Session Two (Part 1): Review of the Laws, Regulations, and Permits Associated with Fish and Wildlife

Moderator: Sharon Shriver, Public Responsibility in Medicine and Research

Sharon Shriver welcomed workshop participants to Session Two. She introduced herself as session moderator and senior director at Public Responsibility in Medicine and Research, a nonprofit whose mission is to advance the highest ethical standards in research by providing support to the human and animal research oversight communities. During the first part of Session Two, speakers identified the diverse regulatory requirements unique to wildlife that exist at multiple levels, including international, national, state, and local, including native lands. Presentations in this session included Adam Ferguson from the Field Museum of Natural History who presented on animal welfare challenges in research and education from a Museum of Natural History perspective. Laurie Baeten from the National Park Service (NPS) presented on challenges from the NPS perspective. Caleb Hickman, representing the Eastern Band of Cherokee Indians’ (EBCI’s) Office of Fisheries and Wildlife Management, presented on the research conducted on tribal lands.

ANIMAL WELFARE CHALLENGES IN RESEARCH AND EDUCATION ON WILDLIFE: A NATURAL HISTORY MUSEUM PERSPECTIVE

Adam W. Ferguson manages more than 245,000 specimens of mammals ranging in size from pygmy mice to elephants in his work as Negaunee Collection Manager of Mammals at the Field Museum of Natural History in Chicago. Ferguson, who spends about 80% of his time on the care, access, and support of the collections and 20% on research, shared his unique perspective on the many factors that can influence which animals are used in research and how that research is carried out. Ferguson provided examples of how regulations often drive research, and how emotions can drive regulations, both of which can impede or limit the scientific process, especially as it relates to museum science.

Regulations can drive research in a number of ways and may influence which species to study, Ferguson said. For example, a researcher may choose to study invertebrates versus vertebrates to avoid dealing with Institutional Animal Care and Use Committee (IACUC) regulations, he said. Additionally, regulations may influence study objectives and methods, whether researchers conduct domestic or international work, and in particular lethal versus non-lethal sampling. In turn, emotions can drive these regulations. When it comes to permission for research and specimen collection, Ferguson said, there tends to be a taxonomic bias associated with the types of animals, in particular of mammals, that researchers’ study. For example, sampling non-native rats lethally may not provoke a reaction like the use of primates. In addition to often being biased in terms of permission to collect, regulations are often also taxonomically structured, Ferguson explained. For example, bats and non-human primates are regulated by the U.S. Centers for Disease Control and Prevention (CDC) through the Division of Select Agents and Toxins, while African rodents and certain small carnivores such as the Genets and the family Viverridae are regulated by the Division of Global Migration and Quarantine. For other taxonomic groups such as shrews, he said, it is not clear who regulates them.

Ferguson also pointed to examples of how the law as written does not always follow biological reality. For example, he said, when an import permit is required regarding a potential specimen being infectious or non-infectious, the law states that a permit is not needed if the specimen is rendered noninfectious, such as with the treatment of formalin (or another reagent that renders a pathogen noninfectious). However, this is not the case for bats and non-human primates or their tissues as permits would still be required even after being treated and rendered non-infectious. Under this legal definition, the law can be misconstrued suggesting that treating bat and non-human primate tissues as such with

formalin would not render these specimen non-infectious, unlike the treatment of rodents or rodent tissues with formalin.

