# Endangered and Threatened Wildlife and Plants: Final Listing Determinations on Proposal To List 66 Reef-Building Coral Species and To Reclassify Elkhorn and Staghorn Corals

> Briefs, arguments, decisions, and more.

URL: https://www.frixlaw.com/law-library/documents/fr%3A2014-20814

## Record

- **Collection:** Federal Register
- **Document type:** Rule
- **Published:** September 10, 2014
- **Citation:** 79 FR 53852

## Text

DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
50 CFR Part 223
[Docket No. 0911231415-4826-04]
RIN 0648-XT12
Endangered and Threatened Wildlife and Plants: Final Listing Determinations on Proposal To List 66 Reef-Building Coral Species and To Reclassify Elkhorn and Staghorn Corals

AGENCY:

National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA), Commerce.

ACTION:

Final rule.

SUMMARY:

We, the National Marine Fisheries Service (NMFS), are publishing this final rule to implement our final determination to list the following 20 species as threatened: five in the Caribbean (
Dendrogyra cylindrus, Orbicella annularis, Orbicella faveolata, Orbicella franksi,
and
Mycetophyllia ferox
); and 15 in the Indo-Pacific (
Acropora globiceps, Acropora jacquelineae, Acropora lokani, Acropora pharaonis, Acropora retusa, Acropora rudis, Acropora speciosa, Acropora tenella, Anacropora spinosa, Euphyllia paradivisa, Isopora crateriformis, Montipora australiensis, Pavona diffluens, Porites napopora,
and
Seriatopora aculeata
) under the Endangered Species Act (ESA) of 1973, as amended. The two species currently listed as threatened (
Acropora cervicornis
and
Acropora palmata
) in the Caribbean still warrant listing as threatened. We also determined that a total of 43 proposed species do not warrant listing as endangered or threatened species, and three proposed species are not determinable under the ESA. We have reviewed the status of the species and efforts being made to protect the species, and public comments received on the proposed rule, and we have made our determinations based on the best scientific and commercial data available. We also solicit information that may be relevant to the designation of critical habitat for the 20 species newly listed under this final rule.

DATES:

The effective date of this final rule is October 10, 2014. Responses to the request for information regarding a subsequent ESA section 4(d) Rule and critical habitat designation must be received by November 10, 2014.

ADDRESSES:

Submit responses to the request for information regarding a subsequent ESA section 4(d) Rule and critical habitat designation to National Marine Fisheries Service, Pacific Islands Regional Office, NOAA Inouye Regional Center, 1845 Wasp Blvd., Building 176, Honolulu, HI 96818; or National Marine Fisheries Service, Southeast Regional Office, 263 13th Avenue South, Saint Petersburg, FL 33701.

FOR FURTHER INFORMATION CONTACT:

Lance Smith, NMFS, Pacific Island Regional Office, 808-725-5131; Jennifer Moore, NMFS, Southeast Regional Office, 727-824-5312; or Marta Nammack, NMFS, Office of Protected Resources, 301-427-8469. A list of the literature cited in this rule is available at
http://coral.sero.nmfs.noaa.gov
and
http://www.fpir.noaa.gov/PRD/prd_coral.html.

SUPPLEMENTARY INFORMATION:

Background

On October 20, 2009, the Center for Biological Diversity (CBD) petitioned us to list 83 reef-building corals as threatened or endangered under the Endangered Species Act (ESA) and designate critical habitat. The 83 species included in the petition were:
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,
and
Turbinaria 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 90-day finding (75 FR 6616) that CBD had presented substantial information indicating the petitioned actions may be warranted for all of the petitioned species except for the Caribbean species
Oculina varicosa.
We also announced the initiation of a formal status review of the remaining 82 petitioned species, and 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 No. 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, our implementing regulations

specifically direct us not to take possible economic or other impacts of listing species into consideration (50 CFR 424.11(b)). 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, coral population dynamics and endangered species extinction risk evaluations. The BRT's comprehensive, peer-reviewed Status Review Report (SRR; Brainard
et 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 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. Additionally, we developed a supplementary, peer-reviewed Draft Management Report (NMFS, 2012a) to identify information relevant to ESA 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).

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. Thus on April 17, 2012, we published a
Federal Register
notice announcing the availability of the SRR and the Draft Management Report, and 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 (GHG) emissions globally, and for local threats in the 83 foreign countries and 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), where the 82 petitioned 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 with or we identified approximately 400 relevant scientific articles, reports, or presentations that were 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, 2012c). Additionally, we incorporated all relevant management and conservation information into the Final Management Report (NMFS, 2012b). Therefore, the 82 candidate coral species comprehensive status review consists of the SRR (Brainard
et al.
, 2011), the SIR (NMFS, 2012c), and the Final Management Report (NMFS, 2012b).

On December 7, 2012, we published a proposed rule (77 FR 73219) to list 12 of the petitioned coral species as endangered (five Caribbean and seven Indo-Pacific) and 54 coral species as threatened (two Caribbean and 52 Indo-Pacific), and we determined 16 coral species (all Indo-Pacific) did not warrant listing as threatened or endangered under the ESA. This was the final agency action for those species which we determined were not warranted for listing. We also determined that two currently listed Caribbean corals (
Acropora cervicornis
and
Acropora palmata
) warranted reclassification from threatened to endangered. The findings in the proposed rule were based on the information contained within the reports described above (SRR, SIR, and Final Management Report). During a 90-day comment period, we solicited comments from the public, other concerned governmental agencies, the scientific community, industry, foreign nations in which the species occur, and any other interested parties on our proposal. We later extended the public comment period by 30 days, making the full comment period 120 days. We received approximately 32,000 comments through electronic submissions, letters, and oral testimony from public hearings held in Dania Beach, FL; Key Largo, FL; Key West, FL; Rio Piedras, Puerto Rico; Mayaguez, Puerto Rico; Christiansted, St. Croix, U.S. Virgin Islands; Charlotte Amalie, St. Thomas, U.S. Virgin Islands; Hilo, Hawaii, HI; Kailua Kona, Hawaii, HI; Kaunakakai, Molokai, HI; Wailuku, Maui, HI; Lihue, Kauai, HI; Honolulu, Oahu, HI; Hagatna, Guam; Saipan, Commonwealth of the Northern Marianas Islands (CNMI); Tinian, CNMI; Rota, CNMI; Tutuila, American Samoa; and Washington, DC.

During the public comment period, we received numerous comments on the proposed listing and the sufficiency or accuracy of the available data used to support the proposed listing determinations. In particular, comments raised questions and provided varied, often conflicting, information regarding the following topics:

(1) The proposed species' listing statuses (
e.g.
, certain species proposed as endangered should be threatened);

(2) the sufficiency and quality, or lack thereof, of the species-specific information used for each species' proposed listing determination;

(3) the accuracy of the methods used to analyze the available information to assess extinction risk (including NMFS' “Determination Tool”) and derive listing statuses for each of the proposed species;

(4) the ability of corals to adapt or acclimatize to ocean warming and acidification;

(5) the reliability, certainty, scale, and variability of future modeling and predictions of climate change; and

(6) the effect local management efforts have on coral resilience.

After considering these comments, we found that substantial disagreement existed regarding the sufficiency and accuracy of the available data used in support of the proposed determinations.

As a result, we determined it was necessary to solicit additional data from those scientists who were identified by public comments and others who may have additional data to assist in resolving the substantial disagreement. Therefore, pursuant to the ESA section 4(b)(6)(B)(i), we determined that a 6-month extension of the deadline for final determinations on the proposed rule was necessary (78 FR 57835; September 20, 2013). We completed our data collection effort in the fall of 2013, and the relevant information that we received or collected was considered in the formulation of this final rule. The data collection effort was the final step in our thorough process to assemble the best available information on the status of the species addressed in this final rule. As a result, this final rule represents a logical evolution from the proposed rule, including some changes in our overall decision-making framework and a holistic reconsideration of the key elements that contribute to a species' listing status, as described in detail throughout this rule. Consequently, most of the listing determinations have changed between the proposed and final rules.

Listing Species Under the Endangered Species Act

We are responsible for determining whether the 66 proposed coral species should be listed as threatened or endangered under the ESA, and whether the two species proposed for reclassification should be listed as endangered under the ESA (16 U.S.C. 1531
et seq.
). Clonal, colonial organisms, such as corals, are vastly different in their biology and ecology than vertebrates, which are typically the focus of ESA status reviews. Therefore, concepts and terms that are typically applied to vertebrates have very distinct meanings when applied to corals. A ‘rare’ coral may have millions of colonies as compared to a ‘rare’ vertebrate, which may only have hundreds of individuals. To be considered for listing under the ESA, a group of organisms must constitute a “species,” which is defined in section 3 of the ESA to include “any subspecies of fish or wildlife or plants, and any distinct population segment of any species of vertebrate fish or wildlife which interbreeds when mature.” In the case of reef-building corals, the decision that a species is a listable entity is often complicated by several aspects of their biology including individual delineation, taxonomic uncertainty, identification uncertainty, and life history (
e.g.
, colonialism and clonality).

Section 3 of the ESA further defines an endangered species as “any species which is in danger of extinction throughout all or a significant portion of its range” and a threatened species as one “which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range.” Section 4(a)(1) of the ESA requires us to determine whether any species is endangered or threatened due to any one or a combination of the following five factors: (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) the inadequacy of existing regulatory mechanisms; or (E) other natural or manmade factors affecting its continued existence. We are required to make listing determinations based solely on the best scientific and commercial data available after conducting a review of the status of the species and after taking into account efforts being made by any state or foreign nation to protect the species.

This finding begins with an overview of coral biology, ecology, and taxonomy in the Corals and Coral Reefs section below, including whether each proposed species meets the definition of a “species” for purposes of the ESA. Specifically, are the proposed species determinable under the ESA given any discrepancies between their current morphologically-based taxonomy and any new genetic information that may result in taxonomic reclassification. Other relevant background information in this section includes the general characteristics of the habitats and environments in which the proposed species are found. The finding then summarizes information on factors adversely affecting and posing extinction risk to corals in general in the Threats Evaluation section. The Risk Analyses section then describes the framework applied to each of the species that resulted in final listing statuses for the proposed species. The Species-specific Information and Determinations section provides the best available species-specific information, which, coupled with the general portions of this final rule, provide the basis for the individual determinations for final listing status. Finally, we assessed efforts being made to protect the species and determined if these efforts are adequate to mitigate impacts and threats to the extent that a species does not meet one of the statutory statuses.

