Endangered and Threatened Wildlife and Plants: Proposed Reclassification of Pillar Coral (Dendrogyra cylindrus) From Threatened to Endangered, 59494-59501 [2023-17769]

Agencies

• DEPARTMENT OF COMMERCE
• National Oceanic and Atmospheric Administration

[Federal Register Volume 88, Number 166 (Tuesday, August 29, 2023)]
[Proposed Rules]
[Pages 59494-59501]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2023-17769]


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DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

50 CFR Parts 223 and 224

[Docket No. 230810-0189; RTID 0648-XR126]


Endangered and Threatened Wildlife and Plants: Proposed 
Reclassification of Pillar Coral (Dendrogyra cylindrus) From Threatened 
to Endangered

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

ACTION: Proposed rule; request for comments.

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SUMMARY: We, NMFS, are issuing a proposed rule to change the status of 
pillar coral (Dendrogyra cylindrus) on the Federal List of Threatened 
and Endangered Species from threatened to endangered as recommended in 
the recent 5-year review of the species under the Endangered Species 
Act (ESA) of 1973. We propose this action based on population declines 
and susceptibility to a recently emerged coral disease.

DATES: Written comments must be received on or before October 30, 2023.
    Public hearings: A public hearing on the proposed rule will be held 
online on September 26, 2023, from 1 to 3 p.m. Eastern Daylight Time. 
Members of the public can join by internet or phone, regardless of 
location. Instructions for joining the hearing are provided under 
ADDRESSES. Requests for additional public hearings must be received by 
October 13, 2023.

ADDRESSES: The public hearing will be conducted as a virtual meeting. 
You may join the virtual public hearing using a web browser, a mobile 
app on a phone (app installation required), or by phone (for audio 
only) as specified on this website: https://www.fisheries.noaa.gov/species/pillar-coral#conservation-management.
    You may submit comments on the proposed rule verbally at the public 
hearing or in writing, by any of the following methods:
     Electronic Submission: Submit all electronic public 
comments via the Federal e-Rulemaking Portal. Go to www.regulations.gov 
and enter NOAA-NMFS-2023-0002 in the Search box. Click on the 
``Comment'' icon, complete the required fields, and enter or attach 
your comments; or
     Email: Submit written comments to 
[email protected].
    Instructions: 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 by NMFS. All comments received are a part of the 
public record and will generally be posted for public viewing on 
www.regulations.gov without change. All personal identifying 
information (e.g., name, address, etc.), confidential business 
information, or otherwise sensitive information submitted voluntarily 
by the sender will be publicly accessible. NMFS will accept anonymous 
comments (enter ``N/A'' in the required fields if you wish to remain 
anonymous).

FOR FURTHER INFORMATION CONTACT: Alison Moulding, 727-551-5607, 
[email protected].

SUPPLEMENTARY INFORMATION:

Background

    On September 10, 2014, we published a final rule listing pillar 
coral (Dendrogyra cylindrus), along with 4 other Caribbean coral 
species and 15 Indo-Pacific coral species, as threatened under the ESA 
(79 FR 53851). In early 2021, we announced a 5-year review of

[[Page 59495]]

7 threatened Caribbean coral species, including D. cylindrus (86 FR 
1091, January 7, 2021). A 5-year review is intended to ensure that the 
listing classification of a species is accurate, and this review must 
be based on the best scientific and commercial data available.
    Section 3 of the ESA defines an endangered species as any species 
which is in danger of extinction throughout all or a significant 
portion of its range and a threatened species as one which is likely to 
become an endangered species within the foreseeable future throughout 
all or a significant portion of its range. The statute requires us to 
determine whether a species is threatened or endangered as a result of 
any of the factors listed in section 4(a)(1) of the ESA: (A) the 
present or threatened destruction, modification, or curtailment of its 
habitat or range; (B) overutilization for commercial, recreational, 
scientific, or educational purposes; (C) disease or predation; (D) the 
inadequacy of existing regulatory mechanisms; or (E) other natural or 
manmade factors affecting its continued existence. Changes to a listed 
species' status must be determined on the basis of these factors using 
solely the best scientific and commercial data available (16 U.S.C. 
1533(c)(2)(B)). Implementing regulations in 50 CFR 424.11(b) reiterate 
the requirement that changes in a species' classifications must be 
based solely on the best available scientific and commercial 
information regarding a species' status. Recently proposed revisions to 
the regulations in 50 CFR 424.11(b) would restore the phrase ``without 
reference to possible economic or other impacts of such determination'' 
to the end of the provision, which was removed in 2019 (see 88 FR 
40764, June 22, 2023). This clarification, if finalized, would not 
affect the existing requirements for making classification 
determinations, nor would it affect the proposed reclassification for 
the pillar coral.

Biology and Life History

    Dendrogyra cylindrus is a colonial coral that can form large 
pillars (up to 3 meters (m)) upon an encrusting base. The final listing 
rule (79 FR 53851, September 10, 2014) described D. cylindrus as a 
gonochoric (separate sexes), broadcast spawning coral species that can 
also reproduce asexually through fragmentation and reattachment to the 
substrate. It has a relatively low annual egg production and low sexual 
recruitment (no reports of observed sexual recruitment in the wild).
    Since the listing, new evidence of hermaphroditism (presence of 
both male and female gametes) and plasticity in reproductive mode has 
been observed in histological samples (Kabay, 2016) and in spawning 
colonies observed over several seasons in Florida (Neely et al., 2018; 
Neely et al., 2020a; O'Neil et al., 2021). Histological samples from 
Florida revealed some hermaphroditic colonies that produced eggs and 
sperm within the same polyp and within the same mesentery while most 
colonies only produced eggs or sperm (Kabay, 2016). Dendrogyra 
cylindrus colonies have been observed to spawn as different genders on 
different nights of the same year, as different genders in different 
years, and as hermaphrodites spawning eggs and sperm simultaneously 
(Neely et al., 2018; Neely et al., 2020a; O'Neil et al., 2021). Also, 
separate colonies of the same genotype (genetically identical colonies) 
have been observed to spawn either male or female gametes, and some 
colonies produced both eggs and sperm within separate regions of the 
same colony (Neely et al., 2018). Spawning observations have also 
suggested that eggs may be fertilized within female colonies prior to 
release (Marhaver et al., 2015). This flexibility in reproductive mode 
may be a strategy to improve the chances of successful reproduction for 
a species that is naturally rare and whose potential mates are scarce 
(Neely et al., 2018).

