Site (year initiated)
Prairie dog speciesa
Land ownership
Total # BFFs released
Estimated 2012 population
1Shirley Basin, WY (1991)
Wtpd
Private, federal, state
513
239 (2009)
2UL Bend Natl. Wild. Refuge, MT (1994)
Btpd
Federal
252
18
3Badlands Natl. Park, SD (1994)
Btpd
Federal
225
30
4Aubrey Valley, AZ (1996)
Gpd
Tribal, private
399
123b
5Conata Basin, SD (1996)
Btpd
Federal
161
72
6Fort Belknap Indian Reservation, MT (1997)
Btpd
Tribal
180
0
7Coyote Basin, UT (1999)
Wtpd
Federal
424
10b
8Cheyenne River Indian Reservation, SD (2000)
Btpd
Tribal
350
26b
9BLM 40-Complex, MT (2001)
Btpd
Federal
92
0
10Wolf Creek, CO (2001)
Wtpd
Federal
254
0
11Janos, Mexico (2001)
Btpd
Private, community
299
17 (2006)
12Rosebud Indian Reservation, SD (2003)
Btpd
Tribal
150
30 (2006)
13Lower Brule Indian Reservation, SD (2006)
Btpd
Tribal
107
25b
14Wind Cave Natl. Park, SD (2007)
Btpd
Federal
61
67
15Espee Ranch, AZ (2007)
Gpd
Private
70
0
16Butte Creek/Smoky Valley Ranch, KS (2007)
Btpd
Private
125
39b
17Northern Cheyenne Indian Reservation, MT (2008)
Btpd
Tribal
88
0
18Vermejo Park Ranch, NM
Btpd
Private
255
5b
19Grasslands Natl. Park, Canada (2009)
Btpd
Federal
75
12b
20Vermejo Park Ranch, NM (2012)
Gpd
Private
20
11
Total
4,100
2 Management of the Black-footed Ferret Recovery Program
The Black-footed Ferret Species Survival Plan® (SSP) collectively manage a core breeding population and house a small group of ferrets not suitable for reintroduction. The SSP’s primary goal is to produce as many black-footed ferret kits as possible in order sustain future captive breeding and supply excess captive-born animals for ongoing reintroduction efforts (Garelle et al. 2012). Since 2000, six facilities across North America comprise the SSP, including: the USFWS’s National Black-footed Ferret Conservation Center (Colorado), Smithsonian Conservation Biology Institute (Virginia, of the Smithsonian’s National Zoological Park), Louisville Zoological Garden (Kentucky), Cheyenne Mountain Zoo (Colorado), Phoenix Zoo (Arizona) and Toronto Zoo (Ontario, Canada). The number and demography of the SSP population has been maintained at relatively consistent levels since the late 1990s; however, new genetic software programs have altered decision making processes surrounding pairings and identifying reintroduction candidates. Prioritizing or determining which male should be paired with each female is accomplished using MateRx (Ballou et al. 2001). This analytical software program, developed jointly by the Smithsonian National Zoological Park (Washington, DC) and Lincoln Park Zoo (Chicago, IL) provides captive breeding facilities a numerical rating for every possible breeding pair. These ratings or Mate Suitability Indices (MSI) integrate several genetic factors, including the expected change in genetic diversity due to resultant offspring, the relative rareness or commonness of the parent’s genetic make-up, inbreeding coefficient of offspring produced by a pair, and proportion, if any, of unknown pedigree (Garelle et al. 2012). The target number of ferrets allocated to reintroduction sites is determined by the USFWS prior to the annual SSP Master Planning meeting. Dynamic culling is utilized to designate individuals for release until the desired age and sex structure for the SSP is attained. A collaborative workshop sponsored by USFWS, the Black-footed Ferret Recovery Implementation Team (BFFRIT) and CBSG was held in 2003 and addressed recovery challenges facing captive and field populations.
Black-footed ferrets were extinct in the wild by 1987 after the remaining 18 were removed and placed into captivity. Successful captive breeding efforts have produced enough kits that wild reintroductions began in 1991 and have continued today. Partners and sites request black-footed ferrets from the USFWS through an annual allocation process (Jachowski and Lockhart 2009). Initial years of reintroduction focused on rearing and acclimation strategies (Biggins et al. 1998), habitat selection and use and techniques to monitor populations. Recent efforts have shifted towards disease management/mitigation in addition to finding and developing new release sites. Reintroduction sites occur on a variety of land ownership patterns including federal, state, tribal and private lands in eight US States, Mexico and Canada (Table 7.1; Fig. 1).
