# Endangered and Threatened Species; Critical Habitat for the Threatened Caribbean Corals

> Briefs, arguments, decisions, and more.

URL: https://www.frixlaw.com/law-library/documents/fr%3A2023-16556

## Record

- **Collection:** Federal Register
- **Document type:** Rule
- **Published:** August 9, 2023
- **Citation:** 88 FR 54026

## Text

DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
50 CFR Parts 223 and 226
[Docket No. 230726-0177]
RIN 0648-BG26
Endangered and Threatened Species; Critical Habitat for the Threatened Caribbean Corals

AGENCY:

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

ACTION:

Final rule.

SUMMARY:

We, NMFS, designate critical habitat for five threatened Caribbean coral species,
Orbicella annularis, O. faveolata, O. franksi, Dendrogyra cylindrus,
and
Mycetophyllia ferox,
pursuant to section 4 of the Endangered Species Act (ESA). Twenty-eight mostly overlapping specific occupied areas containing physical features essential to the conservation of these coral species are designated as critical habitat. These areas contain approximately 16,830 square kilometers (km
2
; 6,500 square miles (mi
2
)) of marine habitat. We have considered economic, national security, and other relevant impacts of designating these areas as critical habitat, and we exclude one area from the designations due to anticipated impacts on national security.

DATES:

This rule becomes effective September 8, 2023.

ADDRESSES:

The final rule, maps, and Final Information Report can be found on the NMFS website at
https://www.fisheries.noaa.gov/action/final-rule-designate-critical-habitat-threatened-caribbean-corals.

FOR FURTHER INFORMATION CONTACT:

Jennifer Moore, NMFS, SERO, 727-824-5312,
Jennifer.Moore@noaa.gov;
Celeste Stout, NMFS, Office of Protected Resources, 301-427-8436,
Celeste.Stout@noaa.gov.

SUPPLEMENTARY INFORMATION:

In accordance with section 4(b)(2) of the ESA and our implementing regulations (50 CFR 424.12), this final rule is based on the best scientific data available concerning the range, biology, habitat, threats to the habitat, and conservation objectives for the threatened Caribbean boulder star coral (
Orbicella franksi
), lobed star coral (
O. annularis
), mountainous star coral (
O. faveolata
), pillar coral (
Dendrogyra cylindrus
), and rough cactus coral (
Mycetophyllia ferox
). We have reviewed the available data and public comments received on the proposed rule. We used the best data available to identify: (1) a composite physical feature essential to the conservation of each coral species; (2) the specific areas within the occupied geographical areas that contain the physical essential feature that may require special management considerations or protection; (3) the Federal activities that may impact the critical habitat; and (4) the potential impacts of designating critical habitat for the corals. This final rule is based on the biological information and the economic, national security, and other relevant impacts described in the document titled, Final Information Basis and Impact Considerations of Critical Habitat Designations for Threatened Caribbean Corals (Final Information Report). This supporting document is available at
https://www.regulations.gov
or upon request (see
ADDRESSES
).

Background

We listed 20 coral species as threatened under the ESA effective October 10, 2014 (79 FR 53851, September 10, 2014). Five of the corals occur in the Caribbean:
Orbicella annularis, O. faveolata, O. franksi, Dendrogyra cylindrus,
and
Mycetophyllia ferox.
The final listing determinations were based on the best scientific and commercial data available on a suite of demographic, spatial, and susceptibility factors that influence the species' vulnerability to extinction in the face of continuing threats over the foreseeable future. All of the species had undergone population declines and are susceptible to multiple threats, including ocean warming, diseases, ocean acidification, ecological effects of fishing, and land-based sources of pollution. However, aspects of the species' demography and distribution buffered the effects of the threats. We determined that all the Caribbean coral species were likely to become endangered throughout all of their ranges within a foreseeable future of the next several decades as a result of a combination of threats, of which the most severe are related to climate change, and we listed them as threatened.

On November 27, 2020, NMFS proposed to designate critical habitat for the five listed Caribbean coral species within U.S. waters, and opened a 60-day public comment period (85 FR 76302). The proposed coral critical habitat consisted of a substrate and water column feature essential for the reproduction, recruitment, growth, and maturation of the listed corals. A total of 28 mostly-overlapping areas within the species' ranges in Florida, Puerto Rico, the U.S. Virgin Islands (USVI), Navassa Island, and the Flower Gardens Banks were identified to contain the essential feature. The area covered by the Naval Air Station Key West (NASKW) Integrated Natural Resource Management Plan (INRMP) was ineligible for designation pursuant to section 4(a)(3)(B)(i) of the ESA due to the conservation benefits it affords the threatened corals. Pursuant to section 4(b)(2) of the ESA, only one area was proposed for exclusion from the designation on the basis of national security impacts, and no areas were proposed for exclusion on the basis of economic or other relevant impacts.

The proposed designation was developed in accordance with the ESA section 4 implementing regulations applicable at that time (in 50 CFR 424), which included changes made in 2019 to the definition of physical or biological feature and the designation of unoccupied critical habitat (84 FR 45020, August 27, 2019). On July 5, 2022, the U.S. District Court for the Northern District of California issued an order vacating the ESA section 4 implementing regulations that were revised or added to 50 CFR part 424 in 2019 (“2019 regulations”; 84 FR 45020, August 27, 2019) without making a finding on the merits. On September 21, 2022, the U.S. Court of Appeals for the Ninth Circuit granted a temporary stay of the district court's July 5 order. On November 14, 2022, the Northern District of California issued an order granting the government's request for voluntary remand without vacating the 2019 regulations. The District Court issued a slightly amended order 2 days later on November 16, 2022. As a result, the 2019 regulations remain in effect, and we are applying the 2019 regulations here. For purposes of this designation and in an abundance of caution, we considered whether the analysis or conclusions would be any different under the pre-2019 regulations. We have determined that our analysis and conclusions related to the physical or biological features essential to conservation of the species would not be any different under the 2019 or pre-2019 regulations. Our analysis of unoccupied critical habitat would be different under the pre-2019 regulations but, as explained below, this does not change our prior conclusion that it is not appropriate to designate any unoccupied critical habitat.

Statutory and Regulatory Background for Critical Habitat Designations

The ESA defines critical habitat under section 3(5)(A) as the (1) specific areas

within the geographical area occupied by the species at the time it is listed, on which are found those physical or biological features essential to the conservation of the species (hereafter also referred to as “PBFs” or “essential features”) and which may require special management considerations or protection; and (2) specific areas outside the geographical area occupied by the species at the time it is listed, upon a determination by the Secretary of Commerce (Secretary) that such areas are essential for the conservation of the species (16 U.S.C. 1532(5)(A)). Conservation is defined in section 3(3) of the ESA as to use, and the use of, all methods and procedures which are necessary to bring any endangered species or threatened species to the point at which the measures provided pursuant to this Act are no longer necessary (16 U.S.C. 1532(3)). Section 3(5)(C) of the ESA provides that, except in those circumstances determined by the Secretary, critical habitat shall not include the entire geographical area which can be occupied by the threatened or endangered species. Our regulations provide that critical habitat shall not be designated within foreign countries or in other areas outside U.S. jurisdiction (50 CFR 424.12(g)).

Section 4(a)(3)(B)(i) of the ESA prohibits designating as critical habitat any lands or other geographical areas owned or controlled by the Department of Defense (DOD) or designated for its use, that are subject to an INRMP prepared under section 101 of the Sikes Act (16 U.S.C. 670a), if the Secretary determines in writing that such plan provides a benefit to the species for which critical habitat is designated. Section 4(b)(2) of the ESA requires us to designate critical habitat for threatened and endangered species on the basis of the best scientific data available and after taking into consideration the economic impact, the impact on national security, and any other relevant impact, of specifying any particular area as critical habitat. Pursuant to this section, the Secretary may exclude any area from critical habitat upon determining that the benefits of such exclusion outweigh the benefits of specifying such area as part of the critical habitat. However, the Secretary may not exclude areas if this will result in the extinction of the species.

Once critical habitat is designated, section 7(a)(2) of the ESA requires Federal agencies to ensure that actions they fund, authorize, or carry out are not likely to destroy or adversely modify that habitat (16 U.S.C. 1536(a)(2)). This requirement is in addition to the section 7(a)(2) requirement that Federal agencies ensure their actions are not likely to jeopardize the continued existence of ESA-listed species. Specifying the geographic location of critical habitat also facilitates implementation of section 7(a)(1) of the ESA by identifying areas where Federal agencies can focus their conservation programs and use their authorities to further the purposes of the ESA. Critical habitat requirements do not apply to citizens engaged in actions on private land that do not involve a Federal agency. However, designating critical habitat can help focus the efforts of other conservation partners (
e.g.,
state and local governments, individuals, and non-governmental organizations).

Summary of Changes From the Proposed Rule

We evaluated the comments and information received from the public during the public comment period. Based on our consideration of these comments and information (as noted below in the Summary of Comments and Responses section), we made four substantive changes to the boundaries of critical habitat: (1) the reduction of the maximum depth of the Florida units from 90 m (295 ft) to 40 m (131 ft); (2) the addition of an area north of the Florida Keys within the Florida Keys National Marine Sanctuary (FKNMS) for the three
Orbicella
species; (3) the addition of Bright, McGrail, and Geyer Banks within the Flower Garden Banks National Marine Sanctuary (FGBNMS) for the three
Orbicella
species; and (4) the reduction of the shallow depth limit from 17 m (56 ft) to 16 m (53 ft) in the FGBNMS units. Together, these changes resulted in adding 1,622 sq km (626 sq mi) to the total area of designated critical habitat in FKNMS and 48 sq km (19 sq mi) to the total area of designated critical habitat in FGBNMS.

Reduction of the Maximum Depth of the Florida Units

In the proposed rule, we assumed
O. faveolata, O. franksi, and M. ferox
were present to 90 m (295 ft) in Florida, based on information on the depth limits of the species in other areas in the Caribbean. We received a public comment that the maximum depth limit of these species in Florida was 40 m (131 ft) based on personal observations. Furthermore, a new report on coral species distribution on the mesophotic reefs of Florida confirms that the deepest distribution of
O. faveolata, O. franksi, and M. ferox
is limited to 40 m (131 ft), with a few extremely rare occurrences slightly deeper (1 colony at 43 m (141 ft)) and the majority of the observations less than 37 m (121 ft) (Reed 2021). Based on this information, we changed the portions of the boundaries of the three Florida critical habitat units that were formerly based on the 90-m depth contour to the 40-m contour for
O. faveolata, O. franksi,
and
M. ferox.

Addition of the Area North of the Florida Keys

We received a public comment that the three
Orbicella
species occur in the areas north of the Florida Keys in the FKNMS. Following receipt of this comment, we conducted a further inspection of the data we have collected on the locations of all ESA-listed corals. We also received additional location data specifically on the occurrence of these three species in the area north of the Florida Keys from the FKNMS. Based on this information, we are including this area in the Florida critical habitat units for
O. annularis, O. faveolata,
and
O franksi.

Addition of Bright, McGrail, and Geyer Banks Within the FGBNMS

We received a public comment that the three
Orbicella
species occur at three additional banks within the FGBNMS. The FGBNMS provided data to support the presence of these species within Bright, McGrail, and Geyer Banks, which were recently added to the FGBNMS. Based on this information, we are adding these three banks to the FGBNMS critical habitat units for
O. annularis, O. faveolata,
and
O franksi.

Changing the Shallow Depth Limit in the FGBNMS Units

We also received a public comment that the shallow depth limit of the three
Orbicella
species is 16 m (53 ft), not 17 m (56 ft) as we had proposed. Based on the information provided by the FGBNMS, we are changing the shallow depth limit to 16 m in the Flower Garden Banks (FGB) critical habitat units for
O. annularis, O. faveolata,
and
O franksi.

Other Changes

In addition to these four substantive changes in the final rule, we also made some minor, clarifying changes to the final rule, and to the Final Information Report and its appendices, in response to public comments and new information. Specifically, we made two minor edits to the regulatory language for clarity. The first edit revises the first two sentences of the description of the essential feature to more clearly articulate that this feature is comprised of the sites that support the normal function of all life stages. The second

minor edit is to change “does not” to “cannot” in paragraph (d)(2). This second minor edit is intended to clarify, and thus improve the understanding of, this sentence. All sections of the Final Information Report were updated with information based on the additional reports and studies. The final economic impact analysis took into account the latest economic data and ESA section 7 consultation history, and the Final Regulatory Flexibility Analysis took into account the latest economic information and data. Note, however, that, as in the proposed rule, this final rule does not include any economic exclusions.