Acquiring mammals involves a complex array of permits and agencies that Ferguson called “somewhat of a choose your own adventure.” For example, importing and exporting requires U.S. Fish & Wildlife Service (FWS) involvement, as well as IACUC involvement, Ferguson said. Certain individual specimens and taxonomic groups, such as those of bat and non-human primate origin, have requirements through the CDC with import permits being required for animal species known to host high-consequence pathogens. Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) permits are required based on the International Union for Conservation of Nature (IUCN) Red List of Threatened Species status of a given species. In the case of marine mammals, the Marine Mammal Act involves the U.S. Department of Commerce’s National Oceanic and Atmospheric Administration (NOAA), as well as other groups; tenrecs, brush tail possums, and ungulates require U.S. Department of Agriculture (USDA) involvement. Ferguson asserted that certain animals are no longer collected at all by museum scientists because of the amount of regulations and the difficulty with obtaining permissions. To further exemplify the complexities of the regulatory patchwork, Ferguson laid out what is needed to set up a study for two different marten species: the American marten (Martes americana), which is domestically distributed in the United States and North America, and the yellow-throated marten (Martes flavigula), which is sourced internationally. For the American marten, differences in state regulations could also impact research, Ferguson said. For example, in Wisconsin, this species is treated as a state endangered mammal with no harvest, but in Montana, it is treated as a furbearer with no limit during a certain season as long as standard guidelines are followed. However, Montana’s regulations cater to commercial interests but apply differently to scientists, who would encounter difficulties in acquiring American martens in that state, Ferguson added. Therefore, a study that requires lethal collection is more likely to meet obstacles in terms of regulations. Research with the American marten is made easier when studies are being conducted within the United States. Additionally, the American marten is not listed as protected under CITES and the Endangered Species Act (ESA) of 1973 (U.S. Fish & Wildlife Service. 16 U.S.C. § 1531) or listed as being of conservation concern through the IUCN.

Although similar to the American marten in terms of the impacts on taxonomic and tropic status on studies, in particular lethal studies involving this animal species, there are other obstacles and barriers with regulations with the yellow-throated marten, for which studies would have to occur outside the United States, Ferguson added. In particular, he said there are challenges related to the IACUC and obtaining permission to acquire and transport drugs needed for anesthesia or euthanasia, which is often illegal given the illicit nature of these drugs in the United States and in other countries. The issue of who owns the specimen—the country, the museum, or the animal’s community—is also called into question, Ferguson said. Then there are other regulatory bodies to consider, Ferguson said, which would include CITES in the case of the yellow-throated marten. India has listed this species as CITES III, which means that even if it is studied outside of India, a certificate of origin related to CITES is still required. Although CITES is not a regulatory body, Ferguson has found that it does influence permission to study these animals.

In relation to the animal care and use in research, Ferguson said that while the three Rs (replace, reduce, and refine) are fitting guidelines for studies of animals, they are often difficult when these terms are applied to natural history museums. For example, it is not possible to replace a physical specimen in a natural history museum. In this case, there is no substitute. While it is possible to reduce the number of animals used to a minimum, controlling or limiting the number of specimens also limits the ability to study such things as variation and disease. If the prevalence in a study is 0.01 and the researcher is allowed to collect only five animals, the probability of detecting disease or certain parasites, for example, becomes infinitesimally small. Oftentimes these limits are subjective and not based on species biology. Researchers are often allowed to collect only 10 animals per species per site, which is not based in biological reality. Ferguson also said that studies have been conducted on the impacts of these lethal collections and have shown that there are minimal or limited impacts on diversity measured in different ways for especially small mammals. Ferguson advocated for more studies and more limits that are based

in biology for lethal collecting. For the third R (refine), Ferguson pointed out that, although no testing occurs at museums, guidelines do exist within the museum community and they are refined constantly for minimizing stress during the trapping and collecting of specimens in different settings.

Ferguson argued that, in the context of both a museum perspective and science in general, it is worth adding to the three Rs (replace, reduce, and refine) a fourth R for “responsibly.” This is the idea that research and regulations be “responsibly” represented to match biological reality, which often is not the case, he said. He suggested that objective data-driven scientific evidence be used for establishing and implementing regulations and guidelines for animal care and use in research and education. Ferguson mentioned some of the most impressive considerations about the care and use of animals in Australia:

• Requiring the deposition of incidental mortalities (whether ecological or museum-based) into a scientific collection
• Regulating (justifiable) the lethal take of animals based on biology
• Realigning regulations aimed at scientists to match other sectors
• Re-examining restrictions not found in biological reality
• Reinforcing effective communication and dialogue between scientists and regulators
• Recognizing that regulations can hinder research

In closing, Ferguson also pointed out biases that are not helpful, for example, assuming that only natural history studies seeking voucher specimens explicitly result in lethal sampling of animals. He stated that ecology studies may accidently also result in death, and he sees this as a big loss for adding value to those specimens and reconciling that a non-lethal study may result in accidental mortality. Pointing out the bias between the private sector and the scientific sector, Ferguson explained that in Texas, the mountain lion Puma concolor is a non-game animal that, as long as hunters possess a valid hunting license, can be killed without any limits. Meanwhile, for a scientist to collect such animals, it would be nearly impossible. Re-examining restrictions not founded in biological realities (e.g., formalin fixation under evaluation by the CDC) and reinforcing effective communication and dialogue between scientists and regulators is important, Ferguson said. Finally, he said that it is vital to recognize that regulations can and do hinder research and the types of questions asked, which naturally inhibits or blocks the advancement of scientific research and knowledge.