A site in Chihuahua, Mexico, at the southernmost portion of the black-footed ferret range, is within the Janos Biosphere Reserve (List et al. 2010) and includes private and community-owned lands. This site once contained the largest remaining complex of black-tailed prairie dogs (i.e. black-footed ferret habitat) in contemporary North America, but extreme drought has caused degradation and desertification of much of those grasslands. In recent years area drug violence has prevented biologists from assessing the status of reintroduced black-footed ferrets at the Mexico site.
Tribal lands are important for black-footed ferret recovery and account for seven of the 20 black-footed ferret reintroduction sites. Releases on private lands in Wyoming, Arizona, Kansas and New Mexico have also occurred and private land partnerships are regarded as vital to ultimate recovery success. Eco-capitalist Ted Turner and the Turner Endangered Species Fund have put considerable effort into prairie dog restoration and subsequent releases of black-footed ferrets onto his Vermejo Park Ranch in New Mexico. With the release of black-footed ferrets into Grasslands National Park, Saskatchewan in 2009, black-footed ferrets were returned to the Canadian prairies, near the northern limit of their historical range.
A total of 4,100 black-footed ferrets were released 1991–2012 with 213 of those being of wild origin, captured, and translocated to other reintroduction sites. Wild kits used for direct translocation originated primarily from Conata Basin, South Dakota prior to the spread of plague into that population and subsequent site impacts. Translocation of wild black-footed ferrets has been a successful tool, and is regarded as one of the most effective means of initiating new reintroduction projects or supplementing existing sites (Biggins et al. 2001). Five of 20 reintroduction sites are currently considered devoid of black-footed ferrets, mostly because of plague, but may be re-considered if plague can be mitigated.
Within reintroduction sites, we observed both genotypic and phenotypic differences based on the length of time of population persistence since captive-born black-footed ferrets were first released, and if subsequent augmentations of captive-reared ferrets occurred. Based on nine microsatellite loci, the Wyoming reintroduction site, which had a slow establishment and population growth and had not been augmented with captive black-footed ferrets for >10 years, had reduced heterozygosity and fewer polymorphic loci compared with the Conata Basin, South Dakota reintroduced population (rapid population growth following initial establishment and augmentation within the last 5 years) and Aubrey Valley, Arizona (yearly augmentation). The Wyoming black-footed ferrets also had phenotypic changes, specifically shorter limbs and smaller overall body size, than other three populations (Wisely et al. 2007).
Previous morphological research demonstrated that captive black-footed ferrets were on average 4–10 % smaller and differently shaped based on skull morphology than historical museum specimens (Wisely et al. 2002). Because captive black-footed ferrets are the source population of all reintroduced black-footed ferrets, we expected that wild-born black-footed ferrets would be smaller than historical specimens; however, it was recently determined that wild-born individuals from reintroduction areas were 2–5 % larger than their captive-born counterparts and had returned to historical size, suggesting that reduced size was an environmental not a genetic effect (Wisely et al. 2005). Interestingly, based on these morphometric data, it was also determined that canine width can be used to age black-footed ferrets, which assists with demographic assessments of reintroduction sites (Santymire et al. 2012). These results demonstrate the importance of monitoring the genetic health and signs of inbreeding in the wild populations so that management strategies, such as translocation or augmentation with additional captive black-footed ferrets, can be employed.
3 Disease Management
Disease has limited the sustainability of both captive and wild black-footed ferret populations. Specifically, CDV has long been known to cause morbidity and mortality in this species, and contributed to the decline of the original Meeteetse population. Black-footed ferrets in captivity also succumbed to CDV (Williams et al. 1998), and others administered a modified-live CDV vaccine died from vaccine-induced infection (Carpenter et al. 1976). Even with supportive care, the mortality rate of CDV approaches 100 %. PureVax® Ferret Distemper Vaccine, a live, monovalent canarypox-vectored vaccine developed by Merial, Inc., Athens, GA, has proven safe and effective in the Siberian polecat (Wimsatt et al., 2003) and has been subsequently tested in the black-footed ferret. These trials have indicated that a minimum of two doses of vaccine produce protective neutralizing antibody titers (Marinari and Kreeger 2004). Currently, all captive born ferrets and many wild ferrets receive two doses of PureVax® Ferret Distemper Vaccine beginning as early as 60 days of age.