Summary of Comments and Responses

We solicited comments on the proposed rule and its supporting documents in a 60-day public comment period (85 FR 76302; November 27, 2020). To facilitate public participation, the proposed rule was made available on our website and comments were accepted via both standard mail and through the Federal eRulemaking portal,
www.regulations.gov.

We received 552 comments through
www.regulations.gov,
which included a combination of comments in support of the action, comments providing additional information, and comments requesting changes to the rule. In addition, we received one comment submission containing a list of 20,566 signatories to a campaign by the Center for Biological Diversity in support of the proposed rule. Comments were received from a range of sources including global and local environmental non-profit groups, local, state, and federal government agencies, trade associations, and concerned citizens. Of the 552 comments submitted, most expressed general support for the proposed rule but did not include substantive content. We considered all public comments and below we provide responses to all substantive issues raised by commenters that are relevant to the proposed coral critical habitat. We do not respond to comments or concerns that we received outside the scope of this rulemaking. As described above in the Summary of Changes from the Proposed Rule section, we incorporated information provided by commenters into the Final Information Report and this final rule.

Comments on the Essential Feature

Comment 1:
One commenter requested that we add a quantitative threshold to the temperature component of the water quality attribute of the essential feature and suggested it could be reworded to “Marine water with temperatures (not to exceed 1.0 °C of location-specific total warming), aragonite saturation, nutrients, and water clarity that have been observed to support any demographic function.” The commenter provided two references to support the 1 °C threshold, Donner
et al.,
2005 and Donner
et al.,
2009.

Response:
In the Draft Information Report and the proposed rule, we described the conditions that may lead to thermal stress, citing several studies that identify the various intensities and durations that lead to stress and mortality. We reviewed the references provided by the commenter, and they have been added to the Final Information Report and this final rule. The majority of this information further supported the information already included in the proposed rule and Draft Information Report. However, we also explained that temperature thresholds are variable in both time (
e.g.,
season) and geographic location (
i.e.,
latitude and longitude) and may be nonlinear. Therefore, we determined that it is not appropriate to identify a standard threshold that applies to all locations and temporal scales as described in the
Physical or Biological Feature Essential to Conservation
section below.

Comment 2:
One commenter stated that the designation “. . . does not take into consideration the protection for any habitats critical to those species that are involved in crucial interactions with the coral species.”

Response:
We understand this comment to mean that we did not consider habitats that support other species, such as parrotfish, that provide specific beneficial functions for healthy coral reefs. The ESA requires us to designate critical habitat for listed species, not associated species such as parrotfish. The proposed rule contemplated the physical and biological features essential to the conservation of the threatened corals and identified one composite feature that supports successful reproduction, recruitment, survival, and growth of all life stages of the five coral species. We did not identify any other features that are essential to the conservation of these species. Coral reef ecosystems are a complex mosaic of habitat and species interactions. The composite essential feature does include many of those interactions within the attributes that determine the quality of the area that contains the essential feature and influences the value of the associated feature. For example, one attribute of the substrate component of the essential feature is low occupancy by fleshy and turf macroalgae, which is mediated by herbivores. Therefore, species interactions that influence the essential feature have already been contemplated in the critical habitat designations.

Comments on the Boundaries of Critical Habitat Areas

Comment 3:
One commenter requested that we add the area on the north side of the Florida Keys (also known as “the backcountry”) within the FKNMS to the critical habitat designations for the three
Orbicella
species due to their presence in that area. The commenter also requested we look at monitoring data to determine the presence of
Mycetophyllia ferox
in the same area and include that species within the designation if the species is present.

Response:
Based on the information provided by the commenter and our review of various monitoring reports, we agree that the area north of the Florida Keys within the boundaries of the FKNMS are occupied by the 3
Orbicella
spp. and these areas are now included in the final designation. We did not find any evidence of
Mycetophyllia ferox
being present within the area; therefore, we are not including the area within the designation for that species.

Comment 4:
One commenter requested that we add several areas in the FGBNMS. They requested that we add the occupied areas within McGrail, Bright, and Geyer Banks. They also requested that we add the unoccupied areas of Stetson and Sonnier Banks. Last, they requested that the shallow depth limit be 16 m (53 ft), rather thant 17 m (56 ft) as identified in the proposed rule.

Response:
As discussed above in the Summary of Changes from the Proposed Rule section, we have included the occupied areas within McGrail, Bright, and Geyer Banks in the final designation. However, as described in the
Unoccupied Critical Habitat Areas
section below, neither the proposed rule nor this final rule include any unoccupied areas within the final designation; therefore, we are not including Stetson and Sonnier Banks. In addition, we have changed the shallow depth limit to 16 m for all occupied areas within the final designation, based on the information that the FGBNMS provided on the depth distribution of these species on these banks.

Comment 5:
One commenter requested that we not include the Dry Tortugas National Park within the critical habitat designation citing the remoteness of the area and existing protections afforded by being a national park.

Response:
The ESA defines critical habitat as: (i) the specific areas within

the geographical area occupied by the species, at the time it is listed in accordance with the provisions of section 4 of the ESA, on which are found those physical or biological features (I) essential to the conservation of the species and (II) which may require special management considerations or protections; and (ii) specific areas outside the geographical area occupied by the species at the time it is listed in accordance with the provisions of section 4 of the ESA, upon a determination by the Secretary that such areas are essential for the conservation. If an area is occupied by the species, contains the essential feature, and may require special management, it meets the definition of critical habitat unless there is a specific basis to exclude the area (
i.e.,
national security or economic, with the benefits of exclusion outweigh the benefits of designating the area). The areas within the boundaries of the Dry Tortugas National Park meet the ESA definition of critical habitat. Furthermore, we did not identify any basis for exclusion (national security, economic, or other relevant) of this area. Although the area in the Dry Tortugas National Park is remote and has existing protections, the area is essential to the conservation of the threatened corals, and it is included in the final designation.

Comment 6:
One commenter requested that we extend the offshore depth boundary for
Orbicella annularis
in the U.S. Virgin Islands to 80 m (263 ft).

Response:
The commenter did not provide any evidence of the presence of
O. annularis
deeper than 20 m in the U.S. Virgin Islands. We do not have any record of the species occurring deeper than 20 m. Therefore, we did not change the boundary for
O. annularis
in the U.S. Virgin Islands.

Comments on the Threats to Critical Habitat

Comment 7:
One commenter stated that the current levels of dissolved inorganic nitrogen concentrations in Florida are detrimental to corals.

Response:
In the proposed rule and Draft Information Report, we identify that excess nutrients, which include inorganic nitrogen, are a threat to corals and their habitat. Excess nutrients are included in the critical habitat designation as part of the attribute, “nutrient levels that have been observed to support any demographic function” of the essential feature.

Comment 8:
One commenter requested that we include the impact on oil and gas exploration and development in areas that may be affected by oil- and gas-related activity in our analysis of the impact of critical habitat, specifically in the Gulf of Mexico, given the location of the Flower Gardens Banks.

Response:
We have included an analysis of potential future consultations on oil and gas exploration in the Final Information Report. We concur that oil and gas exploration and development may affect the essential feature and would be subject to ESA section 7 consultation. Any future Federal activities that may affect the essential feature within the designated critical habitat would require consultation.

Comment 9:
One commenter expressed concern that the decision not to include “managed areas,” such as dredged channels and harbors, in the designation of critical habitat could be detrimental to the survival of corals in the surrounding areas.

Response:
We agree that sedimentation caused by channel dredging is a threat to the five coral species and their habitat. All Federal actions involving potential effects of sedimentation on the threatened corals or their designated critical habitat will be subject to ESA section 7 consultation. However, those areas that are consistently disturbed and that will continue to be disturbed as part of planned management activities by local, state, or Federal government entities (as of the time this rule becomes effective) do not support the essential feature, and, therefore, designation of those areas would not provide for the conservation of the species.

Comment 10:
One commenter discussed our identification of sunscreen ingredients as a threat to corals. They stated that the European Chemicals Agency and the U.S. Environmental Protection Agency (EPA) have data reliability assessment guidelines to determine whether a peer-reviewed study can be used for an environmental risk assessment (ERA). They also stated that Benzophenone-2 is not an approved ultraviolet (UV) filter in the United States and should not be referenced in the rule.

Response:
In the Final Information Report and this final rule (as in the proposed rule), we include the best available information on the threats to corals and their habitat, which includes literature on the impacts of chemicals included in sunscreens and personal care products on corals. Our standard is to use the best available information in designating critical habitat. Thus, we included the best available information on the contaminants that have been found to cause adverse effects in corals, including Benzophenone-2. Furthermore, the reference to the EPA data reliability assessment guidelines for ERAs is not relevant to a critical habitat designation under the ESA. ERAs are a separate Federal process for a separate purpose.

Natural History

This section summarizes life history and biological characteristics of the five corals to provide context for the identification of the physical and biological features essential for the conservation of these species. In this section, we cover several topic areas, including an introduction to reef-building corals, reproduction, settlement and growth, coral habitat types, and coral reef ecosystems. The amount of information available on life history, reproductive biology, and ecology varies for each of the five corals that occur in U.S. waters of the Caribbean. We provide specific information for each species where possible. In addition, we provide information on the biology and ecology of Caribbean corals in general, highlighting traits that these five corals share. The information below is largely summarized from the final listing rule (79 FR 53852, September 10, 2014), and updated with the best scientific information available to date.

Reef-building corals, in the phylum Cnidaria, are marine invertebrates that occur as polyps. The Cnidaria include true stony corals (class Anthozoa, order Scleractinia), the blue coral (class Anthozoa, order Helioporacea), and fire corals (class Hydrozoa, order Milleporina). These species secrete massive calcium carbonate skeletons that form the physical structure of coral reefs. Reef-building coral species collectively produce coral reefs over time when growth outpaces erosion. Corals may also occur on hard substrate that is interspersed among other benthic features (
e.g.,
seagrass beds in the back reef lagoon) in the coral reef ecosystem, but not on the physical structure of coral reefs. Corals also contain symbiotic algae within their cells. As described below, corals produce clones of themselves by several different means, and most corals occur as colonies of polyps.

Reef-building corals are able to grow and thrive in the characteristically nutrient-poor environments of tropical and subtropical regions due to their ability to form mutually beneficial symbioses with unicellular photosynthetic algae (zooxanthellae) belonging to the dinoflagellate genus
Symbiodinium
living within the host coral's tissues. Zooxanthellae provide a

food source for their host by translocating fixed organic carbon and other nutrients. In return, the algae receive shelter and nutrients in the form of inorganic waste metabolites from host respiration. This exchange of energy, nutrients, and inorganic metabolites allows the symbiosis to flourish and helps the coral secrete the calcium carbonate that forms the skeletal structure of the coral colony, which in turn contributes to the formation of the reef. Thus, reef-building corals are also known as zooxanthellate corals. Some corals, which do not contain zooxanthellae, form skeletons much more slowly, and therefore are not considered reef-building. The five corals discussed in this rule are zooxanthellate species, and thus are reef-building species that can grow large skeletons that contribute to the physical structure of coral reefs.

Only about 10 percent of the world's approximately 800 reef-building coral species occur in the Caribbean. The acroporids were once the most abundant and most important species on Caribbean coral reefs in terms of accretion of reef structure, characterizing the “palmata” and “cervicornis” zones in the classical descriptions of Caribbean reefs (Goreau, 1959). The three species (
O. annularis, O. faveolata,
and
O. franski
) in the
Orbicella
star coral species complex have also been dominant components on Caribbean coral reefs, characterizing the “buttress zone” and “annularis zone.” After the die-off of
Acropora
spp., the star coral species complex became the major reef-builder in the greater Caribbean due to their large size.

