The effect of thermal history on the susceptibility of reef-building corals to thermal stress

Abstract

SUMMARYThe mutualistic relationship between corals and their unicellular dinoflagellate symbionts (Symbiodinium sp.) is a fundamental component within the ecology of coral reefs. Thermal stress causes the breakdown of the relationship between corals and their symbionts (bleaching). As with other organisms, this symbiosis may acclimate to changes in the environment, thereby potentially modifying the environmental threshold at which they bleach. While a few studies have examined the acclimation capacity of reefbuilding corals, our understanding of the underlying mechanism is still in its infancy. The present study focused on the role of recent thermal history in influencing the response of both corals and symbionts to thermal stress, using the reef-building coral Acropora aspera. The symbionts of corals that were exposed to 31°C for 48·h (pre-stress treatment) 1 or 2 weeks prior to a 6-day simulated bleaching event (when corals were exposed to 34°C) were found to have more effective photoprotective mechanisms. These mechanisms included changes in non-photochemical quenching and xanthophyll cycling. These differences in photoprotection were correlated with decreased loss of symbionts, with those corals that were not prestressed performing significantly worse, losing over 40% of their symbionts and having a greater reduction in photosynthetic efficiency. These results are important in that they show that thermal history, in addition to light history, can influence the response of reef-building corals to thermal stress and therefore have implications for the modeling of bleaching events. However, whether acclimation is capable of modifying the thermal threshold of corals sufficiently to cope as sea temperatures increase in response to global warming has not been fully explored. Clearly increases in sea temperatures that extend beyond 1-2°C will exhaust the extent to which acclimation can modify the thermal threshold of corals. Supplementary material available online at

Mechanisms of Thermal Tolerance in Reef-Building Corals across a Fine-Grained Environmental Mosaic: Lessons from Ofu, American Samoa

“…Certainly, the extreme temperature profiles of the HV pool are not unique to Ofu; corals are found in a variety of extreme environments and are exposed to temperatures that would cause bleaching in their conspecifics from other areas (Coles and Riegl, 2013;Kline et al, 2015;Richards et al, 2015;Camp et al, 2017). Wide variation in thermal tolerance and genetic divergence has been reported across latitudes and at large-spatial scales (Middlebrook et al, 2008;Howells et al, 2013;Dixon et al, 2015;Thomas et al, 2017), and it is becoming increasingly clear that locally adapted thermally tolerant pockets of corals exist at fine-spatial scales within a variety of coral reef systems (Goreau and Macfarlane, 1990;Barshis et al, 2010;Castillo et al, 2012;Kenkel et al, 2013bKenkel et al, , 2015Schoepf et al, 2015). For example, Porites astreiodes colonies from the thermally variable inshore patch reef environment of south Florida have greater thermal tolerance than offshore populations less than 10 km away (Kenkel et al, 2013a).…”

“…More recently, focus has shifted toward understanding the plasticity of thermal tolerance in corals, and numerous studies have identified a direct link between thermal preconditioning and bleaching susceptibility from both field observations (Castillo and Helmuth, 2005;Maynard et al, 2008;Thompson and van Woesik, 2009;Castillo et al, 2012;Shuail et al, 2016) and experimental manipulation (Brown et al, 2000(Brown et al, , 2002Dove et al, 2006;Middlebrook et al, 2008;Bellantuono et al, 2012b;Bay and Palumbi, 2015). For example, Acropora, Pocillopora, and Porites from the Great Barrier Reef showed lower rates of bleaching during the 2002 bleaching event than the 1998 event, despite more intense conditions during the 2002 event (Maynard et al, 2008).…”

The role of stochastic thermal environments in modulating the thermal physiology of an intertidal limpet, Lottia digitalis

“…Some intertidal organisms are also better able to tolerate heat stress if first exposed to a sublethal heat shock (Todgham et al, 2005;Dong et al, 2010;Giomi et al, 2016;Pasparakis et al, 2016). This phenomenon, known as heat hardening (Bowler, 2005), is a very important inducible stress tolerance mechanism in many organisms, both terrestrial and aquatic, inhabiting variable environments (Maness and Hutchinson, 1980;Rutledge et al, 1987;Middlebrook et al, 2008;Bilyk et al, 2012). Previous studies have shown fluctuating thermal environments increase thermal tolerance (Feldmeth et al, 1974;Otto, 1974;Threader and Houston, 1983;Woiwode and Adelman, 1992;Schaefer and Ryan, 2006;Oliver and Palumbi, 2011;Manenti et al, 2014;Kern et al, 2015), with intertidal species exposed to tidal cycle fluctuations being more stress-tolerant than those that are exposed to constant temperatures (Tomanek and Sanford, 2003;Podrabsky and Somero, 2004;Todgham et al, 2006;Giomi et al, 2016).…”

The physiological response of reef corals to diel fluctuations in seawater temperature

“…Several experimental studies have suggested that the role of temperature in coral bleaching may not lie only in the threshold value eliciting the response, but also the sublethal intensities that create the potential for acclimatization (McClanahan and Maina, 2003;Middlebrook et al, 2008;Edmunds, 2009). For instance, the rate of change in temperature and the capacity for acclimatization influence the ways in which corals respond to elevated temperature (Coles and Jokiel, 1977;Brown et al, 2002;D'Croz and Maté, 2004;Castillo and Helmuth, 2005), with one of the best examples of these effects coming from intertidal corals in Thailand.…”

“…In this location, Goniastrea aspera that were emerged at low tide and exposed to high light intensities from January to March subsequently displayed acquired resistance (i.e., acclimatization) 2-5 months later to elevated seawater temperatures, most likely as a result of increases in cellular defenses in the cnidarian host (Brown et al, 2002). Similarly, for sub-tidal corals, their physiological response to increased temperature can be ameliorated by their temperature history (Castillo and Helmuth, 2005;Middlebrook et al, 2008;Edmunds, 2009).…”