**3. Discussion**

Ecological restoration is broadly defined as: 'the process of assisting the recovery of an ecosystem that has been degraded, damaged, or destroyed' [127], and is becoming the major ubiquitous strategy for increasing ecosystem services, as well as for reversing biodiversity decline. As a relatively new discipline it is fraught with hindrances, which is to be expected [128]. In contrast, the science of restoration ecology (primarily the facets that deal with terrestrial ecosystems), has rapidly developed over the past century, maturing into a cohesive body of theory that is backed by an established toolbox of restoration practices. Notwithstanding the growing interest in ecological restoration, the added challenges posed by climate change further reveal that the available adaptation toolkit associated with ecological restoration is still meager [129]. This is also emphasized in the coral restoration arena, a field

that has not ye<sup>t</sup> developed to the level of scientific maturity comparable to that of terrestrial ecological restoration [1,17].

On top of anthropogenic activities, climate change significantly challenges the concepts, practices and outcomes of ecological restoration. It is now more than a decade since the realization that it makes less sense to establish current restoration approaches on historical references, as they are all under the influence of rapidly changing climate regimes. Although historical references are of interest, they are less useful as ways to establish direct objectives [127]. Furthermore, the forecasted climate change scenarios will pose further challenges, some of which are ye<sup>t</sup> to be experienced. Additionally, restoration efforts will have to address, in addition to restitution of biodiversity and ecosystem services, the ecosystem's resilience in the face of anticipated climate change scenarios [114,130].

This manuscript deals with the currently developing active reef restoration toolbox, used to enhance coral resilience and adaptation in a changing world. Seven classes of avenues and tools were described (Table 1) and discussed, including: the improved gardening methodologies, ecological engineering approaches, assisted migration/colonization, assisted genetics/evolution, assisted microbiome, coral epigenetics and coral chimerism. These tools are further classified into three levels of operation (Figure 3), each is based on the success of the former level, altogether compiling the most current active reef restoration toolbox. This toolbox is based on the rational and methodologies developed for the 'coral gardening' concept [13–19,21,26–28].

**Figure 3.** A theoretical illustration depicting how the seven classes of the suggested novel avenues and tools (improved gardening methodologies, ecological engineering approaches, assisted migration/colonization, assisted genetics/evolution, assisted microbiome, coral epigenetics, coral chimerism), further classified into three operation levels, compiling a unified active reef restoration toolbox, under the umbrella of the gardening tenet. Using the currently available restoration methodologies (based on the gardening approach) reef statuses that are anticipated to decline (the red trajectory towards the near future) are improving, or not ([the red trajectory towards the future] depending on the level of stress imposed by anthropogenic activities and climate change drivers). The next evolved level of progress in reef status is achieved by applying improved methodologies and ecological engineering approaches. They may maintain an improved reef status, but not the desirable advanced state. Yet, this level provides the ground for the operational level of 'assisted' approaches and the apex operational level of epigenetics and chimerism approaches, altogether maximizing reef statuses and enhancing coral resilience and adaptation in a changing world, developing to the 'best to be applied' status with current research avenues, ye<sup>t</sup> not approaching the primeval reef status.

The basic and first level (Figure 3) includes two classes of tools, the improved gardening methodologies and the ecological engineering approaches, which are aimed at further enhancing the efficiency of the coral restoration approach, towards the development of sustainable ecosystems that have human and ecological significance. The research in both classes of coral restoration tools, either on the nursery or the transplantation phases, is highly active, performed in various reefs worldwide on a wide range of coral species, and various new approaches and methodologies are frequently suggested and tested. In addition to maximizing the survival and growth rates of corals in the nursery and after transplantation, the new approaches (primarily the ecological engineering approaches) tackle major issues in reef restoration. These include the phase-shifting of coral reef surfaces from turf algae back to coral dominated layers [60], the creation, within very short time periods, of large coral colonies of ecological importance [53,59,60], and the establishment of new biological corridors through stepping stone mechanisms [17] just to name a few of the ramifying approaches.