Most reef-building coral species are colonial, producing colonies made up of polyps that are connected through tissue and skeleton. In a colonial species, a single larva will develop into a discrete unit (the primary polyp) that then produces modular units of itself (
i.e.,
genetically-identical copies, or clones, of the primary polyp). Each polyp consists of a column with mouth and tentacles on the upper side growing on top of a calcium carbonate skeleton that the polyps produced through the process of calcification. Colony growth is achieved mainly through the addition of more cloned polyps. The colony can continue to exist even if numerous polyps die or if the colony is broken apart or otherwise damaged. The five corals are all colonial species, although polyp size, colony size, and colony morphology vary considerably by species, and can also vary based on environmental variables in different habitats. Colonies can produce clones, most commonly through fragmentation or budding (described in more detail below). The five corals are all clonal species with the ability to produce colonies of cloned polyps as well as clones of entire colonies. The way they produce colony-level clones varies by species. For example, branching species are much more likely than encrusting species to produce clones via fragmentation.

Corals use a number of reproductive strategies that have been researched extensively; however, many individual species' reproductive modes remain poorly described. Most coral species use both sexual and asexual propagation. Sexual reproduction in corals is primarily through gametogenesis (
i.e.,
the development of eggs and sperm within the polyps near the base). Some coral species have separate sexes (gonochoric), while others are hermaphroditic (individuals simultaneously containing both sexes), and others are a combination of both (Richmond, 1997). Strategies for fertilization are either by brooding (internal fertilization) or broadcast spawning (external fertilization). Asexual reproduction in coral species usually occurs by fragmentation, when colony pieces or fragments are dislodged from larger colonies to establish new colonies, or by the budding of new polyps within a colony.

Depending on the mode of fertilization, coral larvae (called planulae) undergo development either mostly within the mother colony (brooders) or outside of the mother colony, adrift in the ocean (broadcast spawners). In either mode of larval development, larvae presumably experience considerable mortality (up to 90 percent or more) from predation or other factors prior to settlement and metamorphosis (Goreau
et al.,
1981). Such mortality cannot be directly observed, but is inferred from the large number of eggs and sperm spawned versus the much smaller number of recruits observed later. Coral larvae are relatively poor swimmers; therefore, their dispersal distances largely depend on the duration of the pelagic phase and the speed and direction of water currents transporting the larvae.

All three species of the
Orbicella
star coral species complex are hermaphroditic broadcast spawners, spawning over a 3-night period, 6 to 8 nights following the full moon in late August, September, or early October (Levitan
et al.,
2004). Fertilization success measured in the field was generally below 15 percent for all three species and correlated to the number of colonies concurrently spawning (Levitan
et al.,
2004). The minimum colony size at first reproduction for the
Orbicella
species complex is 83 cm
2
(Szmant-Froelich, 1985). Successful recruitment by the
Orbicella
species has seemingly always been rare with many studies throughout the Caribbean reporting negligible to no recruitment (Bak and Engel, 1979; Hughes and Tanner, 2000; Rogers
et al.,
1984; Smith and Aronson, 2006).

Dendrogyra cylindrus
is a gonochoric (having separate sexes) broadcast spawning species with relatively low annual egg production for its size. The combination of gonochoric spawning with persistently low population densities is expected to yield low rates of successful fertilization and low larval supply. Spawning has been observed several nights after the full moon of August in the Florida Keys (Neely
et al.,
2013; Waddell and Clarke, 2008). In Curaçao,
D. cylindrus
was observed to spawn over a 3-night period, 2-5 nights after the full moons in August and September (Marhaver
et al.,
2015). Lab-reared embryos developed into swimming planulae larvae within 16 hours after spawning and were competent to settle relatively soon afterward (Marhaver
et al.,
2015). Despite the short duration from spawn to settlement competency in the lab, sexual recruitment of this species is low, and there are no reported juvenile colonies in the Caribbean (Bak and Engel, 1979; Chiappone, 2010; Rogers
et al.,
1984).
Dendrogyra cylindrus
can propagate by fragmentation following storms or other physical disturbance (Hudson and Goodwin, 1997). Recent investigations determined that there is no genetic differentiation along the Florida Reef Tract, meaning that all colonies belong to a single mixed population (Baums
et al.,
2016). The same study found that all sampled colonies from Curaçao belonged to a single population that was distinct from the Florida population. Similar studies have not been conducted elsewhere in the species' range.

Mycetophyllia ferox
is a hermaphroditic brooding species producing larvae during the winter months (Szmant, 1986). Brooded larvae are typically larger than broadcast spawned larvae and are expected to have higher rates of survival once settled. However, recruitment of
M. ferox
appears to be very low, even in studies from the 1970s (Dustan, 1977; Rogers and Garrison, 2001).

Spatial and temporal patterns of coral recruitment are affected by substrate availability and community structure, grazing pressure, fecundity, mode and timing of reproduction, behavior of larvae, hurricane disturbance, physical

oceanography, the structure of established coral assemblages, and chemical cues. Additionally, several other factors may influence reproductive success and reproductive isolation, including external cues, genetic precision, and conspecific signaling.

Like most corals, the threatened Caribbean corals require hard, consolidated substrate, including attached, dead coral skeleton, for their larvae to settle. The settlement location on the substrate must be free of macroalgae, turf algae, or sediment for larvae to attach and begin growing a colony. Further, the substrate must provide a habitat where burial by sediment or overgrowth by competing organisms (
i.e.,
algae) will not occur. In general, on proper stimulation, coral larvae settle and metamorphose on appropriate hard substrates. Some evidence indicates that chemical cues from crustose coralline algae (CCA), microbial films, and other reef organisms or acoustic cues from reef environments stimulate planulae's settlement behaviors. Calcification of the newly-settled larva begins with the forming of the basal plate. Buds formed on the initial corallite develop into daughter corallites. Once larvae have metamorphosed onto appropriate hard substrate, metabolic energy is diverted to colony growth and maintenance. Because newly settled corals barely protrude above the substrate, juveniles need to reach a certain size to limit damage or mortality from threats such as grazing, sediment burial, and algal overgrowth. In some species, it appears there is virtually no limit to colony size beyond the structural integrity of the colony skeleton, as polyps apparently can bud indefinitely.

Polyps are the building blocks of colonies, and colony growth occurs both by increasing the number of polyps, as well as extending the supporting skeleton under each polyp. Reef-building corals combine calcium and carbonate ions derived from seawater into crystals that form their skeletons. Skeletal expansion rates vary greatly by taxa, morphology, location, habitat and other factors. For example, in general, branching species (
e.g.,
most
Acropora
species) have much higher skeletal extension rates than massive species (
e.g., Orbicella
species). The energy required to produce new polyps and build calcium carbonate skeleton is provided by the symbiotic relationship corals have with photosynthetic zooxanthellae. Therefore, corals need light for their zooxanthellae to photosynthesize and provide the coral with food, and thus also require low turbidity for energy, growth, and survival. Lower water clarity sharply reduces photosynthesis in zooxanthellae and results in reductions in adult colony calcification and survival (79 FR 53852, September 10, 2014). Some additional information on the biological requirements for reproduction, settlement, and growth is provided below in the
Physical or Biological Features Essential to Conservation
section.

Coral reefs are fragile ecosystems that exist in a narrow band of environmental conditions that allow the skeletons of reef-building coral species to grow quickly enough for reef accretion to outpace reef erosion. High-growth conditions for reef-building corals include clear, warm waters with abundant light, and low levels of nutrients, sediments, and freshwater.

There are several categories of coral reefs: fringing reefs, barrier reefs, patch reefs, platform reefs, and atolls. Despite the differences between the reef categories, most fringing reefs, barrier reefs, atolls, and platform reefs consist of a reef slope, a reef crest, and a back-reef, which in turn are typically characterized by distinctive habitats. The characteristics of these habitat types vary greatly by reef categories, locations, latitudes, frequency of disturbance,
etc.,
and there is also much habitat variability within each habitat type. Temporal variability in coral habitat conditions is also very high, both cyclically (
e.g.,
from tidal, seasonal, annual, and decadal cycles) and episodically (
e.g.,
storms, temperature anomalies,
etc.
). Together, all these factors contribute to the habitat heterogeneity of coral reefs.

The five corals vary in their recorded depth ranges and habitat types. Additionally, each species has different depth ranges depending on the geographic location. All five corals generally have overlapping ranges and occur throughout the wider-Caribbean. The major variance in their distributions occurs at the northern-most extent of their ranges in FGBNMS in the northwest Gulf of Mexico. As described below, critical habitat can be designated only in areas under U.S. jurisdiction, thus we provide the species' distribution in U.S. waters.

Critical Habitat Identification and Designations

The purpose of designating critical habitat is to identify the areas that are essential to the species' recovery. Once critical habitat is designated, it can contribute to the conservation of listed species in several ways, including by identifying areas where Federal agencies can focus their section 7(a)(1) conservation programs, and helping focus the efforts of other conservation partners, such as States and local governments, nongovernmental organizations, and individuals (81 FR 7414, February 11, 2016). Designating critical habitat also provides significant regulatory protection by ensuring that Federal agencies consider the effects of their actions in accordance with section 7(a)(2) of the ESA and avoid or modify those actions that are likely to destroy or adversely modify critical habitat. This requirement is in addition to the section 7 requirement that Federal agencies ensure that their actions are not likely to jeopardize the continued existence of ESA-listed species. Critical habitat requirements do not apply to citizens engaged in activities that do not involve a Federal agency. However, section 3(5)(C) of the ESA clarifies that, except in those circumstances determined by the Secretary, critical habitat shall not include the entire geographical area which can be occupied by the threatened or endangered species.

Our step-wise approach for identifying potential critical habitat areas for the threatened corals was to determine: (1) the geographical area occupied by each coral at the time of listing; (2) the physical or biological features essential to the conservation of the corals; (3) whether those features may require special management considerations or protection; (4) the specific areas of the occupied geographical area where these features occur; and, (5) whether any unoccupied areas are essential to the conservation of any of the corals.

Geographical Area Occupied by the Species

“Geographical area occupied” in the definition of critical habitat is defined as an area that may generally be delineated around species' occurrences, as determined by the Secretary (
i.e.,
range). Such areas may include those areas used throughout all or part of the species' life cycle, even if not used on a regular basis (
e.g.,
migratory corridors, seasonal habitats, and habitats used periodically, but not solely by vagrant individuals) (50 CFR 424.02). The ranges of the five threatened corals span the wider-Caribbean, and specifically include marine waters around Florida, Puerto Rico, USVI and Navassa in the United States (79 FR 53851, September 10, 2014). We did not consider geographical areas outside of the United States, because we cannot designate critical habitat areas outside of U.S. jurisdiction (50 CFR 424.12(g)).

Physical or Biological Features Essential to Conservation

Within the geographical area occupied, critical habitat consists of specific areas on which are found those PBFs essential to the conservation of the species and that may require special management considerations or protection. PBFs essential to the conservation of the species are defined as the features that support the life-history needs of the species, including but not limited to, water characteristics, soil type, geological features, sites, prey, vegetation, symbiotic species, or other features. A feature may be a single habitat characteristic, or a more complex combination of habitat characteristics. Features may include habitat characteristics that support ephemeral or dynamic habitat conditions. Features may also be expressed in terms relating to principles of conservation biology, such as patch size, distribution distances, and connectivity (50 CFR 424.02).

One of the first steps in recovery planning we completed after listing these coral species was to develop a Recovery Outline that contains a Recovery Vision, which describes what the state of full recovery looks like for the species. We identified the following Recovery Vision for the five corals listed in 2014: populations of the five threatened Caribbean corals should be present across their historical ranges, with populations large enough and genetically diverse enough to support successful reproduction and recovery from mortality events and dense enough to maintain ecosystem function (
https://www.fisheries.noaa.gov/resource/document/5-caribbean-coral-species-recovery-outline
). Recovery of these species will require conservation of the coral reef ecosystem through threats abatement to ensure a high probability of survival into the future (NMFS, 2015). The key conservation objective that facilitates this Recovery Vision, and that can be assisted through these critical habitat designations, is supporting successful reproduction and recruitment, and survival and growth of all life stages, by abating threats to the corals' habitats. In the final listing rule, we identified the major threats contributing to the five corals' extinction risk: ocean warming, disease, ocean acidification, trophic effects of reef fishing, nutrient enrichment, and sedimentation. Five of the six major threats (
i.e.,
all but disease) impact corals in part by changing the corals' habitat, making it unsuitable for them to carry out the essential functions at all life stages. Although they were not considered to be posing a major threat at the time of listing, we also identified contaminants as a potential threat to each of these corals (79 FR 53852, September 10, 2014). Thus, we identify ocean warming, ocean acidification, trophic effects of reef fishing, nutrient enrichment, sedimentation, and contaminants as the threats to the five corals' habitat that are impeding their recovery. Protecting essential features of the corals' habitat from these threats will facilitate the recovery of these threatened species.

