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      The combined effects of reactant kinetics and enzyme stability explain the temperature dependence of metabolic rates

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          Abstract

          A mechanistic understanding of the response of metabolic rate to temperature is essential for understanding thermal ecology and metabolic adaptation. Although the Arrhenius equation has been used to describe the effects of temperature on reaction rates and metabolic traits, it does not adequately describe two aspects of the thermal performance curve ( TPC) for metabolic rate—that metabolic rate is a unimodal function of temperature often with maximal values in the biologically relevant temperature range and that activation energies are temperature dependent. We show that the temperature dependence of metabolic rate in ectotherms is well described by an enzyme‐assisted Arrhenius ( EAAR) model that accounts for the temperature‐dependent contribution of enzymes to decreasing the activation energy required for reactions to occur. The model is mechanistically derived using the thermodynamic rules that govern protein stability. We contrast our model with other unimodal functions that also can be used to describe the temperature dependence of metabolic rate to show how the EAAR model provides an important advance over previous work. We fit the EAAR model to metabolic rate data for a variety of taxa to demonstrate the model's utility in describing metabolic rate TPCs while revealing significant differences in thermodynamic properties across species and acclimation temperatures. Our model advances our ability to understand the metabolic and ecological consequences of increases in the mean and variance of temperature associated with global climate change. In addition, the model suggests avenues by which organisms can acclimate and adapt to changing thermal environments. Furthermore, the parameters in the EAAR model generate links between organismal level performance and underlying molecular processes that can be tested for in future work.

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          Most cited references42

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          Integrating Thermal Physiology and Ecology of Ectotherms: A Discussion of Approaches

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            Systematic variation in the temperature dependence of physiological and ecological traits.

            To understand the effects of temperature on biological systems, we compile, organize, and analyze a database of 1,072 thermal responses for microbes, plants, and animals. The unprecedented diversity of traits (n = 112), species (n = 309), body sizes (15 orders of magnitude), and habitats (all major biomes) in our database allows us to quantify novel features of the temperature response of biological traits. In particular, analysis of the rising component of within-species (intraspecific) responses reveals that 87% are fit well by the Boltzmann-Arrhenius model. The mean activation energy for these rises is 0.66 ± 0.05 eV, similar to the reported across-species (interspecific) value of 0.65 eV. However, systematic variation in the distribution of rise activation energies is evident, including previously unrecognized right skewness around a median of 0.55 eV. This skewness exists across levels of organization, taxa, trophic groups, and habitats, and it is partially explained by prey having increased trait performance at lower temperatures relative to predators, suggesting a thermal version of the life-dinner principle-stronger selection on running for your life than running for your dinner. For unimodal responses, habitat (marine, freshwater, and terrestrial) largely explains the mean temperature at which trait values are optimal but not variation around the mean. The distribution of activation energies for trait falls has a mean of 1.15 ± 0.39 eV (significantly higher than rises) and is also right-skewed. Our results highlight generalities and deviations in the thermal response of biological traits and help to provide a basis to predict better how biological systems, from cells to communities, respond to temperature change.
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              Increased temperature variation poses a greater risk to species than climate warming

              Increases in the frequency, severity and duration of temperature extremes are anticipated in the near future. Although recent work suggests that changes in temperature variation will have disproportionately greater effects on species than changes to the mean, much of climate change research in ecology has focused on the impacts of mean temperature change. Here, we couple fine-grained climate projections (2050-2059) to thermal performance data from 38 ectothermic invertebrate species and contrast projections with those of a simple model. We show that projections based on mean temperature change alone differ substantially from those incorporating changes to the variation, and to the mean and variation in concert. Although most species show increases in performance at greater mean temperatures, the effect of mean and variance change together yields a range of responses, with temperate species at greatest risk of performance declines. Our work highlights the importance of using fine-grained temporal data to incorporate the full extent of temperature variation when assessing and projecting performance.
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                Author and article information

                Contributors
                jpdelong@unl.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                23 April 2017
                June 2017
                : 7
                : 11 ( doiID: 10.1002/ece3.2017.7.issue-11 )
                : 3940-3950
                Affiliations
                [ 1 ] School of Biological SciencesUniversity of Nebraska – Lincoln Lincoln NEUSA
                [ 2 ]Present address: The University of California, Merced Merced CAUSA
                Author notes
                [*] [* ] Correspondence

                J. P. DeLong, School of Biological Sciences, University of Nebraska – Lincoln, Lincoln, NE, USA.

                Email: jpdelong@ 123456unl.edu

                Author information
                http://orcid.org/0000-0003-0558-8213
                Article
                ECE32955
                10.1002/ece3.2955
                5468145
                28616189
                5303dcb9-d1f2-4eba-b850-eaf2d8818709
                © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 12 December 2016
                : 28 February 2017
                : 07 March 2017
                Page count
                Figures: 5, Tables: 0, Pages: 11, Words: 8340
                Funding
                Funded by: United States‐Israel Binational Science Foundation
                Award ID: 2014295
                Funded by: Directorate for Biological Sciences
                Award ID: 1501668
                Award ID: 1505247
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece32955
                June 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.1.1 mode:remove_FC converted:12.06.2017

                Evolutionary Biology
                acclimation,metabolic rate,thermal adaptation,thermal performance curve
                Evolutionary Biology
                acclimation, metabolic rate, thermal adaptation, thermal performance curve

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