Injurious Wildlife Species; Listing Salamanders Due to Risk of Salamander Chytrid Fungus, 2170-2221 [2024-31203]

Agencies

• Fish and Wildlife Service
• DEPARTMENT OF THE INTERIOR

[Federal Register Volume 90, Number 6 (Friday, January 10, 2025)]
[Rules and Regulations]
[Pages 2170-2221]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2024-31203]



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Vol. 90

Friday,

No. 6

January 10, 2025

Part III





 Department of the Interior





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Fish and Wildlife Service





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50 CFR Part 16





Injurious Wildlife Species; Listing Salamanders Due to Risk of 
Salamander Chytrid Fungus; Final Rule

Federal Register / Vol. 90, No. 6 / Friday, January 10, 2025 / Rules 
and Regulations

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DEPARTMENT OF THE INTERIOR

Fish and Wildlife Service

50 CFR Part 16

RIN 1018-BA77
[Docket No. FWS-HQ-FAC-2015-0005; FXFR13360900000-245-FF09F14000]


Injurious Wildlife Species; Listing Salamanders Due to Risk of 
Salamander Chytrid Fungus

AGENCY: Fish and Wildlife Service, Interior.

ACTION: Affirmation of interim rule as final; second interim rule and 
request for public comment.

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SUMMARY: The U.S. Fish and Wildlife Service is affirming as final the 
2016 interim rule that added all species of salamanders from 20 genera 
to the list of injurious amphibians. Under the injurious wildlife 
prohibitions of the Lacey Act, this final rule prohibits the 
importation into the United States and shipment between the continental 
United States, District of Columbia, Hawaii, Commonwealth of Puerto 
Rico, or any territory or possession of the United States of any live 
or dead specimen, including hybrids and parts, of those 20 genera of 
salamanders, except by permit for certain purposes or by Federal 
agencies solely for their own use. In addition to finalizing the 
listing of those 20 genera, we are publishing a new interim rule to add 
to the injurious amphibian list 16 genera that recent studies 
determined are also carriers of the fungus and to clarify some 
provisions from the final rule. This interim rule includes any live or 
dead specimen, hybrid, or parts of the 16 genera and opens a public 
comment period. We take these actions to protect U.S. ecosystems from 
the introduction, establishment, and spread of the lethal chytrid 
fungus Batrachochytrium salamandrivorans, which infects and is carried 
by salamanders, and which is not yet known to be found in the United 
States.

DATES: Effective date: The interim rule published at 81 FR 1534 on 
January 13, 2016, was effective January 28, 2016. This final rule 
affirming the January 13, 2016, interim rule and the interim rule set 
forth in this document are effective January 25, 2025.
    Comment submission: Interested persons are invited to submit 
written comments on the issues raised in the second interim rule as 
described below under Information Requested on or before March 11, 
2025.

ADDRESSES: Comment submission: You may submit comments by one of the 
following methods:
    (1) Electronically: Go to the Federal eRulemaking Portal: https://www.regulations.gov. In the Search box, enter FWS-HQ-FAC-2015-0005, 
which is the docket number for this action. You may submit a comment by 
clicking on ``Comment.''
    (2) By hard copy: Submit by U.S. mail to: Public Comments 
Processing, Attn: FWS-HQ-FAC-2015-0005, U.S. Fish and Wildlife Service, 
MS: PRB/3W, 5275 Leesburg Pike, Falls Church, VA 22041-3803.
    We request that you send comments only by the methods described 
above. We will post all comments on https://www.regulations.gov. This 
generally means that we will post any personal information you provide 
us (see Information Requested, below, for more information).
    Supplementary materials: Background documents related to this 
rulemaking action, including the final economic analysis for the 
affirmation of the 2016 interim rule, are available at https://www.regulations.gov in Docket No. FWS-HQ-FAC-2015-0005.

FOR FURTHER INFORMATION CONTACT: Kristen Sommers, Injurious Wildlife 
Listing Coordinator, U.S. Fish and Wildlife Service, Branch of Aquatic 
Invasive Species; MS: FAC; 5275 Leesburg Pike; Falls Church, VA 22041-
3803; 571-329-2214. Individuals in the United States who are deaf, 
deafblind, hard of hearing, or have a speech disability may dial 711 
(TTY, TDD, or TeleBraille) to access telecommunications relay services. 
Individuals outside the United States should use the relay services 
offered within their country to make international calls to the point-
of-contact in the United States.

SUPPLEMENTARY INFORMATION: 

Table of Contents

I. Executive Summary
II. Current Rulemaking Action
III. Final Rule to the 2016 Interim Rule
    A. Background
    B. Summary of Comments Received on the 2016 Interim Rule
    C. Affirmation of the 2016 Interim Rule
    D. Required Determinations
IV. Second Interim Rule
    A. Species Information for Salamanders
    B. Species Information for Batrachochytrium salamandrivorans
    C. Population-Level and Ecosytem-Level Effects of Bsal
    D. Invasiveness of Salamanders and Bsal
    E. Pathway Analysis
    F. Risk Assessments of Bsal
    G. Factors That Contribute to Injuriousness of Salamanders
    H. Measures That Reduce or Remove Injuriousness of Salamanders
    I. Summary and Conclusion for Interim Rule
    J. Required Determinations
    K. Information Requested

I. Executive Summary

    Why we need to publish a rule. We, the U.S. Fish and Wildlife 
Service (Service or FWS), are charged with administering 18 U.S.C. 
42(a), as amended (commonly known as the injurious wildlife provision 
of the Lacey Act). Under this authority, the Secretary of the Interior 
may list by regulation those wild mammals, wild birds, fish, mollusks, 
crustaceans, amphibians, reptiles, and the offspring or eggs of any of 
the foregoing that are injurious to human beings, to the interests of 
agriculture, horticulture, or forestry, or to the wildlife or wildlife 
resources of the United States.
    We have determined that salamanders that can carry the fungus 
Batrachochytrium salamandrivorans (Bsal) are injurious to wildlife and 
wildlife resources of the United States. This determination was based 
on a review of the literature and an evaluation under the criteria for 
injuriousness by the Service. The purpose of listing these species as 
injurious wildlife is to prevent the introduction, establishment, and 
spread of Bsal in the wild in the United States. The fungus primarily 
affects salamanders, has lethal effects on many salamander species, and 
is not yet known to be found in ecosystems of the United States.
    What this document does. This document serves two purposes: It 
finalizes a rulemaking action initiated with publication of an interim 
rule in 2016, and it promulgates a new and related interim rule.
    On January 13, 2016, we published an interim rule that amended our 
regulations pertaining to injurious wildlife (81 FR 1534). That interim 
rule (hereafter referred to as ``the 2016 interim rule'') amended our 
regulations to add all species of salamanders from 20 genera, of which 
there were 201 species, to the list of injurious amphibians. Under the 
injurious wildlife prohibitions of the Lacey Act, the 2016 interim rule 
prohibited both importation into the United States and interstate 
transportation between States, the District of Columbia, the 
Commonwealth of Puerto Rico, or any territory or possession of the 
United States (the latter was clarified by a court decision in 2017) of 
any live or dead specimen, including parts, of these 20 genera of 
salamanders, except by permit

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for zoological, educational, medical, or scientific purposes (in 
accordance with permit conditions) or by Federal agencies without a 
permit solely for their own use.
    A second interim rule is now needed because of recent studies 
documenting additional genera that also share the same traits that make 
them injurious as carriers of Bsal. We are also revising some 
provisions from the 2016 interim rule in the final rule to make minor 
corrections to and improve clarity of the rule.
    The basis for our action. Defensible scientific evidence indicates 
that we need to list a total of 36 genera of salamanders as injurious 
wildlife to protect U.S. ecosystems. Therefore, we hereby affirm the 
injurious wildlife listings in the 2016 interim rule of all species in 
the following 20 genera: Chioglossa, Cynops, Euproctus, Hydromantes, 
Hynobius, Ichthyosaura, Lissotriton, Neurergus, Notophthalmus, 
Onychodactylus, Paramesotriton, Plethodon, Pleurodeles, Salamandra, 
Salamandrella, Salamandrina, Siren, Taricha, Triturus, and 
Tylototriton. We also add new injurious wildlife listings of all 
species in the following 16 genera through the second interim rule: 
Ambystoma, Andrias, Aneides, Aquiloeurycea, Calotriton, 
Chiropterotriton, Cryptobranchus, Desmognathus, Ensatina, Eurycea, 
Laotriton, Ommatotriton, Pachytriton, Proteus, Pseudobranchus, and 
Pseudotriton.
    The United States has the greatest diversity of salamanders in the 
world, salamanders are a vital part of native ecosystems, and numerous 
salamander populations are at risk of endangerment from Bsal. A risk 
assessment conducted by the U.S. Geological Survey (USGS) concluded 
that the potential for Bsal introduction into the United States is 
high, the United States has suitable conditions for Bsal survival, and 
the consequences of introduction into the United States are expected to 
be severe and occur across a wide geographic range within the United 
States. The most likely pathway of Bsal into the United States would be 
on the bodies of salamanders in the commercial salamander trade. Aside 
from our Bsal regulations, the ability and effectiveness of measures to 
prevent or control Bsal is currently low. Trade in wildlife occurs on a 
global scale, and amphibians are one of the most commonly traded 
animals.
    Therefore, listing the genera as determined in this rulemaking 
action will help to reduce the likelihood that Bsal enters the United 
States and presents a threat to native salamander species.

II. Current Rulemaking Action

    This document does the following:
     Affirms the current listing of 20 genera of salamanders as 
injurious species by the 2016 interim rule as described above and any 
species within those genera.
     Revises provisions in the preamble of the 2016 interim 
rule in response to a court decision that pertained to interstate 
transport of injurious wildlife as described below.
     Removes the 201 itemized species names from the list in 50 
CFR 16.14. This itemized list of scientific and common names is 
unnecessary because the regulations in 50 CFR 16.14(a) state that the 
prohibitions pertain to the 20 genera ``including but not limited to, 
the species listed in this paragraph.'' We provided the itemized list 
of species in the 2016 interim rule largely for the convenience of the 
public and our law enforcement staff, but the taxonomy of salamanders 
is evolving, and the list is not static. However, while many scientific 
and common names have changed, all of the listed species remain in 
their same genera.
     Clarifies prohibitions pertaining to hybrids and frozen 
specimens; clarifies what is not prohibited (including eggs or gametes; 
parts or tissues that have been chemically preserved, chemically 
treated, or heat treated so that the pathogen Batrachochytrium 
salamandrivorans, if present, is rendered non-viable; and molecular 
specimens consisting of only the nucleic acids from organisms).
     Adds 16 genera to the list in 50 CFR 16.14(a), as 
explained below, and solicits comments on these new genera.

III. Final Rule to the 2016 Interim Rule

A. Background

    On January 13, 2016, under the authority of 18 U.S.C. 42(a)(1), as 
amended, we, the U.S. Fish and Wildlife Service, published an interim 
rule in the Federal Register (81 FR 1534) to add all species from 20 
genera to the list of injurious amphibians and announced the 
availability of the draft economic analysis and the draft environmental 
assessment of the 2016 interim rule. The rule took effect on January 
28, 2016, and revised the lists of injurious wildlife in part 16 of 
title 50 of the Code of Federal Regulations (CFR), specifically the 
list of injurious amphibians at 50 CFR 16.14. The 60-day public comment 
period closed on March 14, 2016. We solicited comments and supporting 
data to gain additional information. We also solicited peer review at 
the same time.
    In this document, we present our consideration of the public 
comments and peer review received on the 2016 interim rule to inform 
our final determinations. We present a summary of the peer-review 
comments and the public comments and our responses to them in the 
``Summary of Comments Received on the 2016 Interim Rule'' portion of 
the preamble to this final rule. The comments did not provide any 
substantive evidence that supported changing the genera in the interim 
rule. However, some comments did provide justification for modifying 
certain requirements stipulated in the 2016 interim rule.
    The Service published an interim rule in 2016 instead of issuing a 
proposed rule for the listing under the Administrative Procedure Act 
(APA) (5 U.S.C. 551 et seq.). As explained in the 2016 interim rule, we 
had good cause to forgo notice and public comment on a proposed rule 
and instead take immediate action in the form of an interim rule to 
help prevent the fungus Bsal from being introduced, established, or 
spread in the United States for the reasons listed above. The fungus, 
lethal to many salamander species in the United States, is carried on 
the skin of salamanders and can be unintentionally imported by 
salamanders in trade. The 2016 interim listing of the 20 genera of 
salamanders has prohibited the importation of high-risk species under 
the injurious wildlife prohibitions of the Lacey Act, and the fungus 
has remained absent from the United States.
    In this document, a clarification from the 2016 interim rule 
reflects a court decision in 2017. Under the D.C. Circuit Court of 
Appeals decision in United States Association of Reptile Keepers, Inc. 
v. Zinke, 852 F.3d 1131 (D.C. Cir. 2017), import of injurious wildlife 
into the United States remains prohibited. In addition, transport of 
injurious wildlife between the enumerated jurisdictions in the shipment 
clause of 18 U.S.C. 42(a) (the continental United States, the District 
of Columbia, Hawaii, the Commonwealth of Puerto Rico, and any territory 
or possession of the United States) remains prohibited. However, the 
court held that 18 U.S.C. 42(a) does not prohibit interstate movement 
between States within the continental United States. This means that 
transportation of injurious wildlife between the 49 States within the 
continental United States (the contiguous 48 States and Alaska) is not 
prohibited by the statute, unless that movement of the wildlife is 
restricted due to conditions associated with issued injurious wildlife 
permits. We note that transport from the lower 48 States to

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Alaska through Canada, or vice versa, remains prohibited, because that 
transport includes an import into the United States.
    The language in 50 CFR 16.14(a) was, and still is, correct in that 
it does not prohibit interstate transport between States within the 
continental United States. The final economic analysis affirming the 
2016 interim rule reflects the clarification of interstate transport 
authority between States within the continental United States since the 
court decision on April 7, 2017. However, injurious wildlife unlawfully 
imported into the United States or transported between the enumerated 
jurisdictions is still unlawful to transport within the continental 
United States. Under the Lacey Act amendments of 1981, 16 U.S.C. 
3372(a)(1), it is unlawful for any person to import, export, transport, 
sell, receive, acquire, or purchase any wildlife transported in 
violation of any law of the United States. This includes transport of 
any injurious wildlife imported into the United States or transported 
between the enumerated jurisdictions in violation of 18 U.S.C. 42.

B. Summary of Comments Received on the 2016 Interim Rule

    The following comments were submitted during the peer and public 
comment period for the 2016 interim rule. Knowledge about Bsal has 
improved since then due to the many excellent studies by researchers 
and our own understanding of the disease. In the following responses to 
the comments under Peer Review Summary and Public Comments Summary, 
respectively, we have endeavored to answer the comments both as they 
related to the knowledge of Bsal, trade, and related issues at the time 
of the 2016 interim rule and as of the current knowledge as 
appropriate. The current knowledge from recent research affirms the 
2016 interim rule, supports the second interim rule set forth in this 
document, and can be found below in IV. Second Interim Rule. In our 
responses to the comments, when we refer to ``this rule,'' we mean that 
the information and the changes apply both to the final rule for the 
2016 interim rule and the second interim rule.
Peer Review Comments and Our Responses
    In accordance with peer review guidance of the Office of Management 
and Budget ``Final Information Quality Bulletin for Peer Review,'' 
released December 16, 2004, we solicited expert opinion on information 
contained in the 2016 interim rule from three knowledgeable individuals 
selected from specialists in the relevant taxonomic group and 
ecologists with scientific expertise that includes familiarity with 
alien herpetological introductions and invasions, predictive tools for 
risk assessment, and invasion biology. We posted our peer review plan 
on the Service's Science website (https://www.fws.gov/media/peer-review-plan-listing-salamanders-injurious-due-risk-salamander-chytrid-fungus), explaining the peer review process and providing the public 
with an opportunity to comment on the peer review plan. No comments 
were received regarding the peer review plan. The Service solicited 
independent scientific reviewers who submitted individual comments in 
written form. We avoided using individuals who had already expressed 
strong support for or opposition to the subject and individuals who 
were likely to experience personal gain or loss (such as financial or 
prestige) or otherwise could be perceived as having a conflict of 
interest as a result of the Service's decision. We received responses 
from three peer reviewers. A scientist with the USGS served as one of 
the peer reviewers.
    We requested that the reviewers provide comments that were specific 
to the 2016 interim rule and the draft economic analysis. We reviewed 
all comments for substantive issues and any new information they 
provided. We consolidated their comments (without attribute) and our 
responses into key issues in this section. Some peer reviewer comments 
that called for technical changes or more minor corrections have not 
been noted, but we have made our best effort to correct those 
grammatical or biological errors and clarify certain ambiguous 
statements in the second interim rule and supporting documents. We 
prepared the second interim rule and second draft economic analysis to 
reflect peer reviewer comments and new scientific information where 
appropriate.
    The comments we received indicated support for the 2016 interim 
rule and for the analysis that we conducted given the need to prevent 
harm to native species from Bsal. All three peer reviewers concluded 
that the data and analyses we used in the interim rule were appropriate 
and the conclusions we drew were logical and reasonable. All three peer 
reviewers provided additional insights (which we used to clarify points 
in the second interim rule) or references to recently published 
studies, which support the final rule. In general, the peer reviews 
supported the Service's conclusions and agreed that they were 
reasonable, though they did note that we generalized some of our 
findings, such as the average temperature of salamander habitats as an 
indicator of Bsal vulnerability with regards to salamanders nationwide. 
We have clarified these issues where practical in the second interim 
rule. The peer reviewers suggested that there was a need to expand our 
discussion regarding possible treatment options, which we have added to 
the second interim rule. The peer reviewers also acknowledged that, 
while the rule is important, research questions remain that could shed 
light on ways to better prevent the introduction of Bsal into the 
United States.
General Comments
    (PR1) Comment: In support of the 2016 interim rule, prevention 
provides an environmental and biodiversity benefit; the probability of 
introduction is at the very least reduced; and host species need not 
become established in the environment to transmit Bsal. If an owner 
houses multiple salamander species, transmission can occur in captivity 
to other species that may be able to establish a population in the 
wild. The commenter also agrees with the exclusion from the rule of 
tailless amphibians (frogs and toads), which were uniformly resistant 
in the tests by Martel et al. (2014).
    Response: We concur with the comments. At the time of the 2016 
interim rule publication, we lacked evidence of tailless amphibians as 
carriers, and this final rule simply affirms our findings on 
salamanders.
    (PR2) Comment: The average temperature of salamander habitats as an 
indicator of Bsal vulnerability with regard to salamanders nationwide 
would be difficult to defend. The rule provides a very broad average, 
and extrapolating it weakens the point.
    Response: We have clarified the rule under Bsal Risk Assessments in 
response to this comment to reflect more specifically the areas that 
the risk assessments identified as highest risk. We intended to 
demonstrate that most salamander species in the United States are not 
protected from Bsal by living outside of the Bsal optimal growth range 
or in areas beyond the threshold where Bsal can survive.
    (PR3) Comment: If time allowed, a few simple tests to improve the 
scientific foundation of the interim rule could have strengthened the 
decision to include or exclude species.
    Response: The Service is not a research agency, and we utilized

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available research when we found in 2016 that there was good cause to 
forgo notice and public comment on a proposed rule and instead take 
immediate action in the form of an interim rule to help prevent Bsal 
from being introduced, established, or spread in the United States. In 
this rule, we also utilize newly published or otherwise available 
research. In the years since the 2016 interim rule was published, many 
of the relevant studies affirmed our interim findings, while others 
support additional genera as documented in our second interim rule. 
None substantively contradicted our findings.
    (PR4) Comment: Given the long time that Bsal has been around (150 
years), the massive number of imported salamanders, and only recent 
characterization of Bsal, it may be possible that earlier Bsal was 
characterized as a related chytrid fungus, Batrachochytrium 
dendrobatidis (Bd).
    Response: As of the completion of this rule, resource managers, 
scientists and other researchers have been utilizing the latest 
scientific techniques to actively look for Bsal in nonresearch captive 
populations and in wild populations in the United States. The USGS 
conducted a massive sampling effort of 11,189 samples from 594 sites in 
223 counties within 35 U.S. States and 1 site in Mexico specifically 
for Bsal in wild populations (Waddle et al. 2020). The sites were 
chosen based on the species' susceptibility (including some frog 
species) and highest risk geographically. No Bsal was found. As of the 
completion of this rule, we are unaware of any positive Bsal detections 
in the wild. Testing of archived samples by other laboratories has been 
done, and no Bsal has been detected to our knowledge. The evidence is 
not conclusive that Bsal has never been in the wild in the United 
States, but there is no evidence that it has.
    (PR5) Comment: When the rule repeats the information about invasive 
species, the point should be made that, even if a salamander found to 
be injurious could not establish a population in the wild, an infected 
salamander in captivity can still transmit Bsal to native populations 
if that salamander escapes or if material touching it is disposed of 
improperly.
    Response: We agree and have incorporated the suggested language 
into the second interim rule.
    (PR6) Comment: The 2016 interim rule states that the main pathway 
for the global spread of Bsal is the international trade in salamanders 
and that the most likely pathway of a salamander that is a host to Bsal 
into the United States would include a pet store or online retailer. 
Since neither the United Kingdom or Germany Bsal outbreaks were related 
to a pet store or online retailer, the commenter recommends stating, 
``The most likely pathway of a salamander that is a host to Bsal into 
the United States would be the captive salamander commercial trade'' to 
cover the diverse salamander trade.
    Response: We have edited the second interim rule accordingly.
    (PR7) Comment: Given that Bd was probably introduced by release of 
laboratory animals as well as pets, institutional use of listed 
salamanders should also be regulated to protect U.S. ecosystems from 
Bsal.
    Response: This rule is intended to prevent the introduction of 
Bsal, whereas Bd was already widespread in the United States when that 
fungus was identified as the cause of major amphibian mortality. 
Importation of listed salamanders is regulated by this rule within the 
authorities under the injurious wildlife provisions of 18 U.S.C. 42. 
Any listed salamanders that are imported under a permit exception for 
zoological, educational, medical, or scientific purposes are required 
to observe sanitary procedures and double containment to prevent escape 
and are not allowed to be released. The Service may also establish 
additional permit conditions if deemed appropriate to ensure 
responsible use, maintenance, and containment of injurious wildlife 
specimens posing a risk of pathogen transfer and continued protection 
of the public interest and health, under 18 U.S.C. 42(a)(3) and the 
Service's permitting regulations in 50 CFR part 13 and part 16.
    (PR8) Comment: What is the citation for the statements, ``Based on 
scientific evidence, we know that the fungus is lethal to at least two 
salamander species native to the United States. Of the 190 native U.S. 
species, we find that at least 67 species are carriers and 20 are not 
carriers''?
    Response: Martel et al. 2014 was the source for the first sentence, 
and we used a combination of sources for information about native 
species and the testing that was done. We stated our sources and 
findings for these statements in the relevant sections in this rule.
Vulnerability and Carrier Status of Native Species
    (PR9) Comment: One of the considerations was that, even if a 
salamander listed by the 2016 interim rule could not establish a 
population in the wild, an infected salamander in captivity (or the 
water and soil in which it came into contact) can transmit Bsal to 
native populations. In addition to water and soil, how about if there 
is affected foliage or paper that was used in transit?
    Response: The commenter is correct that a variety of materials 
could become contaminated with fungal spores if in contact with 
infected salamanders. However, it is not possible to provide a complete 
list of these potential fomites (materials, such as water, that can act 
as passive carriers and can transfer pathogens) in the text of the 
rule. Rather, we believe that listing the salamander species that may 
be carriers of Bsal as injurious wildlife, thereby prohibiting the 
importation of potentially infected individuals, reduces the risk for 
pathogen spread by any substrate.
    (PR10) Comment: The considerations say that controlling Bsal is not 
practical. The peer reviewer recommends revising to note that, while 
there are control methods available for infected individual salamanders 
in captivity (Blooi et al. 2015a, 2015b), there are no practical 
control measures for free-ranging salamanders.
    Response: We agree with the comment. In the second interim rule, we 
clarify that, while treatment options exist that may help reduce the 
threat posed by Bsal for imported and captive-held specimens, those 
options have not been standardized and their effectiveness remains 
uncertain for large-scale application.
Pathways
    (PR11) Comment: The pathway by which Bsal spreads is unknown, 
except that water is involved. Thus, the States should be responsible 
for implementing measures on waterways that prevent the introduction of 
Bsal.
    Response: We agree that the U.S. States should be strong partners 
in helping to prevent the introduction, establishment, and spread of 
Bsal. We conclude that the main pathway for the potential global spread 
of Bsal is the introduction into the United States through 
international trade in salamanders, and we are acting with this rule to 
reduce those risks.
    (PR12) Comment: The pathway analysis, epidemiology of the disease, 
and investigation of the origins of the outbreak need more 
investigation. In addition, no laws or regulations exist to control the 
disposal of untreated water from captive salamander enclosures. Given 
the virulence of the disease, how did Bsal enter the European 
environment? Was it the result of open-system housing, such as outdoor 
pens or open-system water flow? Intentional

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release of pets seems an unlikely source since the course of the 
disease is rapid with signs of infection within 8 days.
    Response: While it is possible that Bsal can be transmitted through 
other pathways and vectors, the comment does not provide any evidence 
that other pathways are more likely than international trade. Drawing 
on the evidence cited in this rule in the Pathway Analysis, we conclude 
that the primary potential pathway for the entry of Bsal into the 
United States is through the international trade in salamanders. Our 
analysis concludes that Bsal can survive on infected animals long 
enough for the pathogen to be introduced into the environment and 
transmitted to species that are negatively impacted by Bsal.
    (PR13) Comment: We suggest another pathway that should be addressed 
is that fishes, plants, and invertebrates may be co-cultured with 
newts. It is unknown if they can act as a fomite. For Bd, there is 
evidence for foliage and invertebrates as substrates. Amphibians can 
enter the United States as stowaways on agricultural and other imports. 
For example, the Cuban tree frog that invaded Florida hitchhiked in 
shipping crates coming from the Caribbean. It is also possible that 
Bsal could be transported in contaminated water that is entering the 
United States with imported fish for aquaculture or the pet trade.
    Response: We concur with the comment. Other pathways are a concern; 
however, the Service concludes that the trade pathway in salamanders is 
the most significant means by which Bsal could be introduced into the 
United States. The final and second interim rules will be protective 
because a co-cultured salamander that has also been found to be a 
carrier would be prohibited from importation into the United States. 
The Service will also continue to seek opportunities to work with 
partners to minimize the risk from other pathways.
Species Additions
    (PR14) Comment: Some of the Bd infections observed in species from 
Ambystoma may have been Bsal. California tiger salamanders (Ambystoma 
californiense) can survive chytrid infections that would make them 
likely carriers. Another peer reviewer stated that the rule states, 
``At least four [native species] are resistant to Bsal infection, of 
which one is expected to be a carrier because Bsal was able to invade 
the skin of that species long enough to move or transmit the fungus to 
other salamanders.'' This is a reasonable assumption. The commenter 
makes the same assumption for Ambystoma based on their ability to be 
infected by Bd.
    Response: The testing results available to the Service at the time 
of the 2016 interim rule provided no evidence that some species within 
Ambystoma are carriers of Bsal. However, subsequent research provides 
that evidence. Please see IV. Second Interim Rule below for that 
evidence.
Prohibition on Interstate Transportation
    (PR15) Comment: Enforcing the interstate prohibition will be 
difficult. Also, it seems unnecessary if Bsal is not known to exist in 
the United States. While it is possible that Bsal may be present on a 
pet in the United States, the interstate transportation prohibition 
could prevent movement of that pet.
    Response: As stated above under A. Background in III. Final Rule to 
the 2016 Interim Rule, the D.C. Circuit Court of Appeals held on April 
7, 2017, that transportation of injurious wildlife between the 49 
States within the continental United States (the contiguous 48 States 
and Alaska) is not prohibited by the Lacey Act, unless that movement of 
the wildlife is restricted due to conditions associated with issued 
injurious wildlife permits. The language in 50 CFR 16.14(a) was and 
still is correct in that it does not prohibit interstate transport 
between States within the continental United States. Transport of 
injurious wildlife between the enumerated jurisdictions set forth in 
the shipment clause of 18 U.S.C. 42 (the continental United States, the 
District of Columbia, Hawaii, the Commonwealth of Puerto Rico, and any 
territory or possession of the United States), codified in Federal 
regulations at 50 CFR 16.3, remains prohibited. The Service will 
continue to seek opportunities to encourage affected members of the 
public to take responsible actions related to listed species.
Prohibition on Preserved Specimens and Parts
    (PR16) Comment: There is little risk of Bsal transmission from 
chemically preserved specimens. Even if contaminated with Bsal DNA, it 
is unlikely that the chytrid would be viable or lead to introduction of 
Bsal into the United States. However, the prohibition should be 
maintained for live or frozen specimens, because it is unclear whether 
Bsal can survive freezing. Experimental studies are needed to elucidate 
the viability of Bsal after preservation and freezing.
    Response: In response to comments we received explaining that 
preserved salamanders or their preserved parts pose a low risk of 
transmitting Bsal, the Service is removing chemically preserved 
specimens and body parts from the injurious wildlife listing as long as 
chemical preservation is adequate to render the fungus inviable. Frozen 
specimens remain regulated as parts of injurious wildlife as clarified 
in A.
Species Capable of Carrying Bsal
    (PR17) Comment: The 2016 interim rule states in the section 
``Invasiveness and Transmission of Bsal'' that the rough-skinned newt 
and the eastern newt are capable of carrying Bsal. What is the evidence 
for this?
    Response: Martel et al. (2014) found that the eastern newt and 
rough-skinned newt were found to be lethally vulnerable to Bsal. Below 
in E. Pathway Analysis, Introduction Pathways, we added that Bsal can 
remain viable inside dead host tissue (Martel et al. 2013). We have 
concluded that lethally vulnerable salamanders are also carriers. More 
recent information affirms the newts as carriers (please see II. 
Current Rulemaking Action below for that evidence).
Invasiveness of Salamanders
    (PR18) Comment: The rule states that Oriental fire-bellied newts 
(Cynops orientalis) and paddle-tailed newts (Paramesotriton 
(Pachytriton) labiatus or brevipes), which are native to China, have 
been found in the wild near an animal importer's facility in Florida. 
Because they were found outside of the facility does not necessarily 
mean that they are a breeding, invasive, reproducing population.
    Response: We concur with the comment that being found outside of a 
facility does not necessarily mean that the species in question is 
actually invasive, although a released salamander could persist long 
enough in the ecosystem to transmit Bsal if the salamander was exposed 
to viable spores.
    (PR19) Comment: The rule states that Picco and Collins (2008) found 
that salamanders sold as bait were highly infected with both ranavirus 
and Bd, thereby increasing the likelihood of pathogen transmission into 
new areas of the United States through the act of fishing. Have 
declines from this pathway been documented? If not, the point is rather 
moot or at least weak.
    Response: That comment refers to the section on invasiveness of 
salamanders. The Picco and Collins (2008) reference demonstrates that 
anglers routinely release salamanders into the areas where they fish, 
which serves as one

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pathway for salamanders being introduced into the environment, 
including nonnative habitats. This pathway may also serve as a vector 
for pathogens, including Bsal.
    (PR20) Comment: The 2016 interim rule states that the four 
salamander genera most commonly imported into the United States from 
2004 to 2014 were Cynops, Paramesotriton, Triturus, and Pachytriton. 
You should check Krysko et al. (2011) against the fire-bellied newt.
    Response: Krysko et al. (2011) was cited by the USGS in its fact 
sheet for the Oriental fire-bellied newt in reporting nonindigenous 
occurrences, although none have been reported since 2010 (USGS 
Nonindigenous Aquatic Species (NAS) 2021 [CYOR]).
    (PR21) Comment: In evaluating the potential to eradicate or manage 
established populations, the 2016 interim rule says that, while some 
introduced salamanders in the United States have been successfully 
controlled, others have not. However, evidence for control is sparse. 
There is a difference between a small population living in exceptional 
circumstances and an invasive species. In many cases, small populations 
of animals will persist but not spread. These are not invasive and 
should not be used as examples of the removal of invasives.
    Response: Executive Order 13751 defines an invasive species as a 
nonnative organism whose introduction causes or is likely to cause 
economic or environmental harm or harm to human, animal, or plant 
health. Establishment and spread can increase the threat that a 
particular species causes, but establishment and spread are not in 
themselves mandatory criteria for defining a species as invasive or 
injurious. The analysis under Potential To Eradicate or Manage 
Established Populations in the 2016 interim rule was intended to show 
that there is a risk of harm from the introduction of Bsal even if a 
nonnative salamander population could be successfully controlled or 
eradicated in the environment.
    (PR22) Comment: The 2016 interim rule states that the total risk of 
Bsal to native salamanders is high. It should probably take Bsal 
invasive risk into account.
    Response: The total risk to native salamanders was based on a USGS 
risk assessment (Richgels et al. 2016). We took invasive risk into 
account in other sources. We discussed the issues related to invasion 
risk of Bsal under Likelihood of Release or Escape. To make our listing 
determination for salamanders, we drew upon the results of multiple 
independent risk assessments and our own analysis and found that Bsal 
is likely to be introduced into the United States if no additional risk 
mitigation steps were taken by the Service.
Bsal Infection
    (P23) Comment: The 2016 interim rule states that Bsal can also be 
introduced into the environment through the improper disposal of 
contaminated water or other materials used to transport salamanders and 
that the fungus can likely persist in such materials independent of 
whether a salamander is present. Although the fungus can persist in the 
environment, it may not be at infectious levels.
    Response: The number of fungal spores required to initiate a Bsal 
infection has not been well researched, and this number may vary among 
host species and with other disease-related factors (environmental and 
Bsal-specific factors). The Service's analysis was based on whether the 
available evidence showed that a given genera was capable of carrying 
Bsal and introducing it into U.S. environments.
    (PR24) Comment: The 2016 interim rule states that the discharge of 
untreated water used to house infected, captive animals could be a 
pathway for releasing infective zoospores into the environment and 
exposing native salamanders to Bsal. There is some evidence for Bd, 
such as the 30,000 zoospores detected after 10 hours in DiRenzo et al. 
(2014), but a more direct experiment occurred in Carey et al. (2006), 
where the solutions that had housed toadlets being tested were used to 
infect other toads. This is strong evidence and should be included.
    Response: We concur with the comment and have added the reference 
to Carey et al. 2006 in the second interim rule.
Likelihood of Release or Escape
    (PR25) Comment: An outbreak of Bsal in Germany was discovered in a 
captive salamander collection (Sabino-Pinto et al. 2015).
    Response: The comment is correctly stated, and this point is now 
referenced in the second interim rule.
Ability To Prevent or Control the Spread of Pathogens or Parasites
    (PR26) Comment: The two treatments from Blooi et al. 2015(a) should 
be changed from ``in development'' to ``available.'' A sentence 
explaining that this treatment is limited in feasibility and 
applicability (that is, not all salamander species can tolerate the 
temperature treatment recommended) should be added.
    Response: We concur with the commenter's statements as reflected in 
Blooi et al. 2015(b) and modified the second interim rule consistent 
with the comment.
    (PR27) Comment: Control measures are available for Bsal-infected 
salamanders, but these would be more relevant for captive salamanders 
rather than free-ranging salamanders.
    Response: We have edited the second interim rule accordingly by 
recognizing that control measures for Bsal-infected salamanders are 
more relevant for captive rather than free-ranging salamanders.
Impacts on Wildlife Resources or Ecosystems
    (PR28) Comment: The 2016 interim rule states that, ``[i]f rough-
skinned newts were to experience severe declines from Bsal infection, a 
result could be significant additional inputs of carbon to the 
atmosphere as has been observed with other species. The commenter 
recommends modifying the sentence to read, ``If rough-skinned newt 
populations were to experience severe declines from Bsal infection, 
atmospheric inputs of carbon may be altered, as has been observed with 
other species (Wyman 1998; Best and Welsh 2014).''
    Response: We have edited the second interim rule consistent with 
the peer reviewer's comment.
    (PR29) Comment: The 2016 interim rule noted that scientists and 
diagnostic laboratories are working to standardize laboratory 
protocols. What happens if they do?
    Response: Standardized laboratory protocols are an important part 
of disease management, but the ability to validate, document, and 
enforce disease testing requirements is also necessary. Additionally, 
the capacity to implement quarantines and live-animal inspections may 
be required. Publication of the final rule does not preclude future 
regulatory action based on emerging science and increased capabilities.
Economic Analysis, Regulatory Flexibility Analysis, and Effect on 
Industry
    (PR30) Comment: Alternative 3 was preferred over Alternative 4 in 
the draft economic analysis. It was not clear whether salamanders were 
excluded from Alternative 3 because they were not tested or whether all 
of the ones tested showed no infection. If they simply were not tested, 
Alternative 4 seems like the more responsible option given a 
precautionary approach since many salamander genera appear to be at 
risk and given that the difference in cost

[[Page 2176]]

between Alternatives 3 and 4 seemed relatively small ($3.8 million 
versus $4 million). Moreover, untested genera may become substitutes 
when the genera under Alternative 3 are no longer available, which 
remains a problem if it is reasonable to expect some risks associated 
with the untested salamander genera.
    Response: Under Alternative 3, we listed genera for which we have 
evidence that at least one species in a genus is a carrier of Bsal with 
no conclusive countervailing evidence that other species in that genus 
are not carriers. Alternative 3 does not include species from genera 
that have not been tested for Bsal vulnerability. Alternative 4 would 
include the listing of all salamander species. The expected increase in 
cost from Alternative 3 to Alternative 4 was not considered in our 
determination about the injuriousness of the species because the 
determination is based on defensible scientific evidence. The Service 
determined that there was unknown risk from genera where no species 
have yet been tested for Bsal and, therefore, could not list those 
genera at this time.
    (PR31) Comment: It was not clear in Alternative 5 whether there 
would be administrative costs associated with health certificates and 
whether there is a probability of making a mistake.
    Response: While most of the testing costs of administering a 
health-certificate program may not fall on the government or public, 
there would still be costs to the Service involved in staff time to set 
up the program and oversee it, as well as wildlife inspectors checking 
import shipments for the additional requirements. The draft economic 
analysis lumps the administrative costs with costs of testing, and both 
are mentioned as a concern in sections 4.1.1.5 and 5.0. A health-
certificate program was not our preferred alternative for a nationwide 
regulatory program by the Service at this time because of uncertainties 
with its effectiveness, including the effectiveness and sensitivity of 
current testing methods (including the return of false negatives); lack 
of validation and sufficient testing capacity; lack of standardized 
treatment methods; and lack of agency resources required to conduct 
inspections, interpret results, and issue health certificates.
    (PR32) Comment: Has inflation been taken into account in the 
analyses of economic costs to adjust costs of today's dollar values?
    Response: All prices in the draft economic analysis were updated 
for the final economic analysis to the 2021 price level Consumer Price 
Index for All Urban Consumers that was used for all indexing purposes 
(see section 3.1.2). Salamander retail price data was received in 2015 
dollars during the course of the study. Tables labeled as 2021$, or 
2015$, have either been adjusted for inflation or did not need 
adjustment. The original price level is the year for the citation 
unless otherwise noted. Tables without a price level or data origin 
year have been amended.
    (PR33) Comment: The economic costs appear to reflect the maximum 
costs since it does not appear that alternative sales were considered. 
For example, if buyers cannot buy salamanders, would they buy other 
amphibians instead or would they simply buy nothing? Only the latter 
would result in the estimated costs. Similarly, the market for 
``local'' salamanders may increase as a response.
    Response: Section 3.1.2 of the analysis of economic costs explains 
three points. Estimated importation losses are stated as maximums due 
to the unknown effect on domestic breeding and consumer substitution. 
Domestic losses are also estimated at the maximum (loss of entire 
industry) due to the lack of data on transport between the enumerated 
jurisdictions in the shipment clause of 18 U.S.C. 42 (codified in 
Federal regulations at 50 CFR 16.3). We also added detail to this 
section to clarify why the losses may range from zero to the maximums 
stated in each alternative analysis section later in the report.
    (PR34) Comment: The pet industry will not be altered significantly 
by this rule, but Bsal would likely impact wild populations of 
salamanders. Perhaps with the exception of breeders, pet sales would 
probably shift to another animal with little loss of revenue.
    Response: Exit from an industry or substituting a legal product is 
dependent on multiple factors as discussed in the report beginning in 
section 3.1.2 of the economic analysis. We added details and 
clarification to this section in the final economic analysis. 
Substitution can occur with other salamander species, an animal from 
another order, or another category of goods altogether.
    (PR35) Comment: The draft economic analysis states under ES 1.1 
Economic Analysis, ``In addition, we used data from IMPLAN[supreg] 
(Minnesota IMPLAN Group, 2013) to estimate the direct effects of this 
rulemaking.'' MIG changed their name. They now go by IMPLAN Group LLC. 
In addition, what data year did you use?
    Response: We changed the name to ``IMPLAN Group LLC'' in the final 
economic analysis. We used study area data from 2013 for the economic 
analysis.
    (PR36) Comment: Regarding the draft economic analysis under ES 
1.4.5 Alternative 5, does the cost estimate of the loss of revenue to 
companies or individuals involved in the importation or interstate 
movement of any salamander species consider the cost of health-
certificate examinations and inspections by veterinarians affiliated 
with the Department of Defense, zoos, and industry as well as private 
practitioners?
    Response: Due to data limitations, the final economic analysis does 
not explicitly estimate the cost of health certificates. The analysis 
assumes that any additional costs for examinations and inspections 
would be absorbed by the importer or passed on to the consumer, but 
data limitations restrict the analysis from estimating whether the 
importer or consumer would pay. Thus, we assume the estimated losses 
for all alternatives including Alternative 5 is the average sales price 
of a salamander. On average, we assume the estimated maximum loss 
(sales price) would include all testing costs.
    (PR37) Comment: The commenter believes a job in IMPLAN is 
annualized. IMPLAN's definition is ``A job in IMPLAN = the annual 
average of monthly jobs in that industry.''
    Response: We have changed the final economic analysis to reflect 
the above definition.
    (PR38) Comment: The draft economic analysis, at ES 1.6 Conclusion, 
states that it is unclear how much testing, treatment, and the health 
certification processes would cost.
    Response: It is correct that these costs are unknown and could not 
be estimated unless a compliance method is developed.
    (PR39) Comment: The commenter found locating the tables and figures 
in the draft economic analysis to be challenging. For example, figure 1 
is not shown for several pages after first being noted in 2.2 
Salamander Market.
    Response: Placement of tables and figures was determined by the 
progression of the analysis. As many numbers are referred to many 
times, they will not always be near all discussions. Table and figure 
numbers are given to allow the reader to find them.
    (PR40) Comment: The draft economic analysis states in Table 3-Pet 
Stores Industry that the annual payroll for all is less than the annual 
payroll for small business. That does not seem right.
    Response: We corrected the table in the final economic analysis.

