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Response Diversity in Mediterranean Coralligenous Assemblages Facing Climate Change: Insights from a Multispecific Thermotolerance Experiment

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Response Diversity in Mediterranean Coralligenous Assemblages Facing Climate Change: Insights from a Multispecific Thermotolerance Experiment Received: 10 October 2018 | Revised: 25 January 2019 | Accepted: 15 February 2019 DOI: 10.1002/ece3.5045 ORIGINAL RESEARCH Response diversity in Mediterranean coralligenous assemblages facing climate change: Insights from a multispecific thermotolerance experiment Daniel Gómez‐Gras1 | Cristina Linares2 | Sonia de Caralt3,4 | Emma Cebrian3,4 | Maša Frleta‐Valić1 | Ignasi Montero‐Serra2 | Marta Pagès‐Escolà2 | Paula López‐Sendino1 | Joaquim Garrabou1 1Departament de Biologia Marina, Institut de Ciències del Mar (CSIC), Barcelona, Spain Abstract 2Departament de Biologia Evolutiva, Climate change threatens coastal benthic communities on a global scale. However, Ecologia i Ciències Ambientals, the potential effects of ongoing warming on mesophotic temperate reefs at the com‐ Institut de Recerca de la Biodiversitat (IRBIO), Universitat de Barcelona, Barcelona, munity level remain poorly understood. Investigating how different members of Spain these communities will respond to the future expected environmental conditions is, 3Centre d' Estudis Avançats de Blanes (CSIC), Blanes, Spain therefore, key to anticipating their future trajectories and developing specific man‐ 4GR MAR, Institut d’Ecologia Aquàtica, agement and conservation strategies. Here, we examined the responses of some of Facultat de Ciències, Universitat de Girona, the main components of the highly diverse Mediterranean coralligenous assemblages Girona, Spain to thermal stress. We performed thermotolerance experiments with different tem‐ Correspondence perature treatments (from 26 to 29°C) with 10 species from different phyla (three Daniel Gómez‐Gras, Departament de Biologia Marina, Institut de Ciències del Mar anthozoans, six sponges and one ascidian) and different structural roles. Overall, we (CSIC), Barcelona, Spain. observed species‐specific contrasting responses to warming regardless of phyla or Email: [email protected] growth form. Moreover, the responses ranged from highly resistant species to sensi‐ Funding information tive species and were mostly in agreement with previous field observations from Organismo Autónomo Parques Nacionales, Grant/Award Number: CORCLIM mass mortality events (MMEs) linked to Mediterranean marine heat waves. Our re‐ 759S/2012 and CORCLIM 766S/2012; sults unravel the diversity of responses to warming in coralligenous outcrops and H2020 European Research Council, Grant/ Award Number: MERCES/689518; Prince suggest the presence of potential winners and losers in the face of climate change. Albert II de Monaco Foundation, Grant/ Finally, this study highlights the importance of accounting for species‐specific vulner‐ Award Number: MIMOSA/1983; European Regional Development Fund, Grant/Award abilities and response diversity when forecasting the future trajectories of temperate Number: Interreg MED programme and benthic communities in a warming ocean. MPA-ADAPT; Total Foundation, Grant/ Award Number: CLIMCARES . Ministerio de Educación, Cultura y Deporte, Grant/Award KEYWORDS Number: FPU15/05457 Benthic communities, corals, ocean warming, sponges, temperate reefs, thermotolerance 1 | INTRODUCTION organization (Doney et al., 2012; Poloczanska et al., 2016; Scheffers et al., 2016). Moreover, this anthropogenic pressure will continue to From polar oceans to tropical seas, climate change dramatically affects cause unprecedented impacts in the oceans during the next decades marine ecosystems by influencing processes at all levels of biological as global sea surface temperatures continue to rise and marine heat This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2019;1–13. www.ecolevol.org | 1 2 | GÓMEZ‐GRAS ET AL. waves become more frequent and intense (Bellard, Bertelsmeier, exhibit slow population dynamics and long life spans (+100 years; Leadley, Thuiller, & Courchamp, 2012; Oliver et al., 2018). However, Garrabou & Harmelin, 2002; Linares, Doak, Coma, Diaz, & Zabala, climate change effects have contrasting impacts on biotas (McKinney 2007; Teixidó, Garrabou, & Harmelin, 2011); therefore, they are very & Lockwood, 1999). Therefore, understanding how different species, sensitive to disturbances, including climate change (Balata, Piazzi, populations and communities will respond to warming is key to de‐ & Benedetti-Cecchi, 2007; Ferrigno, Appolloni, Russo, & Sandulli, veloping specific conservation and management strategies aimed at 2018; Garrabou et al., 2009; Montero-Serra et al., 2015). In fact, enhancing the resilience of vulnerable marine