[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 [www.gpo.gov]
[FR Doc No: 2021-27631]


=======================================================================
-----------------------------------------------------------------------

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.

-----------------------------------------------------------------------

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:
     Electronic Submission: Submit all electronic public 
comments via the Federal e-Rulemaking Portal. Go to https://www.regulations.gov 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.
     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 
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: Adam Brame, NMFS Southeast Regional 
Office, [email protected], (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: 
https://www.noaa.gov/organization/information-technology/peer-review-plans. 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