrial and aquatic biota remain poorly understood. Our goal is to increase knowledge by providing a comprehensive assessment of the combined effects of warming and increased UV‐B on organisms across these domains. Location Global. Time period 1995–2016. Major taxa studied Terrestrial plants and animals, and marine and freshwater microalgae, macroalgae and animals. Methods We examined, using a meta‐analysis based on 1,139 published experimental assessments, the combined effects of temperature and UV‐B across terrestrial, freshwater and marine biota. We characterized the prevailing mode of combined effects (additive, synergistic or antagonistic), and assessed whether these were dose‐dependent or differed between terrestrial, freshwater and marine species, or between organisms growing in the Northern and Southern Hemispheres. Results Our results show that the two stressors generally acted opposingly, with a significant positive effect of increased temperature and a significant adverse effect of elevated UV‐B radiation. Regarding their interactive impact, additive interactions (84%) appeared to be much more common compared with multiplicative (16%) effects. The frequencies of interaction types differed significantly among the three habitats and different plant functional groups. The proportion of both synergistic and antagonistic effects increased with increasing magnitude of temperature and UV‐B changes, suggesting that additivity is constrained by an organism's thermal and physiological limits. Main conclusions Our analysis demonstrates that due to their mostly opposing nature, elevated temperature, within the thermal limits of organisms, tends to compensate for the negative impact of UV‐B radiation when acting together, while their additive interaction is likely to assist impact prognosis. Our study, therefore, provides new insights into the predictions of the interactive effects of global change drivers across different habitats.

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Section: Discussionmentioning

confidence: 90%

Increasing temperature within thermal limits compensates negative ultraviolet‐B radiation effects in terrestrial and aquatic organisms

Jin

Overmans

Duarte

et al. 2019

Global Ecol Biogeogr

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“…Overall, both molluscs and echinoderms seem equally vulnerable to ocean acidification at premetamorphic stages (Fig. 6) (Parker et al, 2010;Byrne et al, 2011), although intertidal and infaunal species may show increased resilience due to adaptation to pH fluctuations in rock pools (Davis et al, 2013) or low pH in sediments (Talmage & Gobler, 2011;Styf et al, 2013;Nguyen & Byrne, 2014). The impacts of acidification on calcification on echinoderms appear largely due to metabolic change (Byrne et al, 2013a;Evans et al, 2014) and less so to their vulnerable high magnesium calcite skeleton (Andersson et al, 2008).…”

Section: Vulnerable and Resilient Taxamentioning

confidence: 99%

“…An understanding of physiology may help explain complex responses to multiple stressors (e.g. Davis et al, 2013), as has been shown in the variation in the metabolic responses of amphipods . In addition, physiological investigations will help increase the taxonomic resolution of predictions of impact.…”

Section: Future Directions and Recommendationsmentioning

confidence: 99%

A review and meta‐analysis of the effects of multiple abiotic stressors on marine embryos and larvae

Przeslawski

Byrne

Mellin

2015

Global Change Biology

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411

391

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Marine organisms are simultaneously exposed to anthropogenic stressors with likely interactive effects, including synergisms in which the combined effects of multiple stressors are greater than the sum of individual effects. Early life stages of marine organisms are potentially vulnerable to the stressors associated with global change, but identifying general patterns across studies, species and response variables is challenging. This review represents the first meta-analysis of multistressor studies to target early marine life stages (embryo to larvae), particularly between temperature, salinity and pH as these are the best studied. Knowledge gaps in research on multiple abiotic stressors and early life stages are also identified. The meta-analysis yielded several key results: (1) Synergistic interactions (65% of individual tests) are more common than additive (17%) or antagonistic (17%) interactions. (2) Larvae are generally more vulnerable than embryos to thermal and pH stress. (3) Survival is more likely than sublethal responses to be affected by thermal, salinity and pH stress. (4) Interaction types vary among stressors, ontogenetic stages and biological responses, but they are more consistent among phyla. (5) Ocean acidification is a greater stressor for calcifying than noncalcifying larvae. Despite being more ecologically realistic than single-factor studies, multifactorial studies may still oversimplify complex systems, and so meta-analyses of the data from them must be cautiously interpreted with regard to extrapolation to field conditions. Nonetheless, our results identify taxa with early life stages that may be particularly vulnerable (e.g. molluscs, echinoderms) or robust (e.g. arthropods, cnidarians) to abiotic stress. We provide a list of recommendations for future multiple stressor studies, particularly those focussed on early marine life stages.

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“…responses under ocean acidification of Aplysia or any other sea hare species (the clade Anaspidea); low pH was shown to increase mortality in the embryos of a tropical sea hare (Davis et al, 2013). One additional study found increased respiratory pumping in Aplysia californica in seawater into which CO 2 was bubbled, causing extreme and rapid hypercapnia (a decrease to 5.9 pH over 10 min ;Croll, 1985).…”

Section: Discussionmentioning

confidence: 99%

Sea HareAplysia punctata(Mollusca: Gastropoda) Can Maintain Shell Calcification under Extreme Ocean Acidification

Carey

Dupont

Sigwart

2016

The Biological Bulletin

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Abstract. Ocean acidification is expected to cause energetic constraints upon marine calcifying organisms such as molluscs and echinoderms, because of the increased costs of building or maintaining shell material in lower pH. We examined metabolic rate, shell morphometry, and calcification in the sea hare Aplysia punctata under short-term exposure (19 days) to an extreme ocean acidification scenario (pH 7.3, ϳ2800 atm pCO 2 ), along with a group held in control conditions (pH 8.1, ϳ344 atm pCO 2 ). This gastropod and its congeners are broadly distributed and locally abundant grazers, and have an internal shell that protects the internal organs. Specimens were examined for metabolic rate via closed-chamber respirometry, followed by removal and examination of the shell under confocal microscopy. Staining using calcein determined the amount of new calcification that occurred over 6 days at the end of the acclimation period. The width of new, pre-calcified shell on the distal shell margin was also quantified as a proxy for overall shell growth. Aplysia punctata showed a 30% reduction in metabolic rate under low pH, but calcification was not affected. This species is apparently able to maintain calcification rate even under extreme low pH, and even when under the energetic constraints of lower metabolism.This finding adds to the evidence that calcification is a largely autonomous process of crystallization that occurs as long as suitable haeomocoel conditions are preserved. There was, however, evidence that the accretion of new, noncalcified shell material may have been reduced, which would lead to overall reduced shell growth under longerterm exposures to low pH independent of calcification. Our findings highlight that the chief impact of ocean acidification upon the ability of marine invertebrates to maintain their shell under low pH may be energetic constraints that hinder growth of supporting structure, rather than maintenance of calcification.

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Complex Responses of Intertidal Molluscan Embryos to a Warming and Acidifying Ocean in the Presence of UV Radiation

Cited by 36 publications

References 45 publications

Increasing temperature within thermal limits compensates negative ultraviolet‐B radiation effects in terrestrial and aquatic organisms

Increasing temperature within thermal limits compensates negative ultraviolet‐B radiation effects in terrestrial and aquatic organisms

A review and meta‐analysis of the effects of multiple abiotic stressors on marine embryos and larvae

Sea HareAplysia punctata(Mollusca: Gastropoda) Can Maintain Shell Calcification under Extreme Ocean Acidification

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