Abundance, Trends, and Distribution

    Dendrogyra cylindrus is present in the western Atlantic and 
throughout the greater Caribbean. It is absent in the Flower Garden 
Banks in the Gulf of Mexico and from the southwest Gulf of Mexico. It 
inhabits most reef environments in water depths ranging from 1 to 25 m 
and is most common in reef environments in water depths between 5 and 
15 m. It has a naturally uncommon to rare occurrence, appearing as 
scattered, isolated colonies; it is sometimes found in highly clonal 
aggregations, likely resulting from fragmentation events (Chan et al., 
2019).
    At the time of listing (79 FR 53851, September 10, 2014), available 
information indicated that colony density and cover were low (generally 
less than 1 colony per 10 square meters (m\2\) and less than 1 percent 
cover). Estimates of frequency of occurrence of D. cylindrus ranged 
from 1 percent of sites in Florida to a high of 30 percent in the U.S. 
Virgin Islands. Based on extrapolations of abundance from stratified 
random samples, abundance in Florida was estimated at tens of thousands 
of colonies. There was no available population trend information at the 
time of listing.
    Since the listing, there has been a new survey of D. cylindrus 
abundance in Los Roques National Park, Venezuela (Cavada-Blanco et al., 
2020). Surveys were conducted between 2014 and 2015 at 106 sites where 
the species had been reported by the local community. A total of 1,490 
D. cylindrus colonies were located within 49 percent of the sites 
surveyed, and colony abundance ranged between 1 and 68 colonies per 
site. Average height of colonies was 72 centimeters (cm) (range 5-290 
cm), though most of the colonies were below 60 cm in height. Disease 
presence was low overall (0.2 and 0.3 percent of colonies with white 
plague and black band disease, respectively) and 29 percent of the 
1,490 colonies exhibited partial mortality (Cavada-Blanco et al., 
2020).
    New studies published since the listing provide some population 
trend information. Surveys of D. cylindrus were conducted in 2012 in 
Old Providence and St. Catalina Islands, which host more than 90 
percent of the D. cylindrus population in Colombia (Bernal-Sotelo et 
al., 2019). Results were compared to surveys of the same area conducted 
in 2002 to discern population trends. The surveys revealed that D. 
cylindrus was present in 2012 in 3 of the 4 reef areas where it was 
present in 2002, but its spatial extent was reduced (i.e., D. cylindrus 
occupied a smaller amount of the reef areas in 2012 relative to 2002). 
Half of the radial plots (60 m diameter) that contained more than 4 
colonies of D. cylindrus in 2002 contained no living colonies of D. 
cylindrus 10 years later. The number of colonies and fragments (i.e., 
tissue remnants on standing colonies) observed in 2002 were 213 and 70, 
respectively, versus 261 colonies and 585 fragments in 2012. Almost 97 
percent of the fragments observed in 2012 were produced as a result of 
partial colony mortality. Average colony and fragment size was also 
smaller in 2012, and the number of colonies with partial mortality and 
the amount of partial mortality were higher. Larger colonies (>=115 cm) 
had higher partial and total mortality. In summary, compared to 2002, 
in 2012 there were more D. cylindrus colonies and fragments that likely 
resulted from partial mortality. Colonies and fragments in 2012 were 
smaller in size, had a higher prevalence of partial mortality, and had 
higher amounts of partial mortality within individual colonies. The 
authors concluded that the reduced amount of living tissue, dominance 
of asexually produced

