# Endangered and Threatened Species; Critical Habitat for the Threatened Indo-Pacific Corals

> Briefs, arguments, decisions, and more.

URL: https://www.frixlaw.com/law-library/documents/fr%3A2020-21226

## Record

- **Collection:** Federal Register
- **Document type:** Proposed Rule
- **Published:** November 27, 2020
- **Citation:** 85 FR 76262

## Text

DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
50 CFR Part 223 and 226
[Docket No: 200918-0249]
RIN 0648-BJ52
Endangered and Threatened Species; Critical Habitat for the Threatened Indo-Pacific Corals

AGENCY:

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

ACTION:

Proposed rule; request for comments.

SUMMARY:

We, the National Marine Fisheries Service (NMFS), propose to designate critical habitat for the seven threatened corals in U.S. waters in the Indo-Pacific (
Acropora globiceps, Acropora jacquelineae, Acropora retusa, Acropora speciosa, Euphyllia paradivisa, Isopora crateriformis,
and
Seriatopora aculeata
) pursuant to section 4 of the Endangered Species Act (ESA). Seventeen specific occupied areas containing physical features essential to the conservation of these coral species are being proposed for designation as critical habitat; these areas contain approximately 600 square kilometers (km
2
; 230 square miles) of marine habitat. We have considered positive and negative economic, national security, and other relevant impacts of the proposed designations, and we propose to exclude two areas from the critical habitat designations due to anticipated impacts on national security. We are soliciting comments from the public on all aspects of the proposal, including our identification of the geographical area and depths occupied by the species, the physical and biological feature essential to the coral species' conservation and identification, areas not included and excluded, and consideration of impacts of the proposed action.

DATES:

Comments on this proposal must be received by January 26, 2021.

Public hearings:
If requested, we will hold at least one public hearing on this proposed rule.

ADDRESSES:

You may submit comments, identified by the docket number NOAA-NMFS-2016-0131, by any of the following methods:

•
Electronic Submissions:
Submit all electronic public comments via the Federal eRulemaking Portal. Go to
www.regulations.gov/#!docketDetail;D=NOAA-NMFS-2016-0131
click the “Comment Now” icon, complete the required fields, and enter or attach your comments.

•
Mail:
Lance Smith, Protected Resources Division, NMFS, Pacific Islands Regional Office, NOAA Inouye Regional Center, 1845 Wasp Blvd., Bldg. 176, Honolulu, HI 96818.

Instructions:
You must submit comments by one of the previously described methods to ensure that we receive, document, and consider them. Comments sent by any other method, to any other address or individual, or received after the end of the comment period, may not be considered. All comments received are a part of the public record and will generally be posted to
http://www.regulations.gov
without change. All Personal Identifying Information (for example, name, address, etc.) voluntarily submitted by the commenter may be publicly accessible. Do not submit confidential business information or otherwise sensitive or protected information.

NMFS will accept anonymous comments (enter “N/A” in the required fields if you wish to remain anonymous).

FOR FURTHER INFORMATION CONTACT:

Lance Smith, NMFS, Pacific Islands Regional Office, 808-725-5131,
lance.smith@noaa.gov;
or, Celeste Stout, NMFS, Office of Protected Resources, 301-427-8436,
celeste.stout@noaa.gov.

SUPPLEMENTARY INFORMATION:

In accordance with section 4(b) of the ESA (16 U.S.C. 1533) and our implementing regulations (50 CFR 424.12), this proposed rule is based on the best scientific information available concerning the range, biology, habitat, threats to the habitat, and conservation objectives for the seven threatened corals in U.S. waters of the Indo-Pacific (
Acropora globiceps, A. jacquelineae, A. retusa, A. speciosa, Euphyllia paradivisa, Isopora crateriformis,
and
Seriatopora aculeata
). We reviewed the available information and have used it to identify physical and biological features essential to the conservation of each coral, the specific areas within the occupied areas that contain the essential physical and biological features that may require special management considerations or protections, the Federal activities that may impact the physical or biological features or areas, and the potential impacts of designating critical habitat for these seven Indo-Pacific corals. The economic, national security, and other relevant impacts of the proposed critical habitat designations for these coral species are described in the draft document titled, “Endangered Species Act Critical Habitat Information Report: Basis and Impact Considerations of Critical Habitat Designations for Threatened Indo-Pacific Corals,” hereafter referred to as the Draft Information Report (NMFS, 2019). This supporting document is available at
https://www.fisheries.noaa.gov/action/proposed-rule-designate-critical-habitat-threatened-indo-pacific-corals,
at
www.regulations.gov,
or upon request (see
FOR FURTHER INFORMATION CONTACT
).

Background

We listed 20 coral species as threatened under the ESA on September 10, 2014 (79 FR 53851). Although 15 of the listed species occur in the Indo-Pacific, only 7 of the listed coral species have been found in U.S. waters:
A. globiceps, A. jacquelineae, A. retusa, A. speciosa, E. paradivisa, I. crateriformis,
and
S. aculeata.
These seven species have been found in the U.S. jurisdictions of American Samoa, Guam, the Commonwealth of the Northern Mariana Islands (CNMI), and the Pacific Remote Island Area (PRIA). The final listing determinations were based on the best available information on a suite of demographic, spatial, and susceptibility components that influence the species' vulnerability to extinction in the face of continuing threats over the foreseeable future. All 20 listed species have undergone some level of population decline and are susceptible to multiple threats, including: Ocean warming, diseases, ocean acidification, ecological effects of fishing, and land-based sources of pollution. We found that aspects of the species' demography and distribution buffer the effects of these threats. Although we have no information that indicates that these species are currently in danger of extinction, we determined that they all are likely to become endangered throughout all of their ranges within the foreseeable future as a result of a combination of threats, the most severe of which are related to climate change. As such, we listed them as threatened. The following proposed rule is based on our Draft Information Report and peer review comments on the report. All of the information that we used to make our determinations in this proposed rule is contained in that report. The Draft Information Report is available at
https://www.fisheries.noaa.gov/action/proposed-rule-designate-critical-habitat-threatened-indo-pacific-corals,
at
www.regulations.gov,
or upon request (see
FOR FURTHER INFORMATION CONTACT
).

Natural History

This section summarizes life history and biological characteristics of Indo-

Pacific reef-building corals to provide context for the identification of the physical and biological feature essential for the conservation of these species. In this section, we cover several topic areas including an introduction to reef-building corals, as well as reproduction, settlement and growth, coral habitat types, and coral reef ecosystems. There is little species-specific information available on the life history, reproductive biology, and ecology for the seven corals that occur in U.S. waters of the Indo-Pacific, because many of the several hundred Indo-Pacific reef-building corals resemble one another, thus most investigations to date have been at the genus level. We provide specific information for each species where possible. In addition, we provide general information on the biology and ecology of the Indo-Pacific corals, highlighting traits that these seven corals share. The information below is largely summarized from the final listing rule (79 FR 53851; September 10, 2014), and it has been updated with the best available scientific information to date. The seven ESA-listed Indo-Pacific corals are reef-building corals. 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 in high-growth conditions, but they also occur in non-reef habitats. That is, they are reef-building, but not reef-dependent. About 90 percent of the world's approximately 800 reef-building coral species occur in the Indo-Pacific (Veron, 2000). These unique animals contain symbiotic algae within their cells, they produce clones of themselves by different means, and most of them occur as colonies of polyps. 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 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) living within the host coral's tissues. Zooxanthellae belong to the dinoflagellate genus
Symbiodinium
and provide nutrition to the host coral by translocating fixed organic carbon and other nutrients. In return, they receive inorganic waste metabolites from host respiration as well as protection from grazing. This exchange of nutrients allows both partners 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 do not contain zooxanthellae, and these species form much smaller skeletons, and therefore are not considered reef-building. The seven ESA-listed Indo-Pacific corals discussed in this proposed rule are zooxanthellate species, and thus are reef-building, because they contain symbiotic algae in their cells, enabling them to grow large skeletons that contribute to the physical structure of coral reefs.

