Interpreting the sign of coral bleaching as friend versus foe

Coral bleaching is a major concern to researchers, conservations and the general public worldwide. To date, much of the high profile attention for bleaching has coincided with major environmental impacts and for many the term coral bleaching is synonymously associated with coral mortality (so-called “lethal” bleaching episodes). Whilst this synonymous association has undoubtedly been key in raising public support, it carries unfair representation: non-lethal bleaching is, and always has been, a phenomenon that effectively occurs regularly in nature as corals acclimatize to regular periodic changes in growth environment (days, seasons etc). In addition, corals can exhibit sub-lethal bleaching during extreme environmental conditions whereby mortality does not occur and corals can potentially subsequently recover once ambient environmental conditions return. Perhaps not surprisingly it is the frequency and extent of these nonand sub-lethal processes that yield key evidence as to how coral species and reef systems will likely withstand environmental and thus climatic change. Observations of nonand sub-lethal bleaching (and subsequent recovery) are arguably not as readily reported as those of lethal bleaching since (1) the convenient tools used to quantify bleaching yield major ambiguity (and hence high potential for mis-identification) as to the severity of bleaching; and (2) lethal bleaching events inevitably receive higher profile (media) attention and so are more readily reported. Under-representation of nonand sub-lethal bleaching signs may over-classify the severity of bleaching, under-estimate the potential resilience of reefs against environmental change, and thus ultimately limit (ifnot depreciate) the validity and effectiveness of reef management policies and practices. Whilst bleaching induced coral mortality must remain our key concern it must be better placed within the context of bleaching signs that do not result in a long-term loss of reef viability. Introduction— Coral bleaching is a global phenomenon that continually draws widespread attention from both scientific and public arenas. Researchers strive to gain greater understanding of the fundamental mechanisms involved, variability that exists across species and geographical regions, and to refine models predicting likely impacts of future events towards reef susceptibility and resilience. Simultaneously, assessors, conservationists and managers have expanded our knowledge of both temporal and spatial variability in bleaching episodes and consequences for society. However, such widespread efforts have potentially come at a cost of how bleaching is uniformly perceived and thus the ultimate accuracy of conclusions returned of bleaching severity. Anyone can in essence detect coral bleaching since the term simply refers to coral discolouration, specifically through loss of pigmentation (from corals’ symbiotic microalgae, termed zooxanthellae, but also from the coral cnidarian host tissue) as well as loss of entire zooxanthellae cells from the cnidarian tissue (Brown 1997, Fitt et al. 2001, Smith et al. 2005). Importantly, “non-lethal” coral discoloration, and by inference coral bleaching, is and always has been a natural phenomenon that is driven by inherent system variability in environmental condition, such as temperature, light, sediment loading and salinity (Stimson 1997, Brown et al. 1999, Fagoonee et al. 1999, Fitt et al. 2000; also Lesser 2004, Baker et al. 2008; see Fig. 1) as well as biological interactions, including disease, and microbial and corallivore activity (Rosenberg et al. 2007, Rotjan & Lewis 2008). Bleaching is consequently a sign of numerous (not necessarily mutually exclusive) causative factors and in reality not straightforward to describe with a single underlying definition. For the purposes of this article we use the term bleaching to describe coral discolouration. Given the link between coral colouration and variability of environmental condition, it was perhaps inevitable that reports of coral bleaching episodes have increased over recent decades as reef environments have simultaneously experienced an unprecedented rate of environmental change (e.g. Lesser 2004, 2007, Hoegh-Guldberg et al. 2007, Baker et al. 2008). Importantly, an increase in the amplitude and frequency of environmental variability beyond that of the status quo, i.e. beyond average cycles of days, seasons etc., exacerbates coral bleaching (Hoegh-Guldberg et al 1999, Lesser 2007, see also Baker et al. 2008). Here, corals may be driven towards “sub-lethal” stress (e.g. Fitt & Warner 1995, Fitt et al. 2001, Fig. 1) whereby bleaching does not result in coral mortality and is ultimately reversible should ‘natural’ scales of environmental variability return for sufficient time (Fig. 1). Sub-lethal bleaching thus in essence affords some capacity to ride out periods of ‘stress’ (sensu Obura 2009). However, under the most extreme