High prevalence of <Emphasis Type="Italic">Yersinia pestis</Emphasis> in black-tailed prairie dog colonies during an apparent enzootic phase of sylvatic plague

Sylvatic plague (Yersinia pestis) was introduced into North America over 100 years ago. The disease causes high mortality and extirpations in black-tailed prairie dogs (Cynomys ludovicianus), which is of conservation concern because prairie dogs provide habitat for the critically endangered black-footed ferret (Mustela nigripes). Our goal was to help elucidate the mechanism Y. pestis uses to persist in prairie ecosystems during enzootic and epizootic phases. We used a nested PCR protocol to assay for plague genomes in fleas collected from prairie dog burrows potentially exposed to plague in 1999 and 2000. No active plague epizootic was apparent in the 55 prairie dog colonies sampled in 2002 and 2003. However, 63% of the colonies contained plague-positive burrows in 2002, and 57% contained plague-positive burrows in 2003. Within plague-positive colonies, 23% of sampled burrows contained plague-positive fleas in 2002, and 26% contained plague-positive fleas in 2003. Of 15 intensively sampled colonies, there was no relationship between change in colony area and percentage of plague-positive burrows over the two years of the study. Some seasonality in plague prevalence was apparent because the highest percentages of plague-positive colonies were recorded in May and June. The surprisingly high prevalence of plague on study area colonies without any obvious epizootic suggested that the pathogen existed in an enzootic state in black-tailed prairie dogs. These findings have important implications for the management of prairie dogs and other species that are purported to be enzootic reservoir species.     

Sylvatic plague reduces genetic variability in black-tailed prairie dogs

Small, isolated populations are vulnerable to loss of genetic diversity through in-breeding and genetic drift. Sylvatic plague due to infection by the bacterium Yersinia pestis caused an epizootic in the early 1990s resullting in declines and extirpations of many black-tailed prairie dog (Cynomys ludovicianus) colonies in north-central Montana, USA. Plague-induced population bottlenecks may contribute to significant reductions in genetic variability. In contrast, gene flow maintains genetic variability within colonies. We investigated the impacts of the plague epizootic and distance to nearest colony on levels of genetic variability in six prairie dog colonies sampled between June 1999 and July 2001 using 24 variable randomly amplified polymorphic DNA (RAPD) markers. Number of effective alleles per locus (n(e)) and gene diversity (h) were significantly decreased in the three colonies affected by plague that were recovering from the resulting bottlenecks compared with the three colonies that did not experience plague. Genetic variability was not significantly affected by geographic distance between colonies. The majority of variance in gene fieqnencies was found within prairie clog colonies. Conservation of genetic variability in black-tailed prairie dogs will require the preservation of both large and small colony complexes and the gene flow amonog them.     

Burrow Dusting or Oral Vaccination Prevents Plague-Associated Prairie Dog Colony Collapse

Plague impacts prairie dogs (Cynomys spp.), the endangered black-footed ferret (Mustela nigripes) and other sensitive wildlife species. We compared efficacy of prophylactic treatments (burrow dusting with deltamethrin or oral vaccination with recombinant “sylvatic plague vaccine” [RCN-F1/V307]) to placebo treatment in black-tailed prairie dog (C. ludovicianus) colonies. Between 2013 and 2015, we measured prairie dog apparent survival, burrow activity and flea abundance on triplicate plots (“blocks”) receiving dust, vaccine or placebo treatment. Epizootic plague affected all three blocks but emerged asynchronously. Dust plots had fewer fleas per burrow (P < 0.0001), and prairie dogs captured on dust plots had fewer fleas (P < 0.0001) than those on vaccine or placebo plots. Burrow activity and prairie dog density declined sharply in placebo plots when epizootic plague emerged. Patterns in corresponding dust and vaccine plots were less consistent and appeared strongly influenced by timing of treatment applications relative to plague emergence. Deltamethrin or oral vaccination enhanced apparent survival within two blocks. Applying insecticide or vaccine prior to epizootic emergence blunted effects of plague on prairie dog survival and abundance, thereby preventing colony collapse. Successful plague mitigation will likely entail strategic combined uses of burrow dusting and oral vaccination within large colonies or colony complexes.     

