Coral reef managers are faced with a new decision crisis: deteriorating environmental conditions are reducing the health and functioning of coral reef ecosystems worldwide, creating a need for new management responses. Established tools for managing coral reefs are not sufficient or designed to preserve coral reefs as the climate changes. Increasing episodes of sustained above-average water temperatures have increased the frequency of coral bleaching events—during which corals expel their symbiotic algae—from which many corals do not recover (Hughes et al., 2018; NOAA, 2018). Increased temperatures are also linked to increasing disease prevalence, which has devastated reefs already in decline from multiple stressors (Carpenter et al., 2008; Harvell et al., 2007). As excess atmospheric carbon dioxide dissolves into the ocean and lowers the pH of seawater, corals will have a reduced ability to calcify and grow the hard skeletons that support the reef structure. These stresses will compound the impacts from local sources of stress such as pollution, habitat destruction, overfishing, and invasive species (Bellwood et al., 2004; Pandolfi et al., 2003).
Local stressors have historically been the main cause of coral reef loss and degradation, and control of local stressors is integral to continued coral persistence (Mcleod et al., 2019; see Bruno et al., 2019, for questions regarding the contribution of local management to coral reef resilience). However, even in areas free from local stress, coral reef cover is being lost (Hughes et al., 2017a). At the same time, limiting future greenhouse gas emissions is necessary to maintain a global environment
within which corals can survive; average temperature increases as little as 1°C to 2°C can lead to coral bleaching (Donner et al., 2005; Frieler et al., 2013; Hoegh-Guldberg, 1999; Sheppard, 2003; van Hooidonk et al., 2013, 2014). These powerful changes have driven interest in approaches that improve the ability of corals to survive in a high-emission environment (as described in NASEM, 2019). These “coral interventions” include those that affect the corals’ genetics, reproduction, physiology, ecology, or local environment. Many arise from a growing understanding of how the coral holobiont—the coral and its symbiotic algae and the rest of the microbiome—responds, acclimatizes, and adapts to stress. These interventions will alter the reef in some way, frequently by shifting population structures, altering genes, or changing the composition of symbiont communities. Their ultimate goal is stabilization or increases in coral cover, diversity, and reef functioning. However, these changes provide very different benefits across sites and may have unintended consequences that will similarly vary across locations.
A committee was convened by the National Academies of Sciences, Engineering, and Medicine to consider interventions that have the potential to increase the survival and persistence of coral reefs in deteriorating environmental conditions. This study was requested and funded by the National Oceanic and Atmospheric Administration, with additional support from the Paul G. Allen Family Foundation. In its first report (NASEM, 2019), the committee described 23 interventions that have the potential to increase the persistence of coral reefs as environmental conditions deteriorate. While management of the entire reef community is essential for coral persistence and delivery of vital reef services, the interventions explored by the committee are those that improve the resilience of individuals, populations, or communities of corals directly. Reef-associated species are often targets of existing management practices, such as control of overfishing and invasive species.
The committee has used the term “resilience” to refer to a system’s ability to both resist disturbances and recover from them (Edmunds et al., 2019; Holling, 1973; Hughes et al., 2010). To date, most of the conventional approaches used to manage reefs, such as improving water quality and managing herbivores, have tended to focus on ways that facilitate the recovery potential of reefs following disturbances, and many of these approaches have drawn their inspiration from the study of Caribbean reefs (e.g., Hughes, 1994). Most of the novel approaches and interventions discussed in this report and its predecessor (NASEM, 2019) emphasize approaches that increase the resistance of the coral organisms to disturbances (particularly climate change and disease) in order to avert widespread coral mortality, or for the community to recover to a coral-dominated state on its own through inclusion of stress-resistant types.
Note that the committee included some interventions that may improve coral persistence by reducing their exposure to disturbance, though this may not improve their resilience.
These interventions are summarized in Table 1.1. The interventions fall into four categories:
- Genetic and reproductive interventions provide an opportunity for increased selection and breeding of stress-tolerant traits that may improve the resilience of coral populations and species. In addition to naturally resilient corals or members of their microbiome, genetic manipulation may provide the opportunity to create corals that can withstand increasingly severe environmental conditions.