or rapid environmental change, corals exhibit an irreversible “end point” of the bleaching process, that of coral mortality. Extreme loss of coral zooxanthellae cells and/or host tissue necrosis occurs to leave only the bare underlying CaCO3 skeleton with no chance of recovery once favourable environmental conditions return. Such “lethal” bleaching induced coral mortality can result in negative cascade effects, via reductions to the net balance of reef accretion and the eventualchange in reef architecture that in turn impact reef form and function to the detriment of ecosystem diversity and service provision (e.g. Bellwood et al. 2006, Baker et al. 2008). Whilst these have direct consequences to the viability of populations directly dependent on reefs for subsistence, such cascades may further impact the aesthetic and diverse nature of reefs that ultimately generates income. It is thus not surprising that both local and international emphasis has been increasingly placed on detecting bleaching events that lead to coral mortality. Increased bleaching monitoring efforts have importantly increased the scales of data available to assess coral bleaching patterns (Spalding 2009); however, it is important to realise that all reports of bleaching are dependent upon what we, as both non-specialist assessors and specialist researchers, perceive to be bleached coral, i.e. nature, extent and severity. Impact afforded by both public and academic media reports is inextricably linked to consequence, and so bleaching events that result in coral mortality will inevitably gain more attention than non-lethal bleaching events associated with ‘natural’ environmental fluctuations. Less than ca. 5% of all scientific publications consider natural variability of coral bleaching (as of 1 November 2009 ISI Web Of Science, Thompson Scientific); thus knowledge transfer of the patterns and processes of bleaching from the academic arena to non-specialists is arguably already weighted towards a synonymous association of bleached corals with (impending) mortality. Such potential unfair representation should raise serious concerned, in particular where non-specialists must be increasingly responsible for locally collating data sets of coral bleaching that drive the management or policy decisions. It is undeniable that the common association between bleaching and mass coral mortality, in particular during recent thermal anomaly episodes, has been important for raising global support for reef research and conservation efforts. Following the ‘precautionary principle’ (see Raffensberger & Tickner 1999) to assume a worst case scenario following the appearance of signs of bleaching potentially supports initiation of at least some mitigation. However, understanding when bleaching is truly ‘a problem’ and not part of the current status quo is a critical step if we are to generate the most informed and ultimately most effective management decisions. Bleaching induced mass mortality events undoubtedly have a resounding impact upon reef viability and economics; however, it is important that observations of bleaching not detrimental to coral viability, i.e. those indicative of a positive physiological response by corals to a change of their growth environment, are not misinterpreted as impending mortality and consequently that a reef is in a ‘state of decline’. The aim of this opinion article is thus to briefly highlight how signs of coral bleaching manifest in nature. In particular, how the capacity for positively responding (acclimatizing, sensu Gates & Edmunds 1999) to environmental change via physiology and behaviour carries a sign of bleaching that may (1) on occasion be misinterpreted as a stress response preceding mortality; and in fact (2) inform of species/systems that can best withstand stress conditions. For this, we consider how commonly used non-invasive tools, that have been increasingly contributing to global data bases quantifying coral bleaching, can yield signals that can be interpreted as both non-lethal and (sub)lethal responses. We further briefly discuss the implications of potentially misinterpreting nonlethal bleaching as impending mortality. Importantly, this is not a review of the coral bleaching phenomenon (but we refer the reader to comprehensive reviews by Glynn 1996, Brown 1997, Hoegh-Guldberg 1999, Fitt et al. 2001, Smith et al. 2005, Baker et al. 2008, Weiss 2008 and Baird et al. 2009; see also van Oppen & Lough 2009) but instead a call (1) for more accurate interpretation and communication of the sign (and hence severity) of bleaching; in doing so, (2) to re-focus effortstowards nonand sub-lethal bleaching (including subsequent recovery), i.e. those phenomena that receive less attention and are perhaps less frequently reported, in understanding reef resilience under environmental change. Observing bleaching as evidence of impending mortality— The term bleaching can be used to describe a continuum from non-lethal to lethal episodes; thus, it is no wonde