Coral polyps can occur as free-living, solitary polyps (
e.g.,
fungiids) or as colonies of polyps, depending on the species. Most reef-building coral species are colonial, producing colonies made up of dozens to thousands of polyps that are connected seamlessly 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, otherwise known as clones). Each polyp consists of a column with mouth and tentacles on the upper side growing on top of a calcium carbonate skeleton, which the polyps produce through the process of calcification. 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 seven listed Indo-Pacific corals are all colonial species, although polyp size, colony size, and colony morphology vary considerably by species and also based on environmental variables in different habitats. Colonies themselves can produce clones, most commonly through fragmentation or budding (described in more detail below). Clones can also be produced in some species by asexual larvae or polyp bail-out (a rare case when an individual polyp breaks away from the colony due to poor environmental conditions and re-settles elsewhere). The seven listed Indo-Pacific corals are all clonal species, both as colonies of cloned polyps, and with the ability to produce clones of individual 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; Brainard
et al.,
2011).

Corals use a number of diverse reproductive strategies that have been researched extensively; however, many individual species' reproductive modes remain poorly described. Most coral species use both sexual and asexual propagation. Sexual reproduction in corals is primarily through gametogenesis (
i.e.,
development of eggs and sperm within the polyps). Some coral species have separate sexes (gonochoric), while others are hermaphroditic. Strategies for fertilization are either by brooding (internal fertilization) or broadcast spawning (external fertilization). Asexual reproduction in coral species most commonly involves fragmentation, by which colony pieces or fragments are dislodged from larger colonies and establish new colonies, although the budding of new polyps within a colony can also be considered asexual reproduction. In many species of branching corals, fragmentation is a common and sometimes dominant means of propagation (79 FR 53852, September 10, 2014).

Of the seven listed Indo-Pacific species,
A. retusa, A. globiceps,
and
A. jacquelineae
are all hermaphroditic spawners. The reproductive characteristics of
A. speciosa
have not yet been determined, but most other
Acropora
species are also hermaphroditic spawners.
Euphyllia paradivisa'
s reproductive mode is unknown and other
Euphyllia
species exhibit a variety of reproductive characteristics, so it is unclear which is most probable for the species. The reproductive characteristics of
I. crateriformis
and
S. aculeata
have also not been determined, but other similar species of both
Isopora
and
Seriatopora
are simultaneous hermaphroditic brooders. As for skeletal growth, there is no species-specific information available, but branching
Acropora
species such as the four listed
Acropora
species are typically relatively fast-growing (Brainard
et al.,
2011).

Coral larvae presumably experience considerable mortality from predation or other factors prior to settlement and metamorphosis. 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. Little is known concerning the settlement patterns of planulae (free-swimming larvae) of the listed Indo-Pacific corals. In general, upon proper

stimulation, coral larvae, whether released from parental colonies or developed in the water column external to the parental colonies (like
Acropora
spp.), settle and metamorphose on appropriate substrates. Biological and physical factors that have been shown to affect spatial and temporal patterns of coral recruitment include 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. Like most corals, the listed Indo-Pacific corals require hard, consolidated substrate, including attached, dead coral skeleton, for their larvae to settle. Algal growth limits the amount of hard substrate available to coral settlement, and a low nutrient environment is less conducive to algal growth. Once larvae are able to settle onto appropriate hard substrate, metabolic energy is diverted to colony growth and maintenance.

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.,
massive
Porites
species). The energy required to produce new polyps and build calcium carbonate skeleton is provided by the symbiotic relationship corals have with photosynthetic zooxanthellae. The zooxanthellae require light to photosynthesize, thus lower water clarity (
i.e.,
poor transparency) reduces the host coral's energy, growth and survival by limiting the amount of light that penetrates the water. Lower water clarity sharply reduces photosynthesis in zooxanthellae with moderate reductions in adult colony survival and calcification. The skeletons of coral colonies are bound together by cementation, resulting in the formation of coral reefs. Species with high recruitment rates or fast growth rates may have the ability to recover more quickly from disturbances. Additionally, long-lived species with large colony size can sustain partial mortality (fission) and still have the potential for persistence and regrowth (79 FR 53852, September 10, 2014). Additional information on the biological requirements for reproduction, settlement, and growth is provided below in the
Physical and Biological Features Essential for Conservation
section.

Shallow 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. The three broad categories of coral reefs are fringing reefs, barrier reefs, and atolls. Fringing reefs are mostly close to coastlines, and usually have a high component of non-carbonate sediment. Barrier reefs are offshore and are composed of wave-resistant consolidated limestone. Atolls are usually a wall of reefs partially or completely enclosing a central lagoon. There are not sharp differences that clearly mark boundaries between reef types. For example, fringing reefs gradually become barrier reefs with increasing distance from shore. Also, the shape of both barrier reefs and atolls is largely determined by the bathymetry of the substratum, producing many irregularly shaped reefs that are intermediary between the two types. Isolated reefs that do not fit any of these descriptions are referred to as platform reefs. 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 coral reef habitat vary greatly by reef categories, locations, latitudes, frequency of disturbance, etc
.,
and there is also much 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 across the Indo-Pacific, as described in more detail in the final listing rule (79 FR 53852; September 10, 2014).

As described previously, reef-building corals are not dependent on coral reefs, and many of these species can thrive in low-growth conditions where skeletal growth is inadequate to result in accretion of coral reefs. “Non-reef habitat” refers to hard substrates where reef-building corals can grow, including marginal habitats where conditions prevent reef development (
e.g.,
turbid or high-latitude or upwelling-influenced areas) and recently available habitat (
e.g.,
lava flows). All the listed species can occur in both shallow coral reef and non-reef habitats, provided that hard substrate and suitable water quality are present. The term “mesophotic habitat” refers to hard substrates deeper than 30 m. Shallow coral reefs, non-reef habitats, and mesophotic habitats are not necessarily sharply delineated from one another, thus one may gradually blend into another. The total area of non-reef and mesophotic habitats is likely greater than the total area of shallow coral reef habitats within the ranges of the listed corals (79 FR 53852; September 10, 2014). Despite the large amount of variability in habitats occupied by corals, they have several characteristics in common that provide the fundamental support necessary for coral settlement and growth, including hard substrate and low-nutrient, clear water with good light penetration.

The seven listed Indo-Pacific species within U.S. waters vary in their recorded depth ranges and habitat types.
Acropora globiceps
occurs on upper reef slopes, reef flats, and adjacent habitats. In the final listing rule, the best available information indicated this species occurs in depths ranging from 0 to 8 meters (m). However, in 2015, we learned that
A. globiceps
has been observed in American Samoa at 11 m (Asili, Tutuila) and 18 m in the National Park of American Samoa on the north side of Tutuila (D. Fenner, pers. comm., 2015). Based on the new information, we consider the rangewide depth distributions of
A. globiceps
to be 0 to 20 m.
Acropora jacquelineae
is found in numerous subtidal reef slope and back-reef habitats, including but not limited to, lower reef slopes, walls and ledges, mid-slopes, and upper reef slopes protected from wave action, and its depth range is 10 to 35 m (D. Fenner, pers. comm. 2015).
Acropora retusa
occurs in shallow reef slope and back-reef areas, such as upper reef slopes, reef flats, and shallow lagoons. In the final listing rule, the best available information indicated its depth range to be 0 to 5 m. In 2015, we learned that
A. retusa
has been observed in American Samoa at 10 m near Asili on Tutuila Island (D. Fenner, pers. comm. 2015). Based on the previously described new information combined with the fact that it's almost always found in shallower waters, we consider the rangewide depth distribution of
A. retusa
to be 0 to 10 m in this rule.
Acropora speciosa
occurs on lower reef slopes and walls, especially those characterized by clear water and high
Acropora
diversity, in a depth range of 12 to 40 m (Veron, 2014).
Euphyllia paradivisa
is found in environments protected from wave action on at least upper reef slopes, mid-

slope terraces, and lagoons at a depth range of 2 to 25 m (Veron, 2014).
Isopora crateriformis'
s predominant habitat is shallow, high-wave energy environments, including reef flats and reef crests, and it also occurs in adjacent habitats such as upper reef slopes. It has a depth distribution of 0 to 12 m, and has been reported as common at 5 to 10 m (D. Fenner, pers. comm. 2015).
Seriatopora aculeata
occurs in a broad range of habitats on the reef slope and back reef, including but not limited to upper reef slopes, mid-slope terraces, lower reef slopes, reef flats, and lagoons in a depth range of 3 to 40 m (Veron, 2014).

