Coral reefs sit at the interface of two powerful societal trends. On the one hand, coral reef ecosystems provide vast resources to human communities, resources that are increasingly needed as the human population grows. On the other hand, coral reef ecosystems are existentially threatened by increased human-driven stresses, particularly the extensive coral mortality from severe bleaching events caused by warming seas on top of local stressors such as sedimentation, pollution, invasive species, and overfishing. Continuing disease threats and concerns about increasingly acidifying waters compound the risk posed to coral reefs. The increased reliance by humans on an ecosystem increasingly at risk of collapse has led to a widespread call for interventions that might preserve the services provided by coral reefs into the future.
A growing body of research on coral ecology, molecular biology, and responses to stress has revealed the complex nature of corals and their associated microbiome (including symbiotic algal, prokaryotic, fungal, and viral components). Some of this knowledge is poised to provide practical interventions in the short term, whereas other discoveries are poised to facilitate research that may later open the doors to additional interventions.
The committee reviewed the current literature on new approaches with the potential to increase the resilience and persistence of coral reefs as global environmental conditions deteriorate. Current approaches that focus on management of local stressors, while important to continue, are not adequate, nor are they particularly designed to address these rapidly
changing environmental conditions. Reduction and mitigation of carbon emissions will go a long way in reversing and preventing future coral reef losses. However, even with such reductions, committed warming from the current accumulation of greenhouse gases is expected to expose the majority of the world’s reefs to harmful thermal stress events annually by 2050. Global bleaching events are already occurring due to the sensitivity of coral reefs to even small, sustained increases in maximum temperatures (as low as 1°C). Thus, interventions that increase the persistence and resilience of coral reefs to current and deteriorating environmental scenarios are important to explore.
The constellation of interventions includes working with corals at a variety of ecological levels with a variety of tools. These levels include individual corals, their algal symbionts, microbial communities, populations within species, species, reef communities, and the associated gene repertoire at all these levels. Tools include movement of coral colonies, increasing populations through fragmentation or culturing, increasing natural resilience through artificial selection or selective breeding of corals and symbionts, preservation of coral stem cells or gametes, genetic intervention through gene editing in corals and symbionts, manipulation of microbial communities, and physical intervention to reduce stress. Table 6.1 provides an overview of the interventions as categorized by the committee.
The interventions range widely in their state of readiness. The committee explored these varied interventions and their potential for broadscale implementation based on their benefits and goals, risks, scale of impact, limitations, and infrastructure needs. Layered over this discussion is that the risk of doing nothing is increasing quickly and is shown to be high in some reef environments experiencing significant losses.
Identifying Versus Creating Resilience
Corals currently show a wide range of tolerance for heat and other types of environmental stresses, can inhabit a strong mosaic of environments, and can be associated with a diverse array of symbionts and microbes. This variability across populations of a species represents capacity for adaptation via natural selection. For instance, corals living in warm water microclimates are already adapted or acclimated to these conditions. A strong component of increasing the adaptive capacity of coral reefs is to map these adaptations, understand their function in the holobiont, and use them as potential targets for further genetic manipulation. Finding natural adaptive capacity for heat tolerance, and using it
in programs of fragment outplanting or managed breeding represents a feasible, scalable approach that can potentially be undertaken in the near term on multiple species (see a similar conclusion in van Oppen et al., 2015b). Similar tools are well known in other fields, such as salmon and shellfish restoration. Interventions that focus on augmenting such natural resilience may have minimal barriers to implementation (e.g., permitting). While not risk free, if such tolerant variants can be found locally for multiple species, then there are fewer risks than, for example, genomic manipulation or long-distance relocation. However, it is not certain that natural levels of stress resistance, even for selectively bred and selected lines, will prove adequate to protect corals across the extreme conditions that might occur with future climate changes. To withstand unprecedented heat levels, it may be necessary to generate unprecedented genetic changes. Genomic manipulation of corals or symbionts is in very early research stages and faces a number of research hurdles before it is likely to be operational. Even when the technology is available for genetic transformation, it is currently unknown which genes are the best targets for alteration. Instead, there are a wide variety of potential targets in different corals that will need to be experimentally tested. Thus, the development of gene manipulation technology in corals and symbionts is simultaneously a tool for hypothesis testing about the most efficient gene targets, and a tool for generating manipulated genomes for use on reefs.
