The black-footed ferret (Mustela nigripes) is one of the rarest mammal species in North America. Captive breeding has prevented extinction of this species, but successful reintroduction of ferrets into their native grassland habitat is a complex endeavor. As specialist predators, ferrets depend almost exclusively on prairie dogs (Cynomys spp.) for both food and shelter, so successful black-footed ferret reintroduction hinges on maintaining large colonies of prairie dogs. However, prairie dogs are also considered agricultural pests and are often subjected to eradication programs. These eradication programs hamper efforts to reintroduce ferrets and disrupt the valuable ecosystem services prairie dogs provide in their role as both keystone and foundation species. Even when agreements are reached to maintain prairie dog colonies, plague (Yersinia pestis), which infects both prairie dogs and ferrets, can threaten the success of a ferret reintroduction program. We describe the research on the complex ecological relationships and socio-environmental challenges of reintroducing endangered black-footed ferrets, with a focus on the most abundant prairie dog species, the black-tailed prairie dog (Cynomys ludovicianus).
This case study demonstrates the complexity of ecological interactions by examining the components necessary for successful reintroduction of the endangered black-footed ferret to their native grassland habitat. As a specialist predator, ferrets depend on prairie dogs for food and shelter. In this case study, students will learn that prairie dogs are both a keystone and foundation species, providing valuable ecosystem services. They will consider the challenges of captive breeding and learn about selecting suitable reintroduction sites using an interactive mapping tool. Students will also consider the concerns of stakeholders, some whom view prairie dogs as agricultural pests and disease carriers.
We are living through the Earth’s sixth mass extinction, and evidence points to humans as the direct or indirect cause of most species’ losses . At what point will these extinctions result in the collapse of entire ecosystems or disrupt the vital nutrient and water cycles upon which our agricultural systems depend? Do we have a moral obligation to be better stewards of the Earth and its inhabitants? Extinction is forever, but on rare occasions we are given a second or third chance to save a species. This case study focuses on the remarkable story of the black-footed ferret (Mustela nigripes), a species that has been declared extinct twice, only to be rediscovered allowing us the opportunity to reintroduce it to its native grassland ecosystem. Reintroducing a species is not just simply putting a missing piece into a jigsaw puzzle: success depends on understanding the complex interactions among species. We begin by examining the ecology of black-footed ferrets and their prey, black-tailed prairie dogs and then delve into the complex social and ecological factors involved in black-footed ferret survival.
Black-footed ferrets and black-tailed prairie dogs (Cynomys ludovicianus) are iconic species of the North American Great Plains. Both species’ historical ranges stretched from Southern Canada to Northern Mexico [2–4]. However, black-tailed prairie dog populations have declined an estimated 98% in the last 200 years, largely because prairie dogs are often considered pests and are subjected to eradication programs [5, 6]. Fossil evidence indicates that the ancestors of black-footed ferrets did exploit a broad range of prey , but contemporary black-footed ferrets are specialist predators with as much as 90% of their diet made up of prairie dogs. In the past, scientists have often underestimated the ecological importance of predators; however, they can strongly influence ecosystem composition . Predators indirectly influence plant populations and growth and may also influence disease prevalence and outbreak frequency, due to regulating herbivore populations .
The black-tailed prairie dog is one of five prairie dog species that inhabits the native North American grasslands . They live in large colonies and dig massive burrow systems, creating below-ground habitat for other species and influencing vegetation structure, species composition, productivity, nutrient cycling, water infiltration, and soil chemistry of the surrounding landscape [8, 9]. Because of their influence on grassland ecosystems and unique ecological role, black-tailed prairie dogs, like other species of prairie dogs, are considered both a keystone species and a foundation species [8, 10]. One of the main mechanisms that illustrate the role prairie dogs play in the ecosystem is that ferrets exclusively use prairie dog burrows for shelter, mating, and movement through the landscape. With prairie dogs being a keystone species, their absence from the ecosystem can have significant effects on the abundance and distribution of ferret populations . However, one of the challenges in studying the ecology of this system is that researchers have never been able to study it intact, because Euro-American settlers drastically altered the Great Plains landscape as soon as they arrived [2, 5, 8].
