Daily Rules, Proposed Rules, and Notices of the Federal Government
You can obtain the petition and reference materials regarding this determination via the NMFS Pacific Island Regional Office Web site:
On October 20, 2009, the Center for Biological Diversity (CBD) petitioned us to list 83 reef-building coral species as either threatened or endangered under the ESA and to designate critical habitat. The 83 species included in the petition are:
On February 10, 2010, we published a positive 90-day finding (75 FR 6616; February 10, 2010) in which we described our determination that the petition contained substantial scientific and commercial information indicating that the petitioned actions may be warranted for all of the petitioned species except the Caribbean species
The ESA requires us to make determinations on whether species are threatened or endangered “solely on the basis of the best scientific and commercial data available * * * after conducting a review of the status of the species * * * ” (16 U.S.C. 1533). Further, consistent with case law, our implementing regulations specifically direct us not to take possible economic or other impacts of listing species into consideration (50 CFR 424.11(b)). In order to conduct a comprehensive status review for this petition, given the number of species, the geographic scope and issues surrounding coral biology and extinction risk, we convened a Coral Biological Review Team (BRT) composed of seven Federal scientists from NMFS' Pacific Islands, Northwest, and Southeast Fisheries Science Centers, as well as the U.S. Geological Survey and National Park Service. The members of the BRT are a diverse group of scientists with expertise in coral biology, coral ecology, coral taxonomy, physical oceanography, global climate change, and coral population dynamics. The BRT's comprehensive, peer-reviewed Status Review Report (SRR, Brainard
On April 17, 2012, we published a
Therefore, the 82 candidate coral species comprehensive status review consists of the SRR (Brainard
We are responsible for determining whether each of the 82 candidate corals are threatened or endangered under the ESA (16 U.S.C. 1531
This finding begins with an overview of coral biology, ecology, and taxonomy in the Introduction to Corals and Coral Reefs section below, which also discusses whether each candidate species meets the definition of a “species” for purposes of the ESA. Other relevant background information in this section includes the general characteristics of the habitats and environments in which the 82 candidate species are found. The finding then summarizes information on factors adversely affecting and posing extinction risk to corals in general in the Threats to Coral Species section. The Risk Analyses section then describes development and application of the Determination Tool that resulted in proposed listing statuses for the 82 candidate species.
Corals are marine invertebrates in the phylum Cnidaria that occur as polyps, usually forming colonies of many clonal polyps on a calcium carbonate skeleton. The Cnidaria include true stony corals (class Anthozoa, order Scleractinia), the blue coral (class Anthozoa, order Helioporacea), and fire corals (class Hydrozoa, order Milleporina). Members of these three orders are represented among the 82 candidate coral species (79 Scleractinia, one Helioporacea, and two Milleporina). All 82 candidate species are reef-building corals, because they secrete massive calcium carbonate skeletons that form the physical structure of coral reefs. Reef-building coral species collectively produce coral reefs over time in high-growth conditions, but these species also occur in non-reef habitats (
Most reef-building coral species are in the order Scleractinia, consisting of over 25 families, 100 genera, and the great majority of the approximately 800 species. Most Scleractinian corals form complex colonies made up of a tissue layer of polyps (a column with mouth and tentacles on the upper side) growing on top of a calcium carbonate skeleton, which the polyps produce through the process of calcification. Scleractinian corals are characterized by polyps with multiples of six tentacles around the mouth for feeding and capturing prey items in the water column. In contrast, the blue coral,
Reef-building coral species are capable of rapid calcification rates because of their symbiotic relationship with single-celled dinoflagellate algae, zooxanthellae, which occur in great numbers within the host coral tissues. Zooxanthellae photosynthesize during the daytime, producing an abundant source of energy for the host coral that enables rapid growth. At night, polyps extend their tentacles to filter-feed on microscopic particles in the water column such as zooplankton, providing additional nutrients for the host coral. In this way, reef-building corals obtain nutrients autotrophically (
In addressing the species question, the BRT had to address issues related to the considerable taxonomic uncertainty in corals (
Studies elucidating complex taxonomic histories were available for several of the genera addressed in the status review, and the BRT was able to incorporate those into their species determinations. Thus, while the BRT made species determinations for most of the 82 candidate coral species on the nominal species included in the petition, it deliberated on the proper taxonomic classification for the candidate species
Corals use a number of diverse reproductive strategies that have been researched extensively; however, many individual species' reproductive modes remain poorly described. Most coral species use both sexual and asexual propagation. Sexual reproduction in corals is primarily through gametogenesis (