Given the precedential and complex nature of this rule-making process, we took extra steps to assemble the best available information for informing the final listing determinations. Efforts to acquire this information first included the formation of an expert scientific panel (BRT) that used the best available scientific information at that time in a structured decision-making process to inform and write the SRR. Further, this process provided numerous opportunities for public input, including a public comment period after the 90-day finding in 2010 (75 FR 6616; February 10, 2012), a unique public information-gathering period (77 FR 22749; April 17, 2012) prior to the release of the proposed rule in 2012, and a 120-day formal public comment period after the publication of the proposed rule. Finally, in a targeted data-solicitation effort to resolve substantial scientific disagreement in the public comments on the proposed rule, we published a 6-month extension in September 2013 to gather additional information to further inform our final decisions (78 FR 57835; September 20, 2013). Over the course of this multi-year process, we gathered and reviewed thousands of scientific papers, journal articles, reports, and presentations (bibliography and select documents available at
http://www.nmfs.noaa.gov/pr/species/invertebrates/corals.htm
). In addition, we held a total of 19 public hearings in 2012 and 2013 throughout the Southeast and Pacific Islands regions, and received and reviewed over 75,000 public comments during the information-gathering period in 2012 and the proposed rule public comment period in 2012-2013, combined. These efforts ensure that this final rule is based upon the best available information on the proposed species at this time, as explained in more detail below.

Summary of Comments Received

Below we address the comments received pertaining to the proposed listings or reclassifications of the 68 coral species in the December 7, 2012, proposed rule (77 FR 73219). During the 120-day public comment period from December 7, 2012, to April 6, 2013, we received 1,120 written and verbal responses (including public testimony during the 19 public hearings). This included 1,119 unique comments on the proposed listings or reclassifications and 32,000 action alert responses in support of the rule organized by the petitioner CBD, which substantively constitutes one unique comment, and. The public comments received covered a wide breadth of topics, many of which

were significant and within the scope of this rule-making. We summarized the comments, and these summaries and our responses are organized according to the sections of the proposed rule on which those comments were based. We have considered all public comments, and we provide responses to all relevant issues raised by comments. We have not responded to comments outside the scope of this rulemaking, such as comments regarding the potential economic impacts of ESA listings, comments suggesting that certain types of activities be covered in any future regulations pursuant to ESA section 4(d) for threatened species, or whether ESA listings are appropriate for species threatened by climate change. As explained in the Background above, this final rule was extended by 6 months to resolve substantial scientific disagreement in the public comments on six topics related to the proposed listing.

Comments on Taxonomic Uncertainty in Reef-Building Corals

Comment 1:
Many public comments on the proposed listing rule stated that species identification uncertainties and taxonomic uncertainties associated with many reef-building corals are problematic for the ESA listing determination process. Four comments specifically stated that the ability to determine the status of coral species under the ESA is impeded by the taxonomic uncertainty of many coral species. Two comments stated that genetic and genomic science is just beginning for corals, and as it develops it will likely show the current morphologically-based taxonomy is incorrect, completely changing current coral taxonomy. Therefore, management decisions based on the current taxonomy should be approached with caution. One comment stated that proper species identification, especially for the Indo-Pacific
Acropora
genus, is difficult and exacerbated by the use of outdated and inadequate information.

Most of these comments are based on species identification uncertainties and the conflicting taxonomic results between recent genetics studies and traditional morphology-based taxonomy, and comments identified two potential problems: (1) Species identification and taxonomic uncertainty prevents many reef-building coral taxa, especially in the Indo-Pacific, from being determinable species under the ESA; and (2) even if these taxa are determinable species under the ESA, the taxonomic uncertainty confounds the available information regarding the status of each species, thus it is not possible to determine the listing status of these species with adequate confidence.

Response:
The comments correctly note that in some instances, lack of information, or ambiguity and uncertainty in available information, is so great that any listing determination on such a basis would be arbitrary. In our judgment, that is not the case for the proposed species, with a few exceptions noted below. The SRR concluded that the 68 species in the proposed rule were determinable, including the species for which the SRR found that splitting or lumping petitioned species was necessary based on genetic studies. For the proposed rule, we agreed with the SRR, and considered the 68 species to be determinable for purposes of conducting a status review and determining listing status under the ESA.

The public comments did not provide any studies or results, nor did we find any new studies or results, that significantly contradict the consideration of the traditional, morphologically described species as determinable species, with the exception of
Pocillopora.
We acknowledged in the proposed rule, however, that the taxonomic uncertainty for reef-building corals is not only real (Brainard
et al.,
2011), but increasing in recent years as genetics studies have advanced (Stat
et al.,
2012; Veron, 2013). In the case of
Pocillopora
species, the taxonomic uncertainty has recently increased substantially such that the three proposed species in this genus are not determinable under the ESA (see Comment 2). For the remaining 65 species, the best available scientific information continues to support their classification as species. The taxonomic uncertainty associated with each species is considered along with other types of uncertainty when determining the status of each species in the Species-specific Information and Determinations section. In this way, the species identification and taxonomic uncertainty for each species is acknowledged and incorporated into each of the 65 determinations in this final rule.

In this final rule, even though
Millepora foveolata
and
Montipora lobulata
were affirmed to be valid species, and there are few if any taxonomic uncertainty issues, the two species are so difficult to identify in the field that there is very little reliable information available for either species (Fenner, 2014b). Thus, as described in the Species-specific Information and Determinations below for
M. foveolata
and
M. lobulata
, the species identification uncertainty is so high for these species that there is not sufficient evidence to support listing determinations of threatened or endangered for either species. This is explained in more detail in each species' individual determination.

Comment 2:
Related to Comment 1, one comment identified
Pocillopora
as a problematic taxon and provided a recent scientific paper describing new genetic evidence of taxonomic contradictions between genetic and morphologic results for
Pocillopora
species (Pinzón
et al.,
2013).

Response:
Based on information summarized in the SRR, the proposed rule split
P. elegans
into Indo-Pacific and Eastern Pacific nominal species, and proposed
P. elegans
(Indo-Pacific),
P. elegans
(Eastern Pacific), and
P. danae
for listing (
P. danae
only occurs in the Indo-Pacific). However, after considering new information on taxonomic uncertainty throughout the genus
Pocillopora
that has become available since the publication of the proposed rule, including the paper (Pinzón
et al.,
2013) submitted by the commenter, we no longer consider the three
Pocillopora
species that were proposed for listing to be determinable under the ESA. A range-wide phylogeographic survey that included most currently recognized pocilloporid species found that reliance on colony morphology is broadly unreliable for species identification, and that several genetic groups have highly limited geographic distributions. The study concluded that “a taxonomic revision informed foremost by genetic evidence is needed for the entire genus” (Pinzón
et al.,
2013). Similarly, a phylogeographic survey of several currently recognized pocilloporid species representing a range of atypical morphologies thought to be rare or endemic to remote locations throughout the Indo-Pacific found that: (1) The current taxonomy of Pocillopora based on colony morphology shows little correspondence with genetic groups; (2) colony morphology is far more variable than previously thought; and (3) there are numerous cryptic lineages (
i.e.,
two or more distinct lineages that are classified as one due to morphological similarities). The study concluded that “the genus
Pocillopora
is in need of taxonomic revision using a combination of genetic, microscopic characters, and reproductive data to accurately delineate species” (Marti-Puig
et al.,
2013). Likewise, a more limited study of several currently recognized pocilloporid species in Moorea found that genetic groups do not correspond to colony morphology, and exhibit a wide range of morphological variation

(Forsman
et al.,
2013). These studies demonstrate that colony morphology in pocilloporids is a poor indicator of taxonomic relationships, for the following reasons: (1) Morphologically similar colonies may not be the same species (
i.e.,
colonies of different species appear similar because of similar environmental conditions or other reasons); and (2) morphologically different colonies may be the same species (
i.e.,
colonies of the same species appear different because of different environmental conditions or other reasons).

While the current literature supports the taxonomic division of pocilloporids geographically into Indo-Pacific and Eastern Pacific groups, it indicates a high level of taxonomic uncertainty for all
Pocillopora
species that are found in both areas, such as
P. elegans.
Within these two geographic areas, colonies that resemble
P. elegans
may be different species, including possibly still undescribed species. That is, colonies may merely resemble
P. elegans
because of similar environmental conditions or other reasons, but actually may be different species. And the opposite type of taxonomic uncertainty also appears to be common, as colonies that do not resemble
P. elegans
may actually be
P. elegans.
That is, colonies that are
P. elegans
appear different because of different environmental conditions or other reasons (Forsman
et al.,
2013; Marti-Puig
et al.,
2013; Pinzón
et al.,
2013). The recently appreciated taxonomic uncertainty is in addition to the historical morphological taxonomic uncertainty within the genus
Pocillopora
and for
P. elegans
specifically (Veron, 2013; Veron, 2014). While
P. danae
does not occur in the Eastern Pacific, similar taxonomic uncertainty problems occur for this species. That is, this species also had historical morphological taxonomic uncertainty (Veron, 2013), which has recently been compounded by genetic taxonomic uncertainty, leading Veron (2014) to conclude that the species likely requires a taxonomic revision. A new taxonomic revision of
Pocillopora
was published, in which
P. danae
was found to be a synonym of
P. verrucosa,
resulting in the traditional
P. danae
being included within
P. verrucosa
(Schmidt-Roach
et al.,
2014). However, the overall taxonomic uncertainty within
Pocillopora,
including for
P. elegans
and
P. danae,
has not been resolved, and in fact continues to increase as more studies are conducted. Thus, at this time,
Pocillopora
species are not determinable under the ESA. Therefore, we are withdrawing our proposal to list
P. elegans
(Indo-Pacific) as threatened,
P. elegans
(Eastern Pacific) as endangered, and
P. danae
as threatened; these species are not considered further in this final rule.

Comment 3:
Several comments objected to our agreement with the SRR's (Brainard
et al.,
2011) lumping of
Montipora dilitata,

M. flabellata,
and
M. turgescens
into a single species, as well as the lumping of
M. patula
and
M. verrilli
into a single species, based on the results of a single genetics study by Forsman
et al.
(2010).

Response:
The objections in the public comments to lumping
Montipora dilitata
/
M. flabellata
/
M. turgescens
and
M. patula
/
M. verrilli
did not provide any new or supplemental information, nor did we find any new or supplemental information, contradicting the key study used by the SRR to consider these species as a group. We must use the best available science on which to base our determinations, and there is no indication that Forsman
et al.
(2010) is in error. However, as discussed in the response to Comment 1, we acknowledge that coral taxonomy is a rapidly growing field and that is creates uncertainty in determining a species under the ESA. This taxonomic uncertainty is considered in the individual Species-specific Information and Determination for the
Montipora.