In summary, based on the best currently available information, we consider the rangewide depth distributions of the seven listed species as follows:
A. globiceps,
0 to 20 m;
A. jacquelineae,
10 to 35 m;
A. retusa,
0 to 10 m;
A. speciosa,
12 to 40 m;
E. paradivisa,
2 to 25 m;
I. crateriformis,
0 to 12 m; and
S. aculeata,
3 to 40 m (Table 1).

Table 1—Confirmed Geographic and Depth Distributions of Threatened Indo-Pacific Corals in the U.S.

Jurisdiction

Unit
1

Am Samoa
1
2
3
4
Mariana Islands (Guam and CNMI)
5
6
7
8
9
10
11
12
13
Pacific Remote Island Area
14
15
16
17
18
19

A. globiceps
, (0-20 m)

X
X
X
X
X
X
X
X
X
X
X
X
X

X
X

X

A. jacquelineae
, (10-35 m)

X

A. retusa
, (0-10 m)

X
X
X
X
X

X

X

X
X
X
X

A. speciosa
, (12-40 m)

X

X

E. paradivisa
, (2-40 m)

X

I. crateriformis
, (0-12 m)

X
X
X

S. aculeata
, (3-40 m)

X

X

Depths of all listed spp.
2

a
b
b
b
a
b
b
b
a
b
b
b
b
c
B
a
c
b
c

1

Unit Key:
(1) Tutuila & Offshore Banks; (2) Ofu & Olosega; (3) Ta'u; (4) Rose Atoll; (5) Guam & Offshore Banks; (6) Rota; (7) Aguijian; (8) Tinian and Tatsumi Reef; (9) Saipan and Garapan Bank; (10) Farallon de Medinilla; (11) Anatahan; (12) Pagan; (13) Maug Islands & Supply Reef; (14) Howland Island; (15) Palmyra Atoll; (16) Kingman Reef; (17) Johnston Atoll; (18) Wake Atoll; and (19) Jarvis Island.

2

Depth Key:
(a) 0-40 m; (b) 0-20 m; (c) 0-10 m.

Species identification of many Indo-Pacific reef-building corals is challenging, even for experts who have worked in the field for decades. There are a multitude of reasons for this, including: Poor quality type specimens; lack of samples to verify photos; inter-specific and intra-specific morphological plasticity and variability; inherent human subjectivity; and unreliable published information. For the seven listed species considered here, current species identification uncertainty is rated as moderate or high for six species (all but
E. paradivisa
). In addition, because traditional coral identification is based on colony morphological characteristics, and recent genetics results often contradict morphological identifications, species identification uncertainty is predicted to increase for most of these species (Fenner, 2015).

Critical Habitat Identification and Designation

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 a significant regulatory protection by ensuring that the Federal government considers the effects of its actions in accordance with section 7(a)(2) of the ESA and avoids or modifies 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 on private land that do not involve a Federal agency.

Section 3(5)(A) of 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 of the species (16 U.S.C. 1532(5)(A)). Conservation is defined in section 3 of the ESA as 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 chapter are no longer necessary (16 U.S.C. 1532(3)). Therefore, critical habitat is the habitat essential for the species' recovery. 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.

To identify and designate critical habitat, we considered information on the distribution of the seven threatened Indo-Pacific corals, their major life stages, habitat requirements of those life stages, threats to the species, and conservation objectives that can be supported by identifiable essential physical or biological features (hereafter also referred to as “PBFs” or “essential features”). In the final listing rule, ocean warming, diseases, ocean acidification, trophic effects of reef fishing, nutrient enrichment, sedimentation, and inadequacy of regulatory mechanisms were found to be the main threats contributing to the threatened status of all seven corals. Several other threats also contributed to the species' statuses, but were considered to be relatively lower in importance as compared to the main threats. Therefore, we evaluated physical and biological features of their habitats to determine what features are essential to the conservation of each coral.

Accordingly, 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 interpreted to mean the entire range of the species at the time it was listed, inclusive of all areas they use and move through seasonally (81 FR 7413; February 11, 2016). 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)). As noted previously, seven of the listed species have been confirmed within U.S. Pacific Islands waters (Table 1), and only these seven are currently being considered for critical habitat designation. We first identified the U.S. jurisdictional areas where observations of listed coral species have been confirmed. In summary, six listed species are confirmed in American Samoa (
A. globiceps, A. jacquelineae, A. speciosa, A. retusa, I. crateriformis,
and
E. paradivisa
); three listed species are confirmed in Guam and CNMI (
A. globiceps, A. retusa,
and
S. aculeata
); and three listed species are confirmed in PRIA (
A. globiceps, A. retusa,
and
A. speciosa
). We further broke down the areas under consideration for critical habitat designation into 19 units based on information on the confirmed locations of each species within these jurisdictions, in order to better describe the geographic areas occupied by each species. The units generally consist of individual islands or atolls and nearby shoals or banks. Table 1 shows the distributions of the seven listed species by both jurisdiction and critical habitat unit. The proposed units are shown in the figures at the end of this rule. More detailed information on the distributions of the seven listed species in these units is provided in the Draft Information Report (NMFS, 2019).

Physical or Biological Features Essential for 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 occur in specific areas and that are essential to support the life-history needs of the species, including 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).

In the final listing rule, we determined that the seven corals were threatened under the ESA. This means that while the species are not in danger of extinction currently, they are likely to become so within the next several decades based on their current abundances and trends in abundance, distributions, and threats they experience now and in the future. The goal of an ESA listing is to first prevent extinction, and then to recover the species so they no longer meet the definition of a threatened species and no longer need the protections of the ESA. 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 15 Indo-Pacific corals listed in 2014, including the 7 species covered by this critical habitat rule: Populations of the 15 listed Indo-Pacific corals should be present throughout as much of their historical ranges as future environmental changes will allow, and may expand their ranges into new locations with more favorable habitat conditions in the future (
https://www.fisheries.noaa.gov/resource/document/15-indo-pacific-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 seven 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 it was 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 seven corals' habitat that are impeding their recovery. Protecting essential features of the corals' habitat from these threats will facilitate the Recovery Vision.

We then turned to determining the physical or biological features essential to this conservation objective of supporting successful reproduction and recruitment, and survival and growth of all life stages. Specifically, we evaluated whether particular habitat features will facilitate recovery through enhancing population growth. 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 the conservation objective 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. Due to corals being 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. A detailed discussion of how this feature was determined will follow. 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 seven 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 identify the following physical feature essential to the conservation of the seven corals. Our proposed definition for the essential feature is:

Reproductive, recruitment, growth, and maturation habitat.
Sites that support the normal function of all life stages of the corals 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.

As described in detail in the Draft Information Report (NMFS, 2019), all corals require exposed natural consolidated hard substrate for the settlement and recruitment of larvae or asexual fragments. Substrate provides the physical surface and space necessary for settlement of coral larvae, a stable environment for metamorphosis of the larvae into the primary polyp, growth of juvenile and adult colonies, and re-attachment of fragments. Larvae can settle and attach to dead coral skeleton (Brainard
et al.,
2011). A number of attributes have been shown to influence coral larval settlement. Positive cues include the presence of crustose coralline algae (Heyward and Negri, 1999), biofilms (Webster
et al.,
2004), and cryptic habitat such as crevices and holes (Nozawa, 2008). Attributes that negatively affect settlement include presence of sediment and algae (Vermeij
et al.,
2009). Coral recruitment tends to be greater when macroalgal biomass is low (Birrell
et al.,
2005). In addition to preempting space for coral larvae settlement, many fleshy macroalgae produce substances that may inhibit larval settlement, recruitment, and survival (Jompa and McCook, 2003). Furthermore, algal turfs can trap sediments (Purcell and Bellwood, 2001), which then create the potential for algal turfs and sediments to act in combination to hinder coral settlement (Birrell
et al.,
2005).