A key feature of any intervention scheme for coral reefs is the movement of coral colonies to areas where they are needed to support reef stability. Whether new adaptive capacity is found on native reefs or generated in the laboratory, the most tolerant corals are likely to be a subset of the population with the expectation that this tolerance is heritable and will spread. Supporting the spread of tolerant types can take several forms. First, promoting propagation and breeding can support local stress-resistant populations so that their offspring can seed other reefs. Second, moving stress-tolerant colonies to adjacent reefs can help them pass their heat tolerance to future offspring in a wider location. Third, long-distance movement of tolerant corals from laboratories or warm water regions can potentially build thermal resistance in new or depleted areas. Short-distance relocation techniques are well known, and take advantage of decades of effort in coral colony nurseries. No known long-distance introductions of corals have been done purposefully. Marine research centers, extensive restoration programs, and the aquarium trade have already driven the developed techniques for outcropping and relocation over virtually any geographic scale. Movement of local stress-resistant colonies
TABLE 6.1 Overview of Interventions Examined in This Report
|Intervention||What It Is||Current Feasibility||Potential Scale||Limitations||Risks|
|Genetic and Reproductive Interventions|
|Managed Selection||Creating increased frequency of existing tolerance genes||In laboratory and at small local scales||Local reef scale; potentially transgenerational||Needs large populations||Decrease in genetic variation|
|Managed Breeding: Supportive Breeding||Enhancing population size by captive rearing and release||Success with some species at small scales||Local reef population; potentially transgenerational||Depends on sufficient population sampling and recruitment success of released individuals||Decrease in genetic variation|
|Managed Breeding: Outcrossing Between Populations||Introducing diversity from other populations through breeding||Demonstrated in laboratory for a few species||Local reef population; potentially transgenerational||Requires transport of gametes or colonies across distances and field testing across generations||Outbreeding depression; native genotypes may be swamped|
|Managed Breeding: Hybridization Between Species||Creation of novel genotypes through breeding||Demonstrated in laboratory for a few species||Local reef population; potentially transgenerational||Limited ability to create hybrids; requires testing for fertility and fitness||Outbreeding depression; competition with native species|
|Gamete and Larval Capture and Seeding||Collection and manipulation in the field and laboratory and release into the wild||Feasible at local scales||Laboratory to local reef scale; potentially transgenerational||Site-specific reproductive timing, recruitment success can be poor||Limited genetic diversity; selection for laboratory versus field success|
|Coral Cryopreservation||Frozen storage of gametes and other cells for later use and transport||Feasibility is high for sperm, and growing for other tissue types||Materials can be transported globally||Requires excess gametes, larvae, or tissues||Long-term survival uncertain; genetic variation reflects only current conditions|
|Genetic Manipulation: Coral||Altering coral genes for new function||Technically feasible for larvae||Would occur in laboratory; can be self-perpetuating||Gene targets and cellular raw material unidentified, long lead time to roll out to reefs||Might alter wrong genes; unknown risks|
|Genetic Manipulation: Symbionts||Altering symbiont genes for new function||Not yet feasible||Would occur in laboratory; can be self-perpetuating||Technology not established; gene targets and cellular raw material unidentified||Might alter wrong genes; kill target cells; unknown risks|
|Pre-exposure||Using stress exposure to make colonies more tolerant||In laboratory and small-scale field trials||Local reef scale; may be temporary or transgenerational||Difficult to scale up beyond local||Could be detrimental if applied incorrectly|
|Algal Symbiont Manipulation||Changing algal symbionts to more tolerant types||Observed after bleaching events; demonstrated in laboratory||Individual coral colony or large spawning events; unknown longevity||Difficult to scale; easier for some coral species than others||Ecological tradeoffs, e.g., slower growth|
|Microbiome Manipulation||Maintaining/increasing abundance of the native or new beneficial microbes||Demonstrated in laboratory and nursery facilities for limited coral species||Locations on reefs to reef scale; applied at times of stress||Reef-wide delivery mechanisms are lacking; lack of known beneficial microbes; little understanding of direct or indirect effects||Potential to increase deleterious microbes, decrease beneficial ones|
|Antibiotics||Adding antibiotics to control pathogenic microbes||Used in aquaculture and demonstration in small-scale field trials||Laboratory, aquarium, and colonies on reef; requires repeated application||Lack of specificity to target pathogens limits effectiveness||Promote antibiotic resistance in deleterious microbes; destabilization of native beneficial microbiomes|
|Intervention||What It Is||Current Feasibility||Potential Scale||Limitations||Risks|
|Phage Therapy||Adding phage viruses to control pathogenic microbes||Demonstrated in laboratory experiments||Local reef scale; potential to self-propagate||Lack of identified target coral pathogens||Undesirable gene transfers across microbial populations; impact on beneficial microbes|
