Daily Rules, Proposed Rules, and Notices of the Federal Government


National Oceanic and Atmospheric Administration

50 CFR Parts 223 and 224

[Docket No. 0911231415-2625-02]

RIN 0648-XT12

Endangered and Threatened Wildlife and Plants: Proposed Listing Determinations for 82 Reef-Building Coral Species; Proposed Reclassification ofAcropora palmataandAcropora cervicornisfrom Threatened to Endangered

AGENCY: National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA), Commerce.
ACTION: Proposed rule; request for comments.
SUMMARY: We, NMFS, have completed comprehensive status reviews under the Endangered Species Act (ESA) of 82 reef-building coral species in response to a petition submitted by the Center for Biological Diversity (CBD) to list the species as either threatened or endangered. We have determined, based on the best scientific and commercial data available and efforts being made to protect the species, that 12 of the petitioned coral species warrant listing as endangered (five Caribbean and seven Indo-Pacific), 54 coral species warrant listing as threatened (two Caribbean and 52 Indo-Pacific), and 16 coral species (all Indo-Pacific) do not warrant listing as threatened or endangered under the ESA. Additionally, we have determined, based on the best scientific and commercial information available and efforts undertaken to protect the species, two Caribbean coral species currently listed warrant reclassification from threatened to endangered. We are announcing that 18 public hearings will be held during the public comment period to provide additional opportunities and formats to receive public input. SeeSUPPLEMENTARY INFORMATIONfor public hearing dates, times, and locations.
DATES: Comments on this proposal must be received by March 7, 2013. SeeSUPPLEMENTARY INFORMATIONfor public hearing dates, times, and locations.
ADDRESSES: *Electronic Submission:Submit all electronic public comments via the Federal e-Rulemaking submit comments via the e-Rulemaking Portal, first click the "submit a comment" icon, then enter NOAA-NMFS-2010-0036 in the keyword search. Locate the document you wish to comment on from the resulting list and click on the "Submit a Comment" icon on the right of that line.

*Mail:Submit written comments to Regulatory Branch Chief, Protected Resources Division, National Marine Fisheries Service, Pacific Islands Regional Office, 1601 Kapiolani Blvd., Suite 1110, Honolulu, HI 96814; or Assistant Regional Administrator, Protected Resources, National Marine Fisheries Service, Southeast Regional Office, 263 13th Avenue South, Saint Petersburg, FL 33701, Attn: 82 coral species proposed listing.

*Fax:808-973-2941;Attn:Protected Resources Regulatory Branch Chief; or 727-824-5309; Attn: Protected Resources Assistant Regional Administrator.

Instructions:You must submit comments by one of the above methods to ensure that we receive, document, and consider them. Comments sent by any other method, to any other address or individual, or received after the end of the comment period, may not be considered. All comments received are a part of the public record and will generally be posted for public viewing onwww.regulations.govwithout change. All personal identifying information (e.g.,name, address, etc.) you submit will be publicly accessible. Do not submit confidential business information, or otherwise sensitive or protected information. We will accept anonymous comments (enter "N/A" in the required fields if you wish to remain anonymous). Attachments to electronic comments will be accepted in Microsoft Word or Excel, WordPerfect, or Adobe PDF file formats only.

You can obtain the petition and reference materials regarding this determination via the NMFS Pacific Island Regional Office Web site:;NMFS Southeast Regional Office Web site:;NMFS HQ Web site:;or by submitting a request to the Regulatory Branch Chief, Protected Resources Division, National Marine Fisheries Service, Pacific Islands Regional Office, 1601 Kapiolani Blvd., Suite 1110, Honolulu, HI 96814, Attn: 82 coral species. SeeSUPPLEMENTARY INFORMATIONfor public hearing dates, times, and locations.

FOR FURTHER INFORMATION CONTACT: Chelsey Young, NMFS, Pacific Islands Regional Office, 808-944-2137; Lance Smith, NMFS, Pacific Island Regional Office, 808-944-2258; Jennifer Moore, NMFS, Southeast Regional Office, 727-824-5312; or Marta Nammack, NMFS, Office of Protected Resources, 301-427-8469.

