Abstract Refugia can facilitate the persistence of biodiversity under changing environmental conditions, such as anthropogenic climate change, and therefore constitute the best chance of survival for many coral species in the wild. Despite an increasing amount of literature, the concept of coral reef refugia remains poorly defined; so that climate change refugia have been confused with other phenomena, including temporal refuges, pristine habitats and physiological processes such as adaptation and acclimatization. We propose six criteria that determine the capacity of refugia to facilitate species persistence, including long-term buffering, protection from multiple climatic stressors, accessibility, microclimatic heterogeneity, size, and low exposure to non-climate disturbances. Any effective, high-capacity coral reef refugium should be characterized by long-term buffering of environmental conditions (for several decades) and multi-stressor buffering (provision of suitable environmental conditions with respect to climatic change, particularly ocean warming and acidification). Although not always essential, the remaining criteria are important for quantifying the capacity of potential refugia. Introduction Coral reefs worldwide are severely threatened by human activities (Burke et al., 2011). Increasing carbon emissions as a result of human activities are driving global change, warming and acidifying oceans worldwide (Hoegh-Guldberg et al., 2007; van Hooidonk et al., 2014). This is exacerbating existing stressors and is predicted to seriously threaten the persistence of these ecosystems, with large-scale coral reef destruction and degradation, and species extinctions, predicted by the end of this century (Hoegh-Guldberg et al., 2007; Carpenter et al., 2008; Hughes et al., 2017). However, refugia have facilitated survival of coral reefs and related biodiversity in the past (Greenstein and Pandolfi, 2008; Pellissier et al., 2014; Smith et al., 2014) and may do so again in the future, possibly providing the only hope of survival for many species. Refugia can retain environmental conditions suitable for particular species when regional or global changes cause surrounding areas to become inhospitable (Ashcroft, 2010; Stewart et al., 2010; Keppel et al., 2012). For example, during the last glacial maximum (LGM) refugia with warmer climates facilitated the persistence of Eurasian and North American terrestrial biota (Stewart et al., 2010; Fedorov and Stenseth, 2002). In southern Australia, persistence during drier glacial periods was facilitated by refugia providing moister conditions (Byrne, 2008). Refugia therefore have the potential to facilitate the persistence of species threatened by anthropogenic climate change (Ashcroft, 2010; Loarie et al., 2008; Keppel and Wardell-Johnson, 2012). Thus, refugia are considered important tools in conservation planning in both marine and terrestrial ecosystems (Keppel et al., 2015; Gattuso et al., 2015). In the past few years, the concept of climate change refugia has been widely applied in terrestrial environments to identify and prioritize important refugia for conservation planning under future anthropogenic climate change (Ashcroft, 2010; Loarie et al., 2008; Keppel et al., 2015; Morelli et al., 2016). This has been achieved using data that is sufficiently fine-scaled for the target species, and applying that data in models to pinpoint refugia and quantify their capacity to buffer climate change (e.g. Keppel et al., 2015; Maher et al. 2017). Future (warmer climates) refugia have been found to be mostly different from those in the past (e.g., cooler climate during the LGM), with only limited geographic overlap (Mokany et al. 2017). Although climate change refugia for coral reefs were proposed at least 20 years ago (Glynn, 1996), our understanding of such refugia remains limited. Published literature in the field has been increasing (Supplementary Figure S1) but also reveals persistent confusion about the concept, with climate change refugia for coral reefs being poorly defined and mistakenly identified as reserves or short-term refuges. This, in our opinion, is complicating a targeted discussion and action to identify and protect the spots most likely to facilitate survival of coral reefs in rapidly changing oceans. In this paper, we explore and clarify confusion about refugia for coral reefs, outline the history of the concept of climate change refugia for coral reefs, and identify six criteria that characterize and determine the capacity of such refugia. What are climate change refugia for coral reefs? Keppel et al., (2012) define refugia as “habitats that components of biodiversity retreat to, persist in and can potentially expand from under changing environmental conditions”. Refugia are characterized by their ability to provide long-term (over several generations) mitigation of environmental changes that make surrounding areas unsuitable (Dobrowski, 2010; Keppel and Wardell-Johnson, 2012). For coral reefs, refugia should therefore be able to buffer regional changes in stressors related to climate change, in particular ocean temperature and acidity over decades or centuries (generation time for corals is species-specific and varies from about 4 to 40 years; Babcock, 1991; Carpenter