|Antioxidants||Reducing cellular oxidative damage derived from stress using chemical treatments||Demonstrated in some laboratory experiments||Laboratory only; requires repeated application||Little understanding of direct or indirect effects||May affect other reef species|
|Nutritional Supplementation||Using nutrients to improve fitness and increase stress tolerance||Regular use in coral research and aquaculture||Laboratory and aquarium; requires repeated application||Poor understanding of balanced coral diets; reef-wide delivery mechanisms are lacking||Shifts carbon, nitrogen, and phosphate balance and may benefit coral competitors|
|Coral Population and Community Interventions|
|Managed Relocation: Assisted Gene Flow||Increasing abundance of stress-tolerant genes or colonies within population range||Technically feasible with information gaps regarding successful methods||Regional reef scale; can be permanent||Uncertain maintenance of stress tolerance over time||Moving nontarget genes; ecological tradeoffs|
|Managed Relocation: Assisted Migration||Moving stress-tolerant or diverse genes or colonies just outside species’ range||Technically feasible with information gaps regarding project design||Regional reef scale; can be permanent||Uncertain maintenance of stress tolerance and persistence over time between locations||Moving nontarget genes, species, and microbes; ecological tradeoffs|
|Managed Relocation: Introduction to New Areas||Moving stress-tolerant or diverse genes or colonies to new regions||Untested though technically feasible with information gaps regarding project design||Global movement impacting individual reef scale; can be permanent||Uncertain maintenance of stress tolerance and persistence over time between locations||High risk of moving nontarget genes, species, and microbes; ecological tradeoffs|
|Shading: Atmospheric||Sky brightening to relieve light and heat stress||Untested||Local to regional scale; temporary||Needs appropriate atmospheric conditions and technology||Altered light regimes; aerosol (salt) deposition|
|Shading: Marine||Reducing sunlight to relieve light and heat stress||Operational at small scales||Sites within reefs; temporary||Retention and advection limit application||Altered light regimes; plastic pollution|
|Mixing of Cool Water||Pumping cool water onto reef to reduce heat stress||Small-scale field tests with unknown efficacy||Local reef scale; temporary||Energetically costly or impossible to scale up||Altered physical and chemical (pH, nutrients) regimes|
|Abiotic Ocean Acidification Interventions||Reducing CO2 levels chemically||Effective in small-scale laboratory experiments||Sites within reefs depending on environmental setting; requires consistent input||Costly to scale up chemical quantities||Impact of chemicals on environment|
|Seagrass Meadows and Macroalgal Beds||Reducing daytime CO2 levels biologically||Some efficacy shown in field measurements||Local reefs depending on environmental setting; long-term benefit||Limited environmental settings; need to remove macroalgae||Detritus; altered nutrient loads; competition from macroalgae; increased CO2 at night|
over short distances likely has the fewest risks and costs, and has the best potential to scale up. Movement of laboratory-generated colonies and movement across large distances have higher risks and costs.
The Value of Diversity
Coral reef ecosystems are built on diversity at the habitat, species, genetic, symbiont, and microbial levels. Large, diverse populations have a higher capacity for future adaptation and are likely to maintain abilities to respond to other stressors besides heat. Diversity also supports coral reef ecosystem function and the sustainable delivery of associated ecosystem services including fisheries and recreation. Interventions that focus on single species, genotypes, or symbionts may be important milestones in developing intervention technology and rescuing coral at these scales in the short term. However, sustaining coral reef ecosystems that will be exposed to a diversity of stressors will require multispecies approaches and consideration of the broad suite of both biological and ecological processes that underpin ecosystem resilience. This could potentially include the implementation of multiple interventions in one location.
Conceivably, all of the ecological and genetic interventions will change the diversity of a population or community. While these changes are intentional, they may come with unforeseen risks, particularly if they become uncontrolled. Even the use of seagrasses or macroalgae for mitigating ocean acidity may displace other corals and change the carbon and nutrient balance of the local system. Managed relocation of corals outside of their current range may cause corals to become invasive or move associated species that may overwhelm resident populations. Additionally, relocation of corals may inadvertently spread diseases. Manipulation of the symbiotic algae and microbiome similarly alters the diversity of the holobiont system. The microbiome impacts coral health in multiple ways that are not yet completely understood, and shifting the microbiome may have unintended consequences on health. A clear concern known from other fields is that the overuse of antibiotics, especially in open systems, can result in the emergence of unwanted antibiotic-resistant bacteria. Important context is the fact that changing climate conditions will also likely result in the development of novel communities with altered phenotypes and species assemblages (Lurgi et al., 2012).