ecosystems. more than 30 coralligenous species from different phyla and dif‐ Coastal benthic communities such as tropical and temperate ferent structural roles have been affected in various mass mortal‐ reefs are among the most biologically diverse and socioeconomi‐ ity events (hereafter MMEs) associated with Mediterranean heat cally valuable systems on the planet (Ballesteros, 2006; Bennett et waves, suffering extensive tissue necrosis (partial and total mortal‐ al., 2016; Spalding, Ravilious, & Green, 2001). Nonetheless, when ity) and long‐term population declines (Cerrano et al., 2000; Crisci, facing global warming, they are especially under threat. As migrat‐ Bensoussan, Romano, & Garrabou, 2011; Garrabou et al., 2009; ing toward more thermally suitable conditions is not an option for Garrabou, Perez, Sartoretto, & Harmelin, 2001; Linares et al., 2005). most sessile species, most organisms from these communities will Moreover, for some key habitat‐forming species, these population be compelled to rely on effective acclimatization (an adjustment of declines have been shown to potentially drive detrimental effects at physiology via phenotypic plasticity) or adaptation (an increased the community level, such as the reduction of structural complexity abundance of tolerant genotypes over generations) processes to and resilience (Linares et al., 2017; Ponti et al., 2014). However, while prevail. Although these two mechanisms that evolved for coping some species have been massively and recurrently affected during with environmental change will likely allow diverse species and/or these warming events, other taxonomically and morpho‐functionally populations to persist (Palumbi, Barshis, Traylor-Knowles, & Bay, related organisms seem to remain unaffected, triggering the ques‐ 2014), increasing evidence indicates that the unusually high rates tion of whether there could be different levels of thermal sensitiv‐ of warming and the increasing frequency of extreme events may ity within these communities in the context of climate change. This prevent many others from effectively doing so (Heron et al., 2017; could have further implications for the future composition of these Hoegh-Guldberg, Poloczanska, Skirving, & Dove, 2017; Hughes et habitats and the loss (or maintenance) of the many associated func‐ al., 2017, 2018). In this situation, it is likely that as temperatures con‐ tions and services they provide. tinue to rise species with lower thermal thresholds will more fre‐ In this study, we experimentally assessed the thermal response quently be exposed to temperatures beyond their tolerance limits of 10 abundant, representative and widely distributed species from (especially during marine heat waves), potentially hindering adap‐ these communities that belong to different phyla and encompass con‐ tion/acclimatization processes and favoring responses that range trasting growth forms. The main aim was to explore whether co‐oc‐ from sublethal effects to death and local extinction (Somero, 2010). curring species of these highly diverse habitats differ in their thermal The likely loss of such sensitive species would not only change the sensitivities, as field observations suggest, in view to discuss the impli‐ composition of benthic communities but also diminish the functions cations of climate change on the composition and functioning of these and services that they provide. However, if there is response diver‐ key Mediterranean habitats. Our results contribute to filling the gap of sity among functionally redundant organisms, the insurance hypoth‐ thermotolerance data for coralligenous assemblages and suggest the esis of biodiversity suggests that the overall ecosystem functionality presence of potential winners and losers in the face of ocean warming. may be stabilized through compensatory dynamics among species (Gonzalez & Loreau, 2009; Mori, Furukawa, & Sasaki, 2013; Yachi 2 | MATERIALS AND METHODS & Loreau, 1999). Exploring species-specific thermal sensitivities among different components of benthic communities is, therefore, 2.1 | Model species a key step toward forecasting the future composition and function‐ ality of these communities in the face of climate change. However, We used a total of 10 abundant and representative species from while important efforts in this direction have been taken in shallow three different phyla (cnidaria, porifera, and tunicata) and four differ‐ tropical reefs, thermotolerance analyses in temperate benthic com‐ ent growth forms (including encrusting, massive, cup and/or tree‐like munities largely lag behind (Kersting et al., 2015; Linares, Cebrian, forms) that are commonly and ubiquitously found in Mediterranean Kipson, & Garrabou, 2013; Savva, Bennett, Roca, Jordà, & Marbà, coralligenous assemblages over the whole Mediterranean
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