[[Page 2177]]

    (PR41) Comment: The draft economic analysis states in 2.3.5 U.S. 
Bred Salamanders, ``Domestically bred salamanders would represent less 
than one percent of the United States salamander sales between 2012 
through 2014 if this data depicts the entire domestic supply.'' This is 
confusing because table 10 states that 76 percent of commercial 
salamanders are U.S. bred.
    Response: The 1 percent refers to all salamanders, whereas the 76 
percent refers to the species and genera listed in table 10. We amended 
table 10 in the final economic analysis to clarify this point.
    (PR42) Comment: The draft economic analysis states under 3.1.1 
Analysis of Economic Benefits, ``Fewer outdoor recreationists could 
lead to a decrease in expenditures; to demonstrate we use $25,000. 
Implementing a fictional alternative, Alternative Y would reduce the 
probability of Bsal establishment to 10 percent from 80 percent. The 
expected costs in the current situation would be $20,000 ($25,000 x 
0.8); with Alternative Y, the expected costs would be $2,500 ($25,000 x 
0.1). Net avoided costs would be $17,500 ($20,000-$2,500), one measure 
of the benefits of Alternative Y.'' The commenter finds this example to 
be confusing and suggests omitting.
    Response: We deleted the example in the final economic analysis.
    (PR43) Comment: In the Executive Summary of the draft economic 
analysis, you describe some of the potential costs of the regulation 
(for example, lost consumer surplus for pet owners). It seems in the 
discussion under 3.1.2 Analysis of Economic Costs that the costs in the 
cost/benefit sense are being conflated with lost revenue and the 
economic analysis. This is okay, but this section could be more clear.
    Response: The Executive Summary indicates that consumer surplus 
cannot be estimated under the scope of this report and that an 
alternate methodology will be used. Sections 3.1.1-3.1.2 explain how 
the analysis uses the maximum sales as a proxy for the direct economic 
losses. No economic benefits are evaluated for the existence of a 
species in this report.
    (PR44) Comment: The draft economic analysis states under 3.1.2.2 
Small Business, ``Estimates using the unique importers (average of 5 a 
year), or one breeder, yield the maximum adverse impacts; no fewer 
entities would be impacted under the status quo. Applying these two 
methods brackets the impacts on importers and pet stores.'' It is 
unclear what ``average of 5 a year'' means.
    Response: We changed ``average of 5 a year'' to ``annual average'' 
in the final economic analysis. The analysis was also updated to an 
annual average of six importers.
    (PR45) Comment: In the draft economic analysis, the numbers in the 
sectors columns of tables 12-14 do not seem to correspond to anything. 
Could this column be omitted?
    Response: The columns were deleted in the tables.
Public Comments and Our Responses
    We reviewed all 280 comments we received during the public comment 
period for the 2016 interim rule (81 FR 1534, January 13, 2016). We 
received comments from Federal agencies, State agencies, commercial and 
trade organizations, conservation organizations, nongovernmental 
organizations, and private citizens. The comments provided a range of 
views on the proposed listing as follows: (1) Unequivocal support for 
the listing with no additional information included; (2) unequivocal 
support for the listing with additional information provided; (3) 
equivocal support for the listing with or without additional 
information included; (4) unequivocal opposition to the listing with no 
additional information included; and (5) unequivocal opposition to the 
listing with additional information included.
    While all comments were reviewed and considered, several comments 
did not contain information that was new compared to other comments or 
included substantial information that required analysis. Comments 
included individual ideas, data, recommendations, or suggestions on the 
interim listing and the draft economic analysis. Some commenters 
addressed the 14 questions we posed in the 2016 interim rule. We 
consolidated comments and responses into key issues in this section. We 
edited some comments for brevity or grammar while maintaining the 
intent. We combined comments that expressed similar perspectives.
Use of Scientific and Common Names
    (1) Comment: The Service asked, for the species being listed in the 
2016 interim rule, if the scientific and common names are the most 
appropriate ones accepted by the scientific community. Most of the 
herpetological community uses the Society for the Study of Amphibians 
and Reptiles joint societies-endorsed list (Crother 2012); both the 
Association of Fish and Wildlife Agencies (AFWA) and Partners in 
Amphibian and Reptile Conservation (PARC) use this nomenclature in our 
formal publications. However, some States use other nomenclature, while 
some others use older nomenclature simply due to the inability to 
update frequently.
    Response: The comment identifies the disparate use of scientific 
and common names used among herpetological and management entities. We 
believe this approach supports our decision to remove the enumerated 
list of species within each genus in 50 CFR 16.14 for the second 
interim rule. Each species within each genus will therefore be included 
as injurious wildlife in the list of injurious amphibians.
    (2) Comment: There are quite a few errors (some species listed 
twice under different Latin names) in the proposal.
    Response: The commenter did not provide specific examples, so we 
cannot check this comment with additional references. The comment does 
support, however, our decision to remove the enumerated list of species 
within each genus in 50 CFR 16.14 for the second interim rule.
Listing of Preserved Specimens, Parts, and Eggs and Gametes
    (3) Comment: Scientific specimens of salamanders that are 
desiccated or have been fixed or preserved in formalin or alcohol 
should be exempt from this rule because Bsal is no longer viable.
    Response: We concur that preserved specimens do not pose a risk for 
pathogen transmission as long as chemical preservation is adequate to 
kill Bsal, and we have removed chemically preserved specimens from the 
reach of this final rule.
    (4) Comment: What is included in the definition of ``parts of 
salamanders'' and why? Listing swabs makes testing for disease more 
difficult, which could adversely affect the intended effect of the 
rule. Please provide an exemption for tissue samples (including 
histological samples), molecular extractions, swabs, and other parts.
    Response: Any item that contains cells or genetic material from a 
listed species is considered a ``part'' of the listed animal. This 
definition is not unique to the salamander rule but is consistent with 
standard regulatory definitions used by the Service. Specimens, such as 
skin swabs and tissue samples for microscopic analysis (histology), are 
included as ``parts'' in the rule consistent with the definition of 
``fish or wildlife'' outlined in 50 CFR 10.12, which includes ``any 
part, product, egg, or offspring thereof.'' Also, 50 CFR 10.12 states 
that ``amphibians'' means a member of the class, Amphibia, including, 
but not limited to, frogs, toads, and salamanders; including any

[[Page 2178]]

part, product, egg, or offspring thereof, or the dead body or parts 
thereof (excluding fossils), whether or not included in a manufactured 
product or in a processed food product. Specimens such as swabs 
intended for culture or in transport or growth media will require 
permits. We may issue permits to facilitate all of the above-described 
activities. For purposes of this rule, eggs and gametes and purified 
extracted genetic material of salamanders are excluded from the 
prohibitions as ``parts'' because they are unable to cause pathogen 
transmission. However, swabs and histological samples that are 
preserved or fixed in appropriate concentrations of ethanol or 
formaldehyde-based solutions are also not injurious as long as chemical 
preservation is adequate to kill Bsal as described in current peer-
reviewed literature. The appropriate concentration and minimum exposure 
time for a given chemical preservative or fixative to render any Bsal 
organisms non-viable varies with the precise chemical formulation and 
should be utilized as described in association with such actions in the 
peer-reviewed literature. Please also refer to IV. Second Interim Rule.
Purpose of Listing as Injurious
    (5) Comment: Several comments provided feedback on whether eggs and 
gametes should be included in this rule. As a comment noted, specimens 
require transport with some form of medium, such as water or plant 
materials, to remain viable, and that medium could harbor Bsal, thus 
constituting a threat by indirectly moving disease vectors with the 
eggs or gametes and increasing the risk of indirect Bsal transmission. 
Further, eggs at certain stages of development could contain 
keratinized tissues (for example, Xie and Yu (1992)), which could 
transmit the Bsal pathogen. However, other comments noted that if 
entire genera are excluded from the listing because they cannot be 
infected, then the relative risk from the transport of eggs is no 
greater.
    Response: Our authority does not include the listing of the medium, 
such as water or plant materials, that the specimens are transported 
in. As noted in this rule, there is no evidence that salamander 
reproductive material also contains keratin that might harbor Bsal. 
Therefore, eggs and gametes are not listed by this rule.
Effect of Rule on Scientific Research
    (6) Comment: The rule will have a negative impact on scientific 
research, especially on native taxa. The prohibition should not apply 
to scientific research, providing that the biologist in question is in 
possession of an approved permit from the State where the specimen(s) 
were originally collected.
    Response: Permits from the Service for injurious listed species can 
be obtained for scientific, zoological, educational, and medical use 
for importation, shipment between the enumerated jurisdictions in 18 
U.S.C. 42(a)(1) (codified in Federal regulations in 50 CFR 16.3), and 
transport for a previously permitted salamander. The statute does not 
cover collection of native species or transport of injurious listed 
salamanders across State lines within the continental United States 
(see PR15).
Species Not on the List
    (7) Comment: Several commenters advocated for adding various genera 
or listing at the family level, such as Salamandridae, while others 
advocated for listing all species.
    Response: The salamander species listed by this final rule and the 
second interim rule are those found within a genus for which we have 
confirmation that at least one species in that genus is a carrier of 
Bsal, and there is no conclusive countervailing evidence suggesting 
that some species within the genus are not carriers. Although 
additional salamander species could be at risk from Bsal infection or 
could serve as a carrier, we are not listing species in those genera 
because they had not yet been tested. We considered listing more 
species based on the comments we received. However, the logic we used 
for listing at the genus level breaks down at the family level for one 
family. In the family Plethodontidae, the genus Gyrinophilus is not 
known to be a carrier, but the genera Hydromantes and Plethodon are 
carriers. As a result, we cannot list all species within 
Plethodontidae. We also cannot list a species without science-based 
documentation. We can list for the statutorily defined purposes under 
the statute codified at 18 U.S.C. 42(a); any other purpose is beyond 
the scope of this rulemaking. Please see IV. Second Interim Rule below 
for additional genera we have documented as injurious and are therefore 
listing.
    (8) Comment: Some comments noted that while some salamander species 
appeared to be resistant to Bsal in infection experiments, it is 
unclear how strong this resistance will be outside of the optimal 
husbandry conditions found in laboratory settings.
    Response: As part of the justification for listing, the Service 
acknowledges that salamander species known to be tolerant of Bsal 
infection under experimental conditions may demonstrate more severe 
clinical disease when infection is combined with additional stressors 
in the wild, as has been found for other diseases, including those in 
amphibians (Wobeser 2007; Kerby et al. 2011; Kiesecker 2011). However, 
the Service needed evidence that a species was a carrier or likely to 
be a carrier before listing the genus as injurious.
    (9) Comment: Tylototriton podichthys was recently described and 
should be added to the list (Phimmachak et al. 2015).
    Response: All species in a genus are also listed as injurious even 
if they are not specifically identified in the rule. Because we 
identified Tylototriton as one of the genera listed in the 2016 interim 
rule and hereby affirmed, T. podichthys is one of the species listed as 
injurious. The comment supports our decision to remove the enumerated 
list of species within each genus in 50 CFR 16.14 for the second 
interim rule.
    (10) Comment: The Service should establish an expedited process by 
which additional salamander species can be added to the list as new 
information becomes available.
    Response: Rulemaking under 18 U.S.C. 42 is governed by the APA, 
under which we promulgated the 2016 interim rule and this final rule. 
The Service is adding new genera to the list with the second interim 
rule in this document.
Species Should Be Removed From the List
    (11) Comment: Species from the genera Cynops, Salamandra, 
Pleurodeles, Siren, Notophthalmus, and Triturus should be removed. They 
are the most commonly kept species and listing will significantly 
affect those who raise, study, or keep animals from these species.
    Response: Due to shared characteristics by species within a genus, 
other species within these genera are also likely to be carriers of 
Bsal. The Service found that species from the genera Cynops, 
Salamandra, Pleurodeles, Siren, Notophthalmus, and Triturus can carry 
Bsal and, therefore, pose a substantive risk to native salamander 
populations. The listing of these species as injurious wildlife does 
not regulate possession, transport, breeding, or sale within the 
continental United States unless regulated under permit. Other Federal, 
State, Tribal, or Territorial laws may apply.
    (12) Comment: No native species should be listed. Listing native 
species as injurious wildlife solely on the basis of their 
vulnerability or capacity to carry

[[Page 2179]]

an absent foreign pathogen is concerning. Additionally, most of the 
animals tested that were lethally vulnerable were dead within about a 
month, as per Martel et al. (2014), and the odds of any of these 
animals being available for sale while carrying the disease are almost 
nonexistent.
    Response: We listed native species in the 2016 interim rule partly 
because some native species that we concluded can be carriers of Bsal 
are raised outside the United States and imported into the country and 
partly because listing would prohibit transport of injurious 
salamanders between the enumerated jurisdictions in the shipment clause 
of 18 U.S.C. 42 (codified in Federal regulations at 50 CFR 16.3), in 
order to prevent introduction, establishment, and spread of the 
pathogen in U.S. ecosystems. Several native species of newts were 
already known to be highly susceptible to dying from Bsal. Not all 
species die immediately upon exposure to Bsal, and there is no evidence 
that lethally vulnerable species cannot survive long enough for Bsal to 
be transmitted within the United States if they are infected prior to 
their movement. At the time of the drafting of the 2016 interim rule, 
most of the research was being conducted on Asian and European species 
to find out where the fungus may have originated and why wild European 
salamanders were dying. After the 2016 interim rule published, many 
studies by U.S. researchers began to provide information for the 
conservation of native species in the event Bsal is introduced into the 
American environment. These studies demonstrate that many native 
salamanders are susceptible and can be Bsal carriers.
    (13) Comment: Many of the listed species in some genera, such as 
Plethodon, Taricha, and Notophthalmus, have never been found to carry 
Bsal. These species should be delisted.
    Response: New information confirms that species from the genera 
Plethodon, Taricha, and Notophthalmus can carry Bsal based on 
laboratory studies. As of the drafting of the second interim rule, all 
three species of Notophthalmus have been found to be lethally 
susceptible to Bsal (Gray et al. 2023), and two of the four Taricha 
species are carriers (Gray et al. 2023).
    (14) Comment: The listing of the entire genus Plethodon is based on 
the Martel et al. (2014) study from a sample of two wild-caught P. 
glutinous imported to Europe. Under the circumstances, the evidence 
suggests that all species in the genus Plethodon should be removed from 
the list.
    Response: We disagree with the comment. While Martel et al. (2014) 
classified the slimy salamander (Plethodon glutinous) as resistant to 
infection, the study also demonstrated by histology that Bsal could 
invade the skin of the slimy salamander, even though it apparently 
cleared the infection and did not show signs of clinical disease. Our 
examination of the supplementary data of Martel et al. (2014), 
including histology (microscopy) tests and subsequent discussions with 
the authors, indicates that there is sufficient evidence that Bsal was 
able to invade the skin of this species long enough to move or transmit 
the infection to other salamanders (Martel et al. 2014; A. Martel, 
University of Ghent, pers. comm. 2015; K. Lips, University of Maryland, 
pers. comm. 2015). Because we expect all species within a genus to 
respond in a similar way for Bsal carrier status, we conclude that all 
species of Plethodon are potential carriers. Since the 2016 interim 
rule published, additional studies have shown multiple species in the 
genus Plethodon can be carriers (DiRenzo et al. 2021); see IV. Second 
Interim Rule.
    (15) Comment: Some species from the genus Neurergus have been bred 
over many generations and are in private collections (N. crocatus, N. 
kaiseri, and N. strauchii). N. kaiseri, which is listed under the 
Convention on International Trade in Endangered Species of Wild Fauna 
and Flora (CITES) Appendix I, has not been imported for years, and most 
of the animals in the United States are descendants of zoo colonies and 
hobbyist captive-bred animals. Because they are protected by other laws 
and not imported, they do not have any risk of transmitting Bsal and 
there is no need to list them.
    Response: Regardless of protection level under other laws, these 
species are still injurious wildlife under 50 CFR 16.14 as part of the 
genus Neurergus. Their protection level under these other laws does not 
change the characteristics of the species that we find to be injurious 
to wildlife and the wildlife resources of the United States by reason 
of their potential to serve as vectors for the pathogen Bsal. Also, 
there is no way to confirm that captive-bred salamanders have not been 
exposed to Bsal through contact with other individuals. Neurergus has 
been confirmed to carry Bsal in a European collection (Fitzpatrick et 
al. 2018), and there is a chance a co-housed salamander of a different 
species could be imported into the United States.
Need for Rule
    (16) Comment: The rule is unnecessary. The prohibition can be 
justified only if Bsal is found to be present in the United States. 
Other commenters stated that the rule is unnecessary because Bsal must 
be here already given the number of salamanders imported annually and 
their belief in the low likelihood of a captive salamander coming into 
contact with the wild populations and transmitting Bsal.
    Response: Since the publication of the 2016 interim rule, Waddle et 
al. (2020) conducted a large-scale surveillance for Bsal across 594 
counties in 35 States and 1 site in Mexico with 11,189 swab samples of 
wild salamanders and some frogs and toads, with no positive results for 
Bsal. The purpose of listing these species as injurious wildlife is to 
prevent the introduction of the Bsal fungus in the wild in the United 
States. A species does not need to be already present in trade or in 
the environment to be listed as injurious wildlife. In fact, it is 
often difficult to achieve a prevention outcome once a species or 
pathogen occurs in the environment. To make the listing determination 
for salamanders, we drew upon the results of multiple independent risk 
assessments and our own analysis and found that Bsal is likely to be 
introduced into the United States if no additional risk mitigation 
steps are taken. Additional discussion on this topic can be found in 
IV. Second Interim Rule under the section Likelihood of Release or 
Escape.
    (17) Comment: To list a native species of wildlife as injurious 
simply because it may act as a host to a rare but potentially 
devastating pathogen that has not been detected in the United States is 
an unmanageable proposition. Every native species of wildlife fits this 
criterion and would need to be listed as injurious for some rare 
pathogen detected in a very isolated outbreak on another continent, as 
has occurred with Bsal.
    Response: The purpose of listing these species as injurious 
wildlife is to act preemptively to prevent the introduction, 
establishment, and spread of the Bsal fungus in the wild in the United 
States. The fungus affects many native salamanders, with lethal effects 
on many salamander species, and it is not yet known to be found in the 
wild in the United States. There is an existing pathway for the fungus 
to arrive by importation of salamanders, including species native to 
the United States that are raised in captivity outside of the United 
States and then imported back

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into the continental United States and the enumerated jurisdictions of 
the shipment clause. This regulatory action is being taken to prevent 
Bsal's arrival through the organisms-in-trade pathway. If we wait until 
the fungus arrives, it will likely be impossible to eradicate. We will 
continue to evaluate other species for possible risks and consider 
injurious wildlife actions as appropriate and authorized under 18 
U.S.C. 42(a).
    (18) Comment: Bsal can be treated and cured in captivity, so there 
is no reason to limit availability of the species in question.
    Response: Voluntary actions, such as applying heat therapy as 
described in Blooi et al. (2015a) and Blooi et al. (2015b), may help 
reduce the threat posed by Bsal for specimens held in captivity. 
However, at this time it is not possible to determine the likelihood of 
success of such measures for all species or of achieving compliance 
with prophylactic treatment or treatment following the onset of 
symptoms. Therefore, it is unknown how effective treatment will be in 
preventing Bsal's introduction, establishment, and spread in the United 
States, and no Bsal control is known for salamanders in the wild.
    (19) Comment: If a species that is not a carrier is similar in 
appearance with another species, neither species should be removed from 
the list unless both species are confirmed that they are not 
susceptible to or carriers of Bsal.
    Response: The Service does not have the authority under the statute 
to list a species based solely on its similarity of appearance to 
another species. We list based on our determination of injuriousness.
    (20) Comment: There is no case in the United States where 
salamanders, native or nonnative, have been proven as invasive or 
injurious. The 2016 interim rule does not substantiate injury by 
transplanted or exotic salamanders.
    Response: The salamanders are listed because they are carriers of a 
fungus that makes them harmful to other salamanders, not because the 
salamanders are invasive. We concluded that even if the salamander 
species listed by this rule do not become established, some species 
capable of carrying Bsal and listed by this rule can survive long 
enough in the wild to transmit Bsal. Our findings are discussed in 
Potential To Survive, Become Established, and Spread in IV. Second 
Interim Rule.
Listing Purpose Is To Regulate Disease or Manage Native Species
    (21) Comment: Listing salamanders as injurious is not an 
appropriate means to regulate an animal disease. The injurious wildlife 
provisions of 18 U.S.C. 42 pertain to animals and not diseases or 
pathogens. The focus of the 2016 interim rule is Bsal, a fungus that 
the Service possesses no authority to regulate as acknowledged in the 
interim rule. The law provides no provisions for testing, surveillance, 
or certification of health to allow for movement in trade.
    Response: As we described in Listing Species That Carry Pathogens 
in the 2016 interim rule, the Service can list as injurious any member 
of the enumerated taxa that are hosts to or carriers of pathogens that 
cause the host or carrier to be harmful by its presence to one or more 
of the interests listed in the statute. We have previously listed 
species that serve as hosts to or carriers of pathogens, as in the case 
of fishes in the salmon family (Salmonidae) (32 FR 20655, December 21, 
1967). We noted in the 2016 interim rule that there are concerns 
regarding the effectiveness and sensitivity of current testing methods 
(including the return of false negatives), lack of validation and 
sufficient testing capacity, and agency resources required to conduct 
inspections, interpret results, and issue health certificates. If these 
issues are resolved, it may be possible to establish a health 
certificate for salamanders that are free of Bsal. A health certificate 
was established for import of salmon under the authority of 18 U.S.C. 
42. While the concerns remain, and therefore a Bsal health 
certification has not been established, this does not mean that there 
is no authority to establish a health certification if circumstances 
were to change. Appropriate conditions may also be included in 
injurious wildlife permits under the authority of and consistent with 
the purposes of 18 U.S.C. 42.
    (22) Comment: Several commenters noted that, by definition, 
``pathogens'' are injurious and are regulated under the authority of 
other agencies. The World Trade Organization and the United States 
Department of Agriculture (USDA) recognize the World Organisation for 
Animal Health [WOAH, formerly OIE] as the proper body to set animal 
health standards. The WOAH helps develop and revise international 
standards for the safe trade of animals and animal products. The proper 
course to prevent the importation of salamanders carrying Bsal is to 
list the pathogen as a WOAH reportable disease, and instead of the 2016 
interim rule, there should be a cooperative effort to respond to the 
disease threat as provided through the WOAH, World Trade Organization, 
and the National Aquaculture Health Plan and Standards (formerly called 
the National Aquatic Animal Health Plan) for the United States.
    Response: The USDA and the Centers for Disease Control and 
Prevention have authority to regulate wildlife pathogens when those 
pathogens pose a risk to agriculture or human health, respectively. No 
such effects are currently known in the case of Bsal. The Service has 
authority to regulate the importation of certain species that pose a 
risk to wildlife and the wildlife resources of our country. This 
authority has been applied in the present case in response to a clear 
and immediate risk.
    After the 2016 interim rule took effect, the WOAH did add Bsal as a 
reportable disease, but that action does not prevent importation. We 
work through such mechanisms as those provided by the WOAH and National 
Aquaculture Health Plan and Standards, and we support all efforts by 
the international community to participate in the global response to 
this pathogen. The Service, operating within its relevant regulatory 
authority to list injurious wildlife, took action through the 2016 
interim rule due to the urgent need required to manage the threat Bsal 
poses to salamanders in the United States.
    (23) Comment: This salamander rule not only prevents safe commerce, 
it eliminates any incentive for industry to pursue research into the 
detection and treatment of Bsal. Other comments expressed similar 
issues and asked whether it would be possible to make testing mandatory 
to allow interstate movement.
    Response: While the Service acknowledges that some economic 
incentive may have been removed due to the prohibitions imposed by the 
injurious wildlife provisions of the Lacey Act as a result of listing 
species of salamanders as injurious wildlife under this rule, many 
salamander genera were not listed due to insufficient evidence at the 
time as carriers, and they remain a possible threat. Furthermore, 
research for detection and treatment of Bsal has increased considerably 
in the United States since the rule took effect. Permits allowing 
importation can be obtained for zoological, educational, medical, and 
scientific use. This final rule explains that interstate transportation 
between States within the continental United States is not prohibited 
as of 2017; however, the injurious wildlife listing still prohibits 
import into the United States, and transport of injurious wildlife 
between the enumerated jurisdictions in the shipment clause of 18 
U.S.C. 42(a)(1) (the continental United States, the District of 
Columbia,

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Hawaii, the Commonwealth of Puerto Rico, and any territory or 
possession of the United States), codified in Federal regulations at 50 
CFR 16.3.
    (24) Comment: The Lacey Act does not provide authority to list 
native species. The Lacey Act has been examined and critiqued over the 
last few decades within a variety of peer-reviewed and gray-literature 
publications (Dentler 1993, U.S. Congress 1993, Anderson 1995, Whalen 
1998, Biber 1999, Jenkins et al. 2007, Alexander 2013). In no instance 
did these authors construe Lacey Act provisions to allow the listing of 
native animals as injurious. Notably, the U.S. Congress, Office of 
Technology Assessment, recommended in 1993: Congress could provide the 
Service with increased guidance on the purpose of this [injurious] list 
and the specific criteria for adding species to it.
    Response: The provisions of 18 U.S.C. 42(a)(1) do not limit 
wildlife subject to the law to species not native to the United States. 
Under the law, the Service may list species that are indigenous to the 
United States if they cause injury to the interests enumerated in the 
law. The publications mentioned reflect the interpretations of the 
authors. Congress has also listed native species as injurious by 
statute, such as the Mariana fruit bat (Pteropus mariannus), further 
demonstrating that the authority of 18 U.S.C. 42 is not limited to 
nonnative wildlife.
Additional Science and Data for Rule
    (25) Comment: In the 2016 interim rule, the Service asked what 
species listed as threatened or endangered by one or more States would 
be affected by the introduction of Bsal. AFWA and several States 
indicated that several salamander species are of interest to them, 
though it is not yet evident how Bsal would affect all of these 
species. A number of State threatened and endangered or protected 
species (restricted or prohibited from take, possession, sale, or other 
activities) were provided during the public-comment period.
    Response: We appreciate the additional information on State 
threatened and endangered species. While the Service concluded that 
some species identified by the States are not carriers, others are, 
such as species in the genus Plethodon. The carrier status of several 
species, at the time the public-comment period closed, had not yet been 
identified. However, more have been identified since then, including 
affirming the genus Plethodon in this final rule. This additional 
information helps provide additional justification for listing species 
that are capable of carrying Bsal, as Bsal presents a risk to wildlife 
and wildlife resources of the United States, including those identified 
by the States as in need of protection.
Pathways and Spread
    (26) Comment: The Service asked the question, ``Are there other 
pathways for Bsal into the United States that we should address? If so, 
what are they?'' According to AFWA, a pathway of concern that appears 
to have little or no Federal regulatory authority or enforcement 
pertains to biological supply companies. Others include internet sales 
involving small shipments using couriers such as FedEx or UPS, 
traditional medicine or foreign food markets, and ceremonial uses of 
these species. AFWA is aware of interstate shipments of some 
salamanders, though not necessarily the currently included species, for 
the purposes of the bait trade, but AFWA would like to see some 
exploration of whether there are imports for this purpose.
    Another comment noted that, while the pet trade is an important 
pathway, salamanders may stow away in nursery stock, as was observed 
with northwestern salamanders (Ambystoma gracile) in Christmas trees 
(Rochford et al. 2015). In addition to terrestrial nursery stock, the 
aquatic plant and animal trade may also spread Bsal in shipment water.
    Response: The Service's pathway analysis found that the main 
pathway for the global spread of Bsal is the international trade in 
salamanders, such as Martel et al. (2014) noted. While not explicitly 
discussed, that international trade could include the uses noted in the 
comment, whether intentional or as a hitchhiker. Biological supply and 
bait companies are commercial entities. These companies have always had 
to comply with import and export regulations under 50 CFR part 14. With 
this injurious listing, these commercial businesses will be subject to 
the same prohibitions as other entities. Likewise, animals 
unintentionally imported or transported between the enumerated 
jurisdictions in the shipment clause of 18 U.S.C. 42(a) (also set forth 
at 50 CFR 16.3) through nursery stock or other pathways would also be 
in violation of the injurious wildlife listing's prohibitions. As 
explained in A. Background in Final Rule to the 2016 Interim Rule, 
interstate transport between States within the continental United 
States is not prohibited by the current prohibitions of 18 U.S.C. 
42(a).
    (27) Comment: Bsal is known to persist in a moist environment for 
up to 7 weeks, even without an amphibian host. This ability creates an 
alarming pathway for the potential spread of Bsal into the United 
States through a variety of means not fully addressed by the 2016 
interim rule. This unchecked pathway of Bsal into the United States 
presents a major limitation in our ability to prevent introduction of 
this potentially devastating infectious wildlife disease.
    Response: Materials that can transmit pathogens, such as water, 
represent a potential pathway. However, the Service does not have 
authority under the injurious wildlife listing provisions in 18 U.S.C. 
42(a) to prohibit importations of water and fomites that may be 
infected with the Bsal pathogen. Listing the species that can carry 
Bsal is expected to limit the movement of such materials, but they do 
remain a concern. The Service will continue to explore opportunities to 
address this issue with partners and stakeholders.
    (28) Comment: A comment suggested that it is premature to discount 
frogs and toads (anurans) and caecilians from getting Bsal.
    Response: Under this final rule, we listed salamanders for which we 
had affirmation at the time of the rule drafting that they could carry 
Bsal into the United States, and subsequent evidence confirms the 
determination. We do know about positive Bsal test results for several 
species of anurans and will continue to monitor research on them and 
caecilians and on salamanders for which data is currently unavailable.
    (29) Comment: The rule is unnecessary and will only hurt hobbyists. 
Hobbyists who keep salamanders may be tempted to release them into the 
wild if they cannot find alternatives and do not want to euthanize 
them. If so, the risk of Bsal being introduced into the wild might be 
increased.
    Response: We believe this regulatory action will safeguard the 
health of wild salamanders and those kept in captivity. We have taken 
action with this rule to list salamanders that we find can carry Bsal. 
Pet owners will still be allowed to keep their salamanders and sell or 
give them away within the enumerated jurisdictions of 18 U.S.C. 42, 
also set forth at 50 CFR 16.3. In addition, many States have laws 
making it illegal to release certain animals into the wild, and 
injurious listed species cannot be released into the wild under Federal 
law. Some States have amnesty programs that accept unwanted pets. The 
Service believes that the majority of pet owners and hobbyists would 
not intentionally release their animals into the wild; however, the pet 
trade was

[[Page 2182]]

identified as the major vector for a potential Bsal invasion. To assist 
pet owners who might need to find homes for their animals, we posted 
information about responsible alternatives to releasing salamanders on 
our website when we published the 2016 interim rule. That updated 
information can be found at https://www.fws.gov/node/266100.
    (30) Comment: The interstate prohibition will not help prevent the 
spread as the zoospores are most likely going to be spread through 
moving water. Also, many wildlife diseases are moved by wildlife 
themselves, including migratory birds. Without evidence of infected 
animals in the trade, it is inappropriate to indict an industry or to 
blockade any trade based on speculation. Additional studies are needed 
to determine sources and causes for outbreaks. Without further 
surveillance and supportive data, it cannot be substantiated that the 
international and interstate trade is the vector for spread of this 
disease.
    Response: As we note in the final rule, the interstate prohibition 
has been clarified. In the 2016 interim rule, we did not indicate that 
the absolute cause of the spread of Bsal is the wildlife trade, 
although we concluded that the most likely pathway of Bsal into the 
United States is on the bodies of salamanders in the commercial 
salamander trade. We cited peer-reviewed journal articles that suggest 
the spread of Bsal has been human mediated due to the discontinuity of 
the global distribution of Bsal between Asia and Europe, and we cite 
the detection of the pathogen in imported captive exotics. Both of 
these pieces of information suggest the spread of Bsal has been human 
mediated. Other pathways for Bsal introduction are not expected to be 
as significant compared to the international-trade pathway. While the 
Service is concerned about contaminated water, Bsal is not yet known to 
be present in the United States. Listing is intended to prevent the 
introduction, establishment, and spread of Bsal. Salamanders would have 
to come into contact with Bsal-contaminated water for the pathogen to 
be introduced. If no infected salamanders are here, they cannot 
transmit the pathogen to waters that can further spread the pathogen.
    Research suggests that waterfowl can carry Bd on their toes, 
although Bd could not survive more than 60 minutes of desiccation on 
the scale tissue (Garmyn et al. 2012). As a result, while Bd could be 
transmitted from one habitat to another on short flights, transmission 
is unlikely to be an intercontinental threat. Given the similarities 
between Bd and Bsal, Bsal is not likely to be introduced to the United 
States through bird migrations.
Border Interstate Transportation
    (31) Comment: The prohibition on importation will help to prevent 
the movement of Bsal into the United States provided that it is also 
prevented from entering Canada. If an infected salamander enters 
through Canada, Bsal could be transported via water and waterfowl into 
the United States, negating the prohibition's benefits.
    Response: In 2017, after the 2016 interim rule was published, 
Canada passed a law prohibiting importation of all species of the order 
Caudata, alive or dead, and their gametes (ECCC 2017, 2018). Canada, 
Mexico, and the United States actively coordinate in wildlife 
conservation issues through the Canada/Mexico/U.S. Trilateral Committee 
of Wildlife and Ecosystem Conservation and Management meetings.
    (32) Comment: The interstate prohibition will make it harder to 
acquire scarce animals. Prohibiting interstate movement will hurt 
honest hobbyists who are working hard to find or produce healthy 
captive-bred animals. The prohibition should apply only to wild-caught 
animals or importation only but allow for movement of captive-bred 
animals in the United States that have been tested and found to be free 
of Bsal, especially since Bsal has not been found in the United States.
    Response: As explained under A. Background in II. Final Rule to the 
2016 Interim Rule, the interstate prohibition has been clarified. Under 
18 U.S.C. 42, the Service does not have the authority to selectively 
prohibit the importation of wild-caught or captive-bred animals for a 
species listed as injurious wildlife. Permits can be acquired for 
zoological, educational, medical, or scientific purposes.
Effect on Hobbyists
    (33) Comment: Captive-breeding should be legal for private and 
hobbyist purposes.
    Response: Captive-breeding is not prohibited by the injurious 
wildlife provisions of the Lacey Act as a result of listing species of 
salamanders as injurious wildlife under the rule.
    (34) Comment: The rule will have a direct effect on both amphibian 
business owners and hobbyists as well as native ecosystems. The species 
that are listed are those most important to the hobby--animals that are 
easy to breed and that do well in captivity. The rule effectively 
transitions the hobby almost entirely away from captive-breeding. 
Captive-bred animals are healthier, less likely to carry diseases, more 
likely to thrive in captivity, and do not harm wild populations. 
Commercially wild-collecting animals can cause long-term damages to 
populations and has been known to play a role in disease transmission 
as collectors travel between areas and do not disinfect their 
equipment.
    Response: The commenter states that captive-bred animals are 
healthier and less likely to carry diseases but does not provide 
evidence to support this statement. State wildlife agencies are 
responsible for regulating the collection of most wild salamanders, 
including injurious listed ones, and State authorities can be used to 
protect populations from overharvest.
    (35) Comment: The science is wrong on the number of salamanders 
crossing State lines. The commenter knows one individual who sold 1,500 
captive-bred tiger salamanders last year outside their State. The 
interstate prohibition will cause a drop in the diversity of captive-
bred species and related expertise in the country. This prohibition 
will severely limit many forms of research since expert American 
salamander keepers will be unable to maintain and share their 
experience through captive-breeding programs. Researchers will be 
limited largely to axolotls (Ambystoma mexicanum), which may not work 
for their needs. Even Martel et al. (2014) was largely dependent on 
captive-bred animals; in a few years, a similar study will be 
impossible from the United States.
    Response: The rule will not end scientific endeavors that would 
benefit the injurious listed species. Additionally, as explained in 
this final rule, the prohibition on interstate movement between States 
within the continental United States has been clarified.
    (36) Comment: The rule interferes with educational opportunities 
and exposes exhibitors, nature centers, wildlife rehabilitators, 
private citizen hobbyists, and commercial breeders to Federal 
prosecution and penalties under the Lacey Act.
    Response: The rule is intended to protect native species, which 
will help ensure that the public maintains the opportunity to enjoy 
them in their wild habitats. Also, the injurious wildlife provisions of 
the Lacey Act do not prohibit ownership or breeding of injurious 
wildlife, unless unlawfully imported or transported between the 
enumerated jurisdictions or otherwise restricted due to conditions 
associated with issued permits. People and