- Physiological interventions influence the physiological responses of corals without changing their genomes (though it may be through genetic mechanisms) through improvements in health and resilience.
- Coral population and community interventions seek to directly alter the composition of an entire population or communities of corals through managed relocation at varying scales—from movement within their range to across ocean basins.
- Environmental interventions reduce exposure of coral reefs to increasing temperatures or acidifying waters at a local level (as opposed to methods of global climate engineering).
The previous report reviews the state of science on each of the interventions covering the following categories: What It Is, How to Do It, Benefit and Goals, Current Feasibility, Potential Scale, Risk, Limitations, and Infrastructure. The report is a snapshot of a fast-moving field of research; for example, since publication of the report, Hagedorn et al. (2018) have published their demonstration of the use of cryopreserved coral sperm to conduct assisted gene flow across genetically isolated Acropora palmata populations in the Caribbean. While the information in the first report informs the framework laid out in this second report, it is important to realize that the state of science will continue to change. New ideas might arise, uncertainty might diminish, and perceptions of risks and benefits may change with new information.
Coral interventions have varying degrees of benefits and risks, and there are varying degrees of probability and certainty around these benefits and risks. At the same time, there is a strong possibility that the risks
TABLE 1.1 Overview of Interventions Examined in the Committee’s First 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 of 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|
of not intervening to increase coral persistence are growing as greenhouse gases continue to accumulate. Moreover, different interventions vary in their feasibility in different places and at different times. Whether action or inaction on specific interventions is more likely to produce coral reef gains is at the heart of the decision that will need to be made in local regions across the tropical oceans.
In this report, the committee builds on its first report by outlining the necessary components of a structured decision process and providing an example framework within which to evaluate the information available
about risks and benefits of novel interventions. The specific tasks of the committee are outlined in Box 1.1; this report addresses items 2 through 5. In addition to the workshops held in Miami, Florida, and Honolulu, Hawaii, during the development of its first report, the committee held an open meeting on October 30, 2018, in Washington, DC, with experts in decision science to explore these elements of its task.
The committee is not tasked with developing a framework that can be immediately applied to an individual area. This is primarily because it is outside the committee’s task to consider the social, policy, legal,
and ethical drivers that would be central to any management decisions. Because these drivers need to be defined and comprehensively explored with a broad set of stakeholders for any specific decision, the committee’s goal is to highlight universal concepts and best practices of structured decision making and provide an illustrative model of a simplified reef and decision scenario based on an example set of interventions. In Chapter 2, the committee first reviews the interventions from the first report to assess their practical readiness and context dependencies to illuminate how managers may select interventions most suited to their situation for further assessment in a decision framework. Chapter 3 describes the best practices for structured decision making and risk assessment for taking an intervention from research to inclusion in a management strategy, and the available decision tools that have been, or might be, applied to coral reef management. In Chapter 4, the committee provides an illustrative model and decision analysis to exemplify the challenges and insights associated with decision making around coral interventions. In Chapter 5, the committee identifies research areas that would inform decision making by improving understanding of the baseline reef system, assessing risks, and managing the beneficial impacts of potential interventions. Finally, Chapter 6 highlights the tropical western Atlantic/Caribbean region as a case study for how managers may consider their individual context and objectives in an evaluation of possible intervention strategies.
The process described in this report is meant to guide a particular component of the reef management decision process with which reef managers and other decision makers evaluate the risks and benefits of using innovative interventions within their restoration and conservation programs. Overarching questions driving the selection and implementation of interventions presented in this report begin with addressing the present status and trends of coral reefs in a jurisdiction, the needs of stakeholders, and the mandates of local, state, and federal regulatory agencies. Although the committee does not incorporate these broader questions into its example framework, highlighted here are the intersections with the committee’s task and other management considerations.