Before continuing, discuss the difference between a foundation and a keystone species. Why prairie dogs are considered both a foundation and a keystone species?
Why Have Black-Footed Ferrets Disappeared?
Native grasslands are considered North America’s most endangered ecosystem , and like many species dependent on this habitat, black-footed ferret populations have declined sharply since the 1900s . The decline in ferrets is directly linked to the decline in prairie dogs. By examining what has happened to prairie dog populations, we can explain the disappearance of black-footed ferrets. Four driving factors of prairie dog decline are as follows: (1) conversion of native grassland habitat to cropland and other land uses; (2) efforts to eradicate prairie dog populations to prevent crop, livestock, and property damage; (3) recreational shooting of prairie dogs; and (4) the spread of Yersinia pestis, the bacterium that causes sylvatic plague [2, 4, 13, 16].
Land conversion and attempts to eradicate prairie dogs started as soon as Euro-American settlers reached the Great Plains . Changes in land use from grazing by wild bison or domestic cattle to cultivated crops destroyed potential prairie dog habitat and severely fragmented the ecosystem. Settlers, who viewed prairie dogs as a threat to crops, used tilling the land, drowning, shooting, trapping, and poisoning to eradicate prairie dogs . In the early 1900s, the present-day equivalent of billions of dollars was spent in federal efforts aimed to exterminate prairie dogs through poisoning . The resulting decline in black-tailed prairie dogs, exacerbated by their susceptibility to sylvatic plague, led to their listing as a candidate species for endangered status in the United States in 2000 . However, after black-tailed prairie dogs were removed from the candidate list in August 2004 , several large-scale poisoning projects were once again initiated and both South Dakota and Nebraska created legislation that classifies prairie dogs as pests [9, 16].
Historically, recreational shooting minimally impacted prairie dog populations, but shooting has a much larger impact on today’s diminished populations . Recreational shooting is often used as a method of prairie dog eradication. However, because some farmers and ranchers have started using colonies as a source of income by charging for recreational shooting access on their land, they have incentive to sustainably manage populations . Maintaining healthy prairie dog populations is also important to some Indigenous communities who sustainably harvest them as a traditional food source .
On top of all of these issues, both ferrets and prairie dogs also have to deal with sylvatic plague: a bacterial disease transmitted between mammals by fleas. Some mammal species are not symptomatic from plague, but for others, plague is deadly . Black-tailed prairie dogs have nearly 100% mortality from plague, while other species of prairie dog species have mortality rates close to 85% [18, 19]. Black-footed ferrets and other predators were previously assumed to be immune to the plague bacterium ; however, plague also kills ferrets [20, 21]. While there were still plague-free areas in the Great Plains in 2005, plague is now found throughout the entire black-tailed prairie dog historical range [2, 18].
Each of the above factors has influenced prairie dog and ferret populations. Discuss the importance of each of these factors in the decline of black-footed ferret populations.
Sylvatic Plague, Also Known As “Black Death”
Sylvatic plague is caused by the bacterium, Y. pestis, and it was this bacterium that was responsible for pandemic outbreaks of plague in the human population, such as the Black Death in medieval Europe . Y. pestis is not native to North America so how did the Black Death bacterium end up in prairie dog colonies? It hitched its way on ships and was first identified in the United States in 1899 . Although ships on both coasts harbored Y. pestis, plague only became established on the west coast, and by 1908 had spread through fleas from introduced rats (Rattus spp.) to native California ground squirrels (Spermophilus beecheyi); by the 1930s, plague had spread to prairie dogs . Today, plague in North America has a much greater impact on wildlife than on humans, who can be treated with antibiotics when infected.
In areas with the longest history of plague, the prairie dog colonies are smaller, more dispersed, less stable, occupy a lower percentage of suitable habitat, and are less likely to be recolonized after plague-induced colony collapse [2, 18]. These colony conditions slow the spread of plague but are the opposite to those that make an ideal ferret reintroduction site. In other words, the best sites for black-footed ferrets—large, densely populated prairie dog colonies with nearby colonies for easy dispersal—may also be the most susceptible to plague outbreaks .