There are many physical and biological features that are important in supporting the corals' habitat; therefore, we focused on a composite habitat feature that supports their conservation through its relevance to the major threats and threats impeding recovery. The essential feature we ultimately identified is sites with a complex combination of substrate and water column characteristics that support normal functions of all life stages of the corals. Because corals are sessile for almost their entire life cycle, they carry out most of their demographic functions in one location. Thus, we have identified sites with a combination of certain substrate and water column characteristics as the essential feature. Specifically, these sites have attributes that determine the quality of the appropriate attachment substrate, in association with warm, aragonite-supersaturated, oligotrophic, clear marine water, which are essential to reproduction and recruitment, survival, and growth of all life stages of all five species of coral. These sites can be impacted by ocean acidification and ocean warming, trophic effects of reef fishing, nutrient enrichment, sedimentation, and contamination.

Based on the best scientific information available we identified the following essential physical feature for the five corals:

Sites that support the normal function of all life stages of the corals, including reproduction, recruitment, and maturation. These sites are natural, consolidated hard substrate or dead coral skeleton free of algae and sediment at the appropriate scale at the point of larval settlement or fragment reattachment, and the associated water column. Several attributes of these sites determine the quality of the area and influence the value of the associated feature to the conservation of the species:

(1) Substrate with presence of crevices and holes that provide cryptic habitat, the presence of microbial biofilms, or presence of crustose coralline algae;

(2) Reefscape (all the visible features of an area of reef) with no more than a thin veneer of sediment and low occupancy by fleshy and turf macroalgae;

(3) Marine water with levels of temperature, aragonite saturation, nutrients, and water clarity that have been observed to support any demographic function; and

(4) Marine water with levels of anthropogenically-introduced (from humans) chemical contaminants that do not preclude or inhibit any demographic function.

Some new information relevant to the essential feature has been added to the Final Information Report and this final rule. The new information did not result in any changes to the definition of the essential feature from the proposed rule, although this final rule includes minor clarifying edits in the definition, as described in the Summary of Changes from Proposed Rule section.

As described in detail in the Final Information Report, all corals require exposed natural consolidated hard substrate for the settlement and recruitment of larvae or asexual fragments. Recruitment substrate provides the physical surface and space necessary for settlement of coral larvae, and a stable environment for metamorphosis of the larvae into the primary polyp, growth of juvenile and adult colonies, and re-attachment of fragments. The substrate must be available at appropriate physical and temporal scales for attachment to occur. In other words, the attachment location must be available at the physical scale of the larva or fragment, and at the temporal scale of when the larva or fragment is “seeking” recruitment. Larvae can also settle and attach to consolidated dead coral skeleton (Grober-Dunsmore
et al.,
2006; Jordán-Dahlgren, 1992).

A number of features have been shown to influence coral larval settlement. Positive cues include the presence of particular species of crustose coralline algae (Morse and Morse, 1996; Ritson-Williams
et al.,
2010), microbial biofilms (Sneed
et al.,
2014; Webster
et al.,
2004), and cryptic habitat such as crevices and holes (Edmunds
et al.,
2004; Edwards
et al.,
2014; Nozawa, 2012). Features that negatively affect settlement include presence of sediment, turf algae, sediment bound in turf algae, and macroalgae (Birrell
et al.,
2005; Kuffner
et al.,
2006; Richmond
et al.,
2018; Speare
et al.,
2019; Vermeij
et al.,
2009). While sediment, turf algae, and macroalgae are all natural features of the coral reef ecosystem, it is the relative

proportion of free space versus occupied space that influences recruitment; recruitment rate is positively correlated with free space (Connell
et al.,
1997). The recruitment substrate feature is adversely affected by four of the major threats to the five corals: ocean acidification, trophic effects of reef fishing, nutrient enrichment, and sedimentation.

The dominance of fleshy macroalgae as major space-occupiers on many Caribbean coral reefs impedes the recruitment of new corals. A shift in benthic community structure over recent decades from the dominance of stony corals to fleshy algae on Caribbean coral reefs is generally attributed to the greater persistence of fleshy macroalgae under reduced grazing regimes due to human overexploitation of herbivorous fishes (Edwards
et al.,
2014; Hughes, 1994; Jackson
et al.,
2014) and the regional mass mortality of the herbivorous long-spined sea urchin in 1983-84 (Hughes
et al.,
1987). As overall coral cover has declined, the absolute area occupied by macroalgae has increased and herbivore grazing capacity is spread more thinly across a larger relative amount of space (Williams
et al.,
2001). A recent study found that when herbivorous fish biomass was relatively high, macroalgae declined and juvenile coral density increased (Steneck 2019). Further, impacts to water quality (principally nutrient input) coupled with low herbivore grazing are also believed to enhance fleshy macroalgal productivity. Fleshy macroalgae are able to colonize dead coral skeleton and other available substrate, preempting space available for coral recruitment (McCook
et al.,
2001; Pastorok and Bilyard, 1985). The increasing frequency of coral mortality events, such as the 2014-2016 global bleaching event, continues to increase the amount of dead skeleton available to be colonized by algae in the absence of coral recruitment.

The persistence of fleshy macroalgae under reduced grazing regimes also negatively impacts CCA growth, potentially reducing settlement cues, which may reduce settlement of coral larvae (Sharp
et al.,
2010). Most CCA are susceptible to fouling by fleshy algae, particularly when herbivores are absent (Steneck, 1986). Patterns observed in St. Croix and USVI, also indicate a strong positive correlation between CCA abundance and herbivory (Steneck and Testa, 1997). Both turf and macroalgal cover increases and CCA cover decreases with reductions in herbivory, which may last for a period of time even when herbivores are reintroduced (de Ruyter van Steveninck and Bak, 1986; Liddell and Ohlhorst, 1986; Miller
et al.,
1999). The ability of fleshy macroalgae to affect growth and survival of CCA has indirect, yet important, impacts on the ability of coral larvae to successfully settle and recruit.

In addition to the direct impacts of ocean acidification on the corals from reduced aragonite saturation state (discussed later in this section), significant impacts to recruitment habitat are also expected. Kuffner
et al.
(2007) and Jokiel
et al.
(2008) showed dramatic declines in the growth rate of CCA and other reef organisms, and an increase in the growth of fleshy algae at atmospheric CO
2
levels expected later this century. The decrease in CCA growth, coupled with rapid growth of fleshy algae, will result in less available habitat and more competition for settlement and recruitment of new coral colonies.

Several studies show that coral recruitment tends to be greater when macroalgal biomass is low (Birrell
et al.,
2008a; Birrell
et al.,
2005; Birrell
et al.,
2008b; Connell
et al.,
1997; Edmunds
et al.,
2004; Hughes, 1985; Kuffner
et al.,
2006; Rogers
et al.,
1984; Vermeij, 2006). In addition to preempting space for coral larvae settlement, many fleshy macroalgae produce secondary metabolites with generalized toxicity that also may inhibit larval settlement, recruitment, and survival (Kuffner and Paul, 2004; Kuffner
et al.,
2006; Paul
et al.,
2011). Furthermore, algal turfs can trap sediments (Kendrick, 1991; Nugues and Roberts, 2003a; Purcell and Bellwood, 2001; Purcell, 2000; Steneck and Testa, 1997; Wilson and Harrison, 2003), which can act in combination to hinder coral settlement (Birrell
et al.,
2005; Nugues and Roberts, 2003a). These turf algae-sediment mats also can suppress coral growth under high sediment conditions (Nugues and Roberts, 2003b) and may gradually kill the marginal tissues of stony corals with which they come into contact (Dustan, 1977). There is also evidence that benthic cyanobacterial mats are becoming more prevalent and can also inhibit coral recruitment (Benjarano 2018).

Coral recruitment habitat is also adversely impacted by sediment cover, itself. Sediments enter the reef environment through many processes that are natural or anthropogenic in origin, including coastal erosion, coastal development, resuspension of bottom sediments, terrestrial erosion and run-off, in-water construction, dredging for coastal construction projects and navigation purposes, and in-water and beach placement of dredge spoils. The rate of sedimentation affects reef distribution, community structure, growth rates, and coral recruitment (Dutra
et al.,
2006). Accumulation of sediment can smother living corals, cover dead coral skeleton, and exposed hard substrate (Erftemeijer
et al.,
2012; Fabricius, 2005). Sediment accumulation on dead coral skeletons and exposed hard substrate reduces the amount of available substrate for coral larvae settlement and fragment reattachment (Rogers, 1990). The location of larval settlement must be free of sediment for attachment to occur (Harrington
et al.,
2004; Mundy and Babcock, 1998).

The depth of sediments over hard substrate affects the duration that the substrate may be unavailable for settlement. The deeper the sediment, the longer it may take for natural waves and currents to remove the sediment from the settlement substrate. Lirman
et al.
(2003) found sediment depth next to live coral colonies was approximately 1 cm deep and significantly lower than the mean sediment depth collected haphazardly on the reef. Sediment deposition threshold criteria have recently been proposed for classifying sediment impacts to reef habitats based on threshold values in peer-reviewed studies and new modeling approaches (Nelson
et al.,
2016). Nelson
et al.
(2016) suggest that sediment depth greater than 1 cm represents a significant impact to corals, while sediment between 0.5 and 1 cm depth represents a moderate impact, with the ability to recover. Nelson
et al.
(2016) identify sediment depth less than 0.5 cm as posing minimal stress to corals and settlement habitat.

Sediment grain size also affects the severity of impacts to corals and recruitment substrate. Fine grain sediments have greater negative effects to live coral tissue and to recruitment substrate (Erftemeijer
et al.,
2012). Accumulation of sediments is also a major cause of mortality in coral recruits (Fabricius
et al.,
2003). In some instances, if mortality of coral recruits does not occur under heavy sediment conditions, then settled coral planulae may undergo reverse metamorphosis and die in the water column (Te, 1992). Sedimentation, therefore, impacts the health and survivorship of all life stages (
i.e.,
adults, fragments, larvae, and recruits) of corals, in addition to adversely affecting recruitment habitat.

The literature provides several recommendations on maximum sedimentation rates for coral reefs (
i.e.,
levels that managers should strive to stay under). De'ath and Fabricius (2008) and The Great Barrier Reef Marine Park Authority (GBRMPA) (2010)

recommend that sedimentation on the Great Barrier Reef (GBR) be less than a mean annual rate of 3 mg/cm
2
/day, and less than a daily maximum of 15 mg/cm
2
/day. Rogers (1990) recommends that sedimentation rates on coral reefs globally be less than a mean maximum of 10 mg/cm
2
/day to maintain healthy corals, and also notes that moderate to severe effects on corals are generally expected at mean maximum sedimentation rates of 10 to 50 mg/cm
2
/day, and severe to catastrophic effects at >50 mg/cm
2
/day. Similarly, Erftemeijer
et al.
(2012) suggest that moderate to severe effects to corals are expected at mean maximum sedimentation rates of >10 mg/cm
2
/day, and catastrophic effects at >50 mg/cm
2
/day. Nelson
et al.
(2016) suggest that sediment depths of >0.5 cm result in substantial stress to most coral species, and that sediment depths of >1.0 cm are lethal to most coral species. The above generalizations are for coral reef communities and ecosystems, rather than individual species.

Sublethal effects of sediment to corals potentially occur at much lower levels than mortality. Sublethal effects include reduced growth, lower calcification rates and reduced productivity, bleaching, increased susceptibility to diseases, physical damage to coral tissue and reef structures (breaking, abrasion), and reduced regeneration from tissue damage (see reviews by Fabricius
et al.,
2005; Erftemeijer
et al.,
2012; Browne
et al.,
2015; and Rogers, 1990). Erftemeijer
et al.
(2012) states that sublethal effects for coral species that are sensitive, intermediate, or tolerant to sediment (
i.e.,
most reef-building coral species) occur at mean maximum sedimentation rates of between <10 and 200 mg/cm
2
/day, depending on species, exposure duration, and other factors.