Comments on Reproductive Life History of Reef-Building Corals

Comment 4:
There were only a few comments related to the reproductive life history of corals. One comment stated that coral reef connectivity data are sparse, and while the majority of published studies on coral larval dispersal report evidence of local seeding and replenishment of reefs, other models and studies report sporadic periods of longer distance dispersal and recruitment events. The commenter felt that the proposed rule did not adequately address coral population dynamics and connectivity in determining the status of the candidate coral species under the ESA. Another comment stated that there is almost no information on any of the species' trends or recruitment rates, and the limited information available is based on qualitative opinion, not quantitative data. The comment also pointed out that the proposed rule agreed that the term `recruit' could be difficult to apply in the case of corals, which reproduce both sexually and asexually, and that the number of recruits per spawner depends on the age or size at which an entity is defined as a recruit. These comments assert that there is insufficient information on productivity and connectivity on which to base listing decisions.

Response:
Coral reproduction and connectivity are addressed generally in the Reproductive Life History of Reef-building Corals section. As each proposed coral species has a different reproductive life history, we more comprehensively address each species' reproduction, connectivity, and recruitment (when that information was available) as they relate to each species' status under the ESA in the Species-specific Information and Determinations section. The public comments did not provide any studies or information on reproduction or connectivity for any species except for
Acropora cervicornis
(see Species-specific Information and Determinations section). Any supplemental information we found is included in Species-specific Information and Determinations section.

Comments on Distribution and Abundance of Reef Building Corals

Comment 5:
We received several comments regarding the distribution and abundance of reef-building corals, mainly regarding the lack of species-specific information for many species' geographic distributions and population abundances. There were only a few comments related to determining the distribution and abundance of reef building corals, specifically on extrapolating individual corals to overall population abundance and distribution, on which to base a listing decision. One comment stated that coral population size and structure across the world's oceans is nearly impossible to determine with any accuracy because we use crude substitutes for individual animals in determining population and range information within a species. For example, there is a significant difference between using colony population and range estimates versus using polyp population and range estimates, which are essentially impossible to estimate. Another comment stated that it is not accurate to equate percent coral cover on reefs to population abundance (
i.e.
, numbers of individuals). Any loss of coral cover often is manifest by loss of coral tissue over large portions of still living colonies, without the loss of the individual. Furthermore, it is unclear whether the loss of many separate but genetically-identical colonies (`clones') equates to the loss of a single but genetically-distinct individual if some of the clone colonies survive. Another commenter noted that the distributions of the Indo-Pacific species are largely unknown due to their incredibly vast ranges encompassing numerous

archipelagos that include thousands of islands and atolls. The commenter emphasized this point by noting that there are between 30,000 and 40,000 islands in Oceania which could potentially have populations of the proposed coral species. The comments described above collectively assert that listing decisions cannot be made due to the lack of species-specific information.

Response:
We acknowledge that it is difficult to quantify and qualify distribution and abundance for individual coral species. The ambiguity associated with the delineation of the individual in reef-building corals is addressed in the Individual Delineation sub-section in the Corals and Coral Reefs section, including how we characterize the delineation of the individual for the species covered by this final rule. In response to public comments, we more adequately address each species' distribution and abundance as those characteristics relate to each species' determination status under the ESA in the Species-specific Information and Determinations section. The public comments provided some useful information on the distribution and abundance of specific coral species, and we also collected supplemental information on distribution and abundance that is included in the Species-specific Information and Determinations section.

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

Comment 6:
Some comments asserted that the proposed rule focused too much on coral reefs rather than focusing on coral species. A couple of comments stated that corals thrive in places that are not coral reefs, even when nearby coral reefs are not thriving, underscoring the notion that reefs are not species. Another couple of comments stated that the focus on coral reefs and reef ecosystems, and the importance they have to reef-associated species, is improper for ESA listing analysis and added that NMFS cannot simply decide to treat reefs as a species under the ESA simply because evaluating reefs is easier.

Response:
The proposed rule acknowledged that reef-building coral species are not reef-dependent and provided a description of non-reefal habitats. Public comments did not provide information on how to interpret non-reefal habitat in our analysis, but in the Coral Habitats sub-section of this final rule we clarify the relevance of non-reefal habitats in determining each species' status under the ESA (
e.g.
, providing variability in environmental conditions).

Further, in the Coral and Coral Reefs section (Individual Delineation and Species Identification sub-sections), we explain that we define a coral species as the “physiological colony” (
i.e.,
unit of the species that can be identified as an individual in the field) to ensure that we are evaluating the individual species and not coral reefs generally for determining ESA status. Public comments did not offer any information on how to define a coral species, but our explanations in the Individual Delineation and Species Identification sub-sections makes clear that we do not consider coral reefs as species in this final rule. However, it should be noted that defining an individual coral as the physiological colony in this final rule did not change how we interpreted abundance data for any species.

Comment 7:
A few comments stated that the proposed rule lacked species-specific information for mesophotic habitats (deep, lower-light areas, usually between 30 and 100 m deep). One comment stated that the coral communities of many Indo-Pacific jurisdictions have received little attention, with vast areas of reef remaining unexplored, especially for corals occurring in the mesophotic zone, which likely harbors populations of species that can also be found at shallower depths. Another comment stated that recent data from NOAA-supported studies of mesophotic reefs found these extensive and poorly studied ecosystems serve as refugia for numerous shallow water coral species, yet no survey data from these ongoing studies were included in the proposed rule. We also received two papers (Bridge and Guinotte, 2013; Kahng
et al.,
2014) that suggested the global diversity of some mesophotic corals may be underestimated and the biogeographic ranges of mesophotic corals are not fully explored.

Response:
The proposed rule briefly described mesophotic habitats and acknowledged that the amount of mesophotic habitat available is unknown and likely greater than the amount of shallow reef habitat. The proposed rule also stated there is greater coral cover on mesophotic reefs in the Indo-Pacific than in the Caribbean. However, more information has become available on this habitat type since publication of the proposed rule. Two papers (Bridge and Guinotte, 2013; Kahng
et al.,
2014) provided more information on the global diversity and biogeographic ranges of mesophotic corals and we have collected information on the magnitude and diversity of mesophotic habitat. The extent of mesophotic habitat is addressed in the Coral Habitats sub-section. Mesophotic habitat's potential function as refugia for corals from ocean warming is addressed in the Spatial and Temporal Refugia sub-section. Where mesophotic habitat information is available for an individual coral species we have included and considered that information in the Species-specific Information and Determinations section.

Comment 8:
With regard to coral habitats being divided into only two global regions (
i.e.,
Caribbean and Indo-Pacific), a couple of comments stated that the Indo-Pacific region was too coarse. Specifically, the comments stated that the Hawaiian Islands should be considered its own region or sub-region with Hawaiian species evaluated separately, due to Hawaii's isolated nature and significant number of endemic species.

Response:
We recognize that there may be numerous distinct sub-regions throughout the Caribbean and Indo-Pacific basins for some or all species, and that some coral species are endemic to Hawaii. However, under the ESA, we must evaluate the status of the species throughout their entire ranges. Invertebrate species, such as corals, cannot be divided further into Distinct Populations Segments (DPS) under the ESA, since DPS specifically refer only to vertebrate species. Therefore, we cannot identify sub-regions, such as Hawaii, as its own distinct geographic range and evaluate the status of more broadly distributed species only within that specific area. In addition, as described in the Risk Analyses—Statutory Standard sub-section of this final rule, we were not able to identify a significant portion of its range (SPOIR) for any of the proposed corals and therefore could not evaluate whether the status of the species within that portion of its range impacts the overall status of the species throughout its range.

Comment 9:
We received a few comments regarding the consideration and inclusion of Traditional Ecological Knowledge (TEK), particularly from local island cultures (Hawaiian, Chamorro, and Samoan), as best available information for our listing determination process. One comment noted the importance of corals and coral reefs to island cultures in the Pacific Islands region, in particular to native Hawaiians. The comment criticized the lack of TEK in the SRR and proposed rule for the candidate corals, stating that coral biology and ecology is a fundamental part of TEK, and that their TEK is part of best available science.

Response:
We agree that TEK provides an important and unique perspective on local ecosystems, their status, threats, and changes over time; when relevant information was made available to us, we incorporated it into the proposed rule. We also acknowledge that this information is not necessarily accessible in academic peer reviewed journals or text books. Therefore, we requested any additional TEK-related information on the biology, ecology, threats, and extinction risks of the 65 coral species on numerous occasions for inclusion within this final rule. While we received public comments and listened to several public testimonies from community members in both the Pacific Islands and Southeast regions that disagreed with our proposed listing determinations, we did not receive any TEK-related information or data on the biology, ecology, threats, or extinction risks for any of the 65 coral species within this final rule.

Comments on Threats Evaluation

Comment 10:
We received a large number of public comments on the various threats to corals and coral reefs. In addition to the specific comments on the nine most important threats, one comment stated that there should be no doubt that corals and coral reefs throughout the world are in serious trouble and in decline due to the effects of anthropogenic stressors. Another commenter asked whether the mere threats from anthropogenic impacts are sufficient for ESA listing. Yet another commenter requested that recreational boating activities should be recognized as a specific threat, even though recreational boating activities may only present a relatively minor risk to coral species.

Response:
As described in the proposed rule, there are nine threats considered to be the most significant to the current or expected future extinction risk of reef-building corals. The comments and responses on these nine threats (ocean warming, disease, ocean acidification, trophic effects of fishing, sedimentation, nutrients, sea-level rise, predation, and collection and trade) are addressed individually below. We acknowledged that recreational boating activities may present some risk to coral species and it was included in the description of the threat “Human-induced Physical Damage” in the SRR. However, we determined that threat's contribution to the extinction risk of corals, generally, is negligible to low.

We also recognized that anthropogenic threats are affecting coral species worldwide and may be sufficient for an ESA listing if the species meets the definition of threatened or endangered. That is, if the species is currently in danger of extinction or may become so in the foreseeable future due to any one or a combination of the five factors under Section 4 of the ESA (in which the various threats are categorized) then the species may be listed.

Comments on Global Climate Change—General Overview

Comment 11:
We received many comments on the general treatment of global climate change in the proposed rule and supporting documents. The Global Climate Change—General Overview section in the proposed rule and the global climate change portion of the SRR describe past, current, and future GHG emissions and atmospheric concentrations and the associated past, current, and future general effects on coral reef ecosystems, based primarily on the International Panel on Climate Change's (IPCC) Fourth Assessment Report (AR4), The Physical Basis (IPCC, 2007) and supporting literature.