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fragments, and smaller fragment size limit the potential for population 
growth, making this population vulnerable and at risk of local 
extinction (Bernal-Sotelo et al., 2019).
    Beginning in 2013, all known colonies of D. cylindrus in Florida (n 
= 819 colonies) were tracked in an effort to monitor colony health and 
status (Neely et al., 2021a). There were consecutive thermal bleaching 
events in 2014 and 2015, as well as ongoing and emerging disease 
events, which affected the monitored D. cylindrus colonies. Recovery 
from bleaching was calculated to take 11 years (in the absence of 
additional severe stressors) based on colony growth rates (~4 percent 
annual increase in live tissue) observed after bleaching but before 
disease affected the colonies (Neely et al., 2021a). In a separate 
study using the same tracked colonies, demographic modeling of D. 
cylindrus was conducted to examine the effects of thermal stress events 
on population persistence. The model used different survival scenarios 
of 80, 50, and 20 percent of the population after the 2014 and 2015 
thermally-induced bleaching and disease outbreak and assumed no sexual 
reproduction, no establishment of asexual recruits, and no successful 
restoration (Chan et al., 2019). The model predicted that the number of 
thermal stress events before local extinction occurred was 31 for the 
80 percent survival scenario, 11 for the 50 percent survival scenario, 
and 6 for the 20 percent survival scenario (Chan et al., 2019). 
Assuming 2 stress events per decade until 2042 when thermal stress 
events are predicted to become annual, local extinction of D. cylindrus 
in Florida was predicted to occur in 2066 for the 80 percent survival 
scenario, in 2046 for the 50 percent survival scenario, and in 2039 for 
the 20 percent survival scenario (Chan et al., 2019). These modeling 
predictions did not account for disease, which, as described below, 
caused near extirpation from Florida much sooner than the model's 
predicted dates for local extinction (Neely et al., 2021a).
    The Florida D. cylindrus colonies that were monitored between 2013 
and 2020 included 819 colonies of an assumed 190 genotypes based on 
genetic testing or colony distances from each other (Neely et al., 
2021a). Distances between genotypes on average was about 1 kilometer 
(km), ranging from 2.5 m to 6.6 km. Half of the colonies represented 
clones of only five genotypes, and 62 percent of the genotypes were 
represented by a single colony. Asexual reproduction accounted for 77 
percent of the colonies. During baseline surveys in 2013-2014 (542 
colonies, 533 alive), average tissue mortality was 30 percent (n = 
542), and 22 percent of the colonies exhibited low (2.2 percent) recent 
mortality. During the monitoring period, there were chronic stressors 
that occurred on about 1 percent of colonies and caused minor damage 
(on average less than 1 percent tissue loss), including damselfish 
gardens/nests, predation by the corallivorous snail (Coralliophila 
abbreviata), competition with other benthic organisms, and abrasion and 
burial. However, acute stressors, including the 2014 and 2015 bleaching 
events, ongoing outbreaks of white plague and black band disease, and 
the outbreak of a novel, particularly devastating disease, termed stony 
coral tissue loss disease (SCTLD), resulted in extremely high mortality 
(Lewis, 2018; Lewis et al., 2017; Neely et al., 2021a). By the end of 
the monitoring period in 2020, there had been a 94 percent loss of 
coral tissue, 93 percent loss of colonies, and 86 percent loss of 
genotypes due primarily to disease. At the end of 2020, there were 25 
known genotypes remaining (out of the 190 genotypes assumed at the 
beginning of the study), half of which had declined to less than 2 
percent live tissue, and the other half were actively experiencing 
rapid tissue loss due to SCTLD. Only two genotypes remained unaffected 
and were located in the Dry Tortugas where SCTLD had not yet reached at 
the time of the study (but has now). Based on the extreme loss of 
colonies and live tissue, D. cylindrus is now considered functionally 
extinct along the Florida reef tract (Neely et al., 2021a).
    Although quantitative population trend data are only available from 
Florida and Colombia, we assume the species is in decline throughout 
most of its range based on the evidence from these regions (northern 
and southwestern portions of its range) and the more widespread 
evidence of severe disease impacts described in the ``Threats'' section 
below.

Threats

    The ESA requires us to determine whether a species is endangered or 
threatened as a result of any of the following factors: (A) the present 
or threatened destruction, modification, or curtailment of its habitat 
or range; (B) overutilization for commercial, recreational, scientific, 
or educational purposes; (C) disease or predation; (D) the inadequacy 
of existing regulatory mechanisms; or (E) other natural or manmade 
factors affecting its continued existence. The final listing rule (79 
FR 53851, September 10, 2014) identified and described the 
susceptibility of D. cylindrus to multiple threats including ocean 
warming (Factor E), ocean acidification (Factor E), disease (Factor C), 
nutrient enrichment (Factors A and E), sedimentation (Factors A and E), 
and trophic effects of fishing (Factor A). In addition, D. cylindrus 
was determined to be at heightened extinction risk due to inadequate 
regulatory mechanisms to address global threats (i.e., climate change 
that results in ocean warming and acidification and has been linked to 
increasing coral disease; Factor D).
    Since the listing of D. cylindrus as threatened (79 FR 53851, 
September 10, 2014), SCTLD has emerged as a new and deadly disease, 
impacting at least 24 Caribbean coral species, including D. cylindrus 
(Florida Coral Disease Response Research & Epidemiology Team, 2018). 
SCTLD was first observed in Miami, Florida, in 2014 and then spread 
throughout the Florida reef tract over the next several years (Neely, 
2018; Precht et al., 2016). SCTLD has continued to spread throughout 
much of the Caribbean and has been observed along the Mesoamerican 
Reef, Bahamas, Greater Antilles, and in the Lesser Antilles as far 
south as Grenada (see https://www.agrra.org/coral-disease-outbreak/ for 
a map of confirmed sightings of SCTLD in the greater Caribbean). The 
disease is unprecedented in temporal and geographic scope as well as 
the number of susceptible species, prevalence, and rates of mortality 
(Neely, 2018; Precht et al., 2016). In almost all affected species, 
tissue loss occurs rapidly and leads to full colony mortality. The 
disease appears to be both waterborne and transmissible through direct 
contact (Aeby et al., 2019). In addition, sediment can act as a SCTLD 
vector by transmitting SCTLD in the absence of direct contact between 
diseased and healthy corals Studivan et al., 2022). SCTLD does not 
appear to be seasonal like many other coral diseases that will ramp up 
during higher temperatures but then decrease as water temperatures 
cool.
    Dendrogyra cylindrus is highly susceptible to SCTLD and is often 
one of the first species to become infected (Florida Coral Disease 
Response Research & Epidemiology Team, 2018). Surveys of the 
progression and impact of SCTLD have shown that D. cylindrus exhibits 
high disease prevalence and colony mortality. As previously described, 
between 2014 and 2020 the Florida population of D. cylindrus was 
heavily impacted by SCTLD; there was a loss of 93 percent of colonies 
and 94 percent of live tissue (Neely et al., 2021a). In surveys of the 
Bahamas, 67 percent of D. cylindrus colonies (n = 15,