et al., 2008), while providing other conditions conducive to coral growth and reproduction, for a large complement of corals and associated species. However, many studies investigating climate change refugia for coral reefs refer to different phenomena, such as refuges, pristine habitats and higher tolerance to environmental stress, suggesting persistent confusion about the concept of climate change refugia for coral reefs. Various concepts have been confused with refugia. Refuges are habitats that provide short-term spatial and/or temporal shelter from environmental stressors or advantages in biotic interactions (Keppel and Wardell-Johnson, 2012), and are therefore distinct from refugia which facilitate persistence of biota over several generations. For example, while storms can provide cooler waters, and hence reduce coral mortality during a single bleaching event (see Carrigan and Puotinen, 2014), they are unlikely to provide long-term protection. Therefore, cooler waters caused by storms and other intermittent phenomena (e.g. cloud cover: Mumby et al., 2001) provide temporary shelter from warmer ocean temperatures, but not long-term protection, and should be referred to as refuges. Pristine habitats, locations (such as remote coral reefs) that remain little impacted by direct human impacts, and marine reserves do not necessarily constitute coral reef refugia (Riegl and Piller, 2003; Darling et al., 2010; Gilmour et al. 2013; Hughes et al. 2017) because they do not necessarily provide protection from long-term environmental change, such as warming oceans. Such habitats should therefore be referred to as pristine habitats and reserves, respectively, and not be called “refugia”. In addition, higher tolerance of coral species to extreme climatic conditions (e.g. van Woesik et al., 2012), does not imply refugia—but populations that are better adapted to warmer temperatures. Therefore, lower bleaching and/or mortality rates in one location may result from the presence of refuges, pristine habitats, or populations with higher physiological tolerance and not necessarily from the presence of more favourable, stable environments (i.e. refugia). Although the ability of refugia to facilitate the persistence of species under anthropogenic climate change may be enhanced by such characteristics, their principal functionality would still be dependent on being able to mitigate key climate change stressors. History of the refugia concept for modern coral reefs In his pioneering work referring to coral reef refugia, Glynn (1996) suggested high latitudes, moderate depths and isolated reefs with vigorous currents may provide refugia from global warming. He, therefore, referred to habitats that consistently provided lower temperatures as refugia. However, Glynn (1996) did not provide a definition, or criteria, for refugia. As a result, any site with lower bleaching/mortality of corals than surrounding areas was often considered a refugium, regardless of the mechanisms causing this phenomenon (Supplementary Table S1). Riegl and Piller (2003) revisited the refugia proposed by Glynn (1996) but also did not define refugia. They used the presence of healthier coral reefs where cold currents have been reducing thermal stress as an indicator for the presence of potential refugia, which is reasonable. On the other hand, they focused on health status of offshore reefs as the main criterion for refugia. However, healthier (or more pristine) habitats do not necessarily imply long-term environmental stability (e.g. see Gilmour et al., 2013; Hughes et al., 2017). Riegl (2003) suggested that areas with “slower local climate change” and “historically most stressed areas” may provide refugia. Although the former indeed suggests refugia, the latter does not imply refugia, despite potentially facilitating higher coral survival during bleaching events as a result of higher physiological tolerances displayed by resident coral taxa. Salm et al. (2006) and others (e.g., Ateweberhan and McClanahan, 2010; Mumby et al., 2011) highlighted the importance of long-term favourable temperatures (stability) as a characteristic of refugia. However, this important criterion has hardly been applied to identify refugia for coral reef refugia in situ studies (Supplementary Table S1; but see van Hooidonk et al., 2013, 2014; Cacciapglia and van Woesik, 2015 for large-scale modelling approaches considering long-term temperature stability). Lack of long-term in situ monitoring data of relevant environmental parameters (e.g. temperature, acidity) has likely contributed to the implementation of misleading approaches (e.g. coral mortality during a single bleaching event) for identifying coral reef refugia (see Edmunds, 2013). Refugia have mostly been identified using coarse-scaled (>4 km) climate models, which mostly predict dramatic losses of coral reefs over entire regions by the end of the century (van Hooidonk et al., 2014; Freeman, 2015), with some potential large-scale refugia (Freeman, 2015). However, spatial variation in coral performance has been observed at finer scales (e.g. Swain et al., 2016). A holistic understanding of this fine-scale temperature and physiochemical variation within coral reefs would allow identifying and locating microrefugia but is currently