Live Fast, Die Young: Experimental Evidence of Population Extinction Risk due to Climate Change

RESEARCH ARTICLE Live Fast, Die Young: Experimental Evidence of Population Extinction Risk due to Climate Change Elvire Bestion1,2,3*, Aimeric Teyssier2,4, Murielle Richard1, Jean Clobert1, Julien Cote2* 1 CNRS USR 2936, Station d'Ecologie Expérimentale de Moulis, Moulis, France, 2 CNRS, Université Toulouse III Paul Sabatier, ENFA; UMR5174 EDB (Laboratoire Évolution & Diversité Biologique), Toulouse, France, 3 Environmental and Sustainability Institute, College of Life and Environmental Sciences, University of Exeter, Penryn, United Kingdom, 4 Terrestrial Ecology Unit, Ghent University, Ghent, Belgium * (EB); (JC) Abstract OPEN ACCESS Citation: Bestion E, Teyssier A, Richard M, Clobert J, Cote J (2015) Live Fast, Die Young: Experimental Evidence of Population Extinction Risk due to Climate Change. PLoS Biol 13(10): e1002281. doi:10.1371/ journal.pbio.1002281 Academic Editor: Georgina M Mace, University College London, UNITED KINGDOM Received: July 13, 2015 Accepted: September 17, 2015 Published: October 26, 2015 Copyright: © 2015 Bestion 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. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Raw data are available as supporting S1 data and S2 data. Funding: This work was supported by the French Laboratory of Excellence project "TULIP" (ANR-10LABX-41; ANR-11-IDEX-0002-02) and by an ANR12-JSV7-0004-01 to JCo. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Evidence has accumulated in recent decades on the drastic impact of climate change on biodiversity. Warming temperatures have induced changes in species physiology, phenology, and have decreased body size. Such modifications can impact population dynamics and could lead to changes in life cycle and demography. More specifically, conceptual frameworks predict that global warming will severely threaten tropical ectotherms while temperate ectotherms should resist or even benefit from higher temperatures. However, experimental studies measuring the impacts of future warming trends on temperate ectotherms' life cycle and population persistence are lacking. Here we investigate the impacts of future climates on a model vertebrate ectotherm species using a large-scale warming experiment. We manipulated climatic conditions in 18 seminatural populations over two years to obtain a present climate treatment and a warm climate treatment matching IPCC predictions for future climate. Warmer temperatures caused a faster body growth, an earlier reproductive onset, and an increased voltinism, leading to a highly accelerated life cycle but also to a decrease in adult survival. A matrix population model predicts that warm climate populations in our experiment should go extinct in around 20 y. Comparing our experimental climatic conditions to conditions encountered by populations across Europe, we suggest that warming climates should threaten a significant number of populations at the southern range of the distribution. Our findings stress the importance of experimental approaches on the entire life cycle to more accurately predict population and species persistence in future climates. Author Summary Ongoing climate change has potentially drastic impacts on biodiversity. Because their body temperature depends on their external environment, ectotherm (“cold-blooded”) species are thought to be more at risk from warming climates than endotherm (“warmblooded”) species that regulate their temperature internally. Tropical ectotherms should PLOS Biology | DOI:10.1371/journal.pbio.1002281 October 26, 2015 1 / 19 Experimental Evidence of Population Extinctions from Climate Change Abbreviations: IPCC, Intergovernmental Panel on Climate Change; RCP, Representative Concentration Pathway; PCV, proportion change in variance; SE, Standard Error. be particularly threatened by climate change, while temperate ectotherms should resist or even benefit from higher temperatures. While most of the evidence on the impacts of climate change comes from long-term field studies, experimental evidence of the impact of future climatic conditions is still lacking. Here we investigate the impacts of future climates on a temperate lizard using a seminatural warming experiment. We find that warmer temperatures led to a highly accelerated life cycle and a decrease in adult survival. As a result, we postulate that populations in such warm climates would be expected to go extinct in around 20 y. Comparing our experimental conditions to climatic conditions in European populations of common lizards, we show that many populations should be threatened in the next century, particularly in Southern Europe. Our findings challenge the optimistic view that climate change is only a threat for tropical ectotherms and stress the importance of experimental approaches to predicting the consequences of future warming trends. Introduction Over the last decades, consequences of global warming on biodiversity have become obvious [1–3], with many species likely to be committed to extinction by 2050 [4]. Climate warming has already led to changes in species phenology [1], physiology (increased metabolic rates [5]), morphology (shrinking body size [6]), life cycle demography [7], and distribution [1], and, as a consequence, in community structure [8]. Because their body temperature, and hence their basic physiological functions, directly depend on environmental conditions, ectotherms are particularly at risk with climate change [5], while the number of studies assessing their response to changing climate is far lower than for endotherms [9]. The evaluation of their vulnerability is therefore urgent. For instance, a recent study predicted local extinctions of populations from various lizard families worldwide to reach 39% by 2080 due to climate change [10]. Theoretical studies predict that climate change will principally threaten tropical ectotherms [11–14], while temperate ectotherms should resist or even benefit from the warmer temperatures [13,15–17]. However, most evidence on the impacts of climate change on species comes from long-term field survey data [1,8], or on the contrary, on short term laboratory experiments lacking ecological realism and complexity [18–20]. Despite the growing evidence on the strong impact of ecological context on species adaptation to temperature [21], there is little large scale realistic experimental evidence on animals, especially on vertebrates [20,22–25]. More importantly, to our knowledge, the impact of climate change on a species’ entire life cycle and population persistence has never been experimen (...truncated)