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March 2020) were infected with SCTLD in Grand Bahama, and 13 percent of 
D. cylindrus colonies (n = 8, June 2020) were infected in New 
Providence (Dahlgren et al., 2021). In surveys across Mexico, 71 
percent of D. cylindrus colonies (n = 7) surveyed in 2018 to 2019 were 
infected with SCTLD, and D. cylindrus was extirpated from several 
mainland coastal sites (Alvarez-Filip et al., 2019). In separate 
surveys conducted in Cozumel, Mexico, between 2018 and 2020, surveyors 
observed that D. cylindrus colonies were heavily affected by SCTLD, 
though no quantitative prevalence data are available because no D. 
cylindrus colonies occurred in the survey transects (Estrada-Saldivar 
et al., 2021). In 54 sites surveyed in 2020 around St. Thomas, U.S. 
Virgin Islands, 67 percent of the D. cylindrus colonies (n = 3) were 
infected with SCTLD, and D. cylindrus was the species with the highest 
prevalence of SCTLD within the epidemic zone (Costa et al., 2021). In 
long-term monitoring transects in the U.S. Virgin Islands, 50 percent 
of D. cylindrus colonies (n = 2) surveyed in February 2019 were 
infected, and by July 2020, no D. cylindrus colonies remained alive in 
the transects (Brandt et al., 2021). Prior to the documentation of 
SCTLD in the U.S. Virgin Islands, there were 11 colonies of D. 
cylindrus present in the monitoring transects between 2005 and 2018, 
suggesting loss of nine colonies from unknown causes (Brandt et al., 
2021). The study also noted that numerous recently dead colonies of D. 
cylindrus, presumably from SCTLD, were observed and that it was 
increasingly rare to find live colonies, even in locations where the 
species previously had been relatively abundant (Brandt et al., 2021).
    SCTLD has spread from Florida, where it was initially documented, 
to the eastern and western Caribbean. Although it has not yet been 
confirmed in all areas of the Caribbean (i.e., the most southern part), 
we assume SCTLD will eventually reach all areas of the range of D. 
cylindrus based on its previous spread and the fact that it is 
waterborne.

Conservation Measures

    Coral colonies infected with SCTLD have been effectively treated to 
stop the progression of the disease. Initial ex situ (in aquaria) 
treatment of D. cylindrus consisted of amputation of diseased tissue 
and dipping the corals (13 fragments from 6 colonies) in a Lugol's 
iodide solution, which is commonly used in the aquarium industry as a 
treatment for bacterial infections. After repeated treatments, this 
method was effective in arresting disease progression about 53 percent 
of the time (O'Neil et al., 2018). Additional ex situ treatment with 
the antibiotic amoxicillin applied directly to the diseased tissue 
margin in a custom-made paste formulation (modified from a dental 
paste) increased survival of infected D. cylindrus to about 97 percent 
(Miller et al., 2020). However, this antibiotic dental paste has to be 
applied to corals out of water (corals were placed back in the water 
after antibiotic paste application). To treat corals in situ (in the 
ocean), slow-release antibiotic pastes were developed that could be 
applied underwater (O'Neil et al., 2018). Antibiotics pastes have been 
successfully applied in situ to coral species infected with SCTLD in 
Florida (67 to 95 percent effectiveness, Neely et al., 2020b; Neely et 
al., 2021c; Shilling et al., 2021; Walker et al. 2021), though no 
reports of effectiveness on in situ D. cylindrus colonies have been 
published, likely because most of these studies have been performed in 
Florida after the near-extirpation of the species. The treatment only 
has the ability to stop progression of the disease lesion, but it does 
not prevent new lesions from forming (Neely et al., 2020b; Shilling et 
al., 2021; Walker et al., 2021).
    During the widespread and severe decline of D. cylindrus in 
Florida, a rescue effort was undertaken to collect fragments of live 
colonies and bring them under human care to preserve the remaining 
genetic diversity. From November 2015 to November 2019, fragments were 
collected from most remaining D. cylindrus genotypes (Kabay, 2016; 
Neely et al., 2021b; O'Neil et al., 2021). A total of 574 fragments 
representing 128 genotypes were collected between 2015 and 2019 (Neely 
et al., 2021b), and an additional 4 fragments were collected in August 
2021 from newly found colonies in the Dry Tortugas (K.L. Neely, Nova 
Southeastern University, personal communication). Fragments were 
brought under human care in both land-based and ocean-based nurseries 
for preservation and to aid in propagation and future restoration 
(Kabay, 2016; Neely et al., 2021b; O'Neil et al., 2021). As of the end 
of 2020, 543 fragments of 123 Florida genotypes of D. cylindrus were 
being held in nurseries (Neely et al., 2021a).
    Increased understanding of the reproductive biology and early life 
history of D. cylindrus has contributed to attempts to sexually 
propagate D. cylindrus for use in conservation efforts (Marhaver et 
al., 2015; Neely et al., 2020a; O'Neil et al., 2021; Villalpando et 
al., 2021). The first report of successful settlement from larval 
propagation resulted from collection and fertilization of gametes in 
Cura[ccedil]ao (Marhaver et al., 2015). The resulting D. cylindrus 
larvae were settled and maintained in the lab and reached the primary 
polyp stage (Marhaver et al., 2015). However, settlers did not survive 
longer than 7 months and showed no formation of new polyps through 
budding (Marhaver et al., 2015). Subsequent larval propagation efforts 
in Florida produced a small number of longer-surviving settlers. Gamete 
collections from wild colonies in 2016 produced 3 settlers that 
survived to at least 3 years of age. In 2018, gamete collections from 
colonies maintained ex situ produced 10 settlers that survived to at 
least 1 year old (Neely, 2019). In another attempt at sexual 
propagation, larvae of D. cylindrus were produced from gamete 
collections from wild colonies, settled in the lab, and transferred to 
an offshore coral nursery in the Dominican Republic 1 month after 
settlement (Villalpando et al., 2021). An estimated 380 corals were 
transferred to the nursery, and 1 year after they were transferred,1 
surviving coral was observed (Villalpando et al., 2021). The following 
year (2020), gametes were again collected from wild colonies, settled 
in the lab, and transferred to an in situ nursery after settlement; 28 
settlers have survived from this cohort for more than two years (M. F. 
Villalpando, FUNDEMAR, personal communication).
    Dendrogyra cylindrus has also successfully reproduced in captivity 
in Florida in an induced spawning system designed to mimic natural 
environmental light and temperature regimes (O'Neil et al., 2021). In 
2020, the induced spawning tanks held 21 D. cylindrus genotypes, and 
over 50,000 viable D. cylindrus larvae were produced from only a 
fraction of the spawn that was collected (O'Neil et al., 2021). A total 
of 4,330 larvae settled, and as of February 2022, 38 small colonies (1-
3 cm in diameter) were alive and remained in captivity (K.L. O'Neil, 
The Florida Aquarium, personal communication). In 2021, colonies in the 
induced spawning tanks produced 150 surviving D. cylindrus recruits (<1 
cm in diameter) that are also being held in captivity (K.L. O'Neil, the 
Florida Aquarium, personal communication). These advances in 
propagation methods have the potential to benefit the species.