CHALLENGES FROM THE NATIONAL PARK SERVICE PERSPECTIVE

Laurie A. Baeten is the attending veterinarian and IACUC chair for the NPS. As part of the Biological Resources Division, the NPS IACUC established in 2010 uses a One Health approach to protect and promote the health of wildlife, humans, and the environment within national parks, focusing primarily on managing and researching free-ranging wildlife populations. Baeten’s 20 years of experience includes working with a wide variety of species ranging from rodents, birds, and small mammals scaling all of the way up to moose and camels, including work with wild caught or captive bred animals maintained in captivity, as well as free-ranging wildlife.

The NPS interacts with wildlife in a variety of ways, Baeten said. For example, many of the national parks have long-term inventory and monitoring programs. She explained that most parks use an integrated management approach for monitoring and controlling pest species, and biologists use a diverse set of management tools for monitoring and maintaining populations within various ecosystems. These are all in addition to conducting or hosting a wide variety of management and research projects. Park staff often work closely with surrounding state and tribal agencies on these projects, as well as the many collaborative efforts with academic institutions. The NPS IACUC is registered as a research institution with APHIS and reviews approximately 150 protocols and amendments per year, with half of those received from academics with concurrent IACUC reviews. Interagency Research Animal Committee guidance is followed and all protocols that involve the handling of vertebrates are reviewed.

There are more than 400 locations managed by the NPS, and these include the large national parks, Baeten said, as well as the smaller national monuments, preserves, historic sites, military parks, or battlefields. This makes it challenging, she said, because each unit establishes their own risk tolerances and resource management criteria, which also makes it difficult to offer training opportunities, provide technical assistance, or conduct post-approval monitoring. Conducting research within the national parks requires park-specific scientific collection permits. This process can be cumbersome as researchers are required to have a separate permit for conducting research within multiple park units. Because wildlife do not recognize park boundaries, many research efforts also need to be coordinated with surrounding state and tribal land agencies, Baeten added.

The NPS IACUC is tasked with reviewing all proposed research projects within park boundaries and tries to work closely with permitting staff at each park to ensure compliance. In review of academic submitted research protocols, the NPS IACUC may defer final animal welfare oversight to the concurrent institution, but often finds that modifications are needed for some activities to meet the higher standard of care expected. Conditions for approval often need to be added to protect the welfare of non-target species, Baeten explained, and considerations need to be given to visitor and environmental impacts, as well as seasonal impacts, such as disturbances during animal breeding and rearing stages. Appropriate euthanasia and capture methods are always used, she said, including appropriate trap checking intervals, and necessary biosecurity measures are also taken. Another challenge faced by the NPS IACUC is the recent change by journal editors requiring review statements with submissions of manuscripts, which is impacting the NPS’s ability to utilize data collected from the many long-term inventory and monitoring programs in scientific publications, Baeten said.

Baeten said that while the NPS’s philosophies have varied since the first park was established in 1916, current policies allow for the management of wildlife populations as long as the management efforts do not cause unacceptable impacts. Management may be necessary because populations are unbalanced within an ecosystem, and efforts may be needed to protect cultural resources, humans, property, or other flora or fauna species within the ecosystem, or for accommodation of development. One of the most common questions that comes to the IACUC, Baeten said, Does this proposed activity require an IACUC review? Discussions then ensue to determine whether the activities should be considered as a field study, a research project, or a management effort, and the NPS IACUC reviews protocols when they involve any vertebrate species. During initial assessments, any capture and handling is considered to have the potential to materially alter behavior, so it is suggested that protocols be submitted for review. Baeten commented that the poor distinction between research and management can pose challenges (Lindsjö et al. 2019), explaining that this is further complicated by the lack of definitions for “management,” “harm,” and assessment of “materially altering behavior” in the AWA. She expressed that, in her opinion, the most difficult term to define is “momentary pain or suffering,” because there is clear variation when comparing the impacts of routine procedures for a laboratory animal species and trying to apply that to a free-ranging wildlife species.