Controlling plague has become a high priority in the black-footed ferret recovery plan. Vaccines have been developed for both species, and prairie dog colonies are “dusted” with the insecticide deltamethrin to kill fleas that carry plague. Treated colonies are less susceptible to colony collapse than untreated colonies . Dusting colonies for fleas provides apparent protection against plague even to unvaccinated ferrets . Unfortunately, deltamethrin is non-specific and kills all arthropods which make their homes in the prairie dog burrows, so its widespread use could have ecosystem-level impacts.
What are some of the benefits and drawbacks to the different strategies for controlling plague?
Ferrets Presumed Extinct
The decline of prairie dogs decimated black-footed ferret populations . By the late 1950s, there were no observations of wild ferrets, and the species was presumed extinct . However, in 1964, ferrets were rediscovered in South Dakota. Nine ferrets were recruited into a captive breeding program; unfortunately, the program failed, and the species was declared extinct again . Two years later, a ranch dog in Wyoming killed a black-footed ferret; again, the species was rediscovered . When canine distemper threatened this population, the remaining 18 individuals were brought into captivity, but only seven reproduced [3, 19]. This captive breeding program was successful and is the source for our current ferret populations; all living black footed ferrets are descended from the initial seven individuals [3, 24, 25].
What are some problems that might occur when a captive breeding program is based on only seven individuals?
Current Status and Protection
Black-footed ferrets are on the IUCN red list and categorized globally as endangered . They are listed federally as an endangered species under the U.S. Endangered Species Act , but most of the reintroduced wild populations are classified as “experimental/non-essential” . Black-footed ferrets are considered extirpated within Canada under Canada’s Species at Risk Act  and they have no official designation in Mexico, although several ferret reintroductions have taken place in Mexico .
In contrast, black-tailed prairie dogs have mixed levels of protection. They are categorized as “threatened” and protected in both Canada  (Box 1) and Mexico [29, 30], but black-tailed prairie dog eradication efforts continue in the United States . In states like Colorado, where prairie dogs are common at the wildland-urban interface, conflicts include property damage and potential exposure of humans and their pets to sylvatic plague, adding to the perception that prairie dogs are pests .
Black-tailed prairie dogs reach their northernmost extent in Southern Canada where they experience the shortest growing season and harshest winter conditions throughout their range . This is the only location where prairie dogs have been recorded to use extensive hibernation to survive winter . The Canadian population of prairie dogs consists of just 18 colonies located in and near Grasslands National Park, Saskatchewan . Consequently, Canadian black-tailed prairie dogs are listed as “threatened” and protected under Canada’s Species at Risk Act . A protected population of prairie dogs in a protected area sounds like the perfect location to reintroduce black-footed ferrets. Ferrets were first released into Grasslands National Park in 2009 with subsequent releases in the following years . In total, 79 captive-bred ferrets were released and 13 kits were born in the wild . However, plans to establish a self-sustaining ferret population have been stalled since the discovery of sylvatic plague in the park’s prairie dogs in 2010. For now, further ferret reintroductions in Canada are on hold.
CAPTIVE BREEDING AND REINTRODUCTION CHALLENGES
Captive breeding programs aim to maintain maximum genetic diversity of a species. Low genetic diversity means that many individuals carry the same alleles (gene variants) for most gene loci resulting in reduced fecundity and increased vulnerability to both genetic and infectious diseases, therefore decreasing survival . The seven ferrets that started the captive population would not have carried all the gene variants of the original population, so this population bottleneck reduced the genetic diversity of the species [24, 25, 28]. Using specific genetic markers, scientists compared the current diversity of ferrets to that of museum specimens collected before the population bottleneck to understand how this species’ genetic diversity has changed over time [24, 25]. Small reintroduced populations are at risk of losing further genetic diversity because not all individuals breed successfully. To combat these losses, additional captive-bred ferrets are added to the reintroduced population on an annual basis until the population stabilizes (usually at 200+ individuals ). Black-footed ferret recovery plans suggest a minimum of 3,500 ferrets are needed for a sustainable wild population .