[[Page 2183]]

zoological institutions can still own salamanders where consistent with 
other Federal, State, and Tribal laws and regulations applicable to the 
species. The listing also will not prevent the continued use of these 
species for education, and prohibited activities may be authorized by 
permit for zoological, educational, medical, or scientific purposes (in 
accordance with permit conditions). Finally, as explained in the final 
rule, the interstate prohibition between States within the continental 
United States has been clarified.
Effect on Conservation Efforts
    (37) Comment: Captive-breeding has been proven to be the most 
reliable way of ensuring the survival of endangered (or common) 
species. Furthermore, captive-breeding provides a backup gene pool for 
wild populations that may be drastically reduced from Bsal. Also, the 
listing would make it illegal to transport listed salamander species 
across State lines and would devastate conservation programs across the 
United States. The permitting process will keep many zoos and aquariums 
from participating in propagation efforts of salamander species on the 
list, many of which need help.
    Response: While captive-breeding is useful in many cases to ensure 
survival, it is less so when a novel, lethal pathogen is the cause. 
Listing the species as injurious in this rule will not affect 
legitimate conservation efforts that U.S. breeders can carry out for 
the species. The law allows for the issuance of permits authorizing 
otherwise prohibited movement or imports for scientific or zoological 
purposes, including non-commercial conservation breeding operations. 
The Service has provided information online to help people apply for a 
permit (see Permitting Difficulties below in this comment discussion 
for additional details). Finally, as explained in the final rule, the 
current prohibition on interstate transport in 18 U.S.C. 42(a) has been 
clarified and does not apply to interstate transport between States 
within the continental United States.
    (38) Comment: When scientists collect tissues or specimens for lab 
experiments, the animals are never released into the wild and therefore 
pose no threat to the spread of Bsal or any other pathogen. The 
Service's imposition of increased Federal permitting will inhibit 
scientists who are studying the biology of regulated species and may 
dissuade graduate students or other biologists from such work. This 
type of regulatory change can hinder conservation efforts before their 
need can even be evaluated.
    Response: This listing should not adversely affect any valid 
conservation efforts. In general, all wildlife species must be declared 
at the time of importation (see 50 CFR part 14), but most do not 
require special permits. Prior to this rule, only species of 
salamanders listed under the Endangered Species Act (ESA) or CITES 
required import permits under those wildlife laws implemented by the 
Service. For injurious wildlife, permits are not needed for interstate 
transport between the States within the continental United States 
(except into or out of the District of Columbia), and permits to allow 
import and transport between the enumerated jurisdictions in the 
shipment clause of 18 U.S.C. 42(a) may be granted for bona fide 
scientific purposes. This rule should have no significant effect on any 
conservation efforts that are currently being or will be carried out.
    (39) Comment: One commenter has never owned a pet frog or 
salamander yet has educated more than 3,000,000 people about amphibians 
via online and printed educational materials and through live 
presentations and hikes to amphibian habitats to see local, native wild 
amphibians. The commenter states that truly inspirational amphibian 
experiences occur when humans come across wild amphibians, not captive 
amphibians.
    Response: The Service encourages visitors to the Service's national 
wildlife refuges and other public lands to appreciate salamanders in 
their natural environments. The purpose of listing these salamander 
species as injurious wildlife is to prevent the introduction, 
establishment, and spread of Bsal in the wild in the United States to 
protect wildlife and wildlife resources, including native salamanders 
in the wild.
    (40) Comment: The rule prevents the ability of salamander owners to 
further test their collections and, therefore, could unintentionally 
increase the spread of this disease rather than decrease it, if it 
arrives in this country. Another commenter noted that the current 
prohibition, especially on interstate movement, will discourage 
cooperation to get domestic collections tested for the disease.
    Response: As explained in the final rule, the current prohibition 
on interstate transport in 18 U.S.C. 42(a) has been clarified and does 
not apply to interstate transport between States within the continental 
United States. Treatment and testing that does not involve import into 
the United States, transport between the enumerated jurisdictions in 18 
U.S.C. 42(a) (also set forth at 50 CFR 16.3), or injurious wildlife 
permits are not regulated by this rule.
    (41) Comment: The rule does not list members of the Ambystoma 
genus, so this omission may increase the chances of legal and illegal 
collection of Ambystoma.
    Response: Listing a species as injurious wildlife results in 
prohibitions on import into the United States and shipment between the 
enumerated jurisdictions in 18 U.S.C. 42(a), codified in Federal 
regulations at 50 CFR 16.3. Neither listing a species as injurious nor 
not listing it results in a prohibition on collection. It is the 
responsibility of a person who may be engaged in salamander collection 
to be aware of any Federal, State, Tribal, or territorial law or 
regulation that applies to such activity. For example, some salamanders 
are federally protected from take (including, but not limited to, 
collection) under the Endangered Species Act, and other laws or 
regulations may otherwise prohibit or regulate collection of other 
salamanders in national wildlife refuges, national parks, or other 
Federal lands, or in accordance with State or Tribal laws. While it is 
possible that some people will switch to Ambystoma spp. in place of a 
listed species if they want to keep salamanders, they may currently do 
so in States where it is legal under State law. We are listing the 
genus Ambystoma with the second interim rule as a way to prevent the 
potential introduction of the fungus.
Permitting Difficulties
    (42) Comment: Multiple commenters expressed concern that the 
listing would complicate research efforts or breeding programs for 
recovery efforts for some native salamanders due to extended permit-
application processing time and limited Federal resources to adequately 
address an increased number of applications.
    Response: As explained in the final rule, the current prohibition 
on interstate transport in 18 U.S.C. 42(a) has been clarified and does 
not apply to interstate transport between States within the continental 
United States. Fewer permit requests will be required because 
interstate transport between States within the continental States is 
not prohibited.
    (43) Comment: The Service should consider adopting a cooperative 
agreement or memorandum of agreement to allow easier movement of 
prohibited species for certain purposes.
    Response: Several commenters suggested memoranda of understanding 
(MOUs) or other mechanisms in lieu of

[[Page 2184]]

permits. Those arrangements cannot be used to authorize import or 
transport between the enumerated jurisdictions in the shipment clause 
of 18 U.S.C. 42 (the continental United States, the District of 
Columbia, Hawaii, the Commonwealth of Puerto Rico, and any territory or 
possession of the United States), which are codified in Federal 
regulations at 50 CFR 16.3. Other interstate transport between States 
within the continental United States is not prohibited by 18 U.S.C. 
42(a). The text of 18 U.S.C. 42(a)(3) requires that exceptions to 
otherwise prohibited activities with injurious wildlife be authorized 
by permit, and only if there has been a proper showing of 
responsibility and continued protection of the public interest and 
health. The regulations at 50 CFR 16.22 specifically provide that the 
Service may issue a permit authorizing the importation into or shipment 
between the continental United States. Thus, MOUs cannot be utilized 
for authorizing import or shipment between the enumerated 
jurisdictions. We have provided information online that helps people 
who are requesting a permit understand and navigate the process at 
https://www.fws.gov/node/266100. The Service is committed to processing 
permit applications as quickly as possible to minimize any delay or 
disruption of legitimate activities. Permit applications can be found 
here: https://fws.gov/service/3-200-42-import-acquisitiontransport-injurious-wildlife-under-lacey-act.
    (44) Comment: A commenter recommends that, to receive a permit to 
transport potentially infectious (non-inactivated) material, be it live 
or dead salamanders, parts of dead salamanders, or biological samples, 
one of the requirements should be proving absence of infection with 
Bsal. To acquire a permit, the sender or receiver or both would have to 
quarantine the salamanders or other material (and demonstrate that the 
quarantine measures are adequate to contain spread of the pathogen), 
sample a percentage of the total number of animals or biologic 
materials to be shipped, and submit those samples, such as skin swabs 
from live or dead non-fixed salamanders, to a diagnostic laboratory for 
PCR testing. Permit granting would depend upon confirmation of the 
negative status of the animals or biologic materials.
    Response: While testing of specimens and live animals before moving 
them would be advisable, testing could not be a prerequisite for 
receiving a permit at this time because the details of reliable testing 
from all exporting countries have not been confirmed. And, as mentioned 
in IV. Second Interim Rule below, interstate transport between States 
within the continental United States is not prohibited under the 
current prohibitions of 18 U.S.C. 42(a) for the listed salamanders, 
making the requirement not necessary for many domestic shippers. We 
recommend that salamander transporters conduct best practices to reduce 
the risk of introducing, transporting, or spreading Bsal within the 
United States.
    (45) Comment: The 2016 interim rule should be amended to allow 
accredited veterinary medical diagnostic laboratories to exchange, 
receive, and accept live or dead specimens, including parts of the 201 
listed species, without the requirement of first obtaining a Federal 
permit. The first step in any Bsal response is to obtain an accurate 
and confirmed diagnosis of Bsal. Requiring accredited labs to first 
obtain a permit is an unnecessary burden that slows the diagnostic 
process and any confirming diagnostic testing at different labs.
    Response: We agree that the first step to any Bsal response is 
obtaining accurate diagnosis of Bsal. However, a permit is no longer 
necessary for shipment between States within the continental United 
States, as explained below in the preamble to this final rule.
    (46) Comment: The double-containment requirements for transport and 
storage and uncertainties therein are concerning. More explicit 
guidance is requested regarding the double-containment requirements for 
transport, housing, or storage, or handling of animals, tissues, or 
other samples. Specifically, how does this requirement apply to species 
repatriation projects or State-approved releases of injurious listed 
salamanders back into the wild? Many States conduct health testing (in 
collaboration with diagnostic lab partners) and have established 
standards that must be met before repatriation is conducted. Such 
State-sponsored activities should be exempt. Another solution is to 
permit exemptions for double containment of fixed tissues, where the 
threat of Bsal transmission is removed by virtue of the fixative agent.
    Response: The Service posted additional guidance on our website 
that includes further discussion about the ``double escape-proof'' 
containment for live animals and samples (https://www.fws.gov/node/266100). It is possible, however, in situations where live animals have 
been permitted and for which the ``double escape-proof'' containment 
requirements would apply, that repatriation would run counter to that 
requirement. This is the first time that native species that might be 
part of repatriation or recovery efforts have been listed as injurious. 
Because injurious wildlife must be carefully handled, all of the 
containment requirements must be met when salamanders are in captivity. 
However, the Service will work with people or institutions that are 
involved in State-approved repatriation efforts to facilitate these 
efforts. Finally, we clarify in A. Background in II. Final Rule to the 
2016 Interim Rule that preserved tissues are not considered injurious.
Other Impacts
    (47) Comment: Collection of fishes for shipment cannot totally 
ensure that other species of ``free riders,'' such as non-marketed 
amphibians, are not unintentionally included in the shipment process. 
Unintentionally including a single regulated amphibian, regardless of 
whether it is infected with Bsal, would subject the transporting farmer 
to severe civil and even criminal penalties. Notably, actual interstate 
transport of Bsal by some means not including a listed amphibian would 
not violate the rule.
    Response: As explained in the final rule, interstate transport 
prohibitions have been clarified. We encourage anyone who transports 
live fishes to use best management practices that include transporting 
only the traded species and their uncontaminated media. Unintentional 
importation or transport between the enumerated jurisdictions in the 
shipment clause of 18 U.S.C. 42 (the continental United States, the 
District of Columbia, Hawaii, the Commonwealth of Puerto Rico, and any 
territory or possession of the United States), which are also set forth 
at 50 CFR 16.3, through nursery stock or other pathways would also be a 
violation of the prohibitions from listing.
Inaccurate or Incomplete Science
    (48) Comment: The rule does not account for pressures that 
amphibians are already facing, such as habitat loss, rising 
temperatures, pesticide use, and siltation from agriculture. The 
Service's focus should be on the systematic degradation of the 
ecosystems in which the amphibians live and the capacity of the 
salamanders to fight the fungus.
    Response: The Service noted in the rule that salamanders may 
demonstrate more severe clinical disease when infection is combined 
with additional stressors in the wild. The comment does not provide any 
evidence of how habitat loss, rising temperatures, pesticide use, and 
siltation from agriculture diminishes the need for or benefits of the 
rule that may prevent salamander

[[Page 2185]]

mortality. Native salamander species known to be negatively affected by 
Bsal infection under experimental conditions may demonstrate more 
severe clinical disease when infection is combined with additional 
stressors in the wild, as has been found for other diseases. Besides 
this rule, the Service is engaged in many other conservation measures 
designed to help improve and protect salamander habitats across the 
United States.
    (49) Comment: Using a method of infecting a salamander from one 
genus with Bsal in a laboratory setting and then extrapolating results 
to all species within that genus is not in conformance with the 
framework of the World Organisation for Animal Health code or the 
National Aquatic Animal Health Plan (National Aquaculture Health Plan 
and Standards) for the United States and is contrary to the credible 
scientific findings of Martel et al. (2014). Therefore, the 2016 
interim rule is arbitrary and capricious in violation of the APA. In 
addition, other aquatic diseases have shown laboratory infection, but 
the affected fish species are not included in regulatory lists.
    Response: The WOAH has a different purpose than the injurious 
wildlife listing provisions of the Lacey Act, and the standards the 
WOAH uses are appropriate for their purposes. We followed the standards 
in 18 U.S.C. 42 and the APA. The issue of fishes that may carry 
diseases is beyond the scope of this rulemaking. Surrogate species are 
used elsewhere in the 2016 interim rule, such as for Bd for where 
information is lacking for Bsal and is common in scientific literature.
    (50) Comment: The spread dynamics of Bd and Bsal are considerably 
different. Given that Bd is endemic to the United States, the estimated 
potential for Bsal distribution has been overestimated. This 
overestimation is confirmed by salamander import data, the lack of 
presence of Bsal in animals entering the United States, and its lack of 
presence in wild populations.
    Response: The commenter states that Bd originated in the United 
States and is therefore endemic. We agree that Bd has occurred in the 
United States for many years and is currently ubiquitous throughout 
North America; however, we do not consider Bd endemic to the United 
States. For reasons identified in the 2016 interim rule and this second 
interim rule, we conclude that Bsal does pose a risk to native 
salamander populations. We have updated the research cited and still 
conclude that there is a risk of Bsal entering the country with 
salamanders, and that risk is greatly reduced by listing the genera in 
this rule.
    (51) Comment: The 2016 interim rule reports that there is no 
accurate way to test for or eliminate Bsal in captivity. PCR-based 
testing has been well established for many years for the related Bd and 
has been effectively demonstrated for Bsal. Effective measures for 
clearing salamanders using heat alone or heat in conjunction with anti-
fungal medications have also been published. The authors of both of 
those studies have reiterated in personal communication that the stated 
Service position in the rule justification is contradictory to the 
published data. Another comment noted that combined experience from 
members of Caudata.org in the captive maintenance and breeding of the 
species subject to this rule has shown that the temperatures required 
by these treatments are safe and will not harm the majority of 
salamanders of the Salamandridae, the family containing the bulk of the 
regulated species.
    Response: While the comments do not provide any information on how 
the Service's finding is contradictory to the published data, the 
second interim rule clarifies these issues. We have revised the rule to 
note that testing and prophylactic treatments of imports of salamanders 
to manage Bsal are available but have uncertain effectiveness when 
applied as a nationwide regulatory tool by the Service.
    (52) Comment: There is likely no Bsal in the United States, even 
with the huge numbers of salamanders that have recently been imported, 
because it gets too hot in the summer and too cold in the winter.
    Response: As discussed under Bsal Risk Assessment, we found that 
there is a significant risk that Bsal can establish and spread in the 
United States. Some areas, such as south Florida, are likely to have 
low consequences from Bsal introduction, in part due to temperatures 
found in the region. The areas most likely to have consequences from 
Bsal introduction are the Pacific Coast and Appalachian Mountains 
(Richgels et al. 2016). Based on environmental suitability, areas of 
the United States most suited to Bsal growth (Blooi et al. 2015a), 
including the Southwest, Southeast (except south Florida as just 
noted), and Pacific regions, are also the areas of highest salamander 
diversity. The large land mass of the United States has a broad range 
of climates, many of which are similar to the other continents where 
Bsal is currently found.
    (53) Comment: The Service did not publish the text of articles or 
the risk assessment it used for the 2016 interim rule.
    Response: The file for the references used, as well as other 
supporting information used to develop the 2016 interim rule, was 
posted under ``Supporting & Related Material'' in https://www.regulations.gov (Docket No. FWS-HQ-FAC-2015-0005), and is available 
for public inspection as noted under ADDRESSES in the 2016 interim 
rule. Comments and materials we received, as well as citations for 
supporting documentation we used in preparing the interim rule, were 
available for public inspection. The texts of publications are often 
covered by copyright laws and those are therefore not posted.
    (54) Comment: Species from the genera Ambystoma and Gyrinophilus 
were not listed because they were tested and proved resistant to Bsal. 
Why then were all Plethodon listed, since the one species tested (P. 
glutinosus) was also demonstrated to be resistant?
    Response: We did not believe that there was enough evidence to list 
Ambystoma or Gyrinophilus at the time of the 2016 interim rule, but we 
found evidence to support listing Plethodon. Three native salamander 
species identified as resistant to Bsal infection included the spring 
salamander (Gyrinophilus porphyriticus), marbled salamander (Ambystoma 
opacum), and spotted salamander (A. maculatum) (Martel et al. 2014). At 
the time the public-comment period closed, there was no evidence that 
any species within these genera are carriers of Bsal. We discuss our 
reasoning for listing all Plethodon species in the second interim rule 
under Vulnerability and Carrier Status. In short, however, further 
histological analysis of the slimy salamander revealed that Bsal could 
invade the skin long enough to move or transmit the pathogen to other 
salamanders. No such evidence existed then or now for any species in 
the genus Gyrinophilus; therefore, we are not listing species from that 
genus. As explained in the second interim rule under Vulnerability and 
Carrier Status of Native Species, we have evidence now of carrier 
capability for Ambystoma maculatum, A. mexicanum, and A. opacum and are 
listing the genus.
    (55) Comment: In Europe, where Bsal is believed to have been 
introduced by Asian imports, Bsal was found in populations of 
Salamandra and Alpine newts (Ichthyosaura alpestris) in the Netherlands 
and in Belgium. It has also been found in captive Salamandra in the 
United Kingdom and Germany, and

[[Page 2186]]

possibly in wild German populations. Martel et al. (2014) shows that 
most lethally vulnerable species exposed to Bsal in the lab showed 
signs of infection within 8 days and were dead within 3 to 4 weeks. 
This means that non-resistant infected species in captive collections 
would have died during the comment period on the 2016 interim rule.
    Response: The comment suggests that there are no specimens carrying 
Bsal at this time that might enter the United States and allow Bsal to 
be introduced, establish, and spread, but does not provide evidence 
that we can use in our analysis of the rule. Lethally vulnerable 
specimens can still appear if the pathogen spreads, or if Bsal persists 
in tolerant or susceptible populations or carcasses.
    (56) Comment: The 2016 interim rule states that surveys of anglers 
have indicated that they routinely release salamanders into the areas 
where they fish, which includes areas that are not part of the 
salamanders' native U.S. habitats, suggesting that animals are 
routinely moved long distances. No similar survey data exists for pet 
owners, so assuming the pet trade is the problem for releases is 
unfounded and targeting the pet trade simply because it is an easy 
target is unjust.
    Response: Our statement relating to anglers was used to note that 
this invasion expansion pathway has been attributed to the use and 
subsequent release of salamanders used as fishing bait. Along with the 
other evidence we documented, we found that there is the potential for 
salamanders carrying Bsal to escape or be released into the wild where 
they can transmit the pathogen to native species. We provided evidence 
in the rule that we used to conclude that international trade is the 
main pathway for the global spread of Bsal.
Additional Science Needed
    (57) Comment: Several areas would benefit from further 
investigation. For example, the origins of Bsal in wild salamanders 
needs to be better understood. It is important to continue and expand 
testing of salamanders in the wild and in trade in various locations. 
Additional testing of species within the same genus would be beneficial 
to guide field and collection surveillance.
    Response: Since the 2016 interim rule was published, many studies 
have been published that address the commenter's concerns and are 
applicable to the rule, including a major surveillance of salamanders 
in the wild by the USGS. We have reviewed the studies, and they support 
our final and second interim rules. We agree that additional science 
will help address issues related to better understanding of this 
pathogen and preventing its introduction into the United States, but we 
understand the need to take action now to list the species in the 
genera in this rule to prevent the introduction, spread, and 
establishment of Bsal.
Economic and Trade Data
    (58) Comment: If the salamanders are already here, and Bsal is not, 
then that means that any salamanders traveling across State lines pose 
no risk. This law estimates that it will cause $3.8 million in damage 
to the U.S. economy, mostly in the small business sector (``Regulatory 
Flexibility Act,'' paragraph nine). Those numbers could be greatly 
lessened if interstate travel were allowed.
    Response: As explained above in III. Final Rule to the 2016 Interim 
Rule in A. Background and D. Required Determinations, the current 
prohibition on interstate transport in 18 U.S.C. 42(a) has been 
clarified and does not apply to interstate transport between States 
within the continental United States. Thus, the costs incurred are 
expected to be less than originally estimated in the 2016 draft 
economic analysis.
    (59) Comment: Caudata.org conducted an online public survey from 
February 1 to March 12, 2016, to gather additional data of U.S. 
domestically bred animals. A total of 797 respondents to the survey 
reported shipping 25,649 domestically bred caudates across State lines 
in 1 year. Due to the low response rate relative to the number of U.S. 
registered members on Caudata.org (8 percent) and the short duration of 
the survey, this number likely represents a small fraction of the 
actual trade. It can be safely extrapolated that the Service has 
underestimated the trade in captive-bred newts and salamanders by at 
least two orders of magnitude. Caudata.org is uniquely situated at the 
interface of hobbyists, entrepreneurs, researchers, zoos, and 
aquariums. A summary of that data and some important numbers are 
presented here. Respondents to the survey possessed a total of 28,228 
domestically bred salamanders or newts, the majority of which are 
subject to the rule. Respondents shipped on average 25,649 salamanders 
or newts over State lines per year. This number is nearly two orders of 
magnitude greater than the ``338'' cited by the rule and represents 
just a small fraction of our members. The total yearly salamander- and 
newt-related revenue reported by our respondents was $207,528 for 2015.
    The commenter further stated that Caudata.org has more than 10,000 
unique registered U.S. members who have accessed their website in the 
past 5 years. Their total number of unique U.S. visitors (people who 
did not register for an account) in that time is orders of magnitude 
greater than this number. The commenter stated that, apparently, the 
Service did not perform due diligence in ascertaining the number of 
private U.S. citizens affected by this rule.
    Response: While we did obtain data from the Pet Industry Joint 
Advisory Council (PIJAC; currently known as the Pet Advocacy Network) 
for the 2016 interim rule, we appreciate Caudata.org for supplying 
additional data. The survey does not indicate: (1) whether the 
salamanders are domestically bred; (2) the net importation for each 
State; or (3) what species they are. Since the survey data did not 
include information on species or whether they are transported between 
the listed jurisdictions, it is unknown if any of the revenue discussed 
would be lost due to prohibitions under the rule. Consequently, the 
data are not used in the final economic analysis for the 2016 interim 
rule. Furthermore, unlike the 2016 interim rule, the final rule 
clarifies that the current prohibition on interstate transport in 18 
U.S.C. 42(a) does not apply to interstate transport between States 
within the continental United States.
    (60) Comment: The economic figures provided by the Service are a 
gross understatement. Caudata.org has submitted the results of a survey 
on the numbers of animals sold across State lines, and just from their 
members, reported roughly $207,528 in income. Actual figures are 
probably much higher, given that this amount likely represents just a 
portion of the trade in the entire United States, and Caudata.org 
pertains only to captive-bred animals. In addition to the money spent 
purchasing animals, there's also food, lighting, enclosures, plants, 
decorations, filters, shipping and packaging fees, and other costs 
associated with keeping salamanders. To house a pair of salamanders can 
cost $100 to $200 or more, with ongoing feeding costs. Overall, the 
U.S. salamander hobby probably represents well over $5 million to $10 
million in economic activity each year.
    Response: Regarding the Caudata.org data, see also response to 
Comment 59. The economic analysis addresses primary support services 
(such as food and shipping) and secondary economic impacts in Sections 
2.3.2 and 3.1.3, respectively.

[[Page 2187]]

    (61) Comment: The 2016 interim rule states that ``a minimum of 338 
domestically bred salamanders may be affected due to the interstate 
transportation prohibition.'' As an individual, the commenter has 
legally shipped 150-plus live specimens (eggs, larvae, and adults) in a 
single year and knows that many more people legally ship more specimens 
than that amount in the same period. The commenter has also received 
dozens of animals in a single year and knows that this occurrence is 
not unique. Many individuals will be affected by the listing.
    Response: The minimum is based on available data from PIJAC and is 
stated as a minimum due to the expectation of the actual number being 
potentially larger. For this salamander breeding data, it is unclear 
which species are shipped and whether these specimens are shipped 
between listed jurisdictions. Unlike the 2016 interim rule, the final 
rule clarifies that the current prohibition on interstate transport in 
18 U.S.C. 42(a) does not apply to interstate transport between States 
within the continental United States. Therefore, it is not incorporated 
into the final economic analysis.
    (62) Comment: Many small businesses have commented that the 
prohibition on interstate transport will have a greater impact than the 
Service anticipates. In the 2016 interim regulatory flexibility 
analysis, the Service stated that it does not believe that the impact 
of prohibiting interstate transport will be significant. However, 
several small breeders and hobbyists involved in selling salamanders in 
the United States have indicated a substantial domestic trade in 
salamanders. The U.S. Small Business Administration Office of Advocacy 
commented that a small business representative indicated that this 
number could be as high as 1,500 specimens shipped in a year for 
certain businesses. The difference between the limited information in 
the analysis and the information provided by commenters indicates that 
the analysis underestimates the effect of the prohibition of interstate 
transport.
    Response: As explained above in III. Final Rule to the 2016 Interim 
Rule in A. Background, the current prohibition on interstate transport 
in 18 U.S.C. 42(a) has been clarified and does not apply to interstate 
transport between States within the continental United States. 
Therefore, the interstate data provided are not incorporated into the 
final economic analysis and final regulatory flexibility analysis. As 
discussed in Comment 61, salamander breeding data that are submitted 
without specific details regarding species type are too general to be 
incorporated into the final economic analysis. It is possible that the 
domestic market is more robust than estimated. However, it is unclear 
whether any additional sales are related to species that are listed or 
not listed under the rule.
    (63) Comment: Many breeders who produce these animals as their main 
source of income will lose significant income or go out of business 
without the ability to sell across State lines. For example, last year, 
a business owner produced more than 100 neotenic Ichthyosaura 
alpestris, and this year [2016] they will have to cull those eggs in 
light of the prohibition.
    Response: The comment is incorrect that they will have to cull 
eggs, because eggs of listed salamander species are not considered 
injurious because they do not have the potential to serve as carriers 
of Bsal. Furthermore, as explained above in III. Final Rule to the 2016 
Interim Rule in A. Background, the current prohibition on interstate 
transport in 18 U.S.C. 42(a) has been clarified and does not apply to 
interstate transport between States within the continental United 
States after April 7, 2017. Therefore, the interstate data provided are 
not incorporated into the final economic analysis and final regulatory 
flexibility analysis.
    (64) Comment: Many States also prohibit or limit sale by biological 
supply companies of certain native species, and the authority to 
regulate nonnative species may be either with the State fish and 
wildlife agency or the State's department of agriculture or shared in 
some instances. For example, commercial production of native 
salamanders is currently not legal in California, and the State's 
department of agriculture does not regulate or track production or sale 
of nonnative salamanders in the State. The only way to legally sell 
native salamanders in California is as a biological supply house with a 
permit to collect wild specimens for sale to scientific and educational 
facilities. Only one business is currently in possession of this 
permit, and it has not collected or sold salamanders.
    Response: We appreciate the information.
    (65) Comment: One commenter's company produces about 1,000 
Neurergus kaiseri, 100 N. crocatus, 100 N. strauchii, and 200 
Ichthyosaura alpestris a year.
    Response: We appreciate the commenter supplying domestic breeding 
data. It has been incorporated as appropriate into the appendix to the 
final economic analysis.
    (66) Comment: An international prohibition on trading gives small-
time breeders within the United States an economic boost to supply the 
demand for these pets.
    Response: We acknowledge that an international prohibition can have 
an indirect effect of reducing competition for domestic breeders in 
some markets. The rule was not implemented to provide an advantage to 
domestic breeders but rather to prevent Bsal introduction, 
establishment, and spread in the United States by salamander species 
that are carriers of the pathogen.
    (67) Comment: The Service estimates that, without the 2016 interim 
rule, 217,000 salamanders would be imported each year. These imports 
will be prohibited if the 20 genera are listed under the Lacey Act as 
set forth in the 2016 interim rule. The Service further estimates that 
338 domestically bred salamanders would be affected by the interstate 
transportation prohibition per year, resulting in impacts to domestic 
breeders of up to $23,000. These domestic production numbers do not 
pass a straight-face test; for the estimate to be accurate, each 
salamander would need to be worth an average of $68. In reality, 
salamanders typically sell for between $10 and $50, depending on the 
species. As several USARK members and others in the herpetoculture 
industry have reported to the Service in written comments, including 
trade numbers provided by Caudata.org, the actual number of 
domestically bred salamanders shipped across State lines is far higher 
than 338. The species listed in the 2016 interim rule comprise the 
overwhelming majority of those in the pet trade, so the economic effect 
of the listing will amount to nearly the full total of the industry's 
value.
    Response: The minimum number for domestic production (338) and the 
corresponding prices for those salamanders were provided by PIJAC. The 
detailed data they provided is in table A1-2. Furthermore, after the 
2016 interim rule was issued, as explained above in A. Background in 
III. Final Rule to the 2016 Interim Rule, the current prohibition on 
interstate transport in 18 U.S.C. 42(a) has been clarified and does not 
apply to interstate transport between States within the continental 
United States.
Use of Categorical Exclusion
    (68) Comment: The interim rule is not possible without the recently 
implemented categorical exclusion that bypasses the requirement to 
consider economic and social impacts under the National Environmental 
Policy Act (NEPA). The decision to use the

[[Page 2188]]

categorical exclusion for the 2016 interim rule is flawed.
    Response: We determined the categorical exclusion for injurious 
wildlife listing, located in the Department of the Interior Manual at 
516 DM 8.5 C(9), applies to the action in accordance with the 
requirements of NEPA. The categorical exclusion does not bypass NEPA. 
We reviewed the rule under NEPA requirements and prepared an 
environmental action statement for the 2016 interim rule that was 
available for review (see ``Supporting & Related Material'' at https://www.regulations.gov under Docket Number FWS-HQ-FAC-2015-0005). Under 
NEPA, the human environment is interpreted comprehensively to include 
the natural and physical environment and the relationship of people 
with that environment (40 CFR 1508.14), and the economic or social 
effects are not intended by themselves to require preparation of an EIS 
(40 CFR 1508.14). We prepared a draft economic analysis and regulatory 
flexibility analysis separately as part of the required determinations 
under the APA for the 2016 interim rule and made them available for 
public comment. We determined that the regulations in that rule will 
not individually or cumulatively have a significant effect on the human 
environment.
Inaccurate Use of 18 U.S.C. 42(a)(1)
    (69) Comment: The use of the Lacey Act in this manner opens the 
door for similar regulations of other animals, such as dogs, cats, 
fishes, horses, and chickens. The list of species is infinite, as would 
be the economic impact they could have.
    Response: Under the authorities provided under the injurious 
wildlife provisions of the authorizing statute (18 U.S.C. 42), the 
Service can list only wild mammals, wild birds, fishes, mollusks, 
crustaceans, amphibians, and reptiles as injurious wildlife, meaning 
the Service cannot list domesticated species, thus eliminating the 
possibility to list domesticated dogs, domesticated cats, domesticated 
horses, and domesticated chickens.
    (70) Comment: Congress has never interpreted the Lacey Act to apply 
to shipment between States within the continental United States.
    Response: After the 2016 interim rule was issued, as explained 
above in III. Final Rule to the 2016 Interim Rule, A. Background, the 
current prohibition on interstate transport in 18 U.S.C. 42(a) has been 
clarified and does not apply to interstate transport between States 
within the continental United States. The final rule has been modified 
consistent with the prohibition in the shipment clause of 18 U.S.C. 42, 
which has been codified in Federal regulations at 50 CFR 16.3, for 
transport between the enumerated jurisdictions (the continental United 
States, the District of Columbia, Hawaii, the Commonwealth of Puerto 
Rico, and any territory or possession of the United States).
    (71) Comment: Although the pet trade is primarily regulated by USDA 
agencies, including the Animal and Plant Health Inspection Service, 
requirements for the movement of pets across State lines are generally 
reserved to individual States. Furthermore, courts have often found 
individual animals to be exempt from livestock regulations that would 
otherwise apply when those animals are characterized as household pets. 
Salamanders in the pet trade should similarly not be considered 
``wildlife'' for purposes of Federal regulation of interstate 
transport. Other commenters also stated that the Service should defer 
this issue to another agency with additional resources for controlling 
importation (such as the USDA) because the Service has stated that an 
injurious listing under the Lacey Act is their only means of attempting 
to control Bsal.
    Response: The provisions of 18 U.S.C. 42 make no distinction 
between pet salamanders and other salamanders. The purpose of listing 
these salamander species as injurious wildlife is to prevent the 
introduction, establishment, and spread of Bsal in the wild in the 
United States to protect wildlife and wildlife resources. The authority 
to take action to list species as injurious wildlife under 18 U.S.C. 42 
lies solely with the U.S. Department of the Interior.
    (72) Comment: The regulations promulgated in the 2016 interim rule 
restrict not only international and interstate transport but any 
movement whatsoever of the listed genera. The regulatory language 
prohibits the importation, transportation, or acquisition of any live 
or dead specimen, including parts, but not eggs or gametes, of the 
genera. There is simply no authority in the Lacey Act to prohibit 
acquisition. Because the Lacey Act does not forbid acquisition of a 
listed animal, the interim regulation is beyond the law to the extent 
it purports to prohibit the same. The Service must amend the 2016 
interim rule to clarify that the prohibitions do not apply to 
intrastate activities.
    Response: Under the Lacey Act Amendments of 1981, 16 U.S.C. 
3372(a)(1), it is unlawful among other things for any person to sell, 
receive, acquire, or purchase any wildlife transported in violation of 
any law of the United States. This includes acquiring any injurious 
wildlife imported into the United States or transported between the 
enumerated jurisdictions in violation of the shipment clause of 18 
U.S.C. 42 (the continental United States, the District of Columbia, 
Hawaii, the Commonwealth of Puerto Rico, and any territory or 
possession of the United States), also set forth at 50 CFR 16.3. The 
conditions of injurious wildlife permits may also place limitations on 
subsequent sale or transfer of injurious wildlife under the permit 
without prior authorization from the Service. Those activities are in 
connection with transport of injurious wildlife between the listed 
jurisdictions in the shipment clause or import into the United States 
under 18 U.S.C. 42. It is the responsibility of a person who may be 
engaged in salamander acquisition to be aware of any Federal, State, 
Tribal, or territorial law or regulation that applies to that activity.
    The rule adding injurious salamanders to the lists of species does 
not change the scope of the prohibitions in 18 U.S.C. 42, 16 U.S.C. 
3372, 50 CFR 16.3, or otherwise found in 50 CFR part 16. The regulatory 
language referenced by the commenters (50 CFR 16.14) is identical to 
longstanding, existing language that appears at 50 CFR 16.11, 16.12, 
16.13, and 16.15. Revision of the general regulations found at 50 CFR 
part 16 is beyond the scope of this rulemaking.
    (73) Comment: The Lacey Act defines ``transport'' as ``to move, 
convey, carry, or ship by any means, or to deliver or receive for the 
purpose of movement, conveyance, carriage, or shipment.'' Even if the 
law did authorize the Service to bar personal transport, which it does 
not, this definition would reach solely intrastate activities. Although 
the Service has agreed that States, not the Service, have the power to 
regulate ownership and sales within their borders, the commenter is 
concerned that the Service is laying the groundwork to involve itself 
in Federal regulation of wholly intrastate activities.
    Response: The definition quoted by the commenter applies to the law 
codified at 16 U.S.C. 3371(j), also known as the Lacey Act Amendments 
of 1981. Consistent with this definition, Service regulations also 
provide a definition of transport found in 50 CFR 10.12. It is the 
responsibility of a person who may be engaged in salamander 
transportation to be aware of any Federal, State, Tribal, or 
territorial law or regulation that applies to such activity. For 
further information see also response to Comment 72.

