[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
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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