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      Physiological and Behavioral Plasticity of the Sea Cucumber Holothuria forskali (Echinodermata, Holothuroidea) to Acidified Seawater

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          Abstract

          Research into the effects of reduced pH caused by rising CO 2 on echinoderms has been strongly biased toward those groups which rely heavily on calcification, such as sea urchins. There is very limited information available for groups that are less reliant on calcification, such as sea cucumbers. Moreover, plasticity in physiology and behavior in holothurians, which is considered to be critical to cope with ocean acidification, remains even less understood. Here, we examined the effects of a 22-week exposure to three pH levels (pH 7.97, 7.88, and 7.79) on the responses of adult Holothuria forskali. This is an abundant and ecologically important sea cucumber in shallow waters of the northeast Atlantic and Mediterranean. The holothurians did not exhibit serious acidosis after a 4-week gradually decreased pH exposure, possibly due to the slow acclimation period. After an additional 18 weeks of exposure, coelomic acid–base parameters did not differ significantly among the pH treatments, whereas they were higher than in week 4. Gonad development, defense behavior, and the structure and Ca 2+ and Mg 2+ concentrations of calcareous endoskeleton deposited in the body wall were all unaffected by decreased levels of seawater pH. No statistical differences were found after 22 weeks, and adult H. forskali showed strong physiological and behavioral plasticity to the effects of lowered seawater pH. While the interpretation of our results is restricted due to small sample sizes, this first long-term study of the effects of seawater acidification on sea cucumbers revealed resilience within the wide natural range of pCO 2 found in NE Atlantic coastal waters.

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          Carbon dioxide in water and seawater: the solubility of a non-ideal gas

          R.F. Weiss (1974)
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            High-Frequency Dynamics of Ocean pH: A Multi-Ecosystem Comparison

            The effect of Ocean Acidification (OA) on marine biota is quasi-predictable at best. While perturbation studies, in the form of incubations under elevated pCO2, reveal sensitivities and responses of individual species, one missing link in the OA story results from a chronic lack of pH data specific to a given species' natural habitat. Here, we present a compilation of continuous, high-resolution time series of upper ocean pH, collected using autonomous sensors, over a variety of ecosystems ranging from polar to tropical, open-ocean to coastal, kelp forest to coral reef. These observations reveal a continuum of month-long pH variability with standard deviations from 0.004 to 0.277 and ranges spanning 0.024 to 1.430 pH units. The nature of the observed variability was also highly site-dependent, with characteristic diel, semi-diurnal, and stochastic patterns of varying amplitudes. These biome-specific pH signatures disclose current levels of exposure to both high and low dissolved CO2, often demonstrating that resident organisms are already experiencing pH regimes that are not predicted until 2100. Our data provide a first step toward crystallizing the biophysical link between environmental history of pH exposure and physiological resilience of marine organisms to fluctuations in seawater CO2. Knowledge of this spatial and temporal variation in seawater chemistry allows us to improve the design of OA experiments: we can test organisms with a priori expectations of their tolerance guardrails, based on their natural range of exposure. Such hypothesis-testing will provide a deeper understanding of the effects of OA. Both intuitively simple to understand and powerfully informative, these and similar comparative time series can help guide management efforts to identify areas of marine habitat that can serve as refugia to acidification as well as areas that are particularly vulnerable to future ocean change.
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              Ocean acidification may increase calcification rates, but at a cost.

              Ocean acidification is the lowering of pH in the oceans as a result of increasing uptake of atmospheric carbon dioxide. Carbon dioxide is entering the oceans at a greater rate than ever before, reducing the ocean's natural buffering capacity and lowering pH. Previous work on the biological consequences of ocean acidification has suggested that calcification and metabolic processes are compromised in acidified seawater. By contrast, here we show, using the ophiuroid brittlestar Amphiura filiformis as a model calcifying organism, that some organisms can increase the rates of many of their biological processes (in this case, metabolism and the ability to calcify to compensate for increased seawater acidity). However, this upregulation of metabolism and calcification, potentially ameliorating some of the effects of increased acidity comes at a substantial cost (muscle wastage) and is therefore unlikely to be sustainable in the long term.
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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                25 September 2018
                2018
                : 9
                : 1339
                Affiliations
                [1] 1Marine Biology and Ecology Research Centre, University of Plymouth , Plymouth, United Kingdom
                [2] 2Plymouth Marine Laboratory , Plymouth, United Kingdom
                [3] 3National Marine Environmental Monitoring Center, State Oceanic Administration , Dalian, China
                [4] 4Department of Biological Sciences, Florida State University , Tallahassee, FL, United States
                [5] 5School of Geography and Ocean Science, Nanjing University , Nanjing, China
                [6] 6Shimoda Marine Research Centre, University of Tsukuba , Tsukuba, Japan
                Author notes

                Edited by: Youji Wang, Shanghai Ocean University, China

                Reviewed by: Zhijun Dong, Yantai Institute of Coastal Zone Research (CAS), China; Sam Dupont, University of Gothenburg, Sweden; Kennedy Wolfe, The University of Queensland, Australia

                *Correspondence: Xiutang Yuan, xtyuan@ 123456nmemc.org.cn

                This article was submitted to Aquatic Physiology, a section of the journal Frontiers in Physiology

                Article
                10.3389/fphys.2018.01339
                6167980
                7db1252b-bbf8-4d89-b481-b5dbf98bcf32
                Copyright © 2018 Yuan, McCoy, Du, Widdicombe and Hall-Spencer.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 26 March 2018
                : 05 September 2018
                Page count
                Figures: 4, Tables: 2, Equations: 0, References: 60, Pages: 10, Words: 0
                Categories
                Physiology
                Original Research

                Anatomy & Physiology
                holothurians,ne atlantic,physiological plasticity,antipredator behavior,ocean acidification

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