To assist researchers, biologists, and academics who wish to work within the parks, the NPS IACUC developed a flow chart that provides clear definitions and decision points to address the challenges of differing perspectives or interpretations, Baeten said. Using laws, policies, and guidance from the USDA, the criteria to distinguish research versus management activities is based on the intent of the proposed work (Thompson et al. 2022). Baeten provided two example scenarios to highlight the lack of differentiation between research and management and demonstrate the use of the decision-making model. In the first example scenario, a project is proposed by a park biologist interested in re-establishing a marten population that had been extirpated from the park. The plan is to release capture-bred martens from a zoo into their national park using established release protocols and fit all animals with collars to monitor survival. In the second scenario, a project is proposed by researchers from an academic institution who are interested in trapping and collaring a population of martens in another park; the intent for this study is to assess habitat use and reproduction in wilderness areas compared to martens living in high human traffic areas. In both instances, martens will be handled, collared, and followed for several

years, with both projects hoping to recapture the animals when the collar batteries are due to fail. Thus, in both scenarios, animals are essentially handled in the same manner.

Using this decision-making model, both projects can be evaluated to determine if they should be considered as research or a management project. The first step is to ask: What is the intent of the project? Does it achieve a desired resource objective? If so, then it could be considered as animal management. These activities are typically proposed by wildlife biologists or natural resource managers and are usually based on well-established scientific knowledge. Examples include population control or stewardship actions. Additionally, many parks take actions to decrease human health risks and the likelihood of zoonotic disease transmission from contact with wildlife, and these involve well-established management protocols for dealing with situations such as human habituated large carnivores or the removal of bats or rodents from high human traffic areas. These types of activities might also include animal handling and testing to monitor for disease emergence; for example, there are white-nose syndrome (WNS) or chronic wasting disease (CWD) surveillance programs in many of the parks. Baeten explained that in accordance with the AWA, these management activities are not subject to review, regardless of whether animals are harmed or undergo stressful procedures, and she mentioned that many wildlife professionals struggle with this fact.

Considering this, Baeten explained, the first marten project might be considered management because it meets the desired resource objective of establishing an extirpated population. If the intent of the project is to answer a scientific question, it is considered to be research based on the decision-making model. These types of projects use a scientific study design to test a hypothesis, compare or refine different techniques or treatments, or improve understanding of a biological or ecological system. Projects are also reviewed as research if they involve the use of animals to teach science or animal research procedures, as well as if the intent is to generate a peer-reviewed scientific publication. Considering these criteria, the second marten project would likely be considered as a research project. But what if the biologists and the zoo staff in the first project want to generate a scientific publication using the captive release survival data? Would both protocols require IACUC review?

Many projects that occur in parks are purely observational or use humane methods for the lethal removal of specimens for archiving in park or museum collections, Baeten said, and these types of activities are exempt from the AWA. Other projects involving inventory and monitoring that require minimal handling are often referred to as bio blitzes. In these cases, animals are captured by minimally invasive methods, handling does not cause harm, and procedures do not materially alter animal behavior. Examples could include the inventorying of amphibian species in watersheds or bat species in caves. These activities, which are considered field studies, are repeated at regular intervals to detect changes over time and often help to inform management decisions. The NPS IACUC has a specific submission form in these cases, and if the project is deemed to meet the criteria for a field study, an approval memo is issued and no further IACUC oversight is required unless significant changes are made to the animal and handling activities, Baeten said. Looking back at the marten scenarios, either research group might choose to refine their animal monitoring procedures in future years and switch to the use of camera capture to collect reproduction data at den sites, at which point, their monitoring efforts would be considered field studies.