Spread of plague among black-tailed prairie dogs is associated with colony spatial characteristics

Sylvatic plague (Yersinia pestis) is an exotic pathogen that is highly virulent in black-tailed prairie dogs (Cynomys ludovicianus) and causes widespread colony losses and individual mortality rates >95%. We investigated colony spatial characteristics that may influence inter-colony transmission of plague at 3 prairie dog colony complexes in the Great Plains. The 4 spatial characteristics we considered include: colony size, Euclidean distance to nearest neighboring colony, colony proximity index, and distance to nearest drainage (dispersal) corridor. We used multi-state mark–recapture models to determine the relationship between these colony characteristics and probability of plague transmission among prairie dog colonies. Annual mapping of colonies and mark–recapture analyses of disease dynamics in natural colonies led to 4 main results: 1) plague outbreaks exhibited high spatial and temporal variation, 2) the site of initiation of epizootic plague may have substantially influenced the subsequent inter-colony spread of plague, 3) the long-term effect of plague on individual colonies differed among sites because of how individuals and colonies were distributed, and 4) colony spatial characteristics were related to the probability of infection at all sites although the relative importance and direction of relationships varied among sites. Our findings suggest that conventional prairie dog conservation management strategies, including promoting large, highly connected colonies, may need to be altered in the presence of plague. © 2011 The Wildlife Society     

Prevalence of Yersinia pestis in rodents and fleas associated with black-tailed prairie dogs (Cynomys ludovicianus) at Thunder Basin National Grassland, Wyoming

Rodents (and their fleas) that are associated with prairie dogs are considered important for the maintenance and transmission of the bacterium (Yersinia pestis) that causes plague. Our goal was to identify rodent and flea species that were potentially involved in a plague epizootic in black-tailed prairie dogs at Thunder Basin National Grassland. We collected blood samples and ectoparasites from rodents trapped at off- and on-colony grids at Thunder Basin National Grassland between 2002 and 2004. Blood samples were tested for antibodies to Y. pestis F-1 antigen by a passive hemagglutination assay, and fleas were tested by a multiplex polymerase chain reaction, for the presence of the plague bacterium. Only one of 1,421 fleas, an Oropsylla hirsuta collected in 2002 from a deer mouse, Peromyscus maniculatus, tested positive for Y. pestis. Blood samples collected in summer 2004 from two northern grasshopper mice, Onychomys leucogaster, tested positive for Y. pestis antibodies. All three positive samples were collected from on-colony grids shortly after a plague epizootic occurred. This study confirms that plague is difficult to detect in rodents and fleas associated with prairie dog colonies, unless samples are collected immediately after a prairie dog die-off.     

A plague epizootic in the white-tailed prairie dogs (Cynomys leucurus) of Meeteetse, Wyoming

Surveillance for sylvatic plague (Yersinia pestis) was conducted near Meeteetse, Wyoming (USA) from 24 May to 14 June 1985. Ten species of fleas were collected from white-tailed prairie dogs (Cynomys leucurus), and from their burrows and associated rodents. Five of these flea species and two adult prairie dogs were positive for plague. The progression of this plague epizootic appeared to be slower and the intensity was less than in previous epizootics in other prairie dog colonies. The plague epizootic occurred within the only known colony of black-footed ferrets (Mustela nigripes) and was a potential threat to the food source of this endangered species.     

Possible vector dissemination by swift foxes following a plague epizootic in black-tailed prairie dogs in northwestern Texas

To determine whether swift foxes (Vulpes velox) could facilitate transmission of Yersinia pestis to uninfected black-tailed prairie dog (Cynomys ludovicianus) colonies by acquiring infected fleas, ectoparasite and serologic samples were collected from swift foxes living adjacent to prairie dog towns during a 2004 plague epizootic in northwestern Texas, USA. A previous study (1999-2001) indicated that these swift foxes were infested almost exclusively with the flea Pulex irritans. Black-tailed prairie dogs examined from the study area harbored only Pulex simulans and Oropsylla hirsuta. Although P. irritans was most common, P. simulans and O. hirsuta were collected from six swift foxes and a single coyote (Canis latrans) following the plague epizootic. Thus, both of these canids could act as transport hosts (at least temporarily) of prairie dog fleas following the loss of their normal hosts during a plague die-off. All six adult swift foxes tested positive for antibodies to Y. pestis. All 107 fleas from swift foxes tested negative for Y. pestis by mouse inoculation. Although swift foxes could potentially carry Y. pestis to un-infected prairie dog colonies, we believe they play only a minor role in plague epidemiology, considering that they harbored just a few uninfected prairie dog fleas (P. simulans and O. hirsuta).     