lacking. Collecting such fine-scale (10 of metres) variation in relevant environmental variables would allow extrapolation and modelling of microenvironments over large areas, as has been done in terrestrial habitats (e.g. Ashcroft, 2010; Franklin et al., 2013). The first definition of refugia that was applied to coral reefs was “restricted areas in which plants and animals persisted during a period of … climatic change that made surrounding areas uninhabitable … later … might serve as a center of dispersal for the repopulation” (Riegl et al., 2009 from Neuendorf et al., 2005). Based on this definition Riegl et al. (2009) suggested that “refugia should be therefore characterized by bigger, more viable or more fertile populations than those in neighbouring, increasingly less suitable areas” and be connected to other reefs. Although such characteristics may indeed indicate refugia, they may also be the result of higher physiological tolerances or having benefitted from the existence of refuges. In recent years, the concept of refugia for coral reefs as long-term safe-havens from environmental stressors has been increasingly understood and implemented (Beger et al., 2014; Makino et al., 2014; Chollett et al., 2014). The importance of considering multiple climatic stressors, especially ocean warming and acidification, is also being increasingly considered (Couce et al., 2013; van Hooidonk et al., 2014; Freeman, 2015). However, the concept of climate change refugia for coral reefs continues to be misunderstood (Supplementary Table S1), possibly as a result of persisting confusion from earlier works. Criteria to identify climate change refugia Similar to terrestrial environments, long-term, reliable fine-scale environmental data will be key to identifying refugia for coral reefs (Keppel and Kavousi, 2015). For example, van Hooidonk et al. (2013) suggested that potential coral reef refugia in the Caribbean Sea will face annual bleaching only 5 years after the global median using 1° × 1° resolution data. However, using finer-scale data (i.e. 11 and 4 km) revealed areas that may provide protection for coral reefs for an additional 10–15 years (van Hooidonk et al., 2015). Refugia are taxon-specific, dynamic entities in space and time that may buffer different environmental conditions (Stewart et al., 2010; Keppel et al., 2012; Cacciapaglia and Woesik, 2015; Bongaerts et al., 2017). Therefore, high coral bleaching/mortality of one taxon at a given site (e.g. an upwelling site) does not exclude that site from being a refugium for other taxa or other sites (e.g. a different upwelling site with weaker/stronger currents) from constituting a refugia for that taxon. Furthermore, refugia differ in their capacity to facilitate taxon persistence (Keppel and Wardell-Johnson, 2015). This capacity is determined by the combined effect of several factors and related to the target taxon under consideration. We have used the term taxon here because coral populations of the same species may display different responses to climatic changes (McClanahan, 2004; Miller et al., 2011; Shamberger et al., 2014), implying that the taxonomic level that should be considered for the identification of refugia will vary depending on the circumstances. However, many coral taxa within a reef are likely to have similar or overlapping physiological requirements (Sheppard et al., 2009). Therefore, refugia could be defined for a single target taxon (based on its physiological limits) or a group of taxa (using their collective physiological requirements). Considering the high species diversity of coral reefs (Sheppard et al., 2009; Dubinsky and Stambler, 2011) protecting a single coral taxon may be of limited conservation value. Therefore, suitability for multiple coral taxa should be considered when identifying climate change refugia for coral reefs. From the literature, we propose six factors that define the capacity of refugia. These include long-term buffering, multi-stressor protection, accessibility, microclimatic heterogeneity, size and low exposure to other disturbances. Of these factors, long-term buffering and protection from multiple climatic stressors are essential for effective coral reef refugia from the impacts of anthropogenic climate change. The remaining factors play important roles in determining the capacity of coral reef refugia and hence for conservation planning. Long-term buffering Refugia must retain favourable environmental conditions as stress related to the impacts of climate change increases over the next decades (Mumby et al., 2011; Makino et al., 2014). However, refugia differ in their ability to buffer environmental stressors and should be considered as occurring along a continuum of different capacities (Keppel and Wardell-Johnson, 2015). The capacity of refugia to buffer changes in regional climate is very variable, with decoupling and stability being extreme cases (Figure 1). Decoupling is defined as the isolation of environmental conditions in a locality from regional changes (Dobrowski, 2010), meaning that environmental changes in refugia are not dictated by regional trends. Stability is an extreme form of decoupling and refers to a refugium maintaining near constant environmental conditions in the face of regional change. Figure 