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:Acanthastrea brevis, Acanthastrea hemprichii, Acanthastrea ishigakiensis, Acanthastrea regularis, Acropora aculeus, Acropora acuminata, Acropora aspera, Acropora dendrum, Acropora donei, Acropora globiceps, Acropora horrida, Acropora jacquelineae, Acropora listeri, Acropora lokani, Acropora microclados, Acropora palmerae, Acropora paniculata, Acropora pharaonis, Acropora polystoma, Acropora retusa, Acropora rudis, Acropora speciosa, Acropora striata, Acropora tenella, Acropora vaughani, Acropora verweyi, Agaricia lamarcki, Alveopora allingi, Alveopora fenestrata, Alveopora verrilliana, Anacropora puertogalerae, Anacropora spinosa, Astreopora cucullata, Barabattoia laddi, Caulastrea echinulata, Cyphastrea agassizi, Cyphastrea ocellina, Dendrogyra cylindrus, Dichocoenia stokesii, Euphyllia cristata, Euphyllia paraancora, Euphyllia paradivisa, Galaxea astreata, Heliopora coerulea, Isopora crateriformis, Isopora cuneata, Leptoseris incrustans, Leptoseris yabei, Millepora foveolata, Millepora tuberosa, Montastraea annularis, Montastraea faveolata, Montastraea franksi, Montipora angulata, Montipora australiensis, Montipora calcarea, Montipora caliculata, Montipora dilatata, Montipora flabellata, Montipora lobulata, Montipora patula, Mycetophyllia ferox, Oculina varicosa, Pachyseris rugosa, Pavona bipartita, Pavona cactus, Pavona decussata, Pavona diffluens, Pavona venosa, Pectinia alcicornis, Physogyra lichtensteini, Pocillopora danae, Pocillopora elegans, Porites horizontalata, Porites napopora, Porites nigrescens, Porites pukoensis, Psammocora stellata, Seriatopora aculeata, Turbinaria mesenterina, Turbinaria peltata, Turbinaria reniformis,andTurbinaria stellulata.Eight of the petitioned species occur in the Caribbean and 75 of the petitioned species occur in the Indo-Pacific region.Most of the 83 species can be found in the United States, its territories (Puerto Rico, U.S. Virgin Islands, Navassa, Northern Mariana Islands, Guam, American Samoa, Pacific Remote Island Areas), or its freely associated states (Republic of the Marshall Islands, Federated States of Micronesia, and Republic of Palau), though many occur more frequently in other countries.

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 speciesOculina varicosa.Subsequently, we announced the initiation of a formal status review of the remaining 82 species (hereinafter referred to as “candidate species”) as required by section 4(b)(3)(A) of the ESA. Concurrently, we solicited input from the public on six categories of information: (1) Historical and current distribution and abundance of these species throughout their ranges (U.S. and foreign waters); (2) historical and current condition of these species and their habitat; (3) population density and trends; (4) the effects of climate change on the distribution and condition of these coral species and other organisms in coral reef ecosystems over the short and long term; (5) the effects of all other threats including dredging, coastal development, coastal point source pollution, agricultural and land use practices, disease, predation, reef fishing, aquarium trade, physical damage from boats and anchors, marine debris, and aquatic invasive species on the distribution and abundance of these coral species over the short and long term; and (6) management programs for conservation of these species, including mitigation measures related to any of the threats listed under (5) above.