New records of sylvatic plague in Kansas

Sylvatic plague, or plague of wild rodents is caused by Yersinia pestis and entered California (USA) from Asia about 1899. Extensive sampling during the 1930's and 1940's documented the spread of plague to approximately its current distribution in North America. Records from the Centers for Disease Control and Prevention document plague in Kansas (USA) between 1945 and 1950, but since then there has been no documentation of plague in the state. Following a die-off of a black-tailed prairie dog (Cynomys ludovicianus) colony on the Cimarron National Grassland, in the southwestern corner of Kansas (3710'N, 10145'W), we sampled fleas from burrows in June 1997, and tested them for Yersinia pestis. Twelve of 13 pools of Oropsyla hirsuta and one of two Pulex sp. were positive. A similar sample of fleas, from another colony where black-tailed prairie dogs were active at the time, yielded no positive fleas.     

Climate-driven spatial dynamics of plague among prairie dog colonies

We present a Bayesian hierarchical model for the joint spatial dynamics of a host-parasite system. The model was fitted to long-term data on regional plague dynamics and metapopulation dynamics of the black-tailed prairie dog, a declining keystone species of North American prairies. The rate of plague transmission between colonies increases with increasing precipitation, while the rate of infection from unknown sources decreases in response to hot weather. The mean annual dispersal distance of plague is about 10 km, and topographic relief reduces the transmission rate. Larger colonies are more likely to become infected, but colony area does not affect the infectiousness of colonies. The results suggest that prairie dog movements do not drive the spread of plague through the landscape. Instead, prairie dogs are useful sentinels of plague epizootics. Simulations suggest that this model can be used for predicting long-term colony and plague dynamics as well as for identifying which colonies are most likely to become infected in a specific year.     

The absence of concordant population genetic structure in the black‐tailed prairie dog and the flea,Oropsylla hirsuta,with implications for the spread of Yersinia pestis

The black‐tailed prairie dog (Cynomys ludovicianus) is a keystone species on the mid‐ and short‐grass prairies of North America. The species has suffered extensive colony extirpations and isolation as a result of human activity including the introduction of an exotic pathogen, Yersinia pestis, the causative agent of sylvatic plague. The prairie dog flea, Oropsylla hirsuta, is the most common flea on our study colonies in north‐central Montana and it has been shown to carry Y. pestis. We used microsatellite markers to estimate the level of population genetic concordance between black‐tailed prairie dogs and O. hirsuta in order to determine the extent to which prairie dogs are responsible for dispersing this potential plague vector among prairie dog colonies. We sampled fleas and prairie dogs from six prairie dog colonies in two regions separated by about 46 km. These colonies were extirpated by a plague epizootic that began months after our sampling was completed in 2005. Prairie dogs showed significant isolation‐by‐distance and a tendency toward genetic structure on the regional scale that the fleas did not. Fleas exhibited higher estimated rates of gene flow among prairie dog colonies than the prairie dogs sampled from the same colonies. While the findings suggested black‐tailed prairie dogs may have contributed to flea dispersal, we attributed the lack of concordance between the population genetic structures of host and ectoparasite to additional flea dispersal that was mediated by mammals other than prairie dogs that were present in the prairie system.     

Deltamethrin flea-control preserves genetic variability of black-tailed prairie dogs during a plague outbreak

Genetic variability and structure of nine black-tailed prairie dog (BTPD, Cynomys ludovicianus) colonies were estimated with 15 unlinked microsatellite markers. A plague epizootic occurred between the first and second years of sampling and our study colonies were nearly extirpated with the exception of three colonies in which prairie dog burrows were previously dusted with an insecticide, deltamethrin, used to control fleas (vectors of the causative agent of plague, Yersinia pestis). This situation provided context to compare genetic variability and structure among dusted and non-dusted colonies pre-epizootic, and among the three dusted colonies pre- and post-epizootic. We found no statistical difference in population genetic structures between dusted and non-dusted colonies pre-epizootic. On dusted colonies, gene flow and recent migration rates increased from the first (pre-epizootic) year to the second (post-epizootic) year which suggested dusted colonies were acting as refugia for prairie dogs from surrounding colonies impacted by plague. Indeed, in the dusted colonies, estimated densities of adult prairie dogs (including dispersers), but not juveniles (non-dispersers), increased from the first year to the second year. In addition to preserving BTPDs and many species that depend on them, protecting colonies with deltamethrin or a plague vaccine could be an effective method to preserve genetic variability of prairie dogs.     