The current trend for biomedical research is the emphasis on non-lethal experimentations, and domestic species such as cats, dogs, rabbits, and horses used in research projects are subsequently put up for adoption or can be used in multiple research projects over time. As such, the question as to whether animals brought into captivity should be returned to the wild is often brought up for discussion. Baeten argued that similar considerations could be applied to re-introductions with captive bred wildlife species. Although the NPS does not have any dedicated research facilities, it does have a few that temporarily house wild animals for various reasons, including a captive breed and release project, as well as the California Condor facilities where condors with lead poisoning are treated and released back into the wild. Animals are occasionally captured in parks and transported outside of the park for research purposes, and although the IACUC does not recommend the return of these individuals, final decisions are made at the park level. When this does occur, strict biosecurity measures are outlined in written

protocols, animals are returned to their site of capture, and seasonal considerations are made to ensure there are no disruptions to breeding or rearing. Baeten explained that the emphasis is to maintain the park’s natural resource stewardship, so factors such as risk of disease transmission, possible alterations to genetic and ecological integrity, and animal health concerns resulting from being held in captivity are considered.

In closing, Baeten provided reference materials: two articles on research versus management (Lindsjö et al. 2019; Thompson et al. 2022); five articles on animal welfare and wildlife research (Mulcahy 2003; Curzer et al. 2013; Sikes 2013; Paul 2015; Sikes and Bryan 2015); and one article on publishing (Mulcahy 2017). These references provide information for the review of wildlife protocols, including citations for the decision-making model she discussed and a paper by Curzer and colleagues (2013) that outlines a Nine R Theory for ethical considerations.

RESEARCH ON TRIBAL LANDS: UNIQUE EXAMPLES

Caleb R. Hickman, supervisory biologist for the EBCI in North Carolina (southern Appalachian Mountains) and tribal citizen of the Cherokee Nation of Oklahoma, shared experiences from 20 years working on research projects with both game and non-game species, including research projects with other tribes. For example, Hickman worked on a range of projects on conservation target species inventory, monitoring, management, research, and restoration for species ranging from fish to large mammals. Many of the tribes work on the same types of projects, Hickman said, especially when it comes to regulatory processes or trying to understand their resources and harvesting potentials. It is noteworthy, he added, that they accomplish all of this with just a few staff members, and some tribes do not have any biological staff but still achieve the same goals. For many of these projects, partnerships with universities are common if animal care and use is to occur.

Hickman explained that tribes are recognized by the U.S. government as sovereign nations, with independent governments themselves. Unlike the states, this is a government-to-government relationship. Currently there are 574 federally recognized Native American tribes in the United States. Many of these have their own form of government and may or may not have land, Hickman said, but all have this government-to-government relationship with the United States and it is managed largely through the U.S. Department of the Interior’s Bureau of Indian Affairs (BIA). Hickman shared that one important aspect of tribes is their natural resource management and how it is performed. Tribes are diverse throughout the continent, with different languages, cultures, and ecosystems. Land ownership can be different than for states, because the idea of ownership is probably unfamiliar to many of the tribes but is important, Hickman added. Tribal lands are protected largely by the tribes, but also by the U.S. government resulting in biodiversity that rivals some of the world’s most protected lands (NLIS n.d.). Tribes have a long history connected to these environments. This would be valuable to researchers for managing and adapting to dramatic changes. Tribes also share resources with state, federal, and private land holders as animals and waterways move across boundaries.

In comparison to the states, tribes encounter many inequalities, Hickman asserted. For example, conservation-related funding for management and research is limited to competitive Tribal Wildlife Grants and funding from the BIA. Meanwhile, states benefit from excise taxes and non-game funds from Wildlife Action Plans, both of which tribes often contribute to but do not benefit from. Most tribes have an average poverty rate of 25%, which is three times that of Americans and is attributed to geographic isolation and generational trauma. There is also poor representation in academia, he said, as there are only 41 Tribal Colleges and Universities, and few of these have any sort of research focus. Only 0.7% of biologists in the United States are tribal citizens, and most tribes can only afford to pay a single biologist and a couple of technicians to do a variety of projects for economic development, harvesting, and regulatory processes. Thus, he said, tribes have a limited research and management capacity and may be reliant on partnerships or risk mismanaging their resources.