Presence and amount of sediment is a particularly important determinant of the quality of substrate for reef-building coral habitat. Sediments enter the reef environment through many processes that are natural or anthropogenic in origin, including erosion of the coastline, resuspension of bottom sediments, terrestrial run-off, and nearshore dredging for coastal construction projects and navigation purposes. The rate of sedimentation affects reef distribution, community structure, growth rates, and coral recruitment (Dutra
et al.,
2006). 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). Sediment impedes settlement of coral larvae (Babcock and Smith, 2002). The deeper the sediment, the longer it may take for natural waves and currents to remove the sediment from the settlement substrate. Sediment texture 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). Accumulation of sediment can smother living corals, cover dead coral skeleton, and exposed hard substrate (Erftemeijer
et al.,
2012; Fabricius, 2005). Sedimentation, therefore, impacts the health and survivorship of all life stages of corals (
i.e.,
adults, fragments, larvae, and recruits).

The literature provides several recommendations on maximum sediment levels 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 sediment levels on the Great Barrier Reef (GBR) be less than a mean annual sedimentation rate of 3 mg/cm
2
/day, and less than a daily maximum of 15 mg/cm
2
/day. Rogers (1990) recommends that sediment levels 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) suggests that moderate to severe effects to corals are expected at mean maximum sediment levels of >10 mg/cm
2
/day, and catastrophic effects at >50 mg/cm
2
/day. Nelson
et al.
(2016) suggests 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 previously described 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.

Finally, 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 typically man-made 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 substrates. Our definition of recruitment substrate 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 within the Geographical Areas Occupied by the Species
section of this proposed 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 exist 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 Draft 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. This 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, and consequently ocean warming is one of the most important threats to reef-building corals. Corals occur in a 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 narrow range (typically 25°C-29°C) as indicated by the global distribution of coral reefs (Brainard
et al.,
2011; Kleypas
et al.,
1999). Short-term exposures (days) to temperature increases of a few degrees (
i.e.,
3°C-4°C increase above mean maximum summer temperature) or long-term exposures (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). In addition to coral bleaching, elevated seawater temperatures impair coral fertilization and settlement (Nozawa and Harrison, 2007) and cause increases in coral disease (Miller
et al.,
2009).

Effects of elevated seawater temperatures are well-studied for reef-building corals, and many approaches have been used to estimate temperature thresholds for coral bleaching and mortality (see reviews by Brown, 1997; Berkelmans, 2002; Coles and Brown, 2003; Jokiel, 2004; Baker
et al.,
2007; Jones, 2008; Coles and Riegl, 2013). The tolerance of corals to temperature is species-specific (van Woesik
et al.,
2011; Vega-Rodriguez, 2016) and depends on suites of other variables that include acclimation temperature, aragonite saturation state, dissolved inorganic nitrogen (Cunning and Baker, 2012; Fabricius, 2005; Wooldridge, 2013); and physical, physiological, and chemical stressors, including suspended sediments and turbidity (Anthony
et al.,
2007; Woods
et al.,
2016); trace metals such as copper (Negri and Hoogenboom, 2011; Woods
et al.,
2016); ultraviolet radiation (Anthony
et al.,
2007); and salinity, nitrates, and phosphates (Negri and Hoogenboom, 2011).

Ocean warming is one of the most significant threats to the seven ESA-listed Indo-Pacific corals. Mean seawater temperatures in reef-building coral habitat in the 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). Even so, evaluating the effects that changes in water temperatures have on the conservation value of coral habitat is very complex and contextually-driven, and simple numeric effect thresholds are not easily assigned to listed corals to establish when stress responses occur. 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). Corals can withstand mild to moderate bleaching; however, severe, repeated, or prolonged bleaching can lead to colony death (Brown, 1997). In addition to coral bleaching, other effects of ocean warming detrimentally affect virtually every life-history stage in reef-building corals. Impaired fertilization and developmental abnormalities (Negri and Heyward, 2000), mortality, and impaired settlement success (Nozawa and Harrison, 2007) 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 (Jones
et al.,
2004; Miller
et al.,
2009). Outbreaks also follow seasonal patterns of high seawater temperatures (Willis
et al.,
2004).

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. GBRMPA (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). NOAA's Coral Reef Watch Program utilizes the Degree Heating Week method (Glynn and D'Croz, 1990; Eakin
et al.
2009), which defines a general bleaching threshold for reef-building corals as seawater temperatures of 1°C above maximum monthly mean at a given location for four 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 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. For corals, the mineral form

of calcium carbonate in their skeletons is called “aragonite.” The more carbonate ions there are 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, 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 less than this. 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. These general characterizations and thresholds were identified for coral reef communities and ecosystems, rather than individual species.

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. Ocean acidification is one of the most significant threats to reef-building corals (Brainard
et al.,
2011; Jokiel, 2015).

A variety of laboratory studies conducted on corals and coral reef organisms (
e.g.,
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). 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, acclimatization to localized nutrient regimes, and other factors.

Nitrogen and phosphorous are two of the main nutrients that affect the suitability of coral habitat (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 (PO4
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. Nutrients are a major component of land-based sources of pollution (LBSP), one of the most important threats to reef-building corals (Brainard
et al.,
2011). Excessive nutrients affect corals through two main mechanisms: direct impacts 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 large increase in a nutrient may result in a severe adverse response, just as a chronic, lower concentration might.

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
, above which NO
3
and PO
4
are excessive (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
et al.,
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 and Fabricius, 2007). Thus, 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 previously, 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, and 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), 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 total suspended solids (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 (especially 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/m2) of 450 μmol photons second/m2 globally for coral reefs. The previously described 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 intensity and duration. 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). Turbidity reduces water clarity and so 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, and 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). 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). Toxicity of copper 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 effects of oil pollution on corals include growth impairments, mucus production, and decreased reproduction, especially at increased temperature (Kegler
et al.,
2015). Hydrocarbons have also been found to affect early life stages of corals. Oil-contaminated seawater reduced settlement of
Orbicella faveolata
and of
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). Oil, dispersant, and a combination of oil and dispersant on significantly decreased settlement and survival of
Porites astreoides
and
O. faveolata
larvae (Goodbody-Gringley
et al.,
2013).

Anthracene (a PAH used in dyes, wood preservatives, insecticides, and coating materials) exposure to apparently healthy and diseased (Caribbean yellow band disease) fragments 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 the exposure to PAHs such as anthracene than apparently 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” 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 isolated zooxanthellae (Shaw
et al.,
2012b). 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. However, reduced larval survivorship was not detected in exposure of up to 6.0 µg/L of permethrin. 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.,
shampoo, body lotions, soap, detergents), product coatings (oil-based paints, polyurethanes), acrylic adhesives, and plastics that protects against damage from ultraviolet light. It is released into the ocean through municipal and boat/ship wastewater discharges, landfill leachates, residential septic fields, and unmanaged cesspits. BP-2 is a known endocrine disruptor and a DNA mutagen, and its effects are worse in the light. It caused deformation of
Stylophora pistillata
larvae changing them from a motile planktonic state to a deformed sessile condition at low concentrations. 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 ultraviolet 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. Exposure to oxybenzone transformed
S. pistillata
larvae from a motile state to a deformed, sessile condition. 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 pollutants 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 web. A study of the effects of the PCB Aroclor 1254 on the scleractinian coral
S. 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 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 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. The combined effects of LAS exposure with increased temperature (+3°C 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 previously, 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 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 previously 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 previous summaries constitute the best available information at the time of this rulemaking. It is possible that future scientific research will identify species-specific values for some of these parameters that become more applicable to the seven listed coral species, though it is also possible that future species-specific research will document that conducive or tolerance ranges for the seven 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.