Risk of Extinction

    As noted above, D. cylindrus was listed as threatened because of 
its susceptibility to multiple threats, including ocean warming, ocean 
acidification, disease, nutrient

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enrichment, sedimentation, trophic effects of fishing, and inadequate 
regulatory mechanisms to address global threats. Future projections of 
these threats indicate the species is likely to be in danger of 
extinction within the foreseeable future throughout its range. 
Circumstances and demographic risks that contributed to our assessment 
of the species' risk of extinction in 2014 were: (1) geographic 
location in the Caribbean where localized human impacts were high and 
threats were predicted to increase, exposing a high proportion of the 
population to threats over the foreseeable future; (2) uncommon to rare 
occurrence of the species, which heightened the potential effect of 
mortality events and made the species vulnerable to becoming of such 
low abundance within the foreseeable future that it could be at risk 
from depensatory processes, environmental stochasticity, or 
catastrophic events, and (3) low sexual recruitment which limited the 
species' capacity for recovery from threat-induced mortality events 
throughout its range over the foreseeable future.
    The final listing rule (79 FR 53851, September 10, 2014) also 
explained that D. cylindrus was not in danger of extinction at the time 
and did not warrant listing as an endangered species because: (1) there 
was little evidence of population declines, (2) D. cylindrus showed 
evidence of resistance to bleaching from warmer temperatures in some 
portions of its range under some circumstances (e.g., Roatan, 
Honduras), and (3) while its distribution within the Caribbean 
increased its risk of exposure to threats, its occurrence in numerous 
reef environments that would experience highly variable thermal regimes 
and ocean chemistry on local and regional scales at any given point in 
time moderated its vulnerability to extinction.
    We are now proposing to change the status of D. cylindrus from 
threatened to endangered. We make this determination based on the best 
scientific and commercial information available since the original 
listing of D. cylindrus that indicates that there have been declines in 
the abundance and distribution of D. cylindrus in multiple locations 
with the most severe in the northern portions of its range and that D. 
cylindrus is highly susceptible to SCTLD, which has emerged as a 
devastating and deadly new disease. Though SCTLD is not yet present in 
all areas of the Caribbean, the disease spread between 2014 and 2021 
from Florida throughout the northern, western, and eastern Caribbean 
including the Mesoamerican Reef System, the Bahamas, the Greater 
Antilles, and as far south as Grenada in the Lesser Antilles. We expect 
SCTLD to continue to spread throughout the species' range based on the 
previous spread and the fact that it is waterborne. In locations where 
SCTLD has been observed, D. cylindrus has experienced high disease 
prevalence, fast disease progression within infected colonies, and high 
mortality rates from the disease. The distribution of D. cylindrus has 
diminished with the loss of almost all wild colonies in Florida, and 
though the occurrence of D. cylindrus has historically been uncommon to 
rare, the species has become even more rare as a result of SCTLD, 
disappearing from individual sites in Florida, Mexico, and the U.S. 
Virgin Islands. Furthermore, no observed sexual recruitment has been 
reported in the wild, and reductions in population size and local 
extinctions will further inhibit the species' ability to persist and 
replenish diminished populations through asexual and sexual 
reproduction.
    In conclusion, D. cylindrus continues to be susceptible to multiple 
threats such as ocean warming (ESA Factor E), disease (C), 
acidification (E), nutrient enrichment (A and E), sedimentation (A and 
E), trophic effects of fishing (A), and inadequate existing regulatory 
mechanisms to address global threats (D). In addition, the following 
characteristics contribute to its risk of extinction:
    (1) It is geographically located in the highly disturbed Caribbean 
where localized human impacts are high and threats are predicted to 
increase. A range constrained to this particular geographic area that 
is likely to experience severe and increasing threats indicates that a 
high proportion of the population of this species is likely to be 
exposed to those threats;
    (2) It has an uncommon to rare occurrence throughout its range, 
which heightens the potential effect of localized mortality events and 
leaves the species vulnerable to becoming of such low abundance that it 
may be at risk from depensatory processes, environmental stochasticity, 
or catastrophic events;
    (3) Its low sexual recruitment limits its capacity for recovery 
from threat-induced mortality events throughout its range; and
    (4) It has experienced population declines, primarily due to SCTLD, 
in multiple locations throughout its range, including severe declines 
in the northern portion of its range, which has resulted in diminished 
distribution and local extirpation.
    The combination of these characteristics indicates that D. 
cylindrus is in danger of extinction throughout its range and warrants 
listing as an endangered species due to factors A, C, D, and E.
    Conservation actions include treatment of individual colonies for 
SCTLD, ex situ banking, and propagation of D. cylindrus for future 
restoration. The conservation actions will no doubt have benefits to 
the species, but we do not find that the current conservation efforts 
will affect the status of D. cylindrus to the point at which listing as 
endangered is not warranted. Further, because current conservation 
actions do not directly address the root causes of threats such as 
disease, they are insufficient to protect the species from the risk of 
extinction.

