Persistence and Change in Community Composition of Reef Corals through Present, Past, and Future Climates Peter J. Edmunds1*", Mehdi Adjeroud2,3, Marissa L. Baskett4, Iliana B. Baums5, Ann F. Budd6, Robert C. Carpenter1, Nicholas S. Fabina7, Tung-Yung Fan8, Erik C. Franklin9, Kevin Gross10, Xueying Han11,12, Lianne Jacobson1,13, James S. Klaus14, Tim R. McClanahan15, Jennifer K. O’Leary12, Madeleine J. H. van Oppen16, Xavier Pochon17, Hollie M. Putnam9, Tyler B. Smith18, Michael Stat19, Hugh Sweatman16, Robert van Woesik20, Ruth D. Gates9" 1 Department of Biology, California State University Northridge, Northridge, California, United States of America, 2 Institut de Recherche pour le De´veloppement, Unite´ de Recherche CoReUs, Observatoire Oce´anologique de Banyuls, Banyuls-sur-Mer, France, 3 Laboratoire d’Excellence "CORAIL", Perpignan, France, 4 Department of Environmental Science and Policy, University of California Davis, Davis, California, United States of America, 5 Department of Biology, The Pennsylvania State University, University Park, Pennsylvania, United States of America, 6 Department of Earth and Environmental Sciences, University of Iowa, Iowa City, Iowa, United States of America, 7 Center for Population Biology, University of California Davis, Davis, California, United States of America, 8 National Museum of Marine Biology and Aquarium, Taiwan, Republic of China, 9 Hawaii Institute of Marine Biology, School of Ocean and Earth Science and Technology, University of Hawaii, Kaneohe, Hawaii, United States of America, 10 Biomathematics Program, North Carolina State University, Raleigh, North Carolina, United States of America, 11 Department of Ecology, Evolution and Marine Biology and the Coastal Research Center, Marine Science Institute, University of California Santa Barbara, Santa Barbara, California, United States of America, 12 National Center for Ecological Analysis and Synthesis, Santa Barbara, California, United States of America, 13 Department of Biology, University of Florida, Gainesville, Florida, United States of America, 14 Department of Geological Sciences, University of Miami, Coral Gables, Florida, United States of America, 15 Wildlife Conservation Society, Marine Program, Bronx, New York, United States of America, 16 Australian Institute of Marine Science, Townsville, Queensland, Australia, 17 The Cawthron Institute, Nelson, New Zealand, 18 Center for Marine and Environmental Studies, University of the Virgin Islands, St. Thomas, Virgin Islands, United States of America, 19 The University of Western Australia Oceans Institute and the Centre for Microscopy, Characterisation and Analysis, University of Western Australia, Crawley, Western Australia, Australia, 20 Department of Biological Sciences, Florida Institute of Technology, Melbourne, Florida, United States of America Abstract The reduction in coral cover on many contemporary tropical reefs suggests a different set of coral community assemblages will dominate future reefs. To evaluate the capacity of reef corals to persist over various time scales, we examined coral community dynamics in contemporary, fossil, and simulated future coral reef ecosystems. Based on studies between 1987 and 2012 at two locations in the Caribbean, and between 1981 and 2013 at five locations in the Indo-Pacific, we show that many coral genera declined in abundance, some showed no change in abundance, and a few coral genera increased in abundance. Whether the abundance of a genus declined, increased, or was conserved, was independent of coral family. An analysis of fossil-reef communities in the Caribbean revealed changes in numerical dominance and relative abundances of coral genera, and demonstrated that neither dominance nor taxon was associated with persistence. As coral family was a poor predictor of performance on contemporary reefs, a trait-based, dynamic, multi-patch model was developed to explore the phenotypic basis of ecological performance in a warmer future. Sensitivity analyses revealed that upon exposure to thermal stress, thermal tolerance, growth rate, and longevity were the most important predictors of coral persistence. Together, our results underscore the high variation in the rates and direction of change in coral abundances on contemporary and fossil reefs. Given this variation, it remains possible that coral reefs will be populated by a subset of the present coral fauna in a future that is warmer than the recent past. Citation: Edmunds PJ, Adjeroud M, Baskett ML, Baums IB, Budd AF, et al. (2014) Persistence and Change in Community Composition of Reef Corals through