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, Brainardet al.,2011) incorporates and summarizes the best available scientific and commercial information as of August 2011 on the following topics: (1) Long-term trends in abundance throughout each species' range; (2) potential factors for any decline of each species throughout its range (human population, ocean warming, ocean acidification, overharvesting, natural predation, disease, habitat loss, etc.); (3) historical and current range, distribution, and habitat use of each species; (4) historical and current estimates of population size and available habitat; and (5) knowledge of various life history parameters (size/age at maturity, fecundity, length of larval stage, larval dispersal dynamics, etc.). The SRR evaluates the status of each species, identifies threats to the species, and estimates the risk of extinction for each of the candidate species out to the year 2100. The BRT also considered the petition, comments we received as a result of the 90-day Finding (75 FR 6616; February 10, 2010), and the results of the peer review of the draft SRR, and incorporated relevant information from these sources into the final SRR. Given the scope of the undertaking to gather and evaluate biological information for an 82-species status review, the BRT elected not to evaluate adequacy of existing regulatory mechanisms and conservation efforts in addressing threats to the 82 coral species. Thus, we developed a supplementary, peer-reviewed Draft Management Report (NMFS, 2012a) to identify information relevant to factor 4(a)(1)(D), inadequacy of existing regulatory mechanisms, and protective efforts that may provide protection to the corals pursuant to ESA section 4(b). We combined the information from the SRR and the Draft Management Report to develop and apply the listing Determination Tool (discussed below).

On April 17, 2012, we published aFederal Registernotice announcing the availability of the SRR and the Draft Management Report. The response to the petition to list 83 coral species is one of the broadest and most complex listing reviews we have ever undertaken. Given the petition's scale and the precedential nature of the issues, we determined that our decision-making process would be strengthened if we took additional time to allow the public, non-federal experts, non-governmental organizations, state and territorial governments, and academics to review and provide information related to the SRR and the Draft Management Report prior to issuing our 12-month finding. We specifically requested information on the following: (1) Relevant scientific information collected or produced since the completion of the SRR or any relevant scientific information not included in the SRR; and (2) Relevant management information not included in the Draft Management Report, such as descriptions of regulatory mechanisms for greenhouse gas emissions globally, and for local threats in the 83 foreign countries and the U.S. (Florida, Hawaii, Puerto Rico, U.S. Virgin Islands, Guam, American Samoa, and Northern Mariana Islands), where the 82 coral species collectively occur. Further, in June 2012, we held listening sessions and scientific workshops in the Southeast region and Pacific Islands region to engage the scientific community and the public in person. During this public engagement period, which ended on July 31, 2012, we received over 42,000 letters and emails. Also, we were provided or we identified approximately 400 relevant scientific articles, reports, or presentations either produced since the SRR was finalized or not originally included in the SRR. We compiled and synthesized all relevant information that we identified or received into the Supplemental Information Report (SIR; NMFS, 2012b). Additionally, we incorporated all relevant management and conservation information into the Final Management Report (NMFS, 2012c).

Therefore, the 82 candidate coral species comprehensive status review consists of the SRR (Brainardet al.,2011), the SIR (NMFS, 2012b), and the Final Management Report (NMFS, 2012c). The findings on the petition described in this notice are based on the information contained within these reports.

Listing Species Under the Endangered Species Act

We are responsible for determining whether each of the 82 candidate corals are threatened or endangered under the ESA (16 U.S.C. 1531et seq.) We first must consider whether each candidate species meets the definition of a “species” in section 3 of the ESA, then whether the status of each speciesqualifies it for listing as threatened or endangered under the ESA. As described above, we convened the BRT which produced the SRR (Brainardet al.,2011), then a public engagement period was opened which led to the SIR and Final Management Report (NMFS, 2012b; NMFS, 2012c). We developed a Determination Tool to consistently interpret and apply the information in the three reports to the definitions of “endangered” and “threatened” species in the ESA, in order to produce proposed listing determinations for each of the 82 species (the Determination Tool is introduced and described in the Risk Analyses section below). The BRT participated in the implementation of the Determination Tool, and concurred that its inputs (demographic, spatial, and threat vulnerability ratings for each species) are the best available information. Further, the BRT believes our listing determinations for the 82 candidate species are consistent with their extinction risk analyses.

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.

Introduction to Corals and Coral Reefs

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 (i.e.,they are reef-building, but not reef-dependent). There are approximately 800 species of reef-building corals in the world.

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,Heliopora coerulea,is characterized by polyps always having eight tentacles, rather than the multiples of six that characterize stony corals. The blue coral is the only species in the suborder Octocorallia (the “octocorals”) that forms a skeleton, and as such is the primary octocoral reef-building species. Finally,Milleporafire corals are also reef-building species, but unlike the scleractinians and octocorals, they have near microscopic polyps containing tentacles with stinging cells.