Some comments stated that we did not adequately account for the uncertainty in climate change modeling. A few comments stated that global temperature has been stable for the last ten years or that warming has slowed down since 2000. One commenter provided two recent papers (Guemas
et al.,
2013; Hansen
et al.,
2012) that showed global mean surface temperatures did not increase as much as had been predicted from 2000 to 2010.

Some comments stated that GHG emissions and global temperatures continue to rise unabated. One comment referenced two studies (Frieler
et al.,
2012; van Hooidonk
et al.,
2013b) that projected the frequency of coral reef bleaching under different levels of warming and emissions scenarios, indicating that significant and immediate GHG reductions are critical to prevent coral reefs from degradation and collapse. Another comment also referenced van Hooidonk
et al.
(2013b) and stated that targets for atmospheric carbon dioxide (CO
2
) concentrations must be lower than 450 parts per million (ppm) to protect coral reef ecosystems. Yet another comment stated that scientific modeling indicates that within 40 to 50 years, reef decline will pass a tipping point, largely due to the increasing impacts of climate change, and may not be reversible over ecological time scales. Another comment pointed out that climate change also could likely increase corals' exposure to cold water stress, which studies have shown can cause extensive mortality of corals (Colella
et al.,
2012; Schopmeyer
et al.,
2012).

Response:
We agree with commenters and acknowledge that there is uncertainty associated with climate change projections. Climate change projections over the foreseeable future are associated with three major sources of uncertainty: (1) The projected rate of increase for GHG concentrations; (2) strength of the climate's response to GHG concentrations; and (3) large natural variations. The recent warming slow-down is an example of a large natural variation that was not anticipated by previous models. However, AR4's projections were built upon scientifically accepted principles, which fairly simulated many large scale aspects of present-day conditions, providing the best available information on climate change at the time the proposed rule was published. The IPCC's Fifth Assessment Report (AR5), Climate Change 2013: The Physical Science Basis (IPCC, 2013), commonly referred to as the Working Group I Report (WGI) became available in September 2013, and supersedes AR4; accordingly, this final rule relies on the information provided in AR5's WGI. Despite the advance of climate change science in recent years, there is still complexity and uncertainty associated with projections of global climate change. However, the current state of climate change science is capable of producing informative projections that provide a rational basis for considering likely patterns in future climate change-related threats to reef-building corals. More detail on the overall complexity associated with projections of global climate change, major sources of uncertainty in climate change projections, and a summary of AR5's WGI, including the pathway that we consider the most impactful to corals, are addressed in Threats Evaluation—Global Climate Change Overview sub-section.

We also acknowledge the observed recent hiatus/slow-down in the rate of global surface air temperature increase, and we have accordingly provided a description of the hiatus/slowdown and its implications in the Threats Evaluation—Ocean Warming sub-section. In summary, despite unprecedented levels of GHG emissions in recent years, a slow-down in global mean surface air temperature warming has occurred since 1998, which AR5's WGI refers to as a “hiatus.” Despite this slowdown in warming, the period since 1998 is the warmest recorded and “Each of the last three decades has been successively warmer at the Earth's surface than any preceding decade since

1850.” The slow-down in global mean surface warming since 1998 is not fully explained by AR4 or AR5 WGI's models, but is consistent with the substantial decadal and interannual variability seen in the instrumental record and may result, in part, from the selection of beginning and end dates for such analyses.

Public comments provided supplemental information on several aspects of global climate change, as described above. We also collected information to inform how we assess the effects of global climate change to corals, including the IPCC Working Group II report on impacts, adaptation, and vulnerability. We maintain that global climate change is central to assessing extinction risk for the corals in this final rule. As described in more detail in the Threats Evaluation—Global Climate Change Overview sub-section below, the supplemental information underscores the complexity and uncertainty associated with projecting the extent and severity of effects of global climate change across the ranges of reef-building corals.

Comments on Ocean Warming (High Importance Threat, ESA Factor E)

Comment 12:
We received several comments on general future projections of ocean warming levels. One commenter stated that climate change models applied in our assessment are too coarse to accurately predict the conditions reefs will experience in the future and that real conditions are impacted by bathymetry, water mixing, wind patterns, fresh water inputs, and other bio-geographic factors. The commenter concluded that existing projections for sea surface temperature are not sufficient to conclude the species face an existential threat. Other comments also criticized the use of AR4's worst-case scenario as the basis for determining the most likely future scenario with regard to ocean warming, and related topics such as the proposed rule's lack of consideration for the post-1998 hiatus in global warming.

Response:
In the proposed rule, we discussed the numerous, complex spatial and temporal factors that compound uncertainty associated with projecting effects of ocean warming on corals in the future, and we have determined that ocean warming will not affect all species in all locations uniformly over the foreseeable future. We believe that different bio-geographic factors such as bathymetry, water mixing, wind patterns, and fresh water will likely impact conditions corals will experience over the foreseeable future. We also recognized that global climate change models are associated with uncertainty, as discussed in response to comment 11 above. However, in response to comments on ocean warming projections, such as criticism of the reliance of the proposed rule and supporting documents on AR4 (IPCC, 2007) and the lack of consideration of the ocean warming hiatus, we provide a review of the best available information on these topics, including AR5's WGI Report (IPCC, 2013), in the Threats Evaluation—Global Climate Change Overview, Representative Concentration Pathways (RCP) 8.5 Projections, and Ocean Warming sub-sections below. These data support the conclusion in the proposed rule that ocean warming is increasing in severity, and is likely to continue increasing in severity within the ranges of reef-building corals. However, a key difference between the proposed and final rule is that we now more fully consider the ability of each species' spatial and demographic traits to moderate exposure to threats, including warming, and place appropriate emphasis on the non-uniform nature of global threats at the regional and local levels that allows habitat heterogeneity to play a role in buffering a species against vulnerability to extinction. The significance of coral abundance and distribution, and habitat heterogeneity, to this final rule is described in more detail in the Corals and Coral Reefs, Risk Analyses and Species-specific Information and Determinations sections of this rule.

After reviewing the public comments and information provided in AR5's WGI our conclusion regarding the threat of ocean warming remains unchanged from the proposed rule. We maintain that ocean warming is a high importance threat in assessing global extinction risk for the corals in this final rule, while we also acknowledge that the interpretation of future climate change threats to corals is associated with complexity and uncertainty, and that effects on individual species of reef-building corals are difficult to determine as described in more detail in the Threats Evaluation—Global Climate Change Overview subsection below.

Comment 13:
Many comments criticized the proposed rule for not accounting for spatial variability in ocean warming and overlooking regional and local variability in conditions leading to warming-induced bleaching, which may be more or less severe regionally or locally than the overall warming. For example, we received two comments requesting us to review the literature for information regarding current and projected regional differences in sea surface temperature anomalies and for variations in the responses of individual coral species across their ranges. Comments noted that coral species and their symbionts are not uniformly susceptible and/or resilient to climate change across their ranges. That variability results in heterogeneous responses of coral species to ocean warming both in different parts of the ranges and also at different rates in the future. Another comment provided information from van Hooidonk (2013b) regarding spatial and temporal variability of ocean warming within different regions. The commenter identified reef locations that appear to be less vulnerable to bleaching, including the southern Great Barrier Reef (GBR), the western Indian Ocean, Persian Gulf, Red Sea, Thailand, New Caledonia and French Polynesia, as well as other locations that appear to be more vulnerable to bleaching, including the western Pacific warm pool, northwestern Australia, west Papua New Guinea and the central Pacific islands of Tokelau. Another commenter stated that the corals at Flower Garden Banks National Marine Sanctuary seem to be less affected by elevated sea surface temperatures that are impacting corals in other parts of the wider Caribbean.

Response:
We discussed spatial (
i.e.,
regional and/or local) variability of ocean warming impacts to corals in the proposed rule and we agree that ocean warming will not affect all species in all locations uniformly over the foreseeable future, and that different regions are predicted to experience the effects of ocean warming on different time scales and at different magnitudes than others. We provide a review of all the best available information on spatial variability in ocean warming, including any information provided via public comment or gathered ourselves since the proposed rule was published, in the Threats Evaluation—Global Climate Change Overview, RCP8.5 Projections, and Ocean Warming sub-sections below. These data support the conclusion in the proposed rule that ocean warming is increasing in severity, and likely to continue increasing in severity within the ranges of reef-building corals. This review also underscores the complexity and uncertainty associated with spatial variability in ocean warming across the ranges of reef-building corals. A key difference between the proposed and final rule is that we now more fully consider the ability of each species' spatial and demographic traits to moderate exposure to threats, including warming, and place appropriate emphasis on the non-uniform nature of

global threats at the regional and local levels which allows habitat heterogeneity to play a role in buffering a species against vulnerability to extinction. The significance of coral abundance and distribution and habitat heterogeneity to this final rule is described in more detail in the Corals and Coral Reefs, Risk Analyses and Species-specific Information and Determinations sections of this rule.

Comment 14:
Comments on the overview of ocean warming and coral reefs focused on projected effects of ocean warming on coral reef ecosystems, rather than on reef-building coral species. These comments comprise two distinct views. Some comments emphasized that coral reefs are likely to decline sharply in the future because of increasing GHG emissions, while other comments emphasized that recent reviews indicate a wide range of possible responses by coral species. For example, one commenter cited Frieler
et al.
(2012) and stated that the estimated frequency of coral bleaching at different levels of global warming showed that limiting warming to 1.5 °C above pre-industrial levels is unlikely to protect most of the world's reefs from degradation. The commenter further explained that even under the lowest of the IPCC AR5 emissions scenarios (RCP3-PD) and optimistic assumptions regarding thermal adaptation, approximately one-third (range from 9 to 60 percent) of the world's coral reefs will experience long-term degradation. Another commenter cited Donner (2009) and similarly stated that the projected increase in sea surface temperatures due to the physical commitment from the present accumulation of GHGs due to anthropogenic activity, as well as the amount of GHGs likely to be emitted, is sufficient to cause frequent and higher magnitude heat stress for the majority of the world's coral reefs by 2050. Another commenter provided information from Kiessling
et al.
(2004) and Carpenter
et al.
(2008) and asserted that if bleaching events become very frequent, many species may be unable to maintain breeding populations as repeated bleaching causes potentially irreversible declines, perhaps mimicking conditions that led to previous coral extinctions. In contrast, some commenters disagreed with our conclusion of the projected effects of ocean warming on corals and coral reef ecosystems in the proposed rule. As described above in Comment 13, many commenters pointed out several studies showing regional and local variability in responses of corals and coral reefs to ocean warming.

