Dean E. Biggins

INFLUENCES OF INTRODUCED PLAGUE ON NORTH AMERICAN MAMMALS: IMPLICATIONS FROM ECOLOGY OF PLAGUE IN ASIA

Abstract Intercontinental movements of invasive species continue to modify the worlds ecosystems. The plague bacterium (Yersinia pestis) has colonized and altered animal communities worldwide but has received much more attention as a human pathogen. We reviewed studies on the ecology of Y. pestis in ancient foci of central Asia and in western North America, where the bacterium apparently has become established much more recently. Although rodent populations on both continents are affected dramatically by epizootics of plague, the epidemiologically important species of Asia demonstrate resistance in portions of their populations, whereas those of North America are highly susceptible. Individual variation in resistance, which is widespread in Asian rodents and allows a microevolutionary response, has been documented in few North American species of rodents. Plague increases costs of sociality and coloniality in susceptible hosts, increases benefits of disease resistance in general, and increases benefits of adaptability to variable environments for species at higher trophic levels. Prairie dogs (Cynomys) epitomize taxa with high risk to plague because prairie dogs have uniformly low resistance to plague and are highly social. Relationships to plague are poorly understood for many North American rodents, but more than one-half of the species of conservation concern occur within the geographic range of plague.

Influence of prerelease experience on reintroduced black-footed ferrets (Mustela nigripes)

Captive breeding is increasingly being used to create supplies of endangered animals for release into natural habitats, but rearing strategies vary and debates arise over which methods are most eAcient. We assessed postrelease behaviors and survival of three groups of black-footed ferrets, each with diAerent prerelease experience. Eighteen ferret kits60 days of age were moved with their dams from cages to 80-m 2 outdoor pens with prairie dog burrows. These animals were compared to animals reared in standard cages (na 72), some of which were given experience killing prairie dogs (na 32). Ferrets were released onto white-tailed prairie dog (Cynomys leucurus) colonies in Wyoming, USA, in fall, 1992. Radio-tagged cage-reared ferrets made longer nightly moves and dispersed further from release sites than their pen-reared counterparts. The band return rate was 4-fold higher for pen-reared animals than for cage-reared animals during surveys conducted about 1 month after release. We recommend routine use of quasinatural outdoor pens for prerelease conditioning of black-footed ferrets. Published by Elsevier Science Ltd.

The effect of rearing methods on survival of reintroduced black-footed ferrets

We estimated minimum survival rates for 282 young-of-year, captive-reared, black-footed ferrets (Mustela nigripes) reintroduced into prairie dog (Cynomys spp.) colonies in Wyoming, Montana, and South Dakota. We used night surveys with spotlights to locate ferrets about 1 month and 9 months postrelease. We modeled minimum survival rates using gender, year, site, and 4 rearing methods. Minimum survival rates were highest (30% for 1 month, 20% for 9 months) for ferrets reared from early ages in outdoor pens with simulated prairie dog habitat; survival was lowest for cage-reared ferrets released without pen experience (11% for 1 month, 2% for 9 months). Rearing method and year influenced 1-month survival in a comparison of 3 levels of pen experience (pen rearing as defined above, transfer of kits from zoos to pen facilities at age 60-90 days, transfer at age >90 days) during releases in 1994-95 in Montana. Higher survival was associated with intensive management of coyotes (Canis latrans) in 1995. Survival was not different (P > 0.05) between sites or sexes, regardless of model. We recommend routine use of outdoor pens for prerelease conditioning of black-footed ferret kits.