Present, Past, and Future Climates. PLoS ONE 9(10): e107525. doi:10.1371/journal.pone.0107525 Editor: Erik Sotka, College of Charleston, United States of America Received May 21, 2013; Accepted August 20, 2014; Published October 1, 2014 Copyright: ß 2014 Edmunds 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. Funding: This work was conducted as part of the ‘‘Tropical coral reefs of the future: modeling ecological outcomes from the analyses of current and historical trends’’ Working Group (to RDG and PJE), and while RDG was a Center Fellow supported by the National Center for Ecological Analysis and Synthesis, both funded by NSF (Grant #EF-0553768), the University of California, Santa Barbara, and the State of California. The authors acknowledge additional support from NSF (OCE 04-17413 and 10-26851 to PJE and RCC, DEB 03-43570 and 08-51441 to PJE, OCE 07-52604 to RDG, OCE-1041673 for ECF, DEB 01-02544, 97-05199, EAR 92-19138, and 04-45789 to AFB), the US EPA (FP917096 to ECF and FP917199 to HMP), and a postdoctoral fellowship to MS from the UWA-AIMS-CSIRO collaborative agreement. 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. * Email: [email protected] " First and last author determined by organizational roles in the project, other authors listed alphabetically. Introduction coral survival is accelerating as a result of global climate change (GCC) and ocean acidification (OA) [2]. Many coral reefs have Most present-day coral reefs differ from the reefs that were first changed dramatically in benthic community structure over the last described by ecologists and explorers [1], and recent evidence few decades [3], but contemporary research has focused on suggests that the rate of change in environmental factors affecting PLOS ONE | www.plosone.org 1 October 2014 | Volume 9 | Issue 10 | e107525 Corals and Climate Change declining abundances of scleractinian corals rather than on the few insight into the potential ecological fate of coral reefs under cases where reefs have retained coral cover (or recovered following increased thermal stress (i.e., the Future). losses), and where some scleractinian corals have maintained or increased in abundance [4–6]. Present Coral reefs in remote settings provide some of the best examples of reefs with high coral cover and intact trophic structures [6–8], Recent efforts to describe changes in the composition of coral and their distance from localized anthropogenic effects suggest reef communities have typically focused on scleractinian corals isolation and protection, rather than global climate, are determi- and their performance relative to other functional groups such as nants of their present condition. In addition, coral reefs with macroalgae [19]. These efforts have brought attention to the large diverse scleractinian faunas and relatively high coral cover also can losses of coral cover that have taken place since the 1960s [20]. It is be found in marginal locations characterized by high temperature uncommon however, for such studies to explicitly focus on the fluctuations [9], thermal extremes [10], and turbidity [11]. extent to which coral taxa differ in the way they respond to climate Moreover, while many coral genera have declined in abundance, change, a characteristic that could play an important role in some persist in ecologically dominant roles, which have led to the determining the future community structure of coral reefs [21]. suggestion that corals on contemporary reefs can be categorized as One example of the value of such approaches is the analysis of ‘‘losers’’ or ‘‘winners’’ [12]. Massive Porites spp. is an example of a coral bleaching on the reefs of Okinawa in 1998, the results of group of corals that is faring better than others and is increasing in which allowed corals to be categorized based on whether they abundance in the Pacific and Caribbean [4,13], and also is survived (i.e., winners) or died (i.e., losers) on the short-term showing signs of resistance to OA, both in mesocosms [14] and in following the disturbance [12]. Analysis of the same community over 14 years revealed discrepancies between short-term and long- at least one reef environment where volcanic carbon dioxide seeps term winners, both in the trajectories of changing abundance as into the seawater [15]. well as in the demographic mechanisms underpinning those Considerable effort is being dedicated to elucidating the trajectories [22]. Nonetheless, understanding of the community processes driving shifts in coral community structure on contem- dynamics of a reef in Okinawa was well served by considering