Response:
We summarized the best available information on the interaction between ocean warming and corals reefs in the proposed rule, and concluded that ocean warming is a severe and increasing threat to corals. The public comments and supporting papers we received on the overview of ocean warming and coral reefs generally support the conclusion in the proposed rule that ocean warming is an important and increasing threat to coral reefs. However, the other comments underscore the uncertainty associated with projecting the effects of ocean warming on coral reefs in the future, and as described in our response to Comment 13, we also acknowledge that there is and will continue to be regional and local variability in responses of corals to ocean warming over the foreseeable future. We acknowledge that ocean warming will not act uniformly on all species at all times over the foreseeable future. Further, we recognize that the responses of each species to ocean warming will vary across their ranges over the foreseeable future. Additionally, as described in previous comment responses, a key difference between the proposed and final rule is that we now more fully consider the threat-buffering capacity of each species' unique characteristics, and place appropriate emphasis on the non-uniform nature of global threats at the regional and local levels which allows habitat heterogeneity to play a role in buffering a species against vulnerability to extinction.

Comment 15:
We received comments on specific effects of ocean warming on reef-building corals that covered various topics, including the interactions of warming-induced bleaching with other threats. For example, one commenter noted that anthropogenic climate change (
e.g.,
ocean warming) weakens coral colonies and renders them more susceptible to disease, which is also covered in the Threats Evaluation—Disease sub-section below. Other commenters also emphasized the potential for ocean warming to act synergistically with other threats such as nutrification as well as overfishing. Another commenter provided information from Ferrier-Pagès
et al.
(2010) suggesting remarkable tolerance to global change, such as the potential to reduce bleaching vulnerability through increased feeding rates.

Response:
In the proposed rule, we discussed how multiple threats stress corals simultaneously or sequentially, whether the effects are cumulative (the sum of individual stresses) or interactive (
e.g.,
synergistic or antagonistic). The comments and supporting papers we received on these topics provide supplemental information (such as synergistic effects of ocean warming with other threats), which has been incorporated and considered in our assessment, as described in more detail in the Threats Evaluation—Ocean Warming sub-section. The comments and supporting papers support the conclusion in the proposed rule that the impacts of ocean warming on reef-building corals are increasing in severity and likely to continue increasing in severity. This information also underscores the great complexity and high uncertainty associated with the various specific effects of ocean warming, including synergistic effects with other threats, across the ranges of reef-building corals. We continue to acknowledge that susceptibility of a species to a threat depends on the combination of: (1) Direct effects of the threat on the species; and (2) the cumulative and interactive (synergistic or antagonistic) effects of the threat with the effects of other threats on the species. In the proposed rule, we considered how the cumulative or interactive effects altered the rating assigned to a threat susceptibility in isolation. However, upon further consideration, we need to evaluate the extent to which one threat influences the susceptibility of an individual species to another threat with more species-specific information, in connection with all the other elements that influence a species' extinction risk. Generally, cumulative and interactive processes are complex and uncertain and existing information about threats interactions is only based on a few studies on a few species. Where possible, when we have species-specific or applicable genus-level information on cumulative or interactive effects, we have applied this information to that particular species' susceptibilities in a more integrated manner.

Comment 16:
We received several comments on the capacity of reef-building corals for acclimatization and adaptation to ocean warming, covering various specific characteristics of reef-building corals that may contribute to such capacity. Mostly, commenters asserted that we did not adequately consider the ability of corals to acclimatize or adapt to changing temperatures. Several comments cited empirical evidence that corals have already adapted to ocean warming, thereby demonstrating the potential for acclimatization or adaptation. For example, one comment letter provided information from Pandolfi
et al.
(2011) and Cahill
et al.
(2013) stating that more recent analyses incorporating thermal

tolerance of species indicate a wide range of outcomes including maintenance of comparable levels of cover to 2100 and beyond. Another commenter provided data from Maynard
et al.
(2008) and Guest
et al.
(2012) showing that many types of coral show surprisingly large (~0.5-1 °C) increases in thermal tolerance after a single mass bleaching event, due to either adaptation or acclimatization. In another comment letter, information provided from Jones and Berkelmans (2010) and Baker
et al.
(2004) show that the acclimatization potential of corals to increased temperatures is an active area of research, with a focus on identifying heat-resistant phenotypes. Another commenter pointed to the coral species that occur in the Arabian Gulf as an example of species adapting to warmer temperatures.

Response:
In the proposed rule we acknowledged that there is some evidence to suggest that reef-building corals may have various mechanisms for acclimatization and adaptation to ocean warming. These topics were described in the Ocean Warming sub-section of the proposed rule, and we concluded that existing scientific information was inconclusive on how these processes may affect individual corals' extinction risk, given the projected intensity and rate of ocean warming. The public comments and supporting papers have been incorporated and considered in our assessment, as described in more detail in the Threats Evaluation—Ocean Warming sub-section and the Species-specific Information and Determinations section. However, the supplemental information does not alter the conclusion in the proposed rule that the capacity for acclimatization and adaptation of reef-building corals to ocean warming is inconclusive for corals generally at this time.

Comments on Disease (High Importance Threat, ESA Factor C)

Comment 17:
One comment regarding the decline of Caribbean coral populations cited land-use changes as well as disease outbreaks (among other local threats) as the causes of Caribbean coral decline rather than climate change. Some comments also provided such information pertaining to specific species. For example, one comment stated that the genetic diversity of
Acropora cervicornis
in Florida may be sufficient to maintain viability and resilience to environmental perturbations and disease.

Response:
The proposed rule described how disease had a major role in the initial decline of Caribbean coral populations as described in the Coral Reefs, Other Coral Habitats, and Overview of Candidate Coral Environments sections of the proposed rule. Further, in the Threats Evaluation—Disease section of this rule, we acknowledge diseases are of high importance with regard to extinction risk of corals. However, in assessing extinction risk over the foreseeable future, climate change-related threats are highly important to all reef-building corals. Any species-specific information provided on disease is included in the Species-specific Information and Determinations section later in this rule.

Comment 18:
One commenter noted the explicit link between coral bleaching, disease, and the larger driving environmental factor of climate change by citing several studies that show anthropogenic climate change weakens coral colonies and renders them more susceptible to disease (Harvell
et al.,
1999; Harvell
et al.,
2002; Knowlton, 2001). Another commenter provided information from Muller and van Woesik (2012), stating that exceeding environmental disease thresholds will most likely become increasingly common in rapidly warming oceans, leading to more frequent coral-disease outbreaks. The study suggested that that the expression of some coral diseases occurs when (1) environmental thresholds are exceeded and (2) these environmental conditions either weaken the corals, which are then more susceptible to infection, or increase the virulence or abundance of pathogens. In other words, corals that experience bleaching are more likely to suffer from disease outbreaks and subsequent mortality.

Response:
In the proposed rule, we described the importance of disease as a threat to corals and the potential for disease to act synergistically with other threats such as ocean warming. We also understand that assessing the threat of disease is highly complex, as the cause or causes of many coral diseases remains either unknown or poorly understood. Overall, the public comments we received underscored and supported the analysis in the SRR and the proposed rule. In addition to public comments, we collected a significant amount of information on disease that became available since the proposed rule published. Thus, we maintain that disease is a high importance threat to the extinction risks of the 65 corals in this final rule. All of the supplemental information received or otherwise collected has been detailed and summarized in the Threats Evaluation—Disease sub-section of this final rule. The extent to which the extinction risk of a particular coral species is impacted by disease is discussed in more detail in the Species-specific Information and Determinations section below.

Comments on Ocean Acidification (Medium-High Importance Threat, ESA Factor E)

Comment 19:
We received public comments on the description of and future projections of ocean acidification, which provided information on the complexity of ocean chemistry on corals, and criticism of the use of the AR4's worst-case scenario as the basis for determining the most likely future scenario with regard to ocean acidification. For example, one commenter asserted that global projections of ocean acidification are too coarse and do not take into consideration competing and extremely localized factors that affect local CO
2
concentrations (
e.g.,
local atmospheric processes, local biological processes, local temperature, and upwelling from deeper waters). The commenter emphasized that despite acknowledging the multitude of local, regional, and seasonal factors that may cause local CO
2
concentrations to increase and pH to decrease, we opted instead to base our reef-scale threat analysis on generalized acidification predictions from global models. Other commenters also criticized our reliance on the IPCC's AR4 report as the basis for our threat evaluation of ocean acidification to corals.

Response:
In the proposed rule we acknowledged that numerous, complex spatial and temporal factors compound uncertainty associated with projecting effects of ocean acidification on corals in the future. We also acknowledged that global climate change models are associated with uncertainty. We further acknowledge that the interpretation of future climate change threats to corals is complex and that effects on individual species of reef-building corals are difficult to determine, as described in more detail in the Threats Evaluation—Global Climate Change Overview subsection. However, we agree with commenters that ocean acidification will not affect all species in all locations uniformly over the foreseeable future, and that different locations will experience the effects of ocean acidification at different time scales and at different magnitudes than others. We provide a review of all the best available information, including a review of AR5's WGI (IPCC, 2013) in the Threats Evaluation—Global Climate Change Overview, RCP8.5 Projections, and Ocean Acidification sub-sections. Upon review of the information provided in AR5's WGI and public comments, our

conclusion regarding the threat of ocean acidification remains unchanged from the proposed rule. We maintain that ocean acidification is increasing in severity, and is likely to continue increasing in severity, within the ranges of reef-building corals, and is a medium-high importance threat in assessing extinction risk for the 65 corals in this final rule. However, as described in earlier comment responses, a key difference between the proposed and final rule is that we now more fully consider the ability of each species' spatial and demographic traits to moderate the impacts of threats, and we place appropriate emphasis on the non-uniform nature of global threats at the regional and local levels which allows habitat heterogeneity to play a role in buffering a species against vulnerability to extinction.

Comment 20:
We received a comment regarding variability in ocean acidification on coral reefs related to fluctuations in pH from localized factors such as seagrass beds. The commenter provided information from Manzello
et al.
(2012) indicating that local and regional biochemical processes buffer effects of ocean acidification in locations such as the Gulf of Mexico and South Atlantic. Manzello
et al.
(2012) reported that the photosynthetic uptake and sequestering of carbon dioxide by seagrasses and other macroalgae and the positive growth response by seagrasses to increasing dissolved carbon dioxide (Palacios and Zimmerman, 2007) may create ocean acidification refugia for corals. Comments on specific effects of ocean acidification on coral reefs and reef-building corals focused on capacity for acclimatization of corals to acidification, and evidence that some coral species are resistant to low pH.

