Proposed Rule2021-27631
Endangered and Threatened Wildlife and Plants; Removal of Johnson's Seagrass From the Federal List of Threatened and Endangered Species and Removal of the Corresponding Designated Critical Habitat
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Published
December 23, 2021
Issuing agencies
Commerce DepartmentNational Oceanic and Atmospheric Administration
Abstract
We, NMFS, propose to remove Johnson's seagrass (Halophila johnsonii) from the Federal List of Threatened and Endangered Species. To correspond with this action, we are also proposing to remove the critical habitat designation for Johnson's seagrass. We propose these actions based on newly obtained genetic data that demonstrate that Johnson's seagrass is not a unique taxon but rather a clone of an Indo- Pacific species, Halophila ovalis.
Full Text
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<title>Federal Register, Volume 86 Issue 244 (Thursday, December 23, 2021)</title>
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[Federal Register Volume 86, Number 244 (Thursday, December 23, 2021)]
[Proposed Rules]
[Pages 72908-72911]
From the Federal Register Online via the Government Publishing Office [<a href="http://www.gpo.gov">www.gpo.gov</a>]
[FR Doc No: 2021-27631]
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DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
50 CFR Parts 223 and 226
[Docket No. 211215-0260; RTID 0648-XR119]
Endangered and Threatened Wildlife and Plants; Removal of
Johnson's Seagrass From the Federal List of Threatened and Endangered
Species and Removal of the Corresponding Designated Critical Habitat
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, propose to remove Johnson's seagrass (Halophila
johnsonii) from the Federal List of Threatened and Endangered Species.
To correspond with this action, we are also proposing to remove the
critical habitat designation for Johnson's seagrass. We propose these
actions based on newly obtained genetic data that demonstrate that
Johnson's seagrass is not a unique taxon but rather a clone of an Indo-
Pacific species, Halophila ovalis.
DATES: Information and comments on the subject action must be received
by February 22, 2022.
ADDRESSES: You may submit comments on this document, identified by
NOAA-NMFS-2021-0117, by any of the following methods:
<bullet> Electronic Submission: Submit all electronic public
comments via the Federal e-Rulemaking Portal. Go to <a href="https://www.regulations.gov">https://www.regulations.gov</a> and enter NOAA-NMFS-2021-0117 in the Search box.
Click on the ``Comment'' icon, complete the required fields, and enter
or attach your comments.
<bullet> Mail: Submit written comments to Adam Brame, Protected
Resources Division, NMFS Southeast Regional Office, 263 13th Avenue
South, St. Petersburg, FL 33701.
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
<a href="http://www.regulations.gov">www.regulations.gov</a> 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: Adam Brame, NMFS Southeast Regional
Office, <a href="/cdn-cgi/l/email-protection#28694c4945066a5a49454d6846474949064f475e"><span class="__cf_email__" data-cfemail="99d8fdf8f4b7dbebf8f4fcd9f7f6f8f8b7fef6ef">[email protected]</span></a>, (727) 209-5958.
SUPPLEMENTARY INFORMATION:
Background
A small-statured seagrass species found within Florida's
southeastern coastal lagoon system was formally identified as Johnson's
seagrass (Halophila johnsonii) in 1980 (Eiseman and McMillan 1980).
Prior to this designation, it was often referred to as H. decipiens,
though it is most similar to the morphologically diverse Indo-Pacific
species, H. ovalis. Morphological and physiological variations were the
bases for its taxonomic identification as H. johnsonii. For example,
Johnson's seagrass was differentiated from other Atlantic Halophila
species by its smooth leaf margins, angle of the cross veins extending
from the midrib, and the lack of hairs on the blade surface (Eiseman
and McMillan 1980).