Interventions that target a particular resilient trait may result in tradeoffs. For example, symbionts that are naturally more thermotolerant, such as those in Durusdinium (formerly Symbiodinium clade D), impart greater
thermal tolerance to their coral hosts but may result in slower coral growth rates, reduced reproductive output, and disease susceptibility. Additionally, reducing the diversity of genotypes through genetic interventions reduces the ability to adapt via natural selection to unforeseen future stresses. Multiple stressors are often associated with coral declines and the inability to respond to multiple stressors is a risk to reef persistence. Interventions that reduce the light incidence may reduce photosynthetic activity of coral and other nearby organisms such as seagrasses. Artificial upwelling of cool water may lead to both nutrient and CO2 enrichment from deeper waters.
The Complex Holobiont
Corals and their algal symbionts are a unit that responds uniquely to stress depending on the coral and symbiont genomes. Alteration of symbiont communities is known to increase heat tolerance for some corals. Manipulating each of these poses very different barriers to implementation, different levels of permanence, and different needs for technology development. They also impose different risks. Parallel efforts in native gene discovery, physiological testing, genetic manipulation, and selective breeding will be important investments.
Microbial communities associated with corals are highly diverse complexes with a wide spectrum of functions that impact the health and potential heat tolerance of the coral holobiont. Understanding the role of this microbiome in the physiological response of corals to their surrounding environment is just beginning. Therefore, while methods exist for influencing the microbiome through, for example, probiotics or antibiotics, the lack of knowledge of the specific associations between coral and microbe species limits targeted use of microbial intervention tools.
The spatial and temporal scales on which interventions must operate depend on conservation goals, usually related to maintaining a certain level of local diversity and/or ecosystem services. To date, most interventions have operated on experimental or local scales, impacting a limited number of individuals. Some have the potential to be produced and applied at reef scales, including atmospheric shading and application of probiotics, antibiotics, antioxidants, and nutritional supplementation. However, delivering these interventions with specificity, with reduced risk, and at the required scale still has significant knowledge barriers. Others rely on large-scale efforts, at least at first, to achieve results beyond
the individual. This encompasses efforts that require relocation or managed breeding in the laboratory and outplanting.
On the temporal scale, the effect of an intervention may be either permanent or self-perpetuating across generations, or it may be temporary, requiring either continuous or periodic reapplication during times of stress. Genetic interventions are intended to perpetuate themselves to future generations (unless they are limited to an epigenetic response), though it is likely that a degree of captive breeding and release could continue to be necessary. Physiological interventions affecting individual coral holobionts are generally not permanent and are unlikely to convey resilience to future generations. Managed relocation of coral individuals, if successful, has the potential to remain permanent. However, without eventual greenhouse gas mitigation (or other such reduction in the relevant stressor), continued change might drive the need for continued intervention.
Engineering the Local Environment
Although increase in average long-term ocean temperatures chronically stresses corals, bleaching events result in acute impacts that are concentrated in the summer period of weeks or months. These acute reactions to historically abnormally high temperatures might be reduced by transient, local manipulation of the heat or light environment. Furthermore, increasing acidity may have a chronic and significant impact on corals in the future. Potential engineering solutions to these problems are being explored, but none are ready to be deployed on anything but an experimental scale. Additionally, the spatial scale at which they will ultimately have impact is a lingering question. Nevertheless, the ability to deploy this type of transient protection in the future may be important to protect high-value, live reef environments on local scales.
The task for this report is to synthesize current knowledge and lay the groundwork for informed decisions about conserving coral reefs under climate change. These decisions range from building investments in research programs and human capacity (i.e., researchers, practitioners) to deploying the interventions at experiment scales or integrated into restoration and conservation programs. Implementation of interventions in the ocean is regulated by permitting by multiple local, state, and national agencies for collection or outplanting of corals or for infrastructure installation. Overlapping responsibilities among resource agencies can lead to applications taking from months to years to pass all present regulatory
requirements. Unknown risks from novel approaches may further complicate and delay permitting decisions, although permitting requirements are also a mechanism for establishing best management practices to mitigate risk through standardized and informed implementation. Due to the urgency of initiating responses to growing coral reef losses, identification of management and policy challenges is an important consideration along with scientific and technical challenges.