Response:
In the proposed rule, we discussed that numerous, complex spatial and temporal factors compound uncertainty associated with projecting effects of ocean acidification on corals and coral reefs in the future, and we agree with the comment that ocean acidification will not affect all species in all locations uniformly over the foreseeable future, and that different locations will experience the effects of ocean acidification at different time scales and at different magnitudes than others. In response to comments on spatial variability of ocean acidification, such as lack of consideration of localized increase in pH from adjacent seagrass beds, we provide a review of the best available information on spatial variability in ocean acidification, including any information provided by public comments as well as any information we gathered ourselves since the proposed rule was published, in the Threats Evaluation—RCP8.5 Projections and Ocean Acidification sub-sections. These data in our view still support the conclusion in the proposed rule that ocean acidification is increasing in severity, and likely to continue increasing in severity within the ranges of reef-building corals; however, as described in earlier comment responses, a key difference between the proposed and final rule is that we now more fully consider the threat moderation capacity of each species' spatial and demographic traits, and of habitat heterogeneity.

Comment 21:
We received one comment that identified a couple of ocean acidification and coral reef calcification rate studies that were not included in the SRR and proposed rule. The commenter provided two studies: One showing that coral calcification increases with global warming (McNeil
et al.,
2004), and another study showing that corals are already thriving in conditions similar to the ocean acidification conditions predicted by the IPCC for 2100 (Hofmann
et al.,
2011).

Response:
In the proposed rule and supporting documents we acknowledged that some exceptional areas exist where reef-building coral communities appear to be thriving under naturally high CO
2
concentrations. As described in the comment response above to Comment 19, we agree that ocean acidification will not act uniformly on all species in all locations over the foreseeable future. We provide a review of all the best information available on the threat of ocean acidification, including these studies, which we received in public comments, and any information we gathered ourselves in the Threats Evaluation—Ocean Acidification sub-section (
e.g.,
Shamberger
et al.,
in press). This supplemental information supports the proposed rule's conclusion that the threat of ocean acidification has already impacted corals and coral reefs and will become increasingly severe from now to 2100, with increasingly severe consequences for corals and coral reefs. However, as described in previous comment responses, a key difference between the proposed and final rule is that we now more fully consider the capacity of each species' spatial and demographic traits, and habitat heterogeneity, to buffer a species against vulnerability to extinction.

Comment 22:
We received a detailed comment letter with supporting papers regarding specific effects of ocean acidification on reef-building corals, such as effects on reef accretion, effects on larvae and juvenile corals, and interactive or synergistic effects with other environmental variables. For example, the commenter pointed out several studies that underscore the potential impact of ocean acidification on reef calcification rates, noting that even under the most optimistic modeling scenario, 98 percent of reefs would be chemically stressed by 2050. The commenter also emphasized that corals may have a limited ability to adapt to ocean acidification based on an in-situ study of two corals in Florida Bay (Okazaki
et al.,
2013).

Response:
The comment letter and supporting papers support the conclusion in the proposed rule that ocean acidification is increasing in severity, and likely to continue increasing in severity, within the ranges of reef-building corals, resulting in various detrimental impacts. This information also underscores the complexity and uncertainty associated with the various specific effects of ocean acidification, including interactive or synergistic effects with other threats, across the ranges of reef-building corals as well as predicting adaptive capacity. The information provided by the commenter and the supporting papers regarding the specific effects of ocean acidification on corals and coral reefs have been incorporated and described in more detail in the Threats Evaluation—Ocean Acidification sub-section.

Comments on Trophic Effects of Fishing (Medium Importance Threat, ESA Factor A)

Comment 23:
One comment provided supplemental information that was not included in the proposed rule regarding the role of herbivorous fish in terms of building and maintaining reef resilience. The commenter stated that “overfishing also degrades coral reefs, particularly by depleting key functional groups, such as herbivores, that reduce turf algae on reefs and maintain optimal conditions for coral growth and recruitment” and provided Keller
et al.
(2009) as a reference. Another commenter also described the importance of herbivorous functional groups, and stated that limiting or attempting to reduce harvest of predatory fish may cause ecological harm by unbalancing a healthy trophic chain.

Response:
The proposed rule described the importance of trophic interactions which include reducing herbivorous fish species that control algal growth, limiting the size structure of fish populations, reducing species richness of herbivorous fish, and

releasing corallivores from predator control. The supplemental information provided by public comments supports our conclusion in the proposed rule that healthy levels of herbivorous functional groups are essential to coral reef ecosystem resilience in light of climate change-related threats. Detailed information regarding the trophic effects of fishing can be found in the Threats Evaluation—Trophic Effects of Fishing sub-section as well as the Inadequacy of Existing Regulatory Mechanisms—Reef Resilience sub-section.

Comment 24:
One commenter stated that fish landings have been stable for 30 years in St. Thomas, U.S. Virgin Islands, with many species increasing in size, indicating that overfishing is not occurring in this location or contributing to the status of the Caribbean species in that area. The commenter also pointed out numerous sources of sediments and nutrients, and coastal development projects in the U.S. Virgin Islands as the main contributors to coral reef decline rather than overfishing. Other commenters also disagreed that overfishing was contributing to coral reef decline in Hawaii and highlighted significant increases in tourism and in-water recreational activities as local drivers of reef decline in that area.

Response:
Although not explicitly stated in the proposed rule, we agree that levels of fishing effort vary throughout the ranges of the 65 corals under consideration. We did acknowledge that exposure to this threat varies throughout the ranges of the proposed species and between the Caribbean and Indo-Pacific. In the proposed rule, we also recognized that management and regulation of commercial and recreational fisheries are inconsistent throughout the coral reef world. When evaluating the current and potential threat impacts from trophic effects of fishing, we are required to assess this threat throughout the entire ranges of the 65 coral species in this final listing. We understand that levels and impacts of overfishing differ depending on the particular location under evaluation; however, we maintain that the trophic effects of fishing represent a medium importance threat to the extinction risk of all 65 coral species in this final rule.

Comment 25:
One commenter stated that we failed to consider human demography in terms of our analysis of fishing impacts to corals. The commenter noted that large swaths of area throughout Oceania are being depopulated in favor of more metropolitan countries, which reduces the level of human impacts to corals, including fishing pressure.

Response:
The issues of human demography and population trends were covered explicitly in the SRR and considered in the proposed rule. While there may be some areas being depopulated, increased human population and consumption of natural resources are root causes for increases in fishing (particularly of herbivores) at many locations around the globe (Brainard
et al.,
2011). Data from the World Bank show human population abundance and density have increased in all five coral reef regions since 1960 (
i.e.,
Indian Ocean, Caribbean, Southeast Asia, Pacific, and Middle East), with the greatest human population densities and increases in population density in the Southeast Asia and Indian Ocean regions. In these regions, current human population densities are 4-5 times greater than the global average and probably suggest the greatest local human-induced effects to corals and coral reefs. In the areas in closest proximity to coral reefs, the Southeast Asian, Indian Ocean and Middle East regions have the highest densities of people per reef area (Burke
et al.,
2011). However, these data are regional averages. We do not dispute that human demography within any of these regions may be shifting to higher density in metropolitan areas, resulting in a decrease of human disturbance in some portions of these regions. The regional trend data suggest increasing risks to corals and coral reefs overall (Brainard
et al.,
2011). However, because we must consider the extent to which a particular threat impacts each species throughout its entire range, we still maintain that overfishing is a medium importance threat to all 65 coral species in this final rule.

Comments on Sedimentation (Low-Medium Importance Threat, ESA Factors A and E)

Comment 26:
We received some public comments on sedimentation as a threat to the 65 coral species in this final rule. Comments generally underscored the importance of sedimentation as a considerable local threat to corals and pointed out the potential of sedimentation to interact and potentially exacerbate other threats, as well as to reduce coral resilience. For example, we received a detailed comment asserting that prospects for recovery of certain reef sites in the Caribbean from acute episodes of hurricane damage or die-offs from bleaching and disease (brought on by ocean warming) are extremely poor without sustained recruitment, which may be prevented by sediment preempting larval attachment. Further, the commenter identified sedimentation (among other local threats) as a local threat with the capability of exacerbating bleaching and disease impacts, thereby reducing the resilience of corals. One commenter pointed out that mass mortality of
Acropora palmata
at Vega Baja, Puerto Rico, was caused in part by sedimentation. Another commenter stated that near shore marine-origin sediments have almost completely been replaced by terrestrial sediments due to a lack of land use controls, resulting in near total mortality of nearshore
Acropora
stands in the U.S. Virgin Islands. Other commenters identified the negative impacts of sedimentation to reefs on the Hawaiian Island of Molokai, emphasizing the issue of run-off from large rain events in certain areas. In general, these comments emphasize the importance of sedimentation as a threat to the 65 coral species in this final rule, with some asserting that this threat is as important, if not more important, than the higher rated threat of reef fishing.

Response:
We acknowledge all of the public comments and information we received on the threat of sedimentation to the 65 coral species in this final rule. As summarized in the proposed rule, we also recognize the possibility for sedimentation to interact with other global and local threats and potentially reduce the resiliency of coral reef ecosystems and/or impede recovery. In addition to public comments, we also collected supplemental scientific information regarding the impacts of sedimentation to corals that became available after the proposed rule was published. The findings from these studies and more detailed information regarding the evaluation of sedimentation as a threat to coral reefs can be found in the Threats Evaluation—Sedimentation sub-section. We also acknowledge the concern that some comments expressed regarding the importance of this threat in comparison to other local threats. However, for corals in general, we maintain that sedimentation is a low-medium threat to the extinction risk of the 65 corals in this final rule. Any species-specific information we received on sedimentation is included in the Species-specific Information and Determinations section.

Comments on Nutrients (Low-Medium Importance Threat, ESA Factors A and E)

Comment 27:
We received limited public comments on nutrient enrichment of nearshore waters (
i.e.,

eutrophication) and its impacts to coral reef ecosystems. Comments generally underscored the importance of nutrient enrichment as a considerable local threat to corals, and emphasized the potential of nutrient enrichment to interact and potentially exacerbate other threats, as well as reduce coral reef resiliency. For example, we received a detailed comment letter that provided studies regarding the impacts of nutrient enrichment to coral species. These studies, which became available after the proposed rule was published, provide evidence that nutrient enrichment can worsen thermal stress on inshore reef communities, and that management actions to reduce coastal nutrient enrichment can improve the resistance and resilience of vulnerable coastal coral reefs to ocean warming. Another comment detailed some of the impacts of nutrients in the U.S. Virgin Islands. For example, industrial effluent in St. Croix allegedly impacted fisheries in the area to the point where fishermen struggle to sell their catch due to perceived contamination. Further, a sewage pumping station in another area impacted nursery grounds for spiny lobsters. We received other comments regarding the negative impacts of nutrient enrichment in various locations in Florida and Hawaii from sewage outfalls and other land-based sources of pollution. In general, comments emphasized the importance of nutrients as a threat to the 65 coral species in this final rule, some asserting that this threat is as important, if not more, than the higher rated threat of reef fishing.