1. View largeDownload slide Schematic representation of the concepts of buffering, decoupling and stability with regard to refugia using temperature as an example. When regional temperatures change (solid line), any place providing consistently lower temperatures is buffering (shaded area) the regional trend can be considered a refugium of some kind. Any habitat that displays trends different from the regional trend is decoupled from the regional climate (dashed and dotted lines), while habitats maintaining near constant environmental conditions are considered stable (dotted lines). Figure 1. View largeDownload slide Schematic representation of the concepts of buffering, decoupling and stability with regard to refugia using temperature as an example. When regional temperatures change (solid line), any place providing consistently lower temperatures is buffering (shaded area) the regional trend can be considered a refugium of some kind. Any habitat that displays trends different from the regional trend is decoupled from the regional climate (dashed and dotted lines), while habitats maintaining near constant environmental conditions are considered stable (dotted lines). Decoupling and stability may be rare in marine ecosystems. Long-term, fine-scale studies of environmental conditions on reefs will be required to determine the existence, prevalence and extent of decoupling on coral reefs. Furthermore, a refugium that is stable now, or was so in the past, may not be stable in the future (Makino et al., 2014; Descombes et al., 2015). For example, it has been proposed that upwelling currents could potentially become weaker under ongoing global warming (Polovina et al., 2011; Vecchi et al., 2006 but see: McGregor et al., 2007). Therefore, refugia have limits to their ability of providing buffering environmental changes over time (Keppel and Wardell-Johnson, 2015). Thus, stability recorded in two previous coral bleaching events does not imply stability during future events, as this would depend on the intensity of temperature anomalies, impacts of other stressors and the capacity of refugia. For example, Phongsuwan and Chansang (2012) showed that several locations that had provided protection during previous bleaching events, failed to do so during a more intensive subsequent event (For more examples see Sheppard, 2009; Selig et al., 2010). Long-term buffering is important for both in situ (within the current distribution of the target taxa) and ex situ (outside the current range) coral refugia. Although some ex situ refugia, such as higher latitudes (Greenstein and Pandolfi, 2008), are not currently refugia for tropical species, they may become suitable as oceans warm (Beger et al., 2014). However, not every high latitude location can provide refugia for coral reefs (e.g. McClanahan et al., 2009). Only higher latitude refugia with high buffering are likely to provide important safe havens for tropical coral species that migrate poleward by providing locations that are suitable for longer time periods than surrounding habitat (c.f. Beger et al., 2014; Keppel and Wardell-Johnson, 2015). Protection from multiple climatic stressors Climate change is affecting global marine ecosystems including coral reefs in several ways, such as warming of ocean temperatures, ocean acidification, intensified storms, sea level rise, changing thermohaline circulation and ENSO patterns, changes to ocean stratification (Guinotte and Fabry, 2008; Hoegh-Guldberg and Bruno, 2010; Doney et al., 2012) and the exacerbation of existing biological threats such as diseases, invaders, eroders, and competitors (Maynard et al., 2015; Fabricius et al., 2011; Wernberg et al., 2013). An effective coral reef refugium should provide sufficient buffering from all the aforementioned climate-induced stressors to facilitate the persistence of the coral reef community (or the target taxon). In this context, ocean warming and acidification are likely to be particularly important. The combined effect and/or interactions of multiple stressors can have more profound and complex impacts on coral species than isolated stressors (Maina et al., 2008, 2011; Hughes and Connell, 1999; Ateweberhan et al., 2013). Therefore, multiple stressors, in particular at high intensities, reduce the ability of refugia to facilitate the persistence of species. However, magnitude and types of stressors may differ on fine scales (e.g. temperature within reefs; Guadayol et al., 2014). Even global stressors vary locally (e.g. sea level rise: Hu and Deser, 2013). Such fine-scale variation therefore needs to be considered when identifying refugia. Although refugia that protect coral reefs against multiple stressors are likely to be the most effective, refugia buffering only one key stressor (i.e. global warming or acidification) may still play important roles in facilitating the persistence of some species in certain locations. For example, a refugium protecting corals from warming (Riegl and Piller, 2003), but vulnerable to acidification, would increase the survival prospects of coral taxa tolerant to the direct impacts of acidification (e.g. Comeau et al., 2014). Furthermore, single-stressor refugia constitute the locations with the highest probability of survival for coral reefs communities