Depending on the mode of fertilization, coral larvae (called planulae) undergo development either mostly within the mother colony (brooders) or outside of the mother colony, adrift in the ocean (broadcast spawners). In either mode of larval development, planula larvae presumably experience considerable mortality (up to 90 percent or more) from predation or other factors prior to settlement and metamorphosis. (Such mortality cannot be directly observed, but is inferred from the large amount of eggs and sperm spawned versus the much smaller number of recruits observed later.) Coral larvae are relatively poor swimmers; therefore, their dispersal distances largely depend on the duration of the pelagic phase and the speed and direction of water currents transporting the larvae. The documented maximum larval life span is 244 days (
The spatial and temporal patterns of coral recruitment have been studied extensively. Biological and physical factors that have been shown to affect spatial and temporal patterns of coral recruitment include substratum availability and community structure, grazing pressure, fecundity, mode and timing of reproduction, behavior of larvae, hurricane disturbance, physical oceanography, the structure of established coral assemblages, and chemical cues. Additionally, factors other than dispersal may influence recruitment and several other factors may influence reproductive success and reproductive isolation, including external cues, genetic precision, and conspecific signaling.
In general, on proper stimulation, coral larvae, whether brooded by parental colonies or developed in the water column, settle and metamorphose on appropriate substrates. Some evidence indicates that chemical cues from crustose coralline algae, microbial films, and/or other reef organisms or acoustic cues from reef environments stimulate settlement behaviors. Initial calcification ensues with the forming of the basal plate. Buds formed on the initial corallite develop into daughter corallites. Once larvae are able to settle onto appropriate hard substrate, metabolic energy is diverted to colony growth and maintenance. Because newly settled corals barely protrude above the substrate, juveniles need to reach a certain size to limit damage or mortality from threats such as grazing, sediment burial, and algal overgrowth. Once recruits reach about 1 to 2 years post-settlement, growth and mortality rates appear similar across species. In some species, it appears that there is virtually no limit to colony size beyond structural integrity of the colony skeleton, as polyps apparently can bud indefinitely.
Corals need hard substrate on which to settle and form; however, only a narrow range of suitable environmental conditions allows the growth of corals and other reef calcifiers to exceed loss from physical, chemical, and biological erosion. While corals do live in a fairly wide temperature range across geographic locations, accomplished via either adaptation (genetic changes) or acclimatization (physiological or phenotypic changes), reef-building corals do not thrive outside of an area characterized by a fairly narrow mean temperature range (typically 25 °C-30 °C). Two other important factors influencing suitability of habitat are light and water quality. Reef-building corals require light for photosynthetic performance of their zooxanthellae, and poor water quality can negatively affect both coral growth and recruitment. Deep distribution of corals is generally limited by availability of light. Hydrodynamic condition (
The 82 candidate coral species are distributed throughout the wider-Caribbean (
Determining abundance of the 82 candidate coral species presented a unique challenge because corals are clonal, colonial invertebrates, and colony growth occurs by the addition of new polyps. Colonies can exhibit partial mortality in which a subset of the polyps in a colony dies, but the colony persists. Colonial species present a special challenge in determining the appropriate unit to evaluate for status (
Quantitative abundance estimates were available for only a few of the candidate species. In the Indo-Pacific, many reports and long-term monitoring programs describe coral percent cover only to genus level because of the substantial diversity within many genera and difficulties in field identification among congeneric species. In the Caribbean, most of the candidate species are either too rare to document meaningful trends in abundance from literature reports (
A coral reef is a complex three-dimensional structure providing habitat, food, and shelter for numerous marine species and, as such, fostering exceptionally high biodiversity. Scleractinian corals produce the physical structure of coral reefs, and thus are foundational species for these generally productive ecosystems. It has been estimated that coral reef ecosystems harbor around one-third of all marine species even though they make up only 0.2 percent in area of the marine environment. Coral reefs serve the following essential functional roles: Primary production and recycling of nutrients in relatively nutrient poor (oligotrophic) seas, calcium carbonate deposition yielding reef construction, sand production, modification of near-field or local water circulation patterns, and habitat for secondary production, including fisheries. These functional roles yield important ecosystem services in addition to direct economic benefits to human societies such as traditional and cultural uses, food security, tourism, and potential biomedical compounds. Coral reefs protect shorelines, coastal ecosystems, and coastal inhabitants from high seas, severe storm surge, and tsunamis.
