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      Interactions between rates of temperature change and acclimation affect latitudinal patterns of warming tolerance

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          Abstract

          Rates of temperature change and thermal acclimation can alter measures of temperature tolerance. Using new experimental data on springtails and data from the literature, we show that these factors interact and have consequences for estimates of organismal vulnerability to climate change at global scales.

          Abstract

          Critical thermal limits form an increasing component of the estimation of impacts of global change on ectotherms. Whether any consistent patterns exist in the interactive effects of rates of temperature change (or experimental ramping rates) and acclimation on critical thermal limits and warming tolerance (one way of assessing sensitivity to climate change) is, however, far from clear. Here, we examine the interacting effects of ramping rate and acclimation on the critical thermal maxima (CTmax) and minima (CTmin) and warming tolerance of six species of springtails from sub-tropical, temperate and polar regions. We also provide microhabitat temperatures from 26 sites spanning 5 years in order to benchmark environmentally relevant rates of temperature change. Ramping rate has larger effects than acclimation on CTmax, but the converse is true for CTmin. Responses to rate and acclimation effects are more consistent among species for CTmax than for CTmin. In the latter case, interactions among ramping rate and acclimation are typical of polar species, less marked for temperate ones, and reduced in species from the sub-tropics. Ramping rate and acclimation have substantial effects on estimates of warming tolerance, with the former being more marked. At the fastest ramping rates (>1.0°C/min), tropical species have estimated warming tolerances similar to their temperate counterparts, whereas at slow ramping rates (<0.4°C/min) the warming tolerance is much reduced in tropical species. Rates of temperate change in microhabitats relevant to the springtails are typically <0.05°C/min, with rare maxima of 0.3–0.5°C/min depending on the site. These findings emphasize the need to consider the environmental setting and experimental conditions when assessing species’ vulnerability to climate change using a warming tolerance approach.

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          Most cited references23

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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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            Why tropical forest lizards are vulnerable to climate warming.

            Biological impacts of climate warming are predicted to increase with latitude, paralleling increases in warming. However, the magnitude of impacts depends not only on the degree of warming but also on the number of species at risk, their physiological sensitivity to warming and their options for behavioural and physiological compensation. Lizards are useful for evaluating risks of warming because their thermal biology is well studied. We conducted macrophysiological analyses of diurnal lizards from diverse latitudes plus focal species analyses of Puerto Rican Anolis and Sphaerodactyus. Although tropical lowland lizards live in environments that are warm all year, macrophysiological analyses indicate that some tropical lineages (thermoconformers that live in forests) are active at low body temperature and are intolerant of warm temperatures. Focal species analyses show that some tropical forest lizards were already experiencing stressful body temperatures in summer when studied several decades ago. Simulations suggest that warming will not only further depress their physiological performance in summer, but will also enable warm-adapted, open-habitat competitors and predators to invade forests. Forest lizards are key components of tropical ecosystems, but appear vulnerable to the cascading physiological and ecological effects of climate warming, even though rates of tropical warming may be relatively low.
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              Phylogenetic approaches in comparative physiology.

              Over the past two decades, comparative biological analyses have undergone profound changes with the incorporation of rigorous evolutionary perspectives and phylogenetic information. This change followed in large part from the realization that traditional methods of statistical analysis tacitly assumed independence of all observations, when in fact biological groups such as species are differentially related to each other according to their evolutionary history. New phylogenetically based analytical methods were then rapidly developed, incorporated into ;the comparative method', and applied to many physiological, biochemical, morphological and behavioral investigations. We now review the rationale for including phylogenetic information in comparative studies and briefly discuss three methods for doing this (independent contrasts, generalized least-squares models, and Monte Carlo computer simulations). We discuss when and how to use phylogenetic information in comparative studies and provide several examples in which it has been helpful, or even crucial, to a comparative analysis. We also consider some difficulties with phylogenetically based statistical methods, and of comparative approaches in general, both practical and theoretical. It is our personal opinion that the incorporation of phylogeny information into comparative studies has been highly beneficial, not only because it can improve the reliability of statistical inferences, but also because it continually emphasizes the potential importance of past evolutionary history in determining current form and function.
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                Author and article information

                Journal
                Conserv Physiol
                Conserv Physiol
                conphys
                conphys
                Conservation Physiology
                Oxford University Press
                2051-1434
                2016
                09 November 2016
                : 4
                : 1
                : cow053
                Affiliations
                [1 ]Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University , Private Bag X1, Matieland 7602, South Africa
                [2 ]School of Biological Sciences, Monash University , Clayton, VIC 3800, Australia
                Author notes
                [* ] Corresponding author: Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa. Tel: +27 21 8083976. Email: sct333@ 123456sun.ac.za

                Editor: Steven Cooke

                Article
                cow053
                10.1093/conphys/cow053
                5142048
                27933165
                e70bda11-f9d7-4b2e-9e5f-05a63d2a6f41
                © The Author 2016. Published by Oxford University Press and the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 3 June 2016
                : 11 October 2016
                : 17 October 2016
                Funding
                Funded by: National Research Foundation of South Africa;
                Categories
                Research Article

                climate change,ectotherms,macrophysiology,phenotypic plasticity,thermal tolerance

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