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 (i.e.,via photosynthesis) during the day, and heterotrophically (i.e.,via predation) at night. In contrast, non-reef-building coral species do not contain zooxanthellae in their tissues, and thus are not capable of rapid calcification. Unlike reef-building corals, these “azooxanthellate” species are not dependent on light for photosynthesis, and thus are able to occur in low-light habitats such as caves and deep water. We provide additional information in the following sections on the biology and ecology of reef-building corals and coral reefs.

Taxonomic Uncertainty in Reef-Building Corals

In addressing the species question, the BRT had to address issues related to the considerable taxonomic uncertainty in corals (e.g.,reliance on morphological features rather than genetic and genomic science to delineate species) and corals' evolutionary history of reticulate processes (i.e.,individual lineages showing repeated cycles of divergence and convergence via hybridization). To address taxonomic uncertainty, except as described below where there was genetic information available, the BRT accepted the nominal species designation as listed in the petition, acknowledging that future research may result in taxonomic reclassification of some of the candidate species. Additionally, to address complex reticulate processes in corals, the BRT attempted to distinguish between a “good species” that has a hybrid history—meaning it may display genetic signatures of interbreeding and back-crossing in its evolutionary history—and a “hybrid species” that is composed entirely of hybrid individuals (as in the case ofAcropora prolifera,discussed in the status review of acroporid corals in the Caribbean;AcroporaBiological Review Team, 2005). The best available information indicates that, while several of the candidate species have hybrid histories, there is no evidence to suggest any of them are “hybrid species” (all individuals of a species being F1 hybrids); thus, they were all considered to meet the definition of a “species”.

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 speciesMontipora dilatataandM. flabellata; Montipora patula;andPorites pukoensisbased on genetic studies;andPocillopora elegansbecause the two geographically-distant populations have different modes of reproduction. The BRT decided to subsume a nominal species (morpho-species) into a larger clade whenever genetic studies failed to distinguish between them (e.g., Montipora dilatata, M. flabellataandM. turgescens(not petitioned) andPoritesClade 1forma pukoensis). Alternatively, in the case ofPocillopora elegans,the BRT identified likely differentiation within the nominal species. So, for the purposes of this status review, the BRT chose to separateP. elegansinto two geographic subgroups, considered each subgroup asa species as defined by the ESA, and estimated extinction risk separately for each of the two subgroups (eastern Pacific and the Indo-Pacific). The combining of nominal species (i.e., Montiporaspp. andPoritesspp.) and the separation of geographically isolated populations of another species (P. elegans) resulted in 82 candidate species being evaluated for ESA listing status; however, these are not the same 82 “species” included in the petition in that:Montipora dilatataandM. flabellatawere combined into one species; andP. eleganswas separated into two. The combining of the petitioned speciesMontipora patulawith the non-petitioned speciesP. verrillidid not affect the number of candidate species. We did not receive any additional information suggesting alteration to the BRT's species delineation nor indicating any of the other 82 candidates should be separated or combined. We have made listing determinations on the 82 candidate species identified by the BRT in the SRR. Finally, a coral is a marine invertebrate, and as such, we cannot subdivide it into DPSs (16 U.S.C. 1532(15)).

Reproductive Life History of Reef-Building Corals

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 (i.e.,development of eggs and sperm within the polyps near the base). Some coral species have separate sexes (gonochoric), while others are hermaphroditic. Strategies for fertilization are either by “brooding” or “broadcast spawning” (i.e.,internal or external fertilization, respectively). Brooding is relatively more common in the Caribbean, where nearly 50 percent of the species are brooders, compared to less than 20 percent of species in the Indo-Pacific. Asexual reproduction in coral species most commonly involves fragmentation, where colony pieces or fragments are dislodged from larger colonies to establish new colonies, although the budding of new polyps within a colony can also be considered asexual reproduction. In many species of branching corals, fragmentation is a common and sometimes dominant means of propagation.

