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      Physiological constraints to climate warming in fish follow principles of plastic floors and concrete ceilings

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          Abstract

          Understanding the resilience of aquatic ectothermic animals to climate warming has been hindered by the absence of experimental systems experiencing warming across relevant timescales (for example, decades). Here, we examine European perch ( Perca fluviatilis, L.) from the Biotest enclosure, a unique coastal ecosystem that maintains natural thermal fluctuations but has been warmed by 5–10 °C by a nuclear power plant for over three decades. We show that Biotest perch grow faster and display thermally compensated resting cardiorespiratory functions compared with reference perch living at natural temperatures in adjacent waters. However, maximum cardiorespiratory capacities and heat tolerance limits exhibit limited or no thermal compensation when compared with acutely heated reference perch. We propose that while basal energy requirements and resting cardiorespiratory functions (floors) are thermally plastic, maximum capacities and upper critical heat limits (ceilings) are much less flexible and thus will limit the adaptive capacity of fishes in a warming climate.

          Abstract

          Understanding climatic adaptation in fish is limited by a lack of large-scale, long term acclimation studies. Here, Sandblom et al. show that fish exposed to a 5-10 °C increase in water temperature next to a nuclear power plant display contrasting upper and lower cardiorespiratory thermal compensation limits.

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          Most cited references9

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          Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation.

          Physiological thermal-tolerance limits of terrestrial ectotherms often exceed local air temperatures, implying a high degree of thermal safety (an excess of warm or cold thermal tolerance). However, air temperatures can be very different from the equilibrium body temperature of an individual ectotherm. Here, we compile thermal-tolerance limits of ectotherms across a wide range of latitudes and elevations and compare these thermal limits both to air and to operative body temperatures (theoretically equilibrated body temperatures) of small ectothermic animals during the warmest and coldest times of the year. We show that extreme operative body temperatures in exposed habitats match or exceed the physiological thermal limits of most ectotherms. Therefore, contrary to previous findings using air temperatures, most ectotherms do not have a physiological thermal-safety margin. They must therefore rely on behavior to avoid overheating during the warmest times, especially in the lowland tropics. Likewise, species living at temperate latitudes and in alpine habitats must retreat to avoid lethal cold exposure. Behavioral plasticity of habitat use and the energetic consequences of thermal retreats are therefore critical aspects of species' vulnerability to climate warming and extreme events.
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            Climate change effects on fishes and fisheries: towards a cause-and-effect understanding.

            Ongoing climate change is predicted to affect individual organisms during all life stages, thereby affecting populations of a species, communities and the functioning of ecosystems. These effects of climate change can be direct, through changing water temperatures and associated phenologies, the lengths and frequency of hypoxia events, through ongoing ocean acidification trends or through shifts in hydrodynamics and in sea level. In some cases, climate interactions with a species will also, or mostly, be indirect and mediated through direct effects on key prey species which change the composition and dynamic coupling of food webs. Thus, the implications of climate change for marine fish populations can be seen to result from phenomena at four interlinked levels of biological organization: (1) organismal-level physiological changes will occur in response to changing environmental variables such as temperature, dissolved oxygen and ocean carbon dioxide levels. An integrated view of relevant effects, adaptation processes and tolerance limits is provided by the concept of oxygen and capacity-limited thermal tolerance (OCLT). (2) Individual-level behavioural changes may occur such as the avoidance of unfavourable conditions and, if possible, movement into suitable areas. (3) Population-level changes may be observed via changes in the balance between rates of mortality, growth and reproduction. This includes changes in the retention or dispersion of early life stages by ocean currents, which lead to the establishment of new populations in new areas or abandonment of traditional habitats. (4) Ecosystem-level changes in productivity and food web interactions will result from differing physiological responses by organisms at different levels of the food web. The shifts in biogeography and warming-induced biodiversity will affect species productivity and may, thus, explain changes in fisheries economies. This paper tries to establish links between various levels of biological organization by means of addressing the effective physiological principles at the cellular, tissue and whole organism levels. © 2010 The Authors. Journal of Fish Biology © 2010 The Fisheries Society of the British Isles.
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              Plastic and evolutionary responses to climate change in fish

              The physical and ecological ‘fingerprints’ of anthropogenic climate change over the past century are now well documented in many environments and taxa. We reviewed the evidence for phenotypic responses to recent climate change in fish. Changes in the timing of migration and reproduction, age at maturity, age at juvenile migration, growth, survival and fecundity were associated primarily with changes in temperature. Although these traits can evolve rapidly, only two studies attributed phenotypic changes formally to evolutionary mechanisms. The correlation-based methods most frequently employed point largely to ‘fine-grained’ population responses to environmental variability (i.e. rapid phenotypic changes relative to generation time), consistent with plastic mechanisms. Ultimately, many species will likely adapt to long-term warming trends overlaid on natural climate oscillations. Considering the strong plasticity in all traits studied, we recommend development and expanded use of methods capable of detecting evolutionary change, such as the long term study of selection coefficients and temporal shifts in reaction norms, and increased attention to forecasting adaptive change in response to the synergistic interactions of the multiple selection pressures likely to be associated with climate change.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                17 May 2016
                2016
                : 7
                : 11447
                Affiliations
                [1 ]Department of Biological and Environmental Sciences, University of Gothenburg, Box 463 , Gothenburg 405 30, Sweden
                [2 ]University of Tasmania and CSIRO Agriculture Flagship , Tasmania, Hobart 7000, Australia
                [3 ]Department of Animal Environment and Health, Swedish University of Agricultural Sciences, Box 234 , Skara 532 23, Sweden
                [4 ]Department of Animal Ecology/Evolutionary Biology Centre, Uppsala University, Box 592 , Uppsala 751 24, Sweden
                [5 ]Department of Aquatic Resources, Institute of Coastal Research, Swedish University of Agricultural Sciences, Skolgatan 6 , Öregrund 742 42, Sweden
                [6 ]Department of Biology, Norwegian University of Science and Technology , Trondheim NO-7491, Norway
                Author notes
                Article
                ncomms11447
                10.1038/ncomms11447
                4873662
                27186890
                a74cec4b-f9d7-494b-80ad-3922d9072b87
                Copyright © 2016, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 18 June 2015
                : 24 March 2016
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