Habitat selection by mountain plovers in shortgrass steppe

Much of the breeding range for the mountain plover (Charadrius montanus) occurs in shortgrass steppe and mixed-grass prairie in the western Great Plains of North America. Studies of mountain plovers in shortgrass steppe during the 1970s and 1990s were focused in Weld County, Colorado, which was considered a key breeding area for the species. These studies, however, did not include habitats influenced by black-tailed prairie dogs (Cynomys ludovicianus) or prescribed fire. The role of these 2 rangeland disturbance processes has increased substantially over the past 15 years. During 2008–2009, I used radial distance point count surveys to estimate mountain plover densities early in the nesting season in 4 habitats on public lands in Weld County, Colorado. All 4 habitats were grazed by cattle during the growing season at moderate stocking rates but had different additional disturbances consisting of 1) dormant-season prescribed burns, 2) active black-tailed prairie dog colonies, 3) black-tailed prairie dog colonies affected by epizootic plague in the past 1–2 years, and 4) rangeland with no recent history of fire or prairie dogs. Mountain plover densities were similar on active black-tailed prairie dog colonies ( = 6.8 birds/km², 95% CI = 4.3–10.6) and prescribed burns ( = 5.6 birds/km², 95% CI = 3.5–9.1). In contrast, no plovers were detected at randomly selected rangeland sites grazed by cattle but lacking recent disturbance by prairie dogs or fire, even though survey effort was highest for this rangeland habitat. Mountain plover densities were intermediate (2.0 birds/km², 95% CI = 0.8–5.0) on sites where black-tailed prairie dogs had recently been extirpated by plague. These findings suggest that prescribed burns and active black-tailed prairie dog colonies may enhance breeding habitat for mountain plovers in shortgrass steppe and illustrate the potential for suppressed or altered disturbance processes to influence habitat availability for declining wildlife species. © 2011 The Wildlife Society.     

Duration of Plague (Yersinia pestis) Outbreaks in Black-Tailed Prairie Dog (Cynomys ludovicianus) Colonies of Northern Colorado

Plague, caused by the bacterium Yersinia pestis, triggers die-offs in colonies of black-tailed prairie dogs (Cynomys ludovicianus), but the time-frame of plague activity is not well understood. We document plague activity in fleas from prairie dogs and their burrows on three prairie dog colonies that suffered die-offs. We demonstrate that Y. pestis transmission occurs over periods from several months to over a year in prairie dog populations before observed die-offs.     

Testing the Generality of a Trophic-cascade Model for Plague

Climate may affect the dynamics of infectious diseases by shifting pathogen, vector, or host species abundance, population dynamics, or community interactions. Black-tailed prairie dogs (Cynomys ludovicianus) are highly susceptible to plague, yet little is known about factors that influence the dynamics of plague epizootics in prairie dogs. We investigated temporal patterns of plague occurrence in black-tailed prairie dogs to assess the generality of links between climate and plague occurrence found in previous analyses of human plague cases. We examined long-term data on climate and plague occurrence in prairie dog colonies within two study areas. Multiple regression analyses revealed that plague occurrence in prairie dogs was not associated with climatic variables in our Colorado study area. In contrast, plague occurrence was strongly associated with climatic variables in our Montana study area. The models with most support included a positive association with precipitation in April–July of the previous year, in addition to a positive association with the number of “warm” days and a negative association with the number of “hot” days in the same year as reported plague events. We conclude that the timing and magnitude of precipitation and temperature may affect plague occurrence in some geographic areas. The best climatic predictors of plague occurrence in prairie dogs within our Montana study area are quite similar to the best climatic predictors of human plague cases in the southwestern United States. This correspondence across regions and species suggests support for a (temperature-modulated) trophic-cascade model for plague, including climatic effects on rodent abundance, flea abundance, and pathogen transmission, at least in regions that experience strong climatic signals.     