The interventions discussed in this report have not been implemented beyond experimental scales in the ocean, if at all, making their efficacy and impacts uncertain. Adaptive management is thus important for assessing the readiness of interventions for implementation at meaningful scales and their ability to meet conservation goals. An adaptive management approach can help account for and resolve key uncertainties in management practices with uncertain results, such as the approaches described in this report (Holling, 1973; Walters, 1986; Walters and Holling, 1990). The first stage of the adaptive management cycle is planning, based on existing best practices rooted in available science as well as predictive models, which can range from conceptual to statistical to mathematical, that generate expected outcomes for prioritizing management options and managing potential risks. The second stage of the adaptive management cycle is then doing, i.e., implementing a management action or suite of actions, with monitoring to evaluate management efficacy. The third stage of the adaptive management cycle is learning through the comparison of monitoring data to model predictions, which allows identification of knowledge and management gaps. The subsequent management adjustment restarts the adaptive management cycle to continually improve management through time. This adaptive management process can take one of two forms: (1) “passive adaptive management” of trying one best-expected management option at a time, or (2) “active adaptive management” of trying multiple alternative approaches that might have analogous expectations as experiments. Active adaptive management controls for confounding environmental variability and therefore enhances learning and the long-term outcome, at a potential cost to short-term performance.
Effective monitoring in adaptive management requires clear objectives and careful scientific design (Legg and Nagy, 2006). In monitoring for reintroduction projects such as coral reef restoration, a sequence of success metrics, from survival to reproductive success to population growth, can provide near-term feedback and directly measure achievement of long-term goals (Seddon, 1999). While the interventions described
in this report share the long-term goal of increased coral persistence and resilience, the near-term monitoring metrics will inevitably vary by intervention. For example, temperature and its variability provide an immediate and easy-to-measure near-term metric of success for environmental interventions such as shading and mixing of cooling water. For genetic and physiological interventions such as managed selection, managed breeding, pre-exposure, and algal symbiont manipulation. “Omic” (genomic, transcriptomic, or proteomic) data could provide immediate and direct feedback on the increase in stress-tolerant genes or gene expression. Proteomics and transcriptomics can also provide near-term metrics of whether environmental interventions are successful at reducing stress on a level meaningful to coral gene expression and physiology. For any intervention involving coral gardening and outplanting, coral establishment, and growth serve as key near-term metrics of success. In the longer term, monitoring of community- and ecosystem-level metrics such as species diversity, persistence of key functional groups, and resilience to disturbance (SER, 2004) can inform achievement of the goal of maintaining functional coral reef ecosystems.
Monitoring potential drivers of failure (e.g., local stressors and conditions such as herbivore population sizes and sedimentation and pollution loads) is also necessary to engage in adaptive management (Armstrong and Seddon, 2008). While such drivers will factor into the “planning” stage as part of best practices for intervention approaches, given the inevitable variation in such factors between locations and through time, including them in the monitoring and “learning” stage as well will provide additional information for continued improvement of such best practices. For risky interventions such as many of those described here, monitoring of risk indicators (e.g., potential invasive species and diseases for managed relocation) can inform when to cease an intervention (if possible) to reduce the likelihood of unintended consequences.
Benefits, Risk, and Decision Making
Assessment of the state of research on novel approaches alone does not provide the information needed to make decisions about implementing these approaches at large scales in the open ocean. The interventions described in this report have varying degrees and likelihoods of benefits and risks. They alter the environment with consequences that cannot completely be foreseen given the state of knowledge. While adaptive management provides a structured way of improving understanding of these benefits and risks, even this cannot be implemented without the decision to deploy these interventions in the ocean at least at an experimental scale. The presence of risk is not itself a barrier to action when evaluated in the
context of the benefits they will confer. Additionally, comparison of these expected risks and benefits to the more traditional interventions (e.g., pollution reduction or marine protected areas) and to the risk of doing nothing is an important consideration, and one that will be dependent on the state of the environment and predicted risks to coral persistence.
The remainder of the committee’s task, to be documented in a subsequent report, is to provide a framework for evaluating the relative risks and benefits of implementing these interventions. Additionally, the committee will develop a decision pathway to guide movement of these interventions from the research phase to implementation, when and where appropriate. Such a framework can be used to identify intervention strategies for which the consequences and costs may be justified. While it is not the committee’s task to consider the social, policy, legal, and ethical considerations of implementing these approaches, these will be important to decision makers as well.
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