[[Page 2189]]

Interim Rule Is a Regulatory Taking
    (74) Comment: The Service evaluated the 2016 interim rule and 
determined that it does not constitute taking. This conclusion is 
facially false--a restriction on interstate travel with a family pet 
not only is impermissible under the law, but most certainly denies the 
pet owner enjoyment and companionship (amounting to use) of that pet.
    Response: Import and transport of injurious wildlife between the 
enumerated jurisdictions in the shipment clause of 18 U.S.C. 42 (and at 
50 CFR 16.3) of any of the listed species is prohibited. The provisions 
of 18 U.S.C. 42(a) do not prohibit any person who owns one of the 
listed species at time of listing from continuing to possess the 
species (such as listed salamanders) or engaging in transport and other 
activities within the enumerated jurisdictions of the shipment clause, 
as allowed under State, Tribal, or territorial law. Therefore, we 
concluded that the 2016 interim rule and this final rule do not 
constitute a regulatory taking. This action is consistent with all 
previous injurious wildlife listings that have affected listed species 
that members of the public might have owned at the time of listing. It 
is the responsibility of a person who may be engaged in salamander 
transportation to be aware of any Federal, State, Tribal, or 
territorial law or regulation that applies to that activity.
Federalism Assessment Under Executive Order 13132
    (75) Comment: Under Executive Order 13132, the 2016 interim rule 
requires a federalism assessment as the rule's provisions have 
significant federalism effects and will have several direct effects on 
States, which have primary jurisdiction over native wild animals not in 
captivity. The regulation of the movement of pets across State lines is 
reserved to individual States. Under Executive Order 13132, this 
interim rule does have sufficient federalism implications to warrant 
the preparation of a federalism assessment.
    Response: A federalism assessment is not required. Executive Order 
13132 says that policies that have federalism implications refer to 
regulations, legislative comments, or proposed legislation, and other 
policy statements or actions that have substantial direct effects on 
the States, on the relationship between the national government and the 
States, or on the distribution of power and responsibilities among the 
various levels of government. This rule does not limit the policymaking 
discretion of the States or preempt State law. The States are not 
restricted from also regulating the transport of listed salamanders or 
other activities related to such species within their State boundaries, 
such as sale or possession. The commenter did not provide evidence 
showing how the rule would be a substantial direct action impacting the 
States.
Law Enforcement Issues
    (76) Comment: Salamanders will be smuggled into the country or sold 
through the black market once they are prohibited, as all contraband 
inevitably is, with no regard for fungal safety or often the health of 
the animals. One commenter noted that they have received messages from 
overseas asking them to illegally ship animals, with instructions for 
how to package and ship animals to demonstrate how easy it is to do so. 
The rule will not prevent Bsal from entering the United States.
    Response: The injurious wildlife provisions of 18 U.S.C. 42 serve 
an important role in protecting humans, the interests of agriculture, 
horticulture, and forestry, and the wildlife or wildlife resources of 
the United States from injurious wildlife. The rule is intended to 
reduce opportunities for Bsal to spread disease to native species in 
the wild. As previously explained, the listing of salamander species 
that may be carriers of Bsal results in prohibitions on import and 
transport between the enumerated jurisdictions in the shipment clause, 
and violations of these prohibitions are subject to strict liability, 
18 U.S.C. 42(b) (Whoever violates this section, or any regulation 
issued pursuant thereto, shall be fined under this title or imprisoned 
not more than six months, or both.). Additionally, pursuant to 18 
U.S.C. 42(a)(1), all prohibited injurious wildlife imported or 
transported in violation of the Lacey Act ``shall be promptly exported 
or destroyed at the expense of the importer or consignee.'' Where 
applicable, penalties may also be assessed under the Lacey Act 
Amendments of 1981, 16 U.S.C. 3371 et seq. Although we acknowledge that 
some unscrupulous dealers may take advantage of people or engage in 
illegal trade, the regulatory provisions we are promulgating play an 
important role in deterring and, as necessary, penalizing and remedying 
unlawful activity, in order to protect the interests under the Act. We 
strongly encourage compliance with the law, and we may take appropriate 
enforcement action against violations that may occur. However, our 
experience is that pet owners prefer to be responsible, law-abiding 
citizens and would make informed decisions not to engage in import or 
transport contrary to the Lacey Act and thereby reduce the risk of 
spreading Bsal.
    (77) Comment: The final rule will subject exhibitors, nature 
centers, wildlife rehabilitators, private citizen hobbyists, and 
commercial breeders to Federal prosecution and penalties from felonies 
under the Lacey Act.
    Response: The interstate transport language in 18 U.S.C. 42 is 
clarified in A. Background in III. Final Rule to the 2016 Interim Rule. 
Prohibitions remain for importation and transportation between the 
enumerated jurisdictions of 18 U.S.C. 42, also listed in 50 CFR 16.3. 
Violations of the injurious wildlife listing prohibitions are a 
misdemeanor, not a felony.
    (78) Comment: For salamander species not listed as injurious, the 
final rule should incorporate authority for the Service to collect Bsal 
samples from any shipment where dead animals are present upon 
importation. This is a noninvasive procedure, and these data are needed 
to help modify this rule in the future if additional Bsal carrier 
species are discovered. The presence of dead salamanders upon 
importation can be a smoking gun for the presence of Bsal (and other 
harmful pathogens).
    Response: The recommended action is outside the scope of this final 
rule relating to the listing of injurious wildlife under 18 U.S.C. 
42(a).
    (79) Comment: A Federal ban on interstate movement of salamanders 
is unenforceable given the Service's resource limitations. Many of the 
exotic caudate species listed as injurious are already widely 
distributed in private collections in virtually every State. There is 
no system in existence (or resources to create a system) to register or 
effectively monitor their numbers or locations.
    Response: The Federal ban was lifted in 2017 as the result of a 
Federal court decision regarding the interpretation of the statute 18 
U.S.C. 42(a). This final rule has been amended to address interstate 
transport as explained above in III. Final Rule to the 2016 Interim 
Rule in A. Background and D. Required Determinations. Whether a Federal 
ban on interstate movement is enforceable is beyond the scope of this 
rule.
    (80) Comment: Regulation alone will not put a halt to the 
international and interstate traffic in species listed as injurious 
under the Lacey Act or under various State regulations. Accordingly, 
adequate law enforcement, especially at ports of entry, is critical to 
manage the ongoing, and possibly increased, volume of underground 
traffic in regulated wildlife. The commenter

[[Page 2190]]

encourages building cooperative partnerships between State and Federal 
enforcement agencies to increase capacity and to capitalize on the 
specific expertise that the respective programs can bring to bear on 
this problem.
    Response: We agree. The Service's Law Enforcement Office has a 
longstanding relationship with Customs and Border Protection and USDA 
inspectors regarding cooperation for enforcement on the borders. The 
Service's law enforcement officers at ports have and will continue to 
maintain strong working relationships with their State counterparts.
    (81) Comment: The trade in species not listed by the rule needs to 
be monitored. The rule's prohibitions of the vast majority of commonly 
traded species may inadvertently create a new legal market for species 
not previously in demand by the salamander trade community. Those newly 
traded species could be carriers of Bsal.
    Response: The Service collects information on all imported 
salamanders, listed or otherwise. This situation will not change with 
the listing of the species in this rule as injurious wildlife. This 
rule does not preclude the ability to take additional regulatory 
actions if new information emerges.
    (82) Comment: There was a push to acquire species before the 
prohibition could go into effect after it was announced. Prior to the 
ban, some people would have only purchased captive-bred or long-time-
in-captivity amphibians. Due to the prohibition, they stepped out of 
their comfort zone and purchased wild-caught salamanders.
    Response: The comment supports the Service's decision to implement 
an effective date of 15 days after the date of publication for the 2016 
interim rule and again for the second interim rule. We wanted to give 
shipments in transit or pending transit the time needed to complete the 
travel for the welfare of the live animals, but we did not want to 
encourage a rush to import over a longer period. Purchasing a wild-
caught salamander listed under this rule is not prohibited under 18 
U.S.C. 42, provided transport of the specimen occurs only within an 
enumerated jurisdiction of 18 U.S.C. 42 (also listed at 50 CFR 16.3) 
and complies with any permit condition for a specimen traded under an 
injurious wildlife permit. It is the responsibility of a person who may 
be engaged in salamander acquisition to be aware of any Federal, State, 
Tribal, or territorial law or regulation that applies to that activity.
Alternatives to the 2016 Interim Rule
    (83) Comment: Numerous commenters recommended health certification 
as an alternative to the injurious wildlife listing. For example, a 
commenter urged the Service to reconsider the listing of the 201 
salamander species, and instead to employ models proven effective by 
USDA's Animal and Plant Health Inspection Service, such as utilization 
of certificates of veterinary inspection, pre- or post-import 
quarantine and treatment, import permits, and import restrictions based 
on risk assessments for given countries of origin. Another commenter 
urged the Service and other relevant agencies to work with its members 
to develop immediate measures to allow for preventive treatment and 
certification, without causing undue personal impacts.
    Response: While we do work collaboratively with the USDA and 
nongovernmental organizations on many invasive-species issues, the 
authority to list species as injurious wildlife under 18 U.S.C. 42 lies 
with the U.S. Department of the Interior. Although some countries may 
have the necessary skills to prepare a health certificate that 
salamanders are free of Bsal, not all exporting nations may have the 
necessary skills or resources. Scientists and diagnostic laboratories 
are also working to standardize laboratory protocols. Please see 
heading in the second interim rule on Ability To Prevent or Control the 
Spread of Pathogens or Parasites for more explanation. The Service will 
continue to seek opportunities to work with partners to ensure 
salamander conservation consistent with its mission but cannot commit 
to specific actions that do not fall under the scope of this 
rulemaking.
    (84) Comment: Related to other comments about establishing a 
certification system, the Service should consider establishing a permit 
from which the proceeds would help manage certification, testing, and 
conservation efforts and, therefore, could both help fund the program 
and make it more scientifically accurate.
    Response: While we are not establishing a certification system at 
this time under this rule, we acknowledge that the general statutory 
authority to charge fees for processing applications for permits and 
certificates is found in 31 U.S.C. 9701, which states that services 
provided by Federal agencies are to be ``self-sustaining to the extent 
possible.'' Federal user-fee policy, as stated in Office of Management 
and Budget (OMB) Circular No. A-25 Revised, requires Federal agencies 
to recoup the costs of Federal activities that provide ``special 
benefits'' to identifiable recipients. Permits are special services, 
authorizing identifiable recipients to engage in activities not 
otherwise authorized for the general public. Please also see our 
response to Comment PR31.
    (85) Comment: Chain pet stores should be prohibited from selling 
salamanders because it is too hard to regulate them. Only specialty pet 
places and breeders that have a permit should be allowed to sell 
salamanders.
    Response: Regardless of the business size or type, as explained in 
the final rule, all import and transport of injurious wildlife between 
the enumerated jurisdictions in the shipment clause of 18 U.S.C. 42, 
codified in Federal regulations at 50 CFR 16.3, are prohibited for 
salamander species listed by this rule except by permit for authorized 
purposes. Otherwise regulating the sale of salamanders is not within 
the scope of this rulemaking. It is the responsibility of a person who 
may be engaged in salamander sales to be aware of any Federal, State, 
Tribal, or territorial law or regulation that applies to that activity.
    (86) Comment: A mandatory holding period for salamanders should be 
considered for transport across State lines. Studies show that if an 
animal is infected, it will die within a very short period. Only 
animals that test negative for Bsal should be allowed to be shipped. 
All animals in quarantine should also be treated to prevent infection 
and spread of Bsal, once reliable protocols are developed, as they have 
been for Bd (Pessier and Mendelson 2010). Quarantine efforts would 
facilitate both prevention of introduction and compliance.
    Response: Only lethally vulnerable species are expected to die in 
response to Bsal infection. Other species listed by this rule are also 
capable of carrying Bsal without lethal consequences and transmitting 
the fungus to native species. For these and other reasons discussed in 
this rule regarding certification and testing options, while research 
is ongoing, it is currently not feasible to establish such a system. 
The interstate prohibition has also been clarified as discussed in the 
second interim rule.
    (87) Comment: Consider instead a CITES import ban of all species of 
salamanders and newts, under the notion that CITES exists to protect 
endangered species. There are 35 species of amphibians that would be at 
risk of being wiped out entirely if Bsal

[[Page 2191]]

becomes introduced into the United States.
    Response: CITES exists for a different purpose from the injurious 
wildlife provisions of the Lacey Act, and the purpose and use of CITES 
is beyond the scope of this rulemaking.
    (88) Comment: The Service has not acknowledged nonregulatory 
approaches. The pet industry has taken voluntary action to halt the 
import of known carriers. For example, PIJAC called for an immediate, 
temporary moratorium of Oriental fire-bellied newt and paddle-tailed 
newts on November 20, 2015.
    Response: One of our alternatives (Alternative 1) involved taking 
no action on the Service's part. This is our status quo. We would not 
list any species of salamanders as injurious under this alternative. We 
did not select this option because of the significant risk that Bsal 
poses to native species and other wildlife resources in the United 
States. We expect that significantly greater financial and natural 
resources losses will be incurred by us and our partners in having to 
manage and respond to Bsal if the fungus establishes and spreads in the 
United States than by taking action now to prevent its introduction.
    While we appreciate and support voluntary conservation efforts, we 
concluded that regulatory action was necessary to ensure compliance and 
protect native species. For example, the voluntary moratorium called 
for by PIJAC affected only two not-listed species, even though more 
have been identified as carriers (Martel et al. 2014). The species with 
the highest number of imports into the United States from 2004 to 2014 
was the Oriental fire-bellied newt. This species comprised 54 percent 
of the total number of imported salamanders (USFWS OLE 2015). A review 
of LEMIS (Law Enforcement Management Information System) data in August 
2016 shows that there were no shipments after November 20, 2015, for 
Oriental fire-bellied newts declared to the Service, except for 6 
shipments totaling 539 live animals that occurred since the inception 
of the voluntary moratorium (all but 39 were before the rule took 
effect). This situation suggests that the rule is necessary because 
some importers, even if only a few, did not follow the voluntary 
moratorium and imported hundreds of specimens. However, since the 2016 
interim rule took effect and as of the end of 2020, no Pachytriton spp. 
salamanders (not listed) have been imported, and we recognize and 
appreciate the role that the PIJAC moratorium likely played.
    (89) Comment: Although Alternative 3 of the draft economic 
analysis, which declares 201 salamander species as injurious, is deemed 
most effective, the commenter suggests that Alternative 4, which 
declares all species of salamander as injurious, is necessary to fully 
prevent the spread of Bsal in the United States. Furthermore, the 
economic loss associated with Alternative 3 is estimated to be $10 
million, while the economic loss associated with Alternative 4 is $10.7 
million. The benefit of almost certainly preventing the spread of the 
fungus into the United States as provided by Alternative 4 far 
outweighs the marginal cost as compared to Alternative 3.
    Response: The expected increase in cost from Alternative 3 to 
Alternative 4 was not considered in our determination about the 
injuriousness of the species. The Service determined that there was 
unknown risk from genera where no species have yet been tested for Bsal 
and, therefore, could not list those genera at this time.
    (90) Comment: We need more citizen scientists to help with 
salamander conservation. Many knowledgeable hobbyists are available to 
assist if asked.
    Response: We recognize that the public can play a critical role in 
conservation; however, this comment is outside the scope of this 
rulemaking.
    (91) Comment: Put more funding into Bsal research to find a cure, 
treatments, and other ways of reducing the risk.
    Response: We recognize the important contributions made by Bsal 
research; however, this comment is outside the scope of this 
rulemaking.
    (92) Comment: As new evidence becomes available and while Bsal 
remains undetected in the United States, the commenter would like to 
see a proposed rule with a comment period for native U.S. species, 
rather than an interim final rule, before these new listings go into 
effect. For nonnative species, however, we would support other interim 
final rules to further reduce the chances of introduction via the 
importation pathway.
    Response: This second interim rule is adding new nonnative and 
native species to the injurious list. See above in III. Final Rule to 
the 2016 Interim Rule in A. Background. Also, several native species 
are raised outside the United States and then imported into the 
country; this supports the Service's decision to implement a nearly 
immediate effective date of 15 days for all species listed under the 
rule. See also response to Comment 24.
    (93) Comment: The costs to State fish and wildlife agencies to deal 
with pet salamanders that cannot be transported across State lines when 
the owner moves do not appear to have been evaluated and could place a 
significant burden on State agency staff that would be tasked with 
informing the public about the rules, working with rescues and zoos to 
provide rehoming opportunities, and law enforcement. The commenter 
would like to see a Service-administered education and outreach program 
that provides explicit instructions, and assistance, for pet owners to 
properly rehome or dispose of their salamanders. One commenter 
mentioned that the State of Florida has an Exotic Pet Amnesty Program 
in place that allows the public to surrender their regulated or 
unwanted exotic pets without penalty or cost. The commenter encourages 
continued Federal support of this program as an integral part of 
managing risks of nonnative introductions.
    Response: The interstate prohibition was clarified by a court 
decision in 2017 as explained in the final rule, so the costs for 
transporting across State lines between States within the continental 
United States is not an issue now, unless regulated by other State or 
Federal laws. We share concerns about the irresponsible re-homing and 
disposal of pet salamanders into the wild and are working with 
partners, including the industry, to help ensure that release does not 
occur. The Service has been a partner with the State of Florida's 
Exotic Pet Amnesty Program and will continue to work with other 
partners to help encourage the public not to release animals that they 
own into the wild. The Service does not have the funds necessary to 
implement a national amnesty and rehoming program.
    (94) Comment: In the past, increased restrictions on species 
already in widespread possession (personal and commercial) have been 
accompanied by additional releases (such as walking catfishes, 
snakeheads). The commenter recommends consideration of regulatory 
approaches with the flexibility to accommodate existing ownership. 
Further Federal restrictions, without this ``grandfathering'' approach 
for current pet owners, may lead to an increase in the rates of 
release.
    Response: The commenter offers no proof that releases have been 
caused by the new Federal regulation. The injurious wildlife provisions 
of the Lacey Act do not prohibit continued ownership of injurious 
wildlife that members of the public own at the time of listing. Under 
the injurious wildlife provisions of the Lacey Act, the Service is not 
authorized to grandfather in existing salamander owners as exempt

[[Page 2192]]

from subsequent activities that are prohibited with injurious wildlife, 
including import or transport between the enumerated jurisdictions.
    (95) Comment: Prohibit the use of amphibians as fishing bait. It 
has been shown that using animals, such as tiger salamanders, as 
fishing bait has led to species introductions (posing a major threat to 
California tiger salamanders) and the spread of disease, particularly 
Bd and ranaviruses. If Bsal ever enters the United States, it is far 
more likely to be spread through bait shops and fishermen than from 
hobbyists shipping to one another. Even if studies have shown tiger 
salamanders are unlikely to carry Bsal, the practice has already been 
shown to have spread other diseases, and other, more susceptible 
species may be used.
    Response: The request is beyond the scope of this rulemaking. The 
Service, under the injurious wildlife provisions of 18 U.S.C. 42, is 
not authorized to prohibit amphibians for use as fishing bait, unless 
they are imported, transported between the enumerated jurisdictions, or 
subject to injurious wildlife permits. We also note that the Service's 
State partners regulate fishing activities within their States and can, 
and often do, regulate use of amphibians for fishing bait.
    (96) Comment: Include a clause that if a North American species is 
determined to be a carrier or lethally infected, it will immediately be 
included in the prohibition, and any species screened and determined to 
be insensitive and not capable of carrying Bsal will be removed from 
the list in a timely manner.
    Response: The Service does not have authority to include or remove 
species on the injurious wildlife list without evidence regarding 
whether the wildlife is injurious to the interests protected under the 
Lacey Act. The determination of injuriousness is based on defensible 
scientific evidence. This rule does not preclude the ability to take 
additional regulatory actions if new information emerges. If a species 
is found to be incapable of carrying Bsal under all conditions, we may 
consider its removal from the injurious list by conducting an 
evaluation and promulgating a rule. Likewise, if a species is found to 
be a carrier of Bsal, we may consider its addition or the addition of 
its genus to the injurious list through this same regulatory process.
    (97) Comment: Continue exploring a clean-trade program for future 
emerging infectious diseases. As indicated in previous correspondence 
with the Service, the commenter has consistently supported the concept 
of a clean-trade program for salamanders imported into the United 
States rather than restricting interstate movement of salamanders at 
this point. The commenter appreciates that the current situation makes 
executing such a program difficult, if not impossible; however, the 
commenter hopes that the Service will continue exploring options for 
such a program in the future for other emerging infectious diseases 
that are likely to impact U.S. wildlife species.
    Response: The interstate prohibition has been clarified as 
explained in the final rule. Please also see heading in the second 
interim rule on Ability To Prevent or Control the Spread of Pathogens 
or Parasites. The Service will consider other options as opportunities 
arise.
    (98) Comment: The Service cites inadequate agency resources to 
conduct inspections and expenses associated with testing as additional 
reasons supporting its finding that there are not less restrictive 
means to prevent Bsal than those selected for the 2016 interim rule. To 
the extent that those expenses and hardships fall upon the owners of 
salamanders, a commenter would like to work with the Federal Government 
in developing safe, practical procedures. To the extent that those 
burdens fall upon the agency, the Service must not discriminate between 
regulation of salamanders in the pet trade and other species for which 
it has dedicated resources to developing satisfactory testing 
protocols.
    Response: The Service welcomes and encourages engagement by a 
myriad of entities that can develop the science and help better manage 
wildlife pathogens entering, becoming established in, and spreading in 
the United States. No safe, effective alternatives have yet been 
presented to us. The fungus that affects the salamanders was discovered 
in 2013, much more recently than the pathogens infecting salmonids for 
which the Service has testing protocols. Much research needs to be done 
on the tremendous diversity of salamanders and their in situ 
environmental conditions to find an equitable, reliable, economical 
test as well as testing facilities in other countries.
Other Issues
    (99) Comment: The Wildlife Society recommends the development of 
new comprehensive legislation to address the complexities of emerging 
wildlife diseases that encourages investment, increases professional 
capacity, focuses on collaborative prevention, and uses a 
multidisciplinary approach to better understand the interaction and 
transmission mechanisms of wildlife pathogens.
    Response: The comment is outside the scope of this rulemaking.
    (100) Comment: Since no method of pathogen control is likely to 
reduce risk of invasion by 100 percent, it is equally important to 
invest in proactive monitoring for Bsal emergence within the United 
States. In August 2015, the commenter launched a citizen science 
project on iNaturalist for people to report sightings of dead or 
diseased salamanders. The commenter would be happy to work together 
with the Service more quickly to identify and respond to potential 
sites of Bsal emergence. More information about the project ``Saving 
Salamanders with Citizen Science'' can be found at: https://www.inaturalist.org/projects/saving-salamanders-with-citizen-science.
    Response: We shared this feedback with our National Wildlife Refuge 
System's Inventory and Monitoring Program. The Service is also helping 
the National Bsal Task Force and PARC to develop the protocols to 
monitor for Bsal's introduction and to allow for rapid response if it 
is identified in the United States.
    (101) Comment: The commenter requests increased communication and 
education efforts around the Bsal rule. There is still a significant 
amount of confusion around the reasoning behind the scope of the action 
taken in the rule, including, but not limited to, why certain species 
were chosen and why interstate commerce was included. Addressing these 
concerns through a coordinated education and communication initiative 
would likely help garner further support for the implementation of the 
rule. Many groups, such as caudata.org, the National Bsal Task Force, 
and Partners in Amphibian and Reptile Conservation (PARC) would likely 
be able to play a role in helping to disseminate this information.
    Response: The interstate prohibition has been clarified as 
explained in the final rule. The Service is a partner in PARC and a 
member of the Bsal Task Force and appreciates the need to better 
address the communication needs associated with the rule. We have also 
been providing additional information through our website to assist 
stakeholders in understanding the need for the rule and clarifying the 
permit process.
    (102) Comment: The rule is being exploited by animal rights 
organizations who do not represent the majority of views of U.S. 
citizens. This rule was formulated in part due to a petition by the 
``Save the Frogs'' organization.

[[Page 2193]]

    Response: The Service received the petition from the Center for 
Biological Diversity and Save the Frogs! in mid-May 2015. However, we 
began discussions on what action to take in October 2014 and had 
already begun the regulatory process several months before we received 
the petition. Letters to the Service Director from such agencies as 
AFWA urged the Service to take action to prevent the fungus from 
entering the United States, and we took action as soon as we were able 
to make a determination based on defensible scientific evidence and 
comply with applicable rulemaking requirements to promulgate injurious 
wildlife listings under the Lacey Act within our available resources.

C. Affirmation of the 2016 Interim Rule

    After careful consideration of the comments received and 
information presented, we are affirming our 2016 listing of the 20 
genera of salamanders that the 2016 interim rule added to the lists of 
injurious wildlife in 50 CFR part 16 (81 FR 1534, January 13, 2016). 
All species in the 20 genera continue to be listed as injurious 
wildlife. The defensible scientific evidence continues to indicate that 
the importation of these genera poses significant risks of introducing 
Bsal into the United States, and none of the inputs received in 
response to the 2016 interim rule have changed this determination. 
Therefore, with this document, we affirm the addition of the following 
genera to 50 CFR 16.14: Chioglossa, Cynops, Euproctus, Hydromantes, 
Hynobius, Ichthyosaura, Lissotriton, Neurergus, Notophthalmus, 
Onychodactylus, Paramesotriton, Plethodon, Pleurodeles, Salamandra, 
Salamandrella, Salamandrina, Siren, Taricha, Triturus, and 
Tylototriton. Because we consider rulemaking on the 2016 interim rule 
to end with the publication of this document affirming the 2016 interim 
rule, we are not soliciting comments regarding the genera listed in 
this final rule.

D. Required Determinations

    We hereby affirm our responses to the following determinations 
required of the Federal rulemaking process as published in the January 
13, 2016, interim rule (81 FR 1534):
     Executive Orders 12630, 12866, 12988, 13132, 13175, 13211, 
and 13563;
     Regulatory Flexibility Act and Congressional Review Act (5 
U.S.C. 601 et seq. and 804(2)) (except a decrease in the economic 
effect on U.S. industries has occurred due to the clarification of the 
interstate transport prohibition);
     Unfunded Mandates Reform Act (2 U.S.C. 1501 et seq.);
     Paperwork Reduction Act of 1995 (44 U.S.C. 3501 et seq.);
     National Environmental Policy Act (42 U.S.C. 4321 et 
seq.); and
     Government-to-Government Relations with Native American 
Tribal Governments (59 FR 22951 and 512 DM 2).

IV. Second Interim Rule

Summary of Changes to the 2016 Interim Rule

    For the injurious wildlife evaluation in this second interim rule, 
in addition to information used for the 2016 interim rule, we 
considered: (1) comments and new information from the public comment 
period for the 2016 interim rule, (2) comments on the 2016 interim rule 
from three peer reviewers, and (3) new information acquired by the 
Service after the 2016 interim rule published. This new information was 
used to update the science about Bsal and determine if any additional 
genera of salamanders should be added to the list according to the 
criteria laid out in the 2016 interim rule.
    This second interim rule incorporates into 50 CFR 16.14 the 
clarifications and changes to the 2016 interim rule based on comments 
we received that are discussed above in the final rule under B. Summary 
of Comments Received on the 2016 Interim Rule. This is because only one 
revision of 50 CFR 16.14 will be made from both rules and will include 
the clarifications from the final rule and the new genera and 
clarifications from this second interim rule.
    We are clarifying, in response to public and peer-review comments, 
what is and is not injurious on a cellular or molecular level based 
upon chemical preservation or other methods that will kill the fungus. 
Unpreserved swabs are injurious; however, preserving swabs, such as by 
using 70 percent (or higher) ethanol for at least 1 minute (Van Rooij 
et al. 2017), renders the fungus unviable and, therefore, preserved 
swabs are not injurious and are excluded from the prohibitions. In 
addition, purified extracted genetic material of salamanders 
(salamander DNA or RNA) is unable to cause pathogen transmission; 
therefore, it is not injurious. Swabs collected for molecular biology 
applications should be preserved by using a higher ethanol 
concentration (95-99 percent), which is adequate for both the molecular 
preservation of DNA for testing and denaturing the proteins on the 
surface of fungi, rendering them unviable and thus not injurious 
(Marquina et al. 2021).
    We provide evidence here that specimens that are chemically 
preserved to deactivate any live Bsal and purified extracted genetic 
material are not considered injurious. The Service has concluded that 
there is a low risk of transmission of Bsal to native species from eggs 
and gametes, preserved specimens, and purified extracted genetic 
material, which is consistent with the intent of what is not injurious 
in the 2016 interim rule. However, all other parts, such as unpreserved 
salamander tissues, fluids, and cells carried on swabs and on or in 
other media, will continue to be regulated under the listing. Specimens 
that are frozen are also included in the listing.
    The Service reviewed research that has published since the 2016 
interim rule took effect and is adding 16 genera of salamanders to the 
20 already listed in 50 CFR 16.14. This action adds approximately 164 
species in this second interim rule to the previously listed 201 
species. The genera are added under the same criteria that were used 
for the original 20 genera in the 2016 interim rule. However, the 
scientific community has made changes to salamander taxonomy within the 
20 genera in the 2016 interim rule. Thus, the number of species that we 
identified in those genera increased from 201 to 262 species as of May 
1, 2023. The combined total is 36 genera with approximately 426 
species. We note that taxonomic changes within each genus may occur at 
any time for such reasons as new species discovered, subspecies 
elevated to full species, species split into two species, and other 
modifications resulting from genomic testing. All species subsequently 
scientifically added to the genera that we are listing are also 
heretofore considered listed species. For this reason, we are not 
enumerating all of the known salamander species in each of the 36 
listed genera in 50 CFR 16.14.
    The statute (18 U.S.C. 42(a)(1)) refers to ``the offspring or eggs 
of any of the foregoing'' as being injurious. Therefore, we are 
clarifying that hybrids of species in any listed genus, including 
offspring from a listed and a nonlisted parent, are injurious.
    In response to the D.C. Circuit Court of Appeals Decision in United 
States Association of Reptile Keepers, Inc. v. Zinke, 852 F.3d 1131 
(D.C. Cir. 2017), the prohibition on interstate transport in the 2016 
interim rule has been modified. The D.C. Circuit Court of Appeals held 
that 18 U.S.C. 42(a) does not prohibit transport of injurious wildlife 
between States within the

[[Page 2194]]

continental United States. Therefore, this interim rule clarifies that 
50 CFR 16.3 does not prohibit interstate transport between States 
within the continental United States. This means that transportation of 
injurious wildlife between the 49 States within the continental United 
States (the contiguous 48 States and Alaska, provided no international 
borders are crossed) is not prohibited by the statute or injurious 
wildlife regulations, unless that movement of the wildlife is 
restricted due to conditions associated with issued injurious wildlife 
permits. This change took effect as of April 7, 2017. However, import 
of injurious wildlife into the United States remains prohibited. In 
addition, transport of injurious wildlife between the listed 
jurisdictions in the shipment clause (the continental United States, 
the District of Columbia, Hawaii, the Commonwealth of Puerto Rico, and 
any territory or possession of the United States) remains prohibited. 
As before, injurious species may not transit into or out of the 
District of Columbia. Also, injurious wildlife permits under 50 CFR 
16.22 continue to be required to import injurious wildlife and to 
transport injurious wildlife between the listed jurisdictions for 
zoological, educational, medical, and scientific purposes; movements 
within the continental United States may be subject to conditions from 
an injurious wildlife permit.
    Additionally, injurious wildlife unlawfully imported into the 
United States or transported between the enumerated jurisdictions is 
still unlawful to transport, including within the continental United 
States. Under the Lacey Act Amendments of 1981, 16 U.S.C. 3372(a)(1), 
it is unlawful for any person to import, export, transport, sell, 
receive, acquire, or purchase any wildlife transported in violation of 
any law of the United States. This includes transport of any injurious 
wildlife imported into the United States or transported between the 
enumerated jurisdictions in violation of 18 U.S.C. 42(a).

Need for an Interim Rule

    Rulemaking under 18 U.S.C. 42 is governed by the Administrative 
Procedure Act (APA) (5 U.S.C. 551 et seq.). The process of issuing a 
proposed rule, providing the opportunity for public comment, and 
completing a final rule can take a significant amount of time to 
complete. During that time, the species proposed for listing are still 
allowed to be imported and transported, offering increased 
opportunities for introduction, establishment, and harm. Under section 
553(b)(3)(B) of the APA, however, a proposed rule is not required when 
the agency for good cause finds (and incorporates the finding and a 
brief statement of reasons therefor in the rules issued) that notice 
and public procedure thereon are impracticable, unnecessary, or 
contrary to the public interest. There is good cause to forgo notice 
and public comment on a proposed rule in this case and instead take 
immediate action in the form of an interim rule to help prevent the 
Bsal fungus from being introduced, established, or spread in the United 
States. Providing notice and public comment prior to implementing the 
injurious wildlife prohibitions would be contrary to the public 
interest because of the need to take immediate action due to the 
significant risk from Bsal. Not only could the fungus cause the 
devastation of some populations of native salamanders critical to 
ecosystem health, but it could also cause mortality if it spreads in 
the salamander pet trade. For these reasons, we find good cause in 
accordance with 5 U.S.C. 553(d)(3) to make the second interim rule 
effective 15 days after the date of publication in the Federal 
Register.
    This second interim rule is the result of peer-reviewed, scientific 
information published since the publication of the 2016 interim rule. 
At the time the 2016 interim rule published, there was very little 
information on the newly described chytrid fungus species affecting 
salamanders (discovered in 2013). We used defensible scientific 
evidence to quickly stop the importation of the host species 
(salamanders) of the fungus. However, after the 2016 interim rule 
published, many research institutions realized the need for more 
research, both on the novel fungus and on the effect on and variety of 
host amphibians, to assess the validity of previous studies and 
determine other potential carriers. That body of research, done 
primarily in the United States, Europe, and Asia, has taken years to 
develop and put through the peer-review and journal-publication 
processes.
    We have now compiled a more comprehensive picture of the fungus, 
including 16 more genera that we determined are injurious (using the 
same criteria as in the 2016 interim rule). We still have the 
opportunity to prevent the contagious lethal fungus from being 
introduced into the United States on salamanders in trade, hence the 
need for the second interim rule with the new high-risk species. Some 
of the new species are in the pet trade, and a proposed rule would give 
the public the counterproductive opportunity to rush to import the 
proposed species prior to the regulation. We note that a shipment of 24 
live fire salamanders (Salamandra salamandra) was imported into Los 
Angeles on January 26, 2016, which was 2 days before the listing took 
effect (USFWS OLE 2021), although we do not know that the shipment was 
intentionally shipped to preemptively avoid the 2016 interim rule's 
effective date. Fire salamanders are the species that brought this 
lethal fungus to the attention of scientists, and the shipment was 
exported from Germany, where the fungus had been detected in 2015 
(Schultz et al. 2020), making the potential for Bsal introduction from 
this shipment a genuine threat. Fortunately, there is no evidence that 
those imported salamanders carried Bsal.

Purpose of Listing as Injurious

    The purpose of listing the live specimens, dead specimens, hybrids, 
and parts (but not eggs, gametes, preserved specimens or parts 
(including tissue), and purified extracted genetic material) of 16 
genera of salamanders as injurious wildlife is to prevent the 
accidental or intentional introduction of salamanders that are expected 
to serve as carriers of Batrachochytrium salamandrivorans (hereafter, 
Bsal), a fungus that poses a risk to native species of salamanders, 
into the United States. The genera are all from the order Caudata and 
are commonly referred to as salamanders and newts (hereafter, 
salamanders). If Bsal is introduced into wild populations of native 
salamanders, we expect it to cause significant harm to wildlife and the 
wildlife resources of the United States.
    Under 18 U.S.C. 42(a), the Service, through the Secretary of the 
Interior, may prescribe by regulation any wild mammals, wild birds, 
fishes, mollusks, crustaceans, amphibians, reptiles, or the offspring 
or eggs of any of the foregoing found to be injurious to human beings, 
to the interests of agriculture, horticulture, forestry, or to wildlife 
or the wildlife resources of the United States. Salamanders are 
amphibians, and the Service has the authority to list amphibians when 
we find that they are injurious to one or more of the statutory 
interests. We may list species before they are introduced into the 
United States and have the opportunity to harm interests of the United 
States as enumerated under 18 U.S.C. 42.
    We have determined that salamanders that potentially carry Bsal are 
injurious to wildlife and wildlife resources of the United States. With 
this second interim rule, we are attempting to prevent the introduction 
and subsequent establishment and spread of the salamander chytrid 
fungus, Bsal, which

[[Page 2195]]

is a pathogen capable of causing significant harm to native salamander 
species and their ecosystems. As described below under Role of 
Salamanders in the Ecosystem, the benefits that these native salamander 
species provide to ecosystems in ensuring ecosystem health and 
stability, and, in turn, the ecosystem services that benefit people, 
are significant.
    As of the publication of the 2016 interim rule, Martel et al. 
(2014) and Cunningham et al. (2015) identified some of the salamander 
species that can carry Bsal and are at risk from infection. The 
researchers tested a limited number of the approximately 689 (currently 
804) known species of salamanders that exist worldwide and found that 
not every species was negatively affected by the fungus, as determined 
by standard detection methods. However, the results clearly indicated a 
severe threat for many species of salamanders that will be negatively 
affected by this pathogen and others that could carry the fungus to the 
vulnerable species. Research showed that some tested species that are 
native to the United States were found to be lethally vulnerable to the 
fungus. Such an emerging infectious disease of fungal origin can cause 
a significant loss in biodiversity and ecosystem services (Fisher et 
al. 2012). Bsal research results and concerns about emerging infectious 
disease, as described by Spitzen-van der Sluijs et al. (2013), Martel 
et al. (2013), and Martel et al. (2014), generated a strong response 
from academia, industry groups, and conservation and other 
organizations who wrote to the Service seeking quick and decisive 
action to ensure that Bsal does not have a similar impact on salamander 
populations that Batrachochytrium dendrobatidis (Bd) has had on frogs 
(see the 2016 interim rule). In early November 2014, the Service 
initiated a review to determine whether salamanders capable of carrying 
Bsal should be listed as injurious.
    Martel et al. (2014, and others later) used several methods to 
determine vulnerability to Bsal-caused disease of some salamander 
species but do not have a category for the status as a carrier. While 
the vulnerability of native species is of great concern to the Service, 
the 2016 interim rule was primarily concerned with the ability of 
viable Bsal spores to remain on salamander species or their parts, thus 
introducing and spreading the fungus to the United States, causing 
chytridiomycosis disease outbreaks in native salamander populations. We 
reviewed the literature and based our criteria for determining carrier 
status of genera on whether a species was found, as determined by 
microscopic analysis of preserved tissue specimens (histology), qPCR 
(quantitative polymerase chain reaction), or other confirmatory 
approach to harbor viable spores.
    We also looked at challenge studies, where a salamander that is 
free of Bsal as determined by initial pathogen-specific qPCR, is then 
inoculated with Bsal spores. A follow-up swab for qPCR is done at a 
specified period of days later to see if the spores caused disease 
according to field observations or histology or did not cause disease 
but was able to invade the skin of that species long enough to move or 
transmit the fungus to other salamanders, as confirmed by histology. We 
also looked at surveillance studies of swabs of wild and captive 
salamanders, where presence or absence of Bsal was determined by qPCR; 
negative results were not evidence for being classified as noncarrier 
whereas positive results were classified as carriers.
    Regardless of the vulnerability of a species or the ability to 
manifest disease, if the species is a carrier, we consider that genus 
to be listable as injurious. However, if there is conclusive 
countervailing evidence that at least one species in that genus is not 
a carrier, as shown by histology, then we do not list the genus. Case 
definition and diagnostic criteria are described in White et al. 
(2016).
    The 2016 interim rule effectively reduced import volume of targeted 
species, but new research on species susceptibility suggests the list 
of regulated species was incomplete regarding Bsal reservoir species 
(Grear et al. 2021). Since the publication of the 2016 interim rule, 
additional research has provided additional evidence of the diversity 
of species and genera affected by Bsal or determined to be carriers 
(for example, Yuan et al. 2018, Carter et al. 2020, Barnhart et al. 
2020, Gray et al. 2023). Based on the Service's genus-level carrier 
extrapolation from data obtained from the aforementioned publications, 
and because Bsal has not been found in natural environments in the 
United States (Waddle et al. 2020), the opportunity still exists to 
prevent the introduction of Bsal by adding new genera of salamanders to 
the injurious list. In 2017, following the 2016 interim rule and 
Canada's temporary import ban of all living or dead salamanders, eggs, 
sperm, tissue cultures, and embryos (made permanent in 2018; 
Environment and Climate Change (ECCC) 2018), we received a letter from 
the American Society of Ichthyologists and Herpetologists (ASIH 2017) 
requesting the Service prohibit all salamander imports into the United 
States. For reasons explained herein, we are not listing all 
salamanders, but we are adding more genera, which we suggested in the 
2016 interim rule was a possibility. We specifically solicited comment 
on whether there is there any evidence suggesting that additional 
species are carriers of Bsal and should be listed by this rule, and if 
so, what species.
    We reviewed Bsal risk in conjunction with those salamander species 
known or suspected to carry the fungus utilizing injurious wildlife 
evaluation criteria, described in more detail as part of this interim 
rule in G. Factors That Contribute to Injuriousness of Salamanders. 
These criteria were previously developed by the Service to evaluate 
whether a species qualifies as injurious under 18 U.S.C. 42. The 
resulting analyses form the basis for the Service's regulatory 
decisions regarding injurious wildlife-species listings. This rule 
finds that Bsal is a significant threat to the wildlife and wildlife 
resources of the United States and lists 16 genera of salamanders that 
we have determined to be injurious because they are likely carriers of 
Bsal.
    Multiple factors confirm that Bsal can be introduced, become 
established, and spread, thereby causing substantial damage and harm in 
the United States (Spitzen-van der Sluijs et al. 2013; Martel et al. 
2014; Cunningham et al. 2015; Chytridcrisis 2015b). Specifically, these 
factors include: (1) the discovery of the newly emerging fungus Bsal in 
the Netherlands and the associated deleterious effects to native 
salamanders (ibid.); (2) its subsequent spread in the wild to Germany 
and Belgium (Spitzen-van der Sluijs et al. 2016) and Spain (Lastra 
Gonz[aacute]laz et al. 2019; Martel et al. 2020); (3) the appearance in 
captive collections in the United Kingdom, Germany, and Spain (Spitzen-
van der Sluijs et al. 2016; Thumsova et al. 2021); and (4) laboratory 
research (numerous papers cited in this rule). The United States leads 
all other countries in the number of native salamander species; 9 of 
the 10 families of salamanders worldwide are found in the United States 
(AmphibiaWeb 2023a). Based on scientific evidence as of publication of 
the 2016 interim rule, we knew that the fungus is lethal to at least 
two salamander species native to the United States (eastern newt 
Notophthalmus viridescens in the Eastern States and rough-skinned newt 
Taricha granulosa along the Pacific coast).
    Of the 221 native U.S. species known as of the preparation of this 
second interim rule (AmphibiaWeb 2023a), and including both rules in 
this document,