Response:
In the proposed rule we described the threat nutrient enrichment poses to corals. The public comments and supporting papers regarding the impacts of nutrients to coral reef ecosystems have been considered and incorporated into our assessment, as described in more detail in the Threats Evaluation—Nutrients sub-section. We also acknowledge the concern that some comments expressed regarding the importance of this threat in comparison to other local threats. However, for corals in general, we maintain that nutrient enrichment is a low-medium threat to the extinction risk of the 65 corals in this final rule. Any species-specific information we received on nutrient enrichment is included in the Species-specific Information and Determinations section.

Comments on Sea-Level Rise (Low-Medium Threat, ESA Factor A)

Comment 28:
We received one public comment that cited the Consensus Statement on Climate Change and Coral Reefs (drafted by a working group of eminent scientists and endorsed by hundreds of scientists to address the topic of climate change impacts on coral reefs; ICRS, 2012) as a source of estimates of sea-level rise by the end of this century. However, the comment did not expound upon the potential ramifications of these estimates. We did not receive any other public comments or gather new or supplemental information on the threat of sea-level rise to the 65 corals in this final rule.

Response:
Although we received only one public comment on this topic, we collected supplemental information regarding the threat of sea-level rise to corals as a result of the IPCC's AR5. These findings are summarized in the Threats Evaluation—Sea-Level Rise sub-section.

Comments on Predation (Low Threat, ESA Factor C)

Comment 29:
We received very few comments regarding the threat of predation to the 65 corals in this final rule. The majority of comments we received regarding predation were specific to individual species in Guam. For example, we received a detailed comment letter that included suggested changes to individual species vulnerability ratings to predation, as a result of local crown-of-thorns seastar (
Acanthaster planci
) predation levels. One commenter cautioned us in terms of inferring predation vulnerabilities for certain species from genus-level information. Other comments identified predation as a threat to corals, but provided no further information or scientific references.

Response:
We acknowledge all of the public comments and information we received on the threat of predation to the 65 coral species in this final rule. The extent to which the extinction risk of a coral species is impacted by predation is discussed in more detail in the Species-specific Information and Determinations section, including any information we received from specific locations. We also agree that inferring susceptibility to threats from genus-level information is not always appropriate. However, that particular comment referenced a species we deemed Not Warranted for listing under the ESA, and are no longer considering. In addition to public comments, we collected information regarding the variable effects predation has on certain coral species. These studies are detailed and summarized in the Threats Evaluation—Predation sub-section. Overall, we maintain that predation is a low level threat to the extinction risk of corals in general.

Comments on Collection and Trade (Low Threat, ESA Factor B)

Comment 30:
We received hundreds of comments that strongly criticized our characterization of the trade industry as a whole, stating that our analysis failed to use current science and/or commercial information about the coral trade. Commenters also asserted that we did not adequately consider aquaculture and mariculture industries as a potential alternative to alleviate pressures from wild collection practices. For example, we received a detailed comment regarding the mariculture industry in Indonesia, stating that in the last five years, the coral trade communities of Indonesia have developed coral mariculture with long-term objectives of reducing the wild harvest of coral species for the live coral trade. Another comment letter provided information from recent papers by Rhyne
et al.
(2012) and Wood
et al.
(2012) that report declining trade in wild-harvested Pacific corals and remarkable growth in the production and trade in cultured corals from Pacific countries. Overall, many comments asserted that a shift from wild collected corals to cultured corals is occurring as a result of increasing aquaculture and mariculture operations both within the United States and major source countries such as Indonesia.

Response:
We agree with commenters that the SRR and proposed rule did not adequately describe the full scope of the marine ornamental trade industry and the contribution of captive culture in terms of alleviating pressures from wild collection. We agree that some significant progress has been made in terms of shifting from wild collection of corals to trade of aquacultured and/or maricultured corals as a result of both U.S. domestic production and production of corals in major source countries such as Indonesia. In addition to public comments we also collected a large amount of supplemental information on coral collection and trade. Specifically, we collected information about (1) the physical and ecological impacts of wild collection of coral colonies and/or fragments from their natural habitats; and (2) captive culture (
i.e.
, mariculture and aquaculture) including information on operations and the role of home aquaria as it relates to trade. All of the public comments and supporting papers have been considered and incorporated into our assessment as described in more detail in the Threats Evaluation—Collection and Trade sub-section. However, this information does not change our determination that the threat

is of low importance to the extinction risk of corals, generally.

Comment 31:
We also received numerous comments that strongly disagreed with our characterization and conclusion regarding the adequacy of regulatory mechanisms within the coral trade industry, particularly CITES and other laws in major source countries such as Indonesia. Many commenters assert that CITES and various regulations provide adequate restrictions and requirements for the ornamental trade of coral reef species, such that trade has much less of a negative impact on the extinction risk of the 65 coral species than was portrayed by the proposed rule and supporting documents. One commenter also described Indonesia's development of regulations for their mariculture industry that is helping to alleviate wild collection pressures.

Response:
In the proposed rule we described that there are some protections afforded via CITES and various other national regulations in some countries where trade of coral reef species is prevalent. However, we agree that our evaluation of trade regulations was incomplete. There are numerous challenges in documenting trends in trade due to deficiencies of CITES import and export data, and the most recent information is conflicting. Some reports state that 98 percent of reef-building corals within the aquarium trade are still wild collected, with only two percent originating from maricultured sources (Thornhill, 2012). In contrast, another report shows that maricultured corals accounted for approximately 20 percent of the trade in 2010 (Wood
et al.
, 2012). Further, adequate tracking of wild and maricultured corals along the supply chain from ocean to aquarium is extremely difficult, yet necessary for determining the true dimensions and impacts of the industry (Cohen
et al.
, 2013). Additionally, the level of wild collection of reef-building corals may be underestimated due to an undocumented illegal trade and a significant amount of mortality along the supply chain from reef to aquarium (Thornhill, 2012). There are many other issues and discrepancies related to assessing the overall impacts of the trade and the adequacy of regulations like CITES; however, collection and trade was ultimately ranked as a low level threat to corals in general by the BRT and in the proposed rule. Further, no one species of coral was determined to be threatened or endangered solely due to the effects of the coral trade industry, and that is still true for the final determinations in this rule. Therefore, while we agree CITES provides some protections for corals in the trade industry, we maintain that the threat from collection and trade is low and does not dictate the listing status of any individual species. In addition to public comments, we collected some supplemental information on regulatory mechanisms for the global marine ornamental trade industry, including details regarding trade of both live and dead corals and other coral reef wildlife.

In light of the public comments and information we received regarding the ornamental trade industry, the Threat Evaluation—Collection and Trade sub-section discusses the trade and its impacts to corals in detail, including information regarding the physical and ecological impacts as a result of the collection process, advances in aquaculture and mariculture industries, as well as issues and trends in trade of both live and dead coral. Any species-specific information we received on collection and trade is included in the Species-specific Information and Determinations section.

Comments on Inadequacy of Existing Regulatory Mechanisms (ESA Factor D) and Conservation Efforts

Comment 32:
We received several comments that critiqued our evaluation of local regulatory mechanisms and conservation efforts. Some comments asserted that we failed to adequately consider the beneficial effects of local management actions and conservation efforts with regard to building reef resilience in the face of climate change. For example, we received a comment letter that stated a broad consensus exists for management to increase marine ecosystem resilience to climate change by reducing local anthropogenic stressors and reduction of these stressors may boost the ability of species, communities, and ecosystems to tolerate climate-related stresses or recover after impacts have occurred. Another commenter emphasized the importance of local management for increasing coral reef resiliency, including management of land-use changes and water quality, as well as utilizing coral reef restoration techniques. Overall, these comments disagreed with our characterization regarding the effectiveness of local regulatory mechanisms and conservation efforts in the face of climate change related threats and urged us to consider the concept of reef resilience.

Response:
We recognize that certain aspects of local management actions and conservation efforts need more explanation than was provided in the proposed rule and Management Report (NMFS, 2012b). This final rule provides that additional explanation, as summarized here. There is an emerging body of literature regarding the concept of reef resilience, defined as an ecosystem's capacity to absorb recurrent shocks or disturbances and adapt to change without compromising its ecological function or structural integrity (Hughes
et al.
, 2010; Obura, 2005). Recent evidence suggests that managing local scale disturbances for resilience will be crucial to maintaining complex, bio-diverse coral reef ecosystems given the predicted widespread impacts of climate change related threats (Anthony
et al.
, 2011).

Therefore, we recognize that effective local laws and regulations as well as conservation projects and programs may help reduce impacts to corals and coral reefs from threats on an ecosystem level, positively affecting the timeframe at which corals may become in danger of extinction by providing a protective temporal buffer (
i.e.
, resiliency) to individual coral species in the face of climate change related threats. Some evidence suggests that local management actions, particularly of fisheries (specifically, no-take marine reserves) and watersheds, can delay reef loss by at least a decade under “business-as-usual” rises in GHG emissions (Jackson
et al.
, 2014; Kennedy
et al.
, 2013; Marshall and Schuttenberg, 2006; Mumby and Steneck, 2011). However, many scientists strongly suggest that these local actions be combined with a low-carbon economy to prevent further degradation of reef structures and associated ecosystems (Kennedy
et al.
, 2013).

We cannot definitively say whether and to what degree the presence of regulations in a particular location is currently conferring resilience benefits for any particular species. Overall, we agree that local regulatory actions and conservation efforts to reduce threats are imperative for resiliency of coral reef ecosystems in the face of climate change. However, for purposes of evaluating the inadequacy of regulatory mechanisms as well as conservation efforts under the ESA, we are unable to definitively establish the current status and effectiveness of local regulation of impacts from local threats for any particular species in any given location, with the exception of local regulatory mechanisms for
Acropora palmata
and
A. cervicornis
, which were evaluated in detail in the 2005 status review for those species. Further, we maintain that global regulations to reduce impacts from climate change are inadequate at this time. For more detailed information

about our evaluation of how local regulatory mechanisms relate to building coral reef resilience, please refer to the Threats Evaluation—Inadequacy of Existing Regulatory Mechanisms sub-section. Likewise, for more detailed information about our evaluation of conservation efforts please refer to the Conservation Efforts sub-section.