Prairie dog presence affects occurrence patterns of disease vectors on small mammals

Wildlife disease is recognized as a burgeoning threat to imperiled species and aspects of host and vector community ecology have been shown to have significant effects on disease dynamics. The black‐tailed prairie dog is a species of conservation concern that is highly susceptible to plague, a flea‐transmitted disease. Prairie dogs (Cynomys) alter the grassland communities in which they exist and have been shown to affect populations of small rodents, which are purported disease reservoirs. To explore potential ecological effects of black‐tailed prairie dogs on plague dynamics, we quantified flea occurrence patterns on small mammals in the presence and absence of prairie dogs at 8 study areas across their geographic range. Small mammals sampled from prairie dog colonies showed significantly higher flea prevalence, flea abundance, and relative flea species richness than those sampled from off‐colony sites. Successful plague transmission likely is dependent on high prevalence and abundance of fleas that can serve as competent vectors. Prairie dogs may therefore facilitate the maintenance of plague by increasing flea occurrence on potential plague reservoir species. Our data demonstrate the previously unreported ecological influence of prairie dogs on vector species assemblages, which could influence disease dynamics.     

No evidence of persistent Yersina pestis infection at prairie dog colonies in north-central Montana

Sylvatic plague is a flea-borne zoonotic disease caused by the bacterium Yersinia pestis, which can cause extensive mortality among prairie dogs (Cynomys) in western North America. It is unclear whether the plague organism persists locally among resistant host species or elsewhere following epizootics. From June to August 2002 and 2003 we collected blood and flea samples from small mammals at prairie dog colonies with a history of plague, at prairie dog colonies with no history of plague, and from off-colony sites where plague history was unknown. Blood was screened for antibody to Y. pestis by means of enzyme-linked immunosorbent assay or passive hemagglutination assay and fleas were screened for Y. pestis DNA by polymerase chain reaction. All material was negative for Y. pestis including 156 blood samples and 553 fleas from colonies with a known history of plague. This and other studies provide evidence that Y. pestis may not persist at prairie dog colonies following an epizootic.     

Exposure of small rodents to plague during epizootics in black-tailed prairie dogs

Plague, caused by the bacterium Yersinia pestis, causes die-offs of colonies of prairie dogs (Cynomys ludovicianus). It has been argued that other small rodents are reservoirs for plague, spreading disease during epizootics and maintaining the pathogen in the absence of prairie dogs; yet there is little empirical support for distinct enzootic and epizootic cycles. Between 2004 and 2006, we collected blood from small rodents captured in colonies in northern Colorado before, during, and for up to 2 yr after prairie dog epizootics. We screened 1,603 blood samples for antibodies to Y. pestis, using passive hemagglutination and inhibition tests, and for a subset of samples we cultured blood for the bacterium itself. Of the four species of rodents that were common in colonies, the northern grasshopper mouse (Onychomys leucogaster) was the only species with consistent evidence of plague infection during epizootics, with 11.1-23.1% of mice seropositive for antibody to Y. pestis during these events. Seropositive grasshopper mice, thirteen-lined ground squirrels (Spermophilus tridecemlineatus), and deer mice (Peromyscus maniculatus) were captured the year following epizootics. The appearance of antibodies to Y. pestis in grasshopper mice coincided with periods of high prairie dog mortality; subsequently, antibody prevalence rates declined, with no seropositive individuals captured 2 yr after epizootics. We did not detect plague in any rodents off of colonies, or on colonies prior to epizootics, and found no evidence of persistent Y. pestis infection in blood cultures. Our results suggest that grasshopper mice could be involved in epizootic spread of Y. pestis, and possibly, serve as a short-term reservoir for plague, but provide no evidence that the grasshopper mouse or any small rodent acts as a long-term, enzootic host for Y. pestis in prairie dog colonies.     