[[Page 2196]]

we have determined that 13 genera with 164 species may be carriers, and 
9 species are lethally vulnerable. Most of the remaining 10 genera 
(with 57 species) have not been scientifically tested, with a few that 
have had testing that was not conclusive; these may also be found to be 
carriers eventually. While the Service's greatest concerns are for 
species that are likely to die from Bsal, salamander species known to 
be tolerant of, or susceptible to, Bsal infection under experimental 
conditions may also develop clinical disease or experience increased 
severity of disease in the wild. These species may be Bsal carriers and 
are concerning because their long lifespans increase their likelihood 
of spreading the fungal spores and serving as Bsal reservoirs (Gray et 
al. 2023). A disease reservoir may be defined as ``a passive host or 
carrier that harbors pathogenic organisms without injury to itself and 
serves as a source from which other individuals can be infected'' (in 
Laking et al. 2017). Nonlethal infection in salamanders may have other 
negative effects, such as slowing their growth (Barnhart et al. 2020). 
Bsal infections have been found to increase in severity as animals are 
exposed to additional stressors in the wild, including other amphibian 
diseases (Wobeser 2007; Kerby et al. 2011; Kiesecker 2011; Longo et al. 
2019; McDonald et al. 2020).
    Experience with the introduction of Bsal into the Netherlands and 
associated deleterious effects to native salamanders, along with 
laboratory research, confirm that Bsal can be introduced, become 
established, spread, and cause substantial and immediate harm in the 
United States (Spitzen-van der Sluijs et al. 2013; Martel et al. 2014; 
Cunningham et al. 2015; Chytridcrisis 2015b). The United States leads 
all other countries in salamander diversity (PARC 2014). Based on 
scientific evidence, we know that the fungus is lethal to at least nine 
salamander species native to the United States. While the Service's 
greatest concern will be for species that are lethally vulnerable to 
Bsal, salamander species known to be tolerant of or susceptible to Bsal 
infection under experimental conditions may also develop clinical 
disease or increased severity of disease, respectively, when infection 
is combined with additional stressors in the wild, as has been found 
for other diseases, including those in amphibians (Wobeser 2007; Kerby 
et al. 2011; Kiesecker 2011).
    In the United States, Bsal has either not been introduced, has been 
introduced but has failed to become established, or is present but has 
not been positively detected. Although we do not have any conclusive 
evidence showing that introductions have occurred, history from other 
pathogens similar to Bsal, such as Bd, suggests that the fungus is 
likely to spread quickly throughout the United States if it is not 
prevented from being introduced. Moreover, efforts to control or 
eradicate introduced or established invasive species and manage the 
costs they incur to society are generally less effective and more 
expensive and difficult than efforts that prevent establishment (Leung 
et al. 2002; Finnoff et al. 2007). Prevention of invasive species is 
typically the most cost-effective measure to avoid the damage that such 
species cause (Leung et al. 2002; Lodge et al. 2006; Keller and 
Springborn 2014). As noted in the 2016-2018 National Invasive Species 
Management Plan, preventing the introduction of potentially harmful 
organisms is not only the first line of defense for minimizing the 
spread and impact of invasive species, it is also the most cost-
effective strategy; science-based risk analyses are used to inform 
regulations that can prohibit the entry of certain nonnative organisms 
at jurisdictional borders (National Invasive Species Council 2016). 
Invasive species prevention is a priority of the Department of the 
Interior (2021).
    If Bsal has unknowingly been introduced but failed to establish in 
the United States for unknown reasons, it is still important to act now 
because additional introductions increase the likelihood of 
establishment and harm. As more salamanders that can carry Bsal are 
imported into the United States, the probability increases that one or 
more of those salamanders, through a phenomenon called propagule 
pressure or ``introduction effort,'' described in Lockwood et al. 
(2005) as a measure of the number of nonnative individuals released 
into a region, will give Bsal the opportunity to establish in the 
United States and spread. The 2016 interim rule significantly reduced 
the number of salamanders being imported by about 95 percent (average 
per year for the period 2016-2020) from the 6 years before publication 
of the 2016 interim rule.
    The salamander species listed by this second interim rule follow 
the same criteria as for the 20 genera in the final rule to the 2016 
interim rule and are those found within genera for which we have 
evidence that at least one species in that genus is a carrier of Bsal 
with no countervailing conclusive evidence that other species in that 
genus are not carriers. We describe our rationale for this course of 
action below under Vulnerability and Carrier Status. Our decision 
making for the final rule to the 2016 interim rule and the second 
interim rule included the following considerations: All 20 genera of 
salamanders in the final rule to the 2016 interim rule, plus any new 
species identified within the genera listed by this second interim 
rule, are found to be injurious because suitable climate exists in 
parts of the United States to support Bsal; even if a salamander listed 
by this second interim rule could not establish a population in the 
wild, an infected captive salamander (or the water and soil in which it 
came into contact) released into the environment can transmit Bsal to 
native populations; Bsal is capable of causing extensive damage to 
wildlife and wildlife resources, including federally endangered and 
threatened species; eradicating Bsal would be extremely difficult once 
introduced and established; and controlling Bsal in wild salamanders is 
not practical.
    Listing the salamanders as injurious will help keep Bsal out of the 
United States by preventing the importation of salamanders capable of 
carrying the fungus and serving as the vector of introduction into U.S. 
ecosystems, thereby causing injurious effects consistent with 18 U.S.C. 
42. Bsal is not known to be present in U.S. ecosystems (Waddle et al. 
2020). Given the expected consequences that the introduction of Bsal 
would have to wildlife and wildlife resources of the United States, we 
are listing species that we have determined to be injurious. This 
second interim rule lists some species that are currently in U.S. trade 
as well as some that are not. We have the authority to list species as 
injurious even if they are not currently in trade or known to exist in 
the United States. This regulation is not a ban on possessing or 
selling any of the species. The import and transport between the 
enumerated jurisdictions in the shipment clause in 18 U.S.C. 42 (the 
continental United States, the District of Columbia, Hawaii, the 
Commonwealth of Puerto Rico, and any territory or possession of the 
United States), codified in Federal regulations at 50 CFR 16.3, of any 
of the listed species is prohibited. The provisions of 18 U.S.C. 42(a) 
do not prohibit any person who owns one of the listed species at the 
time of listing from continuing to possess the salamander or engaging 
in transport and other activities within the enumerated jurisdictions, 
unless such movement of the wildlife is restricted due to conditions 
associated with issued injurious wildlife permits. Those activities may 
be regulated by other Federal, State, Tribal, or territorial law.

[[Page 2197]]

It is the responsibility of a person who may be engaged in transport or 
use of injurious wildlife to be aware of any Federal, State, Tribal, or 
territorial law or regulation that applies to that activity.
    The salamander species listed by this second interim rule are 
those, in addition to the species listed in the final rule to the 2016 
interim rule, that are found within genera for which we have evidence 
that at least one species in that genus is a carrier of Bsal with no 
conclusive countervailing evidence that other species in that genus are 
not carriers. We describe our rationale for this course of action below 
under Vulnerability and Carrier Status. Our decision making also 
included the following considerations:
     All 16 genera of salamanders, plus any new species 
identified within the genera listed by this second interim rule, are 
found to be injurious because suitable climate exists in parts of the 
United States to support Bsal;
     Even if a salamander listed by this second interim rule 
could not establish a population in the wild, a carrier salamander that 
was released from captivity (or the water and soil in which it came 
into contact) can transmit Bsal spores to native populations;
     Bsal is capable of causing extensive injury to wildlife, 
including federally endangered and threatened salamander species;
     No method is known to eradicate Bsal in the environment 
once it is introduced and established; and
     Controlling Bsal is not practical in free-ranging 
salamanders carrying the fungus.
    We clarify what is considered a salamander part that is not 
injurious and that would not need an injurious wildlife permit 
(partially adapted from WOAH 2021a):
     Heat-sterilized hermetically sealed amphibian products, 
that is, a heat treatment at 121 [deg]C for at least 3.6 minutes (or 
any time or temperature equivalent that has been demonstrated to 
inactivate Bsal) (WOAH 2021a);
     cooked amphibian products that have been subjected to heat 
treatment at 100 [deg]C for at least 1 minute (or any time or 
temperature equivalent that has been demonstrated to inactivate Bsal) 
(WOAH 2021a);
     pasteurized amphibian products that have been subjected to 
heat treatment at 90 [deg]C for at least 10 minutes (or any time or 
temperature equivalent that has been demonstrated to inactivate Bsal) 
(WOAH 2021a);
     mechanically dried amphibian products and skin leather 
(that is, a heat treatment at 100 [deg]C for at least 30 minutes or any 
time or temperature equivalent that has been demonstrated to inactivate 
Bsal) (WOAH 2021a); and
     chemical treatment of amphibian skin leather that 
inactivates Bsal (Van Rooij et al. 2017).
    The above conditions apply to all salamanders listed as injurious 
in 50 CFR 16.14 due to the risk of carrying Bsal. Also not considered 
injurious, and therefore exempt, are eggs, gametes, chemically 
preserved specimens or parts (including tissues), and molecular 
specimens consisting of only the nucleic acids (DNA or RNA) from 
organisms. The appropriate concentration and minimum exposure time for 
a given chemical preservative or fixative to render any Bsal organisms 
non-viable varies with the precise chemical formulation and should be 
utilized as described in association with such actions in the peer-
reviewed literature. For example, Bsal is killed when exposed to 70 
percent ethanol for at least 60 seconds (Van Rooij et al. 2017). 
However, parts that are otherwise preserved by air-drying or at a 
temperature and time that does not meet the above criteria or at a cold 
temperature (such as freezing) are considered injurious because Bsal is 
not inactivated by those methods. Purchase, sale, and other activities 
with the listed salamanders strictly within the boundaries of the 
enumerated jurisdictions within the shipment clause are not regulated 
under 18 U.S.C. 42.
    This second interim rule takes effect on the date specified above 
in DATES, but we are providing the public with a period of time to 
comment on the listing and associated documents. The resulting final 
rule will contain responses to comments received on the second interim 
rule, state the final decision, and provide the justification for that 
decision.

Listing Species That Carry Pathogens

    Pathogens are such agents as viruses, bacteria, and fungi that 
cause disease in animals and plants. The Service does not have the 
direct authority under 18 U.S.C. 42(a)(1) to list pathogens as 
injurious. We also cannot list or regulate fomites (materials, such as 
water, that can act as passive carriers and transfer pathogens). 
However, we can list wild mammals, wild birds, fishes, mollusks, 
crustaceans, amphibians, or reptiles that are hosts to or carriers of 
pathogens and that can be injurious if the likelihood, scope, and 
severity of effects significantly affect one or more of the interests 
listed in the statute. Even if the host species cannot establish 
populations in the wild, the host can present significant risk if the 
pathogen the host is carrying can infect wildlife or wildlife resources 
or affect human beings or the interests of agriculture, horticulture, 
or forestry in the United States. Among other impacts, diseases caused 
by introduced pathogens reduce biodiversity (the variety of different 
types of life in a region) and have been implicated in the local 
extinction of many animal taxa (Daszak et al. 2000).

Listing and Evaluation Process

    The regulations contained in part 16 of title 50 of the Code of 
Federal Regulations (CFR) implement 18 U.S.C. 42(a)(1) and include the 
names of species determined by the Service or by Congress to be 
injurious. Under the terms of the statute, the Secretary of the 
Interior may prescribe by regulation those wild mammals, wild birds, 
fishes, mollusks, crustaceans, amphibians, reptiles, and the offspring 
or eggs of any of the foregoing that are injurious to humans, to the 
interests of agriculture, horticulture, or forestry, or to the wildlife 
or wildlife resources of the United States. The lists of injurious 
wildlife species are found at 50 CFR 16.11-16.15, with Sec.  16.14 
being for amphibians. Under these regulations, species are added to the 
lists of injurious wildlife to protect statutorily enumerated interests 
from potential and known negative effects. Most species listed have the 
capacity to establish populations in the wild, spread, and cause harm. 
However, a species can be listed based solely on its capacity to cause 
harm. For example, uneviscerated dead salmonids without a health 
certificate are not capable of establishing in the United States, but 
they are injurious because the pathogens they may carry are harmful.
    Under 18 U.S.C. 42, the Service can list species that are nonnative 
and those that are indigenous to the United States. In the case of an 
indigenous species, for example, the Service may find that it is 
injurious because its transport and release outside the species' range 
may cause harm to human beings, agricultural or forestry interests, or 
natural systems. Furthermore, a species does not have to be currently 
imported or present in the wild in the United States for the Service to 
list it as injurious. For species not yet imported into the United 
States, the objective of listing is to prevent that species' 
importation and likely introduction and possible establishment and 
spread in the wild, thereby preventing injurious effects consistent 
with the purposes of 18 U.S.C. 42.
    In response to the D.C. Circuit Court of Appeals Decision in United 
States Association of Reptile Keepers, Inc. v.

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Zinke, 852 F.3d 1131 (D.C. Cir. 2017), the prohibition on interstate 
transport in the 2016 interim rule has been modified. Because of the 
court's decision, injurious wildlife listings, including those listed 
by Congress through statutes (fruit bats (genus Pteropus), mongoose, 
zebra mussel, brown tree snake, bighead carp, quagga mussel), no longer 
result in a statutory prohibition on interstate transport of injurious 
wildlife between States within the continental United States. This 
means that transportation of injurious wildlife between the 49 States 
within the continental United States (the contiguous 48 States and 
Alaska) is not prohibited by 18 U.S.C. 42(a) (codified in Federal 
regulations at 50 CFR 16.3), unless that movement of the wildlife is 
restricted due to conditions associated with issued injurious wildlife 
permits. Thus, an injurious wildlife permit is generally not required 
to transport injurious species across State lines of any of the 49 
continental States. However, a permit is still required for the 
movement of an injurious animal that was previously permitted for 
import or for the progeny of an individual that was permitted for 
import.
    Import of injurious wildlife into the United States remains 
prohibited. In addition, transport of injurious wildlife between the 
enumerated jurisdictions in the shipment clause of 18 U.S.C. 42 (the 
continental United States, the District of Columbia, Hawaii, the 
Commonwealth of Puerto Rico, and any territory or possession of the 
United States), codified in Federal regulations at 50 CFR 16.3, remains 
prohibited. These prohibited activities may be undertaken by permit for 
zoological, educational, medical, or scientific purposes (in accordance 
with permit regulations at 50 CFR 16.22), or by Federal agencies 
without a permit solely for their own use, upon filing a written 
declaration with the District Director of Customs and the U.S. Fish and 
Wildlife Service inspector at the port of entry. Interstate transport 
between States within the continental United States is not prohibited 
under the current prohibitions of 18 U.S.C. 42(a), and 18 U.S.C. 42(a) 
does not prohibit intrastate transport (transport within a State or 
territory) or possession of injurious species. However, injurious 
wildlife unlawfully imported into the United States or transported 
between the enumerated jurisdictions is unlawful to transport within 
the continental United States, or to transport within a State or 
Territory, under the Lacey Act Amendments of 1981, 16 U.S.C. 
3372(a)(1). It is the responsibility of a person who may be engaged in 
transport or use of injurious wildlife to be aware of any Federal, 
State, Tribal, or Territorial law or regulation that applies to that 
activity.
    The Service prepares a listing rule by first assessing the relevant 
aspects of the biology of the species, such as its habitat, diet, 
reproductive capacity, climate, predatory capacity, and threats to its 
survival. This assessment is used to develop the next step, which is to 
evaluate whether any of these aspects contribute to the species being 
invasive or otherwise harmful.
    The Service uses one or more of the injurious wildlife listing 
criteria identified below to evaluate whether a species qualifies as 
injurious under 18 U.S.C. 42. The results of the analysis using these 
criteria serve as a general basis for the Service's regulatory 
decisions regarding injurious wildlife species listings. Biologists and 
risk managers within the Service who are knowledgeable about a species 
that is being evaluated assess both the factors that contribute to and 
the factors and measures that reduce or remove the likelihood of 
injuriousness.
    (1) Factors that contribute to injuriousness:
     The likelihood of release or escape;
     Potential to survive, become established, and spread;
     Impacts on wildlife resources or ecosystems through 
hybridization and competition for food and habitats, habitat 
degradation and destruction, predation, and pathogen transfer;
     Impacts to threatened and endangered species and their 
habitats;
     Impacts to human beings, forestry, horticulture, and 
agriculture; and
     Wildlife or habitat damages that may occur from control 
measures.
    (2) Measures that reduce the likelihood of the species being 
considered as injurious:
     Ability to prevent escape and establishment;
     Potential to eradicate or manage established populations 
(for example, making organisms sterile);
     Ability to rehabilitate disturbed ecosystems;
     Ability to prevent or control the spread of pathogens or 
parasites; and
     Any potential ecological benefits to introduction.
    For this second interim rule, we provide a general summary of the 
biology of salamanders and of the fungus, followed by the evaluation 
for both as injurious. For injuriousness of the salamanders, we focused 
on the third bullet above ``Impacts on wildlife resources or ecosystems 
through * * * pathogen transfer.'' The issue in this rule is not about 
a given salamander species or genus being invasive but rather the role 
of salamanders in introducing the Bsal fungus into the United States 
and the scope and severity of effects caused by salamanders that are 
carriers of Bsal on the wildlife or wildlife resources of the United 
States.
    The Service obtains an extensive amount of amphibian import data 
from our Office of Law Enforcement's (OLE) Law Enforcement Management 
Information System (LEMIS). LEMIS is an electronic database utilized by 
all Service law enforcement officers, including the Service's 
conservation officers, wildlife inspectors, refuge officers, and 
special agents. LEMIS serves as the portal in which all Service 
wildlife violations are documented and intelligence is gathered and 
shared between law enforcement offices across the country. LEMIS also 
serves as the conduit for all declared imports and exports of wildlife 
and wildlife products and the database of all such wildlife trade data 
in the United States, both legal and illegal. The database provided us 
with information for this rule on what species were imported; quantity; 
countries of origin; ports of import; whether imported as live, dead, 
eggs, parts, or other; purpose for importing; and other relevant 
variables for the years 2010 to 2020 (USFWS OLE 2021).
    We evaluated Bsal and the salamander species that carry this fungus 
using the injurious wildlife evaluation criteria, described in more 
detail as part of this second interim rule in G. Factors That 
Contribute to Injuriousness of Salamanders, which the Service developed 
to evaluate whether a species qualifies as injurious under the Act. The 
resulting analysis serves as a basis for the Service's regulatory 
decision regarding injurious wildlife species listings. This second 
interim rule finds that Bsal is a significant threat to the wildlife 
and wildlife resources of the United States and lists 16 genera of 
salamanders that we have determined to be injurious because they are 
likely carriers of Bsal and may introduce the fungus into the United 
States.

A. Species Information for Salamanders

Salamander Nomenclature and Taxonomy
    The Service does not have a uniform policy for taxonomically 
identifying amphibians. In this interim rule, we use taxonomic 
nomenclature as described by AmphibiaWeb (https://amphibiaweb.org) with 
some comparison to the Integrated Taxonomic

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Information System (ITIS) (https://www.itis.gov). The system used by 
AmphibiaWeb represents one of the most widely accepted salamander 
taxonomic systems in the scientific community because it relies on 
criteria including, but not limited to, monophyly (common descent from 
a single ancestor), stability, expertise of scientists, and general 
acceptance by the amphibian conservation community and is frequently 
updated. As a Federal resource for taxonomic information, the Service 
also uses ITIS as an agency resource. As of May 1, 2023, AmphibiaWeb 
(2023b) reported 804 species of all salamanders in 68 genera and 10 
families, and ITIS reported 738 species in 70 genera and 9 families.
    In this rule, when we refer to salamanders, we include animals from 
the order Caudata commonly referred to as salamanders and newts. The 
nomenclature and taxonomy of salamander species that we are regulating 
should be provided as accurately as possible to the public so that the 
public and law enforcement officers know what is being regulated. 
However, the science is evolving, making consistency even from the 2016 
interim rule difficult. The classification remained relatively 
unchanged from the 1960s until the 1990s, when advances in DNA 
sequencing enabled researchers to examine species relationships more 
closely (Petranka 1998). Furthermore, dozens of amphibian species from 
remote regions of the world are discovered every year (AmphibiaWeb 
2021). This is generally why the number of species listed increased 
within the 20 genera in the final rule to the 2016 interim rule. For 
these reasons, we are not including the names of the species within 
each listed genus in 50 CFR 16.14. As long as the species is within a 
listed genus, it is covered as an injurious species, as in the final 
rule.
Salamander Biology
    Salamanders belong to the class Amphibia, a group of cold-blooded 
vertebrate animals comprising frogs and toads (order Anura), 
salamanders and newts (order Caudata), and caecilians (order 
Gymnophiona). The word ``amphibian'' is derived from the fact that most 
of the species spend part of their lives in water and part on land. 
Frogs and toads have legs but no tails as adults, and caecilians have 
tails but no legs. Morphologically, salamanders are generally 
characterized by their relatively large, vertically flattened tails, 
two front and two hind legs that are approximately the same size 
(Petranka 1998), and skin with glands that can be either rough or 
smooth (Stebbins and Cohen 1997). Exceptions include Sirenidae, which 
have two small forelimbs and no hindlimbs, and Amphiumidae, which have 
four vestigial limbs. Adult salamanders range in length from around 4 
centimeters (1.5 inches) to over 1.5 meters (5 feet) (Stebbins and 
Cohen 1997). Another distinction between anurans (the frogs and toads) 
and the caudata (salamanders and newts) is that the anurans have 
internal gills as larvae and salamanders have external gills as larvae.
    Salamanders can live for many years, but documented lifespans vary. 
Larger salamanders tend to live longer than smaller ones, and, with 
proper care, salamanders in captivity frequently live longer than those 
in the wild (Duellman and Trueb 1986). Records for captive animals 
range from 5 years for most plethodontids (lungless salamanders) to 55 
years for the Japanese giant salamander (Andrias japonicus) (Duellman 
and Trueb 1986). The Olm or blind cave salamander (Proteus anguinus), 
which lives in caves in southern Europe, has been documented living for 
at least 48 years in the wild, with an estimated lifespan of more than 
100 years (Live Science 2015).
    Salamanders are carnivorous and eat a wide variety of prey, 
depending on habitat and the stage of their life cycle. Terrestrial 
adult salamanders eat earthworms, insect eggs, and other small 
invertebrates, while aquatic salamanders eat all of these in addition 
to small fish, aquatic insects, and other amphibians. Some salamander 
larvae can also be omnivorous and eat plants and animals.
    Many salamanders have unique structural features, including costal 
grooves (grooves on the sides of the body that increase skin surface 
area for water absorption and transport) and nasolabial grooves 
(vertical slits between the nostril and upper lip used for sensing 
chemical stimuli in the environment) that can be used to differentiate 
between salamander species (Petranka 1998). Important features for 
identifying salamanders include head shape and size, fin shape and 
color, gill morphology, color patterns, number of toes, size, body 
shape, tooth patterns, and number of costal grooves. Some species 
appear similar to each other, and similarity of appearance within some 
families, such as Salamandridae, can make it difficult to differentiate 
between species, requiring close inspection of small physical 
characteristics.
    Salamanders occupy a wide range of habitats, including streams, 
trees, land (including forests, grasslands, and rocky slopes), 
underground, and caves. Salamanders are cryptic (difficult to find) 
partly because they occupy moist, cool places, such as underneath logs 
and between rock crevices on land or under rocks and logs in the water.
    Salamander courtship between males and females is regulated by 
chemicals that are released from specialized glands in the skin. Most 
salamanders reproduce by laying eggs in water with two exceptions: most 
members of family Plethodontidae lay their eggs on land, and the 
European species known as the alpine salamander (Salamandra atra) gives 
birth to live young (Stebbins and Cohen 1997). Eggs are surrounded by a 
protective jelly or membrane that keeps them from drying out. Almost 
all species of salamanders breed during specific seasons, and the 
length of time between mating and egg-laying varies considerably 
between species (Petranka 1998). Species that lay aquatic eggs place 
them in either streams or ponds, and species that lay their eggs on 
land choose hidden places, such as underground burrows, decaying logs, 
and moist rock crevices (Petranka 1998), where the young typically 
undergo direct development, whereby metamorphosis occurs in the egg and 
fully formed salamanders emerge from the eggs.
    The majority of the species in Ambystomatidae (mole salamanders) 
spend most of the year underground in rodent burrows and emerge only on 
rainy nights to mate and feed. Ambystomatid salamanders are famous for 
the migration of large numbers of individuals to breeding ponds. One 
example of a species that spends most of its life on land but that 
moves to aquatic areas to breed is the California tiger salamander 
(Ambystoma californiense). During winter rains, this species migrates 
across land to aquatic pools, such as cattle tanks and ephemeral pools, 
to breed. At the breeding pools, individuals come in contact with each 
other, even though they may not come in contact with each other during 
most of the rest of their lives on land (Barry and Shaffer 1994). 
However, the related axolotl (A. mexicanum) is unlike other salamanders 
by being neotenic (they do not undergo metamorphosis). Furthermore, 
some ambystomatids retain their larval morphology as reproductive 
adults until certain environmental cues trigger metamorphosis into 
terrestrial adult morphology.
Habitat Conditions and Native Range of U.S. Salamanders
    With more native salamander species than any other country in the 
world, the

[[Page 2200]]

United States is a salamander diversity hotspot (PARC 2015). 
Salamanders are widespread in the United States (Caudata Culture 2015a; 
U.S. National Park Service 2015). Areas of particularly high salamander 
diversity include the Eastern United States, with large numbers of 
plethodontid salamanders in the southern Appalachian Mountains 
(Richgels et al. 2016).
    Salamanders in the United States occupy a wide range of habitats, 
including streams, trees, land (including forests, grasslands, and 
rocky slopes), underground, and caves. These locations are most 
conducive to the relatively cool, moist conditions under which both 
salamanders and Bsal thrive (Duellman and Trueb 1986; Piotrowski et al. 
2004; Blooi et al. 2015a). Central and North American salamanders as a 
group are active at average temperatures of 11 [deg]C (52 [deg]F) to 20 
[deg]C (68 [deg]F) (Duellman and Trueb 1986), fully encompassing the 
optimum temperature for Bsal growth as described below under Climate 
Tolerance. Salamanders require some amount of constant moisture for 
physiological function, such as osmoregulation (controlling body fluid, 
water, and salt balance) or for cutaneous respiration, as in the 
lungless family Plethodontidae, or for temperature regulation (Duellman 
and Trueb 1986).
    Twenty species of U.S. salamanders from seven genera (Ambystoma, 
Batrachoseps, Cryptobranchus, Eurycea, Necturus, Phaeognathus, 
Plethodon) are currently listed as endangered or threatened under the 
Endangered Species Act of 1973, as amended (16 U.S.C. 1531 et seq.) 
(ESA). The specific vulnerability and carrier status of these species 
to Bsal is described below in Vulnerability and Carrier Status of 
Threatened and Endangered Species.
    Of the 221 salamander species in 23 genera in 9 families native to 
the United States, we expect that at least 164 species in 13 genera and 
in 5 families are capable of being carriers of Bsal: Ambystomatidae, 
Cryptobranchidae, Salamandridae, Sirenidae, and Plethodontidae. In 
North America, species in the family Salamandridae occur on the west 
coast of the United States and Canada, from southern California to 
southeastern Alaska, as well as much of the eastern half of the United 
States and extreme southeastern Canada (Caudata Culture 2015a). Members 
of the family Sirenidae occur throughout the southeastern Atlantic and 
Gulf of Mexico coastal plains and the Mississippi River Valley (Leja 
2005) (lesser siren, Siren intermedia) and in the Atlantic coastal 
plains from south Florida to Virginia (greater siren, Siren lacertina) 
(Hendricks 2005). The distribution of salamanders of the family 
Plethodontidae in the western hemisphere is from southern Canada to 
Bolivia and Brazil, except for members of the genus Hydromantes, which 
occur in California (AmphibiaWeb 2023a, Caudata Culture 2015a). 
Ambystomatidae has only one genus, and the 32 species are widely 
distributed in North America from southern Canada south to Mexico City. 
Cryptobranchidae is represented by one species in North America 
(eastern hellbender Cryptobranchus alleganienesis).
Role of Salamanders in the Ecosystem
    Salamanders play important roles in ecosystem function and as 
indicators of ecosystem health and stability (Davic and Welsh 2004). 
For example, salamanders of family Plethodontidae have life-history 
characteristics that make them highly effective at controlling 
invertebrates that would otherwise consume the leaf litter, thus 
releasing carbon to the environment (Best and Welsh 2014).
    In forests, salamanders are also among the most abundant 
vertebrates. Despite the relatively small size of most salamanders 
compared to most other native vertebrates, this sheer abundance 
contributes to a significant amount of biomass in the ecosystem, and, 
therefore, salamanders make significant contributions to nutrient 
cycling and transport (Burton and Likens 1975). For example, 
Ambystomatid salamanders can make significant contributions to energy 
and nutrient transport in forest ecosystems (Regester et al. 2006) and 
in pond ecosystems (Holomuzki et al. 1994). Many terrestrial 
salamanders consume arthropods (insects and related invertebrates) that 
feed on leaf litter, and the invertebrates' feeding process causes the 
release of carbon dioxide from the ground into the atmosphere. With 
fewer salamanders and more litter-consumers, more carbon is released 
from the soil, contributing to an excess of carbon dioxide in the 
atmosphere. Salamander populations help reduce carbon emissions from 
leaf litter decomposition, which has implications for the global carbon 
cycle (Wyman 1998; Best and Welsh 2014; North American Bsal Task Force 
2020, Laking et al. 2021). This process is known as carbon 
sequestration, which is the storage of carbon dioxide to slow or 
reverse atmospheric carbon dioxide pollution and to mitigate or reverse 
climate change. Salamanders that live underground also contribute to 
soil dynamics by creating, modifying, and otherwise regulating the 
systems of underground burrows in which they live (Davic and Welsh 
2004). Finally, salamanders are important prey species themselves and 
provide energy sources for higher predators (Davic and Welsh 2004), 
including fishes, reptiles, birds, and mammals.
    In vernal pond communities, Ambystoma species are the top predators 
and, therefore, control the abundance of aquatic invertebrates and 
other amphibians (Petranka 1998). The high numbers of many amphibians, 
including salamanders, in some ecosystems also provide a substantial 
source of prey for other vertebrates in the ecosystem (Harper et al. 
2008; Davic and Welsh 2004); therefore, other native species that prey 
on salamanders can also be affected by disease-related declines.

B. Species Information for Batrachochytrium Salamandrivorans

General Information About Bsal
    Bsal is a fungus in the phylum Chytridiomycota and the order 
Rhizophydiales. It was identified in 2013 after reports of a dramatic 
mortality event of fire salamanders in Europe (Martel et al. 2013). In 
drawing some of our conclusions about the effects of Bsal on U.S. 
wildlife and wildlife resources for the 2016 interim rule, the Service 
used Batrachochytrium dendrobatidis (Bd) as a surrogate (similar 
substitute) species because little was known about the emerging disease 
caused by Bsal. Considerably more was known about Bd due to its 
discovery and description more than 15 years earlier (Berger et al. 
1998, Longcore et al. 1999). Bd is found on every continent that 
supports amphibians, while Bsal is known to be only in Europe and Asia. 
Bd has resulted in the serious decline and extinction of more than 200 
species of amphibians worldwide and has posed the greatest threat to 
biodiversity of any known pathogen (Martel et al. 2013). The severe 
effects that Bd, also a fungal pathogen species closely related to 
Bsal, has had on amphibian populations raised additional alarm about 
the expected consequences of a Bsal introduction and the need to take 
immediate action under an interim rule.
    Two scientific risk assessments of Bsal used Bd in determining the 
risk of Bsal based on transmission, spread, and population-level 
effects (Stephen et al. 2015; Richgels et al. 2016). Gray et al. (2015) 
found that both fungi infect the epidermal cells of the amphibian skin, 
and the clinical signs for both include excessive skin shedding, 
lethargy, anorexia, abnormal posture, and death;

[[Page 2201]]

however, the lesions produced by Bd are mainly epidermal hyperplasia 
and hyperkeratosis (rarely ulcerations), and those produced by Bsal are 
mainly skin ulcerations and destruction of the epidermis. Similarities 
and differences between the two fungal pathogens and the diseases they 
cause are discussed in Farrar et al. (2017), Longo et al. (2019), 
Rebollar et al. (2020), and Rollins and Le Sage (2021).
    Since the 2016 interim rule was published, scientists have been 
studying many aspects of Bsal, and this rule reflects new research. 
Relevant studies confirm or expand on our previous information, with 
many adding new insight to the fungus and disease, and some providing 
documentation to support adding new genera as carriers.
    Until Bsal was discovered, the fungal disease chytridiomycosis was 
thought to be caused by a single species of pathogenic fungus, Bd, 
which was the only species from that phylum known to parasitize 
vertebrate hosts (Longcore 1999; Johnson and Speare 2003). Bd has been 
implicated in the decline and extinction of amphibian species at the 
global scale (Berger et al. 1998; Daszak et al. 2003; Lips et al. 2006; 
Walker et al. 2008; Vredenburg et al. 2010; Cheng et al. 2011). Bd has 
been found on every continent except Antarctica, and it is known to 
have affected more than 500 species of amphibians, including all orders 
of amphibians (frogs, salamanders, and caecilians) worldwide 
(Chytridcrisis 2015a; Fisher et al. 2009; Olson et al. 2013).
    Bsal came to the attention of the scientific community in 2013 when 
Spitzen van der Sluijs et al. (2013) observed a 96 percent decline in 
fire salamanders in the Netherlands but was ``unable to attribute this 
to any known cause of amphibian decline, such as Bd, ranavirus or 
habitat degradation.'' Martel et al. (2013) subsequently identified the 
cause of the salamander decline in the Netherlands as a newly described 
species of fungus now known as Bsal. Their work confirmed that Bsal is 
closely related to Bd and is also capable of causing chytridiomycosis; 
both are in the genus Batrachochytrium. Analysis of a broad range of 
representative chytrid fungi show that Bsal represents a previously 
undescribed species that shares early evolutionary origins with the 
pathogenic fungus Bd (Martel et al. 2013).
    The natural amphibian hosts of Bsal remain unknown, but as of 
publication of the 2016 interim rule, Bsal had been found only in 
salamanders and appeared capable of causing lethal chytridiomycosis 
only in salamanders (Martel et al. 2014). Subsequently, several species 
of anurans have been found to be carriers, such as the midwife toad (a 
frog) Alytes obstetricans (Stegen et al. 2017) and small-webbed 
firebelly toad Bombina microdeladigitora (Nguyen et al. 2017).
How the Fungus Affects Salamanders
    The ``salamandrivorans'' in Batrachochytrium salamandrivorans means 
``salamander eating'' and figuratively describes the effects of the 
fungus on salamanders. Bsal infects primarily the skin of salamanders, 
but deeper tissues or internal organs may be affected (McDonald et al. 
2020). The skin of post-embryonic salamanders has a layer of keratin 
(Seifert et al. 2019) covered by a mucosal microbiome of beneficial 
biota that normally protect them from harmful microbes entering the 
body (Bletz et al. 2018; Rebollar et al. 2020), such as a fungus.
    The cells of the fungus (thalli) embed themselves in the skin cells 
of the salamander, thereby causing erosive lesions. Lesions consist of 
sores on the skin that erode and ulcerate, with secondary bacterial 
infection likely occurring after the sores appear (Martel et al. 2013; 
Gray et al. 2015; Bletz et al. 2018), although many of the salamanders 
reported at the beginning of the European Bsal outbreak seemed to lack 
obvious external lesions (Spitzen-van der Sluijs et al. 2013). The loss 
of epidermal integrity from the lesions impairs the skin's ability to 
maintain fluid and electrolyte balance and also perforates the barrier 
that protects the animal from pathogens and compromises their line of 
defense against disease (Gray et al. 2015; Rebollar et al. 2020). 
Experimental infections of fire salamanders in the laboratory caused 
death 12 to 18 days after exposure, with the same clinical signs and 
pathological lesions found in the European outbreak (Martel et al. 
2013) and in another experimental infection around 3 weeks after a high 
dose exposure (Stegen et al. 2017). Martel et al. (2013) found that 
infected fire salamanders developed shallow skin lesions and deep 
ulcerations all over the body, became anorexic and apathetic, and 
suffered from neurological signs including a loss of voluntary movement 
and muscle coordination. Death occurred within 7 days of clinical signs 
first appearing in species with lethal vulnerability. Death is 
generally preceded by a brief episode of abnormal body posture and 
behavior (Gray et al. 2015).
    Some species succumb quickly to Bsal after infection, while others 
seem to tolerate it and eventually clear the infection (Martel et al. 
2014). However, long-term effects on tolerant species are not known. 
Several studies suggest negative long-term effects. For example, the 
long-term proliferation of the fungus within the keratinized limb 
tissue of the olm (Proteus anguinus) may coincide with a more subtle 
cost associated with increased energy expenditure, impaired locomotion, 
or increased vulnerability of the limbs to secondary infection (Li et 
al. 2020). Another study detected potential sublethal reductions of 
growth caused by Bsal exposure in juvenile spotted salamanders soon 
after metamorphosis, although not in older juveniles (Barnhart et al. 
2020). The initial exposure to Bsal may have created a stress response 
that helped activate the immune system; this activation dissipated 
after the threat dissipated but may come at a cost because juvenile 
salamanders with higher corticosterone release rates immediately after 
exposure to Bsal had lower growth compared to control group salamanders 
30 days post-exposure.
    The outcomes of coinfections by Bd and Bsal on salamanders have 
been studied because they both affect the skin. Bd and Bsal are the 
only known Chytridiomycota to have adapted to colonize vertebrates, yet 
Bd infects all three orders of Amphibia (especially Anura), while Bsal 
is currently known to infect primarily the order Caudata (Farrar et al. 
2017). If Bsal enters the Western Hemisphere where Bd is already 
widespread, coinfections could occur, and some research suggests the 
results could be more serious to the Bsal-na[iuml]ve salamanders than 
Bd infection alone (Longo et al. 2019; McDonald et al. 2020). Longo et 
al. (2019) and McDonald et al. (2020) studied coinfection in eastern 
newts (Notophthalmus viridescens), a widespread native salamander. 
Longo et al. (2019) tested newts to see if prior exposure to Bd 
provided immune protection from Bsal or instead reduced the protection. 
They found that newts can clear Bd alone; resistance is specific to Bd 
and does not prevent Bsal infection; simultaneous coinfections were the 
most lethal, even at reduced dosages; host mortality from Bsal can be 
much slower than previously found; and some wild newts may have innate 
Bsal immunity from prior exposure to Bd, but other factors may be 
involved. McDonald et al. (2020) found that Bd and Bsal coinfection 
reduced the host's immune response more than with Bsal alone. Thus, if 
Bsal enters a newt population where Bd already exists, the Bsal 
infection may be compounded by the Bd infection.