Artificial substrates and frequently disturbed “managed areas” are not essential to coral conservation. Only natural substrates provide the quality and quantity of recruitment habitat necessary for the conservation of threatened corals. Artificial substrates are generally less functional than natural substrates in terms of supporting healthy and diverse coral reef ecosystems (Edwards and Gomez, 2007; USFWS, 2004). Artificial substrates are manmade or introduced substrates that are not naturally occurring to the area. Examples include, but are not necessarily limited to, fixed and floating structures, such as aids-to-navigation (AToNs), jetties, groins, breakwaters, seawalls, wharves, boat ramps, fishpond walls, pipes, wrecks, mooring balls, docks, aquaculture cages, and other artificial structures. The essential feature does not include any artificial substrate. In addition, there are some natural substrates that, because of their consistently disturbed nature, also do not provide the quality of substrate necessary for the conservation of threatened corals. While these areas may provide hard substrate for coral settlement and growth over short periods, the periodic nature of direct human disturbance renders them poor environments for coral growth and survival over time (
e.g.,
they can become covered with sediment). Therefore, they are not essential to the conservation of the species. Specific areas that may contain these disturbed natural substrates are described in the
Specific Areas Containing the Essential Features
section of this rule.

The substrate characterized previously must be associated with water that also supports all life functions of corals that are carried out at the site. Water quality conditions fluctuate greatly over various spatial and temporal scales in natural reef environments (Kleypas
et al.,
1999). However, certain levels of particular parameters (
e.g.,
water clarity, water temperature, aragonite saturation) must occur on average to provide the conditions conducive to coral growth, reproduction, and recruitment. Corals may tolerate and survive in conditions outside these levels, depending on the local conditions to which they have acclimatized and the intensity and duration of any deviations from conditions conducive to a particular coral's growth, reproduction, and recruitment. Deviations from tolerance levels of certain parameters result in direct negative effects on all life stages.

As described in the Final Information Report, corals thrive in warm, clear, nutrient-poor marine waters with calcium carbonate concentrations that allow for symbiont photosynthesis, coral physiological processes, and skeleton formation. The water must also have low to no levels of contaminants (
e.g.,
heavy metals, chemicals) that would interfere with normal functions of all life stages. Water quality that supports normal functions of corals is adversely affected by ocean warming, ocean acidification, nutrient enrichment, sedimentation, and contamination.

Seawater temperature is a particularly important limiting factor of coral habitat. Corals occur in a fairly-wide temperature range across geographic locations (15.7 °C-35.5 °C weekly average and 21.7-29.6 °C annual average; Guan
et al.,
2015), but only thrive in areas with mean temperatures in a fairly-narrow range (typically 25 °C-29 °C) as indicated by the formation of coral reefs (Brainard
et al.,
2011; Kleypas
et al.,
1999; Stoddart, 1969; Vaughan, 1919). Short-term exposure (days) to temperature increases of a few degrees (
i.e.,
3 °C-4 °C increase above climatological mean maximum summer temperature) or long-term exposure (several weeks) to minor temperature increases (
i.e.,
1 °C-2 °C above mean maximum summer temperature) can cause significant thermal stress and mortality to most coral species (Berkelmans and Willis, 1999; Jokiel and Coles, 1990; Donner, 2005; Donner 2009).

Ocean warming is one of the most significant threats to the five ESA-listed Caribbean corals considered in this rule (Brainard
et al.,
2011). Mean seawater temperatures in reef-building coral habitat in both the Caribbean and Indo-Pacific have increased during the past few decades, and are predicted to continue to rise between now and 2100 (IPCC, 2013). The primary observable coral response to ocean warming is bleaching of adult coral colonies, wherein corals expel their symbiotic zooxanthellae in response to stress (Brown, 1997). For many corals, an episodic increase of only 1 °C-2 °C above the normal local seasonal maximum ocean temperature can induce bleaching (Hoegh-Guldberg
et al.,
2007; Jones, 2008; Whelan
et al.,
2007). Corals can withstand mild to moderate bleaching; however, severe, repeated, or prolonged bleaching can lead to colony death (Brown, 1997; Whelan
et al.,
2007). Increased sea surface temperatures are occurring more frequently and leading to multiple mass bleaching events (Hughes
et al.,
2017), which are reoccurring too rapidly for coral populations to rebound in between (Hughes
et al.,
2018).

Coles and Brown (2003) defined a general bleaching threshold for reef-building corals as increases in seawater temperatures of 1-3 °C above maximum annual mean temperatures at a given location. Great Barrier Reef Marine Park Authority (2010) defined a general “trigger value” for bleaching in reef-building corals as increases in seawater temperatures of no more than 1 °C above maximum annual mean temperatures at a given location. Because duration of exposure to elevated temperatures determines the extent of bleaching, several methods have been developed to integrate duration into bleaching thresholds, including the number of days, weeks, or months of the elevated temperatures (Berkelmans, 2002; Eakin
et al.,
2009; Goreau and Hayes, 1994; Podesta and Glynn, 1997). NOAA's Coral Reef Watch Program utilizes the

Degree Heating Week method (Glynn & D'Croz, 1990; Eakin
et al.
2009), which defines a general bleaching threshold for reef-building corals as seawater temperatures of 1°C above the maximum monthly mean at a given location for 4 consecutive weeks (
https://coralreefwatch.noaa.gov/
).

These general thresholds were developed for coral reef communities and ecosystems, rather than individual species. Many of these studies are community or ecosystem-focused and do not account for species-specific responses to changes in seawater temperatures, and instead are focused on long-term climatic changes and large-scale impacts (
e.g.,
coral reef distribution, persistence).

In addition to coral bleaching, other effects of ocean warming detrimentally affect virtually every life-history stage of reef-building corals. Impaired fertilization and developmental abnormalities (Negri and Heyward, 2000), mortality, and impaired settlement success (Nozawa and Harrison, 2007; Putnam
et al.,
2008; Randall and Szmant, 2009) have all been documented. Increased seawater temperature also may act synergistically with coral diseases to reduce coral health and survivorship (Bruno and Selig, 2007). Coral disease outbreaks often have either accompanied or immediately followed bleaching events (Brandt and McManus, 2009; Jones
et al.,
2004a; Lafferty
et al.,
2004; Miller
et al.,
2009; Muller
et al.,
2008). Outbreaks also follow seasonal patterns of high seawater temperatures (Sato
et al.,
2009; Willis
et al.,
2004).

In summary, temperature deviations from local averages prevent or impede successful completion of all life history stages of the listed coral species. Identifying temperatures at which the conservation value of habitat for listed corals may be affected is inherently complex and influenced by taxa, exposure duration, and other factors.

Carbonate ions (CO
3
2
−
) are used by many marine organisms, including corals, to build calcium carbonate skeletons. The mineral form of calcium carbonate used by corals to form their skeletons is aragonite. The more carbonate ions dissolved in seawater, the easier it is for corals to build their aragonite skeletons. The metric used to express the relative availability of calcium and carbonate ions is the aragonite saturation state (Ω
arg
). Thus, the lower the Ω
arg
of seawater, the lower the abundance of carbonate ions, and the more energy corals have to expend for skeletal calcification, and vice versa (Cohen and Holcomb, 2009). At saturation states between 1 and 20, marine organisms can create calcium carbonate shells or skeletons using a physiological calcifying mechanism and the expenditure of energy. The aragonite saturation state varies greatly within and across coral reefs and through daily cycles with temperature, salinity, pressure, and localized biological processes such as photosynthesis, respiration, and calcification by marine organisms (Gray
et al.,
2012; McMahon
et al.,
2013; Shaw
et al.,
2012b)).

Coral reefs form in an annually-averaged saturation state of 4.0 or greater for optimal calcification, and an annually-averaged saturation state below 3.3 will result in reduced calcification at rates insufficient to maintain net positive reef accretion, resulting in loss of reef structure (Guinotte
et al.,
2003; Hoegh-Guldberg
et al.,
2007). Guinotte
et al.
(2003) classified the range of aragonite saturation states between 3.5-4.0 as “adequate” and < 3 as “extremely marginal.” Thus, an aragonite saturation state between 3 and 4 is likely necessary for coral calcification. But, generally, seawater Ω
arg
should be 3.5 or greater to enable maximum calcification of reef-building corals, and average Ω
arg
in most coral reef areas is currently in that range (Guinotte
et al.,
2003). Further, Kleypas
et al.
(1999) concluded that a general threshold for Ω
arg
occurs near 3.4, because only a few reefs occur where saturation is below this level. Guan
et al.
(2015) found that the minimum aragonite saturation observed where coral reefs currently occur is 2.82; however, it is not known if those locations hosted live, accreting corals.

Ocean acidification is a term referring to changes in ocean carbonate chemistry, including a drop in the pH of ocean waters, that is occurring in response to the rise in the quantity of atmospheric CO
2
and the partial pressure of CO
2
(pCO
2
) absorbed in oceanic waters (Caldeira and Wickett, 2003). As pCO
2
rises, oceanic pH declines through the formation of carbonic acid and subsequent reaction with water resulting in an increase of free hydrogen ions. The free hydrogen ions react with carbonate ions to produce bicarbonate, reducing the amount of carbonate ions available, and thus reducing the aragonite saturation state.

A variety of laboratory studies conducted on corals and coral reef organisms (Langdon and Atkinson, 2005) consistently show declines in the rate of coral calcification and growth with rising pCO
2
, declining pH, and declining carbonate saturation state. Laboratory experiments have also shown that skeletal deposition and initiation of calcification in newly settled corals is reduced by declining aragonite saturation state (Albright
et al.,
2008; Cohen
et al.,
2009). Field studies from a variety of coral locations in the Caribbean, Indo-Pacific, and Red Sea have shown a decline in linear extension rates of coral skeleton under decreasing aragonite saturation state (Bak
et al.,
2009; De'ath
et al.,
2009; Schneider and Erez, 2006; Tanzil
et al.,
2009). In addition to effects on growth and calcification, recent laboratory experiments have shown that increased pCO
2
also substantially impairs fertilization and settlement success in
Acropora palmata
(Albright
et al.,
2010). Reduced calcification and slower growth will mean slower recovery from breakage, whether natural (hurricanes and storms) or human (breakage from vessel groundings, anchors, fishing gear,
etc.
), or mortality from a variety of disturbances. Slower growth also implies even higher rates of mortality for newly settled corals due to the longer time it will take to reach a colony size that is no longer vulnerable to overgrowth competition, sediment smothering, and incidental predation. Reduced calcification and slower growth means more time to reach reproductive size and reduces sexual and asexual reproductive potential. Increased pCO
2
coupled with increased sea surface temperature can lead to even lower rates of calcification, as found in the meta-analysis by Kornder
et al.
(2018).

In summary, aragonite saturation reductions prevent or impede successful completion of all life history stages of the listed coral species. Identifying the declining aragonite saturation state at which the conservation value of habitat for listed corals may be affected is inherently complex and influenced by taxa, exposure duration, and other environmental and physiological factors.

Nitrogen and phosphorous are two of the main nutrients that affect the suitability of the water column in coral reef habitats (Fabricius
et al.,
2005; Fabricius, 2005). These two nutrients occur as different compounds in coral reef habitats and are necessary in low levels for normal reef function. Dissolved inorganic nitrogen and dissolved inorganic phosphorus in the forms of nitrate (NO
3
−
) and phosphate (PO
4
3
−
) are particularly important for photosynthesis, with dissolved organic nitrogen also providing an important source of nitrogen, and are the dominant forms of nitrogen and phosphorous in coral reef waters.