One of the challenges with captive breeding programs is identifying release locations. It is important to consider all aspects of the ecology of the system to ensure the best chances for a successful reintroduction. Current and future land use, species and habitat management, and larger socio-environmental impacts all need consideration.
The Fort Belknap Indian Reservation in Montana, a black-footed ferret release site, provides public data about their prairie dog colonies, which are integral to ferret survival (Table 1) . Researchers estimate that there are 17–42 prairie dogs per hectare . An adult ferret consumes more than 100 prairie dogs per year, and reproductive females have higher energetic needs . Additionally, because female ferrets are territorial, it is unusual to find more than one female ferret per 25 ha . The prairie dog population must be large enough to allow for predation losses; sustainable losses must be less than 25% of the population . While exact ecosystem dynamics are difficult to predict, estimates help identify which prairie dog colonies can potentially support black-footed ferrets.
|Colony size (ha) .||Number of colonies .|
|Colony size (ha) .||Number of colonies .|
Many collaborators work together for successful breeding and reintroduction. Black-footed ferrets are captively bred at the National Black-footed Ferret Conservation Centre in Wellington, Colorado and the Toronto Zoo in Toronto, Ontario Canada. These organizations work with managers of private, public, and Tribal lands to identify reintroduction sites and monitor reintroduced populations. Since 1991, ferrets have been released at 28 locations in Montana, South Dakota, Wyoming, Colorado, Nebraska, Arizona, New Mexico, Southern Canada, and Northern Mexico .
The majority of prairie dog colonies are the smallest size (0–24 ha, Table 1). What role, if any, could these small colonies play in a black-footed ferret reintroduction program?
As with any issue, black-footed ferrets and black-tailed prairie dogs exist within a larger social-environmental context. Some conflicts have already been discussed in this case, but there are many others. Conflict stems from different opinions about desired land use, private property rights, disease exposure, and cost of conservation and re-introduction. An important part of ecology and natural resource management is being able to integrate data across social and environmental fields.
Prairie dogs have long been considered a pest species in need of eradication. Many people who live near prairie dogs have negative attitudes about them; those that directly interact with prairie dogs (e.g., ranchers and rural residents) are more likely to view them negatively than those without direct contact (e.g., urban residents ). Concerns include: (1) financial loss from crop consumption, (2) potential livestock injury and farm equipment damage, (3) perceptions that prairie dogs symbolize poor land management, (4) wildlife management and conservation may lead to a loss of control and restrictions on public and private grazing lands, (5) fear that burrows will drain water from already arid fields, and (6) prairie dog conservation will threaten rural western lifestyles .
Property rights of private landowners are a major issue in conservation management. The Western United States has a long history of valuing private landowner rights, and many are skeptical of legislation that limits the actions of landowners. “Shoot, shovel, and shut-up” has become notorious, a practice where landowners kill protected species to prevent them from being discovered; if found on their land, owners must manage their land to provide habitat needs and protection for these species . The expansion of the urban landscape and the increasing number of homes in rural areas also increase the wildland-urban interface, leading to conflict with homeowners who may expect a more urban experience in a rural landscape . For these homeowners, yards full of prairie dog holes, and plague exposure are additional concerns .
What are some strategies to mitigate some of these conflicts? How can conservation managers generate public support for reintroduction programs?
The management of black-footed ferrets and black-tailed prairie dogs exemplifies the complexities of conservation biology in our current society. Not only do we need a solid understanding of the science but also it is important to consider social aspects of a problem. To effectively manage endangered species, including black-footed ferrets, we need to understand scientific issues, such as threats to genetic diversity and the ecology of the area, while at the same time considering public risk and stakeholder perspectives. With complex problems that span both social and ecological realms, it is important that we ensure decision-makers consider all aspects of multi-faceted problems, so that research can target key problems that reflect ecological knowledge and balancing the needs and concerns of stakeholders.
CASE STUDY QUESTIONS
Captive breeding programs are often used as a last resort to save endangered species.
Identify some challenges or concerns of the black-footed ferret captive breeding program. List the possible threats to maintaining a sustainable, reproductively healthy population of black-footed ferrets. For each threat that you identify, what are some strategies that could be used to mitigate their negative effects?