As described above in Distribution and Abundance, reef-building corals have specific habitat requirements, including hard substrate, narrow mean temperature range, adequate light, and adequate water flow. These habitat requirements most commonly occur on shallow tropical and subtropical coral reefs, but also occur in non-reefal and mesophotic areas (NMFS 2012b, SIR Section 4.3). While some reef-building corals do not require hard substrates, all of the 82 candidate species in this status review do require hard substrates. Thus, in this finding, “non-reefal habitat” refers to hard substrates where reef-building corals can grow, including marginal habitat where conditions prevent reef development (
The Caribbean and Indo-Pacific basins contrast greatly both in size and in condition. The Caribbean basin is geographically small and partially enclosed, has high levels of connectivity, and has relatively high human population densities. The wider-Caribbean occupies five million square km of water and has 55,383 km of coastline, including approximately 5,000 islands. Shallow coral reefs occupy approximately 25,000 square km (including ≉2,000 square km within US waters), or about 10 percent of the total shallow coral reefs of the world. The amount of non-reefal and mesophotic habitat that could potentially be occupied by corals in the Caribbean is unknown, but is likely greater than the area of shallow coral reefs in the Caribbean (NMFS 2012b, SIR Section 4.3).
The Caribbean region has experienced numerous disturbances to coral reef systems throughout recorded human history. Fishing has affected Caribbean reefs since before European contact. Beginning in the early 1980s, a series of basin-scale disturbances has led to altered community states, and a loss of resilience (
Caribbean-wide meta-analyses suggest that the current combination of disturbances, stressful environmental factors such as elevated ocean temperatures, nutrients and sediment loads, and reduced observed coral reproduction and recruitment have yielded poor resilience, even to natural disturbances such as hurricanes. Coral cover (percentage of reef substrate occupied by live coral) across the region has declined from approximately 50 percent in the 1970s to approximately 10 percent in the early 2000s (
With the exception of coral reefs in the eastern Pacific, ocean basin size and diversity of habitats, as well as some vast expanses of ocean area with only very local, spatially-limited, direct human influences, have provided substantial buffering of Indo-Pacific corals from many of the threats and declines manifest across the Caribbean. The Indo-Pacific is enormous (Indian and Pacific Oceans) and hosts much greater coral diversity than the Caribbean region (∼700 species compared with 65 species). The Indo-Pacific region encompasses the tropical and sub-tropical waters of the Indian Ocean, the western and central Pacific Ocean, and the seas connecting the two in the general area of Indonesia. This vast region occupies at least 60 million square km of water (more than ten times larger than the Caribbean), and includes 50,000 islands and over 40,000 km of continental coastline, spanning approximately 180 degrees of longitude and 60 degrees of latitude. There are approximately 240,000 square km of shallow coral reefs in this vast region, which is more than 90 percent of the total coral reefs of the world. In addition, the Indo-Pacific includes abundant non-reefal habitat, as well as vast but scarcely known mesophotic areas that provide coral habitat. The amount of non-reefal and mesophotic habitat that could potentially be occupied by corals in the Indo-Pacific is unknown, but is likely greater than the area of shallow coral reefs in the Indo-Pacific (NMFS, 2012b; SIR Section 4.3).
