Improving Thermal Tolerance in Reef-Building Corals
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as ocean temperatures rise due to climate change, coral bleaching events are increasing in frequency and severity.
When a coral "bleaches", it expels the tiny endosymbiotic algae (family Symbiodiniaceae) that live in its tissues (Knowlton & Rohwer 2003, Weis et al. 2008, LaJeunesse et al. 2018). Because these algae photosynthesize to provide corals with nutrition and aid with calcification (Muscatine 1967, Pearse & Muscatine 1971), it is harmful and sometimes fatal for corals to lose them (Muscatine & Porter, 1977). However, corals can recover their symbionts within a period of weeks to months if thermal stress ceases (Jones and Yellowlees 1997; Cunning et al. 2016).
By expelling and regaining symbionts, bleaching and recovery may enable shifts in symbiont community composition (Buddemeier and Fautin 1993, Toller et al. 2001). Referred to as “symbiont shuffling” (Baker 2003), this process may modify the relative abundance of different, functionally diverse symbiont types within the host, which may also alter the holobiont phenotype. For example, in the laboratory and in the field, many studies have found that bleached corals tend to recover with Durusdinium (formerly known as Symbiodinium clade D) as the dominant symbiont (Grottoli et al. 2014, Kemp et al. 2014, Silverstein et al. 2015, Cunning et al. 2018). Durusdinium has shown more thermal tolerance than other symbiont types, making the coral host more resistant to future heat stress and increasing its bleaching threshold by ~1-2°C (Berkelmans and van Oppen 2006; Silverstein et al. 2015; Cunning et al. 2015).
Symbiont shuffling, and in particular shifting symbiont communities towards dominance of Durusdinium, may allow corals to rapidly acclimatize when faced with environmental stress and help them become more resilient under climate change (Baker 2004). The Coral Reef Futures Lab has achieved this "stress-hardening" technique in the lab using adults of many key Caribbean coral species, and lab members are currently investigating methods for in situ holobiont manipulation. In addition, one of the primary focuses of my research is encouraging coral recruits to take up Durusdinium from the very beginning of their lives. Since corals spawn during the warmest time of year and juveniles are likely to be exposed to heat stress, associating with heat-tolerant symbionts early on may enhance theor survival. Our hope is that these methods will soon allow restoration practitioners to prime corals with thermotolerant symbionts to increase bleaching thresholds and protect against future heat stress.
Assessing Trade-offs of Thermal Resilience
Although increases in the relative abundance of Durusdinium trenchii (formerly known as Symbiodinium D1a) in corals due to symbiont shuffling may increase thermal tolerance, this shift may cause trade-offs that impact the viability of symbiont shuffling at the ecosystem scale (Ortiz et al. 2012). First, it is possible that the association with D. trenchii will only be fleeting following a disturbance, and that corals will gradually lose D. trenchii in the absence of thermal stress (Coffroth et al. 2010). Thus, the degree of symbiont shuffling and stability of new associations may depend on the severity of the disturbance and the functional advantage under the conditions (Cunning et al. 2018).
While Durusdinium may confer increased thermal tolerance in some corals, it may also lead to other ecophysiological trade-offs are a huge potential shortcoming of hosting Durusdinium in hosts. In both adult and juvenile corals of a variety of species, researchers have observed slower growth in corals dominated by Durusdinium than in those mainly hosting another type (Little et al. 2004, Abrego et al. 2008, Jones & Berkelmans 2010, Pettay et al. 2015, Cunning et al. 2015). Jones and Berkelmans (2010) found that Acropora millepora colonies hosting Durusdinium grew 29% slower in the laboratory and 38% slower in the field than colonies hosting C2. Cunning et al. (2015) reported 35-40% slower growth in Pocillopora damicornis hosting Durusidinum compared to those hosting Cladocopium at 26 degrees Celsius. However, in both studies the growth disadvantage of Durusdinium disappeared at elevated temperature, since warming reduced growth regardless of symbiont type and more severely in corals hosting Clacocopium.
When combined with environmental stressors such as ocean acidification and depressed aragonite saturation (Hoegh-Guldberg et al., 2007), the additional decrease in growth that results from hosting D. trenchii could reinforce coral cover declines and prevent rapid recovery of degraded populations (Ortiz et al. 2012). In particular, if Durusdinium decreases growth rates in coral juveniles, this could result in reduced competitive ability and increased mortality in the field, where size-escape thresholds are important determinants of survival (Doropoulos et al. 2012). With potentially dynamic trade-offs, it will be important to take many potential factors into account when assessing the ultimate capacity for D. trenchii to increase reef resilience.
Interestingly, several studies have revealed a potential interaction between Durusdinium and disease resistance in some scleractinians. In a survey of diseased and healthy colonies in the Florida Keys and the US Virgin Islands, Correa et al. (2009) found that few diseased colonies harbored Durusdinium, while most diseased colonies sampled contained species of Breviolum and Cladocopium. This finding suggests a negative correlation between hosting Durusdinium and disease susceptibility. Furthermore, Rouzé et al. (2016) reported that Acropora cytherea colonies hosting Durusdinium were less likely to develop disease (and specifically infection by Vibrio spp.) compared with those hosting Symbiodinium. Perhaps these results are related to colonies with Durusdinium resisting bleaching despite environmental stress, since bleaching compromises the health status of a coral and has been hypothesized to indirectly increase vulnerability to opportunistic pathogens (Muller et al. 2008, Brandt & McManus 2009, Rodriguez-Lanetty 2009). As such, future studies need to continue unraveling the relationships between bleaching, symbiont shuffling, and disease susceptibility.
Part of my research involves assessing possible eco-physiological trade-offs in coral recruits that have been manipulated to host D. trenchii. After outplanting recruits with D. trenchii and other dominant symbiont types, I compare survivorship, growth rates, bleaching, and disease susceptibility in the field. Ultimately, these data will help me weigh the short- and long-term implications of hosting D. trenchii for coral juveniles, and to assess potential outcomes of hosting D. trenchii for reef recovery and resilience.