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    The Service has no direct evidence that Bsal affects reproductive 
tissue, such as eggs or gametes. Since Bsal attaches to and utilizes 
keratin-containing substrate for growth, and eggs and gametes do not 
contain keratin, we have no evidence that eggs and gametes will carry 
Bsal (L. Sprague, USFWS, pers. comm. 2021). Thus, we do not believe 
that salamander reproductive material can serve as a vector for Bsal 
introduction into the United States.
Thermal Tolerance
    Temperature has a significant effect on the growth and disease 
development of Bsal in salamanders (Martel et al. 2014; Carter et al. 
2021). Bsal appears to prefer an in vitro temperature range for growth 
and infection of 10-15 [deg]C (50-59 [deg]F) (Martel et al. 2013; Blooi 
et al. 2015a; Stephen et al. 2015; Thomas et al. 2019). Bsal has shown 
some spore growth in temperatures as low as 5 [deg]C (41 [deg]F) and 
dies at 25 [deg]C (77 [deg]F) and above (Martel et al. 2013). However, 
the majority of Bsal-infected salamanders in natural Vietnamese ponds 
were in water temperatures of 20-25 [deg]C (68-77 [deg]F) and as high 
as 26.43 [deg]C (79.6 [deg]F) (Laking et al. 2017). In a laboratory 
study, salamanders were most easily infected by Bsal at temperatures of 
15 [deg]C (59 [deg]F) and 20 [deg]C (68 [deg]F), while Bsal growth was 
inhibited at 25 [deg]C (77 [deg]F) (Blooi et al. 2015a). The same 
temperature response was also observed for Bsal raised in culture 
(Blooi et al. 2015a). Grear et al. 2021 used 15 [deg]C (59 [deg]F) as 
the thermal optimum for Bsal growth and evaluated the impact of a 27 
[deg]C (81 [deg]F) thermal maximum to the resulting risk. Carter et al. 
(2021) found that adult and juvenile Notophthalmus viridescens died 
faster due to Bsal chytridiomycosis at 14 [deg]C (57 [deg]F) than at 6 
[deg]C (43 [deg]F) and 22 [deg]C (72 [deg]F).
    These experimental data suggest that salamanders living at cooler 
temperatures are more at risk to infection by Bsal. Animals that 
survive at temperatures above the optimal range for fungal growth are 
likely to be at reduced risk to infection. However, the average 
temperature range of North and Central American salamander species is 
from 11 [deg]C (52 [deg]F) to 20 [deg]C (68 [deg]F) (Duellman and Trueb 
1986; the citation does not separate North and Central American data), 
so salamanders regularly reaching 25 [deg]C (77 [deg]F) in the natural 
environment is uncommon. Bales et al. (2015) noted that the native 
salamander species, and by extension ecosystems, most at risk from a 
Bsal introduction would likely be those that occupy similar thermal 
ranges as the European fire salamander (Bales et al. 2015). Richgels et 
al. (2016) also cited research that Bd is capable of infecting 
amphibians along a larger temperature profile than originally 
predicted, though it is unknown whether this is the case for Bsal.
Ecology and Habitat Preferences
    The chytrid fungus Bd can live outside of a host and requires water 
to disperse because it reproduces asexually by forming motile 
zoospores; preliminary studies of Bsal indicate that similar modes of 
survival and transmission are highly likely (Longcore 1999; Martel et 
al. 2013). As the threat assessment by Stephen et al. (2015) noted, 
``Bd is known to remain viable for several days to weeks in water 
(Johnson and Speare 2013) and moist organic matter (Johnson and Speare 
2003), even in the absence of nutrients. It is likely that Bsal can 
also survive in moist environments, independent of an amphibian host.'' 
Stegen et al. (2017) states that Bsal adopts a dual transmission 
strategy, with environmentally resistant nonmotile spores in addition 
to the motile spores identified in Bd. Bsal retains its virulence in 
water and soil as well as in anurans and less susceptible salamander 
species that function as a reservoir of infectious pathogens. The 
combined characteristics of the disease ecology suggest that Bsal is 
able to rapidly extirpate highly susceptible salamander populations 
across Europe. Stegen et al. (2017) also found that infected fire 
salamanders were shown to contaminate the forest soil and Bsal DNA 
could be detected even after 200 days. Actual transmission through 
contaminated forest soil was demonstrated up to 48 hours after the soil 
had been in contact with an infected animal. Encysted Bsal spores were 
shown to remain infectious in pond water for at least 31 days. 
Together, the presence of a resistant spore with the ability to persist 
environmentally and to transmit through contaminated water and soil, 
combined with the occurrence of long-term-infected and pathogen-
shedding amphibian hosts, creates the potential for extensive 
environmental reservoirs and hampers any effort to eradicate Bsal from 
an infected ecosystem.
Environmental Conditions Needed To Survive
    The transmission and ecology of Bsal in the wild is likely to be 
similar to Bd based on the close taxonomic relationship between the 
species, their structural similarities, and their comparable 
pathophysiology (Martel et al. 2013; Stephen et al. (2015). Disease 
transmission is the means by which communicable pathogenic 
microorganisms, such as fungi, are spread from one organism to another. 
Johnson and Speare (2003) reported that Bd can survive in tap water and 
deionized water for up to 3 and 4 weeks, respectively, and up to 7 
weeks in lake water. Bsal is also likely to survive in moist 
environments independent of an amphibian host; for example, Stegen et 
al. (2017) found that encysted spores can survive and remain infectious 
for at least 31 days in filtered pond water. While we do not have 
information on the response of Bsal to desiccation, Bd is highly 
impacted by drying and can survive desiccation for no more than 1 hour 
in the laboratory (Garmyn et al. 2012); Bsal would likely respond in a 
similar way. Bsal appears to be adapted to lower preferential 
temperatures compared to Bd, with optimal growth between 10 [ordm]C and 
15 [ordm]C, and Bsal spore death occurring at temperatures greater than 
25 [ordm]C (Martel et al. 2013). These findings support the hypothesis 
that the pathogen coevolved with salamanders in the part of the world 
from which it is endemic, most likely in Asia (Martel et al. 2014; 
Laking et al. 2017).

C. Population-Level and Ecosystem-Level Effects of Bsal

Population-Level Effects
    Several pathogens, including Bsal, Bd, ranaviruses, and aquatic 
oomycetes (water molds), have caused significant population-level 
declines in a range of amphibian species, and disease is thought to be 
a major driver of global amphibian decline (Bosch et al. 2001; Daszak 
et al. 2003; Martel et al. 2013). Disease poses a greater risk to 
small, isolated populations as well as those with decreased genetic 
diversity (Smith et al. 2008). Within the United States, diseases have 
been cited as contributing factors in the listing or need for recovery 
of several native amphibian species under the ESA. Examples include Bd 
in the Ozark hellbender (Cryptobranchus alleganiensis bishopi) (76 FR 
61956, October 6, 2011), an undiagnosed disease in Sonora tiger 
salamanders (Ambystoma tigrinum stebbinsi) (62 FR 665, January 6, 
1997), and Bd in the mountain yellow-legged frog (Rana muscosa) (82 FR 
24256, April 29, 2014; Vredenburg et al. 2010).
    As noted above in General Information About Bsal, Bsal is the most 
recently discovered pathogen associated with population-level amphibian 
declines, including a 96 percent reduction in Dutch populations of the 
European fire salamander in the period 2010-2013 (Spitzen-van der 
Sluijs et al. 2013; Martel et al. 2013). Due to the

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overall sensitivity of amphibian populations to disease; a history of 
adverse, population-level effects in native amphibians; a direct 
association between Bsal and the decline of at least one European 
salamander population; and the adverse effects of some native 
salamanders to Bsal under experimental conditions, we conclude that the 
introduction of Bsal into the United States would cause significant, 
adverse, population-level effects in a number of native species.
Ecosystem-Level Effects
    The preferred temperature range of Bsal can help predict those 
ecosystems that are at greatest risk should Bsal be introduced into the 
United States (Stephen et al. 2015). The native salamander species, and 
by extension ecosystems, most at risk from a Bsal introduction would 
likely be those that occupy similar thermal ranges as the European fire 
salamander (Bales et al. 2015).
    Salamanders are important parts of the ecosystems in which they 
occur. Salamanders are often the most abundant vertebrates in 
terrestrial forest and riparian (the banks of watercourses) ecosystems, 
where they may compose a total biomass greater than or equal to birds 
or small mammals (Davic and Welsh 2004). This means that, despite their 
small size, the total weight of all salamanders in a given area may be 
more than the combined total weight of all birds or all small mammals. 
Because of their abundance under normal circumstances, salamanders are 
important prey species themselves and are energy sources for higher 
predators (Davic and Welsh 2004), including fishes, reptiles, birds, 
and mammals.
    Salamanders may be the dominant predator in headwater streams and 
ephemeral waterbodies where fish are absent (Davic and Welsh 2004). 
Within some food webs, salamanders are considered keystone predators 
due to their control of invertebrate prey populations and their 
resulting regulation of detritus decomposition and nutrient cycling 
(Davic and Welsh 2004). By definition, keystone species are those that 
occupy niches that affect ecosystems and have little functional overlap 
with other species (Davic and Welsh 2004). Therefore, loss of these 
keystone species would result in significant ecosystem-level change.
    In addition to their roles in food webs and nutrient cycling, 
salamanders participate in a number of interspecific (between species) 
ecological relationships. Salamander species interact with one another 
through competition and predation to control the composition of their 
assemblages (taxonomically related species that occur within the same 
geographic community) (Davic and Welsh 2004; Fauth et al. 1996). 
Frequently, a single species is dominant within a given assemblage, 
particularly in terrestrial habitats, but which species dominates 
varies by location and ecosystem (Davic and Welsh 2004). We expect that 
ecosystems where the dominant salamander species is susceptible to 
lethal or sublethal Bsal infection would be at risk from an 
introduction of this pathogen.
    Salamanders also interact with invertebrate species in other 
ecologically important ways. Semi-aquatic salamander species can move 
mollusks and shrimp eggs between waterbodies during their migrations, 
allowing these invertebrates to inhabit new areas (Davic and Welsh 
2004). For example, a native species of salamander, the mudpuppy 
(Necturus maculosus), is a required host for developing stages of the 
salamander mussel (Simpsonaias ambigua), a native, freshwater mollusk 
(Davic and Welsh 2004; Gangloff and Folkerts 2006). We conclude that 
invertebrate species that depend on salamanders for aspects of their 
life cycle or ecology are likely to be adversely affected if their host 
species declines in response to a Bsal introduction.

D. Invasiveness of Salamanders and Bsal

Invasiveness of Salamanders
    Executive Order 13751 defines an ``invasive species'' as a 
nonnative organism with regard to a particular ecosystem whose 
introduction causes or is likely to cause economic or environmental 
harm, or harm to human, animal, or plant health. Two key components of 
invasiveness are introduction into nonnative ecosystems and causing 
harm.
    Globally, 90 percent of salamander introductions have occurred 
through intentional releases (Tingley et al. 2010). As of 2010, 
salamanders comprised 22 percent of all recorded amphibian 
introductions, with the highest number of salamander introductions (15) 
from the family Salamandridae, followed by salamanders from the 
families Ambystomatidae (4), Cryptobranchidae (2), and Proteidae (2) 
(Tingley et al. 2010). Nonnative salamander introductions have been 
documented in the United States. The USGS's Nonindigenous Aquatic 
Species database has U.S. records for 17 salamander species that have 
been observed outside their native range (USGS 2023). Of those, 14 are 
native to the United States but were discovered outside of their native 
ranges, and 3 (Japanese fire-bellied newt Cynops pyrrhogaster, Oriental 
fire-bellied newt Cynops orientalis, and paddle-tailed newt 
Paramesotriton (Pachytriton) labiatus) are species native to the 
eastern hemisphere. In Florida, the Oriental fire-bellied newt and 
paddle-tailed newt (family Salamandridae), which are native to China, 
have been found in the wild near an animal importer's facility, either 
as the result of intentional releases or escapes from enclosures 
(Krysko et al. 2011), although none have been reported since 2010 (USGS 
NAS 2021 [CYOR, PALA]). While these two species apparently did not 
establish invasive populations, their presence in the wild demonstrates 
a possibility that escaped individuals can persist long enough in the 
wild to transmit Bsal to native populations.
    Other invasions have been attributed to the use and subsequent 
release of salamanders used as fishing bait. Surveys of anglers have 
indicated that they routinely release salamanders into the areas where 
they fish, which includes areas that are not part of the salamander's 
native habitats, suggesting that animals are routinely moved long 
distances (Picco and Collins 2008). Furthermore, Picco and Collins 
(2008) found that salamanders sold as bait were highly infected with 
both ranavirus and Bd, thereby increasing the likelihood of disease 
transmission into new areas of the United States through the act of 
fishing.
Invasiveness and Transmission of Bsal
    As noted above under General Information About Bsal, Europe has 
been experiencing a severe decline in wild fire salamander populations 
in the Netherlands (Spitzen-van der Sluijs et al. 2013). This decline 
is so significant that fire salamander populations are facing local 
extinction in the Netherlands. A sharp decline in numbers has been 
observed since 2010, despite the species being listed as endangered on 
the Netherlands Red List, and at population levels that were thought to 
be stable. This enigmatic decline was not attributed to any known cause 
of amphibian decline, such as chytridiomycosis due to Bd, ranavirus, or 
habitat degradation. In late 2013, Bsal was isolated from infected fire 
salamanders in the Netherlands (Martel et al. 2013).
    Martel et al. (2014) later established the highly pathogenic nature 
of this new chytrid fungus. Molecular testing found Bsal in specimens 
collected from the wild (though none from North America)

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and even in an archival (museum) sample that was 150 years old (Martel 
et al. 2014). Alpine newts (Ichthyosaura alpestris) and smooth newts 
(Lissotriton vulgaris) in the wild are also now known to be infected 
(Spitzen-van der Sluijs et al. 2016), as are palmate newts (L. 
helveticus; Lastra Gonz[aacute]laz et al. 2019).
    A wide variety of salamanders are negatively affected by the 
pathogen, but 10 species of frogs and toads and the 1 caecilian species 
did not appear to be (Martel et al. 2014). More recently, two anuran 
species have been shown to be carriers of Bsal. Small-webbed fire-
bellied toads from wild populations in Vietnam and from individuals 
from that region imported into Germany tested positive for Bsal by qPCR 
swabs (Nguyen et al. 2017), and the midwife toad was capable of 
infecting fire salamanders for several weeks after experimental 
inoculation (Stegen et al. 2017). However, we are listing only caudate 
genera with this rule, and anurans would need to be considered in 
separate rulemaking. The pathogenic nature of the fungus and its 
ability to infect a wide variety of salamanders, as described below in 
Vulnerability and Carrier Status, definitively demonstrate an invasive 
threat to salamanders in the United States.
    Emerging infectious diseases that can cause mass mortality are 
especially worrisome because they can cause extinction and subsequent 
loss of biodiversity relatively rapidly. The only in situ example of 
the spread of Bsal is with fire salamanders in Europe. Using this 
example, Schmidt et al. (2017) developed a model to explore the effects 
of the recently emerged Bsal. They showed that disease outbreaks can 
occur at very low host densities (one female per hectare (2.5 acres)) 
in the wild and that this is much lower than host densities in the 
wild. Therefore, all naturally occurring populations are at risk, and 
the model predicts a rapid collapse of the host population. Experiments 
have shown that Bd can be transferred from one species to another when 
an uninfected species comes into contact with an infected species 
(active carrier) or infected fomites (Carey et al. 2006) (passive 
carrier). Bsal can similarly be transmitted from one species to another 
(Martel et al. 2014; Stegen et al. 2017; Homan et al. 2018). Bd has 
contributed to the decline of at least 501 amphibian species worldwide 
(6.5 percent of described amphibian species), which is the largest 
documented loss of global biodiversity attributable to a pathogen 
(Scheele et al. 2019). Bsal is expected to have a similar effect, 
although perhaps not as much on anurans.
    Salamanders that breed in ponds and temporary wetlands are often 
explosive breeders, meaning that hundreds to multiple thousands of 
individuals will congregate at the same time (Gill 1978), creating 
dense numbers of individuals and increasing opportunities for the 
pathogen to spread. After breeding, the adults then return by land to 
their original habitats, potentially carrying the pathogen to new 
locations. Pathogens are also likely to be transmitted by salamander 
species that travel long distances for breeding and dispersal 
migrations, such as those that exhibit a metapopulation structure 
(Bancroft et al. 2011). A metapopulation is a group of discrete 
breeding populations of the same species (Gill 1978). For example, 
within salamander metapopulations, California tiger salamanders have 
been documented traveling up to 1.2 miles (1.9 kilometers) from upland 
habitat to aquatic breeding sites (USFWS 2000), and newts travel many 
kilometers to breeding sites (Gill 1978).
    Salamander species that have abundant populations with widespread 
distributions can also contribute to the spread of Bsal because of the 
increased likelihood that they will come in close contact with other 
salamanders that could then become infected. Salamanders that can carry 
Bsal from one place to another are more likely to do so if they have a 
broad range where they will come in contact with other members of the 
same species (for abundant distributions) or other species (for 
widespread distributions). Species with broad distributions are adapted 
to a wide range of environmental conditions that are more likely to 
overlap with habitat suitable for Bsal as well as habitat suitable for 
that species, providing increased opportunities for Bsal to spread.
    For example, the rough-skinned newt has a wide range along the West 
Coast from Alaska to California, and the eastern newt is found widely 
across the Eastern United States and Canada, occurring in 34 States 
(AmphibiaWeb 2023a). Both species have had lethal responses with 
laboratory infections of Bsal (Martel et al. 2014; Carter et al. 2021; 
Gray et al. 2023), and both are capable of carrying Bsal. In addition 
to its broad range, the eastern newt also migrates long distances; this 
species will frequently travel many kilometers to migrate to new ponds 
(Gill 1978), further increasing the risk of this species spreading 
Bsal. The eastern newt's widespread distribution, high dispersal 
ability, high susceptibility, and juxtaposition with a high diversity 
of other salamander species position the species to significantly 
contribute to the spread of Bsal and the decline of salamander 
populations in the Eastern United States (Malagon et al. 2020).

E. Pathway Analysis

Introduction Pathways
    The main pathway for the global spread of Bsal is the international 
trade in salamanders (Martel et al. 2014; Yuan et al. 2018). The 
introduction of Bsal into mainland Europe is linked with the commercial 
trade of Asian salamanders (Cynops spp.) from East Asia, particularly 
Thailand, Vietnam, Japan (Martel et al. 2014), and China (Yuan et al. 
2018). Combined, species from the genus Cynops were by far the most 
commonly imported into the United States from 2004 to 2014 (USFWS OLE 
2015), with Cynops orientalis alone comprising 54 percent of the 
salamander imports. Since the 2016 interim rule went into effect, 
Cynops spp. imports have been restricted to those with approved permits 
from the Service. As described above in How the Fungus Affects 
Salamanders, there is no evidence that eggs and gametes are vectors. 
However, salamanders that have been identified as carriers, whether 
live or dead (except if chemically or heat preserved), appear capable 
of transmitting Bsal through contact with their skin (Gray et al. 2015; 
Van Rooij et al. 2015; Carter et al. 2020), which contains keratin 
(Seifert et al. 2019). We are also concerned that any infected and 
lethally vulnerable salamanders may die in transport and continue post-
mortem to carry Bsal into the United States, or that salamanders may 
knowingly be imported dead. Bsal can remain viable inside dead host 
tissue (Martel et al. 2013), although it is unclear how long a dead 
host remains infectious (WOAH 2021b). One study found that viable Bsal 
loads on carcasses of eastern newts did not decline in 72 hours after 
euthanasia, and carcasses were capable of transmitting Bsal to 
susceptible hosts for at least 72 hours after death; the infections 
that developed in the susceptible animals caused nearly 100 percent 
mortality in cohousing treatments that allowed for contact (Carter et 
al. in review). Therefore, we expect unpreserved, dead salamanders and 
body parts, except for purified extracted genetic material, to be a 
pathway for introduction.
    Individual amphibians in trade are often transported in containers 
with many other individuals of the same species or with many other 
species that can all be from different sources. These

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conditions are highly conducive to pathogen transmission and dispersal. 
Pathogens can transfer from host to host in crowded conditions, and 
crowded conditions create stress on animals that can reduce amphibian 
hosts' natural ability to resist infections (Rowley et al. 2007, 
Rachowicz et al. 2005, Rollins-Smith et al. 2011). Bsal can also be 
introduced into the environment through the improper disposal of 
contaminated water or other materials used to transport salamanders. As 
described above under Environmental Conditions Needed To Survive, the 
fungus can likely persist in those materials independent of the 
presence of a salamander. Water and fomites have served as a 
transmission medium and passive vector, respectively, to introduce 
other similar pathogens into the environment. For example, Bd has been 
found in water used to transport amphibians that were traded in Hong 
Kong (Kolby et al. 2014). As the authors noted, ``[T]he abundance of 
aquatic amphibian species traded by Hong Kong * * *, prolonged 
environmental persistence of infectious * * * Bd particles, and 
employment of trade activities that neither disinfect water nor safely 
dispose of deceased animals creates an ideal pathway for disease 
transmission to native Hong Kong amphibians.'' While experiments of 
fomite transmission for Bsal have not been conducted yet to our 
knowledge, Bd has been shown capable of infecting boreal toads (Bufo 
boreas) if an uninfected individual comes in contact with water where 
an infected individual has shed spores, even if the infected individual 
is no longer present (Carey et al. 2006). Similarly, encysted Bsal 
spores have been shown to remain infectious in pond water for at least 
31 days and capable of adhering to salamander skin and the feet of 
waterfowl (Stegen et al. 2017).
    Disinfecting of containers and substrate is always advisable when 
transporting amphibians. However, Van Rooij et al. (2017) found that 
the cell wall of the zoosporangium and the encysted spores within it 
provide a double barrier against the action of the disinfectants. This 
may explain (partially) why higher disinfectant concentrations or a 
longer contact time are necessary to achieve full fungal killing of 
Bsal, compared to those necessary for inhibition of Bd. Also, the 
clustering of multiple Bsal zoosporangia may protect centrally located 
sporangia from the full impact of a given disinfectant.
    Drawing on this evidence, the primary pathway for the entry of 
salamanders that are carriers of Bsal into the United States is through 
the international commercial wildlife trade. Overall, 99.9 percent of 
live salamander importation into the United States is for commercial 
purposes (USFWS OLE 2021). From 2010 to 2015, live salamanders were 
imported through 20 ports of entry into the United States; the 3 ports 
of entry with the largest numbers of imported salamanders were Los 
Angeles (54.6 percent), Tampa (34.8 percent), and New York (6.8 
percent). From 2016 to 2020, live salamanders were imported through 8 
ports of entry, with the top 4 from Miami (63.3 percent), Boston (11 
percent), Newark (10.5 percent), and New York (9.2 percent). After 
import, many of the salamanders are transported to animal wholesalers, 
who then transport the salamanders to pet retailers.
    The most likely pathway of a salamander that is a host to Bsal into 
the United States would be through captive salamander commercial trade. 
We make that conclusion based on Martel et al. (2014), who noted that, 
given the discontinuity of the global distribution of Bsal, 
introduction from Asia into Europe must have been human mediated. 
Cunningham (2015), Sabino-Pinto et al. (2015), and Grear et al. (2021) 
also implicated trade as a key factor in the spread of Bsal. The United 
States is more isolated than European countries from other countries 
where salamanders could migrate independently, but there is an active 
trade in salamanders into the United States (USFWS OLE 2021), as 
discussed more in the following section (and would be more so without 
the second interim rule and final rules). People can purchase 
salamanders from pet stores or online retailers and keep them in 
captivity. Amphibians and reptiles kept as pets may eventually be 
released by their owners into the wild either intentionally or 
accidentally (Kraus 2009, Krysko et al. 2011). For example, owners may 
no longer be able to care for their captives or an animal may escape 
its enclosure. Sick captive salamanders are often released instead of 
being euthanized; for example, around 200 Japanese fire-bellied newts 
were released in the Miami, Florida, area in 1964 when they became sick 
and unsuitable for sale (USGS NAS 2021 [CYPY]). They died, but 
fortunately, this was before highly contagious amphibian pathogens were 
known to be in the United States.
    In addition to the risk from a release of an infected pet 
salamander into the wild, the water that is used to house an infected 
pet in captivity could feasibly contain Bsal zoospores. As a result, 
the discharge of untreated water used to house infected, captive 
animals could be a pathway for releasing infective zoospores into the 
environment and exposing native salamanders to Bsal (Stephen et al. 
2015). A reduction in the transport of salamanders in trade would 
reduce the potential for contaminated water to carry spores to other 
areas.
International Trade in Salamanders
    Trade in wildlife occurs on a global scale, and amphibians are some 
of the most commonly traded animals (Smith et al. 2009). More than 
52,149,000 documented amphibians were imported into the United States 
from 2004 to 2014, based on the Service's LEMIS data (USFWS OLE 2015), 
and 37,344,000 were imported from 2010 to 2020 (USFWS OLE 2021). 
Salamanders comprised 2,504,590 (4.8 percent) of the total imports of 
amphibians (USFWS OLE 2015) and 892,190 (2.4 percent) from 2010 to 2020 
(USFWS OLE 2021). The 2004 to 2014 LEMIS dataset should be considered 
as a conservative estimate because many import records identified the 
animal being imported only as a member of the Class Amphibia (rather 
than identifying it to species or genus level). In addition, incorrect 
salamander identifications to genus and species level appear to have 
commonly occurred in reporting to LEMIS (USFWS OLE 2015). LEMIS data 
for 2004 to 2014 shows that 65 percent of imported salamanders came 
from captive sources, and 35 percent were from wild sources (USFWS OLE 
2015); for 2016 to 2020, 46 percent came from captive sources, and 54 
percent were wild caught (USFWS OLE 2021). The LEMIS data recorded only 
83 percent of declared salamander imports at the species level, whereas 
17 percent were recorded only to the genus level (USFWS OLE 2015); for 
2010 to 2020, it was 95.5 percent to species and 6.5 percent to genus 
respectively (USFWS OLE 2021).
    The four salamander genera most commonly imported into the United 
States from 2004 to 2014 were Cynops, Paramesotriton, Triturus, and 
Pachytriton (USFWS OLE 2015). Cynops, Triturus, and Paramesotriton are 
three genera that are known to serve as carriers for Bsal (Martel et 
al. 2014). Of the 20 genera listed by the 2016 interim rule, 18 had 
been traded (live or parts) over the 11 pre-interim rule years, and 
they comprised 95 percent of imported salamanders. From 2016 through 
2020, live imports of the top four salamander genera were 
Paramesotriton (524), Cynops (500), Bolitoglossa (191), and Pleurodeles 
(179); all but the Bolitoglossa were under injurious wildlife permits.

[[Page 2206]]

    The species with the highest number of imports into the United 
States from 2004 to 2014 was the Oriental fire-bellied newt. This 
species comprised 54 percent of the total number of imported 
salamanders (USFWS OLE 2015). Twelve species of salamanders that are 
native to the United States were also imported into the United States 
from other countries from 2004 through 2014 (USFWS OLE 2015). From 2016 
through 2020, 16 species of native salamanders were imported. Live eggs 
from the spotted salamander (Ambystoma maculatum), axolotl, and 
Japanese fire-bellied newt were imported between 2016 and 2020.

F. Risk Assessments of Bsal

Bsal Risk Assessments
    Three Bsal risk assessments were used to help determine the risk 
associated with Bsal introduction into North America for the 2016 
interim rule. Richgels et al. 2016 and Yap et al. (2015) conducted risk 
assessments for the United States that helped determine the level of 
risk associated with Bsal introduction. Stephen et al. (2015) also 
conducted a Bsal risk assessment for Canada that showed Canada is also 
at risk.
    Richgels et al. (2016) concluded that the potential for Bsal 
introduction into the United States is high, the United States has 
suitable conditions for Bsal survival, and the consequences of 
introduction into the United States are expected to be severe and occur 
across a wide range of the United States. To evaluate the potential for 
Bsal introduction, the assessment combined information on the number of 
individual salamanders imported at each port of entry and the number of 
pet-supply establishments by county. Based on this evaluation, Bsal 
introduction potential was highest in central and southern Florida, 
southern California, and near New York City, New York (Richgels et al. 
2016).
    As noted in Richgels et al. (2016), the areas of highest potential 
for Bsal introduction are not necessarily the same as the areas of 
greatest risk for impacts to wildlife and wildlife resources. To 
determine the consequences of Bsal introduction into the United States, 
including from the areas where the introduction potential was highest, 
Richgels et al. (2016) evaluated environmental suitability, spatial 
data on imports and pet trade activity, species richness, and predicted 
species susceptibility. Overall, the total risk of Bsal to native 
salamanders is high. While not all areas of the United States are at 
risk from Bsal, based on both likely introduction and resultant 
consequences, the risk of Bsal is highest for the Pacific coast, 
southern Appalachian Mountains, and mid-Atlantic regions (Richgels et 
al. 2016). Some areas, such as south Florida and parts of the West, are 
likely to have low consequences from Bsal introduction. The areas most 
likely to have consequences from Bsal introduction are the Pacific 
Coast and Appalachian Mountains (Richgels et al. 2016). Based on 
environmental suitability, areas of the United States most suited to 
Bsal growth (Blooi et al. 2015a), including the Southwest, Southeast, 
and Pacific regions, are also the areas of highest salamander diversity 
(Richgels et al. 2016).
    In the United States, Yap et al. (2015) identified the Southeastern 
(southern end of the Appalachian Mountains and neighboring southeast 
region) and Western United States (Pacific Northwest and the Sierra 
Nevada) as zones of high risk. Yap et al. (2015) identified a narrower 
total risk in the United States over a smaller area for Bsal compared 
to Richgels et al. (2016). For example, Yap et al. (2015) identified 
south Florida as low risk of Bsal vulnerability, while Richgels et al. 
(2016) found that there was some risk, if not the highest, of Bsal to 
native salamanders in Florida. Richgels et al. (2016) noted differences 
in the methods used between the two papers as the reason. For example, 
Richgels et al. (2016) uses the thermal range of Bsal rather than the 
native Asian host distribution applied in Yap et al. (2015), which 
Richgels et al. (2016) noted may not be vulnerable to infection across 
the entire range of those species. The model in Richgels et al. (2016) 
took environmental suitability into account but also used species 
diversity, proximity to ports of entry, and areas of high pet-trade 
activity to predict total risk. This approach may over- or 
underestimate risk for some areas.
    Some salamander species may be protected from Bsal by temperatures 
in their regions that are outside of the Bsal optimal growth range 
(Richgels et al. 2016) (see Climate Tolerance section). However, the 
average temperature preferences of salamanders from Central and North 
America (Duellman and Trueb 1986), which range from -2.0 [deg]C (28.4 
[deg]F) to 30.0 [deg]C (86.0 [deg]F), suggest that most salamander 
species, including those within the United States, are active near the 
thermal growth optimum for Bsal (Blooi et al. 2015a). As a result, most 
salamander species in the United States are not protected from Bsal by 
living outside of the Bsal optimal growth range or in areas beyond the 
threshold where Bsal can survive.
    Most U.S. salamander species are also dependent upon forests, a 
habitat type dominated by relatively cool, moist conditions, for the 
majority of their life cycle (Davic and Welsh 2004). It is possible 
that cool seasons or microclimate selection by salamanders could 
facilitate disease outbreaks in areas where the average temperatures 
are outside the preferred range of the fungus.
    A fourth risk assessment was added for this second interim rule, 
led by the USGS (Grear et al. 2021). They used post-interim rule 
outcomes and new information to update the Richgels et al. (2016) 
assessment. Grear et al. (2021) evaluated the effects of the 2016 
interim rule on the introduction of Bsal into the United States and 
reviewed new information on species susceptibility to reevaluate the 
risk of Bsal to the United States. Since no comprehensive surveillance 
for Bsal was available prior to the 2016 interim rule, they also used 
the results from Waddle et al. (2020) of their large-scale surveillance 
for Bsal across 594 counties in 35 States and 1 site in Mexico, with 
11,189 swab samples of wild salamanders and some anurans. The 
surveillance sites were strategically chosen for highest risk based on 
species susceptibility and geography. The surveillance did not detect 
any Bsal, which was as hoped, but the surveillance plan they developed 
can continue to be used for early detection of Bsal at high-risk 
locations.
    Grear et al. (2021) also found that the 2016 interim rule reduced 
the importation of listed genera by several orders of magnitude, which 
concurs with our results. They noted several additional genera of 
salamanders and several of anurans (particularly Bombina spp.) that 
could be carriers of Bsal but were not listed in 2016; the additional 
salamander genera are included for listing in this interim rule, while 
the anurans are not (see Impacts on Wildlife Resources or Ecosystems 
for explanation why). Among other variables, Grear et al. (2021) used 
updated information about the thermal tolerance of Bsal that included 
water temperatures associated with detection of Bsal in its presumed 
native geographic and host ranges. They noted that the change and 
spatial variation in risk scores from considering a higher maximum-
temperature threshold had no discernible net effect on the consequence 
score. Therefore, they chose not to use the temperature threshold in 
recalculating the consequence and total-risk estimation;

[[Page 2207]]

instead, they focused their risk comparisons on import regulations, 
host-species range, and surveillance. The study looked at the change in 
ports of import between pre- and post-interim rule and calculated the 
risk change for those regions. They concluded that, while the import 
regulations mitigated some of the import risk, overall risk is still 
driven by the potential of release from undetected Bsal circulating in 
captive amphibians in the United States and the consequences of that 
release in high salamander-biodiversity areas; however, little 
information is known on movement of captive host species and possible 
undetected Bsal in U.S. captives.
Vulnerability and Carrier Status
    The urgent need to prevent Bsal introduction risks with the 2016 
interim rule was raised by evidence presented by Martel et al. (2014), 
who tested Bsal on 35 species from all 3 orders of amphibians: frogs, 
salamanders, and caecilians. Martel et al. (2014) further screened 
5,391 specimens collected from 4 continents for evidence of Bsal 
infection. Martel et al. (2014) defined a ``resistant'' salamander as 
one that either was not infected or developed a short-term infection 
without clinical signs following exposure to Bsal; a ``tolerant'' 
salamander is one that maintains a more prolonged infection with no 
signs of disease; a ``susceptible'' salamander becomes infected and has 
clinical signs of disease with the possibility of subsequent recovery; 
and a salamander that responds in a ``lethal'' manner to Bsal dies as a 
result of infection. According to Martel et al. (2014), resistant 
salamanders are not a risk for transmitting Bsal. However, based on the 
available scientific data, we concluded that resistant species with 
evidence of short-term or transient infection, as well as those 
reported to have tolerant, susceptible, or lethal responses to Bsal, 
are carriers capable of transmitting Bsal to other salamanders and 
introducing the fungus into the United States.
    The Service considered a species to be a ``noncarrier'' when Martel 
et al. (2014) classified the species as ``resistant'' and no histologic 
or field surveillance data was found to suggest that short-term Bsal 
infection could occur; ``noncarriers'' were considered incapable of 
transmitting Bsal to other salamanders or introducing the fungus into 
the United States. If Martel et al. (2014) classified the species as 
resistant with no histology (or qPCR) to verify, its carrier status was 
inconclusive. We use this same definition in this second interim rule.
    We also found, and still maintain, that the likelihood of species 
within the same genus as being carriers can be drawn from a comparison 
to Bd, which, as described above under General Information About Bsal, 
is a close relative of Bsal. As noted earlier, the two risk assessments 
of Bsal used Bd in determining the risk of Bsal based on transmission, 
spread, and population-level effects (Richgels et al. 2016; Stephen et 
al. 2015). Considerably more was known about Bd than Bsal due to its 
discovery and description more than 15 years earlier (Berger et al. 
1998; Longcore et al. 1999), while Bsal was discovered in 2013 (Martel 
et al. 2013). Bd has caused amphibian declines and extinctions 
worldwide (Skerratt et al. 2007). Bd affects species in patterns 
(Skerratt et al. 2007), and more closely related species have similar 
outcomes for Bd at the family level (Smith et al. 2009; Bancroft et al. 
2011).
    Amphibians experiencing the most severe declines are grouped by 
relatedness, which is likely due to the shared evolutionary histories 
of closely related species with a similar response to chytridiomycosis 
(Corey and Waite 2008). The USDA uses a similar approach. Closely 
related species are considered more likely to have similar traits and 
are used in risk assessments to determine threats from a target species 
of interest; a potential pest is regarded as a threat when other 
species in a genus pose a similar threat (Wapshere 1974; Gilbert et al. 
2012). The European Union's study on the feasibility of a movement ban 
of traded salamanders concluded that, due to the complexity of the 
taxonomy as well as the lack of evidence related to all the species, a 
movement ban at the level of taxonomic order is likely to be more 
effective and more feasible than a species-specific ban (EFSA et al. 
2017).
    Many salamanders exhibited a strong, adverse response to 
experimental Bsal infection; many species from outside of the native 
range of the fungus (Asia) exhibited lethal vulnerability. For the 2016 
interim rule, our review of Martel et al. (2014) and follow-up 
communication (A. Martel, University of Maryland, pers. comm. 2015) 
categorized 25 species from 19 genera as carriers of Bsal. Additional 
communications (Chytridcrisis 2015b; Cunningham et al. 2015; P. 
Nanjappa, Association of Fish and Wildlife Agencies, pers. comm. 2015) 
identified another two species from two separate genera as carriers: 
the pygmy marbled newt (Triturus pygmaeus) and the golden striped 
salamander (Chioglossa lusitanica). Because Martel et al. (2014) had 
previously identified members of the Triturus genus as carriers, it was 
already accounted for within the 19 genera. The addition of this 
species brought the total number of known carrier species to 26. In 
addition to Triturus, Chioglossa was identified as another genus 
capable of serving as a Bsal carrier by Chytridcrisis (2015b), 
Cunningham et al. (2015), and P. Nanjappa (Association of Fish and 
Wildlife Agencies, pers. comm. 2015). As a result, the total number of 
genera known to serve as carriers of Bsal was 20 genera, and these were 
Chioglossa, Cynops, Euproctus, Hydromantes, Hynobius, Ichthyosaura, 
Lissotriton, Neurergus, Notophthalmus, Onychodactylus, Paramesotriton, 
Plethodon, Pleurodeles, Salamandra, Salamandrella, Salamandrina, Siren, 
Taricha, Triturus, and Tylototriton.
    Further studies since the 2016 interim rule have included species 
from some of the same genera listed in 2016, which we reviewed to see 
if they were consistent with earlier conclusions. Carrier status is 
further supported for Chioglossa (C. longipes and C. lusitanica in 
Bosch et al. 2021); Lissotriton (L. boscai, Fitzpatrick et al. 2018, 
Bosch et al. 2021; L. lusitanica, Lastra Gonz[aacute]laz et al. 2019), 
Triturus (T. dobrogicus, T. ivanbureschi, T. karelinii, and T. 
marmoratus, Fitzpatrick et al. 2018; T. marmoratus, T. pygmaeus, Bosch 
et al. 2021), Neurergus (Fitzpatrick et al. 2018), Notophthalmus 
(Fitzpatrick et al. 2018; Gray et al. 2023), Plethodon (P. cinereus, P. 
cylindraceus, P. glutinosus, P. montanus, and P. shermani, DiRenzo et 
al. 2021), Salamandra (S. atra, Fitzpatrick et al. 2018), Siren (S. 
lacertina, Gray et al. 2023), and Taricha (T. granulosa, T. torosa, 
Gray et al. 2023). Studies for Chioglossa (Fitzpatrick et al. 2018), 
and Plethodon (Perreira and Woodley 2021) showed no conclusive 
countervailing evidence.
    Using the same criteria as in the 2016 interim rule, this second 
interim rule adds the following 16 genera: Ambystoma, Andrias, Aneides, 
Aquiloeurycea, Calotriton, Chiropterotriton, Cryptobranchus, 
Desmognathus, Ensatina, Eurycea, Laotriton, Ommatotriton, Pachytriton, 
Proteus, Pseudobranchus, and Pseudotriton. This increases the total 
number of species listed by approximately 164.
    In conducting our analysis, the Service initially focused on 
identifying species for listing as injurious that scientific evidence 
demonstrates are capable of carrying Bsal. As we described above, we 
find that, due to shared characteristics by species within a genus, 
other species within these

