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

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          Abstract

          Climate change and ocean acidification will expose marine organisms to synchronous multiple stressors, with early life stages being potentially most vulnerable to changing environmental conditions. We simultaneously exposed encapsulated molluscan embryos to three abiotic stressors—acidified conditions, elevated temperate, and solar UV radiation in large outdoor water tables in a multifactorial design. Solar UV radiation was modified with plastic filters, while levels of the other factors reflected IPCC predictions for near-future change. We quantified mortality and the rate of embryonic development for a mid-shore littorinid, Bembicium nanum, and low-shore opisthobranch, Dolabrifera brazieri. Outcomes were consistent for these model species with embryos faring significantly better at 26°C than 22°C. Mortality sharply increased at the lowest temperature (22°C) and lowest pH (7.6) examined, producing a significant interaction. Under these conditions mortality approached 100% for each species, representing a 2- to 4-fold increase in mortality relative to warm (26°C) non-acidified conditions. Predictably, development was more rapid at the highest temperature but this again interacted with acidified conditions. Development was slowed under acidified conditions at the lowest temperature. The presence of UV radiation had minimal impact on the outcomes, only slowing development for the littorinid and not interacting with the other factors. Our findings suggest that a warming ocean, at least to a threshold, may compensate for the effects of decreasing pH for some species. It also appears that stressors will interact in complex and unpredictable ways in a changing climate.

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          Ecology. Physiology and climate change.

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            Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation.

            Temperature controls the rate of fundamental biochemical processes and thereby regulates organismal attributes including development rate and survival. The increase in metabolic rate with temperature explains substantial among-species variation in life-history traits, population dynamics, and ecosystem processes. Temperature can also cause variability in metabolic rate within species. Here, we compare the effect of temperature on a key component of marine life cycles among a geographically and taxonomically diverse group of marine fish and invertebrates. Although innumerable lab studies document the negative effect of temperature on larval development time, little is known about the generality versus taxon-dependence of this relationship. We present a unified, parameterized model for the temperature dependence of larval development in marine animals. Because the duration of the larval period is known to influence larval dispersal distance and survival, changes in ocean temperature could have a direct and predictable influence on population connectivity, community structure, and regional-to-global scale patterns of biodiversity.
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              Impact of Ocean Warming and Ocean Acidification on Larval Development and Calcification in the Sea Urchin Tripneustes gratilla

              Background As the oceans simultaneously warm, acidify and increase in P CO2, prospects for marine biota are of concern. Calcifying species may find it difficult to produce their skeleton because ocean acidification decreases calcium carbonate saturation and accompanying hypercapnia suppresses metabolism. However, this may be buffered by enhanced growth and metabolism due to warming. Methodology/Principal Findings We examined the interactive effects of near-future ocean warming and increased acidification/P CO2 on larval development in the tropical sea urchin Tripneustes gratilla. Larvae were reared in multifactorial experiments in flow-through conditions in all combinations of three temperature and three pH/P CO2 treatments. Experiments were placed in the setting of projected near future conditions for SE Australia, a global change hot spot. Increased acidity/P CO2 and decreased carbonate mineral saturation significantly reduced larval growth resulting in decreased skeletal length. Increased temperature (+3°C) stimulated growth, producing significantly bigger larvae across all pH/P CO2 treatments up to a thermal threshold (+6°C). Increased acidity (-0.3-0.5 pH units) and hypercapnia significantly reduced larval calcification. A +3°C warming diminished the negative effects of acidification and hypercapnia on larval growth. Conclusions and Significance This study of the effects of ocean warming and CO2 driven acidification on development and calcification of marine invertebrate larvae reared in experimental conditions from the outset of development (fertilization) shows the positive and negative effects of these stressors. In simultaneous exposure to stressors the dwarfing effects of acidification were dominant. Reduction in size of sea urchin larvae in a high P CO2 ocean would likely impair their performance with negative consequent effects for benthic adult populations.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                6 February 2013
                : 8
                : 2
                : e55939
                Affiliations
                [1 ]Institute for Conservation Biology and Environmental Management, School of Biological Sciences, University of Wollongong, Wollongong, New South Wales, Australia
                [2 ]Schools of Medical and Biological Sciences, University of Sydney, Sydney, New South Wales, Australia
                [3 ]National Marine Science Centre, Southern Cross University, Coffs Harbour, New South Wales, Australia
                University of Gothenburg, Sweden
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AD RP. Performed the experiments: DC AB AD. Analyzed the data: RP AD. Contributed reagents/materials/analysis tools: MB SD. Wrote the paper: AD RP AB MB.

                [¤]

                Current address: Coastal Marine and Climate Change Group, Geoscience Australia, Canberra, ACT, Australia

                Article
                PONE-D-12-24453
                10.1371/journal.pone.0055939
                3566103
                23405238
                9e22d2e6-016f-4d14-b9ee-79a7abdf1789
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 August 2012
                : 7 January 2013
                Page count
                Pages: 7
                Funding
                The authors gratefully acknowledge the financial support of the Australian Research Council (to MB and ARD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Developmental Biology
                Organism Development
                Ecology
                Global Change Ecology
                Marine Ecology
                Marine Biology
                Marine Conservation
                Marine Ecology
                Model Organisms
                Zoology
                Malacology
                Earth Sciences
                Marine and Aquatic Sciences
                Oceanography
                Biological Oceanography

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                Uncategorized

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