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      Are lizards sensitive to anomalous seasonal temperatures? Long-term thermobiological variability in a subtropical species

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          Abstract

          Alterations in thermal niches have been widely associated with the Anthropocene erosion of reptiles’ diversity. They entail potential physiological constraints for organisms’ performance, which can lead to activity restrictions and impact fitness and demography. Reptiles are ectotherms which rely on seasonal periodicity to maximize the performance of biological functions. Despite it, the ecological implications of shifts in local temperatures are barely explored at the seasonal scale. This study aims to assess how changes in air temperature and substrate temperature affect the activity, body temperature ( T b) and thermoregulation patterns of the sand lizard, Liolaemus arambarensis (an endangered, microendemic species from southern Brazil), throughout a four-year period. Field surveys were conducted monthly on a restricted population in a sand-dune habitat. The annual fluctuations of the seasonal temperatures led to significant changes in the activity and T b of L. arambarensis and shaped thermoregulation trends, suggesting biological plasticity as a key factor in the face of such variability. Lizards tended to maintain seasonal T b in mild and harsh seasons through increased warming/cooling efforts. Anomalous winter conditions seemed especially critical for individual performance due to their apparent high impact favouring/constraining activity. Activity and thermoregulation were inhibited in frigid winters, probably due to a vulnerable physiology to intense cold spells determined by higher preferred body temperatures than T b. Our results warn of a complex sensitivity in lizards to anomalous seasonal temperatures, which are potentially enhanced by climate change. The current work highlights the importance of multiannual biomonitoring to disentangle long-term responses in the thermal biology of reptiles and, thereby, to integrate conservation needs in the scope of global change.

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          The Global Decline of Reptiles, Déjà Vu Amphibians

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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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              Multiple dimensions of climate change and their implications for biodiversity.

              The 21st century is projected to witness unprecedented climatic changes, with greater warming often reported for high latitudes. Yet, climate change can be measured in a variety of ways, reflecting distinct dimensions of change with unequal spatial patterns across the world. Polar climates are projected to not only warm, but also to shrink in area. By contrast, today's hot and arid climates are expected to expand worldwide and to reach climate states with no current analog. Although rarely appreciated in combination, these multiple dimensions of change convey complementary information. We review existing climate change metrics and discuss how they relate to threats and opportunities for biodiversity. Interpreting climate change metrics is particularly useful for unknown or poorly described species, which represent most of Earth's biodiversity.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: VisualizationRole: Writing – review & editing
                Role: InvestigationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                19 December 2019
                2019
                : 14
                : 12
                : e0226399
                Affiliations
                [1 ] Programa de Pós–Graduação em Biologia Animal, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil
                [2 ] Programa de Pós–Graduação em Ecologia, Departamento de Ecologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil
                Wildlife Conservation Society Canada, CANADA
                Author notes

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

                [¤]

                Current address: CIBIO/InBIO, Research Center in Biodiversity and Genetic Resources, University of Porto, Vairão, Portugal

                Author information
                http://orcid.org/0000-0001-6131-5194
                http://orcid.org/0000-0002-1931-8022
                Article
                PONE-D-19-19184
                10.1371/journal.pone.0226399
                6922334
                31856183
                0ce70fa8-6374-4d4f-ad51-8b6495e9c487
                © 2019 Vicente Liz 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
                : 8 July 2019
                : 26 November 2019
                Page count
                Figures: 6, Tables: 2, Pages: 16
                Funding
                This work was supported by research fellowships from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil ( http://www.capes.gov.br / Postgraduate scholarship – AVL; and Postdoctoral scholarship – MG; financial code 001). Financial support was provided by the Universidade Federal do Rio Grande do Sul – Postgraduate program in Animal Biology ( https://www.ufrgs.br/ppgban/); the European Commission through the program Erasmus Mundus Master Course – International Master in Applied Ecology ( http://www.emmc-imae.org/); and the Celulose Riograndense ( http://cmpcbrasil.com.br/). 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
                Physiology
                Physiological Parameters
                Body Temperature
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
                Body Temperature
                Earth Sciences
                Seasons
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Reptiles
                Squamates
                Lizards
                Earth Sciences
                Seasons
                Spring
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Reptiles
                Earth Sciences
                Seasons
                Winter
                Biology and Life Sciences
                Zoology
                Reptile Biology
                Biology and Life Sciences
                Psychology
                Behavior
                Animal Behavior
                Foraging
                Social Sciences
                Psychology
                Behavior
                Animal Behavior
                Foraging
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Foraging
                Custom metadata
                All field data used in this study are available from the Digital Library of the Universidade Federal do Rio Grande do Sul (LUME - UFRGS; https://lume.ufrgs.br/) and the website of the Herpetology Lab at Universidade Federal do Rio Grande do Sul ( http://www.ufrgs.br/herpetologia/).

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