that we can currently identify—until multi-stressor refugia are demonstrated and located. Additional criteria Accessibility Accessibility of refugia for target taxa is an important criterion for terrestrial (Keppel et al., 2015) and some coral reef refugia (Greenstein and Pandolfi, 2008; Bongaerts et al., 2010). Less isolated refugia have a greater chance of being reached by the target taxon (Keppel et al., 2015). However, accessibility may not be essential for every refugium. For example, a target species may already live inside a refugium. In such in situ refugia, high accessibility may constitute a disadvantage, as this may facilitate the arrival of invasive organisms, coral competitors, and predators to enter the refugia (e.g. Lesser and Slattery, 2011). On the other hand, accessibility is crucial for ex-situ refugia (e.g. higher latitudes). For a refugium to be effective, coral larvae will need to survive, settle and grow when conditions surrounding the refugium become inhospitable. Therefore, geographical, hydrological and biological barriers and availability of suitable substrates for coral larval settlement (Harriott and Banks, 2002; Walker, 2012; Walker and Gilliam, 2013) should be considered when assessing accessibility. However, some potential refugia (e.g. upwelling currents; Riegl and Piller, 2003) are associated with environmental conditions that are generally considered stressful for corals, e.g., high acidity and low temperatures in upwelling currents (Glynn, 1977; Manzello et al., 2008). Although corals existing under such conditions obviously have some adaptation, larvae of taxa migrating to such refugia may struggle to persist. Moreover, even environmental conditions that corals are adapted to may become stressful in interaction with other stressors (Ateweberhan et al., 2013). Therefore, understanding the role of local adaptation and acclimatization will be crucial for evaluating coral accessibility and persistence. Microclimatic heterogeneity Topographical complexity may create unique microclimates and greater heterogeneity. This implies greater chances of suitable microhabitats facilitating the persistence of target taxa (Keppel et al., 2015). Microclimatic heterogeneity is likely to increase the chances of survival for coral taxa, because the probability that a suitable climate will be present in close proximity at any point in time increases with increasing diversity of microclimates. Persistence in such microhabitats through adverse climatic events would also allow reseeding the reef. Indeed, internal waves and deeper parts of some coral reefs have been found to assist with the lower temperatures and subsequent lower bleaching rates of coral reefs (Wall et al., 2015; Smith et al., 2014). Size of refugia Size defines the ability of a refugium to sustain viable populations of target taxa (Gaston and Blackburn, 1996). Furthermore, habitats constituting refugia for multiple species are likely to be of higher conservation value than refugia for single species (Keppel et al., 2015). The protection of multiple species is also essential to retain functioning coral reefs in refugia. A larger refugium can support more species, larger populations and more genetic variation (Gaston and Blackburn, 1996; Palumbi, 1997) and is therefore likely to have a higher capacity to facilitate the long-term persistence of taxa and coral reefs. Low exposure to other disturbances Stressors not caused by climate change, such as habitat degradation, can have severe impacts. Although the effectiveness of a refugium depends mostly on its capacity to maintain or produce environmental conditions suitable for target taxa, it is also affected by other stressors. An increase in the intensity of secondary stressors would be expected to reduce the ability of coral habitat to facilitate the persistence of target taxa. Indeed, threats such as increased sedimentation and pollution have been found to degrade coral reefs directly and to amplify the impacts of climate change (Hoegh-Guldberg et al., 2007; Gattuso et al., 2015). Nonetheless, refugia of potentially high capacity may be found in places with high human impact, but secondary stressors resulting from this impact would need to be reduced or removed for this capacity to be realized. Conclusion Despite a noticeable increase in published papers over past two decades, considerable ambiguity around the concept of climate change refugia for coral reefs remains. This has produced persistent confusion with other processes, including short-term refuges, pristine habitats, and physiological adaptation. To improve clarity, we here proposed six criteria that characterize effective, high-capacity coral reef refugia. Of these criteria, long-term buffering and protection from multiple climatic stressors are essential properties of any effective refugium. However, the other criteria, such as accessibility, may also be important, even essential, for some refugia to be effective for certain target taxa. However, these additional criteria are only relevant, if a potential refugium meets the two key criteria. Given the rapid impacts of anthropogenic climate change on coral reefs, it will be important to identify refugia with the highest capacity. 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