In their search for suitable habitat, prey, and mates, ferrets will disperse across state or national borders and will access private, public, and tribal lands. The ferrets respond to the physical environment, whereas land ownership and jurisdictional boundaries are human constructs. Nonetheless, land management is greatly influenced by ownership and jurisdiction. What are some of the transboundary management issues that will need to be addressed to create a self-sustaining wild ferret population? Can you think of any examples in which land ownership might influence ferret habitat choice?
Use Figure 1 and Table 1, and, if available, the Interactive Maps available at https://tinyurl.com/ ESRI-ferrets to explore the spatial relationships between historical and present ranges of black-footed ferrets and black-tailed prairie dogs. Note that the base map for Interactive Maps 3 and 4 shows native grassland habitat in green and cultivated land in pale yellow.
Historic ranges: How does the historical range of black-footed ferrets compare to the historical range of black-tailed prairie dogs (Figure 1; Interactive Map 1)? Given the ferrets’ dependence on prairie dogs, how do you explain the presence of ferrets outside of the historical range of black-tailed prairie dogs?
Best sites for ferret reintroduction: Table 1 and Interactive Map 4 provide information on the size of prairie dog colonies on the Fort Belknap Reservation.
If the Interactive Map is available, based only on colony size, locate the best three sites to release captive bred ferrets? What are the sizes of these three colonies in hectares?
Other than size, what other factors should be considered when identifying possible release sites? If the Interactive Map is available, consider if the desirability of potential release sites changes from what you proposed in (i).
What types of monitoring are important following release of ferrets? How might adjacent land ownership and land use influence release site selection?
How does the territorial nature of ferrets influence the number of reproductive females that each of these sites can support? Estimate the number of reproductive females that each of the three largest colonies could support.
What might be the effect of introducing a keystone species into an environment that has changed since the species was last present?
It is important to consider more than basic biology and ecology in species conservation. If you were involved in a black-footed ferret release program, what ways could you address the complex socio-environmental issues involved? There are many examples of problematic natural resource management, where managers simply made decisions without consulting those affected and knowledgeable about the system, including local landowners.
Stakeholder engagement: Identify all the stakeholders (everyone who can influence or will be influenced by the situation) and determine how you could involve different stakeholder groups in the decision-making process.
What would be the pros and cons of different forms of engagement (e.g., townhall meetings, online surveys)?
Is it appropriate to use different engagement tools for different stakeholder groups? Why or why not?
Do all stakeholders need to be involved in decision-making? If not, which ones need to be involved and why? At what point should you involve these stakeholders in the decision-making process?
Stakeholder concerns: List the potential concerns of each stakeholder group identified above.
Are the concerns economic, social, or environmental?
What role might peer pressure play in an individual’s decisions about reintroduction in their area?
How could a ferret reintroduction program impact the cohesiveness of a local rural community?
Mitigating concerns: How can you mitigate stakeholder concerns?
What are some of the particularly challenging components of this situation? Will you be able to address the concerns of all the stakeholders?
Should there be a guarantee of economic compensation if stakeholders’ livelihoods are negatively impacted by a reintroduction in their area? Should there be economic compensation for a reintroduction on your land and managing the prairie dogs to support it? Who pays this? Is public gratitude and recognition enough?
Currently, many landowners view having any species at risk on their land as a liability because it limits how they can use and manage their property, and that can be economically costly for them. How do we encourage landowner stewardship of endangered species and habitat?
All three authors, A.M.A.C., D.P.H., and M.K.R., participated in conceptualization, writing, reviewing, and editing of this article.
We thank The National Environmental Socio-Environmental Synthesis Center (SESYNC) and Dr. Cynthia Wei for help in initially developing this case through their case study development short course. Tara Stephens and Sian Wilson of the Centre for Conservation Research, Calgary Zoological Society, Alberta, Canada, provided valuable background information and insights into the challenges of reintroducing black-footed ferrets.
The National Center for Socio-Environmental Synthesis (SESYNC) provided funding for each of the authors to attend a short course on “Teaching Socio-Environmental Synthesis with Case Studies.” The conceptualization and initial development of this project occurred during this workshop.
The authors have declared that no competing interests exist.
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