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      Parental exposure to ocean acidification impacts gamete production and physiology but not offspring performance in Nematostella vectensis

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          ABSTRACT

          Ocean acidification (OA) resulting from anthropogenic CO 2 emissions is impairing the reproduction of marine organisms. While parental exposure to OA can protect offspring via carryover effects, this phenomenon is poorly understood in many marine invertebrate taxa. Here, we examined how parental exposure to acidified (pH 7.40) versus ambient (pH 7.72) seawater influenced reproduction and offspring performance across six gametogenic cycles (13 weeks) in the estuarine sea anemone Nematostella vectensis. Females exhibited reproductive plasticity under acidic conditions, releasing significantly fewer but larger eggs compared to ambient females after 4 weeks of exposure, and larger eggs in two of the four following spawning cycles despite recovering fecundity, indicating long-term acclimatization and greater investment in eggs. Males showed no changes in fecundity under acidic conditions but produced a greater percentage of sperm with high mitochondrial membrane potential (MMP; a proxy for elevated motility), which corresponded with higher fertilization rates relative to ambient males. Finally, parental exposure to acidic conditions did not significantly influence offspring development rates, respiration rates, or heat tolerance. Overall, this study demonstrates that parental exposure to acidic conditions impacts gamete production and physiology but not offspring performance in N. vectensis, suggesting that increased investment in individual gametes may promote fitness.

          Abstract

          Summary: Ocean acidification (OA) threatens the reproduction of marine invertebrates. We investigated how simulated OA affected the reproduction of a model sea anemone, revealing effects with mixed implications for fitness.

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          Most cited references71

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          Fiji: an open-source platform for biological-image analysis.

          Fiji is a distribution of the popular open-source software ImageJ focused on biological-image analysis. Fiji uses modern software engineering practices to combine powerful software libraries with a broad range of scripting languages to enable rapid prototyping of image-processing algorithms. Fiji facilitates the transformation of new algorithms into ImageJ plugins that can be shared with end users through an integrated update system. We propose Fiji as a platform for productive collaboration between computer science and biology research communities.
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            Ocean acidification: the other CO2 problem.

            Rising atmospheric carbon dioxide (CO2), primarily from human fossil fuel combustion, reduces ocean pH and causes wholesale shifts in seawater carbonate chemistry. The process of ocean acidification is well documented in field data, and the rate will accelerate over this century unless future CO2 emissions are curbed dramatically. Acidification alters seawater chemical speciation and biogeochemical cycles of many elements and compounds. One well-known effect is the lowering of calcium carbonate saturation states, which impacts shell-forming marine organisms from plankton to benthic molluscs, echinoderms, and corals. Many calcifying species exhibit reduced calcification and growth rates in laboratory experiments under high-CO2 conditions. Ocean acidification also causes an increase in carbon fixation rates in some photosynthetic organisms (both calcifying and noncalcifying). The potential for marine organisms to adapt to increasing CO2 and broader implications for ocean ecosystems are not well known; both are high priorities for future research. Although ocean pH has varied in the geological past, paleo-events may be only imperfect analogs to current conditions.
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              Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming

              Ocean acidification represents a threat to marine species worldwide, and forecasting the ecological impacts of acidification is a high priority for science, management, and policy. As research on the topic expands at an exponential rate, a comprehensive understanding of the variability in organisms' responses and corresponding levels of certainty is necessary to forecast the ecological effects. Here, we perform the most comprehensive meta-analysis to date by synthesizing the results of 228 studies examining biological responses to ocean acidification. The results reveal decreased survival, calcification, growth, development and abundance in response to acidification when the broad range of marine organisms is pooled together. However, the magnitude of these responses varies among taxonomic groups, suggesting there is some predictable trait-based variation in sensitivity, despite the investigation of approximately 100 new species in recent research. The results also reveal an enhanced sensitivity of mollusk larvae, but suggest that an enhanced sensitivity of early life history stages is not universal across all taxonomic groups. In addition, the variability in species' responses is enhanced when they are exposed to acidification in multi-species assemblages, suggesting that it is important to consider indirect effects and exercise caution when forecasting abundance patterns from single-species laboratory experiments. Furthermore, the results suggest that other factors, such as nutritional status or source population, could cause substantial variation in organisms' responses. Last, the results highlight a trend towards enhanced sensitivity to acidification when taxa are concurrently exposed to elevated seawater temperature.
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                Author and article information

                Contributors
                Journal
                Biol Open
                Biol Open
                BIO
                Biology Open
                The Company of Biologists Ltd
                2046-6390
                15 March 2023
                28 February 2023
                28 February 2023
                : 12
                : 3
                : bio059746
                Affiliations
                Department of Biology, University of Pennsylvania , Philadelphia, PA 19104, USA
                Author notes
                [*]

                These authors contributed equally to this work

                []Author for correspondence ( kbarott@ 123456sas.upenn.edu )

                Competing interests

                The authors declare no competing or financial interests.

                Author information
                http://orcid.org/0000-0002-2288-6389
                http://orcid.org/0000-0001-5235-5928
                http://orcid.org/0000-0002-9828-1888
                http://orcid.org/0000-0001-7371-4870
                Article
                BIO059746
                10.1242/bio.059746
                10003076
                36716103
                8fa76b9a-a6ab-42f8-88d2-455381d24f0a
                © 2023. Published by The Company of Biologists Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 17 November 2022
                : 20 January 2023
                Funding
                Funded by: National Institutes of Health;
                Award ID: T32 HD083185
                Funded by: National Science Foundation, http://dx.doi.org/10.13039/100000001;
                Award ID: 1812191
                Award ID: 1923743
                Funded by: Charles E. Kaufman Foundation;
                Award ID: KA2021-114797
                Funded by: University of Pennsylvania, http://dx.doi.org/10.13039/100006920;
                Categories
                Research Article

                Life sciences
                climate change,acclimatization,carryover effects,reproduction,development,cnidarian
                Life sciences
                climate change, acclimatization, carryover effects, reproduction, development, cnidarian

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