Field evaluation of imidacloprid as a systemic approach to flea control in black‐tailed prairie dogs,Cynomys ludovicianus

Epizootic outbreaks of sylvatic plague have dramatically influenced prairie dog (Cynomys sp.) populations across North America. While a great deal of debate surrounds the cause and persistence of plague, flea control can stop the spread of plague epizootic outbreaks and even increase prairie dog survival under non‐epizootic conditions. We investigated a newly‐developed imidacloprid‐treated grain bait that could potentially reduce flea infestations and mitigate the effects of plague on black‐tailed prairie dogs (C. ludovicianus). We used a study design involving randomly assigned experimental and control study plots to assess the effectiveness of the systemic flea control product. We observed a significant difference in flea prevalence and abundance between experimental and control sites on three of the four sites treated with a single application of imidacloprid‐treated grain bait for up to 90 days post‐treatment. We observed an even greater reduction in flea infestations following the double application of treatment bait on two of three additional experimental sites. While we were unable to reduce flea infestations to the extent reported for more commonly used topical insecticides containing deltamethrin, imidacloprid might still be effective at reducing the risk of plague and halting epizootics. In addition, this systemic product can be more rapidly applied than topical insecticides, providing managers with a tool to quickly reduce flea infestations. Future research is needed to evaluate the effectiveness of different application timing and rates, the utility of the product in limiting plague, and the potential effects on non‐target species that might also consume the treated bait.     

Sylvatic plague management and prairie dogs – a meta‐analysis

Yersinia pestis, a bacterial pathogen that causes sylvatic plague, is present in the prairie dogs (Cynomys spp.) of North America. Epizootics of sylvatic plague through transmission in vectors (fleas) commonly completely extirpate colonies of prairie dogs. Wildlife managers employ a wide variety of insecticidal treatments to suppress plague and conserve prairie dog colonies. I compiled and statistically compared the available literature describing methods of plague control and their relative effectiveness in managing plague outbreaks by using meta‐analyses. Natural log response ratios were used to calculate insecticide‐induced vector mortality and vaccine‐conferred survival increases in prairie dogs in 37 publications. Further, subgroupings were used to explore the most effective of the available vector suppression insecticides and plague suppression vaccines. After accounting for the type of treatment used and the method by which it was applied, I observed plague reduction through use of both insecticides and vaccines. Insecticides resulted in a significant reduction of the abundance of vectors by 91.34% compared to non‐treated hosts (p<0.0001). Vaccines improved survival of prairie dog hosts by 4.00% (p<0.0001) compared to control populations. The use of insecticides such as deltamethrin and carbaryl is recommended to stop actively spreading epizootics, and dual antigen oral vaccines to initially suppress outbreaks.     

Occupancy of Mountain Plover and Burrowing Owl in Colorado

Abstract: Concern over the decline of grassland birds has spurred efforts to increase understanding of grassland bird-habitat relationships. Previous studies have suggested that black-tailed prairie dogs (Cynomys ludovicianus) provide important habitat for shortgrass prairie avifauna, such as mountain plover (Charadrius montanus) and western burrowing owl (Athene cunicularia hypugaea), although such studies are lacking in Colorado (USA). We used methods to estimate occupancy (ψ) of mountain plover and burrowing owl on prairie dog colonies and other shortgrass prairie habitats in eastern Colorado. Mountain plover occupancy was higher on prairie dog colonies (ψ = 0.50, 95% CI = 0.36–0.64) than on grassland (ψ = 0.07, 95% CI = 0.03–0.15) and dryland agriculture (ψ = 0.13, 95% CI = 0.07–0.23). Burrowing owl occupancy was higher on active prairie dog colonies (ψ = 0.80, 95% CI = 0.66–0.89) compared with inactive colonies (ψ = 0.23, 95% CI = 0.07–0.53), which in turn was much higher than on grassland (ψ = 0.01, 95% CI = 0.00–0.07) and dryland agriculture (ψ = 0.00, 95% CI ψ 0.00–0.00). Mountain plover occupancy also was positively correlated with increasing amounts of prairie dog colony in the landscape. Burrowing owl occupancy was negatively correlated with increasing amounts of prairie dog colony in the surrounding landscape. Our results suggest that actions to conserve mountain plovers and burrowing owls should incorporate land management to benefit prairie dogs. Because managing for specific colony attributes is difficult, alternative management that promotes heterogeneity may ensure that suitable habitat is available for the guild of grassland inhabitants.