Building on the example of two martens from the tribal perspective, Hickman said, includes a discussion of the federal protections or regulatory processes involved when an animal is protected, as well

as some of the unique considerations necessary when conducting research on tribal lands. The BIA is responsible for 68.5 million acres of trust land and 57 million acres of subsurface minerals, which it protects for the tribes. Tribes often work through the BIA process but end up taking a lot of the work upon themselves, such as by working with the FWS for the protection of species. This includes a lot of the normal federal processes that might occur on national park or national forest lands. However, the difference, Hickman said, is that tribes have to live and grow an economy on these lands as well, so this can be difficult for them to approach. Additionally, Section 7 of the ESA influences federally recognized tribes with protected lands of significant size or habitat diversity. Listing of species under this act impacts researchers’ ability to work with these animals, and studies with certain species may require a permit, such as a 404 permit, he explained. These ESA guidelines are built to ensure that federal agencies enact programs for conservation of endangered species. Tribes can be involved as well, termed an interagency cooperation. This is the mechanism by which federal agencies ensure the actions they take, including those that they fund, such as protection of certain tribal lands or the management of those lands for the tribes, do not jeopardize the existence of any listed species based on Secretarial Order 3206, Hickman said.

Although the mechanisms for endangered species conservation through interagency cooperation under the ESA may be intended to prevent tribes from bearing a disproportionate burden of regulatory costs (FWS 1973), Hickman said that these laws unfortunately do create hardships. For example, even building a house or cutting down a tree can create difficulties for members of a tribe, because surveys of these species must be conducted beforehand. According to Hickman, these burdens could potentially be alleviated through the use of regulatory compliance processes that encourage federal, tribal, and research partners to work together. This starts with obtaining proper funding, which can be difficult, but is possible through the BIA. Specialists can be hired on particular projects, if capacity is minimal.

Hickman commented that there also needs to be input from tribal citizens, after which a plan can be developed with the FWS. This process never has any sort of animal care and use, even if there are studies that take place and potential threats to these animals, he said. However, involvement of endangered species does require endangered species permits through the FWS. Researchers may approach a tribe to work with a particular species for a variety of reasons. The species may be important to science in some way and may only exist on tribal lands, or this species may cross boundaries and it is important for researchers to study the organism on state, federal, and tribal lands. Tribes hold a significant land base, so including tribes in the research can be important.

Tribes are often included in research through a traditional tribal ecological perspectives, Hickman explained (Berkes 1993). Conducting research on tribal lands involves different kinds of permitting, and although it may not require animal care and use permitting, a significant process is still involved. Hickman mentioned that even though researchers can obtain permits to work with tribes on tribal lands, problems can still arise. He shared that, to many tribes, “Western science is considered to be a ‘settler colonial science.’” He went on to list examples of the problems of research in tribal lands: invasive (engendering broader impacts); paternalistic (in the way tribes are approached); and extractive (when information that is gathered and not shared back with the tribe or is not helpful for the tribe).

Hickman referenced a publication on the co-production of science and policy in integrated climate assessments (Lemos and Morehouse 2005). He drew a parallel with the study’s conclusion that more interactive models with contributions of knowledge and capacities from a variety of different stakeholders with the common goal of co-creating to inform environmental understanding and decision-making may prove to be better than using any single model alone. He added that the animal care and use process is expensive and co-production does not equate to collaboration. Collaboration would be a higher level of transparency with the locus of power, knowledge, project decision-making, project benefits, and project finances being shared equally from the outset of a project. He said this could include contributions from individuals that support the projects and working with tribes on an even footing, which is especially important if animal care and use is required. He pointed out that some tribes may not have the financial resources to keep the animal care and use process in place.

Working with universities or federal partners can institute more research, although this does ultimately take away from the tribes’ sovereignty. Many tribes have their own processes, including for medical and cultural research, Hickman said. As shown in Box 2-1, Hickman also provided the statement from the EBCI for research on the Cherokee Qualla Boundary (EBCI Cultural Research Committee 2021). Any time people are interviewed or are involved in research on tribal lands, an Institutional Review Board (IRB) is necessary and can help in the research process.

Hickman wrapped up his point of view on tribal sovereignty in research by providing four helpful references, with one on traditional knowledge and western science (Mason et al. 2012); one providing information on federal, state, and tribal grants (FWS 2021); and two on the co-production of science and policy (Lemos and Morehouse 2005; Durose and Richardson 2015).