Excessive nutrients affect corals through two main mechanisms: direct

effects on coral physiology, such as reduced fertilization and growth (Harrison and Ward, 2001; Ferrier-Pages
et al.,
2000), and indirect effects through nutrient-stimulation of other community components (
e.g.,
macroalgae seaweeds, turfs/filamentous algae, cyanobacteria, and filter feeders) that compete with corals for space on the reef (79 FR 53851, September 10, 2014). As discussed previously, the latter also affects the quality of recruitment substrate. The physiological response a coral exhibits to an increase in nutrients mainly depends on concentration and duration. A short duration of a high increase in a nutrient may result in a severe adverse response, just as a chronic, lower concentration might. Increased nutrients can result in adverse responses in all life stages and affect most physiological processes, resulting in reduced number and size of gametes (Ward and Harrison, 2000), reduced fertilization (Harrison and Ward, 2001), reduced growth, mortality (Ferrier-Pages
et al.,
2000; Koop
et al.,
2001), increased disease progression (Vega Thurber
et al.,
2013; Voss and Richardson, 2006), tissue loss (Bruno
et al.,
2003), and bleaching (Kuntz
et al.,
2005; Wiedenmann
et al.,
2012).

Most coral reefs occur where annual mean nutrient levels are low. Kleypas
et al.
(1999) analyzed dissolved nutrient data from nearly 1,000 coral reef sites, finding mean values of 0.25 micromoles per liter (μmol/l) for NO
3−,
and 0.13 μmol/l for PO
4
. Over 90 percent of the sites had mean NO
3
values of <0.6 μmol/l, and mean PO
4
values of <0.2 μmol/l (Kleypas
et al.,
1999). Several authors, including Bell and Elmetri (1995) and Lapointe (1997) have proposed threshold values of 1.0 μmol/l for NO
3
, and 0.1-0.2 μmol/l for PO
4
, beyond which reefs are assumed to be eutrophic. However, concentrations of dissolved nutrients are poor indicators of coral reef status, and the concept of a simple threshold concentration that indicates eutrophication has little validity (McCook, 1999). One reason for that is because corals are exposed to nutrients in a variety of forms, including dissolved nitrogen (
e.g.,
NO
3
), dissolved phosphorus (
e.g.,
PO4
3
), particulate nitrogen (PN), and particulate phosphate (PP). Since the dissolved forms are assimilated rapidly by phytoplankton, and the majority of nitrogen and phosphorus discharged in terrestrial runoff is in the particulate forms, PN and PP are the most common bio-available forms of nutrients for corals on coastal zone reefs (Cooper
et al.,
2008). De'ath and Fabricius (2008) and GBRMPA (2010) provide general recommendations on maximum annual mean values for PN and PP of 1.5 μmol/l PN and 0.09 μmol/l PP for coastal zone reefs. These generalizations are for coral reef communities and ecosystems, rather than individual species.

As noted above, identifying nutrient concentrations at which the conservation value of habitat for listed corals may be affected is inherently complex and influenced by taxa, exposure duration, acclimatization to localized nutrient regimes, and other factors.

Water clarity or transparency is a key factor for marine ecosystems and it is the best explanatory variable for a range of bioindicators of reef health (Fabricius
et al.,
2012). Water clarity affects the light availability for photosynthetic organisms and food availability for filter feeders. Corals depend upon their symbiotic algae for nutrition and thus depend on light availability for algal photosynthesis. Reduced water clarity is determined by the presence of particles of sediment, organic matter, and/or plankton in the water, and so is often associated with elevated sedimentation and/or nutrients. Water clarity can be measured in multiple ways, including percent of solar irradiance at depth, Secchi depth (the depth in the water column at which a black and white disk is no longer visible), total suspended solids (TSS), and Nephelometric Turbidity Unit (NTU) (measure of light scatter based on particles in the water column). Reef-building corals naturally occur across a broad range of water clarity levels from very turbid waters on enclosed reefs near river mouths (Browne
et al.,
2012) to very clear waters on offshore barrier reefs, and many intermediate habitats such as open coastal and mid-shelf reefs (GBRMPA, 2010). Coral reefs appear to thrive in extremely clear areas where Secchi depth is ≥ 15 m or light scatter is < 1 NTU (De'ath and Fabricius, 2010). Typical levels of TSS in reef environments are less than 10 mg/L (Rogers, 1990). The minimum light level for reef development is about 6-8 percent of surface irradiance (Fabricius
et al.,
2014).

For a particular coral colony, tolerated water clarity levels likely depend on several factors, including species, life history stage, spatial variability, and temporal variability. For example, colonies of a species occurring on fringing reefs around high volcanic islands with extensive groundwater inputs are likely to be better acclimatized or adapted to higher turbidity than colonies of the same species occurring on offshore barrier reefs or around atolls with very little or no groundwater inputs. In some cases, corals occupy naturally turbid habitats (Anthony and Larcombe, 2000; McClanahan and Obura, 1997; Te, 2001) where they may benefit from the reduced amount of UV radiation to which they are exposed (Zepp
et al.,
2008).

Reductions in water clarity affect light availability for corals. As turbidity and nutrients increase, thus decreasing water clarity, reef community composition shifts from coral-dominated to macroalgae-dominated, and ultimately to heterotrophic animals (Fabricius
et al.,
2012). Light penetration is diminished by suspended abiotic and biotic particulate matter (esp. clay and silt-sized particles) and some dissolved substances (Fabricius
et al.,
2014). The availability of light decreases directly as a function of particle concentration and water depth, but also depends on the nature of the suspended particles. Fine clays and organic particles are easily suspended from the sea floor, reducing light for prolonged periods, while undergoing cycles of deposition and resuspension. Suspended fine particles also carry nutrients and other contaminants (Fabricius
et al.,
2013). Increased nutrient runoff into semi-enclosed seas accelerates phytoplankton production to the point that it also increases turbidity and reduces light penetration, and can also settle on colony surfaces (Fabricius, 2005). In areas of nutrient enrichment, light for benthic organisms can be additionally severely reduced by dense stands of large fleshy macroalgae shading adjacent corals (Fabricius, 2005).

The literature provides several recommendations on maximum turbidity levels for coral reefs (
i.e.,
levels that managers should strive to stay under). GBRMPA (2010) recommends minimum mean annual water clarity, or “trigger values”, in Secchi distances for the GBR depending on habitat type: for enclosed coastal reefs, 1.0-1.5 m; for open coastal reefs and mid-shelf reefs, 10 m; and for offshore reefs, 17 m. De'ath and Fabricius (2008) recommend a minimum mean annual water clarity trigger value in Secchi distance averaged across all GBR habitats of 10 m. Bell and Elmetri (1995) recommend a maximum value of 3.3 mg/L TSS across all GBR habitats. Thomas
et al.
(2003) recommend a maximum value of 10 mg/L averaged across all Papua New Guinea coral reef habitats. Larcombe
et al.
(2001) recommend a maximum value of 40 mg/L TSS for GBR “marginal reefs”,
i.e.,
reefs close to shore with high natural turbidity levels. Guan
et al.

(2015) recommend a minimum light intensity (μmol photons second/m
2
) of 450 μmol photons second/m
2
globally for coral reefs. The above generalizations are for coral reef communities and ecosystems, rather than individual species.

A coral's response to a reduction in water clarity is dependent on the intensity and duration of the particular conditions. For example, corals exhibited partial mortality when exposed to 476 mg/L TSS (Bengtsson
et al.,
1996) for 96 hours, but had total mortality when exposed to 1000 mg/L TSS for 65 hours (Thompson and Bright, 1980). Depending on the duration of exposure, most coral species exhibited sublethal effects when exposed to turbidity levels between 7 and 40 NTU (Erftemeijer
et al.,
2012). The most tolerant coral species exhibited decreased growth rates when exposed to 165 mg/L TSS for 10 days (Rice and Hunter, 1992). By reducing water clarity, turbidity also reduces the maximum depth at which corals can live, making deeper habitat unsuitable (Fabricius, 2005). Existing data suggest that coral reproduction and settlement are more highly sensitive to changes in water clarity than adult survival, and these functions are dependent on clear water. Suspended particulate matter reduces fertilization and sperm function (Ricardo
et al.,
2015), and strongly inhibits larvae survival, settlement, recruitment, and juvenile survival (Fabricius, 2005).

In summary, water clarity deviations from local averages prevent or impede successful completion of all life history stages of the listed coral species. Identifying turbidity levels at which the conservation value of habitat for listed corals may be affected is inherently complex and influenced by taxa, exposure duration, acclimatization to localized nutrient regimes, and other factors.

The water column may include levels of anthropogenically-introduced chemical contaminants that prevent or impede successful completion of all life history stages of the listed coral species. For the purposes of this rule, “contaminants” is a collective term to describe a suite of anthropogenically-introduced chemical substances in water or sediments that may adversely affect corals. The study of the effects of contaminants on corals is a relatively new field and information on sources and ecotoxicology is incomplete. The major groups of contaminants that have been studied for effects to corals include heavy metals (also called trace metals), pesticides, and hydrocarbons. Other organic contaminants, such as chemicals in personal care products, polychlorinated biphenyl, and surfactants, have also been studied. Contaminants may be delivered to coral reefs via point or non-point sources. Specifically, contaminants enter the marine environment through wastewater discharge, shipping, industrial activities, and agricultural and urban runoff. These contaminants can cause negative effects to coral reproduction, development, growth, photosynthesis, and survival.

Heavy metals (
e.g.,
copper, cadmium, manganese, nickel, cobalt, lead, zinc, and iron) can be toxic at concentrations above naturally-occurring levels. Heavy metals are persistent in the environment and can bioaccumulate. Metals are adsorbed to sediment particles, which can result in their long distance transport away from sources of pollution. Corals incorporate metals in their skeleton and accumulate them in their soft tissue (Al-Rousan
et al.,
2012; Barakat
et al.,
2015). Although heavy metals can occur in the marine environment from natural processes, in nearshore waters they are mostly a result of anthropogenic sources (
e.g.,
wastewater, antifouling and anticorrosive paints from marine vessels and structures, land filling and dredging for coastal expansion, maritime activities, inorganic and organic pollutants, crude oil pollution, shipping processes, industrial discharge, agricultural activities), and are found near cities, ports, and industrial developments.

The effects of copper on corals include physiological impairment, impaired photosynthesis, bleaching, reduced growth, and DNA damage (Bielmyer
et al.,
2010; Schwarz
et al.,
2013). Adverse effects to fertilization, larval development, larval swimming behavior, metamorphosis, and larval survival have also been documented (Kwok and Ang, 2013; Negri and Hoogenboom, 2011; Puisay
et al.,
2015; Reichelt-Brushett and Hudspith, 2016; Rumbold and Snedaker, 1997). Copper toxicity was found to be higher when temperatures are elevated (Negri and Hoogenboom, 2011). Nickel and cobalt can also have negative effects on corals, such as reduced growth and photosynthetic rates (Biscere
et al.,
2015), and reduced fertilization success (Reichelt-Brushett and Hudspith, 2016). Chronic exposure of corals to higher levels of iron may significantly reduce growth rates (Ferrier-Pages
et al.,
2001). Further, iron chloride has been found to cause oxidative DNA damage to coral larvae (Vijayavel
et al.,
2012).

Polycyclic aromatic hydrocarbons (PAHs) are found in fossil fuels, such as oil and coal, and can be produced by the incomplete combustion of organic matter. PAHs disperse through non-point sources such as road run-off, sewage, and deposition of particulate air pollution. PAHs can also disperse from point sources such as oil spills and industrial sites. Studies have found adverse effects of oil pollution on corals that include growth impairments, mucus production, and decreased reproduction, especially at increased temperatures (Kegler
et al.,
2015). Hydrocarbons have also been found to affect early life stages of corals. Oil-contaminated seawater reduced settlement of
O. faveolata
and
Agaricia humilis
and was more severe than any direct or latent effects on survival (Hartmann
et al.,
2015). Natural gas (water accommodated fraction) exposure resulted in abortion of larvae during early embryogenesis and early release of larvae during late embryogenesis, with higher concentrations of natural gas yielding higher adverse effects (Villanueva
et al.,
2011). Exposure to oil, dispersants, and a combination of oil and dispersant significantly decreased settlement and survival of
Porites astreoides
and
Orbicella faveolata
larvae (Goodbody-Gringley
et al.,
2013).

Anthracene (a PAH that is used in dyes, wood preservatives, insecticides, and coating materials) exposure to apparently healthy fragments and diseased fragments (Caribbean yellow band disease) of
O. faveolata
reduced activity of enzymes important for protection against environmental stressors in the diseased colonies (Montilla
et al.,
2016). The results indicated that diseased tissues might be more vulnerable to exposure to PAHs such as anthracene compared to healthy corals. PAH concentrations similar to those present after an oil spill inhibited metamorphosis of
Acropora tenuis
larvae, and sensitivity increased when larvae were co-exposed to PAHs and “shallow reef” ultraviolet (UV) light levels (Negri
et al.,
2016).