The second level (Figure 3) includes the three 'assisted' approaches (assisted migration/colonization, assisted genetics/evolution, and assisted microbiome). This level of operation represents restoration strategies and approaches that shift in theory and in practice from former approaches reliant on reference points and historically based goals, towards a common focus on "process-oriented configurations" [130]. The assisted approaches are still either at a conceptual level, or first laboratory trials, and are challenged by the need to guide the transition towards ecosystem states that can maintain key functions and values in a changing environment. For example, the assisted migration/colonization approach as developed may result in a new ecosystem with reduced services and diminished ecological complexity [17]. The assisted genetics/evolution approach is still at the proof-of-concept stage [116], while the assisted microbiome approach and the suggested activities therein, are still problematic to design as they lack the needed baseline studies [116]. The 'assisted' approaches hinge on successful active restoration methodologies, such as nursery grown colonies and transplantation tactics. It is most likely that much of the 'assisted' approaches will be shaped and intermingled in the future with other ecological engineering approaches to form a toolkit, aimed at achieving an improved ecologically-based restoration strategy. Thus, it is envisaged that neither one of the assisted approaches will stand by itself as an independent restoration strategy.

The third operational level (Figure 3) includes the two approaches of coral epigenetics and coral chimerism. While the success in either approach depends on the rationale and methodologies developed for the 'coral gardening' concept, and on the supplementary ecological engineering toolkit, each approach is based on a well-established biological phenomenon with considerable ecological and evolutionary perspectives. Employing the coral epigenetics tool may provide extra tolerance in case of subsequent re-exposure of the organism (or its progeny) to similar or even harsher conditions. At this stage, most studies on the subject were performed under laboratory conditions or on evaluations of coral responses from the field [77–79,81–83] but there is also documentation for novel phenotypic attributes developed following human manipulation under field conditions (increased growth rates of corals, long term enhancement of reproduction output [46]). Employing the coral chimerism tool may further provide cumulative levels of adaptation, as they are expressed by a naturally occurring phenomenon [84–91,125,126].

Coral chimerism (Figures 2 and 3) has already been discussed as a potential evolutionary rescue instrument, reliant on the premise that it may compensate for the immediate need for genetic change [85]. In a similar way, an epigenetic modification can facilitate evolutionary rescue through the creation of novel phenotypic variants [131]. Thus, both instruments may provide coral populations with the resilience to persist through periods of environmental change. Both instruments, alone or in combination, have the potential to facilitate faster adaptation rates and improved adaptation, than those exhibited in traditional genetic mutations, and thus merit special attention.

It should be noted, however, that risks involved in the application of some of the tools are not ye<sup>t</sup> well defined and that the potential of unknown costs versus perceived benefits assigned to the tools should be evaluated [106–108,116]. These include costs for selective breeding that may lead to

reduced genetic variability, and for increased sensitivity of coral populations to other climate change drivers, the introduction of pathogens and predators via coral transplantation [109], and for the flawed allocation of limited human, institutional and financial resources [17,116]. Another topic not addressed here is the scale of future restoration measures at the changing world. While the coral gardening-toolbox could serve as a ubiquitous ecological engineering platform for restoration on a global scale, it is ye<sup>t</sup> facing the most imperative challenge to document restoration manipulations at regional/global levels [17], to determine that the gardening approach indeed supports sustainable coral reefs at large scales. Indeed, results already noted that large-scale coral restoration may have a positive influence on coral survivorship [132], recruitment rates and juvenile density [56]. These acts may further be aided by novel tools, like remote sensing technology [133].

Cumulatively, climate change and anthropogenic impacts pose major challenges for the development of e ffective tools, not only assessing levels of degradation in reef ecosystems under varying states of alteration, but also for the development of rationales and methodologies to e fficiently restore degrading reefs. Based on principles, concepts and theories from silviculture, the "gardening" concept of active reef restoration [13–19,21,26–28] has not only laid the foundation for reef restoration, but is now developing through several seemingly separate approaches (improved gardening methodologies, ecological engineering approaches, assisted migration/colonization, assisted genetics/evolution, assisted microbiome, coral epigenetics and coral chimerism) that are divided here into three operational levels, altogether representing the unified active reef restoration toolbox under the umbrella of the gardening tenet to focus on the development of coral resilience and adaptation in a changing world. This may lead to new policies that will be integrated with other e fforts to scale up reef restoration efforts into a global measure embedded within integrated governance structures.

**Funding:** This research was funded by the AID-MERC program (no M33-001), by the North American Friends of IOLR (NAF/IOLR), by the JNF and by the Israeli-French high council for scientific & technological research program (Maïmonide-Israel).

**Acknowledgments:** This study was supported by Thanks are due to G. Paz for drawing Figure 3.

**Conflicts of Interest:** The author declares no conflicts of interest.