[[Page 72909]]
Johnson's seagrass grows in a variety of conditions within
Florida's intracoastal waters from Sebastian Inlet to Virginia Key in
Biscayne Bay. This is the smallest geographic distribution of any
seagrass worldwide. Within this range, it is among the least abundant
seagrass. It grows in small, sparse patches and may disappear from
areas for months or years before reappearing. It can co-occur with
other seagrasses, but its short stature precludes it from occurring
within dense stands of taller species because it is outcompeted for
light resources. Johnson's seagrass has a broader tolerance range for
light, temperature, and salinity than congeners and seems capable of
growing in suboptimal conditions where other species cannot survive.
Johnson's seagrass grows in the intertidal zone, on dynamic flood
deltas inside ocean inlets, at the mouths of freshwater discharge
canals, and subtidal waters to depths of approximately 3-4 meters.
Johnson's seagrass is dioecious, meaning each plant only contains
the flowers of one sex (male or female). Interestingly, no individual
Johnson's seagrass plants have been found with male flowers. Similarly,
researchers have not found any seedlings. These observations suggest
that Johnson's seagrass reproduces only through vegetative
fragmentation (asexual reproduction) and not through the development
and dispersal of seeds (sexual reproduction). This strategy likely
hinders its ability to expand in range or recolonize following
disturbances.
Given the extremely limited geographical distribution of Johnson's
seagrass (about 200 kilometers (km) of Florida coastline), its limited
reproductive potential (only asexual reproduction), and the variety of
threats that could affect survival, NMFS conducted a status review to
consider whether it should be added to the Federal List of Threatened
and Endangered Species. NMFS published a proposed rule to list the
species as threatened on September 15, 1993 (58 FR 48326), and a
proposed rule to designate critical habitat on August 4, 1994 (59 FR
39716). Additional research on the ecology of this species subsequently
became available and was considered in an updated status review, which
was completed in 1997. NMFS published a final rule listing Johnson's
seagrass as a threatened species in 1998 (63 FR 49035, September 14,
1998) and a final rule designating critical habitat in 2000 (65 FR
17786, April 5, 2000).
At the time of listing, the best available data indicated Johnson's
seagrass: (1) Had perhaps the smallest geographic range of any seagrass
species worldwide; (2) had a sparse, patchy distribution throughout its
range and an ability to survive in a variety of environmental
conditions; (3) lacked male flowers necessary for sexual reproduction
and therefore appeared to only reproduce asexually; and (4) was unique
from other North American Halophila species based on morphology,
physiological ecology, and genetic analyses. However, the 1997 status
review also indicated that more detailed studies were necessary to
evaluate the overall genetic structure and diversity of H. johnsonii.
This need was reiterated in the 2002 Johnson's Seagrass Recovery Plan.
A 1997 genetics study using randomly amplified primer DNA-
polymerase chain reactions (RAPD-PCR) indicated that genetic diversity
was higher than expected at one location within the range of Johnson's
seagrass (Jewitt-Smith et al. 1997). Yet this study relied on a limited
sample size, and a subsequent study using similar techniques indicated
very low genetic diversity within H. johnsonii as compared to the co-
occurring species, H. decipiens (Freshwater 1999). The low genetic
diversity was attributed to the lack of sexual reproduction. The
methodology used in assessing these Halophila samples did not provide
the resolution necessary to make species level conclusions about
phylogeny (history of the evolution of a species or group, including
relatedness within a group).
A molecular phylogenetic analysis of the genus Halophila using
internal transcribed spacer (ITS) regions of nuclear ribosomal DNA
indicated that H. johnsonii could not be distinguished from H. ovalis
and should be further researched (Waycott et al. 2002). Umichura (2008)
came to a similar conclusion and suggested that H. johnsonii and two
other Halophila species should be reclassified as the broadly
distributed H. ovalis. Short et al. (2010) used ITS regions of nuclear
ribosomal sequences and morphology to demonstrate that Halophila
samples from Antigua belonged to H. ovalis and were genetically
identical to H. johnsonii. Short et al. (2010) also found that
Halophila samples from both Antigua and the United States (previously
identified as H. johnsonii) fell within the range of morphological
characteristics diagnostic for H. ovalis, and particularly for H.
ovalis from east Africa. The outcomes of these studies raised more
questions about the taxonomy of Halophila species, particularly H.
johnsonii, given its unusually restricted geographic range, its limited
reproductive strategy, and its morphometric similarities to other Indo-
Pacific species of Halophila.