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 (Montastraea magnistellata), suggesting that the potential for long-term dispersal of coral larvae, at least for some species, may be substantially greater than previously thought and may partially explain the large geographic ranges of many species.

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.

Distribution and Abundance of Reef-Building Corals

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 (e.g.,high wave action) is another important habitat feature, as it influences the growth, mortality, and reproductive rate of each species adapted to a specific hydrodynamic zone.

The 82 candidate coral species are distributed throughout the wider-Caribbean (i.e.,the tropical and sub-tropical waters of the Caribbean Sea, western Atlantic Ocean, and Gulf of Mexico; herein referred to collectively as “Caribbean”), the Indo-Pacific biogeographic region (i.e.,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), and the tropical and sub-tropical waters of the eastern Pacific Ocean. The 82 candidate species occur in 84 countries. Seven of the 82 candidate species occur in the Caribbean (Agaricia lamarcki, Dendrogyra cylindrus, Dichocoenia stokesii, Montastraea annularis, Montastraea franksi, Montastraea faveolaandMycetophyllia ferox) in the United States (Florida, Puerto Rico, U.S. Virgin islands (U.S.V.I.), Navassa), Antigua and Barbuda, Bahamas, Barbados, Belize, Colombia, Costa Rica, Cuba, Dominica, Dominican Republic, France (includes Guadeloupe, Martinique, St. Barthelemy, and St. Martin), Grenada, Guatemala, Haiti, the Netherlands (includes Aruba, Bonaire,Curaçao, Saba, St. Eustatius, and Saint Maarten), Honduras, Jamaica, Mexico, Nicaragua, Panama, St. Kitts and Nevis, St. Lucia, St. Vincent and the Grenadines, Trinidad and Tobago, the United Kingdom (includes British territories of Anguilla, British Virgin Islands, Cayman Islands, Montserrat, and Turks and Caicos Islands), and Venezuela. The remaining 75 species occur across the Indo-Pacific region in the United States (Hawaii, Commonwealth of the Northern Mariana Islands, Territories of Guam and American Samoa, and the U.S. Pacific Island Remote Area), Australia (includes Australian colonies of Cocos-Keeling Islands, Christmas Island, and Norfolk Island), Bahrain, Brunei, Cambodia, Chile, China, Colombia, Comoros Islands, Costa Rica, Djibouti, Ecuador, El Salvador, Egypt, Eritrea, Federated States of Micronesia, Fiji, France (includes French territories of New Caledonia, French Polynesia, Mayotte, Reunion, and Wallis and Futuna), Guatemala, Honduras, India, Indonesia, Iran, Israel, Japan, Jordan, Kenya, Kiribati, Kuwait, Madagascar, Malaysia, Maldives, Marshall Islands, Mauritius, Mexico, Mozambique, Myanmar, Nauru, New Zealand (includes New Zealand colonies of Cook Islands and Tokelau), Nicaragua, Niue, Oman, Palau, Pakistan, Panama, Papua New Guinea, Philippines, Qatar, Samoa, Saudi Arabia, Seychelles, Singapore, Solomon Islands, Somalia, South Africa, Sri Lanka, Sudan, Taiwan, Tanzania, Thailand, Timor-Leste, Tonga, Tuvalu, United Arab Emirates, the United Kingdom (includes British colonies of Pitcairn Islands and British Indian Ocean Territory), Vanuatu, Vietnam, and Yemen.

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 (i.e.,abundance). In addition, new coral colonies, particularly in branching species, can be added to a population by fragmentation (breakage from an existing colony of a branch that reattaches to the substrate and grows) as well as by sexual reproduction (see above, and Fig. 2.2.1 in SRR). Fragmentation results in multiple, genetically identical colonies (ramets) while sexual reproduction results in the creation of new genetically distinct individuals (genotypes or genets). Thus, in corals, the term “individual” can be interpreted as the polyp, the colony, or the genet.