Pesticides include herbicides, insecticides, and antifoulants used on vessels and other marine structures. Pesticides can affect non-target marine organisms like corals and their zooxanthellae. Diuron, an herbicide, decreased photosynthesis in zooxanthellae that had been isolated from the coral host and grown in culture (Shaw
et al.,
2012a). Irgarol, an additive in copper-based antifouling paints, significantly reduced settlement in
Porites hawaiiensis
(Knutson
et al.,
2012).
Porites astreoides
larvae exposed to two major mosquito pesticide ingredients, naled and permethrin, for

18-24 hours showed differential responses. Concentrations of 2.96 µg/L or greater of naled significantly reduced larval survivorship, while exposure of up to 6.0 µg/L of permethrin did not result in reduced larval survivorship. Larval settlement, post-settlement survival, and zooxanthellae density were not impacted by any treatment (Ross
et al.,
2015).

Benzophenone-2 (BP-2) is a chemical additive to personal care products (
e.g.,
sunscreen, shampoo, body lotions, soap, detergents), product coatings (oil-based paints, polyurethanes), acrylic adhesives, and plastics that protects against damage from UV light. It is released into the ocean through municipal and boat/ship wastewater discharges, landfill leachates, residential septic fields, and unmanaged cesspits (Downs
et al.,
2014). BP-2 is a known endocrine disruptor and a DNA mutagen, and its effects are worse in the light. It caused deformation of scleractinian coral
Stylophora pistillata
larvae, changing them from a motile planktonic state to a deformed sessile condition at low concentrations (Downs
et al.,
2014). It also caused increasing larval bleaching with increasing concentration (Downs
et al.,
2014).

Benzophenone-3 (BP-3; oxybenzone) is an ingredient in sunscreen and personal care products (
e.g.,
hair cleaning and styling products, cosmetics, insect repellent, soaps) that protects against damage from UV light. It enters the marine environment through swimmers and municipal, residential, and boat/ship wastewater discharges and can cause DNA mutations. Oxybenzone is a skeletal endocrine disruptor, and it caused larvae of
S. pistillata
to encase themselves in their own skeleton (Downs
et al.,
2016). Exposure to oxybenzone transformed
S. pistillata
larvae from a motile state to a deformed, sessile condition (Downs
et al.,
2016). Larvae exhibited an increasing rate of coral bleaching in response to increasing concentrations of oxybenzone (Downs
et al.,
2016).

Polychlorinated biphenyls (PCBs) are environmentally stable, persistent organic contaminants that have been used as heat exchange fluids in electrical transformers and capacitors and as additives in paint, carbonless copy paper, and plastics. They can be transported globally through the atmosphere, water, and food chains. A study of the effects of the PCB, Aroclor 1254, on the
Stylophora pistillata
found no effects on coral survival, photosynthesis, or growth; however, the exposure concentration and duration may alter the expression of certain genes involved in various important cellular functions (Chen
et al.,
2012).

Surfactants are used as detergents and soaps, wetting agents, emulsifiers, foaming agents, and dispersants. Linear alkylbenzene sulfonate (LAS) is one of the most common surfactants in use. Biodegradation of surfactants can occur within a few hours up to several days, but significant proportions of surfactants attach to suspended solids and remain in the environment. This sorption of surfactants onto suspended solids depends on environmental factors such as temperature, salinity, or pH. Exposure of
Pocillopora verrucosa
to LAS resulted in tissue loss on fragments (Kegler
et al.,
2015). The combined effects of LAS exposure with increased temperature (+3 °C, from 28 to 31 °C) resulted in greater tissue loss than LAS exposure alone (Kegler
et al.,
2015).

In summary, there are multiple chemical contaminants that prevent or impede successful completion of all life history stages of the listed coral species. Identifying contaminant levels at which the conservation value of habitat for listed corals may be affected is inherently complex and influenced by taxa, exposure duration, and other factors.

As described above, the best-available information shows coral reefs form on solid substrate, but only within a narrow range of water column conditions that on average allow the deposition rates of corals to exceed the rates of physical, chemical, and biological erosion (
i.e.,
conducive conditions, Brainard
et al.,
2005). However, as with all ecosystems, water column conditions are dynamic and vary over space and time. Therefore, we also describe environmental conditions in which coral reefs currently exist globally, thus indicating the conditions that may be tolerated by corals and allow at least for survival. To the extent tolerance conditions deviate in duration and intensity from conducive conditions, they may not support coral reproduction and recruitment, and reef growth, and thus would impair the recovery of the species. Further, annually and spatially averaged-tolerance ranges provide the limits of the environmental conditions in which coral reefs exist globally (Guan
et al.,
2015), but these conditions do not necessarily represent the conditions that may be tolerated by individual coral species. Individual species may or may not be able to withstand conditions within or exceeding the globally-averaged tolerance ranges for coral reefs, depending on the individual species' biology, local average conditions to which the species are acclimatized, and intensity and duration of exposure to adverse conditions. In other words, changes in the water column parameters discussed above that exceed the tolerance ranges may induce adverse effects in a particular species. Thus, the concept of individual species' tolerance limits is a different aspect of water quality conditions compared to conditions that are conducive for formation and growth of reef structures.

These values presented in the summaries above constitute the best available information at the time of this rulemaking. It is possible that future scientific research will identify more species-specific values for some of these parameters that become more applicable to the five listed coral species, though it is also possible that future species-specific research will document that conducive or tolerance ranges for the five Caribbean corals fall within these ranges. Because the ESA requires us to use the best scientific information available in conducting consultations under section 7, we will incorporate any such new scientific information into consultations when evaluating potential impacts to the critical habitat.

Special Management Considerations or Protection

Specific areas within the geographical area occupied by a species may be designated as critical habitat only if they contain essential features that may require special management considerations or protection (16 U.S.C. 1532(5)(A)(i)(II). Special management considerations or protection are any methods or procedures useful in protecting physical or biological features for the conservation of listed species (50 CFR 424.02). In determining whether the essential physical or biological features “may require” special management considerations or protection, it is necessary only to find that there is a possibility that the features may require special management considerations or protection in the future; it is not necessary to find that such management is presently or immediately required.
Home Builders Ass'n of N. California
v.
U.S. Fish and Wildlife Serv.,
268 F. Supp. 2d 1197, 1218 (E.D. Cal. 2003).

The essential feature we have identified is particularly susceptible to impacts from human activity because of the relatively shallow water depth range (less than 295 ft (90 m)) the corals inhabit. The proximity of this habitat to coastal areas subjects this feature to impacts from multiple activities, including, but not limited to, coastal and in-water construction, dredging and disposal activities, beach nourishment,

stormwater run-off, wastewater and sewage outflow discharges, point and non-point source discharges of contaminants, and fishery management. Further, the global oceans are being impacted by climate change from greenhouse gas emissions, particularly the tropical oceans in which the Caribbean corals occur (van Hooidonk
et al.,
2014). The impacts from these activities, combined with those from natural factors (
e.g.,
major storm events), significantly affect habitat for all life stages for these threatened corals. We conclude that the essential feature is currently and will likely continue to be negatively impacted by some or all of these factors.

Greenhouse gas emissions (
e.g.,
fossil fuel combustion) lead to global climate change and ocean acidification. These activities adversely affect the essential feature by increasing sea surface temperature and decreasing the aragonite saturation state. Coastal and in-water construction, channel dredging, and beach nourishment activities can directly remove the essential feature by dredging it or by depositing sediments on it, making it unavailable for settlement and recruitment of coral larvae or fragments. These same activities can impact the essential feature by creating turbidity during operations. Stormwater run-off, wastewater and sewage outflow discharges, and point and non-point source contaminant discharges can adversely impact the essential feature by allowing nutrients and sediments, as well as contaminants, from point and non-point sources, including sewage, stormwater and agricultural runoff, river discharge, and groundwater, to alter the natural levels in the water column. The same activities can also adversely affect the essential feature by increasing the growth rates of macroalgae, which preempts available recruitment habitat. Fishery management can adversely affect the essential feature if it allows for the reduction in the number of herbivorous fishes available to control the growth of macroalgae on the substrate.

Given these ongoing threats throughout the corals' habitat, we find that the essential feature may require special management considerations.

Specific Areas Containing the Essential Feature

The definition of critical habitat requires us to identify specific areas on which are found the physical or biological features essential to the species' conservation that may require special management considerations or protection. Our regulations state that critical habitat will be shown on a map, with more-detailed information discussed in the preamble of the rulemaking documents in the
Federal Register
, which will reference each area by the State, county, or other local governmental unit in which it is located (50 CFR 424.12(c)). Our regulations also state that when several habitats, each satisfying requirements for designation as critical habitat, are located in proximity to one another, an inclusive area may be designated as critical habitat (50 CFR 424.12(d)).

For each of the five coral species, boundaries of specific areas were determined by each species' commonly occupied minimum and maximum depth ranges within each coral's range at the time of listing. Across all 5 coral species, a total of 28 specific areas were identified as being under consideration for critical habitat designation. There are five or six specific areas per species, depending on whether the species occurs in FGBNMS; one area each in Florida, Puerto Rico, St. Thomas and St. John, USVI, St. Croix, USVI, FGB, and Navassa Island. Within each of the geographic areas, the individual species' specific areas are largely-overlapping. For example, in Puerto Rico, there are five largely-overlapping specific areas, one for each species, that surround each of the islands. The difference between each of the areas is the particular depth contours that were used to create the boundaries. For example,
Dendrogyra cylindrus'
specific area in Puerto Rico extends from the 1-m contour to the 25-m contour, which mostly overlaps the
Orbicella annularis
specific area that extends from the 0.5-m contour to the 20-m contour. Overlaying all of the specific areas for each species results in the maximum geographic extent of these critical habitat designations, which cover 1.6 to 295 ft (0.5-90 m) water depth around all the islands of Puerto Rico, USVI, and Navassa, 53 ft to 295 ft (16-90 m) in FGB, and 1.6 to 131 ft (0.5-40 m) from St. Lucie Inlet, Martin County to Dry Tortugas, Florida. The minimum depth in FGBNMS was updated from 17 m to 16 m for
Orbicella annularis, O. faveolata,
and
O. franksi
based on public comment (see the response to Comment 4 above). The maximum depth was updated from 90 m to 40 m in Florida for
O. faveolata, O. franksi,
and
Mycetophyllia ferox
based on public comment and new information (Reed, 2021).

To map these specific areas we reviewed available data on species occurrence, bathymetry, substrate, and water quality. We used the highest resolution bathymetric data available from multiple sources depending on the geographic location. In Florida and the FGB, we used contours created from National Ocean Service Hydrographic Survey Data and NOAA ENCDirect bathymetric point data (NPS) and contours created from NOAA's Coastal Relief Model. We also used bathymetry collected with multi-beam sonar in the FGB (USGS, 2002). In Puerto Rico, contours were derived from the National Geophysical Data Center's (NGDC) 2005 U.S. Coastal Relief Model. In USVI, we used contours derived from NOAA's 2004-2015 Bathymetric Compilation. In Navassa, contours were derived from NOAA's NGDC 2006 bathymetric data. These bathymetric data (
i.e.,
depth contours) are used, with other geographic or management boundaries, to draw the boundaries of each specific area on the maps in this final critical habitat designation.

Within the areas bounded by depth and species occurrence, we evaluated available data on the essential feature. For substrate, we used information from the NCCOS Benthic Habitat Mapping program, which provides data and maps at
http://products.coastalscience.noaa.gov/collections/benthic/default.aspx,
summarized in the Coral Reef Data Explorer at
http://maps.coastalscience.noaa.gov/coralreef/#,
and the Unified Florida Reef Tract Map found at
http://geodata.myfwc.com/datasets/6090f952e3ee4945b53979f18d5ac3a5_9.
Using Geographic Information System (GIS) software, we extracted all habitat classifications that could be considered potential recruitment habitat, including hardbottom and coral reef. The benthic habitat information assisted in identifying any major gaps in the distribution of the substrate essential feature. The data show that hard substrate is unevenly distributed throughout the ranges of the species. However, there are large areas where benthic habitat characterization data are still lacking, particularly deeper than 99 ft (30 m). Because the species occurs in these areas, we made the reasonable assumption that the substrate feature does exist in those areas, though in unknown quantities. The available data also represent a snapshot in time, while the exact location of the habitat feature may change over time (
e.g.,
natural sediment movement covering or exposing hard substrate).

