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      Heat tolerance and acclimation capacity in subterranean arthropods living under common and stable thermal conditions


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          Cave‐dwelling ectotherms, which have evolved for millions of years under stable thermal conditions, could be expected to have adjusted their physiological limits to the narrow range of temperatures they experience and to be highly vulnerable to global warming. However, most of the few existing studies on thermal tolerance in subterranean invertebrates highlight that despite the fact that they show lower heat tolerance than most surface‐dwelling species, their upper thermal limits are generally not adjusted to ambient temperature. The question remains to what extent this pattern is common across subterranean invertebrates. We studied basal heat tolerance and its plasticity in four species of distant arthropod groups (Coleoptera, Diplopoda, and Collembola) with different evolutionary histories but under similar selection pressures, as they have been exposed to the same constant environmental conditions for a long time. Adults were exposed at different temperatures for 1 week to determine upper lethal temperatures. Then, individuals from previous sublethal treatments were transferred to a higher temperature to determine acclimation capacity. Upper lethal temperatures of three of the studied species were similar to those reported for other subterranean species (between 20 and 25°C) and widely exceeded the cave temperature (13–14°C). The diplopod species showed the highest long‐term heat tolerance detected so far for a troglobiont (i.e., obligate subterranean) species (median lethal temperature after 7 days exposure: 28°C) and a positive acclimation response. Our results agree with previous studies showing that heat tolerance in subterranean species is not determined by environmental conditions. Thus, subterranean species, even those living under similar climatic conditions, might be differently affected by global warming.


          Heat tolerance and acclimation capacity were studied in four subterranean species of distant arthropod groups but living under similar selection pressures (exposed to the same constant environmental conditions for a long time). Upper thermal limits widely exceeded ambient temperature and differed among the species, as well as acclimation responses. Our results show that heat tolerance in subterranean species is not determined by environmental conditions. Cave species, even those which live under similar climatic conditions, might be differently affected by global warming.

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          Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation.

          The concept of trade-offs is central to our understanding of life-history evolution. The underlying mechanisms, however, have been little studied. Oxidative stress results from a mismatch between the production of damaging reactive oxygen species (ROS) and the organism's capacity to mitigate their damaging effects. Managing oxidative stress is likely to be a major determinant of life histories, as virtually all activities generate ROS. There is a recent burgeoning of interest in how oxidative stress is related to different components of animal performance. The emphasis to date has been on immediate or short-term effects, but there is an increasing realization that oxidative stress will influence life histories over longer time scales. The concept of oxidative stress is currently used somewhat loosely by many ecologists, and the erroneous assumption often made that dietary antioxidants are necessarily the major line of defence against ROS-induced damage. We summarize current knowledge on how oxidative stress occurs and the different methods for measuring it, and highlight where ecologists can be too simplistic in their approach. We critically review the potential role of oxidative stress in mediating life-history trade-offs, and present a framework for formulating appropriate hypotheses and guiding experimental design. We indicate throughout potentially fruitful areas for further research.
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            Variation in the heat shock response and its implication for predicting the effect of global climate change on species' biogeographical distribution ranges and metabolic costs.

            L Tomanek (2010)
            The preferential synthesis of heat shock proteins (Hsps) in response to thermal stress [the heat shock response (HSR)] has been shown to vary in species that occupy different thermal environments. A survey of case studies of aquatic (mostly marine) organisms occupying stable thermal environments at all latitudes, from polar to tropical, shows that they do not in general respond to heat stress with an inducible HSR. Organisms that occupy highly variable thermal environments (variations up to >20 degrees C), like the intertidal zone, induce the HSR frequently and within the range of body temperatures they normally experience, suggesting that the response is part of their biochemical strategy to occupy this thermal niche. The highest temperatures at which these organisms can synthesize Hsps are only a few degrees Celsius higher than the highest body temperatures they experience. Thus, they live close to their thermal limits and any further increase in temperature is probably going to push them beyond those limits. In comparison, organisms occupying moderately variable thermal environments (<10 degrees C), like the subtidal zone, activate the HSR at temperatures above those they normally experience in their habitats. They have a wider temperature range above their body temperature range over which they can synthesize Hsps. Contrary to our expectations, species from highly (in comparison with moderately) variable thermal environments have a limited acclimatory plasticity. Due to this variation in the HSR, species from stable and highly variable environments are likely to be more affected by climate change than species from moderately variable environments.
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              The complex drivers of thermal acclimation and breadth in ectotherms

              Thermal acclimation capacity, the degree to which organisms can alter their optimal performance temperature and critical thermal limits with changing temperatures, reflects their ability to respond to temperature variability and thus might be important for coping with global climate change. Here, we combine simulation modelling with analysis of published data on thermal acclimation and breadth (range of temperatures over which organisms perform well) to develop a framework for predicting thermal plasticity across taxa, latitudes, body sizes, traits, habitats and methodological factors. Our synthesis includes > 2000 measures of acclimation capacities from > 500 species of ectotherms spanning fungi, invertebrates, and vertebrates from freshwater, marine and terrestrial habitats. We find that body size, latitude, and methodological factors often interact to shape acclimation responses and that acclimation rate scales negatively with body size, contributing to a general negative association between body size and thermal breadth across species. Additionally, we reveal that acclimation capacity increases with body size, increases with latitude (to mid-latitudinal zones) and seasonality for smaller but not larger organisms, decreases with thermal safety margin (upper lethal temperature minus maximum environmental temperatures), and is regularly underestimated because of experimental artefacts. We then demonstrate that our framework can predict the contribution of acclimation plasticity to the IUCN threat status of amphibians globally, suggesting that phenotypic plasticity is already buffering some species from climate change.

                Author and article information

                Ecol Evol
                Ecol Evol
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                04 December 2019
                December 2019
                : 9
                : 24 ( doiID: 10.1002/ece3.v9.24 )
                : 13731-13739
                [ 1 ] Marine Biology and Ecology Research Centre School of Biological and Marine Sciences University of Plymouth Plymouth UK
                [ 2 ] Instituto de Ciencias Ambientales Universidad de Castilla‐La Mancha Toledo Spain
                [ 3 ] Departamento de Ecología e Hidrología Universidad de Murcia Murcia Spain
                [ 4 ] Grupo de Espeleología de Villacarrillo Jaén Spain
                [ 5 ] Zoological Research Museum Alexander Koenig Bonn Germany
                [ 6 ] Institut de Biologia Evolutiva (CSIC‐UPF) Barcelona Spain
                Author notes
                [*] [* ] Correspondence

                Susana Pallarés, Marine Biology and Ecology Research Centre, School of Biological and Marine Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK.

                Email: susana.pallares@ 123456um.es

                Author information
                © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                : 30 July 2019
                : 06 October 2019
                : 08 October 2019
                Page count
                Figures: 3, Tables: 1, Pages: 9, Words: 7501
                Funded by: Spanish Ministry of Economy and Competitiveness and Fondo Europeo de Desarrollo Regional, FEDER , open-funder-registry 10.13039/501100003329;
                Award ID: CGL2016‐76995‐P
                Original Research
                Original Research
                Custom metadata
                December 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.4 mode:remove_FC converted:10.01.2020

                Evolutionary Biology
                climate change,physiological plasticity,subterranean biology,troglobiont,upper lethal temperature


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