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

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URL: https://www.frixlaw.com/law-library/documents/fr%3A2024-31203

## Record

- **Collection:** Federal Register
- **Document type:** Rule
- **Published:** January 10, 2025
- **Citation:** 90 FR 2170

## Text

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.

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

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

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

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

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

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

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® (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.

(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 × 0.8); with Alternative Y, the expected costs would be $2,500 ($25,000 × 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

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

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

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,

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

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

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

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

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

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

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Source: Frix Law Library, https://www.frixlaw.com/law-library/documents/fr%3A2024-31203. Public record. Not legal advice.