While the reef communities in the Caribbean have lost resilience, the reefs in the central Pacific (
Even given the relatively higher resilience in the Indo-Pacific as compared to the Caribbean, meta-analysis of overall coral status throughout the Indo-Pacific indicates that substantial loss of coral cover (
In the eastern Pacific (from Mexico in the north to Ecuador in the south, and from the coast west out to the remote Revillagigedo, Clipperton, Cocos, Malpelo, and Galápagos Islands), coral reefs are exposed to a number of conditions that heighten extinction risk. Compared to the Caribbean, coral reefs in the eastern Pacific have approximately one third as many genera, less than half the species, less reef area, and strong regional climate variability. Severe climate swings typical of the region continue to be a hindrance to reef growth today, with major losses of coral cover and even entire reefs lost from Mexico to the Galápagos Islands. Regional climatic variability not only has killed corals in recent decades, it has resulted in major loss of reef structure. This regional climatic variability produces extreme temperature variability (both extreme upwelling and high temperatures during El Niño), storm events, and changes in the abundance, distribution, and behavior of both corallivores and bioeroders. Eastern Pacific reefs have been among the slowest in the world to recover after disturbance. Additionally, the naturally low calcium carbonate saturation state of eastern Pacific waters has made these reefs among the most fragile and subject to bioerosion in the world. In conclusion, there have been
Section 4(a)(1) of the ESA and NMFS's implementing regulations (50 CFR 424) state that the agency must determine whether a species is endangered or threatened because of any one or a combination of five factors: (A) Present or threatened destruction, modification, or curtailment of habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) inadequacy of existing regulatory mechanisms; or (E) other natural or manmade factors affecting its continued existence. The BRT evaluated factors A, B, C, and E in the SRR; the “Inadequacy of Regulatory Mechanisms” (factor D) is evaluated separately in this 12-month Finding and is informed by the Final Management Report. Our consideration of the five factors was further informed by information received during the public engagement period and provided in the SIR, as explained in more detail below. The BRT identified factors acting directly as stressors to the 82 coral species (
We established that the appropriate period of time corresponding to the foreseeable future is a function of the particular type of threats, the life-history characteristics, and the specific habitat requirements for coral species under consideration. The timeframe established for the foreseeable future takes into account the time necessary to provide for the conservation and recovery of each threatened species and the ecosystems upon which they depend, but is also a function of the reliability of available data regarding the identified threats and extends only as far as the data allow for making reasonable predictions about the species' response to those threats. As described below, the more vulnerable a coral species is to the threats with the highest influence on extinction risk (
The BRT qualitatively ranked each threat as high, medium, low, or negligible (or combinations of two;
Overall, the BRT identified 19 threats (see Table 1) as posing either current or future extinction risk to the 82 corals. Of these, the BRT considers ocean warming, ocean acidification, and disease to be overarching and influential in posing extinction risk to each of the 82 candidate coral species. These impacts are or are expected to become ubiquitous, and pose direct population disturbances (mortality and/or impaired recruitment) in varying degrees to each of the candidate coral species. There is also a category of threats (some of which have been responsible for great coral declines in the past) that the BRT considers important to coral reef ecosystems, but of medium influence in posing extinction risk because their effects on coral populations are largely indirect and/or local to regional in spatial scale. This category includes fishing, sea level rise, and water quality issues related to sedimentation and nutrification. The remaining threats can be locally acute, but because they affect limited geographic areas, are considered to be of minor overall importance in posing extinction risk. Examples in this category are predator outbreaks or collection for the ornamental trade. These types of threats, although minor overall, can be important in special cases, such as for species with extremely narrow geographic ranges and/or those species at severely depleted population levels. Based on the BRT's characterization of the threats to corals, the most important threats to the extinction risk of reef-building corals are shown in Table 1 below, and described below. The description of the remaining ten threats can be found in the SRR and SIR. While these ten threats did not rank highly in their contribution to extinction risk, they do adversely affect the species.