Management objectives against which to evaluate interventions are driven by the state of the ecological community and physical environment, local priorities, and risk tolerance in a particular area as well as ethical, economic, cultural, and legal constraints. A clear articulation of objectives is a vital component of the decision process described in this report. Management agencies have the dual responsibilities of protecting both reef resources and the people who depend on them. Thus, the
anticipated outcomes of any intervention will be tied to the objectives of affected human communities. Because these ecosystems provide a variety of ecological, cultural, and economic services, and are at various stages of health, the selection of interventions will vary among sites and jurisdictions. For example, to address the need for coastal protection from wave damage, coral species with massive growth morphologies might be the appropriate choice for restoration and management objectives, as they are often more resistant to wave energy, sediment, and turbidity than branching corals (Ferrario et al., 2014). Alternatively, to replace essential fish habitat through enhanced rugosity, the use of branching, table, columnar, and arborescent growth forms would be appropriate (Komyakova et al., 2018). Rugosity, or structural complexity, is also an important attribute supporting coral larval recruitment, and provides spatial refugia for ultraviolet-sensitive and less competitive species and life history stages. Such differences in objectives from place to place might be a common feature of coral management. The clarification of these objectives is an important starting point in the evaluation of management options, described further in Chapter 3.
A key influence on management options is the existing regulatory framework, through which management authorities, such as permitting and other approvals, are distributed across local, regional, state, and/or federal entities. For example, in the United States, there are eight jurisdictions that possess and regulate reef-building corals: the states of Florida, Hawaii, and Texas; the Territories of American Samoa, Guam, and the U.S. Virgin Islands; and the Commonwealths of the Northern Mariana Islands and Puerto Rico. The U.S. federal government has sole authority and responsibility for other coral reef areas including the Pacific Remote Islands (U.S. Minor Outlying Islands), which are part of a Marine National Monument. Additionally, there are the three Freely Associated States, which receive federal funding under the Compacts of Free Association (the Federated States of Micronesia, the Republic of the Marshall Islands, and the Republic of Palau). In all cases, any activity that includes U.S. federal funding must comply with the appropriate U.S. federal regulations.
There are 14 laws and statutes that regulate activities involving corals in the United States (summarized in Richmond et al., 2007):
- 1899—Rivers and Harbors Act (33 U.S.C. § 403)
- 1900—Lacey Act (16 U.S.C. §§ 3371-3378)
- 1958—Fish and Wildlife Coordination Act (16 U.S.C. §§ 661-667e)
- 1969—National Environmental Policy Act (NEPA) (codified as amended at 42 U.S.C. § 4321 et seq.).
- 1970—Council on Environmental Quality (§ 201 [42 U.S.C. §§ 4341-4347 and 4372-4375] under NEPA)
- 1972—Coastal Zone Management Act (codified as amended at 16 U.S.C. §§ 1451-1466)
- 1973—Endangered Species Act (16 U.S.C. §§ 1531-1544)
- 1975—Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES; the United States is a signatory)
- 1977—Clean Water Act (codified as amended at 33 U.S.C. §§ 1251-1387)
- 1980—Comprehensive Environmental Response, Compensation, and Liability Act (CERCLA) (codified as amended at 42 U.S.C. §§ 9601-9675)
- 1996—Magnuson-Stevens Fishery Conservation and Management Act (codified as amended at 16 U.S.C. §§ 1801 et seq.)
- 1998—Executive Order No. 13089, 3 C.F.R. § 193 on Coral Reef Protection
- 2000—Executive Order No. 13158, 3 C.F.R. § 34909 on Marine Protected Areas
- 2000—Coral Reef Conservation Act (16 U.S.C. §§ 6401 et seq.)
The overriding philosophy behind a set of regulations is to prevent activities that harm corals and coral reefs. This can create challenges for activities and interventions that intend to restore reef resources but that also have unintended or unknown risks. By permitting and/or funding these activities, the various federal and local agencies balance allowing activities that might damage corals with the likelihood of damage should no action be taken. Without clear recognition of how and when inaction could result in greater resource losses than the interventions identified by the committee, there may be difficulty fitting new interventions into the existing regulatory framework. It is important that addressing the regulatory and policy framework for intervention implementation be undertaken concurrently with the scientific and management-directed tasks. Although this is not within the scope of this report, the ability to evaluate risks and benefits, which is the focus of the report, will still be important for informing future regulatory and policy changes.