Population attributes for the black-footed ferret (Mustela nigripes) at Meeteetse, Wyoming, 1981-1985

Numbers of adults and juveniles in the single known free-ranging population of the endangered black-footed ferret ( Mustela nigripes ) at Meeteetse, Wyoming were estimated annually in July from spotlighting as 88 (1983), 129 (1984), and 58 (1985). Population sizes in September, determined from mark-recapture studies, were 128 ± 25 (1984) and 31 ± 8 (1985). Lower population estimates in 1985 reflected, at least in part, an ongoing epizootic of canine distemper in ferrets that decimated the population through November 1985, reducing it to ca. 6 individuals. From 1982 to 1985, adult sex ratio was 1 male: 2.2 females; juvenile sex ratio (1 male: 0.80 females) did not differ significantly from 1:1. The ratio of young to adults averaged 1.95:1 from 1982 to 1984 and 1.2:1 in 1985. At least 224 young were produced in 68 litters from 1982–1985, with a mean litter size at emergence of young of 3.3. Juvenile ferrets reached adult weight by September. Only one female tagged as a juvenile was recaught at 1 year of age, and she reproduced. Intercolony movements were primarily by juvenile males and occurred from September to October. Adults maintained geographic fidelity between years. Disappearance (mortality and emigration) rates ranged from 53 to 86% annually and were highest for juveniles. Observed ferret mortality in the absence of disease was primarily from predation. Reduction of the population during the epizootic suggests persistence of this population in the wild is unlikely.

A proposal to conserve black-footed ferrets and the prairie dog ecosystem

Prairie dogs (Cynomys spp.) have been poisoned throughout this century because of grazing competition with livestock. Recent evidence showed these early claims were exaggerated, but animal control was already entrenched in government policy. As a result, ongoing government subsidized poisoning has reduced prairie dogs to about 2% of their former distribution. The reduction of prairie dogs diminished species diversity in the arid grasslands of North America, including the potential extinction of the black-footed ferret (Mustela nigripes). Cost-benefit analysis revealed that poisoning costs more than any grazing benefits accrued. This analysis did not consider the long-term costs of reversing ecosystem degradation, the intangible value of biological diversity as a public benefit, or the depletion of biotic resources as a loss of actual or potential wealth. The government presently finances the poisoning policy and the preservation of endangered species like the black-footed ferret, two apparently conflicting programs. We, therefore, propose an integrated management plan that considers both interests. We propose that federal monies allocated to the poisoning program be converted into a rebate for ranchers who manage livestock while preserving the prairie dog community. This would redirect funds and personnel already allocated to prairie dog eradication to an incentive for ranchers who manage for livestock and wildlife. Livestock interests and grassland biotic diversity would both benefit.

Vector Control Improves Survival of Three Species of Prairie Dogs (Cynomys) in Areas Considered Enzootic for Plague

Plague causes periodic epizootics that decimate populations of prairie dogs (PDs) (Cynomys), but the means by which the causative bacterium (Yersinia pestis) persists between epizootics are poorly understood. Plague epizootics in PDs might arise as the result of introductions of Y. pestis from sources outside PD colonies. However, it remains possible that plague persists in PDs during interepizootic periods and is transmitted at low rates among highly susceptible individuals within and between their colonies. If this is true, application of vector control to reduce flea numbers might reduce mortality among PDs. To test whether vector control enhances PD survival in the absence of obvious plague epizootics, we reduced the numbers of fleas (vectors for Y. pestis) 96-98% (1 month posttreatment) on 15 areas involving three species of PDs (Cynomys leucurus, Cynomys parvidens in Utah, and Cynomys ludovicianus in Montana) during 2000-2004 using deltamethrin dust delivered into burrows as a pulicide. Even during years without epizootic plague, PD survival rates at dusted sites were 31-45% higher for adults and 2-34% higher for juveniles compared to survival rates at nondusted sites. Y. pestis was cultured from 49 of the 851 flea pools tested (6882 total fleas) and antibodies against Y. pestis were identified in serum samples from 40 of 2631 PDs. Although other explanations are possible, including transmission of other potentially fatal pathogens by fleas, ticks, or other ectoparasites, our results suggest that plague might be maintained indefinitely in PD populations in the absence of free epizootics and widespread mortality among these animals. If PDs and their fleas support enzootic cycles of plague transmission, there would be important implications for the conservation of these animals and other species.