Need for 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).

The proposed essential feature is particularly susceptible to impacts from human activity because of the relatively shallow water depth ranges of the seven listed corals (less than 40 m). The proximity of this habitat to coastal areas subject 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 pollutant discharges, and fishery management. Further, the global oceans are being impacted by climate change from greenhouse gas emissions, particularly the tropical oceans in which the Indo-Pacific 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, allowing them to preempt 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 Features Within the Geographical Areas Occupied by the Species

Our regulations state that each critical habitat area will be shown on a map, with more-detailed information discussed in the preamble of the rulemaking documents published in the
Federal Register
defined by specific limits using reference points and lines on standard topographic maps of the area, and referencing 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)).

We identified 19 units within the geographical area occupied by the seven listed Indo-Pacific species confirmed in U.S. waters, at the time of listing, that contain the essential feature (Table 1): Four in American Samoa (Tutuila and Offshore Banks, Ofu and Olosega, Ta'u, and Rose Atoll); one in Guam (Guam and Offshore Banks); eight in CNMI (Rota, Aguijian, Tinian and Tatsumi Reef, Saipan and Garapan Bank, Farallon de Medinilla, Anatahan, Pagan, and Maug Islands and Supply Reef); and six in PRIA (Howland Island, Palmyra Atoll, Kingman Reef, Johnston Atoll, Wake Atoll, and Jarvis Island).

Within each of these 19 units, we delineated more specific areas that contain the essential feature using a 3-step process: (1) We reviewed available information on substrate and water quality parameters to determine where the essential feature occurs; (2) we established upper and lower depth limits for these areas depending on the species present; and (3) within the depth limits, we identified areas that may have the essential feature but are not necessary for the conservation of the listed species because they are artificial substrates or natural substrates that are consistently disturbed, and therefore do not qualify as critical habitat.

For step 1, determining specific areas that contain the essential feature, we reviewed available substrate and water quality data for each unit. For substrate, we used data and maps from two benthic habitat mapping programs that collect benthic data for coral reef ecosystems throughout the United States (these programs are also available to the public on their websites): (1) For habitat <20 m depth, the National Centers for Coastal Ocean Science's (NCCOS;
https://coastalscience.noaa.gov/
) provides data and maps (except for some of the PRIA); and (2) for habitat >20 m depth, the Pacific Islands Benthic Habitat Mapping Center (PIBHMC;
https://www.soest.hawaii.edu/pibhmc/cms/
) provides data and maps. These two complementary programs provide nearly complete, large-scale coverage of reef-building coral substrate in the U.S. Pacific Islands, except for some of the PRIA areas which are not included in the NCCOS database. For substrate and water quality information, we also used coral reef monitoring and status reports from the Pacific Islands Fisheries Science Center (PIFSC,
https://www.fisheries.noaa.gov/region/pacific-islands#science
) for the Mariana Islands (Brainard
et al.,
2012; except for Farallon de Medinilla (FDM)) and American Samoa (Brainard
et al.,
2008). For the PRIA, we used Miller
et al.
(2008). In contrast to substrate, data for water quality parameters are limited to a few of the parameters over a small overall portion of reef-building coral habitat within the area under consideration for critical habitat.

We applied step 2, establishing upper and lower depth limits for these areas, by using depth distribution information for the listed coral species that occur in each unit to delineate upper and lower depth limits for each unit. Because at least some, if not all, listed corals in each unit occur in shallow habitats (
e.g.,
reef flats), the upper depth limit for all units is mean low water, referred to here as zero (0) m depth. The lower depth limit for each unit is based on the deepest observed record of any listed species in that unit. As previously described in more detail in the Background section, based on the best currently available information, we consider the rangewide depth distributions of the seven listed species as follows:
A. globiceps,
0 to 20 m;
A. jacquelineae,
10 to 35 m;
A. retusa,
0 to 10 m;
A. speciosa,
12 to 40 m;
E. paradivisa,
2 to 25;
I. crateriformis,
0 to 12 m; and
S. aculeata,
3 to 40 m. We used depth distributions for all listed Indo-Pacific species within U.S. waters combined as a comprehensive approach to establish a lower limit because most listed species have overlapping depth distributions, and depth distributions of these species are still not well known for many of the critical habitat units.

We next applied step 3 for each unit by identifying areas that may contain the essential feature, but are not necessary for the conservation of the listed species. There are two types of areas that may contain hard consolidated substrate and suitable water quality parameters, but are not considered necessary for the conservation of the species, and none, one, or both may occur in each unit: (1) artificial substrates; and (2) “managed areas.” Artificial substrates include any human-made structure, regardless of age or level of active management. Examples include, but are not limited to, fixed and floating structures, such as: Jetties, groins, breakwaters, fixed or floating AToNs, seawalls, wharves, boat ramps, fishpond walls, pipes, wrecks, mooring balls, docks, aquaculture cages, and other artificial substrates. Managed areas are areas where the substrate has been disturbed by management and will continue to be periodically disturbed by such management. Examples include, but are not limited to, dredged navigation channels, shipping basins, vessel berths, and AToN chain scour areas around anchor blocks. As noted previously, protecting artificial substrates and managed areas would not facilitate meeting our conservation goal of maintaining functional natural reef ecosystems on which the listed species depend. They do not provide stable natural environments for coral growth and settlement and therefore are not necessary for the conservation of the species.

NMFS is aware that dredging may result in sedimentation impacts beyond the actual dredge channel. To the extent that these impacts are persistent, are 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, then NMFS expects that the federal action agency can assess and identify such areas during their pre-dredging planning and provide their rationale and information supporting this conclusion. To the extent that the federal action agency does so, NMFS proposes that these persistently impacted areas be considered part of the managed areas and excluded from critical habitat.

The application of the 3-step process to each of the 19 specific areas is described in more detail in the Draft Information Report. The resulting delineations of the specific areas are described in Appendix A of the report, and 17 of the 19 are described and shown in the maps at the end of this rule. The entireties of the other two specific areas (Wake and FDM) were determined to be ineligible by the 4(a)(3) analyses summarized below, and described and shown in the Draft Information Report (NMFS, 2019). These are the 19 specific areas to which the ESA section 4(a)(3) and 4(b)(2) analyses were applied. The essential feature is unevenly distributed throughout these 19 specific areas. Within these areas there exists a mosaic of habitats at relatively small spatial scales, some of which naturally contain the essential feature and some that do not. Further, within these large areas, specific managed areas as described previously also exist. If a location within one of these areas does not meet the definition of critical habitat (such as an area of soft substrate or a continuously managed area), it is not included in the designations. Due to the spatial scale at which the essential feature exists interspersed with these other habitats and disturbed areas, and the fact that the precise locations of the essential feature change over time (
e.g.,
seasonally, in response to storms, etc.), we are not able to more finely delineate the essential feature.

Unoccupied Critical Habitat Areas

We have not identified any unoccupied areas for designation of critical habitat. 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. Regulations at 50 CFR 424.12(b)(2) specify that we will identify, at a scale determined to be appropriate, specific areas outside the geographical area occupied by the species that are essential for its conservation, considering the life history, status, and conservation needs of the species based on the best available scientific data.

The threats to these seven corals include ocean warming, ocean acidification, and other threats that are primarily caused by global climate change (Brainard
et al.,
2011). We issued guidance in June 2016 on the treatment of climate change uncertainty in ESA decisions, which addresses critical habitat specifically (NMFS 2016). The guidance states that, when designating critical habitat, NMFS will consider proactive designation of unoccupied habitat as critical habitat when there is 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.