Plague is caused by the bacterium Yersinia pestis. It can be transmitted via flea vector, aerosol or ingestion of contaminated food. Plague entered North America’s west coast in the early 1900s via ships carrying flea-infested rats. It has since been spreading eastward, infecting and killing many native species, including prairie dogs and black-footed ferrets. Interestingly, the domestic ferret appears resistant to plague (Williams et al. 1994), and it was initially believed that the black-footed ferret was as well. But in the 1990s, high susceptibility (with virtually 100 % mortality) to plague was discovered by Williams et al. (1994) and later affirmed by others (Rocke et al. 2004). This led to substantial research into developing a plague vaccine. The U.S. Geological Survey’s National Wildlife Health Center (Madison, WI) in collaboration with United States Army Medical Research Institute for Infectious Diseases (Frederick, MD) was instrumental in developing a vaccine consisting of the plague antigens F1 and V (Rocke et al. 2004). Challenge studies were conducted using two doses of F1-V vaccine, with a 69 % survival rate (Rocke et al. 2004). Now, all captive born and many wild black-footed ferrets are given two doses of F1-V vaccine as part of the recovery management strategy. Unfortunately, vaccination of black-footed ferrets alone is insufficient to eliminate the threat of plague. A major obstacle to black-footed ferret recovery is the high susceptibility and wholesale loss of large prairie dog populations to plague, making control of this disease, both for predator and prey, a high priority. The BFFRIT is currently working with partners on the development of a safe and effective, oral bait plague vaccine for prairie dogs.
Direct manipulation of fleas has been an effective but labor intensive method to manage plague in the wild. Application of powdered insecticides directly into prairie dog burrows can be an effective short term solution but many of these chemicals lose their effectiveness quickly (Barnes et al. 1972; Karhu and Anderson 2000). More recently, the chemical deltamethrin, formulated into a waterproof dust as DeltaDust, has demonstrated protection of both prairie dog and black-footed ferrets for up to 10 months post-application (Biggins et al. 2010; Matchett et al. 2010). Dusting however is labor intensive, costly and has potential secondary effects on non-target species (Cully et al. 2006). Recent evidence from Conata Basin, South Dakota suggests that dusting alone may not be sufficient to maintain black-footed ferret populations during a plague epizootic and vaccination of black-footed ferrets with F1-V significantly increases survivorship in dusted prairie dog colonies (Livieri pers. comm.).
4 Advanced Assisted Reproductive Technology
With over 20 years of development, assisted reproductive technology has maintained the genetic diversity of the black-footed ferret captive population. Specifically, from 1996 through 2008, nearly 140 individuals have been produced through artificial insemination using fresh or frozen/thawed semen (Howard and Wildt 2009). These offspring are from sires that would not have breed naturally due to behavioral problems and/or were given multiple chances to breed on their own, but failed to produce a litter (Howard and Wildt 2009). Excitingly, frozen/thawed semen from the black-footed ferret GRB that had been stored for greater than 10 years was used successfully in two AI procedures resulting in two genetically valuable kits (Howard and Wildt 2009). These successful AIs clearly demonstrate that the black-footed ferret GRB is an integral part of the recovery and conservation program. In response to these successful breeding, efforts are being made to improve semen cryopreservation techniques. Specifically, it was determined that black-footed ferrets produce ejaculates with high osmolality (~500 mOsm) compared to serum levels (320 mOsm; Santymire et al. 2006), and compared to semen osmolality (~300 mOsm) from an array of other species (boar, bull, dog, cat, human, stallion, birds species; Gao et al. 1997; Blanco et al. 2000; Pukazhenthi et al. 2000). Black-footed ferret spermatozoa have also demonstrated sensitivity to osmotic stress with hyperosmotic conditions resulting in reduced sperm motility and acrosomal integrity (Santymire et al. 2006). Additionally, when designing a black-footed ferret specific semen cryopreservation protocol, it was determined that the spermatozoa were sensitive to cooling (from 37 to 4 °C) and required a slower rate (0.12 °C/min; Santymire et al. 2007) than what was previously used (0.20 °C/min; Atherton et al. 1989). Furthermore, it was demonstrated that an egg yolk based medium used with a pellet method of freezing achieved the highest post-thaw sperm viability in domestic ferrets (Howard et al. 1991) and black-footed ferrets (Santymire et al. 2007).