While we received and collected numerous sources of information during the public engagement period pertaining to the 19 threats identified in the SRR, no new threats were identified, and no new information suggested changes to their relative importance. However, some of the new information is relevant to characterizing the important threats, particularly those related to Global Climate Change, and is included in the sections below.
Several of the most important threats contributing to the extinction risk of corals are related to global climate change. Thus, we provide a general overview of the state of the science related to climate change before discussing each threat and its specific impacts on corals. The main concerns regarding impacts of climate change on coral reefs generally, and on the 82 candidate coral species in particular, are the magnitude and the rapid pace of change in greenhouse gas (GHG) concentrations (
Supplemental information gathered during the public engagement period shows that global temperatures continue to increase and that temperature patterns differ regionally. New models (Representative Concentration Pathways or RCPs) developed for the Intergovernmental Panel on Climate Change (IPCC) Fifth Assessment Report (due to publish in 2014) result in a larger range of temperature estimates than the range of scenarios IPCC Fourth Assessment Report (Special Reports on Emission Scenarios or SRES), but the global mean temperature projections by the end of the twenty-first century for the RCPs are very similar to those of their closest SRES counterparts. Another study used the second-generation Canadian earth system model (CanESM2) to project future warming under three of the new RCPs and found simulated atmospheric warming of 2.3
As described above and shown in Table 1, the BRT considered nine threats to be the most important to the current or expected future extinction risk of reef-building corals: ocean warming, coral disease, ocean acidification, trophic effects of reef fishing, sedimentation, nutrients, sea-level rise, predation, and collection and trade. Vulnerability of a coral species to a threat is a function of susceptibility and exposure, considered at the appropriate spatial and temporal scales. In this finding, the spatial scale is the current range of the species, and the temporal scale is from now until the year 2100. Susceptibility, exposure, and vulnerability are described generally below, and species-specific threat vulnerabilities are described in the Vulnerability to Threats under Risk Analyses below.
Susceptibility refers to the response of coral colonies to the adverse conditions produced by the threat. Susceptibility of a coral species to a threat is primarily a function of biological processes and characteristics, and can vary greatly between and within taxa (
Vulnerability of a coral species to a threat also depends on the proportion of colonies that are exposed to the threat. Exposure is primarily a function of physical processes and characteristics that limit or moderate the impact of the threat across the range of the species. For example, prevailing winds may moderate exposure of coral colonies on windward sides of islands to ocean warming, tidal fluctuations may moderate exposure of coral colonies on reef flats to ocean acidification, and large distances of atolls from runoff may moderate exposure of the atoll's coral colonies from sedimentation.
Vulnerability of a coral species to a threat is a function of susceptibility and exposure, considered at the spatial scale of the entire current range of the species, and the temporal scale of from now to the year 2100. For example, a species that is highly susceptible to a threat is not necessarily highly vulnerable to the threat, if exposure is low over the appropriate spatial and temporal scales. Consideration of the appropriate spatial (range of species) and temporal (to 2100) scales is particularly important, because of high variability in the threats over the large spatial scales, and the predictions in the SRR that nearly all threats are likely to increase over the large temporal scale. The nine most important threats are summarized below, including general descriptions of susceptibility and exposure. Species-specific threat vulnerabilities are described in the Vulnerability to Threats under the Risk Analyses section.
Ocean warming is considered under ESA Factor E—other natural or manmade factors affecting the continued existence of the species—because the effect of the threat results from human activity and affects individuals of the species directly, and not their habitats. Mean seawater temperatures in reef-building coral habitat in both the Caribbean and Indo-Pacific have increased during the past few decades, and are predicted to continue to rise between now and 2100. More importantly, the frequency of warm-season temperature extremes (warming events) in reef-building coral habitat in both the Caribbean and Indo-Pacific has increased during the past two decades, and is also predicted to increase between now and 2100.