All seven of these species occur in the Coral Triangle, an area predicted to have rapid and severe impacts from climate change. As a response to changing conditions, these species may shift into previously unoccupied habitats as they become more suitable and as other parts of their range become less suitable in the future. However, the best information available currently does not support a reasonable inference that listed Indo-Pacific corals may expand into unoccupied areas within U.S. waters in the future due to changing climate conditions. In addition, coral reef areas within U.S. jurisdiction provide no more than about 2 percent of each listed species' total range. Without further information, we cannot support the notion that such a small area of unoccupied habitat at the range margin is essential to the conservation of the species.

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 Department of Defense (DoD), or designated for its use, that are subject to an Integrated Natural Resources Management Plan (INRMP) prepared under section 101 of the Sikes Act (16 U.S.C. 670a), if the Secretary of Commerce determines in writing that such plan provides a benefit to the species for which critical habitat is proposed for designation.

Two INRMPs are applicable to proposed coral critical habitat: (1) The Navy's Joint Region Marianas INRMP (JRM INRMP), finalized and signed in 2019 (DoN, 2019); and (2) the Air Force's INRMP for Wake Island Air Field, Wake Atoll, Kokee Air Force Station, Kauai, Hawaii, and Mt. Kaala Air Force Station, Oahu, Hawaii (Wake INRMP), finalized and signed in 2017 (USAF, 2017). The JRM INRMP is a composite of management plans for many distinct DoD controlled areas in the Mariana Islands, including in Guam and CNMI (DoN, 2019).

Summaries of the analyses of whether these two INRMPs are likely to benefit the ESA-listed corals or their habitat in Guam and CNMI (JRM INRMP) and Wake (Wake INRMP) are provided below, following the four considerations outlined in the 2016 guidance for the 4(a)(3) and 4(b)(2) portions of critical habitat designations (81 FR 7413; February 11, 2016). These four considerations are: (1) The extent of the area and essential feature present in the area; (2) The type and frequency of use of the area by the listed 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 (essential feature) from the types of effects that would be addressed through a destruction-or-adverse- modification analysis.

JRM INRMP—Guam

In Guam, the JRM INRMP encompasses three marine areas that overlap with areas proposed for coral critical habitat (hereafter “INRMP marine areas”): (1) Naval Base Guam—Main Base (NBG Main Base) Submerged Lands; (2) Naval Base Guam—Telecommunications Site (NBG TS) Submerged Lands; and (3) Andersen Air Force Base (AAFB) Submerged Lands. A summary of the analyses of whether the INRMP is likely to benefit the habitat of ESA-listed corals in each of these three INRMP marine areas is provided below, summarized from the full analyses in the Draft Information Report (NMFS, 2019).

With regard to the extent of the area and essential feature present: (1) The NBG Main Base Submerged Lands cover approximately 30,000 acres along the coastline from Orote Peninsula to Asan (described in the JRM INRMP, Section 5.3, DoN, 2019); (2) the NBG TS Submerged Lands cover approximately 19,500 acres on the northwestern side of Guam (described in the JRM INRMP, Section 8.3, DoN, 2019); and (3) AAFB Submerged Lands cover approximately 26,500 acres of Submerged Lands on the northern side of Guam (described in the JRM INRMP, Section 9.3, DoN, 2019). Each of the three INRMP marine areas includes extensive potential proposed critical habitat, as shown in Fig. 21 in the Draft Information Report (NMFS, 2019). Most or all of the potential proposed critical habitat within the three INRMP marine areas includes both the substrate and water quality components of the essential feature of coral critical habitat (
i.e.,
characteristics of substrate and water quality support coral life history, including reproduction, recruitment, growth, and maturation), based on information provided previously in the Guam section of the Draft Information Report (NMFS, 2019), the Guam chapter of PIFSC's coral reef monitoring report for the Mariana archipelago (Brainard
et al.,
2012), and the INRMP (DoN, 2019).

With regard to use of the area by the listed species, the listed coral
Acropora globiceps
occurs within each of the three INRMP marine areas. Two other listed coral species,
Acropora retusa
and
Seriatopora aculeata,
have been recorded on Guam at one or two sites, and thus may also occur in one or more of the three INRMP marine areas (DoN, 2019).

With regard to the relevant elements of the INRMP, and certainty that the relevant elements will be implemented, the two parts of this step are addressed separately below. The relevant elements of the JRM INRMP for each INRMP marine area include: (1) For the NBG Main Base Submerged Lands, the INRMP includes a Coral Habitat Enhancement plan (Section 5.4.2.1), consisting of eight specific actions in three categories: (1) Monitoring and adaptive management (3 actions), (2) collaboration with local partners (3 actions), and (3) reduction of vessel impacts (2 actions); (2) for NBG TS Submerged Lands, the INRMP includes a Coral Habitat Enhancement plan (Section 8.4.2.1), consisting of a similar set of eight specific actions as for NBG Main Base; and (3) for AAFB Submerged Lands, the INRMP includes a Coral Habitat Enhancement plan (Section 9.4.2.1), consisting of a similar set of seven specific actions as for NBG Main Base, except that there is less focus on

reduction in vessel impacts because of the much lower vessel traffic there.

NMFS concludes that the Navy will implement the relevant elements of the JRM INRMP for the previously described three INRMP marine areas for three reasons:

(1) Clear and Recent Documentation—the 2019 JRM INRMP includes Coral Habitat Enhancement plans for INRMP marine areas in Guam, with clear strategies and actions that address the habitat conservation needs of ESA-listed corals within these areas. The JRM INRMP's Appendix D also includes annual reports describing how coral conservation efforts have been implemented in recent years. These new coral habitat conservation plans, as well as reports from recent years, clearly articulate how Navy is conserving coral habitat within the INRMP marine areas in Guam, and how it will do so in the future.

(2) Demonstration of Good Faith Efforts for Listed Corals—the Navy has already implemented coral habitat conservation projects that are beneficial to ESA-listed corals within some INRMP marine areas in Guam, as described in the INRMP annual reports in the JRM INRMP's Appendix D (DoN, 2019a), and listed in the Draft Information Report. Many of these projects have been ongoing for several years and are proactive, in that they were not required of the Navy by the ESA. For example, in Fiscal Year 2018 (Oct-18 to Sep-19, FY18), the following coral habitat conservation projects were carried out by the Navy within these waters: (1) 20 mooring buoys were installed within NBG Main Base submerged waters to prevent anchoring on its coral reefs; (2) monitoring of the impacts of coral bleaching and crown of thorns starfish on reef-building corals including listed species; (3) coral surveys of Apra Harbor including listed species; (4) translocation of corals from a dredging area within Apra Harbor (no listed corals); (5) water quality monitoring; and (6) environmental education and outreach (DoN, 2019a, Appendix D, FY18 Annual Report). Many of these projects have been ongoing for several years and are proactive, in that they were not required of the Navy by the ESA.

(3) History of Strong Conservation Work—the Navy has a long history of carrying out successful marine habitat conservation work on Guam, and often takes the initiative on conservation efforts whether requested by NMFS or FWS or not. For example, many of the coral habitat conservation projects in the 2019 JRM INRMP had already been started by the Navy before corals were listed in 2014, and were being done to improve conservation of marine resources on the island, regardless of whether they were required by Federal statute or not.

The coral habitat enhancement elements of the JRM INRMP described previously are expected to substantially reduce the types of effects within the three INRMP marine areas in Guam that would be addressed through the destruction-or-adverse-modification analysis. Navy would accomplish this primarily by using the results of its own monitoring program to develop and implement management actions to enhance coral habitat and measures to minimize the impacts of Navy's (and other DoD branches') actions in Guam on coral habitat within the INRMP marine areas, thereby benefiting listed corals and their habitat.

JRM INRMP—CNMI

In CNMI, the JRM INRMP encompasses two marine areas that overlap with areas considered for coral critical habitat: (1) The Tinian Marine Lease Area (Tinian MLA) Submerged Lands; and (2) the Farallon de Medinilla (FDM) Submerged Lands (DoN, 2019). A summary of the analyses of whether the INRMP is likely to benefit the habitat of ESA-listed corals in each of these two INRMP marine areas is provided below, summarized from the full analyses in the Draft Information Report (NMFS, 2019).