There are areas within the geographical and depth ranges of the species that contain natural hard substrates that, due to their consistently disturbed nature, do not provide the quality of substrate essential for the conservation of threatened corals. These disturbances may be naturally occurring

or caused by human activities, as described below. While these areas may provide hard substrate for coral settlement and growth over short periods, the periodic nature of direct human disturbance renders them poor habitat for coral growth and survival over time. These “managed areas,” for the purposes of this final rule, are specific areas where the substrate has been persistently disturbed by planned management activities authorized by local, state, or Federal governmental entities at the time of critical habitat designation, and expectations are that the areas will continue to be periodically disturbed by such management activities. Examples include, but are not necessarily limited to, dredged navigation channels, vessel berths, and active anchorages. These managed areas were not proposed for designation as critical habitat, and they are not included in the final designations. GIS data of the locations of some managed areas were available and extracted from the maps of the specific areas being considered for critical habitat designation. These data were not available for every managed area; however, regardless of whether the managed area is extracted from the maps depicting the specific areas being designated as critical habitat, no “managed areas” are part of the specific areas that contain the essential feature.

NMFS is aware that dredging may result in sedimentation impacts beyond the actual dredge channel. Where these impacts are persistent, expected to recur whenever the channel is dredged, and are of such a level that the areas in question have already been made unsuitable for coral, these persistently impacted areas are considered part of the managed areas and are thus not part of the specific areas that contain the essential feature.

The nearshore surf zones of Martin, Palm Beach, Broward, and Miami-Dade Counties are also consistently disturbed by naturally-high sediment movement, suspension, and deposition levels. Hard substrate areas found within these nearshore surf zones are ephemeral in nature and are frequently covered by sand, and the threatened coral species have never been observed there. Thus, this area (water in depths from 0 ft to 6.5 ft (0 m to 2 m) offshore St. Lucie Inlet to Government Cut) does not contain the essential feature and is not considered part of the specific areas under consideration for critical habitat. The shallow depth limit (
i.e.,
inshore boundary) was identified based on the lack of these or any reef building corals occurring in this zone, indicating conditions are not suitable for their settlement and recruitment into the population. These conditions do not exist in the area south of Government Cut, nor in the nearshore zones around the islands of Puerto Rico and the U.S. Virgin Islands. In these areas, the hydrodynamics allow for the growth of some (
e.g., Orbicella
spp.) of the threatened coral in the shallow depths.

Due to the ephemeral nature of conditions within the water column and the various scales at which water quality data are collected, this aspect of the essential feature is difficult to map at fine spatial or temporal scales. However, annually-averaged plots of temperature, aragonite saturation, nitrate, phosphate, and light, at relatively large spatial scale (
e.g.,
1° × 1° grid) are available from Guan
et al.
(2015), using 2009 data for some parameters, and updated with newer data from the World Ocean Atlas (2013) for temperature and nutrients. Those maps indicate that conditions that support coral reef growth, and thus coral demographic functions, occur throughout the specific areas under consideration.

Based on the available data, we identified 28 mostly-overlapping specific areas that contain the essential feature. The specific areas, or units, can generally be grouped as the: (1) Florida units, (2) Puerto Rico units, (3) St. Thomas/St. John units (STT/STJ), (4) St. Croix units, (5) Navassa units, and (6) FGB units. Within each group of units, each species has its own unique unit that is specific to its geographic and depth distributions. Therefore, within a group there are five mostly-overlapping units—one for each species. The exception is that there are only three completely-overlapping units in the FGB group, because only the three species of
Orbicella
occur there. The essential feature is unevenly distributed throughout these 28 units. Within these units there exists a mosaic of habitats at relatively small spatial scales, some of which naturally contain the essential features (
e.g.,
coral reefs) and some of which do not (
e.g.,
seagrass beds). Further, within these units, managed areas and naturally disturbed areas, as described above, also exist. Due to the spatial scale at which the essential feature exists interspersed with these other habitats and disturbed areas, we are not able to more discretely delineate the specific areas of critical habitat.

Unoccupied Critical Habitat Areas

ESA section 3(5)(A)(ii) defines critical habitat to include specific areas outside the geographical area occupied by the species at the time of listing if the areas are determined by the Secretary to be essential for the conservation of the species.

In considering whether any unoccupied areas are essential to the threatened coral species, we considered the nature of the threats to the species and their geographic distributions. The threats to these five corals are generally the same threats affecting coral reefs throughout the world (
e.g.,
climate change, fishing, and land-based sources of pollution) and are fully described in the final listing rule (79 FR 53852, September 10, 2014). Specifically, ocean warming, disease, and ocean acidification are the three most significant threats that will impact the potential for recovery of all the listed coral species. Because the primary threats are global in nature, adapting to changing conditions will be critical to the species' conservation and recovery.

We issued guidance in June 2016 on the treatment of climate change uncertainty in ESA decisions, which addresses critical habitat specifically (
https://www.fisheries.noaa.gov/national/endangered-species-conservation/endangered-species-act-guidance-policies-and-regulations
). The guidance states that, when designating critical habitat, NMFS will consider proactive designation of unoccupied habitat as critical habitat when there are adequate data to support a reasonable inference that the habitat is essential for the conservation of the species because of the function(s) it is likely to serve as climate changes. As noted above, we applied the 2019 regulations to evaluate the appropriateness of designating unoccupied critical habitat in the proposed rule. Those regulations state that we will only consider unoccupied areas to be essential where a critical habitat designation limited to geographical areas occupied would be inadequate to ensure the conservation of the species (50 CFR 424.12(b)(2)). However, as noted previously, on July 5, 2022, the United States District Court for the Northern District of California issued an order vacating the regulations finalized in 2019 (84 FR 44976, August 27, 2019), and this order was subsequently temporarily stayed on September 21, 2022, by the U.S Court of Appeals for the Ninth Circuit. Thus, while the 2019 regulations are currently in effect and were applied in this rulemaking, we also considered the pre-2019 regulations and the climate change guidance to determine whether our conclusions would differ. As explained below, we conclude that our determination with respect to unoccupied areas would not have been any different. However, because of the ongoing litigation related to the 2019

regulations, we also explain why application of the pre-2019 regulations results in the same conclusion.

All five corals occur in the Caribbean, an area predicted to have more rapid and severe impacts from climate change as compared to other tropical locations (van Hooidonk
et al.,
2014). Shifting into previously unoccupied habitats that become more suitable as other parts of their range become less suitable may be a strategy these corals employ in the future to adapt to changing conditions. However, due to the nature of the Caribbean basin, there is little opportunity for range expansion. The only area of potential expansion is north up the Florida coast. Several of the five coral species have different northern limits to their current range, with
Orbicella faveolata'
s limit at St. Lucie Inlet, Martin County, Florida, being the farthest north and at the limit of coral reef formation in Florida for these species. A northern range expansion along Florida's coast beyond this limit is unlikely due to lack of evidence of historical reef growth in these areas under warmer climates. Further, northern expansion is inhibited by hydrographic conditions (Walker and Gilliam, 2013). The other corals could theoretically expand into the area between their current northern extents to the limit of reef formation. However, temperature is not likely the factor limiting occupation of those areas, given the presence of other reef-building corals. Thus, there are likely other non-climate-related factors limiting the northern extent of the corals' ranges.

Because the occupied critical habitat we have identified includes specific areas that extend throughout the historical and current range of the listed species, we find that the designations are adequate to provide for the conservation of the five corals. Further, there is no basis to conclude that any specific unoccupied areas are essential to the conservation of the five corals, as described above. Therefore, applying either the 2019 regulations or pre-2019 regulations, we have determined that it is not appropriate to designate any unoccupied areas as critical habitat for the five corals.

Application of ESA Section 4(a)(3)(B)(i) (Military Lands)

Section 4(a)(3)(B)(i) of the ESA prohibits designating as critical habitat any lands or other geographical areas owned or controlled by the DoD, or designated for its use, that are subject to an INRMP prepared under section 101 of the Sikes Act (16 U.S.C. 670a), if the Secretary determines in writing that such plan provides a conservation benefit to the species for which critical habitat is designated. Pursuant to our regulations at 50 CFR 424.12(h) we consider the following when determining whether such a benefit is provided:

(1) The extent of the area and features present;

(2) The type and frequency of use of the area by the species;

(3) The relevant elements of the INRMP in terms of management objectives, activities covered, and best management practices, and the certainty that the relevant elements will be implemented; and

(4) The degree to which the relevant elements of the INRMP will protect the habitat from the types of effects that would be addressed through a destruction-or-adverse-modification analysis.

NASKW is the only installation controlled by the DoD, specifically the Department of the Navy (Navy), that coincides with any of the areas meeting the definition of critical habitat for four of the listed coral species. On September 21, 2015, the Navy requested in writing that the areas covered by the 2014 INRMP for NASKW not be designated as critical habitat, pursuant to ESA section 4(a)(3)(B)(i), and provided the INRMP for our review.

The NASKW INRMP covers the lands and waters—generally out to 50 yards (45.7 m)—adjacent to NASKW, including several designated restricted areas (see INRMP figures C-1 through C-14). The total area of the waters covered by the INRMP that overlaps with areas identified as critical habitat is approximately 800 acres (324 hectares). Within this area, four of the threatened corals (
D. cylindrus, O. annularis, O. faveolata, and O. franksi
) and the essential feature are present in densities and proportions similar to those throughout the rest of the nearshore habitat in the Florida Keys. The species use this area in the same way that they do all areas identified as critical habitat—to carry out all life functions. As detailed in Chapter 4 and Appendix C of the INRMP, the plan provides benefits to the threatened corals and existing
Acropora
critical habitat through the following NASKW broad programs and activities: (1) erosion control—which will prevent sediments from entering into the water; (2) Boca Chica Clean Marina Designation—which eliminates or significantly reduces the release of nutrients and contaminants; (3) stormwater quality improvements—which prevent or reduce the amount of nutrients, sediments, and contaminants; and (4) wastewater treatment—which reduces the release of nutrients and contaminants consistent with Florida Surface Water Quality Standards. Within these categories, there are 15 specific management activities and projects that provide benefit to the corals and their habitat (Table 4-2 of the INRMP). These types of best management practices have been ongoing at NASKW since 1983 and are likely to continue into the future. Further, the plan specifically provides assurances that all NASKW staff have the authority and funding (subject to appropriations) to implement the plan. The plan also provides assurances that the conservation efforts will be effective through annual reviews conducted by state and Federal natural resource agencies. These activities provide a benefit to the species and the identified essential feature in the critical habitat by reducing sediment and nutrient discharges into nearshore waters, which addresses some of the particular conservation and protection needs that critical habitat would afford. These activities are similar to those that we describe below as project modifications for avoiding or reducing adverse effects to critical habitat. Therefore, were we to consult on the activities in the INRMP that may affect critical habitat, we would likely not require any project modifications based on best management practices in the INRMP. Further, the INRMP includes provisions for monitoring and evaluating conservation effectiveness, which will ensure continued benefits to the species. Annual reviews of the INRMP for 2011-2015 found that the INRMP executions, including actions that minimize or eliminate land-based sources of pollution, “satisfied” or “more than satisfied” conservation objectives. Based on these considerations, we conclude the NASKW INRMP provides a conservation benefit to the threatened corals. Therefore, pursuant to section 4(a)(3)(B)(i) of the ESA, we determined that the INRMP provides a benefit to those threatened corals, and we are not designating critical habitat within the boundaries covered by the INRMP.

Application of ESA Section 4(b)(2)

Section 4(b)(2) of the ESA requires that we consider the economic impact, impact on national security, and any other relevant impact, of designating any particular area as critical habitat. Additionally, the Secretary has the discretion to consider excluding any particular are

[Text truncated at 120,000 characters. The full text is on the page linked above.]

---

Source: Frix Law Library, https://www.frixlaw.com/law-library/documents/fr%3A2023-16556. Public record. Not legal advice.