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      Assessing Mammal Exposure to Climate Change in the Brazilian Amazon

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          Abstract

          Human-induced climate change is considered a conspicuous threat to biodiversity in the 21 st century. Species’ response to climate change depends on their exposition, sensitivity and ability to adapt to novel climates. Exposure to climate change is however uneven within species’ range, so that some populations may be more at risk than others. Identifying the regions most exposed to climate change is therefore a first and pivotal step on determining species’ vulnerability across their geographic ranges. Here, we aimed at quantifying mammal local exposure to climate change across species’ ranges. We identified areas in the Brazilian Amazon where mammals will be critically exposed to non-analogue climates in the future with different variables predicted by 15 global circulation climate forecasts. We also built a null model to assess the effectiveness of the Amazon protected areas in buffering the effects of climate change on mammals, using an innovative and more realistic approach. We found that 85% of species are likely to be exposed to non-analogue climatic conditions in more than 80% of their ranges by 2070. That percentage is even higher for endemic mammals; almost all endemic species are predicted to be exposed in more than 80% of their range. Exposure patterns also varied with different climatic variables and seem to be geographically structured. Western and northern Amazon species are more likely to experience temperature anomalies while northeastern species will be more affected by rainfall abnormality. We also observed an increase in the number of critically-exposed species from 2050 to 2070. Overall, our results indicate that mammals might face high exposure to climate change and that protected areas will probably not be efficient enough to avert those impacts.

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          Most cited references16

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          Climate change, deforestation, and the fate of the Amazon.

          The forest biome of Amazonia is one of Earth's greatest biological treasures and a major component of the Earth system. This century, it faces the dual threats of deforestation and stress from climate change. Here, we summarize some of the latest findings and thinking on these threats, explore the consequences for the forest ecosystem and its human residents, and outline options for the future of Amazonia. We also discuss the implications of new proposals to finance preservation of Amazonian forests.
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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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              The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming.

              Increasing concern about the impacts of global warming on biodiversity has stimulated extensive discussion, but methods to translate broad-scale shifts in climate into direct impacts on living animals remain simplistic. A key missing element from models of climatic change impacts on animals is the buffering influence of behavioral thermoregulation. Here, we show how behavioral and mass/energy balance models can be combined with spatial data on climate, topography, and vegetation to predict impacts of increased air temperature on thermoregulating ectotherms such as reptiles and insects (a large portion of global biodiversity). We show that for most "cold-blooded" terrestrial animals, the primary thermal challenge is not to attain high body temperatures (although this is important in temperate environments) but to stay cool (particularly in tropical and desert areas, where ectotherm biodiversity is greatest). The impact of climate warming on thermoregulating ectotherms will depend critically on how changes in vegetation cover alter the availability of shade as well as the animals' capacities to alter their seasonal timing of activity and reproduction. Warmer environments also may increase maintenance energy costs while simultaneously constraining activity time, putting pressure on mass and energy budgets. Energy- and mass-balance models provide a general method to integrate the complexity of these direct interactions between organisms and climate into spatial predictions of the impact of climate change on biodiversity. This methodology allows quantitative organism- and habitat-specific assessments of climate change impacts.
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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
                9 November 2016
                2016
                : 11
                : 11
                : e0165073
                Affiliations
                [1 ]Laboratório de Biogeografia da Conservação, Departamento de Ecologia, Universidade Federal de Goiás, Goiânia, Goiás, Brazil
                [2 ]Programa de Pós-graduação em Ecologia e Evolução, Universidade Federal de Goiás, Goiânia, Goiás, Brazil
                [3 ]Laboratório de Metacomunidades e Ecologia de Paisagens, Departamento de Ecologia, Universidade Federal de Goiás, Goiânia, Goiás, Brazil
                [4 ]Brazilian Research Network on Climate Change–Rede Clima. Instituto Nacional de Pesquisas Espaciais, São José dos Campos, São Paulo, Brazil
                Sichuan University, CHINA
                Author notes

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

                • Conceptualization: BRR RL PDMJ LPS.

                • Data curation: BRR.

                • Formal analysis: BRR LPS.

                • Funding acquisition: RL.

                • Methodology: BRR.

                • Project administration: BRR.

                • Resources: RL.

                • Supervision: RL.

                • Visualization: BRR RL LPS PDMJ.

                • Writing – original draft: BRR.

                • Writing – review & editing: BRR RL LPS PDMJ.

                Article
                PONE-D-16-28419
                10.1371/journal.pone.0165073
                5102461
                27829036
                bb5179d0-f0f2-4755-9319-0e20a13117d8
                © 2016 Ribeiro et al

                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
                : 15 July 2016
                : 5 October 2016
                Page count
                Figures: 3, Tables: 1, Pages: 13
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 308532/2014-7
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 479959/2013-7
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 407094/2013-0
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 563621/2010-9
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 550022/2014-7
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004809, Financiadora de Estudos e Projetos;
                Award ID: 01.13.0353.00
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100009472, Fundação Grupo Boticário de Proteção à Natureza;
                Award ID: PROG_0008_2013
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 131170/2014-7
                Award Recipient :
                BRR and LPS are supported by Conselho Nacional para o Desenvolvimento Científico e Tecnológico ( www.cnpq.br) and Coordenação de Aperfeiçoamento de Nível Superior ( www.capes.gov.br) scholarships, respectively. RL research has been constantly funded by CNPq (grants #308532/2014-7, 479959/2013-7, 407094/2013-0, 563621/2010-9), O Boticário Group Foundation for the Protection of Nature (grant #PROG_0008_2013), and CNCFlora. This paper is a contribution of the Brazilian Network on Global Climate Change Research funded by CNPq (grant #437167/2016-0) and FINEP (grant #01.13.0353.00). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Earth Sciences
                Atmospheric Science
                Climatology
                Climate Change
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Ecology and Environmental Sciences
                Conservation Science
                Earth Sciences
                Atmospheric Science
                Atmospheric Chemistry
                Greenhouse Gases
                Physical Sciences
                Chemistry
                Environmental Chemistry
                Atmospheric Chemistry
                Greenhouse Gases
                Ecology and Environmental Sciences
                Environmental Chemistry
                Atmospheric Chemistry
                Greenhouse Gases
                Biology and Life Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Ecology and Environmental Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Biology and Life Sciences
                Ecology
                Ecosystems
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Biology and Life Sciences
                Ecology
                Biodiversity
                Ecology and Environmental Sciences
                Ecology
                Biodiversity
                Biology and Life Sciences
                Conservation Biology
                Species Extinction
                Ecology and Environmental Sciences
                Conservation Science
                Conservation Biology
                Species Extinction
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Species Extinction
                Custom metadata
                Species distribution data for all terrestrial mammals were downloaded from http://www.iucnredlist.org/technical-documents/spatial-data; the authors selected only mammals present in the Brazilian Amazon. This proceed is described in “Species data” in the Material and Methods section. Climate data were downloaded from http://www.worldclim.org/version1. Data on Protected Areas were downloaded from http://mapas.mma.gov.br/i3geo/datadownload.htm; the authors selected 'Areas Especiais', then 'Unidades de Conservação' and downloaded data from federal, state, and municipal levels.

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