With regard to the extent of the area and essential feature present: (1) The Tinian MLA Submerged Lands cover approximately 47,500 acres surrounding the northern portion of Tinian (described in the JRM INRMP, Section 11.3, DoN, 2019); (2) the FDM Submerged Lands consists of approximately 25,000 acres surrounding FDM (described in the JRM INRMP, Section 12.3, DoN, 2019). Most or all of the potential proposed critical habitat within the two INRMP marine areas includes both the substrate and water quality components of the essential feature of coral critical habitat (
i.e.,
characteristics of substrate and water quality support coral life history, including reproduction, recruitment, growth, and maturation), based on information provided in the Tinian and FDM sections of the Draft Information Report (NMFS, 2019), the Tinian and FDM chapters of PIFSC's coral reef monitoring report for the Mariana archipelago (Brainard
et al.
2012), and the INRMP (DoN, 2019).

With regard to use of the area by the listed species, the listed coral
Acropora globiceps
is distributed widely throughout the Tinian MLA Submerged Lands, and also occurs in the FDM Submerged Lands. One other listed coral species,
Acropora retusa,
has been recorded in the Tinian MLA Submerged Lands, but not in the FDM Submerged Lands. No other listed corals have been reported from either INRMP marine area (DoN, 2019; NMFS, 2019).

With regard to the relevant elements of the INRMP, and certainty that the relevant elements will be implemented, the two parts of this step are addressed separately below. The relevant elements of the JRM INRMP for each INRMP marine area include: (1) For the Tinian MLA Submerged Lands, the INRMP includes a Coral Habitat Enhancement plan, consisting three specific actions to enhance coral habitat by monitoring health and acute impacts (Section 11.4.2.1; DoN, 2019); and (2) for the FDM Submerged Lands, the INRMP includes marine habitat management actions, consisting of surveys and mapping of ESA-listed corals, coral reef, and other marine habitats within the area (Section 12.4.2; DoN, 2019). The INRMP also includes assessment of ESA-listed corals, as required by the 2015 biological opinion on the Navy's Mariana Islands Testing and Training program (Section 12.4.2.2; DoN, 2019).

NMFS concludes that the Navy will implement these relevant elements of the JRM INRMP for three reasons:

(1) Clear and Recent Documentation—the 2019 JRM INRMP includes Coral Habitat Enhancement plans for INRMP marine areas in CNMI (Tinian MLA, FDM Submerged Lands), with clear strategies and actions that address the habitat conservation needs of ESA-listed corals within these areas. The JRM INRMP's Appendix D also includes annual reports describing how coral conservation efforts have been implemented in recent years in INRMP marine areas in CNMI. These new coral habitat conservation plans, as well as reports from recent years, clearly articulate how Navy is conserving coral habitat within the INRMP marine areas in CNMI, and how it will do so in the future.

(2) Demonstration of Good Faith Efforts for Listed Corals—the Navy has already implemented coral projects that have the potential to benefit the habitat of ESA-listed corals within INRMP marina areas in CNMI (Tinian MLA, FDM Submerged Lands). For example, coral species presence and abundance surveys were conducted within the Tinian MLA in 2013 (DoN, 2014) and 2017 (DoN, 2017), and around FDM in 2012 (Smith and Marx, 2016) and 2017 (Carilli
et al.,
2018). These surveys were not required by the ESA, and have the potential to benefit the habitat of ESA-

listed corals by providing information needed to better protect these areas in the future.

(3) History of Strong Conservation Work—the Navy has a long history of carrying out successful marine habitat conservation work in the Mariana Islands, and often takes the initiative on conservation efforts whether requested by NMFS or FWS or not. For example, many of the coral habitat conservation projects in the 2019 JRM INRMP had already been started by the Navy before corals were listed in 2014, and were being done to improve conservation of marine resources on the island, regardless of whether they were required by Federal statute or not. While the great majority of these projects have been implemented in Guam rather than CNMI, the JRM INRMP includes many plans for CNMI (as noted previously), and the same Navy office (Navy Facilities Marianas) is responsible for carrying out such work in both Guam and CNMI.

The coral habitat enhancement elements of the JRM INRMP described previously are expected to substantially reduce the types of effects within the two INRMP marine areas in CNMI that would be addressed through the destruction-or-adverse-modification analysis. Navy would accomplish this primarily by using the results of its own monitoring program to develop and implement management measures to minimize the impacts of Navy's (and other DoD branches') actions in CNMI on coral habitat within the INRMP marine areas, thereby benefiting listed corals and their habitat.

Wake INRMP

On Wake Atoll, the Wake INRMP (USAF, 2017) encompasses the entire area considered for coral critical habitat, as described and shown in the Draft Information Report (NMFS, 2019). A summary of the analyses of whether the INRMP is likely to benefit the habitat of ESA-listed corals in this INRMP marine area is provided below, summarized from the full analyses in the Draft Information Report (NMFS, 2019).

With regard to the extent of the area and essential feature present, the Wake INRMP marine area includes nearly 500,000 acres of Submerged Lands and waters within the lagoon and surrounding the atoll out to 12 nautical miles from the mean low water line (USAF 2017), and thus includes all reef-building corals and coral reefs associated with the atoll. Most or all of the potential proposed critical habitat within the INRMP marine area includes both the substrate and water quality components of the essential feature of coral critical habitat (
i.e.,
characteristics of substrate and water quality support coral life history, including reproduction, recruitment, growth, and maturation), based on information provided in the Wake section of the Draft Information Report (NMFS, 2019) and the INRMP (USAF, 2017).

With regard to use of the area by the listed species, the USFWS coral survey at Wake Atoll in August 2016 recorded colonies of both
Acropora globiceps
and
A. retusa
on the south side of Wake in the vicinity of the three sites (USFWS, 2017; USAF, 2017). Thus, we assume that at least these two listed species occur throughout much of this INRMP marine area. No other listed corals have been reported from Wake (USAF, 2017; NMFS, 2019).

With regard to the relevant elements of the INRMP, and certainty that the relevant elements will be implemented, the two parts of this step are addressed separately below. The relevant element of the Wake INRMP is the coral conservation component that was added to the INMRP in 2017 (Appendix S, Coral Conservation Actions at Wake Atoll; USAF, 2017), which is made up of four groups of actions, each of which include multiple projects: Water quality improvements (six projects), education and outreach (two projects), fisheries management (four projects), and physical DoD presence on Wake Atoll (three projects; USAF, 2017). The actions and projects are described in detail in the Draft Information Report (NMFS, 2019).

NMFS concludes that the Air Force will implement these relevant elements of the Wake INRMP for three reasons:

(1) Clear and Recent Documentation—the Wake INRMP includes a coral conservation plan (Appendix S) with a 4-pronged strategy (water quality improvement, outreach and education for Wake-based staff, fisheries management, and physical DoD presence on Wake Atoll
i.e.,
restriction of access and overall natural resource management) that comprehensively addresses the conservation needs of ESA-listed corals on Wake Atoll. This new official coral conservation plan clearly articulates how USAF is conserving corals on Wake, and how it will do so in the future.

(2) Demonstration of Good Faith Efforts for Listed Corals: USAF has already implemented projects on Wake for each of its 4-pronged coral conservation strategy, as explained in Appendix S of the Wake INRMP. For water quality improvement, in 2016 USAF began implementation of both the stormwater pollution prevention and invasive plant control projects. For outreach and education, in 2016 USAF revised the Wake Island Dive Club Charter to further reduce the potential impacts of recreational activities on corals. For fisheries management, in 2017 USAF updated its fishing rules, which are part of the Wake Island Operating Guidance (PSRC 2017) to prohibit the use of (1) cast nets on the exterior of the atoll, (2) anchoring on coral reef habitat, and (3) and trolling over coral reef habitat. For physical DoD presence on Wake Atoll, in 2016 USAF funded and provided logistical support for a FWS coral survey that documented two ESA-listed corals on the atoll for the first time.

