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      Physiological Limits along an Elevational Gradient in a Radiation of Montane Ground Beetles

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          Abstract

          A central challenge in ecology and biogeography is to determine the extent to which physiological constraints govern the geographic ranges of species along environmental gradients. This study tests the hypothesis that temperature and desiccation tolerance are associated with the elevational ranges of 12 ground beetle species (genus Nebria) occurring on Mt. Rainier, Washington, U.S.A. Species from higher elevations did not have greater cold tolerance limits than lower-elevation species (all species ranged from -3.5 to -4.1°C), despite a steep decline in minimum temperature with elevation. Although heat tolerance limits varied among species (from 32.0 to 37.0°C), this variation was not generally associated with the relative elevational range of a species. Temperature gradients and acute thermal tolerance do not support the hypothesis that physiological constraints drive species turnover with elevation. Measurements of intraspecific variation in thermal tolerance limits were not significant for individuals taken at different elevations on Mt. Rainier, or from other mountains in Washington and Oregon. Desiccation resistance was also not associated with a species’ elevational distribution. Our combined results contrast with previously-detected latitudinal gradients in acute physiological limits among insects and suggest that other processes such as chronic thermal stress or biotic interactions might be more important in constraining elevational distributions in this system.

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          Most cited references22

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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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            Are species' range limits simply niche limits writ large? A review of transplant experiments beyond the range.

            Many species' range limits (RL) occur across continuous environmental gradients without obvious barriers imposing them. Such RL are expected to reflect niche limits (NL) and thus to occur where populations cease to be self-sustaining. Transplant experiments comparing fitness within and beyond species' ranges can test this hypothesis, but interpretive power depends strongly on experimental design. We first identify often overlooked aspects of transplant design that are critical to establishing the causes of RL, especially incorporating transplant sites at, and source populations from, the range edge. We then conduct a meta-analysis of published beyond-range transplant experiments (n = 11 tests). Most tests (75%) found that performance declined beyond the range, with the strongest declines detected when the measure of performance was lifetime fitness (83%), suggesting that RL commonly involve niche constraints (declining habitat quality). However, only 46% supported range limits occurring at NL; 26% (mostly geographic RL) fell short of NL with self-sustaining transplants beyond the range, and 23% (all elevational RL) exceeded NL with range-edge populations acting as demographic sinks. These data suggest an important but divergent role for dispersal, which may commonly constrain geographic distributions while extending elevational limits. Meta-analysis results also supported the importance of biotic interactions at RL, particularly the long-held assertion of their role in causing low-elevation and equatorial limits.
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              Insect thermal tolerance: what is the role of ontogeny, ageing and senescence?

              Temperature has dramatic evolutionary fitness consequences and is therefore a major factor determining the geographic distribution and abundance of ectotherms. However, the role that age might have on insect thermal tolerance is often overlooked in studies of behaviour, ecology, physiology and evolutionary biology. Here, we review the evidence for ontogenetic and ageing effects on traits of high- and low-temperature tolerance in insects and show that these effects are typically pronounced for most taxa in which data are available. We therefore argue that basal thermal tolerance and acclimation responses (i.e. phenotypic plasticity) are strongly influenced by age and/or ontogeny and may confound studies of temperature responses if unaccounted for. We outline three alternative hypotheses which can be distinguished to propose why development affects thermal tolerance in insects. At present no studies have been undertaken to directly address these options. The implications of these age-related changes in thermal biology are discussed and, most significantly, suggest that the temperature tolerance of insects should be defined within the age-demographics of a particular population or species. Although we conclude that age is a source of variation that should be carefully controlled for in thermal biology, we also suggest that it can be used as a valuable tool for testing evolutionary theories of ageing and the cellular and genetic basis of thermal tolerance.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                4 April 2016
                2016
                : 11
                : 4
                : e0151959
                Affiliations
                [1 ]School of Biosciences, University of Melbourne, Parkville, Australia
                [2 ]Bio21 Institute, University of Melbourne, Parkville, Australia
                [3 ]Department of Entomology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America
                University of Cincinnati, UNITED STATES
                Author notes

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

                Conceived and designed the experiments: RAS SDS. Performed the experiments: RAS. Analyzed the data: RAS SDS. Contributed reagents/materials/analysis tools: SDS. Wrote the paper: RAS SDS.

                Article
                PONE-D-15-52091
                10.1371/journal.pone.0151959
                4820226
                27043311
                56273185-a5e4-4790-9d1e-11803ecfef8b
                © 2016 Slatyer, Schoville

                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
                : 30 November 2015
                : 6 March 2016
                Page count
                Figures: 5, Tables: 2, Pages: 19
                Funding
                Funding was provided by a National Geographic Young Explorer’s Grant to RAS (#9502-14), a Seattle City Light Wildlife Research Grant to SDS (#2014-03), the University of Melbourne and the University of Wisconsin. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Beetles
                Biology and Life Sciences
                Zoology
                Entomology
                Insect Physiology
                Biology and Life Sciences
                Zoology
                Animal Physiology
                Invertebrate Physiology
                Insect Physiology
                Earth Sciences
                Atmospheric Science
                Meteorology
                Humidity
                Research and Analysis Methods
                Research Facilities
                Weather Stations
                Biology and Life Sciences
                Biogeography
                Ecology and Environmental Sciences
                Biogeography
                Earth Sciences
                Geography
                Biogeography
                Biology and Life Sciences
                Ecology
                Ecological Niches
                Ecology and Environmental Sciences
                Ecology
                Ecological Niches
                Biology and Life Sciences
                Physiology
                Physiological Parameters
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
                Custom metadata
                All relevant data are within the paper and its Supporting Information files. Genetic data have been published at NCBI Genbank (accession numbers KU641243-KU641255).

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