Reintroduction of the black-footed ferret ( Mustela nigripes )

The black-footed ferret (Mustela nigripes) (Figure 27.1) is a small, secretive, nocturnal member of the family Mustelidae (Hall, 1981; Honacki, Kurman and Koeppl, 1982). Ferrets have an obligate dependence on the prairie dog (Cynomys spp.) community, utilizing the prairie dog for food and its burrows for shelter (Campbell et al., 1987).

Treatment of black-tailed prairie dog burrows with deltamethrin to control fleas (Insecta: Siphonaptera) and plague

Abstract Burrows within black-tailed prairie dog (Cynomys ludovicianus) colonies on the Rocky Mountain Arsenal National Wildlife Refuge, Colorado, were dusted with deltamethrin insecticide to reduce flea (Insecta: Siphonaptera) abundance. Flea populations were monitored pre- and posttreatment by combing prairie dogs and collecting fleas from burrows. A single application of deltamethrin significantly reduced populations of the plague vector Oropsylla hirsuta, and other flea species on prairie dogs and in prairie dog burrows for at least 84 d. A plague epizootic on the Rocky Mountain Arsenal National Wildlife Refuge caused high mortality of prairie dogs on some untreated colonies, but did not appear to affect nearby colonies dusted with deltamethrin.

Development of survival skills in captive-raised Siberian polecats ( Mustela eversmanni ) II: predator avoidance

We exposed naive Siberain polecats (Mustela eversmanni) (aged 2, 3, and 4 months) to a swooping stuffed great horned owl (Buho virginianus) and a stuffed badger (Taxidae taxus) mounted on a remote control toy automobile frame. The first introduction to each was harmless, the second was accompanied by a mild aversive stimulus, the third (1 day after attack) was harmless, and the fourth (30 days after attack) was harmless. Alert behavior increased after a single attack by either predator model. Escape responses of naive polecats did not differ between ages when exposed to the badger, but 4 month old polecats reduced their escape times after a single badger attack. When exposed to the swooping owl, naive 4 month old polecats redponded more quickly than the other two age groups, and 3 and 4 month old polecats reduced escape times after a single owl attack. This indicates an innate escape response to the owl model at 4 months of age, and a short-tert ability to remember a single mild aversive encounter with the badger and owl models at 3 or 4 months of age.

Enzootic Plague Reduces Black-Footed Ferret (Mustela nigripes) Survival in Montana

Black-footed ferrets (Mustela nigripes) require extensive prairie dog colonies (Cynomys spp.) to provide habitat and prey. Epizootic plague kills both prairie dogs and ferrets and is a major factor limiting recovery of the highly endangered ferret. In addition to epizootics, we hypothesized that enzootic plague, that is, presence of disease-causing Yersinia pestis without any noticeable prairie dog die off, may also affect ferret survival. We reduced risk of plague on portions of two ferret reintroduction areas by conducting flea control for 3 years. Beginning in 2004, about half of the ferrets residing on dusted and nondusted colonies were vaccinated against plague with an experimental vaccine (F1-V fusion protein). We evaluated 6-month reencounter rates (percentage of animals observed at the end of an interval that were known alive at the beginning of the interval), an index to survival, for ferrets in four treatment groups involving all combinations of vaccination and flea control. For captive-reared ferrets (115 individuals observed across 156 time intervals), reencounter rates were higher for vaccinates (0.44) than for nonvaccinates (0.23, p = 0.044) on colonies without flea control, but vaccination had no detectable effect on colonies with flea control (vaccinates = 0.41, nonvaccinates = 0.42, p = 0.754). Flea control resulted in higher reencounter rates for nonvaccinates (p = 0.026), but not for vaccinates (p = 0.508). The enhancement of survival due to vaccination or flea control supports the hypothesis that enzootic plague reduces ferret survival, even when there was no noticeable decline in prairie dog abundance. The collective effects of vaccination and flea control compel a conclusion that fleas are required for maintenance, and probably transmission, of plague at enzootic levels. Other studies have demonstrated similar effects of flea control on several species of prairie dogs and, when combined with this study, suggest that the effects of enzootic plague are widespread. Finally, we demonstrated that the experimental F1-V fusion protein vaccine provides protection to ferrets in the wild.