[[Page 2208]]

genera are also highly likely to be carriers of Bsal, even if not every 
species in the genus has been tested to verify that it is a carrier of 
Bsal. This conclusion is because closely phylogenetically related 
species, such as those found within the same genus, share common 
traits. Our analysis found no conclusive evidence to the contrary that 
suggested that some species within such genera are not carriers. We 
have focused our findings on taxa of salamanders and their genera that 
we determined to be capable of carrying Bsal. We included genera 
identified as resistant by Martel et al. (2014) because carrier status 
was inconclusive in that study when histology was not done, and there 
are other studies supporting carrier status; these are Ambystoma, 
Hynobius, Lissotriton, and Plethodon (see Vulnerability and Carrier 
Status of Native Species below). Based on our analysis of their data 
and other studies, we have no evidence for the salamander genera we are 
not listing of being capable of introducing Bsal to the United States 
or otherwise transmitting Bsal to native populations. In addition, we 
are not listing genera where there was no data as of the drafting of 
this second interim rule because we do not have a basis for doing so, 
even though the Service recognizes that it is possible that untested 
genera may also be capable of carrying Bsal.
    We have determined that all species are injurious in the 16 genera 
where at least one species has been conclusively identified as a 
carrier of Bsal and there is no conclusive countervailing evidence 
suggesting that some species within the genus are not carriers. Where 
one species has been identified as a carrier, we expect that the other 
species in that genus are also carriers. This finding includes as 
injurious the intrageneric hybrids (crosses of species found within the 
same genus), intergeneric hybrids of species in two listed genera, and 
intergeneric hybrids from a listed and an unlisted genus.
    For this second interim rule, we maintain that, due to shared 
characteristics by species within a genus, other species within these 
genera are also likely to be carriers of Bsal if one species has been 
identified as a carrier, even if not every species in the genus has 
been tested to verify that it is a carrier of Bsal. Our updated review 
found no conclusive countervailing evidence that species differed 
within a genus with respect to their ability to act as carriers. Thus, 
we expect all species in a genus to respond similarly as carriers or 
noncarriers to Bsal. Therefore, based on existing scientific evidence, 
and as described in more detail below, we are listing all species in 
the 16 genera, including all species, that we now conclude constitute a 
threat to introducing and spreading Bsal in the United States because 
those species can carry the fungus and transmit it to other species 
that would be negatively impacted.
Vulnerability and Carrier Status of Native Species
    Including both the final rule to the 2016 interim rule and this 
second interim rule, we conclude that approximately 426 salamander 
species from around the world are carriers of Bsal (36 genera in 7 
families). The United States currently has approximately 221 species of 
native salamanders in 23 genera (AmphibiaWeb 2023a), and this second 
interim rule includes 164 of those species (13 genera in 5 families) 
that we have determined are carriers of Bsal. Of the remaining 57 
native species, we find that either they are not carriers or the 
vulnerability and carrier status is unknown.
    Of the 190 native U.S. salamander species as of the 2016 interim 
rule, carrier status had not been assessed in 103 species from 16 
genera. The untested genera were Amphiuma, Aneides, Batrachoseps, 
Cryptobranchus, Desmognathus, Dicamptodon, Ensatina, Eurycea, 
Hemidactylium, Necturus, Phaeognathus, Pseudobranchus, Pseudotriton, 
Rhyacotriton, Stereochilus, and Urspelerpes.
    Since the 2016 interim rule went into effect, we have evidence that 
eight more native genera, not previously tested, support listing with 
this second interim rule: Ambystoma, Aneides, Cryptobranchus, 
Desmognathus, Ensatina, Eurycea, Pseudobranchus, and Pseudotriton. We 
previously considered Ambystoma as resistant because Martel et al. 
(2014) had done so for two species, and Bsal was not detected during 
testing. However, Martel et al. did not perform histology on the 
Ambystoma subjects because they did not die, so it was undetermined if 
the individuals harbored encysted zoospores.
    Since the 2016 interim rule, initial or additional testing has been 
done on Ambystoma spp. (Fitzpatrick et al. 2018; Sabino-Pinto et al. 
2018; Barnhart et al. 2020; Gray et al. 2023); Aneides aeneus (Gray et 
al. 2023); Cryptobranchus (Gray et al. 2023); Desmognathus ocoee (Gray 
et al. 2023); Ensatina eschscholtzii (Gray et al. 2023); Eurycea 
lucifuga and E. wilderae (Carter et al. 2020), E. wilderae (DiRenzo et 
al. 2021), and E. bislineata, E. lucifuga and E. wilderae (Gray et al. 
2023); Pseudobranchus striatus (Gray et al. 2023); and Pseudotriton 
ruber (Carter et al. 2020) that provides support for carrier status of 
these native genera. There is no conclusive countervailing evidence. 
Five more native species were found to be lethally affected by Bsal 
(Eurycea bislineata, E. wilderae, Pseudotriton ruber, Ensatina 
eschscholtzii, Aneides aeneus). Gray et al. (2023) tested only native 
North American species specifically to access the conservation risk to 
U.S. species.
    Based on the gradient responses from resisting infection to lethal 
response among the genera Martel et al. (2014) and others tested 
experimentally, other genera could be at risk from Bsal infection or 
could serve as carriers. However, we are not listing species in those 
genera because the genera had not yet been tested or confirmed as 
carriers by the drafting of this second interim rule.
    Controlled Bsal experiments have proliferated since the discovery 
of the fungus. A study by Kumar et al. (2020) shows variation in 
experimental methodologies could thwart knowledge advancement by 
introducing confounding factors that make comparisons difficult among 
studies. They tested whether passage duration of Bsal culture (the 
number of times the fungus was transferred from its culture into fresh 
culture media), exposure method of the host to Bsal (water bath versus 
skin inoculation), Bsal culturing method (liquid versus plated), host 
husbandry conditions (aquatic versus terrestrial), and skin-swabbing 
frequency influenced diseased-induced mortality in a susceptible host 
species, the eastern newt. They found that disease-induced mortality 
was faster for eastern newts when exposed to a low passage isolate (a 
``young'' Bsal isolate that had been passed into fresh culture media 
only 20 times), when newts were housed in terrestrial environments, and 
if exposure to zoospores occurred in a water bath. They did not detect 
differences in disease-induced mortality between culturing methods or 
swabbing frequencies. Their results illustrate the need to standardize 
methods among Bsal experiments, but they do not discount the results of 
the studies used to determine our results.
Vulnerability and Carrier Status of Threatened and Endangered Species
    As of the drafting of this interim rule, 20 native species of 
salamanders in 6 genera are threatened or endangered under the ESA. As 
of the drafting of the 2016 interim rule, none of the salamander 
species listed as endangered or threatened under the ESA in the United 
States had been specifically

[[Page 2209]]

tested for Bsal vulnerability under laboratory conditions. Bsal had not 
been detected in their wild populations (Martel et al. 2014, Bales et 
al. 2015). Since publication of the 2016 interim rule, several species 
have been laboratory-tested.
    One species with two federally endangered subspecies (eastern 
hellbender Cryptobranchus a. alleghaniensis and Ozark hellbender C. a. 
bishopi) has been laboratory tested and is considered a carrier in the 
second interim rule in this document (Gray et al. 2023). Notably, 
Cryptobranchus has only one species in the genus, so if the species is 
extirpated by Bsal, so is the genus.
    As we describe above in Vulnerability and Carrier Status, while the 
Service did find evidence that shows some species within a genus may 
vary in their specific vulnerability, the carrier status of tested 
species can be extrapolated to related species, including those that 
are listed as endangered or threatened, candidates for ESA listing, and 
under review.
    Of the other new genera that include native species that we have 
identified as carriers, the following 12 species are federally listed 
as endangered or threatened: 5 species of Ambystoma (California tiger 
salamander (A. californiense), frosted flatwoods salamander (A. 
cingulatum), reticulated flatwoods salamander (A. bishopi), Sonoran 
tiger salamander (A. mavortium stebbinsi), Santa Cruz long-toed 
salamander (A. macrodactylum)); and 7 species of Eurycea (Austin blind 
salamander (E. waterlooensis), Barton Springs salamander (E. sosorum), 
Georgetown salamander (E. naufragia), Jollyville Plateau salamander (E. 
tonkawae), Salado salamander (E. chisholmensis), San Marcos salamander 
(E. nana), and Texas blind salamander (E. rathbuni)). Notably, 
Ambystoma is the only genus in the family Ambystomatidae, so if the 
genus is extirpated by Bsal, so is the family.
    No information is available regarding the effect of Bsal or carrier 
status of the remaining four ESA-listed species native to the United 
States: the desert slender salamander (Batrachoseps aridus), the 
Alabama waterdog or black warrior waterdog (Necturus alabamensis), 
Neuse River waterdog (N. lewisi), and Red Hills salamander 
(Phaeognathus hubrichti). Three Plethodon species from the 2016 interim 
rule are federally listed as endangered or threatened: Shenandoah 
salamander (P. shenandoah), Cheat Mountain salamander (P. nettingi), 
and Jemez Mountains salamander (P. neomexicanus) (USFWS 2023). There 
were no candidate species of salamanders as of the drafting of this 
second interim rule. Three Plethodon species identified as carriers in 
the 2016 interim rule remained federally listed.

G. Factors That Contribute to Injuriousness of Salamanders

Likelihood of Release or Escape (of Salamanders)
    In general, there is widespread concern over the increasing spread 
of pathogens moved through the wildlife trade (for example, Chinchio et 
al. 2020; IPBES 2020). Substantial evidence shows that Bd has spread 
extensively throughout the world through the amphibian trade (Fisher 
and Garner 2007; Schloegel et al. 2009; Schloegel et al. 2012; Galindo-
Bustos 2014; Kolby 2014; Kolby et al. 2014). Similar mechanisms of 
transmission and persistence in the closely related Bsal pathogen, 
along with detection of Bsal in captive salamanders imported by the pet 
trade into Great Britain, indicate that global movement of Bsal, 
similar to that of Bd, is not only possible but is already occurring 
(Cunningham 2015). Bsal was also found in a private pet collection in 
Germany, where it killed over half of a collection of approximately 200 
salamanders in the genus Salamandra (Sabino-Pinto et al. 2015). 
Although the origin of Bsal in the German collection was unknown, it is 
probable that Bsal is also present in other private or professional 
collections across Germany and possibly also in other European 
countries (Sabino-Pinto et al. 2015). Amphibian trade fairs in Spain, 
where the largest fairs in southern Europe take place, as well as in 
private collections in Spain, had positive test results for Bd and 
Ranavirus (Thumsov[aacute] et al. 2021) and are known to house and co-
house sick amphibians. These collections may serve as a reservoir of 
Bsal within the wildlife trade or as sources of Bsal release into the 
environment.
    Considering the occurrence of Bsal in the global pet trade, the 
risk to North American native species, and the number of salamanders 
that are imported into and transported throughout the United States 
through trade, Bsal is likely to be introduced into and spread 
throughout native salamander populations in the United States unless 
immediate action is taken to limit the importation of salamanders that 
are likely to carry Bsal. The 2016 interim rule has limited 
importation, and this second interim rule is intended to further reduce 
risk.
    Infected salamanders can transmit Bsal to other species even if the 
introduced salamander fails to establish a population. Evidence 
indicates that at least some of the salamanders capable of carrying 
Bsal can escape or be released and introduce Bsal into the environment. 
As described earlier, evidence exists for release of salamanders into 
the wild in the United States (Picco and Collins 2008; USGS 2015a, b, 
c, d, e, f). As noted above in Invasiveness of Salamanders, the USGS's 
Nonindigenous Aquatic Species database (USGS 2023) has records for 17 
salamander species that have been observed in the environment outside 
their native range. Of those, 14 are native to the United States and 
were discovered outside of their native ranges, and 3 are species not 
native to the United States. These findings mean that salamanders have 
been shown to exist, even if temporarily, outside their native range in 
the environment. Thus, they are capable of transmitting Bsal into 
nonindigenous ecosystems. Infected native species that are imported and 
escape or are released into native habitats would also be capable of 
carrying Bsal into native salamander ecosystems where Bsal has not 
previously been found.
    Infectious Bsal zoospores can also be released into the environment 
if water or other materials used to house infected salamanders enter 
the environment due to improper disinfection and disposal methods. The 
water and materials become passive carriers to introduce the fungus 
into the environment if not decontaminated or disposed of properly. As 
described above under Environmental Conditions Needed To Survive, Bsal 
can survive in filtered pond water for at least 31 days (Stegen et al. 
2017). Bd is similarly known to remain viable for weeks in water and 
moist organic matter and is capable of being transmitted to uninfected 
specimens through such means. Given our assumption that Bd can serve as 
a surrogate for predicting Bsal's effects in salamanders at the 
population level, and since Bd does not require an amphibian host to 
remain viable, we expect that Bsal can also persist outside salamanders 
(as long as it has sufficient water or moist soil and conducive 
temperature). Since the effects of desiccation or the viability of 
encysted Bsal spores in deceased hosts have not been thoroughly 
investigated, we also expect that Bsal can be transmitted on 
unpreserved dead salamanders or body parts and tissues.
    As discussed above in Introduction Pathways, there is evidence that 
Bd has escaped into the environment through untreated wastewater, 
increasing the likelihood that Bsal could also escape if brought in via 
contaminated water or

[[Page 2210]]

improperly disposed of materials. While standards for the treatment and 
prevention of Bd exist, in part due to recognition of its status as an 
internationally notifiable disease under the World Organisation for 
Animal Health (WOAH), the effectiveness and widespread application of 
those standards are uncertain given that international protocols for 
responding to Bd do not exist and the need to improve international 
mechanisms to respond to disease-related threats to biodiversity 
(Voyles et al. 2014).
    Given the number of specimens that have been imported into the 
United States and Canada, it is not known why Bsal has not yet been 
found in these countries (Muletz et al. 2014; Bales et al. 2015; 
Stephen et al. 2015; Richgels et al. 2016). A comparison of Bd, which 
has spread in the United States, to Bsal yields some insights. Based on 
genetic analyses and examination of historical specimens, Bd may have 
originated from different places, including Japan, South Africa, or 
South America (Farrer et al. 2011; Rodriguez et al. 2014). In contrast, 
Bsal may have originated only from Asia, giving it fewer pathways to 
the United States (Martel et al. 2014; Laking et al. 2017). Importation 
of salamanders into the United States has also declined in recent 
years, suggesting that the propagule pressure may also be a factor by 
limiting the number of times in which Bsal could possibly be introduced 
into the environment through trade (Lockwood et al. 2005; USFWS OLE 
2015). Bd may have spread more quickly than Bsal because of its ability 
to infect frogs, whereas research so far has found only a few frog 
species that may carry Bsal (see Impacts on Wildlife Resources or 
Ecosystems below). Based on LEMIS data, frogs are traded in higher 
volumes than salamanders, increasing the probability of trade of a Bd-
infected individual over a Bsal-infected individual. The USGS 
Nonindigenous Aquatic Species database also provides evidence for this 
higher level of trade, in that greater numbers of frogs are reported 
than salamanders. In addition, many frogs in trade, such as Rana 
catesbeiana (bullfrogs), are adaptable to a wide variety of 
environments and can easily become invasive once released in a 
watershed, as bullfrogs have become in the American West (Jennings and 
Hayes 1994; Rosen and Schwalbe 1995; Funk et al. 2011; Sepulveda et al. 
2015).
    Taken together with the other data we reviewed, this evidence 
suggests that Bsal is less likely to enter the United States than Bd. 
However, without action, the pathways for introduction and escape of 
Bsal are a significant and imminent threat. Listing salamanders that 
can carry Bsal as injurious wildlife to prohibit their importation 
targets those pathways, thereby minimizing opportunities for Bsal to be 
introduced, become established, and spread in the United States.
Potential To Survive, Become Established, and Spread
    Even if a salamander species does not become established, there is 
evidence that it may be capable of carrying Bsal long enough in the 
wild to transmit Bsal. The USGS Nonindigenous Aquatic Species database 
has records of 17 species and populations that have been observed in 
the United States outside of their native range (USGS 2023). Of those, 
14 are native and have established populations in the United States 
outside of their native U.S. range: Eastern tiger salamander (Ambystoma 
tigrinum), northwestern salamander (A. gracile), blotched tiger 
salamander (Ambystoma mavortium melanostictum), long-toed salamander 
(Ambystoma macrodactylum), three-toed amphiuma (Amphiuma tridactylum), 
California slender salamander (Batrachoseps attenuatus), seal 
salamander (Desmognathus monticola), Santeetlah dusky salamander 
(Desmognathus santeetlah), black-bellied salamander (Desmognathus 
quadramaculatus), mudpuppy, eastern newt, red-spotted newt 
(Notophthalmus viridescens viridescens), large-blotched ensatina 
(Ensatina eschscholtzii klauberi), lesser siren (Siren intermedia), and 
rough-skinned newt (Taricha granulosa). The three species from outside 
the United States are the Japanese fire-bellied newt (Cynops 
pyrrhogaster), Oriental fire-bellied newt (Cynops orientalis), and 
paddle-tailed newt (Paramesotriton (Pachytriton) labiatus), none of 
which are known to have become established. No foreign terrestrial 
salamander species have been detected in USGS surveillance for Bsal (M. 
Adams, USGS, pers. comm. 2021). As discussed earlier under Introduction 
Pathways and Environmental Conditions Needed To Survive, Bsal is 
expected to be able to survive outside of salamander hosts for several 
weeks given suitable conditions in water. If a salamander comes in 
contact with Bsal and then transmits it during a time when salamanders 
congregate, such as during breeding as described above under Salamander 
Biology, the potential for Bsal to survive, establish, and spread 
through animals or animal parts (except for purified, extracted genetic 
material, eggs, and gametes) is significant. As we describe above under 
How the Fungus Affects Salamanders, Bsal can be transmitted on 
unpreserved dead tissue where keratin is present, particularly skin, 
but we do not find that Bsal can be transmitted through reproductive 
tissue, including eggs and gametes. There is no evidence to suggest 
that Bsal can survive in purified, extracted genetic material from 
salamanders; in chemically preserved specimens, tissues, samples, or 
swabs; or in salamander eggs and gametes; hence, these parts are not 
covered by the listing.
    As Richgels et al. (2016) noted, ``Given the large number of 
suspected Bsal carriers imported into the USA each year (Cynops spp. 
and Paramesotriton spp., more than 100,000 [per year]), Bsal is likely 
to be introduced if no additional risk mitigation steps are taken. 
Though precise estimates for the invasion process (proportion of 
imported individuals infected, frequency of release of captive 
individuals, and contact of released animals with native amphibians) do 
not exist for Bsal, the establishment of invasive amphibians common in 
US amphibian trade * * * and the patterns of global Bd spread * * * 
suggest these processes are also likely for Bsal.'' The Service finds 
that the capacity of infected salamanders in trade to potentially 
infect wild salamanders, together with the capacity of Bsal to survive 
for an extended period independent of an amphibian host, suggests that 
Bsal has a high likelihood of surviving, becoming established, and 
spreading once it is introduced into a new area.
    As we noted above in Purpose of Listing as Injurious, even if a 
salamander found to be injurious could not establish a population in 
the wild, an infected or carrier salamander from captivity can still 
transmit Bsal to native populations if that salamander escapes or if 
material touching it is improperly disposed.
Impacts on Wildlife Resources or Ecosystems
    If Bsal is introduced into the United States, we expect the species 
with lethal vulnerability would be at greatest risk. However, disease 
outbreaks can result from a combination of biotic and abiotic factors, 
including species vulnerability, exposure, host behavior, host 
immunity, co-infections, and environmental conditions (Wobeser 2007). 
Therefore, the vulnerability of individuals under laboratory conditions 
is an incomplete predictor of disease effects (Wobeser 2007). Native 
salamander species known to be tolerant of Bsal infection under 
experimental conditions may

[[Page 2211]]

demonstrate more severe clinical disease when infection is combined 
with additional stressors in the wild, as has been found for other 
diseases, including those in amphibians (Wobeser 2007; Kerby et al. 
2011; Kiesecker 2011). For example, Bodinof et al. (2011) noted that Bd 
may be found more frequently in hellbenders that are immunocompromised 
or that Bd infection increases the adverse effects of other co-
infections. Considering these cumulative factors, as well as the lack 
of testing for the majority of native salamander species, our 
assessment of risk in native species is likely conservative.
    Bsal can severely affect wildlife resources. At least nine native 
species are lethally vulnerable to Bsal, and at least one is tolerant 
to Bsal infection. At least 164 native species may act as carriers or 
sources of infection for other species. While not all species have been 
tested for their response to Bsal, based on the high rates of infection 
that have been observed, the fungus may have significant negative 
effects on additional species.
    As described above in Ecosystem-Level Effects, salamanders are 
important parts of the ecosystems in which they occur. They are often 
the most abundant vertebrates in their ecosystems, and, as a vital part 
of the food web, they are both important prey for and predators of many 
species (Holomuzki et al. 1994; Regester et al. 2006). In some places, 
they are considered keystone species that help control some 
invertebrate populations and affect cycling of nutrients in an 
ecosystem, contributing significantly to overall ecosystem health. For 
example, by consuming arthropods that would otherwise release carbon 
dioxide into the atmosphere by decomposing leaf litter in forests, 
salamanders slow carbon emissions from leaf litter decomposition, which 
has implications for the global carbon cycle (Best and Welsh 2014). As 
described earlier, invertebrate species that depend on salamanders for 
aspects of their life cycle or ecology are likely to be adversely 
affected if their host species declines in response to a Bsal 
introduction. Loss of these keystone species would result in 
significant ecosystem-level change.
    Salamanders constitute much of the vertebrate biomass of forests, 
and they play an important role in ecosystems as insect consumers, 
shapers of the landscape, and climate mediators (Burton and Likens 
1975; Davic and Welsh 2004; Wyman 1998; Best and Welsh 2014). If native 
U.S. salamander species do experience declines from Bsal infection as 
the fire salamander experienced in the Netherlands (Spitzen-van der 
Sluijs et al. 2013), we expect detrimental ecological effects. Nine 
native salamanders are documented as lethally vulnerable.
    The eastern newt, one of the lethally vulnerable species (Martel et 
al. 2014; Gray et al. 2023), is one of the most widespread salamander 
species in North America (Roe and Grayson 2008, Martel et al. 2014). As 
top predators in pond ecosystems, eastern newts regulate frog tadpole 
abundance and, therefore, affect the amount and type of nutrients 
available in the ponds, keeping them in ecological balance (Morin et 
al. 1983; Morin 1995). If eastern newt populations decline because of 
Bsal infection in the wild, imbalances could result in ponds and 
ecosystems throughout the Eastern United States. Eastern newts also 
travel long distances between aquatic and terrestrial habitats (Roe and 
Grayson 2008), so if the species was to be eliminated from an area, the 
amount of nutrients available in upland areas would also be affected.
    The rough-skinned newt is another native U.S. species known to be 
lethally vulnerable to Bsal (Martel et al. 2014; Gray et al. 2023) and 
is geographically widespread along the Pacific coast of North America 
from Santa Cruz, California, to southeastern Alaska (AmphibiaWeb 
2023a). The rough-skinned newt plays an important role in ecosystems 
through its consumption of invertebrates that break down leaf litter 
and release carbon into the atmosphere (Davic and Welsh 2004). If 
rough-skinned newt populations do experience severe declines from Bsal 
infection, atmospheric inputs of carbon may be altered, as has been 
observed with other species (Wyman 1998; Best and Welsh 2014).
    The green salamander (Aneides aeneus) was found by challenge tests 
to be lethally vulnerable when all 10 salamanders in the study became 
infected and 5 died as a result (Gray et al. 2023). This species is 
State-listed as endangered in Indiana, Ohio, Maryland, and Mississippi 
and threatened in Pennsylvania (AmphibiaWeb 2023a); it is found in a 
narrow range from southwestern Pennsylvania southwest to Alabama. Of 15 
Blue Ridge two-lined salamanders (Eurycea wilderae) that were 
challenge-tested, all became infected and 10 of those died (Gray et al. 
2023; see also mortality in Carter et al. 2020; DiRenzo et al. 2021), 
and 6 of 9 infected northern two-lined salamanders (of 9 Eurycea 
bislineata challenged; Gray et al. 2023). Red salamanders (Pseudotriton 
ruber), widely found from New York State to Alabama and Florida, had 
100 percent mortality (Carter et al. 2019; Gray et al. 2023). The 
Ensatina salamander (Ensatina eschscholtzii) is the only species in its 
genus, although it has seven subspecies, all found on the West Coast; 
two subspecies were documented as having lethal results (Gray et al. 
2023).
    Other taxa besides salamanders may also be negatively affected by 
Bsal. Several species of anurans have been found to carry Bsal (midwife 
toad Alytes obstetricans, Stegen et al. 2017; fire-bellied toad Bombina 
microdeladigitora, Nguyen et al. 2017; Cuban treefrog Osteopilus 
septentrionalis, Towe et al. 2021; Gray et al. 2023). However, little 
is known about the negative effects of the disease on the anurans. None 
of these species is native to the United States, but all are imported 
in trade. Therefore, there is a risk of spreading Bsal to native frogs 
and toads, the susceptibility of which we do not know, and also a risk 
of spreading to salamanders. As explained above, we are not adding any 
frogs or toads to the list of injurious wildlife because they are in a 
different order (Anura), and we did not include the possibility of 
adding the order Anura in the 2016 interim rule, which would give the 
public a chance to comment.
    As Richgels et al. (2016) noted, some parts of the United States 
may reach temperatures above the thermal range of Bsal on a seasonal 
basis. However, wildlife and habitats would suffer losses if local 
populations of salamanders affected by Bsal prior to temperatures 
rising as part of the regular seasonal cycle suffered declines (and 
possible extirpation) and were unable to return to pre-infection levels 
in those ecosystems.
    Gray et al. (2023) estimated mean infectious and lethal doses for 
the North American species they tested with sufficient infection and 
mortality data and derived an amplification potential. Species with 
high amplification potential may contribute disproportionately to 
transmission events because they are easy to infect, less likely to die 
quickly from infection, and likely to be more infectious due to greater 
pathogen loads on their skin. Species that were susceptible to 
infection but did not die from Bsal are likely to be carriers. 
Considering all the variables, there is an immense potential for 
amphibian communities in North America to harbor carrier species that 
serve as reservoirs, amplification species that disproportionally 
transmit Bsal, and Bsal-susceptible species that are at high risk of 
population decline and extirpation.

[[Page 2212]]

    For the above reasons, we conclude that the negative impact to 
wildlife resources or ecosystems is expected to be high if Bsal is 
introduced into U.S. ecosystems.
Impacts to Threatened and Endangered Species and Their Habitats
    As of publication of the 2016 interim rule, none of the salamander 
species listed as endangered or threatened under the ESA in the United 
States had been specifically tested for Bsal vulnerability under 
laboratory conditions; Bsal had not been detected in their wild 
populations (Martel et al. 2014, Bales et al. 2015). As of the final 
rule to the 2016 interim rule in this document, only the eastern 
hellbender (of which two subspecies are federally endangered) has been 
tested (Gray et al. 2023) and is considered a carrier. Of the genera 
that include native species that we have identified as carriers, 20 
salamander species are federally listed as threatened or endangered and 
2 salamanders are candidates or proposed for listing. Because not all 
species have been tested, it is possible that the fungus will 
negatively affect other ESA-protected species.
Impacts to Human Beings, Forestry, Horticulture, and Agriculture
    We do not expect direct effects to forestry, horticulture, or 
agriculture. Trees and other plants are also not affected. Bsal does 
not appear to infect humans or other animals except for salamanders and 
a few anurans. Indirectly, the introduction or establishment of Bsal 
would have negative effects on humans primarily from the loss of native 
wildlife biodiversity. These losses would affect the aesthetic, 
recreational, and economic values currently provided by native wildlife 
and healthy ecosystems. However, other indirect links to human health 
may occur. Many salamander species prey on mosquito larvae, and if the 
salamander numbers decline (such as from Bsal), the population of 
mosquitoes is likely to increase. Insect repellants used in surface 
waters for mosquito control have been linked to salamander larvae 
mortality and deformities, thus reducing predation on mosquito larvae, 
also leading to increased numbers of mosquitoes (Almeida et al. 2018). 
Similarly, a correlation has been made for Bd causing declines of 
mosquito-eating frogs, which then led to increased numbers of malaria-
carrying mosquitoes (Springborn et al. 2022). Educational values would 
also be diminished through the loss of biodiversity and ecosystem 
health. However, we are not listing the species because of the indirect 
impacts to humans, forestry, horticulture, or agriculture, but rather 
due to their impacts to wildlife and wildlife resources.
Wildlife or Habitat Damages That May Occur From Control Measures
    Richgels et al. (2016) stated, ``[T]here are few known viable 
treatment or management options for responding to the introduction of 
Bsal * * * Strategies focused on prevention or reduction of 
introduction events remain the best control option for emerging 
diseases.'' As discussed below in Ability To Prevent or Control the 
Spread of Pathogens or Parasites, current control strategies appear to 
focus on treating salamanders in a controlled laboratory setting. We 
are not aware of control measures that are effective in treating 
infected free-ranging salamanders over a large-scale area that could 
eliminate Bsal without killing the salamanders themselves, have low 
side effects, or do not require significant resources to implement. In 
addition, the life history of salamanders makes it highly unlikely that 
all individuals, including those that are infected, could be captured 
and treated. Many species are long-lived and inhabit areas that may be 
hard to reach. Furthermore, the effects on other wildlife of chemically 
treating an area, if such a treatment becomes available to eradicate 
infected salamanders and if capturing and treating individually is not 
practical, is unknown but is likely to be severe.

H. Measures That Reduce or Remove Injuriousness of Salamanders

Ability To Prevent Escape and Establishment
    As discussed below in Ability To Prevent or Control the Spread of 
Pathogens or Parasites, the ability and effectiveness of measures to 
prevent or control Bsal is currently low. While less certain, we also 
expect the ability to prevent escape and establishment is also low. 
Nonregulatory actions, such as implementing voluntary Best Management 
Practices or individual State action, are possible. The Service, for 
example, is working with partners on such efforts as Habitattitude\TM\, 
a national campaign that encourages responsible consumer actions with 
respect to pet ownership. Such actions include finding alternatives to 
releasing pets into the environment. In November 2015, PIJAC (currently 
known as the Pet Advocacy Network) asked its member entities to 
voluntarily ban their importation of paddle-tailed newts and Oriental 
fire-bellied newts to prevent the unintentional introduction of Bsal 
(PIJAC 2015). Voluntary actions, such as applying heat and antifungal 
medication therapy as described in Blooi et al. (2015a) and Blooi et 
al. (2015b), may help reduce the threat posed by Bsal for specimens 
held in captivity. However, at this time it is not possible to 
determine the likelihood of success of such measures in preventing the 
introduction, establishment, and spread of Bsal in the United States.
    As described above under Invasiveness of Salamanders and General 
Information About Bsal, nonnative salamanders have escaped into the 
United States, and Bd, a related fungus, has also escaped and 
established in the United States. While treatment options exist that 
may help reduce the threat posed by Bsal for imported and captive-held 
specimens, those options have not been standardized and their 
effectiveness remains uncertain for large-scale regulatory purposes. 
Treatment options for free-ranging specimens are not practical at this 
time. Therefore, we expect the likelihood of the ability to prevent 
escape and establishment of Bsal through infected salamanders to be 
low. Although voluntary actions are vital to help minimize the threat 
of invasive species, the Service is highly concerned about the 
extensive damage that introduction of Bsal would do to our Nation's 
natural resources. Thus, we concluded that we cannot rely on voluntary 
actions alone to address the severity of the threat that Bsal poses and 
that other measures to prevent escape and establishment are not 
sufficient to ensure Bsal is not successfully introduced.
    Therefore, we find that we cannot rely on these approaches to 
prevent escape and establishment of Bsal and that our current capacity 
to prevent escape and establishment is low.
Potential To Eradicate or Manage Established Populations
    While some introduced salamanders in the United States have been 
successfully controlled, such as the lesser siren (which was eliminated 
from a backyard pond outside its native U.S. range), others, such as 
the three-toed amphiuma, have not been as successfully controlled. 
However, evidence for control is sparse. Given the high rates of 
infection among salamanders tested by Martel et al. (2014), and the 
lack of control measures for Bsal that could be employed outside of a 
controlled facility, it is likely that Bsal would persist once 
introduced into the environment given appropriate environmental 
conditions, especially if

[[Page 2213]]

a tolerant or susceptible salamander established a population and 
continued to spread Bsal.
Ability To Rehabilitate Disturbed Ecosystems
    Bsal infection can lead to the loss of keystone species in the 
ecosystem. The ability to rehabilitate disturbed ecosystems is expected 
to be low. We considered whether the Service's National Fish Hatchery 
System (NFHS) could be used to maintain salamanders in refugia while 
areas are treated, assuming the salamanders could be treated for the 
fungus. However, it is impractical to equip NFHS facilities to be able 
to rapidly protect numerous salamander populations and maintain them 
for an extended time, such as might be required due to the introduction 
of Bsal. Although, as described in the next section, a few options 
exist to treat individual salamanders, none have been identified that 
can be used to clear Bsal from a widespread area. Consequently, we 
expect that, once Bsal has been introduced, it will persist and spread 
with little opportunity for widespread disinfection of ecosystems.
    Studies have also questioned the effectiveness of captive-breeding 
programs to address such threats as infectious disease to amphibians, 
including salamanders (Harding et al. 2015). However, a recent study 
showed enhanced resistance following a second exposure of Bsal in 
eastern newts, both for increased survival and decreased Bsal loads by 
QPCR (L. Rollins-Smith, Vanderbilt University, pers. comm. 2021). Also, 
another study found a second higher Bsal dose led to decreases in Bsal 
infection intensity over time as compared to salamanders exposed only 
once to a lower dose that sustained infections over time (DiRenzo et 
al. 2021). Since that study was not designed specifically to study the 
effects of immune priming, these results are indicative but not proven. 
Therefore, it may be possible to stimulate an immune response in 
captive salamander populations that would allow them to be reintroduced 
into ecosystems where Bsal may still exist; however, this response has 
not been demonstrated for Bd, and research is needed in a broader array 
of conditions and species and to determine how resistance or immunity 
works.
    Therefore, the ability to rehabilitate disturbed ecosystems is 
expected to be low because the Service would be unable to ensure that 
all salamander populations expected to be affected by Bsal could be 
treated and protected in the wild.
Ability To Prevent or Control the Spread of Pathogens or Parasites
    The ability and effectiveness of nonregulatory measures to prevent 
or control Bsal on a widespread scale from live specimens is currently 
low. The risk is compounded beyond the effect of a more common type of 
injurious listing (where the species cause harm by being invasive) by 
having two separate variables that can each spread--the fungus and the 
host species (salamanders). Few options can ensure potentially infected 
salamanders do not carry Bsal, and none exist on a broad scale.
    Blooi et al. (2015a) has shown that treating salamanders infected 
with Bsal by exposing them ``to 25 [deg]C [77 [deg]F] for 10 days 
resulted in complete clearance of infection and clinically cured all 
experimentally infected animals. This treatment protocol was validated 
in naturally infected wild fire salamanders.'' The authors found that 
temperature treatment could be an effective option given the host 
salamander's thermal tolerance. However, the treatment does have some 
shortcomings. Not all salamander species can tolerate the thermal 
regime required, and the researchers noted that there is a ``narrow 
margin between the temperature able to limit [Bsal] and the upper 
thermal limit most urodelans tolerate.'' Blooi et al. (2015a) also 
noted that there is some uncertainty as to whether the method is 
completely effective. Evidence of Bsal was found after thermal 
treatment, although it is possible that the evidence consisted of dead 
cells only. While thermal treatment is promising, the paper's 
introduction noted that it was intended to ``help to develop treatment 
protocols'' and, therefore, is not intended to serve as the standalone 
standard treatment. As the treatment has not been standardized as a 
protocol for use at the landscape scale for salamanders in the wild or 
throughout trade, its ability to prevent introduction or control the 
spread of Bsal is low or uncertain.
    In the 2016 interim rule and corresponding economic analysis, one 
of the five alternatives that we considered was requiring a health 
certificate upon import stating that the animal being moved is free of 
Bsal, in lieu of or in addition to listing. During our evaluation for 
the 2016 interim rule, we considered whether it was practical for an 
exporting foreign nation to provide a health certificate stating that a 
possible carrier of Bsal has been tested and found to be free of the 
fungus or treated with antifungal drugs and thermal procedures to 
ensure that any Bsal that the salamanders might be carrying has been 
killed. We acknowledged that these testing and treatment methods 
existed and may be effective under certain circumstances. Requiring a 
health certificate would help ensure that Bsal does not escape from an 
exporting nation by being carried on an infected salamander. However, 
considering information from the public comments and other more recent 
information, we have significant concerns about this requirement's 
feasibility for large-scale regulatory use for exporting countries 
given the effectiveness and sensitivity of current testing methods 
(including the return of false negatives), lack of validation and 
sufficient testing capacity, lack of standardized treatment methods, 
and agency resources required to conduct inspections, interpret 
results, and issue health certificates. The cost of testing could also 
be prohibitive for some exporters, since the cost of testing may be per 
animal. In the United States, qPCR testing can run around $25 to $65 
per salamander, and the salamander may wholesale for only $5.
    In May 2017, the WOAH listed infection with Bsal as an emerging 
disease in its Aquatic Animal Health Code; now WOAH considers Bsal as a 
disease of amphibians, with a chapter in the Aquatic Animal Health Code 
(WOAH 2021a) and a chapter in the manual (WOAH 2021b). The WOAH is the 
intergovernmental organization responsible for improving animal health 
worldwide. The WOAH chapter on Bsal provides recommendations that ``may 
include'' 13 named species of Asian, European, and North American newts 
and salamanders (WOAH 2021b); those species were a portion of the 
species covered by our 2016 interim rule. The recommendations include 
that the consignment be accompanied by an international aquatic animal 
health certificate issued by the Competent Authority of the exporting 
country.
    That recommendation came after the 2016 interim rule took effect. 
The 2016 draft economic analysis did not explain the costs of health 
certification because it was unclear how much testing, treatment, and 
the health-certification processes would cost. Because the details for 
these recommendations were not available for regulatory consideration 
for the 2016 interim rule's public and peer comments and because much 
of those details are still not clear, we are not adding a health 
certification to this second interim rule. However, we believe there 
are valuable recommendations in the WOAH chapter 8.2 (WOAH 2021a) that 
we support for the public to voluntarily help prevent or