NMFS began funding projects to resolve the taxonomic uncertainty of
Johnson's seagrass in 2012. Waycott et al. (2015) used multiple genetic
approaches including microsatellite DNA and next generation sequencing
to detect single nucleotide polymorphisms (SNPs). Results of this work
indicated a complete lack of genetic diversity across the range of
Johnson's seagrass and through time, indicating all samples analyzed
were from a singular clone. Samples collected and analyzed from Antigua
contained the same genetic markers as samples from Florida, suggesting
these too were part of the same clone (Waycott et al. 2015) despite the
Antigua samples having been previously identified as H. ovalis (Short
et al. 2010). Finally, Waycott et al. (2015) genetically compared
samples from both Florida and Antigua with H. ovalis samples collected
throughout that species' range (Indo-Pacific). Results indicated all
samples, regardless of location or identification, had allelic overlap
(same gene variations) at 6 of 10 microsatellite loci analyzed,
suggesting samples from the Atlantic originated from H. ovalis of the
Indo-Pacific. While this report provided further evidence that H.
johnsonii was not a unique taxon, SNP locations for H. ovalis had yet
to be verified for H. johnsonii samples and the report did not present
a comprehensive population genetic analysis of H. ovalis.
NMFS provided support for a follow-up study in 2017, published as
Waycott et al. (2021). This study expanded previous efforts with the
intent of solidifying the methods and providing a robust conclusion
regarding the taxonomic uncertainty within the H. ovalis complex. The
study used multiple methodological approaches and created molecular
data sets for samples of both H. johnsonii and H. ovalis collected
throughout the range of each species. Phylogenetic analyses of 105
samples of Halophila spp. from 19 countries using plastid (17,999 base
pairs (bp)) and nuclear (6,449 bp) DNA sequences derived from hybrid
capture both resolved H. johnsonii within H. ovalis. A third
phylogenetic analysis using 48 samples from 13 populations identified
990 genome-wide SNPs (generated via double digest restriction-site
associated digest sequencing (ddRAD)) and also nested H. johnsonii
within H. ovalis. All three phylogenetic analyses indicated H.
johnsonii samples were most similar to H. ovalis samples from Antigua
and east Africa.
[[Page 72910]]
Waycott et al. (2021) also assessed population-level differences
using both the genome-wide SNPs (990) developed in the phylogenetic
analysis (47 of the 48 samples from 13 populations) and microsatellites
(294 samples at 10 microsatellite loci). Cluster analysis indicated
three populations within the H. ovalis complex, with H. johnsonii being
part of the Indo-Pacific/Atlantic clade. Other results demonstrated
genetic uniformity of all 132 H. johnsonii samples, indicating a
complete lack of genetic diversity that is consistent with clonal
(asexual) reproduction and a single colonization event. These same 132
samples and the 12 H. ovalis samples from Antigua shared a single
multilocus genotype at all nine comparable microsatellite loci.
Furthermore, all 12 H. johnsonii samples and the single H. ovalis
sample from Antigua genotyped with ddRAD loci shared the same
multilocus genotype. In contrast, other H. ovalis populations, such as
those from Australia, generally had multiple multilocus genotypes and
substantial genetic diversity, indicating that the genetic markers
would have detected differences if they were present. The population-
level analyses indicate that H. johnsonii is genetically
indistinguishable from H. ovalis, clustering with samples from Antigua
and east Africa.