Effects of Listing

    Conservation measures provided for species listed as endangered or 
threatened under the ESA include recovery plans (16 U.S.C. 1553(f)), 
critical habitat designations, Federal agency consultation requirements 
(16 U.S.C. 1536), and prohibitions of certain acts under the ESA (16 
U.S.C. 1538). Because D. cylindrus is currently listed as threatened, 
Federal agency consultation requirements are already in effect, and a 
recovery outline has been developed to guide recovery until a full 
recovery plan has been finalized. Critical Habitat has been proposed 
for D. cylindrus (85 FR 76302), and the bases for any final designation 
of critical habitat would not be affected should the status of D. 
cylindrus be changed from threatened to endangered. The ESA section 9 
prohibitions do not currently apply to D. cylindrus because those 
protections are automatically applied only to endangered species and 
NMFS has not promulgated protective regulations for D. cylindrus 
pursuant to ESA section 4(d).
    All of the prohibitions in section 9(a)(1) of the ESA will apply to 
D. cylindrus if it becomes listed as an endangered species. Section 
9(a)(1) includes prohibitions on importing, exporting, engaging in 
foreign or interstate commerce, or ``taking'' of the species. ``Take'' 
is defined under the ESA as ``to harass, harm, pursue, hunt, shoot, 
wound, kill, trap, capture, or collect, or an attempt to engage in any 
such conduct.'' These prohibitions apply to all persons subject to the 
jurisdiction of the United States, including in the United States, its 
territorial sea, or on the high seas. Upon up-listing pillar coral to 
endangered

[[Page 59499]]

status, section 9 of the ESA would expressly prohibit:
    (1) Taking of pillar coral within the U.S. or its territorial sea, 
or upon the high seas;
    (2) Possessing, selling, delivering, carrying, transporting, or 
shipping any pillar coral that was illegally taken;
    (3) Delivering, receiving, carrying, transporting, or shipping in 
interstate or foreign commerce any pillar coral in the course of a 
commercial activity;
    (4) Selling or offering pillar coral for sale in interstate or 
foreign commerce; or
    (5) Importing pillar coral into, or exporting pillar coral from, 
the United States.
    On July 1, 1994, NMFS and FWS published a policy (59 FR 34272) that 
requires us to identify, to the extent known at the time a species is 
listed, those activities that would or would not constitute a violation 
of section 9 of the ESA. The intent of this policy is to increase 
public awareness of the effect of a listing on proposed and ongoing 
activities within a species' range. Based on available information, we 
believe the following categories of activities are likely to meet the 
ESA's definition of ``take'' and therefore result in a violation of the 
ESA section 9 prohibitions. We emphasize that whether a violation 
results from a particular activity is entirely dependent upon the facts 
and circumstances of each incident. The mere fact that an activity may 
fall within 1 of these categories does not mean that the specific 
activity will cause a violation. Further, an activity not listed may in 
fact result in a violation. Activities that are likely to result in a 
violation of section 9 prohibitions include, but are not limited to, 
the following:
    (1) Collection of pillar coral, including colonies, fragments, 
tissue samples, and gametes, from the wild;
    (2) Harming captive pillar coral by, among other means, injuring or 
killing captive pillar coral, through potentially injurious research 
outside the bounds of normal animal husbandry practices;
    (3) Removing, relocating, reattaching, damaging, poisoning, or 
contaminating pillar coral;
    (4) Scientific research activities on wild pillar coral, involving 
the manipulation of the coral or its environment;
    (5) Release of captive pillar coral into the wild. Release of a 
captive coral could have the potential to injure or kill the coral or 
to affect wild populations of pillar coral through introduction of 
disease;
    (6) Harm to pillar coral habitat resulting in injury or death of 
the species, such as removing or altering substrate or altering water 
quality;
    (7) Discharging pollutants, such as oil, toxic chemicals, 
radioactive matter, carcinogens, mutagens, teratogens, or organic 
nutrient-laden water, including sewage water, into pillar corals' 
habitat to an extent that harms or kills pillar coral;
    (8) Shoreline and riparian disturbances (whether in the riverine, 
estuarine, marine, or floodplain environment) that may harm or kill 
pillar coral, for instance by disrupting or preventing the 
reproduction, settlement, reattachment, development, or normal 
physiology of pillar coral. Such disturbances could include land 
development, run-off, dredging, and disposal activities that result in 
direct deposition of sediment on pillar coral, shading, or covering of 
substrate for fragment reattachment or larval settlement; and
    (9) Activities that modify water chemistry in pillar coral habitat 
to an extent that disrupts or prevents the reproduction, development, 
or normal physiology of pillar coral.
    Some categories of activities are unlikely to constitute a 
violation of the section 9 prohibitions should the proposed listing 
become finalized. We consider the following activities to be ones that 
are unlikely to violate the ESA section 9 prohibitions:
    (1) Taking of wild pillar coral, including collection of colonies, 
fragments, tissue samples, and gametes, authorized by a 10(a)(1)(A) 
permit issued by NMFS for the purposes of scientific research or the 
enhancement of propagation or survival of the species and carried out 
in accordance with the terms and conditions of the permit;
    (2) Incidental taking of pillar coral resulting from federally 
authorized, funded, or conducted projects for which consultation under 
section 7 of the ESA has been completed and when the project is 
conducted in accordance with any terms and conditions set forth by NMFS 
in an incidental take statement in a biological opinion pursuant to 
section 7 of the ESA;
    (3) Import or export of pillar coral authorized by a Convention on 
International Trade in Endangered Species (CITES) permit and an ESA 
section 10(a)(1)(A) permit issued by NMFS;
    (4) Continued possession of pillar coral parts or live pillar coral 
that were in captivity at the time of up-listing to an endangered 
species, including any progeny produced from captive corals after the 
rule is finalized, so long as the prohibitions of ESA section 9(a)(1) 
are not violated. Corals are considered to be in captivity if they are 
maintained in a controlled environment or under human care in ocean-
based coral nurseries. Individuals or organizations should be able to 
provide evidence that pillar coral or pillar coral parts were in 
captivity prior to its listing as an endangered species. We suggest 
such individuals or organizations submit information to us on the 
pillar coral in their possession (e.g., type, number, size, source, 
date of acquisition), to establish their claim of possession (see FOR 
FURTHER INFORMATION CONTACT);
    (5) Providing normal care for captive pillar coral. Captive corals 
are still protected under the ESA and may not be killed or injured, or 
otherwise harmed and must receive proper care. Normal husbandry care of 
captive corals includes handling, cleaning, maintaining water quality 
within an acceptable range, extracting tissue samples for the purposes 
of diagnosis of condition or genetics, treating of maladies such as 
disease or parasites using established methods proven to be effective, 
propagating corals by sexual or asexual means (i.e., fragmenting larger 
coral colonies into smaller colonies to increase the number of corals, 
maintain corals of manageable size, or accelerate their growth rate) 
within the bounds of normal husbandry practices, attaching to 
artificial surfaces, and removing dead skeleton;
    (6) Interstate and intrastate transportation of legally-obtained 
captive pillar coral and pillar coral parts provided it is not in the 
course of a commercial activity. If captive corals or pillar coral 
parts are to be moved to a different holding location, records 
documenting transfer of corals must be maintained;
    (7) Stabilization of loose pillar coral, including fragments, in 
the wild by experienced individuals and as authorized by a 10(a)(1)(A) 
permit issued by NMFS;
    (8) Relocation of wild pillar coral from one site to another under 
the authorization of an ESA section 10(a)(1)(A) permit issued by NMFS;
    (9) Use of captive pillar coral for scientific studies under the 
authorization of an ESA Section 10(a)(1)(A) permit issued by NMFS. 
Scientific studies that have the potential to injure or harm captive 
pillar coral (e.g., altered temperature outside of ideal range, 
exposure to contaminants, potentially harmful chemicals, or disease, 
introduction of coral predators) require an ESA section 10(a)(1)(A) 
permit. Scientific studies that are intended to improve the husbandry 
practices of caring for captive pillar coral, where there is a 
reasonable