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 (e.g., Dendrogyra cylindrus), or commonly identified only to genus (MycetophylliaandAgariciaspp.), or potentially misidentified as another species. The only comprehensive abundance data in the Caribbean were for the threeMontastraeaspecies, partially because they historically made up a predominant part of live coral cover. Even for these species, the time series data are often of very short duration (they were not separated as sibling species until the early 1990s and many surveys continue to report them asMontastraea annulariscomplex) and cover a very limited portion of the species range (e.g.,the time series only monitors a sub-section of a single national park). In general, the available quantitative abundance data were so limited or compromised due to factors such as small survey sample sizes, lack of species-specific data, etc., that they were considerably less informative for evaluating the risk to species than other data, and were therefore generally not included as part of the BRT individual species extinction risk evaluations. Thus, qualitative abundance characterizations (e.g.,rare, common), available for all species, were considered in the BRT's individual species extinction risk evaluations.

Coral Reefs, Other Coral Habitats, and Overview of Candidate Coral Environments

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 (e.g.,turbid or high-latitude or upwelling-influenced areas) and recently available habitat (e.g.,lava flows). The term “mesophotic habitat” refers to hard substrates between approximately 30 m and 100 m of depth. The total area of non-reefal and mesophotic habitats is greater than the total area of shallow coral reefs within the ranges of the 82 species, as described in more detail below (NMFS, 2012b, SIR Section 4.3).

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 (i.e.,inability of corals and coral communities to recover after a disturbance event). Massive, Caribbean-wide mortality events from disease conditions of both the keystone grazing urchinDiadema antillarumand the dominant branching coral speciesAcropora palmataandAcropora cervicornisprecipitated widespread and dramatic changes in reef community structure. None of the three important keystone species (Acropora palmata, Acropora cervicornis,andDiadema antillarum) have shown much recovery over decadal time scales. In addition, continuing coral mortality from periodic acute events such as hurricanes, disease outbreaks, and bleaching events from ocean warming have added to the poor state of Caribbean coral populations and yielded a remnant coral community with increased dominance by weedy brooding species, decreased overall coral cover, and increased macroalgal cover. Additionally, iron enrichment in the Caribbean may predispose the basin to algal growth. Further, coral growth rates in the Caribbean have been declining over decades.

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 (i.e.,lower densities throughout the range, not range contraction), with concurrent changes between subregions in overall benthic composition and variation in dominant species. Further, a recent model suggests coral cover is likely to fall below five percent in the Southeastern Caribbean by 2100, even with accounting for potential adaptation by corals to increasing ocean temperatures caused by any warming scenario (NMFS, 2012b, SIR Section 3.2.2). These wide-scale changes in coral populations and communities have affected habitat complexity and may have already reduced overall reef-fish abundances; the trends are expected to continue. In combination, these regional factors are considered to contribute to elevated extinction risk for all Caribbean species.

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 (e.g.,American Samoa, Moorea, Fiji, Palau, and the Northwestern Hawaiian Islands) appear to remain relatively resilient despite major bleaching events from ocean warming, hurricanes, and crown-of-thorns seastar (COTS,Acanthaster planci) predation outbreaks. That is, even though the reefs have experienced significant impacts, corals have been able to recover. Several factors likely result in greater resilience in the Indo-Pacific than in the Caribbean: (1) The Indo-Pacific is more than 10-fold larger than the Caribbean, including many remote areas; (2) the Indo-Pacific has approximately 10-fold greater diversity of reef-building coral species than the Caribbean; (3) broad-scale Caribbean reef degradation likely began earlier than in the Indo-Pacific; (4) iron enrichment in the Caribbean may predispose it to algal growth; (5) there is greater coral cover on mesophotic reefs in the Indo-Pacific than in the Caribbean; and (6) there is greater resilience to algal phase shifts in the Indo-Pacific than in the Caribbean.