Collectively, the Waycott et al. (2021) study concludes that the
entire range of H. johnsonii is a single clone of a morphological
variant of the Indo-Pacific species, H. ovalis. While previous studies
suggested a genetic similarity between the two species, they were
unable to definitively clarify the taxonomy. In Waycott et al. (2021),
the use of multiple, highly variable, co-dominant genetic markers
resolved genetic relationships more clearly than previous studies,
which used low variation and/or dominant genetic markers.
NMFS solicited the assistance of the NOAA Genetics Group to review
Waycott et al. (2021). Four reviewers determined that the laboratory
and statistical methods used by Waycott et al. (2021) were appropriate
and sufficient to support the authors' conclusions. They noted that
multiple independent genetic analyses confirmed that H. johnsonii nests
within H. ovalis, with the greatest similarity to Antigua and East
Africa samples. The reviewers agreed that the research provided in
Waycott et al. (2021) constitutes the best available scientific (in
this case, genetic) information on the taxonomy of Johnson's seagrass.
They confirmed that the concordance of the results from multiple
genetic data types and across complementary analytic methods provides
strong support for the conclusion that H. johnsonii is genetically
indistinguishable from H. ovalis. The reviewers agreed with the
conclusion of the authors that ``lack of genetic diversity and the
absence of sexual reproduction strongly indicate that the total range
of H. johnsonii is actually one clone that is closely related to H.
ovalis populations in Africa and Antigua . . .'' They found this
conclusion was further supported by the complete absence of male H.
johnsonii plants, which suggests that it consists of a single female
clone.
Basis for Determination
Section 3 of the Endangered Species Act (ESA) defines the term
``species'' as any subspecies of fish or wildlife or plants, and any
distinct population segment of any species of vertebrate fish or
wildlife which interbreeds when mature. Pursuant to implementing
regulations in 50 CFR 424.11(a), in determining whether a particular
taxon or population is a species under the ESA, we rely on standard
taxonomic distinctions as well as our biological expertise and that of
the scientific community concerning the relevant taxonomic group.
Under section 4(c)(1) and 4(c)(2) of the ESA, the Secretary is
required to periodically review and revise the Federal List of
Endangered and Threatened Species and consider, among other things,
whether a species' listing status should be changed, including whether
the species should be removed from the list. Pursuant to implementing
regulations for the ESA at 50 CFR 424.11(e)--the Secretary shall delist
a species if, after conducting a status review based on the best
scientific and commercial data available, the Secretary determines: (1)
The species is extinct; (2) the species does not meet the definition of
an endangered species or threatened species; or (3) the listed entity
does not meet the statutory definition of a species. When conducting a
status review, if we determine the entity under review does not meet
the statutory definition of a species, the status review would conclude
at that point without further evaluation because we can only list
entities that qualify as species under the ESA. In this case, our
status review is our assessment of the best scientific and commercial
data available as presented in this proposed rule, which supports the
determination that Johnson's seagrass does not meet the statutory
definition of a species. Therefore, our status review concluded without
a re-assessment of the five listing factors. As presented in Waycott et
al. (2021) and independently confirmed by four expert reviewers from
the NOAA Genetics Group, the results of extensive genetic and
phylogenetic analyses indicate H. johnsonii is a single clone of a
morphological variant of H. ovalis, and therefore, is not a unique
species.
We find the best scientific and commercial data available
demonstrate that H. johnsonii is not a unique taxon but rather a
morphological variant of H. ovalis, and thus is not a species eligible
for listing under the ESA. Therefore, we propose to remove H. johnsonii
from the Federal List of Threatened and Endangered Species.
Effects of the Determination
If we delist H. johnsonii then the protections of the ESA would no
longer apply to it. Since critical habitat can only be designated for
species listed under the ESA, delisting H. johnsonii would also trigger
the need to remove the currently designated critical habitat, as we
propose in this rule. Delisting H. johnsonii and removal of the
designated critical habitat are specific to the ESA and would have no
effect on other Federal, state, county, or local seagrass protections
that may be in place. In addition, because H. ovalis is not listed as
an endangered species or threatened species under the ESA, our proposed
delisting of H. johnsonii would have no effect on the status of H.
ovalis.