[[Page 59500]]

expectation that they would not cause harm to pillar coral (e.g., 
trialing new food supplements, comparing different lighting systems, 
testing different attachment substrates), would not require an ESA 
permit;
    (10) Research activities on pillar coral in the wild under the 
authorization of an ESA section 10(a)(1)(A) permit. Research 
activities, such as observational studies, on pillar coral in the wild 
that do not involve collections of pillar corals or manipulation of 
pillar corals or of their environment do not require an ESA section 
10(a)(1)(A) permit;
    (11) Release of captive pillar coral into the wild, as authorized 
by an ESA section 10(a)(1)(A) permit issued by NMFS; and
    (12) Treatment of wild pillar coral for disease by experienced 
individuals using non-experimental methods proven to be effective and 
as authorized by state and territorial permits.

Information Quality Act and Peer Review

    In December 2004, the Office of Management and Budget (OMB) issued 
a Final Information Quality Bulletin for Peer Review establishing 
minimum peer review standards, a transparent process for public 
disclosure of peer review planning, and opportunities for public 
participation. The OMB Peer Review Bulletin (the Bulletin), implemented 
under the Information Quality Act (Pub. L. 106-554), is intended to 
enhance the quality and credibility of the Federal Government's 
scientific information, and applies to influential or highly 
influential scientific information disseminated on or after June 16, 
2005. To satisfy our requirements under the Bulletin, this proposed 
rule was subject to peer review. A peer review plan was posted on the 
NOAA peer review agenda and can be found at the following website: 
https://www.noaa.gov/information-technology/endangered-species-act-proposed-rule-for-pillar-coral-dendrogyra-cylindrus-id432. Our 
synthesis and assessment of scientific information supporting this 
proposed action was peer reviewed via individual letters soliciting the 
expert opinions of three qualified specialists selected from the 
academic and scientific community. The charge to the peer reviewers and 
the peer review report have been placed in the administrative record 
and posted on the agency's peer review agenda. In meeting the OMB Peer 
Review Bulletin requirements, we have also satisfied the requirements 
of the 1994 joint U.S. Fish and Wildlife Service/NMFS peer review 
policy (59 FR 34270; July 1, 1994).

Public Comments Solicited

    To ensure that any final action resulting from this proposal will 
be as accurate and effective as possible, we are soliciting comments 
from the public, other concerned governmental agencies, the scientific 
community, industry, and any other interested parties. We must base our 
final determination on the best available scientific and commercial 
data when making listing determinations. We cannot, for example, 
consider the economic effects of a listing determination. Final 
promulgation of any regulation on this species or withdrawal of this 
listing proposal will take into consideration the comments and any 
additional information we receive, and such communications may lead to 
a final regulation that differs from this proposal or result in a 
withdrawal of this reclassification proposal.