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 (i.e.,lower densities throughout the range, not range contraction) has already occurred in most subregions. As of 2002-2003, the Indo-Pacific had an overall average of approximately 20 percent live coral cover, down from approximately 50 percent, compared to an overall average of approximately 10 percent live coral cover in the Caribbean at the same time. This indicates that both basins have experienced conditions leading to coral mortality and prevention of full recovery; however, the Caribbean has been more greatly impacted. While basin-wide averages are useful for large scale comparisons, they do not describe conditions at finer, regional scales. For example, decreases in overall live coral cover have occurred since 2002 in some areas, such as on the Great Barrier Reef, while increases have occurred in other areas, such as in American Samoa.

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 beendeclines in coral cover in all basins. However, thus far, the Indo-Pacific has been less affected as a whole, due to the differentiating factors described above. The Caribbean and Eastern Pacific basins continue to experience more severe adverse conditions than the Indo-Pacific.

Threats Evaluation

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 (e.g.,sedimentation and elevated ocean temperatures) as distinct from the sources responsible for those factors (e.g.,land management practices and climate change) and qualitatively evaluated the impact each threat has on the candidate species' extinction risk over the foreseeable future, defined as the year 2100 as described below.

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 (i.e.,“high importance threats”; ocean warming, diseases, ocean acidification), the more likely the species is at risk of extinction. The BRT determined that ocean warming and related impacts of climate change have already created a clear and present threat to many corals, that will continue into the future; the threat posed by the most optimistic scenarios of greenhouse gas emissions in the 21st century and even the threat posed by unavoidable warming due to emissions that have already occurred represents a plausible extinction risk to the 82 candidate coral species. We agree with the BRT's judgment that the threats related to global climate change (e.g.,bleaching from ocean warming, ocean acidification) pose the greatest potential extinction risk to corals and have been assessed with sufficient certainty out to the year 2100. Therefore, we have determined the foreseeable future for the 82 candidate species to be to the year 2100.

The BRT qualitatively ranked each threat as high, medium, low, or negligible (or combinations of two;e.g.,“low-medium”) importance in terms of their contribution to extinction risk of all coral species across their ranges. The BRT considered the severity, geographic scope, the level of certainty that corals in general are affected (given the paucity of species-level information) by each threat, the projections of potential changes in the threat, and the impacts of the threat on each species. The BRT determined that global climate change directly influences two of the three highest ranked threats, ocean warming and ocean acidification, and indirectly (through ocean warming) influences the remaining highest ranked threat, disease.

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.

Table 1—All Threats Considered by the BRT in Assessing Extinction Risks to the 82 Candidate Coral Species. The Table is Ordered by the BRT Estimate of the Threat's Importance to Extinction Risk for Corals in General. The Threat is Paired With its Corresponding ESA Section 4 Factor in the Last Column. The Nine Threats Included in the Threats Evaluation are Shown in bold. EP07DE12.015

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.

Global Climate Change—General Overview

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 (e.g.,carbon dioxide) and atmospheric warming since the Industrial Revolution in the mid-19th century. These changes are increasing the warming of the global climate system and altering the carbonate chemistry of the ocean (ocean acidification), which affects a number of biological processes in corals including secretion of their skeletons. The atmospheric concentration of the main GHG, carbon dioxide (CO2), has steadily increased from ∼ 280 parts per million (ppm) at the start of the Industrial Revolution to over 390 ppm in 2009. Rates of human-induced emissions of CO2are also accelerating, rising from 1.5 ppm/yr during 1990-1999 to 2.0 ppm/yr during 2000-2007. Furthermore, GHG emissions are expected to continue increasing and atmospheric and ocean warming are likely to accelerate. Moreover, because GHGs can remain in the atmosphere for exceptionally long periods of time, even if all anthropogenic sources of GHG emissions ceased immediately, at least another 1.0 °C of atmospheric warming will occur as a result of past emissions, and at our current emissions rate, the earth's atmosphere is expected to warm 4 °C (likely range 2.4 °C-6.4 °C), and waters around coral reefs are expected to warm 2.8 °C-3.6 °C by the year 2100 (NMFS 2012b, SIR Section 3.2.2). As discussed below, temperature increases of this magnitude can have severe consequences for corals, including bleaching and colony death.