Social Capital and Stakeholder Buy-in
Coral reefs are social-ecological systems; humans are responsible for the greatest threats to reef persistence and resilience, yet are also among the primary beneficiaries of healthy and functional coral ecosystems that provide a variety of ecosystem services and benefit streams (Anthony et al., 2015; Aswani et al., 2015; Cinner et al., 2009; Folke, 2006; Hicks et al., 2015; Hughes et al., 2017b; Kittinger et al., 2012). Under global environmental change, ecological, economic, and social elements of reefs will all
be affected, and both conventional and new management strategies thus need to incorporate the environmental and human dimensions. With the well-recognized economic, ecological, and cultural benefits of coral reefs to hundreds of millions of people worldwide (Burke et al., 2011), there are many stakeholder groups that are interested and involved in the decisions surrounding interventions that sustain these ecosystems. There is an important role for the social sciences to be included in future intervention study design, implementation efforts, and the collection of evaluation effectiveness metrics.
A decision pathway from theory to practice involves a multitude of stakeholders. Novel approaches have originated from the growing understanding of coral biology and ecology, which inspires new theories on which new interventions are built. While experimentation in controlled laboratory settings can inform the potential of many intervention approaches, moving into the field improves real-world understanding. This will significantly increase capacity needs, including for data collection and development of models that support decision making. Additionally, cooperation and collaboration with resource managers in one or multiple jurisdictions will inform research priorities and ensure regulatory compliance. Coordinating and convening activities among managers and stakeholders help integrate management strategies, align science with policy, and facilitate buy-in from the general public. In the United States, the Coral Reef Task Force established in 1998 under Executive Order 13089 is already functioning in this convening role and can move quickly to develop guidance and lines of responsibility for intervention strategies.
When developing its first report, the committee was unable to find or estimate potential costs of deploying the interventions; however, just like risks and benefits, costs are likely to vary across interventions and over time. Generally, research and development costs will be high in the early stages, and can decrease as technologies are refined. For example, initial costs of selective breeding might include genotyping, husbandry, outplanting of offspring, and monitoring. Some of these costs might be able to be estimated, but only in a research setting and not at regional or global scales. Deployment after the research and development phase can require large investments in infrastructure or in operations, depending on the intervention. It is important to note that costs of deploying an intervention would be evaluated against the expected benefit, as well as the cost of inaction. It is not in the committee’s scope to do a cost–benefit analysis, but it is important to note that the ecosystem services provided by coral reefs provide high monetary value (e.g., Beck et al., 2018; Costanza et al.,
2014; Storlazzi et al., 2019) and expensive approaches could be justified. For example, the Great Barrier Reef contributed an estimated $6.4 billion to the Australian economy from 2015 to 2016, mainly from tourism but also from fishing, recreation, and scientific activities (Deloitte Access Economics, 2017). Global estimates of the economic value of coral reefs to fisheries, tourism, coastal protection, and biodiversity value (research, conservation, and nonuse) are on the order of $30 billion (Burke et al., 2011; Cesar et al., 2003).
The scale of the problem is massive; global environmental change is causing tropical reefs around the world to be susceptible to increasing loss and degradation. Reef managers will necessarily be addressing coral reef persistence at smaller scales. An important, though not essential, consideration for selecting interventions is their ability to be implemented at relatively large scales. Many small-scale efforts are possible, but expensive. Interventions that depend on coral gardening approaches will benefit from improvements made in the field of restoration. Scalability can be achieved through research, such as in the development of new treatment methods. For example, it is possible to treat individual coral polyps or colonies with antibiotics or nutritional supplements, but there are no known methods of deployment to an entire reef without expensive individual treatments or risky broadcasts to an entire reef. Ultimately, the ability to scale the wide-ranging approaches will vary.