Public Hearing

    A public hearing will be conducted online as a virtual meeting, as 
specified under ADDRESSES. More detailed instructions for joining the 
virtual meeting are provided on our web page: https://www.fisheries.noaa.gov/species/pillar-coral#conservation-management. 
The hearing will begin with a brief presentation by NMFS that will give 
an overview of the proposed rule under the ESA. After the presentation, 
but before public comments, there will be a question-and-answer session 
during which members of the public may ask NMFS staff clarifying 
questions about the proposed rule. Following the question-and-answer 
session, members of the public will have the opportunity to provide 
oral comments on the record regarding the proposed rule. In the event 
there is a large attendance, the time allotted per individual for oral 
comments may be limited. Therefore, anyone wishing to make an oral 
comment at the public hearing for the record is also encouraged to 
submit a written comment during the relevant public comment period as 
described under ADDRESSES and DATES. All oral comments will be 
recorded, transcribed, and added to the public comment record for this 
proposed rule.

References

    A complete list of the references used in this proposed rule is 
available online (see www.fisheries.noaa.gov/species/pillar-coral#conservation-management) and upon request (see FOR FURTHER 
INFORMATION CONTACT).

Classification

National Environmental Policy Act

    The 1982 amendments to the ESA, in section 4(b)(1)(A), restrict the 
information that may be considered when assessing species for listing. 
Based on this limitation of criteria for a listing decision and NOAA 
Administrative Order 216-6 (Environmental Review Procedures for 
Implementing the National Environmental Policy Act), we have concluded 
that ESA listing actions are not subject to requirements of the 
National Environmental Policy Act.

Executive Order 12866, Regulatory Flexibility Act, and Paperwork 
Reduction Act

    As noted in the Conference Report on the 1982 amendments to the 
ESA, economic impacts cannot be considered when assessing the status of 
a species. Therefore, the economic analysis requirements of the 
Regulatory Flexibility Act are not applicable to the listing process. 
In addition, this proposed rule is exempt from review under Executive 
Order 12866. This proposed rule does not contain a collection-of-
information requirement for the purposes of the Paperwork Reduction 
Act.

Executive Order 13132, Federalism

    In accordance with E.O. 13132, we have made a preliminary 
determination that this proposed rule does not have significant 
federalism effects and that a federalism assessment is not required. In 
keeping with the intent of the Administration and Congress to provide 
continuing and meaningful dialogue on issues of mutual state and 
Federal interest, this proposed rule will be given to the relevant 
state agencies in each state in which the species is believed to occur, 
and those states will be invited to comment on this proposal. As we 
proceed, we intend to continue engaging in informal and formal contacts 
with the state, and other affected local or regional entities, giving 
careful consideration to all written and oral comments received.

Executive Order 12898, Environmental Justice

    Executive Order 12898 requires that Federal actions address 
environmental justice in the decision-making process. In particular, 
the environmental effects of the actions should not have a 
disproportionate effect on minority and low-income communities. This 
proposed rule is not expected to have a disproportionately high effect 
on minority populations or low-income populations.

[[Page 59501]]

List of Subjects

50 CFR Part 223

    Endangered and threatened species, Exports, Imports, 
Transportation.

50 CFR Part 224

    Administrative practice and procedure, Endangered and threatened 
species, Exports, Imports, Reporting and recordkeeping requirements, 
Transportation.

    Dated: August 14, 2023.
Samuel D. Rauch, III,
Deputy Assistant Administrator for Regulatory Programs, National Marine 
Fisheries Service.
    For the reason set out in the preamble, NMFS proposes to amend 50 
CFR parts 223 and 224 as follows:

PART 223--THREATENED MARINE AND ANADROMOUS SPECIES

0
1. The authority citation for part 223 continues to read as follows:

    Authority:  16 U.S.C. 1531-1543; subpart B, Sec.  223.201-202 
also issued under 16 U.S.C. 1361 et seq.; 16 U.S.C. 5503(d) for 
Sec.  223.206(d)(9).

0
2. In Sec.  223.102, amend the table in paragraph (e), under the 
subheading ``Corals'', by removing the entry for ``Coral, pillar 
(Dendrogyra cylindrus)''.

PART 224--ENDANGERED MARINE AND ANADROMOUS SPECIES

0
3. The authority citation of part 224 continues to read as follows:

    Authority:  16 U.S.C. 1531-1543 and 16 U.S.C. 1361 et seq.

0
4. In Sec.  224.101, amend the table in paragraph (h), under the 
subheading ``Corals'', by adding the following entry to read as 
follows:


Sec.  224.101  Enumeration of endangered marine and anadromous species.

* * * * *
    (h) The endangered species under the jurisdiction of the Secretary 
of Commerce are:

----------------------------------------------------------------------------------------------------------------
                          Species \1\
---------------------------------------------------------------    Citation(s) for      Critical
                                                Description of         listing           habitat      ESA rules
         Common name          Scientific name   listed entity     determination(s)
----------------------------------------------------------------------------------------------------------------
 
                                                  * * * * * * *
           Corals
Coral, pillar...............  Dendrogyra       Entire species.  [Insert FR Citation            NA            NA
                               cylindrus.                        & Date When
                                                                 Published As A
                                                                 Final Rule].
 
                                                  * * * * * * *
----------------------------------------------------------------------------------------------------------------
\1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement,
  see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56
  FR 58612, November 20, 1991).


[FR Doc. 2023-17769 Filed 8-28-23; 8:45 am]
BILLING CODE 3510-22-P