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°C over the time period 1850-2100 in the lowest RCP emissions scenario (RCP2.6) and up to 4.9 °C in the highest (RCP8.5; NMFS 2012b, SIR Section 3.2.2).

Nine Most Important Threats to Reef-Building Corals

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 (i.e.,family, genus, or species). Susceptibility depends on direct effects of the threat on the species, and it also depends on the cumulative (i.e.,additive) and interactive (i.e.,synergistic or antagonistic) effects of multiple threats acting simultaneously on the species. For example, ocean warming affects coral colonies through the direct effect of bleaching, together with the interactive effect of bleaching and disease, because bleaching increases disease susceptibility. We discuss how cumulative and interactive effects of threats affected individual threat susceptibilities in the Vulnerability to Threats under Risk Analyses section below.

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 (High Importance Threat, ESA Factor E)

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 (e.g.,latitude, depth, bathymetry, habitat type, etc.) and physical processes that affect seawater temperature and its effects on coral colonies (e.g.,winds, currents, upwelling shading, tides, etc.). Colony location can moderate exposure of colonies of the species to ocean warming by latitude or depth, because colonies in higher latitudes and/or deeper areas are usually less affected by warming events. Also, some locations are blocked from warm currents by bathymetric features, and some habitat types reduce the effects of warm water, such as highly-fluctuating environments. Physical processes can moderate exposure of colonies of the species to ocean warming in many ways, including processes that increase mixing (e.g.,wind, currents, tides),reduce seawater temperature (e.g.,upwelling, runoff), or increase shading (e.g.turbidity, cloud cover). For example, warming events in Hawaii in 1996 and 2002 resulted in variable levels of coral bleaching because colony exposure was strongly affected by winds, cloud cover, complex bathymetry, waves, and inshore currents (NMFS 2012b, SIR Section 3.2.2).

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 (e.g.,inter-decadal variability in seawater temperatures and upwelling related to El-Niño Southern Oscillation); and (2) ocean warming is predicted to substantially worsen by 2100. While exposure of the 82 candidate coral species to ocean warming varies greatly both spatially and temporally, exposure is expected to increase for all species across their ranges between now and 2100 (NMFS 2012b, SIR Section 3.2.2).

Multiple threats stress corals simultaneously or sequentially, whether the effects are cumulative (the sum of individual stresses) or interactive (e.g.,synergistic or antagonistic). Ocean warming is likely to interact with many other threats, especially considering the long-term consequences of repeated thermal stress, and ocean warming is expected to continue to worsen over the foreseeable future. Increased seawater temperature interacts with coral diseases to reduce coral health and survivorship. Coral disease outbreaks often have either accompanied or immediately followed bleaching events, and also follow seasonal patterns of high seawater temperatures. The effects of greater ocean warming (i.e.,increased bleaching, which kills or weakens colonies) are expected to interact with the effects of higher storm intensity (i.e.,increased breakage of dead or weakened colonies) in the Caribbean, resulting in an increased rate of coral declines. Likewise, ocean acidification and nutrients may reduce thermal thresholds to bleaching, increase mortality and slowing recovery.

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-PacificAcroporaspecies. In addition to abnormal embryonic development, symbiosis establishment, larval survivorship, and settlement success have been shown to be impaired in Caribbean brooding and broadcasting coral species at temperatures as low as 30°C-32°C. Further, the rate of larval development for spawning species is appreciably accelerated at warmer temperatures, which suggests that total dispersal distances could also be reduced, potentially decreasing the likelihood of successful settlement and the potential for replenishment of extirpated areas.

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 (i.e.,increase bleaching and decrease recovery) and decrease the overall net productivity of coral reef ecosystems (i.e.,fewer nutrients) throughout the tropics and subtropics.

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 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 (Brainardet al.2011). These conclusions are reinforced by the new information in the SIR (NMFS 2012b, SIR Section

Disease (High Importance Threat, ESA Factor C)

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 (e.g.,pathogen, environmental toxicant), the host, and the environment. In the case of corals, the host is a complex community of organisms, referred to as a holobiont, which includes the coral animal, the dinoflagellates, and their microbial symbionts. A