Causes of coral bleaching

141 These contrasting results have stimulated further research, which has suggested differing levels of thermal stress tolerance and acclimatisation of particular coral taxa, or possibly entire reef communities, acquired from past stress exposures and/or local mitigating environmental, abiotic factors (e.g. shading, current speed, upwelling zones or depth;

Maynard et al. 2008; Brown and Cossins 2011)(section 1.6). Nevertheless, the capacity for stress resistance and bleaching resilience appears highly variable and limited, as evidenced by recent mass bleaching events that affected much of the occurring coral taxa, and a subsequent, marginal recovery of these systems (Grimsditch et al. 2006; Baird and Maynard 2008; Baker et al. 2008; Sheppard et al. 2008; Somerfield et al. 2008; Veron et al.

2009). Finally, the physiological capacity for stress acclimatisation may also be closely related to the actual type of active stressors, which will be addressed in more detail in the following sections.

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While thermal stress is viewed as the principal cause of coral bleaching, several other biotic and abiotic factors have been found to impact the stability of the symbiosis, including: reduced seawater temperatures (Muscatine et al. 1991; Gates et al. 1992;

Kobluk and Lysenko 1994; Saxby et al. 2003); supra-optimal levels of visible or ultraviolet radiation (Gleason and Wellington 1993; Lesser and Farrell 2004; Brown and Dunne 2008); ocean acidification (Anthony et al. 2008); salinity fluctuations (Meehan and Ostrander 1997; Kerswell and Jones 2003); bacterial infection (Rosenberg et al. 2009);

and cyanide exposure (Jones and Hoegh-Guldberg 1999). Hoegh-Guldberg (1999) added copper ions and pesticides, while Glynn (1996) included sub-aerial exposure, sedimentation, and oil as contributory factors.

However, of critical importance is that mass coral bleaching events, such as those recorded in 1998, 2002, 2005, and 2010 (Goreau et al. 2000; Berkelmans et al. 2004;

Guest et al. 2012) (section 1.1), have been associated with the effects of anthropogenic global warming (Hughes et al. 2003; Donner et al. 2005), which has resulted in a steady rise of marine baseline temperatures. Consequently, forecasts of warming events on a global scale such as the occurrence of El Niño events serve as early warning indicators of potential bleaching of wide areas of coral reefs. Likewise, a sudden drop in seawater temperature induced by either atmospheric chilling or intense upwelling may also result in coral bleaching across wide areas (Hoegh-Guldberg et al. 2005) and should be monitored and used as an early warning indicator. Finally, ocean acidification and changes in solar radiation have the potential to cause mass bleaching across large spatial scales as climate change occurs (Anthony et al 2008; Lesser 2011). These are indicators of long-term changes in coral reef communities and may be monitored with the use of time series data.

All the large scale stressors mentioned above and their combined effects may have dramatic consequences on the geographic extent, increasing frequency, and regional severity of future mass bleaching events.

Local stressors such as pollutants, nutrient loading or sedimentation result in localised bleaching events (tens to hundreds of kilometres) because of the constrained nature of the stress source. However, these can act synergistically by effectively lowering the threshold temperature at which coral bleaching occurs, thereby reducing coral resistance and resilience to global climate change (Lesser 2004; 2006; Wooldridge 2009; Carilli et al.

2012). Consequently, these local stressors should also be monitored as they can act as

143 indicators of subsequent bleaching events, especially if they occur simultaneously with high summer water temperatures.

While there is consensus in identifying the above described environmental drivers (e.g.

temperature, light) as (direct or indirect) causes of coral bleaching, the scientific community is not in agreement on the role of bacteria as potential causative agents of bleaching. Most coral biologists contend that changes in the microbial community of bleached corals are a mere result of the process. Indeed, during a bleaching event, coral-associated microbial communities show major shifts in their composition and metabolism (Bourne et al. 2007), with an increase in microorganisms capable of pathogenesis (Littman et al. 2011). This has been confirmed by reports that found a positive link between coral bleaching events and subsequent coral disease epizootics (Miller et al.

2006; Muller et al. 2008; Brandt and McManus 2009; Cróquer and Weil 2009;

McClanahan et al. 2009). Consequently, the occurrence of coral diseases might be an indicator of an effect of coral bleaching on both the organism and the ecosystem level, or otherwise bleaching can be used as early warning indicator of subsequent susceptibility of the coral community to disease outbreaks.

However, bleaching has also been found to occur as a direct result of bacterial infection in the coral tissue, particularly by gram-negative bacteria of the genus Vibrio.

Kushmaro et al. (1996) found that bleaching of the Mediterranean coral Oculina patagonica was caused by Vibrio shiloi, which produces extracellular proline-rich peptides referred to as Toxin P, which blocks photosynthesis and bleaches and lyses zooxanthellae. However, the mere presence of the Vibrio bacterium is not sufficient to cause coral bleaching:

virulence factors for adhesion and ingress into the coral and Toxin P are produced by the bacterium only at elevated seawater temperatures (Kushmaro et al. 1998; Toren et al.

1998; Banin et al. 2000). Similarly, V. coralliilyticus in combination with elevated temperature caused bleaching in the coral Pocillopora damicornis (Ben-Haim and Rosenberg 2002; Ben-Haim et al. 2003). These observations led to the ‘Bacterial Bleaching Hypothesis’ (Rosenberg and Falkovitz 2004; Rosenberg et al. 2009), which proposes a microbial infection as the primary trigger of coral bleaching. Conversely, Ainsworth et al.

(2007) found no evidence to support this hypothesis and argued against its generalisation, suggesting that the bacterial infection is opportunistic rather than a primary pathogenic cause of bleaching and that non-microbial environmental stressors trigger coral bleaching in O. patagonica. Nevertheless, a recent experiment with the coral Montipora digitata

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demonstrated that corals exposed to thermal stress in synergy with external bacterial challenge (by different inoculated strains of V. coralliilyticus, V. harveyi, Paracoccus carotinifaciens, Pseudoalteromonas sp., and Sulfitobacter sp.) undergo more severe bleaching than colonies exposed to thermal stress alone (Higuchi et al. 2013). Conversely, a

‘healthy’ microbial community (i.e. the microbial community found in healthy colonies) increases the thermal tolerance of the holobiont compared to that of coral colonies whose bacterial community was treated with antibiotics (Gilbert et al. 2012).

From these findings, it appears likely that environmental drivers act on the coral microorganisms as well as the coral host, causing a change in the microbial community that in some cases contributes directly or indirectly to bleaching (Rosenberg et al. 2009).

Finally, these studies stress the importance of the interaction between abiotic and biotic factors and of the stability of the coral microbiota for the resilience of the holobiont to bleaching, calling attention to a more careful consideration of bacteria as fundamental players in the bleaching process. Because of the present development of molecular techniques (e.g., qPCR, CARD-FISH), which are becoming accessible to more researchers every day, monitoring of the bacterial community or of a particular bacterial bioindicator (such as Vibrio) may serve as an early warning indicator of bleaching events or as an indicator of direct impact on corals once the bleaching process occurs.

As we come to understand the causes of bleaching and the interaction between different biotic and abiotic stressors across spatial and temporal scales, on both the organism and the ecosystem level, it is fundamental to develop environmental indicators that help in managing and protecting coral reef ecosystems from degradation. Finally, monitoring of these indicators, on both a global and local scale should be implemented and response protocols need to be developed if we are to save these ecosystems in the coming decades.