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      Short- and long-term impacts of variable hypoxia exposures on kelp forest sea urchins

      , 1 , 1 , 2

      Scientific Reports

      Nature Publishing Group UK

      Climate-change ecology, Ecophysiology

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          Abstract

          Climate change is altering the intensity and variability of environmental stress that organisms and ecosystems experience, but effects of changing stress regimes are not well understood. We examined impacts of constant and variable sublethal hypoxia exposures on multiple biological processes in the sea urchin Strongylocentrotus purpuratus, a key grazer in California Current kelp forests, which experience high variability in physical conditions. We quantified metabolic rates, grazing, growth, calcification, spine regeneration, and gonad production under constant, 3-hour variable, and 6-hour variable exposures to sublethal hypoxia, and compared responses for each hypoxia regime to normoxic conditions. Sea urchins in constant hypoxia maintained baseline metabolic rates, but had lower grazing, gonad development, and calcification rates than those in ambient conditions. The sublethal impacts of variable hypoxia differed among biological processes. Spine regrowth was reduced under all hypoxia treatments, calcification rates under variable hypoxia were intermediate between normoxia and constant hypoxia, and gonad production correlated negatively with continuous time under hypoxia. Therefore, exposure variability can differentially modulate the impacts of sublethal hypoxia, and may impact sea urchin populations and ecosystems via reduced feeding and reproduction. Addressing realistic, multifaceted stressor exposures and multiple biological responses is crucial for understanding climate change impacts on species and ecosystems.

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          Most cited references 48

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          Thresholds of hypoxia for marine biodiversity.

          Hypoxia is a mounting problem affecting the world's coastal waters, with severe consequences for marine life, including death and catastrophic changes. Hypoxia is forecast to increase owing to the combined effects of the continued spread of coastal eutrophication and global warming. A broad comparative analysis across a range of contrasting marine benthic organisms showed that hypoxia thresholds vary greatly across marine benthic organisms and that the conventional definition of 2 mg O(2)/liter to designate waters as hypoxic is below the empirical sublethal and lethal O(2) thresholds for half of the species tested. These results imply that the number and area of coastal ecosystems affected by hypoxia and the future extent of hypoxia impacts on marine life have been generally underestimated.
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            Quantifying the evidence for ecological synergies.

            There is increasing concern that multiple drivers of ecological change will interact synergistically to accelerate biodiversity loss. However, the prevalence and magnitude of these interactions remain one of the largest uncertainties in projections of future ecological change. We address this uncertainty by performing a meta-analysis of 112 published factorial experiments that evaluated the impacts of multiple stressors on animal mortality in freshwater, marine and terrestrial communities. We found that, on average, mortalities from the combined action of two stressors were not synergistic and this result was consistent across studies investigating different stressors, study organisms and life-history stages. Furthermore, only one-third of relevant experiments displayed truly synergistic effects, which does not support the prevailing ecological paradigm that synergies are rampant. However, in more than three-quarters of relevant experiments, the outcome of multiple stressor interactions was non-additive (i.e. synergies or antagonisms), suggesting that ecological surprises may be more common than simple additive effects.
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              Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living.

              Temperature's pervasive effects on physiological systems are reflected in the suite of temperature-adaptive differences observed among species from different thermal niches, such as species with different vertical distributions (zonations) along the subtidal to intertidal gradient. Among the physiological traits that exhibit adaptive variation related to vertical zonation are whole organism thermal tolerance, heart function, mitochondrial respiration, membrane static order (fluidity), action potential generation, protein synthesis, heat-shock protein expression, and protein thermal stability. For some, but not all, of these thermally sensitive traits acclimatization leads to adaptive shifts in thermal optima and limits. The costs associated with repairing thermal damage and adapting systems through acclimatization may contribute importantly to energy budgets. These costs arise from such sources as: (i) activation and operation of the heat-shock response, (ii) replacement of denatured proteins that have been removed through proteolysis, (iii) restructuring of cellular membranes ("homeoviscous" adaptation), and (iv) pervasive shifts in gene expression (as gauged by using DNA microarray techniques). The vertical zonation observed in rocky intertidal habitats thus may reflect two distinct yet closely related aspects of thermal physiology: (i) intrinsic interspecific differences in temperature sensitivities of physiological systems, which establish thermal optima and tolerance limits for species; and (ii) 'cost of living' considerations arising from sub-lethal perturbation of these physiological systems, which may establish an energetics-based limitation to the maximal height at which a species can occur. Quantifying the energetic costs arising from heat stress represents an important challenge for future investigations.
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                Author and article information

                Contributors
                nlow@stanford.edu
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                14 February 2020
                14 February 2020
                2020
                : 10
                Affiliations
                [1 ]ISNI 0000000419368956, GRID grid.168010.e, Hopkins Marine Station, , Stanford University, ; Pacific Grove, CA 93950 USA
                [2 ]Stanford Center for Ocean Solutions, Pacific Grove, CA 93950 USA
                Article
                59483
                10.1038/s41598-020-59483-5
                7021826
                32060309
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                Funding
                Funded by: FundRef https://doi.org/10.13039/100000001, National Science Foundation (NSF);
                Award ID: DEB-1212124
                Award ID: DEB-1722513
                Award Recipient :
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                © The Author(s) 2020

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                climate-change ecology, ecophysiology

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