Ocean warming is one of the most important threats posing extinction risks to the 82 candidate coral species; however, individual susceptibility varies among species. The primary observable coral response to ocean warming is bleaching of adult coral colonies, wherein corals expel their symbiotic zooxanthellae in response to stress. For corals, an episodic increase of only 1°C-2°C above the normal local seasonal maximum ocean temperature can induce bleaching. Corals can withstand mild to moderate bleaching; however, severe, repeated, or prolonged bleaching can lead to colony death. While coral bleaching patterns are complex, with several species exhibiting seasonal cycles in symbiotic dinoflagellate density, thermal stress has led to bleaching and associated mass mortality in many coral species during the past 25 years. In addition to coral bleaching, other effects of ocean warming detrimentally affect virtually every life-history stage in reef-building corals. Impaired fertilization, developmental abnormalities, mortality, impaired settlement success, and impaired calcification of early life phases have all been documented.
In evaluating extinction risk from ocean warming, the BRT relied heavily on the IPCC Fourth Assessment Report because the analyses and synthesis of information developed for it are the most thoroughly documented and reviewed assessments of future climate and represent the best available scientific information on potential future changes in the earth's climate system. Emission rates in recent years have met or exceeded levels found in the worst-case scenarios considered by the IPCC, resulting in all scenarios underestimating the projected climate condition. Further, newer studies have become available since the completion of the SRR. New information suggests that regardless of the emission concentration pathway, more than 97 percent of reefs will experience severe thermal stress by 2050. However, new information also highlights the spatial and temporal “patchiness” of warming, as described in the next paragraph. This patchiness has the potential to provide refugia for the species from thermal stress if the temperature patches are spatially and temporally consistent, but the distributional nature of the patchiness is not currently well understood (NMFS 2012b, SIR Section 3.2.2).
Spatially, exposure of colonies of a species to ocean warming can vary greatly across its range, depending on colony location (
Temporally, exposure of colonies of a species to ocean warming between now and 2100 will likely vary annually and decadally, while increasing over time, because: (1) Numerous annual and decadal processes that affect seawater temperatures will continue to occur in the future (
Multiple threats stress corals simultaneously or sequentially, whether the effects are cumulative (the sum of individual stresses) or interactive (
There is also mounting evidence that warming ocean temperatures can have direct impacts on early life stages of corals, including abnormal embryonic development at 32°C and complete fertilization failure at 34°C for one Indo-Pacific
Finally, warming is and will continue causing increased stratification of the upper ocean, because water density decreases with increasing temperature. Increased stratification results in decreased vertical mixing of both heat and nutrients, leaving surface waters warmer and nutrient-poor. While the implications for corals and coral reefs of these increases in warming-induced stratification have not been well studied, it is likely that these changes will both exacerbate the temperature effects described above (
Overall, there is ample evidence that climate change (including that which is already committed to occur from past GHG emissions and that which is reasonably certain to result from continuing and future emissions) will follow a trajectory that will have a major impact on corals. If many coral species are to survive anticipated global warming, corals and their zooxanthellae will have to undergo significant acclimatization and/or adaptation. There has been a recent research emphasis on the processes of acclimatization and adaptation in corals, but, taken together, the body of research is inconclusive on how these processes may affect individual corals' extinction risk, given the projected intensity and rate of ocean warming (NMFS 2012b, SIR Section 18.104.22.168). In determining extinction risk for the 82 candidate coral species, the BRT was most strongly influenced by observations that corals have been bleaching and dying under ocean warming that has already occurred. Thus, the BRT determined that ocean warming and related impacts of global climate change are already having serious negative impacts on many corals, and that ocean warming is one of the most important threats posing extinction risks to the 82 candidate coral species between now and the year 2100 (Brainard
Disease is considered under ESA Factor C—disease or predation. Disease adversely affects various coral life history events, including causing adult mortality, reducing sexual and asexual reproductive success, and impairing colony growth. A diseased state results from a complex interplay of factors including the cause or agent (