*2.7. Heterotrophy*

Heterotrophic carbon can become a significant energy source for some coral species when phototrophic carbon is unavailable, such as during a bleaching event (Table 1) [118]. Some studies have shown how heterotrophy replenished energy reserves in corals exposed to high temperatures [119] and during the recovery phase [120]. Similarly, Borell and Bischof [121] showed higher photochemical efficiency in fed corals compared to unfed corals after a mild thermal stress experiment. Also, Borell et al. [122] demonstrated how heterotrophy sustained photosynthetic activity and energy reserves in thermally stressed corals.

In a study which developed an energy-budget model linking coral bleaching and mortality risk, authors concluded that the time between the start of severe bleaching and the beginning of mortality is influenced by the amount of lipid stores corals have before the bleaching event and their capacity to acquire energy through heterotrophy [123]. With a stable isotope 13C pulse-chase labelling experiment, Hughes et al. [124] demonstrated that, after exposure to high temperatures, coral hosts incorporated heterotrophic labelled carbon for storage and to stimulate endosymbiont recovery. Even after recovery from bleaching, 75% of carbon in newly acquired lipids was sourced heterotrophically [125], and corals continued assimilating heterotrophic carbon for up to 11 months after the bleaching experiment [126].

Nonetheless, the capacity for heterotrophic plasticity is compromised after two consecutive bleaching events [127]. Researchers experimentally bleached corals for 2.5 weeks, transferred corals to the field for recovery, and then repeated the bleaching experiment after one year. After the first thermal stress experiment, zooplankton and dissolved organic carbon (DOC) allowed the metabolic demand of bleached corals to be met; however, neither form of heterotrophic carbon was able to contribute to the energy budget of both species after the second bleaching experiment, suggesting that the capacity for heterotrophic plasticity is compromised under annual bleaching events [127] and corals need to depend on their energy reserves and/or symbiont association to survive repeated bleaching [128].

#### **3. Perspectives for the Future**

Because the loss of corals around the world would be a devastating consequence of human influence on earth, strategies to mitigate the damage and improve coral's thermal tolerance are currently being taken into consideration. For example, assisted colonization, migration and/or gene flow contemplate the movement of colonies or larvae of the same species living at different latitudes. 'Warm-adapted' corals can be transplanted to high latitude areas, where conspecifics living in colder environments, are vulnerable to thermal stress [129–131]. Assisted evolution has the potential to increase thermal stress tolerance in corals through various approaches: preconditioning acclimatisation (see Section: 'Thermal stress acclimatisation') and trans-generational acclimatisation, changes in microbial communities [132], selective breeding [133], mutagenesis [134], and the use of "CRISPR/Cas9" genome editing technology [135]. The use of 'strong corals' naturally adapted to high temperature extremes, such as corals originating from the Persian Gulf or Red Sea, as possible seedlings to repopulate areas where corals have disappeared [117,136–138] is also being considered. Unfortunately, none of

these measures seem to be able to keep pace with the current rate of climate change, with the time between recurrent bleaching events becoming increasingly too short to allow complete recovery of coral reef ecosystems [139]. Despite recent advances in research methods and technology, such as transcriptomics [140], financial and logistical limitations to implement these actions remain [141], especially at large scales [130], and it takes many years to safely deploy new technology after social and political scrutiny [142].

Other conservation measures under consideration include designing better marine protected areas (MPAs) [143] or networks of MPAs [144–146], taking into consideration larval dispersal, connectivity and distribution patterns in areas with thermally tolerant corals [147] and including 'refugia' in areas where coral reefs have proven to be resilient to climate change [21,43,148,149]. This might help avoid the "protection paradox" in MPAs, in which vulnerable species are protected from local pressures, like fishing; ye<sup>t</sup> while these species recover, they might be more sensitive to global pressures, like bleaching events [144]. Nevertheless, well-protected reefs within MPAs are not shielded from thermal stress [150,151]. After the last bleaching event, this was confirmed for MPAs [152], and for remote and isolated reefs with almost no direct human pressures [23,24,27,153–155].

The integration of assisted evolution [131,134] into coral reef restoration programs [156,157] to increase the resilience of already degraded ecosystems [41] is one strategy that has proven to be successful. Morikawa and Palumbi [158] used naturally thermal-tolerant corals from American Samoa to show that resilient corals can survive multiple bleaching events, providing the first proof that ecosystem engineering for conservation might be a resilience restoration tool of grea<sup>t</sup> importance in our climate changed future [158].

Evidence from reciprocally transplanted coral clones between sites with different thermal histories shows how individual coral colonies can shift their thermal threshold and thermal tolerance [93,159,160]. It is clear that many coral species are acclimatising and adapting to rapid changes in climate and their mechanisms differ among species and localities [67,82,83,89,90,113,115,161]. However, under current greenhouse gas emission projections, coral reefs worldwide are likely to change into new configurations with new assemblages of species [19,149,162–165]. These changes are happening fast, the GBR being the best example. After the 2014–2017 mass bleaching event, even the most 'pristine' areas in the northern GBR saw high mortality regardless of reefs' individual managemen<sup>t</sup> status, proving that current managemen<sup>t</sup> toolsets are insufficient to protect coral reef ecosystems from climate change [20,152]. The Paris Agreement was a first step to tackle the climate crisis, but no major industrialized country is meeting its pledges to control and reduce their greenhouse gas emissions [166]. It is imperative that societies completely change our dependence on fossil fuels, therefore addressing the root causes of climate change.

**Author Contributions:** Conceptualization, R.C.-B. and C.A.C.; methodology, R.C.-B.; software, R.C.-B.; validation, R.C.-B. and D.S.; formal analysis, R.C.-B.; investigation, R.C.-B.; resources, C.A.C.; data curation, R.C.-B.; writing—original draft preparation, R.C.-B. and D.S.; writing—review and editing, R.C.-B., D.S. and C.A.C.; visualization, R.C.-B.; supervision, C.A.C.; project administration, C.A.C.; funding acquisition, C.A.C. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was funded by Academia Sinica for Life Science Research (no. 4010) and Ministry of Science and Technology, Taiwan (MOST 101-2621-B-001-005-MY3) to C.A.C.

**Acknowledgments:** Many thanks to LK Chou and D Huang for their invitation to contribute to the special issue of "Coral Reef Resilience". We also thank three anonymous reviewers for helping improve this manuscript. R.C.-B. and D.S. are the receipts of PhD fellowship from Taiwan International Graduate Program (TIGP)-Biodiversity in the Academia Sinica. This review is supported by funds from Academia Sinica and Ministry of Science and Technology, Taiwan to C.A.C.

**Conflicts of Interest:** The authors declare no conflict of interest and the funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