Per the joint NMFS-U.S. Fish and Wildlife Service Post-Delisting
Monitoring Plan Guidance (2008, updated in 2018), the post-delisting
monitoring requirements of section 4(g) of the ESA apply without
exception to all species delisted due to biological recovery, but do
not pertain to species delisted for other reasons, such as taxonomic
revision. Based on this reasoning, there is no need for a post-
delisting monitoring plan for H. johnsonii.
References Cited
The complete citations for the references used in this document can
be obtained by contacting NMFS (See ADDRESSES and FOR FURTHER
INFORMATION CONTACT).
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
[[Page 72911]]
participation. The OMB Peer Review 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 the requirements under the OMB Peer Review Bulletin, the
Waycott et al. (2021) manuscript was subjected to peer review in
accordance with the Bulletin. Our proposed action relies upon new
information within the manuscript, which we consider ``influential
scientific information.'' While the manuscript was published in the
peer-reviewed journal Frontiers in Marine Science, and peer reviewed by
that journal prior to publication, we also peer reviewed the
manuscript. We established a peer review plan that consisted of
subjecting the manuscript to review by a panel of four expert reviewers
identified by NOAA's Genetics Group. The peer review plan, which
included the charge statement to the peer reviewers, and the resulting
peer review report are posted on the NOAA peer review agenda at:
<a href="https://www.noaa.gov/organization/information-technology/peer-review-plans">https://www.noaa.gov/organization/information-technology/peer-review-plans</a>. In meeting the OMB Peer Review Bulletin requirements, we have
also satisfied the requirements of the 1994 joint U.S. Fish and
Wildlife Service and NMFS peer review policy (59 FR 34270, July 1,
1994).
Classification
National Environmental Policy Act (NEPA)
The 1982 amendments to the ESA, in section 4(b)(1)(A), restrict the
information that may be considered when assessing species for listing
to the best scientific and commercial data available. Based on this
limitation of criteria for a listing decision and the opinion in
Pacific Legal Foundation v. Andrus, 657 F. 2d 829 (6th Cir. 1981), we
have concluded that NEPA does not apply to ESA listing actions. (See
NOAA Administrative Order 216-6A and the Companion Manual for NOAA
Administrative Order 216-6A, regarding Policy and Procedures for
Compliance with the National Environmental Policy Act and Related
Authorities).
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
E.O. 13132 requires agencies to take into account any federalism
impacts of regulations under development. It includes specific
consultation directives for situations where a regulation will preempt
state and local law, or impose substantial direct compliance costs on
state and local governments (unless required by statute). Neither of
these circumstances is applicable to this proposed rule.
List of Subjects
50 CFR Part 223
Threatened marine and anadromous species.
50 CFR Part 226
Designated critical habitat.
Dated: December 16, 2021.
Samuel D. Rauch, III,
Deputy Assistant Administrator for Regulatory Programs, National Marine
Fisheries Service.
For the reasons set out in the preamble, 50 CFR part 223 and part
226 are proposed to be amended 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).
Sec. 223.102 [Amended]
0
2. In Sec. 223.102, in the table in paragraph (e), under the
subheading ``Marine Plants'', remove the entry for ``Seagrass,
Johnson's (Halophila johnsonii)''.
PART 226--DESIGNATED CRITICAL HABITAT
0
3.The authority citation for part 226 continues to read as follows:
Authority: 16 U.S.C. 1533.
Sec. 226.213 [Removed and Reserved]
0
4. Remove and reserve Sec. 226.213.
[FR Doc. 2021-27631 Filed 12-22-21; 8:45 am]
BILLING CODE 3510-22-P
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