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      Temperature-driven response reversibility and short-term quasi-acclimation of Daphnia magna

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          Abstract

          Analysing the effect water temperature has on Daphnia magna is essential in anticipating the impact climate change will have on this freshwater zooplanktonic keystone species. While many authors have followed this line of research, few have covered an extensive temperature range or complex temperature change scenarios. Global warming is mostly associated with increased extreme temperature events, such as heat waves, as well as earlier and more intense thermal stratification. Both of these events may directly influence D. magna fitness, especially in those populations performing diel vertical migration (DVM). We analysed the effect water temperatures, ranging from 11 to 29°C, have on the filtration capacity (FC) of D. magna, to anticipate the effects of acclimation, temperature change rate (TCR) and potential reversibility of responses to such conditions. Results show that sudden temperature changes have an immediate negative impact on the FC of D. magna and is more severe at higher temperatures and higher TCRs. However, D. magna individuals have shown themselves to be capable of quasi-acclimating to temperatures ranging from 11 to 25°C in around a week and achieving much higher FCs; albeit never reaching the optimal FC achieved at 20°C. That said, 29°C is lethal for D. magna individuals within approximately five days. Finally, non-optimal temperature acclimated individuals can recover maximal FC within 2–4 days of the optimal long-term acclimation temperature (20°C) being re-established, thus proving temperature responses to be reversible.

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          Most cited references53

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          Ecology. Physiology and climate change.

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            Climate change and evolution: disentangling environmental and genetic responses.

            Rapid climate change is likely to impose strong selection pressures on traits important for fitness, and therefore, microevolution in response to climate-mediated selection is potentially an important mechanism mitigating negative consequences of climate change. We reviewed the empirical evidence for recent microevolutionary responses to climate change in longitudinal studies emphasizing the following three perspectives emerging from the published data. First, although signatures of climate change are clearly visible in many ecological processes, similar examples of microevolutionary responses in literature are in fact very rare. Second, the quality of evidence for microevolutionary responses to climate change is far from satisfactory as the documented responses are often - if not typically - based on nongenetic data. We reinforce the view that it is as important to make the distinction between genetic (evolutionary) and phenotypic (includes a nongenetic, plastic component) responses clear, as it is to understand the relative roles of plasticity and genetics in adaptation to climate change. Third, in order to illustrate the difficulties and their potential ubiquity in detection of microevolution in response to natural selection, we reviewed the quantitative genetic studies on microevolutionary responses to natural selection in the context of long-term studies of vertebrates. The available evidence points to the overall conclusion that many responses perceived as adaptations to changing environmental conditions could be environmentally induced plastic responses rather than microevolutionary adaptations. Hence, clear-cut evidence indicating a significant role for evolutionary adaptation to ongoing climate warming is conspicuously scarce.
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              Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals.

              The physiological mechanisms limiting and adjusting cold and heat tolerance have regained interest in the light of global warming and associated shifts in the geographical distribution of ectothermic animals. Recent comparative studies, largely carried out on marine ectotherms, indicate that the processes and limits of thermal tolerance are linked with the adjustment of aerobic scope and capacity of the whole animal as a crucial step in thermal adaptation on top of parallel adjustments at the molecular or membrane level. In accordance with Shelford's law of tolerance decreasing whole animal aerobic scope characterises the onset of thermal limitation at low and high pejus thresholds (pejus=getting worse). The drop in aerobic scope of an animal indicated by falling oxygen levels in the body fluids and or the progressively limited capacity of circulatory and ventilatory mechanisms. At high temperatures, excessive oxygen demand causes insufficient oxygen levels in the body fluids, whereas at low temperatures the aerobic capacity of mitochondria may become limiting for ventilation and circulation. Further cooling or warming beyond these limits leads to low or high critical threshold temperatures (T(c)) where aerobic scope disappears and transition to an anaerobic mode of mitochondrial metabolism and progressive insufficiency of cellular energy levels occurs. The adjustments of mitochondrial densities and their functional properties appear as a critical process in defining and shifting thermal tolerance windows. The finding of an oxygen limited thermal tolerance owing to loss of aerobic scope is in line with Taylor's and Weibel's concept of symmorphosis, which implies that excess capacity of any component of the oxygen delivery system is avoided. The present study suggests that the capacity of oxygen delivery is set to a level just sufficient to meet maximum oxygen demand between the average highs and lows of environmental temperatures. At more extreme temperatures only time limited passive survival is supported by anaerobic metabolism or the protection of molecular functions by heat shock proteins and antioxidative defence. As a corollary, the first line of thermal sensitivity is due to capacity limitations at a high level of organisational complexity, i.e. the integrated function of the oxygen delivery system, before individual, molecular or membrane functions become disturbed. These interpretations are in line with the more general consideration that, as a result of the high level of complexity of metazoan organisms compared with simple eukaryotes and then prokaryotes, thermal tolerance is reduced in metazoans. A similar sequence of sensitivities prevails within the metazoan organism, with the highest sensitivity at the organismic level and wider tolerance windows at lower levels of complexity. However, the situation is different in that loss in aerobic scope and progressive hypoxia at the organismic level define the onset of thermal limitation which then transfers to lower hierarchical levels and causes cellular and molecular disturbances. Oxygen limitation contributes to oxidative stress and, finally, denaturation or malfunction of molecular repair, e.g. during suspension of protein synthesis. The sequence of thermal tolerance limits turns into a hierarchy, ranging from systemic to cellular to molecular levels.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Writing – original draft
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Formal analysisRole: MethodologyRole: ResourcesRole: SupervisionRole: Visualization
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                21 December 2018
                2018
                : 13
                : 12
                : e0209705
                Affiliations
                [001]Department of Physics, University of Girona, Girona, Spain
                VIT University, INDIA
                Author notes

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

                Author information
                http://orcid.org/0000-0001-6547-1004
                http://orcid.org/0000-0002-9330-0269
                Article
                PONE-D-18-27453
                10.1371/journal.pone.0209705
                6303020
                30576390
                b8411b66-0ef9-43f8-9afc-411694470c62
                © 2018 Müller et al

                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
                : 19 September 2018
                : 10 December 2018
                Page count
                Figures: 3, Tables: 2, Pages: 14
                Funding
                This work was supported by the University of Girona funding MPCUdG2016 and by the INNOQUA project from the European Union’s Horizon 2020 research and innovation program (Ares2016-1770486) to MFM, TS, and JC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Physical Sciences
                Chemistry
                Chemical Elements
                Oxygen
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Plankton
                Zooplankton
                Daphnia
                Earth Sciences
                Marine and Aquatic Sciences
                Bodies of Water
                Lakes
                Ecology and Environmental Sciences
                Aquatic Environments
                Freshwater Environments
                Lakes
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Freshwater Environments
                Lakes
                Earth Sciences
                Hydrology
                Surface Water
                Earth Sciences
                Atmospheric Science
                Climatology
                Climate Change
                Biology and Life Sciences
                Physiology
                Biological Locomotion
                Swimming
                Medicine and Health Sciences
                Physiology
                Biological Locomotion
                Swimming
                Ecology and Environmental Sciences
                Aquatic Environments
                Freshwater Environments
                Fresh Water
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Freshwater Environments
                Fresh Water
                Earth Sciences
                Atmospheric Science
                Climatology
                Climate Change
                Global Warming
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information file.

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