(3) History of Strong Conservation Work—USAF has a long history of carrying out successful conservation work on Wake, and often takes the initiative on conservation efforts whether requested by NMFS or FWS or not. For example, many of the projects in the new INRMP's coral conservation strategy had already been started by USAF before corals were listed in 2014, and were being done to improve conservation of marine and terrestrial resources on the atoll, regardless of whether they were required by Federal statute or not. Likewise, in 2016, USAF funded and supported the FWS coral survey of the atoll, leading to the discovery of two ESA-listed corals. In addition, USAF has historically been an excellent conservation partner with NMFS and FWS, supporting a wide variety of marine and terrestrial conservation projects, and actively engaging both agencies in the INRMP planning and implementation process.

The coral conservation component of the Wake INRMP (Appendix S, Coral Conservation Actions at Wake Atoll; USAF, 2017) is expected to reduce both direct and indirect impacts to listed corals via minimization or avoidance of recreational impacts (fishing, diving, anchoring), and terrestrial impacts (
i.e.,
run-off from land-based activities; USAF, 2017). Thus, implementation of the Wake INRMP is likely to provide substantial protection to the essential feature of coral critical habitat (reproductive, recruitment, growth, and maturation habitat) within the INRMP marine area from the types of effects that would be addressed through critical habitat consultation, thereby benefiting listed corals and their habitat.

4(a)(3) Conclusion

Based on the analyses summarized previously and provided in the Draft Information Report (NMFS, 2019), implementation of the JRM INRMP (DoN, 2019) and the Wake INRMP (USAF, 2017) both are likely to benefit

the habitats of ESA-listed coral species within all INRMP marine areas on Guam, CNMI, and Wake. Thus, the potential proposed coral critical habitat within the INRMP marine areas on Guam, Tinian, FDM, and Wake are ineligible for coral critical habitat. The partial overlap of these INRMP marine areas with potential proposed coral critical habitat are shown in Figures 21 (Guam) and 22 (Tinian) of the Draft Information Report (NMFS, 2019). On FDM and Wake, the INRMP marine areas completely encompass all the potential proposed coral critical habitat, as shown in Figures 11 (FDM) and 19 (Wake) of the Draft Information Report (NMFS, 2019).

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 area from critical habitat if (s)he determines that the benefits of exclusion (that is, avoiding some or all of the impacts that would result from designation) outweigh the benefits of designation based upon the best scientific and commercial data available. The Secretary may not exclude an area from designation if exclusion will result in the extinction of the species. Because the authority to exclude is discretionary, exclusion is not required for any particular area under any circumstances.

The ESA provides the U.S. Fish and Wildlife Service (USFWS) and NMFS (the Services) with broad discretion in how to consider impacts. (See, H.R. Rep. No. 95-1625, at 17, reprinted in 1978 U.S.C.C.A.N. 9453, 9467 (1978). Economics and any other relevant impact shall be considered by the Secretary in setting the limits of critical habitat for such a species. The Secretary is not required to give economics or any other relevant impact predominant consideration in his specification of critical habitat. The consideration and weight given to any particular impact is completely within the Secretary's discretion.). Courts have noted the ESA does not contain requirements for any particular methods or approaches. (See,
e.g., Bldg. Indus. Ass'n of the Bay Area et al.
v.
U.S. Dept. of Commerce et al.,
No. 13-15132 (9th Cir., July 7, 2015), upholding district court's ruling that the ESA does not require the agency to follow a specific methodology when designating critical habitat under section 4(b)(2)). For this proposed rule, we followed the same basic approach to describing and evaluating impacts as we have for several recent critical habitat rulemakings, as informed by our Policy Regarding Implementation of Section 4(b)(2) of the ESA (81 FR 7226, February 11, 2016).

The following sub-sections describe the economic, national security, and other relevant impacts that we projected would result from including the specific areas described previously in these proposed critical habitat designations. We considered these impacts when deciding whether to exercise our discretion to propose excluding particular areas from the designation. Both positive and negative impacts were identified and considered (these terms are used interchangeably with benefits and costs, respectively). Impacts were evaluated in quantitative terms where feasible, but qualitative appraisals were used where that is more appropriate.

The primary impacts of a critical habitat designation result from the ESA section 7(a)(2) requirement that Federal agencies ensure that their actions are not likely to result in the destruction or adverse modification of critical habitat, and that they consult with NMFS in fulfilling this requirement. Determining these impacts is complicated by the fact that section 7(a)(2) also requires that Federal agencies ensure their actions are not likely to jeopardize the species' continued existence. One incremental impact of designation is the extent to which Federal agencies modify their proposed actions to ensure that they are not likely to destroy or adversely modify the critical habitat beyond any modifications they would make because of listing and the jeopardy requirement. When the same modification would be required due to impacts to both the species and critical habitat, the impact of the designation is co-extensive with the ESA listing of the species (
i.e.,
attributable to both the listing of the species and the designation critical habitat). To the extent possible, our analysis identified impacts that were incremental to the proposed designations of critical habitat, meaning those impacts that are over and above impacts attributable to the species' listing or any other existing regulatory protections. Relevant, existing regulatory protections (including the species' listing) are referred to as the “baseline” and are also discussed in the following sections.

The following economic and national security impact analyses describe projected future Federal activities that would trigger section 7 consultation requirements because they may affect the essential feature, and consequently may result in economic or national security impacts. Additionally, these analyses describe broad categories of project modifications that may reduce impacts to the essential feature, and state whether the modifications are likely to be solely a result of the critical habitat designation or co-extensive with another regulation, including the ESA listing of the species. These analyses incorporate recent guidance provided in the final rule on 4(b)(2) analyses (81 FR 7413 February 11, 2016).

Economic Impacts

Economic impacts of the critical habitat designations result through implementation of section 7 of the ESA in consultations with Federal agencies to ensure their proposed actions are not likely to destroy or adversely modify critical habitat. These economic impacts may include both administrative and project modification costs. Economic impacts that may be associated with the conservation benefits of the designations are described later.

An economic impact analysis was conducted in 2016 on the proposed coral critical habitat that projected annual economic impacts during the 10-year period 2016-2025, as described in section 5.1 of the Draft Information Report. Due to a large number of uncertainties, low-end and high-end estimates of economic impacts were developed in terms of the incremental cost of implementing coral critical habitat in addition to the cost of section 7 consultations without critical habitat. A key uncertainty in estimating the economic impacts of coral critical habitat is the lack of critical habitat for any marine species in the affected areas, which means that the historic record of section 7 consultations in these areas does not provide a good predictor of either the future number of total consultations, or the proportion of formal vs. informal consultations resulting from coral critical habitat. Consequently, there is a very large difference between the low-end and high-end economic impact estimates. Low-end total incremental costs resulting from the listed corals' critical habitat are estimated at just under $350,000 over ten years, with an annualized cost of approximately $50,000. High-end total incremental costs are estimated at more than $13 million over 10 years, with an annualized cost of approximately $1.9 million, although this number is unrealistic, as explained below (Draft Information Report, section 5.1).

The high-end estimate is 40 times higher than the low-end estimate primarily because of the assumption that critical habitat would result in all

future coral consultations being formal, and that the resulting biological opinions would require modifications to all activities that would not be required in the absence of critical habitat. Critical habitat could only have a high-end level of economic impact if (1) all managed areas such as navigation channels, harbors, and marinas are included in critical habitat, as this is where the action areas for most activities requiring consultation would be located; and (2) the action areas contain the essential feature but not the listed corals, so formal consultation would be required solely because of critical habitat. However, managed areas are not included in the proposed critical habitat, as explained in the Specific

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Source: Frix Law Library, https://www.frixlaw.com/law-library/documents/fr%3A2020-21226. Public record. Not legal advice.