Comment 33:
We received some comments that disagreed with our characterization of local regulatory mechanisms in general, asserting that certain local laws are sufficient for protection of corals, thus rendering additional protection via the ESA unnecessary. For example, we heard from several commenters who believe there are adequate regulations to prohibit the damage of reef-building corals, such that additional protections from the ESA are redundant. We also received comments that disagreed with our characterization of conservation efforts. For example, we received a comment that disagreed with our conclusion regarding conservation efforts, asserting that coral conservation actions already have, and will continue to, contribute to coral species recovery. Examples of conservation efforts that were not included in the Final Management Report (FMR; NMFS, 2012b) include ongoing coral reef restoration projects, specifically in Florida and the wider-Caribbean, as well as aquaculture and mariculture efforts both internationally (
e.g.
, Indonesia) and within the United States to try to alleviate wild collection pressure on coral reef ecosystems. Comments urged us to take these efforts into consideration for evaluating the status of the 65 corals in this final rule.

Response:
We recognize that certain locations have effective local laws, regulations, and programs that address local threats and provide for the protection and conservation of coral species. For example, it is illegal to collect or harvest reef-building coral species in all U.S. states, territories, and commonwealths. Some laws even prohibit harming any reef-building coral species through activities such as boat groundings and impose penalties and fines for doing so. However, we must evaluate whether regulatory mechanisms are inadequate for corals across their entire ranges rather than in any one specific location. Likewise, our analysis of conservation efforts must also include the entirety of the species' ranges, and it must consider whether those efforts will result in recovering the species to the point of ameliorating threats throughout the species' range to such a degree that a species should be listed as threatened rather than endangered or even not at all. Therefore, we cannot solely consider whether regulations or conservation efforts in the United States or any other particular location are sufficient for reducing threats to corals. The importance of global climate change-related threats to the extinction risk of these corals makes it even more problematic to limit our assessment of conservation efforts and the adequacy of regulatory mechanisms to individual countries. For these corals, we are required to consider the adequacy of regulatory mechanisms for reducing GHG emissions and curbing the rate of global climate change.

For this final rule, we assessed regulatory mechanisms and conservation efforts in a more species-specific approach. To better capture the full breadth of existing regulatory mechanisms, in addition to the individual country descriptions in the Final Management Report, we re-characterized and summarized the presence of existing regulatory mechanisms throughout all the countries in the range of each individual species. The Inadequacy of Threats Evaluation—Existing Regulatory Mechanisms sub-section provides more detailed information on that range-wide evaluation process, as well as the Species Descriptions for the results. For more detailed information about our evaluation of the inadequacy of local management actions, please refer to the Threats Evaluations—Inadequacy of Existing Regulatory Mechanisms sub-section. For more detailed information about our evaluation of conservation efforts, please refer to the Conservation Efforts sub-section of this rule.

Comment 34:
Several comments identified potential errors, omissions, and/or inaccurate characterizations within the Final Management Report (NMFS, 2012b). For example, we received a comment letter pointing out several omissions and inaccuracies regarding Federal management responsibilities for an extensive area of lands and waters in the Pacific Ocean. Many other comments provided additional laws, regulations, or conservation efforts that were not described in the Final Management Report or identified previously during the public engagement period during the summer of 2012. For example, one commenter requested our inclusion of Guam Public law 24-87 that ensures Guam's marine preserves are protected from recreational/commercial activities that may prove detrimental to fragile ecosystems. Another commenter pointed out that we omitted information regarding certain National Wildlife Refuges and National Parks that include coral reefs. We also received a public comment letter requesting us to consider information regarding Indonesia's Coral Reef Rehabilitation and Management Program as a conservation effort.

Response:
We acknowledge that the Final Management Report had some minor errors and omissions. However, it should be noted that the Final Management Report was not intended to be an exhaustive document; rather, it aimed to capture the breadth of existing regulatory mechanisms and conservation efforts that may reduce threat impacts to corals and coral reefs. Due to the immense number of regulatory mechanisms that exist throughout the entire ranges of the 65 coral species (
i.e.
, 84 countries), the Management Report was not intended to identify every individual law and regulation that may have an effect on corals or their threats in every country within the species' ranges. However, any additional laws and regulations that were brought to our attention through the public comments were noted and considered in the analysis of inadequacy of existing regulatory mechanisms presented in this final rule under the Threats Evaluation—Inadequacy of Existing Regulatory Mechanisms sub-section.

Comments on Risk Analyses

Comment 35:
We received many comments regarding the composition of the BRT. Some comments disagreed with the selection of BRT members, asserting that because all seven members of the BRT were Federal employees, non-Federal coral biologists with expertise in the field within specific regions (
e.g.
, Hawaii) were overlooked, thus casting doubt on the qualifications of the BRT members and the results of the status review. One comment suggested that the BRT member votes should have been weighted to reflect their level of expertise in the different types of corals undergoing review. Another comment stated that it would not be possible for certain members of the BRT to act in a neutral or unbiased manner because they are strong proponents of establishing Marine Monuments, sanctuaries, and MPAs for the protection of coral reef systems throughout the U.S. Pacific Islands. Yet another comment stated there was no independent verification from experts who did not have a stake in the Federal ESA listing processes.

Response:
According to agency guidance, members of the BRT should have expertise in the particular species'

biology, population dynamics or ecology, or other relevant disciplines (
e.g.
, ocean/environmental/climate processes, analytical techniques, population genetics, extinction risk, or pertinent threats). Additionally, NMFS must also consider team composition in light of the Federal Advisory Committee Act (FACA). Generally, any committee or group established for the purpose of providing consensus advice or recommendations to a Federal agency is subject to the procedural requirements of FACA. Biological Review Teams are subject to FACA because their assessments constitute group advice upon which NMFS may base its determinations as to whether to list species as endangered or threatened under the ESA. Based on the requirements of FACA, the team must therefore be composed of Federal officials and employees, and specific classes of state employees, unless specifically exempted. As such, the coral BRT was composed of seven Federal scientists from NMFS's Pacific Islands, Northwest, and Southeast Fisheries Science Centers and 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. Additionally, the BRT consulted with numerous non-Federal scientists and subject matter experts during the status review, and had their work peer reviewed, to ensure the best available information was utilized in the SRR. These subject matter experts are detailed in the Acknowledgements of the SRR. Last, we provided extraordinary opportunities for non-Federal scientists to provide their expertise prior to the publication of the proposed rule, including two scientific workshops held in the summer of 2012. All information received was considered in the proposed rule.

Comment 36:
We received numerous criticisms regarding the evaluation methods used by the BRT. Many comments criticized the Critical Risk Threshold voting method used by the BRT for developing extinction risk values for the 82 corals within the proposed rule. Some comments asserted that the voting process relied on subjective opinion rather than scientific facts, while other comments stated that the anonymous scoring system by the BRT could not truly be anonymous. Still, other comments pointed out critical errors or flaws in the BRT's methods. For example, one comment stated that ranking each coral species relative to the rankings of other coral species does not inform NMFS of the risk status of an individual coral species. Another comment stated the Critical Risk Threshold graphs have an inappropriate and misleading quantitative horizontal axis, which suggests higher threat levels than estimated by the BRT. A couple of comments questioned the assignment of levels of confidence in the outcomes of the BRT voting process given the lack of information on which those outcomes were based, noting there was not a high degree of certainty between the experts.

Response:
The voting methods used by the BRT are consistent with previous agency listing determinations that utilized similar structured decision making techniques. This approach is typically used when quantitative modeling of extinction risk is not a viable option due to a lack of precise quantitative population data. The BRT's voting relied upon professional interpretation of the best available scientific information at the time, including qualitative assessments. This approach allowed the BRT to explicitly address various ranges of uncertainty within their voting. We also emphasize that the determinations in the proposed rule did not solely rely on information within the SRR and the voting outcomes of the BRT. As described previously in the proposed rule and throughout this final rule, numerous sources of information were considered and incorporated in the listing determination process, as described in explicit detail in the Risk Analyses and Species-specific Information and Determinations sections. Additionally, the ESA does not require quantitative precision when estimating extinction risk and determining whether a species warrants listing as threatened or endangered under the ESA. Rather, the decision must be reasonable and based solely on the best scientific and commercial information available at the time of the decision, even in light of considerable uncertainty.

Comment 37:
We received several comments that criticized how the proposed rule and supporting documents inferred species' characteristics based on genus-level information (
i.e.
, the proposed rule assumed that information for other species in the genus applied to the proposed species in that genus). A few comments stated that the BRT only considered threats to the taxonomic class and therefore it conducted no individual species threat analysis for any of the candidate coral species. Most comments stated that genus-level info on response to threats, abundance, and other characteristics were improperly extrapolated to species because there are numerous examples in the literature in which ecological or physiological traits are not consistent across species within a genus.

Response:
In the proposed rule, we relied on higher taxonomic level (
i.e.,
genus or family) information for threats susceptibilities when species-specific susceptibilities were not available. We acknowledge that there is intra-genus or intra-family variability in response to threats in many cases. In response to criticism of how the proposed rule and supporting documents inferred species' characteristics based on genus-level information, this final rule does not automatically assume that genus-level information for other species in the genus applies to the proposed species in that genus. Rather, a careful analysis of genus-level information is incorporated into the Species-specific Information and Determination sections below for each of the 21 genera in which the 65 species belong. That is, as a preface to the Species-specific Information and Determinations for species in a genus, this final rule includes a description of the available information for other species in the genus that are not part of this final rule, and an analysis of the degree of applicability of that information to the species included in this final rule. Further, in no case in this final rule do we extrapolate from family-level information.

Comment 38:
We received multiple comments criticizing the definition of “foreseeable future” in the proposed rule and supporting documents out to the year 2100 because it is too far into the future. One comment stated that climate change projections beyond 50 years have a high degree of uncertainty and may be impacted by numerous unforeseen and unpredictable circumstances, and thus identifying the foreseeable future as out to the year 2100 is not appropriate. Another comment stated that our use of 2100 for the foreseeable future is contrary to previous decisions made by FWS and NMFS, and there have been no breakthroughs in climate modeling to justify our new position on the reliability of long-term climate modeling.

Response:
Consistent with our practice for all species listing determinations, 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 the coral species under consideration.

The timeframe established for the foreseeable future considered the time necessary to provide for the conservation and recovery of each threatened species and the ecosystems upon which they depend. It was 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. In the proposed rule, we explained that our choice of the year 2100 as the “foreseeable future” for analysis of global climate change was based on AR4's use of 2100 as the end-point fo

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Source: Frix Law Library, https://www.frixlaw.com/law-library/documents/fr%3A2014-20814. Public record. Not legal advice.