[[Page 2214]]

control the spread of Bsal. They include, but are not limited to 
(summarized from WOAH 2021a; details found there):
     quarantine;
     treating or disposing of shipment water, equipment, 
containers, and packaging in a biosecure manner; and
     treating effluent and waste materials (fomites) to 
inactivate Bsal.
    The European Union, Switzerland, and United Kingdom have each 
implemented Bsal-specific health-certification requirements, and their 
regulations are similar to each other's. Imports to these countries are 
prohibited unless they are from WOAH member countries and accompanied 
by a health certificate. The European Union's implementing decision 
lays out testing and quarantine protocols along with providing a model 
health certificate. The United Kingdom costs for Bsal quarantining 
starts at [pound]250 ($340) per consignment monitored and [pound]40 
($54) for testing where required, and these could be untenable for most 
importers. Although some countries may have the necessary expertise to 
certify that salamanders are free of Bsal, not all exporting nations 
may have the necessary skills or resources, nor do we know which ones 
do. At some point in the future we may be able to propose health-
certification criteria that are reliable and tenable, with the costs 
borne by the trade.
    Scientists and diagnostic laboratories are also working to 
standardize laboratory protocols, but there are currently no 
standardized sampling, testing, and screening protocols in the United 
States, and we do not know the standards, if any, in the various 
countries from which salamanders are currently being or may be 
exported. Assay sensitivity can vary between laboratories. A wide 
variety of laboratory equipment, reagents, techniques, protocols, and 
personnel experience is available, thus contributing to non-
standardized techniques that can lead to variable or inconsistent 
results. Each laboratory has different equipment and uses different 
reagents (L. Sprague, USFWS, pers. comm., 2021). The North American 
Bsal Task Force recommends corroborative assays or further testing to 
validate a positive PCR or qPCR result, although WOAH does not state 
this; they also recommend quarantining under various scenarios (North 
American Bsal Task Force 2022). Considering the lack of amphibian 
quarantine facilities at ports of import and the unknown standards of 
testing for certification, we conclude it is currently not sufficient 
to rely on methods similar to those of the European Union and United 
Kingdom for preventing the introduction and establishment of Bsal. We 
need more information on this, which we requested below in K. 
Information Requested in question (10).
    Some treatment options also exist, such as treatment with 
antifungal medications that can be applied on animals that do not 
tolerate 25 [deg]C (77 [deg]F) (A. Martel, University of Ghent, pers. 
comm. 2015; Blooi et al. 2015b). It may be possible to treat amphibians 
in the wild for Bd with antifungals by capturing individuals and 
soaking them in a bath of the chemical, then releasing them back into 
the environment. As Hardy et al. (2015) showed for Cascades frogs (Rana 
cascadae), this process does not seem to be as effective as desired 
given possible side effects, but it may delay the eventual outcome of 
an outbreak enough to help individuals persist in the population. 
However, this process left unanswered questions about its applicability 
for salamanders and whether reinfection from fomites could still occur. 
Blooi et al. (2015b) identified a method for treating infected fire 
salamanders for Bsal with a combination of antifungals and temperature 
control that successfully cleared the fungus. However, such treatment 
worked only for controlled settings, such as those found in a 
laboratory or conservation facility, and side effects are unknown.
    It is impractical to treat widespread areas in the natural 
environment given the likely cost, personnel, and time needed to locate 
and treat all salamanders in the wild. Additionally, without a 
standardized process it is impractical to set required protocols that 
would apply to all specimens in trade. The possibility also exists for 
unknown and unintended consequences from such large-scale treatments, 
such as possible side effects from the widespread use of antifungal 
drugs. While promising, the treatment has not been standardized for use 
in a widespread manner for any salamander species. As we have noted 
above under Environmental Conditions Needed To Survive, Bsal is likely 
capable of persisting in the environment without a host by transmission 
to infected materials. Even if all individuals of a population could be 
successfully treated, the threat of reintroduction from environmental 
contamination would still exist.
    Even without the capacity to treat animals, research has shown that 
it is possible to identify whether a salamander is infected with Bsal, 
which would allow animals to be screened prior to importation. Blooi et 
al. (2013) presented a method of sampling salamanders and testing them 
to determine whether they carry Bsal. However, if certification occurs 
prior to importation, the process would require trained technicians in 
the country of origin, specialized equipment, and certainty that the 
salamanders would not become infected following certification. The 
results of those tests must then be interpreted by qualified health 
professionals and documented through a health-certification process. We 
cannot rule out the possibility of false negative tests or falsified 
documentation that could allow Bsal to be introduced into the United 
States. Post-import health certification by the Service at ports of 
entry would require holding salamanders at least 1 day for processing, 
testing, and diagnosis. Quarantine facilities would be needed while 
samples are processed and the health of the salamanders is certified. 
In addition, wildlife inspectors at ports of entry would need to be 
trained in testing and diagnosis procedures.
    In comparison, the certification process for listed salmonid 
species is standardized and salmonids are easier to test. For example, 
the tests for regulated salmonids are non-molecular, validated, require 
pathogen culture, and are, therefore, more straightforward. There are 
also only 12 countries (Australia, Canada, Chile, Denmark, Finland, 
Iceland, Isle of Man, New Zealand, Northern Ireland, Norway, Scotland, 
and Wales) that have officials certified to sign health certificates to 
export salmonids (generally as eggs) to the United States. Generally, 
only a few countries export to the United States in a given year. For 
example, in 2019, the Service received requests to import salmonid eggs 
from Canada, Denmark, Finland, and Iceland. The Service concluded that 
there is currently insufficient certainty that a certification program 
utilizing the method described by Blooi et al. (2013) would be 
effective in preventing the introduction or spread of Bsal in the 
United States. However, we may consider a certification system in the 
future and have posed a question below for public comment.
    Given the expected severity of consequences of Bsal introduction, 
imported salamanders that could be carriers may need to be treated, 
even with a health-certification process, which is not practical at 
this time for implementation by the Service as a broad-scale regulatory 
tool. The studies that have been conducted have not been standardized 
or agreed to as a suitable diagnostic or treatment effort on a large 
scale for treating all of the specimens that would potentially be 
imported. Not all species will tolerate treatment, and

[[Page 2215]]

reliable diagnostic capacity is needed to verify that animals do not 
carry Bsal following treatment. If an outbreak occurs, it would not be 
practical to locate and treat all free-ranging individuals in the wild 
in U.S. ecosystems. While antifungal agents could be applied to all 
animals, either in the laboratory or perhaps applied over a large 
geographic area, we are concerned about side effects on the animals 
being treated or nontarget species. We are also concerned about 
possible negative environmental effects if a chemical was widely 
applied (Gyllenhammar et al. 2009; Hasselberg et al. 2008).
    Researchers are also looking into the composition of the skin 
microbiome of various salamander species to gauge if it is possible to 
determine natural resistance to Bsal. For example, Bletz et al. (2018) 
found that European fire salamanders maintain complex skin microbiotas 
that have some Bsal-inhibiting properties, but the bacterial numbers 
are too low to protect sufficiently against Bsal. Currently, we do not 
know if skin microbiota can be enhanced to inhibit Bsal sufficiently 
because of the complexities involved.
    In contrast to live specimens, salamanders that are chemically 
preserved with common scientific and museum collection protocols 
present no risk of introducing or transmitting Bsal. Tissue samples 
fixed in 10 percent formalin or embedded in paraffin (usually both in 
sequence) after routine histological processing (or both), including 
those from amphibians known to, or suspected of, carrying Bsal, contain 
only nonviable material and, thus, are not considered injurious (M. 
Forz[aacute]n, Bsal Task Force, pers. comm. 2021). In addition, 
experimental trials have demonstrated that Bsal is killed when exposed 
to 70 percent ethanol for at least 60 seconds (Van Rooij et al. 2017). 
Therefore, skin swabs preserved in 70 percent ethanol are not 
considered injurious and may be used for PCR testing since this 
chemical does not damage DNA quality. However, freezing a salamander as 
a way to kill Bsal spores is not a proven method to kill Bsal to our 
knowledge. For Bd, analysis of some sample results suggest that the 
freeze-shock treatment reduced the probability that Bd will grow, but 
all the Bd strains had at least a portion of samples that grew and 
produced zoospores following a freeze shock of -12 [deg]C (10.4 [deg]F) 
for 24 hours (Voyles et al. 2017). Since we know of no evidence that 
unpreserved dead salamanders, including species that may be frozen, are 
not capable of carrying Bsal, they are considered injurious.
    In conclusion, various methods for mitigating the spread of Bsal by 
salamanders have been studied. We reviewed studies on thermal 
treatments, health certifications, anti-fungal medications, and 
resistance by skin microbiota, and none individually or in combination 
are sufficiently effective, safe, and broadly applicable to negate the 
need to list salamanders as injurious.
Any Potential Ecological Benefits to Introduction
    No known benefits would result from Bsal or salamanders carrying 
Bsal occurring in the United States. The risks to native wildlife and 
wildlife resources greatly outweigh any unlikely benefits. Moreover, we 
are aware of no other potential ecological benefits for the 
introduction of Bsal or of Bsal-infected or Bsal-carrier salamanders 
into the United States.

I. Summary and Conclusion for Interim Rule

    Overall, there is a high risk to the wildlife and wildlife 
resources of the United States from salamanders that are capable of 
carrying Bsal. The United States harbors 221 species of salamanders, 
more than any other country. Of the 23 native genera, 13 genera were 
found to be vulnerable to or carriers of Bsal as of the drafting of 
this second interim rule. We find that the fungus is lethal to at least 
9 native salamander species in 6 genera and that 164 native species are 
considered carriers of Bsal. As of the drafting of this document, the 
vulnerability to disease and carrier status of 10 genera have not been 
tested or do not have conclusive results as carriers, many of which may 
have species vulnerable to this potentially deadly fungus. Under wild 
conditions, the disease may stress species to a point below the lethal 
threshold, and if these species are stressed by other factors, Bsal 
could cause cumulative harm to additional species. The benefits that 
these native salamander species provide to ecosystems, and in turn the 
ecosystem services that benefit people, are significant. The Service 
concludes that preventing Bsal from infecting native salamanders will 
prevent harmful effects to the wildlife and wildlife resources of the 
United States and merits listing of salamanders capable of carrying 
Bsal as injurious.
    Salamanders capable of carrying Bsal have the potential to escape 
and spread Bsal into the environment. Species capable of carrying Bsal 
can survive long enough in the wild to transmit the fungus or can 
transmit it to other carriers while in transit. Bsal can also be 
introduced and infect native salamanders by people improperly disposing 
of material that comes in contact with infected salamanders and can 
persist long enough in the environment without a host to represent a 
threat.
    Substantive evidence exists that all species within a genus where 
at least one species has been identified as a carrier of Bsal can also 
be a threat. Our review found no conclusive countervailing evidence. We 
find that, due to shared characteristics by species within a genus, 
other species within these genera are also highly likely to be carriers 
of Bsal, even if not every species in the genus has been tested to 
verify that it is a carrier of Bsal. For these same reasons, hybrids of 
species found in a genus that has at least one carrier species are also 
expected to be carriers.
    The main pathway for the global spread of Bsal is the international 
trade in salamanders. The most likely pathway of Bsal into the United 
States would be from salamanders being imported into the United States 
for commercial trade, including native species that are propagated 
outside the United States and subsequently imported into the United 
States. Listing salamanders that can carry Bsal as injurious wildlife 
will significantly confine this pathway and limit the capacity of Bsal 
to be introduced, become established, and spread in the United States.
    The current capacity to prevent escape and establishment is low. 
Rehabilitation of disturbed ecosystems is expected to be low, if not 
impossible. The ability and effectiveness of measures to prevent or 
control established Bsal is currently low. There are no known benefits 
of Bsal.
    The Service is listing live or dead specimens, hybrids, including 
parts, as injurious, but not eggs, gametes, preserved specimens or 
parts (including tissue), or purified extracted genetic material, where 
``preserved'' means the preservation techniques kill the pathogen and 
thereby prevent transmission of Bsal. We find the risk of transmission 
of Bsal to other salamanders is high from both live and unpreserved 
dead specimens. Any salamanders that are infected and lethally 
vulnerable may die in transport and continue to carry Bsal into the 
United States. The risk is also high from improper disposal of 
materials that might be contaminated by those live or unpreserved dead 
specimens. Dead specimens, including those that are or were frozen, are 
considered injurious. Although under the authority of 18

[[Page 2216]]

U.S.C. 42 we cannot list contaminated materials (fomites) as injurious, 
by listing the carriers of Bsal, we seek to prevent the introduction of 
those materials. Conversely, material that is not injurious includes 
purified extracted genetic material because it carries a low risk of 
infection by Bsal; however, other tissue samples, such as skin swabs, 
are listed unless they have been chemically preserved to deactivate any 
live Bsal. Swabs that are preserved by exposing to 70 percent ethanol 
for at least 60 seconds are not considered injurious. The Service is 
not listing specimens that are chemically preserved. We conclude the 
risk of infection from such specimens is low.
    The Service is not adding eggs or gametes to the listing because 
there is no evidence that Bsal affects salamander reproductive tissue, 
such as eggs or gametes. The Service is not listing genera that we 
concluded are not carriers of Bsal because we do not have direct 
evidence that they are capable of introducing Bsal to the United States 
or otherwise transmitting it to native populations. We are also not 
listing genera where there is no data, even though it is possible that 
untested genera may also be capable of carrying Bsal.
    For the reasons stated, the Service finds the 16 genera comprising 
approximately 164 species of salamanders to be injurious to the 
wildlife and wildlife resources of the United States. The potential for 
Bsal introduction into the United States is high, the United States has 
suitable conditions for Bsal survival, and the consequences of 
introduction into the United States are expected to be significant and 
occur across a wide range of the United States. By listing species that 
can carry Bsal, we are taking preemptive action to help ensure the 
fungus does not enter the United States and infect native salamander 
populations and cause severe individual mortality, population declines, 
and ecosystem and economic harm.

J. Required Determinations

Regulatory Planning and Review
    Executive Order 12866 (E.O. 12866), as reaffirmed by E.O. 13563 and 
E.O. 14094, provides that the Office of Information and Regulatory 
Affairs (OIRA) in the Office of Management and Budget (OMB) will review 
all significant rules. OIRA has determined that this rulemaking action 
is not significant.
    Executive Order 14094 reaffirms the principles of E.O. 12866 and 
E.O 13563 and states that regulatory analysis should facilitate agency 
efforts to develop regulations that serve the public interest, advance 
statutory objectives, and are consistent with E.O. 12866 and E.O. 
13563. Regulatory analysis, as practicable and appropriate, shall 
recognize distributive impacts and equity, to the extent permitted by 
law. E.O. 13563 emphasizes further that regulations must be based on 
the best available science and that the rulemaking process must allow 
for public participation and an open exchange of ideas. We have 
developed this rule in a manner consistent with these requirements.
    The economic analysis for the second interim rule is provided in 
this section of the preamble. We are presenting the alternatives 
considered to identify whether there is a more effective option that 
can achieve the desired goals of the rule. The Service considered three 
alternatives for the economic analysis: Alternative 1: No action; 
Alternative 2: listing all species in 16 genera in which there is at 
least one confirmed carrier and all species in the genus are likely to 
be a carrier; and Alternative 3: listing all salamanders. We eliminated 
two alternatives that were considered for the 2016 interim rule. One 
was ``listing species that were identified by Martel et al. (2014) and 
other scientific sources to be carriers of Bsal.'' This alternative was 
eliminated because new research provided evidence that this narrow 
approach could allow potential carriers to be imported. The other 
alternative was ``requiring a health certificate stating that the 
animal being moved is free of Bsal, in lieu of or in addition to 
listing.'' This alternative was eliminated because we do not have 
enough information to develop a reliable health certificate system at 
this time.
    To establish the baseline, analysis of current market conditions 
for imports and domestically bred salamanders is necessary. However, 
available U.S. salamander market data are minimal. The analysis uses 
two data sources to estimate the imported salamander industry: the 
Service's LEMIS (USFWS OLE 2021) for data on the number of imported 
salamanders (live, dead specimens, hybrids, or parts) and the data 
submitted during the comment period for the 2016 interim rule by the 
Pet Industry Joint Advisory Council (PIJAC 2016) on live salamander 
pricing (updated to 2021 dollars). Due to limited data availability, we 
cannot estimate domestically bred salamander sales that are transported 
between the enumerated jurisdictions. We expect impacts to domestically 
bred salamanders to be minimal because, as determined by the 2017 court 
decision discussed above in this document, none of the alternatives 
prohibit interstate transport between States within the continental 
United States. We are requesting public comment on the number and sales 
of salamanders (by species) that are domestically bred and the 
percentage that are transported between the enumerated jurisdictions 
(see Information Requested below).
    We establish the baseline as the years 2017 to 2019. This baseline 
accounts for the changes in imports and sales that resulted in January 
2016 from the first interim rule (after the rule published, only 20 
salamanders were imported in 2016); the April 2017 court decision that 
overturned the prohibition on interstate transport between States 
within the continental United States; and the outlier 2020 data due to 
the pandemic. The second interim rule prohibits the importation of live 
or dead specimens, hybrids, including parts, as injurious, but not 
eggs, gametes, preserved specimens or parts (including tissue), unless 
an exemption is issued for scientific purposes. From 2017 to 2019, 11 
genera of live salamanders (of which 5 genera are herein being listed; 
table 1), and 16 genera of salamander specimens (that is, dead 
salamanders or parts; of which 6 genera are herein being listed; table 
2) were imported with no discernible trend. Live imports of the genera 
being listed herein are minimal, totaling 373 salamanders and 
approximately $18,000 (table 1). From 2017 to 2019, approximately 1,000 
salamander specimens were imported (table 2), of which 25 percent would 
qualify as injurious under the second interim rule. The values for live 
salamanders with scientific purposes and for salamander specimens are 
unknown. No other salamanders (dead or parts) were imported during the 
baseline period, except for eggs, which would not be affected by this 
rule.

[[Page 2217]]



                    Table 1--Total Number of All Live Imported Salamanders, 2017-2019 (2021$)
                                           [Data from USFWS OLE 2021]
----------------------------------------------------------------------------------------------------------------
                                                                                          Live        Estimated
                    Genus *                                    Purpose                 salamanders      sales
----------------------------------------------------------------------------------------------------------------
Ambystoma......................................  Commercial........................              90       $8,000
                                                 Scientific........................              13         (**)
Amphiuma.......................................  Commercial........................               1      <$1,000
Andrias........................................  Zoos..............................               4       $3,000
Bolitoglossa...................................  Commercial........................               5      <$1,000
Cynops.........................................  Personal..........................               1         (**)
Desmognathus...................................  Commercial........................             119       $3,000
Eurycea........................................  Commercial........................             137       $3,000
Necturus.......................................  Commercial........................             163       $4,000
Pleurodeles....................................  Scientific........................             108         (**)
Pseudotriton...................................  Commercial........................              10      <$1,000
Salamandra.....................................  Scientific........................             100         (**)
                                                ----------------------------------------------------------------
    Total all genera...........................  ..................................             751   ** $24,000
                                                ----------------------------------------------------------------
    Total new genera...........................  ..................................             373   ** $18,000
----------------------------------------------------------------------------------------------------------------
* Genera in bold are listed under the second interim rule. Amphiuma, Cynops, Pleurodeles, and Salamandra are
  listed under the final rule to the 2016 interim rule.
** The value of live salamanders for scientific purposes is unavailable, and estimating this value is beyond the
  scope of this analysis.


Table 2--Total Number of All Imported Salamander Specimens,\1\ 2017-2019
                       [Data from USFWS OLE 2021]
------------------------------------------------------------------------
                                                            Salamander
             Genus \2\                     Purpose         specimens \1\
------------------------------------------------------------------------
Ambystoma.........................  Scientific..........             200
Amphiuma *........................  Commercial..........             200
Bolitoglossa *....................  Scientific..........              99
                                    Commercial..........              80
Cryptobranchus....................  Traveling Exhibit...               1
Desmognathus......................  Scientific..........              24
Eurycea...........................  Scientific..........               9
Laotriton.........................  Scientific..........               2
Necturus *........................  Commercial..........               6
Notophthalmus.....................  Scientific..........               9
Nototriton *......................  Scientific..........               6
Oedipina *........................  Scientific..........               2
Paramesotriton....................  Scientific..........               4
Plethodon.........................  Scientific..........               6
Salamandra........................  Scientific..........             187
Triturus..........................  Scientific..........              11
Tylototriton......................  Scientific..........             111
                                   -------------------------------------
    Total.........................  ....................             957
------------------------------------------------------------------------
\1\ Specimens are animals that are preserved for scientific or museum
  use; however, it is unknown whether these specimens would meet the
  preservation standards and be exempt from listing.
\2\ Genera in bold are listed under the second interim rule. Genera with
  * are not listed under either rule.

    Alternative 1 is the no action alternative and is the status quo. 
We would not list additional species of salamanders as injurious. 
Retail sales of imported salamanders would continue; there would be no 
prohibition on transportation between the enumerated jurisdictions; and 
imports would continue. Salamander and ancillary industries would not 
incur any additional costs unless Bsal is introduced in the United 
States.
    Alternative 1 would not reduce the risk of introducing Bsal to the 
United States, and any benefits that accrue under Alternative 2 (this 
second interim rule) would not accrue under Alternative 1. Under 
Alternative 1, Bsal would continue to pose risk to native species and 
other wildlife resources in the United States. Furthermore, Alternative 
1 does not meet the purpose of the listing, which is to prevent the 
introduction, establishment, and spread of Bsal in the wild in the 
United States. Therefore, we expect that greater financial and natural 
resources losses would be incurred due to managing and responding to 
Bsal if the fungus establishes and spreads in the United States 
compared to taking action now to prevent and minimize its introduction.
    Alternative 2 (second interim rule) lists all species in 16 genera 
for which there is at least one confirmed carrier and all species in 
that genus are likely to be a carrier. From 2017 through 2019, live 
individuals imported from genera that would be listed under Alternative 
2 were in Ambystoma, Desmognathus, Eurycea, and Pseudotriton, and 
specimens (dead individuals or parts) were in Ambystoma, 
Cryptobranchus, Desmognathus, Eurycea, and Laotriton. Under this 
alternative, live commercial imports totaled about 370 salamanders and 
$14,000, which represented approximately 47 percent of all live

[[Page 2218]]

salamander imports and 77 percent of sales. Live imports for scientific 
and zoological purposes totaled 17 salamanders and represented 8 
percent of scientific imports. All specimens under this alternative 
(235 specimens) were imported for scientific purposes, and importers 
would be eligible to apply for a permit. Under Alternative 2, imports 
of these genera would discontinue unless the importer is approved for a 
scientific permit.
    In the long term, the second interim rule is expected to benefit 
the economy. Efforts to control or eradicate invasive species (in this 
case, an invasive pathogen on a host wildlife species) and manage the 
costs they incur to society, once they have become established, are 
generally recognized as being less effective and more expensive than 
efforts to prevent potentially invasive species from establishing in 
the first place (Cuthbert et al. 2022). Emerging pathogens are 
currently underrepresented in databases of the cost of invasives, so 
adding them would greatly increase the estimated costs in the framework 
of biological invasions (Diagne et al. 2021). As a result, sectors of 
the economy that will not need to expend resources to control or manage 
injurious wildlife will be expected to gain from a timely listing 
process.
    Alternative 3 proposes listing all 804 species of salamanders in 
the world. Although some species may or may not serve as carriers of 
Bsal, this alternative takes immediate action against those genera for 
which current scientific research and analysis has provided evidence 
are carriers of Bsal, along with other genera that may eventually be 
found to be carriers of Bsal. Under Alternative 3, all salamander 
imports would be prohibited (tables 1 and 2). This alternative would 
have the largest impact on salamander imports and the highest 
probability of preventing the introduction of Bsal in the wild. We did 
not select this option because we do not have enough evidence at this 
time that all genera could be carriers. However, evidence could be 
established in the future, or another reason could surface, such as the 
appearance of a hypervirulent variant of the fungus.
    We considered other alternatives that we rejected because we do not 
have sufficient information at this time that they could be effectively 
implemented to prevent introduction, establishment, and spread of Bsal 
from salamanders. For example, we do not have the capacity to establish 
and enforce a quarantine system or confidence in its effectiveness at 
preventing Bsal. We noted in the 2016 interim rule that, absent 
concerns regarding the effectiveness and sensitivity of current testing 
methods (including the return of false negatives), the lack of 
validation and sufficient testing capacity, and agency resources 
required to conduct inspections, interpret results, and issue health 
certificates, it may be possible to establish a health certification 
for salamanders that are free of Bsal. These concerns remain, and no 
such health certification has been established. However, this situation 
does preclude us from establishing health certification in the future 
if circumstances change. Appropriate conditions may also be included in 
injurious wildlife permits under the authority of and consistent with 
the purposes of 18 U.S.C. 42.
    We also considered encouraging partners to take nonregulatory 
action, such as voluntary best management practices or individual State 
action. The Service will pursue such actions as we move forward, and we 
are working with partners on such efforts as Habitattitude\TM\, which 
encourages responsible consumer behaviors with respect to pet 
ownership. Voluntary actions, such as applying heat therapy as 
described in Blooi et al. (2015a) and Blooi et al. (2015b), may help 
reduce the threat posed by Bsal, but standardization and widespread 
application of the methods remain as challenges. Although voluntary 
actions are vital to help minimize the threat of invasive species, the 
Service is highly concerned about the extensive damage that 
introduction of Bsal would do to our Nation's natural resources and 
concluded that we cannot rely on voluntary actions alone in this 
instance to address the severity of the threat that Bsal poses.
Regulatory Flexibility Act
    Under the Regulatory Flexibility Act (as amended by the Small 
Business Regulatory Enforcement Fairness Act (SBREFA) of 1996), 
whenever a Federal agency is required to publish a notice of rulemaking 
for any proposed or final rule, it must prepare and make available for 
public comment a regulatory flexibility analysis that describes the 
effect of the rule on small entities (i.e., small businesses, small 
organizations, and small government jurisdictions) (5 U.S.C. 601 et 
seq.). However, no regulatory flexibility analysis is required if the 
head of an agency certifies that the rule would not have a significant 
economic impact on a substantial number of small entities. Thus, for a 
regulatory flexibility analysis to be required, impacts must exceed a 
threshold for ``significant impact'' and a threshold for a 
``substantial number of small entities.'' See 5 U.S.C. 605(b). SBREFA 
amended the Regulatory Flexibility Act to require Federal agencies to 
provide a statement of the factual basis for certifying that a rule 
would not have a significant economic impact on a substantial number of 
small entities.
    The U.S. Small Business Administration defines a small business as 
one with annual revenue or employment that meets or is below an 
established size standard for industries described in the North 
American Industry Classification System (NAICS). To assess the effects 
of the rule on small entities, we focus on (1) entities that import 
animals or animal parts and hybrids of listed genera and (2) entities 
with sales of animals, animal parts, and hybrids that are transported 
between the enumerated jurisdictions listed in 18 U.S.C. 42(a)(1) and 
50 CFR 16.3. Small entities affected by the rule are represented by 
categories and standards from the NAICS. The NAICS categories 
pertaining to this rule are those entities with:
    (1) receipts less than $32.0 million for ``Pet and Pet Supplies 
Stores'' (NAICS 459910);
    (2) receipts less than $2.75 million for ``All Other Animal 
Production'' (NAICS 112990);
    (3) receipts less than $34.0 million for ``Zoos and Botanical 
Gardens'' (NAICS 712130);
    (4) receipts less than $34.5 million for ``Colleges, Universities 
and Professional Schools'' (NAICS 611310); and
    (5) fewer than 1,000 employees for ``Research and Development in 
the Physical, Engineering, and Life Sciences'' (NAICS 541715).
    Under the second interim rule, we expect the effect on entities 
that import the 16 genera to be small. From 2017 to 2019, seven 
businesses imported live salamanders from some of those genera, which 
represented 0.1 percent of all pet and pet-supplies establishments and 
less than 0.1 percent of all other animal-production establishments. 
Three businesses imported the listed specimens for scientific purposes, 
which represented less than 0.1 percent of all universities and 
research facilities (USFWS OLE 2021). We expect the effect on entities 
that sell the 16 genera between the enumerated jurisdictions to be 
small as well, because the interim rule does not prohibit interstate 
transport between the 49 States in the continental United States. 
Furthermore, pet stores outside the 49 States in the continental United 
States represent less than 1 percent of all stores and less than 1 
percent of total pet store sales (USCB 2017).

[[Page 2219]]

    Therefore, we certify that this interim rule will not have a 
significant economic effect on a substantial number of small entities 
as defined under the Regulatory Flexibility Act (5 U.S.C. 601 et seq.). 
An initial regulatory flexibility analysis is not required. 
Accordingly, a small entity compliance guide is not required.
    The second interim rule makes no changes in the compliance 
requirements of any business. The Service is unaware of any 
duplicative, overlapping, or conflicting Federal rules. Several States 
implement similar acts that are more restrictive than the Federal law.
Congressional Review Act
    The interim rule is not a major rule under 5 U.S.C. 804(2), the 
Congressional Review Act. This rule:
    a. Would not have an annual effect on the economy of $100 million 
or more. The rule listing 16 genera of salamanders, including 
approximately 164 species, would prohibit an estimated 125 live 
salamanders imported per year and prohibit the transport of 
domestically bred individuals between the enumerated jurisdictions. In 
addition, businesses would also face the risk of fines if caught 
transporting these salamanders or their parts between the enumerated 
jurisdictions in the shipment clause of 18 U.S.C. 42(a)(1), which is 
codified in Federal regulations at 50 CFR 16.3. The penalty for 
violation of this law is not more than 6 months in prison and not more 
than a $5,000 fine for an individual and not more than a $10,000 fine 
for an organization.
    b. Would not cause a major increase in costs or prices for 
consumers, individual industries, Federal, State, or local government 
agencies, or geographic regions.
    c. Would not have significant adverse effects on competition, 
employment, investment, productivity, innovation, or the ability of 
United States-based enterprises to compete with foreign-based 
enterprises.
Unfunded Mandates Reform Act (2 U.S.C. 1501 et seq.)
    In accordance with the Unfunded Mandates Reform Act (2 U.S.C. 
1501), the Service makes the following findings:
    a. This rule would not produce a Federal mandate. In general, a 
Federal mandate is a provision in legislation, statute, or regulation 
that would impose an enforceable duty upon State, local, or Tribal 
governments, or the private sector.
    b. The rule would not have a significant or unique effect on State, 
local, or Tribal governments or the private sector. A statement 
containing the information required by the Unfunded Mandates Reform Act 
(2 U.S.C. 1531 et seq.) is not required.
Takings
    In accordance with Executive Order 12630 (Government Actions and 
Interference with Constitutionally Protected Private Property Rights), 
the rule does not have significant takings implications. A takings 
implication assessment is not required. This rule would not impose 
significant requirements or limitations on private property use. While 
import and transport between the enumerated jurisdictions of any of the 
listed species is prohibited, 18 U.S.C. 42(a) does not prohibit any 
person who owns one of the listed species at the time of listing from 
continuing to possess the salamander or engaging in intrastate 
transport and other activities within their State or territory, as 
allowed under State, Tribal, or territorial law.
Federalism
    In accordance with Executive Order 13132 (Federalism), this interim 
rule does not have significant federalism effects. A federalism 
assessment is not required. This rule would not have any direct effects 
on States, on the relationship between the Federal Government and the 
States, or on the distribution of power and responsibilities among the 
various levels of government. Therefore, in accordance with Executive 
Order 13132, we determine that this rule does not have sufficient 
federalism implications to warrant the preparation of a federalism 
assessment.
Civil Justice Reform
    In accordance with Executive Order 12988, the Office of the 
Solicitor has determined that the interim rule does not unduly burden 
the judicial system and meets the requirements of sections 3(a) and 
3(b)(2) of the Executive order. The interim rule has been reviewed to 
eliminate drafting errors and ambiguity, was written to minimize 
litigation, provides a clear legal standard for affected conduct rather 
than a general standard, and promotes simplification and burden 
reduction.
Paperwork Reduction Act of 1995 (44 U.S.C. 3501 et seq.)
    This rule does not contain any new collections of information that 
require approval by the Office of Management and Budget (OMB) under the 
Paperwork Reduction Act of 1995 (44 U.S.C. 3501 et seq.). OMB has 
previously approved the information collection requirements associated 
with filing declarations and the importation of injurious wildlife and 
assigned the following OMB Control Numbers:
     1018-0012, ``Declaration for Importation or Exportation of 
Fish or Wildlife, 50 CFR 14'' (expires 03/31/2024, and in accordance 
with 5 CFR 1320.10, an agency may continue to conduct or sponsor this 
collection of information while the submission is pending at OMB), and
     1018-0078, ``Injurious Wildlife; Importation Certification 
for Live Fish and Fish Eggs (50 CFR 16)'' (expires 01/31/2024, and in 
accordance with 5 CFR 1320.10, an agency may continue to conduct or 
sponsor this collection of information while the submission is pending 
at OMB).
    An agency may not conduct or sponsor, and a person is not required 
to respond to, a collection of information unless it displays a 
currently valid OMB control number.
National Environmental Policy Act
    We have reviewed this rule in accordance with the criteria of the 
National Environmental Policy Act (NEPA) and our Departmental Manual in 
516 DM. This rule does not constitute a major Federal action 
significantly affecting the quality of the human environment. Under 
Department of the Interior agency policy and procedures, this rule is 
covered by a categorical exclusion (516 DM 8.5 C(9)), and preparation 
of a detailed statement under NEPA is not required because it adds 
species to the list of injurious wildlife under 50 CFR subchapter B, 
part 16, which prohibits the importation into the United States and 
shipment between some jurisdictions of wildlife found to be injurious 
(for further information on the categorical exclusion, see 80 FR 66554, 
October 29, 2015). The categorical exclusion states, ``The adding of 
species to the list of injurious wildlife regulated under the Lacey Act 
(18 U.S.C. 42, as amended) as implemented under 50 CFR subchapter B, 
part 16, which prohibits the importation into the United States * * * 
of wildlife found to be injurious.'' We have also determined that the 
rule does not involve any of the extraordinary circumstances listed in 
43 CFR 46.215 that would require further analysis under NEPA.
Government-to-Government Relationship With Tribes
    In accordance with the President's memorandum of April 29, 1994, 
``Government-to-Government Relations with Native American Tribal

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Governments'' (59 FR 22951), Executive Order 13175, and the Department 
of the Interior's manual at 512 DM 2, we readily acknowledge our 
responsibility to communicate meaningfully with recognized Federal 
Tribes on a government-to-government basis. In accordance with 
Secretarial Order 3206 of June 5, 1997 (American Indian Tribal Rights, 
Federal-Tribal Trust Responsibilities, and the Endangered Species Act), 
we readily acknowledge our responsibilities to work directly with 
Tribes in developing programs for healthy ecosystems, to acknowledge 
that Tribal lands are not subject to the same controls as Federal 
public lands, to remain sensitive to Indian culture, and to make 
information available to Tribes. For this interim rule, we sent a 
letter to the leaders of the almost 580 federally recognized Tribes 
providing some background and asking for their comments. We received 
none. We have evaluated potential effects on federally recognized 
Indian Tribes and have determined that there are no potential effects. 
This rule involves the importation of salamanders and shipment of 
salamanders between the enumerated jurisdictions of the shipment clause 
of 18 U.S.C. 42, also set forth in 50 CFR 16.3. We are unaware of such 
movement in these species by Tribes.
Effects on Energy
    Executive Order 13211 requires agencies to prepare statements of 
energy effects when undertaking certain actions. This rule is not 
expected to affect energy supplies, distribution, and use. Therefore, 
this action is a not a significant energy action and no statement of 
energy effects is required.
Clarity of Rule
    We are required by Executive Orders 12866 and 12988 and by the 
Presidential Memorandum of June 1, 1998, to write all rules in plain 
language. This means that each rule we publish must:
    a. Be logically organized;
    b. Use the active voice to address readers directly;
    c. Use clear language rather than jargon;
    d. Be divided into short sections and sentences; and
    e. Use lists and tables wherever possible.
    If you feel that we have not met these requirements, send us 
comments by one of the methods listed in ADDRESSES. To help us revise 
the rule, your comments should be as specific as possible. For example, 
you should tell us the numbers of the sections or paragraphs that are 
unclearly written, which sections or sentences are too long, and the 
sections where you feel lists or tables would be useful.

K. Information Requested

    We are soliciting public comments and supporting data for this 
second interim rule to add 16 new genera to the current list of 20 
genera of salamanders that are listed as injurious amphibians under 18 
U.S.C. 42, including comments and supporting data on the economic 
information as described above in the Required Determinations. As 
stated above in this document, we are not soliciting comments regarding 
the listing of the genera that were listed in the 2016 interim rule. We 
will review the public comments for the preparation of a second final 
rule.
    You may submit your comments and materials concerning this second 
interim rule by one of the methods listed in ADDRESSES. We will not 
accept comments sent by email or fax or to an address not listed in 
ADDRESSES. We will post your entire comment--including your personal 
identifying information--on https://www.regulations.gov. If your 
written comments provide personal identifying information, you may 
request at the top of your document that we withhold this information 
from public review. However, we cannot guarantee that we will be able 
to do so.
    Comments and materials we receive, as well as supporting 
documentation we used in preparing this second interim rule, will be 
available for public inspection on https://www.regulations.gov under 
Docket No. FWS-HQ-FAC-2015-0005, or by appointment, during normal 
business hours at the Service's office in Falls Church, VA (see FOR 
FURTHER INFORMATION CONTACT).
    We are soliciting public comments and supporting data to gain 
additional information, and we specifically seek comment on the 
following questions:
    (1) How many of the new genera listed by this interim rule are 
currently in domestic production for wholesale or retail sale, and in 
how many and which States?
    (2) How many businesses sell salamanders from the genera listed by 
this interim rule, and how many businesses transport these listed 
genera between enumerated jurisdictions?
    (3) How many businesses breed salamanders of one or more of the 
genera listed by this interim rule?
    (4) What species listed as threatened or endangered by one or more 
States would be affected by the introduction of Bsal?
    (5) What provisions in this interim rule should the Service have 
considered with regard to: (a) the impact of the provision(s) 
(including any benefits and costs), if any, and (b) the alternatives, 
if any, that the Service should consider, as well as the costs and 
benefits of those alternatives, paying specific attention to the effect 
of the rule on small entities?
    (6) How could this interim rule be modified to reduce costs or 
burdens for some or all entities, including small entities, consistent 
with the Service's requirements? For example, we seek comment on the 
distinct benefits and costs, both quantitative and qualitative, of (a) 
the prohibitions on importation and (b) the prohibitions on transport 
between enumerated jurisdictions of the genera listed by this rule. 
What are the costs and benefits of the modifications?
    (7) Is there any evidence suggesting that Bsal has been introduced 
into the United States or may have already established?
    (8) Is there evidence suggesting that any of the genera listed by 
this interim rule are not carriers of Bsal? If so, which ones?
    (9) Is there evidence suggesting that additional salamander genera 
are carriers of Bsal and should be listed as injurious? If so, which 
ones?
    (10) Could a reliable health certificate within the Service's 
authority be developed that would allow Bsal-free salamander imports? 
Are there treatments that would ensure salamanders imported into the 
United States are reliably free of Bsal, and how could compliance be 
monitored?
    (11) Are there other means of preserving or treating salamander 
specimens, parts, or products that are not identified in this rule and 
that are proven adequate to render Bsal non-viable?
    (12) Should the Service add eggs or other reproductive material of 
listed salamanders to the list of injurious wildlife because they may 
also carry Bsal?
    (13) What are relevant Federal, State, or local rules that may 
duplicate, overlap, or conflict with this interim rule?
    We will also submit the rule for peer review concurrent with public 
comments. In conducting peer review, we will follow guidance from the 
Office of Management and Budget ``Final Information Quality Bulletin 
for Peer Review'' (OMB 2004) and the Service's own guidance.

References Cited

    A complete list of all references used in this rulemaking is 
available at https://

[[Page 2221]]

www.regulations.gov under Docket No. FWS-HQ-FAC-2015-0005.

Authors

    The primary authors of this rule are the staff members of the U.S. 
Fish and Wildlife Service's Branch of Aquatic Invasive Species.

List of Subjects in 50 CFR Part 16

    Animal diseases, Imports, Reporting and recordkeeping requirements, 
Transportation, Wildlife.

Regulation Promulgation

    For the reasons discussed in the preamble, the U.S. Fish and 
Wildlife Service amends part 16, subchapter B of chapter I, title 50 of 
the Code of Federal Regulations, as set forth below:

PART 16--INJURIOUS WILDLIFE

0
1. The authority citation for part 16 continues to read as follows:

    Authority:  18 U.S.C. 42.


0
2. Revise Sec.  16.14(a) to read as follows:


Sec.  16.14   Importation of live or dead amphibians or their eggs.

    (a) The importation, transportation, or acquisition of any live or 
dead specimen or hybrid, including parts (except for eggs or gametes; 
parts or tissues that have been chemically preserved, chemically 
treated, or heat treated so that the pathogen Batrachochytrium 
salamandrivorans, if present, is rendered non-viable; and molecular 
specimens consisting of only the nucleic acids from organisms), of all 
species in the genera Ambystoma, Andrias, Aneides, Aquiloeurycea, 
Calotriton, Chioglossa, Chiropterotriton, Cryptobranchus, Cynops, 
Desmognathus, Ensatina, Euproctus, Eurycea, Hydromantes, Hynobius, 
Ichthyosaura, Laotriton, Lissotriton, Neurergus, Notophthalmus, 
Ommatotriton, Onychodactylus, Pachytriton, Paramesotriton, Plethodon, 
Pleurodeles, Proteus, Pseudobranchus, Pseudotriton, Salamandra, 
Salamandrella, Salamandrina, Siren, Taricha, Triturus, and Tylototriton 
is prohibited except as provided under the terms and conditions set 
forth at Sec.  16.22 of this part.
* * * * *

Shannon Estenoz,
Assistant Secretary for Fish and Wildlife and Parks.
[FR Doc. 2024-31203 Filed 1-8-25; 8:45 am]
BILLING CODE 4333-15-P