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.     

A plague epizootic in the black-tailed prairie dog (Cynomys ludovicianus)

Plague is the primary cause for the rangewide decline in prairie dog (Cynomys spp.) distribution and abundance, yet our knowledge of plague dynamics in prairie dog populations is limited. Our understanding of the effects of plague on the most widespread species, the black-tailed prairie dog (C. ludovicianus), is particularly weak. During a study on the population biology of black-tailed prairie dogs in Wyoming, USA, plague was detected in a colony under intensive monitoring, providing a unique opportunity to quantify various consequences of plague. The epizootic reduced juvenile abundance by 96% and adult abundance by 95%. Of the survivors, eight of nine adults and one of eight juveniles developed antibodies to Yersinia pestis. Demographic groups appeared equally susceptible to infection, and age structure was unaffected. Survivors occupied three small coteries and exhibited improved body condition, but increased flea infestation compared to a neighboring, uninfected colony. Black-tailed prairie dogs are capable of surviving a plague epizootic and reorganizing into apparently functional coteries. Surviving prairie dogs may be critical in the repopulation of plague-decimated colonies and, ultimately, the evolution of plague resistance.     

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.     

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.     

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     

Connectivity of prairie dog colonies in an altered landscape: inferences from analysis of microsatellite DNA variation

Connectivity of populations influences the degree to which species maintain genetic diversity and persist despite local extinctions. Natural landscape features are known to influence connectivity, but global anthropogenic landscape change underscores the importance of quantifying how human-modified landscapes disrupt connectivity of natural populations. Grasslands of western North America have experienced extensive habitat alteration, fragmenting populations of species such as black-tailed prairie dogs (Cynomys ludovicianus). Population sizes and the geographic range of prairie dogs have been declining for over a century due to habitat loss, disease, and eradication efforts. In many places, prairie dogs have persisted in the face of emerging urban landscapes that carve habitat into smaller and smaller fragments separated by uninhabitable areas. In extreme cases, prairie dog colonies are completely bounded by urbanization. Connectivity is particularly important for prairie dogs because colonies suffer high probabilities of extirpation by plague, and dispersal permits recolonization. Here we explore connectivity of prairie dog populations using analyses of 11 microsatellite loci for 9 prairie dog colonies spanning the fragmented landscape of Boulder County, Colorado. Isolation-by-resistance modeling suggests that wetlands and high intensity urbanization limit movement of prairie dogs. However, prairie dogs appear to move moderately well through low intensity development (including roads) and freely through cropland and grassland. Additionally, there is a marked decline in gene flow between colonies with increasing geographic distance, indicating isolation by distance even in an altered landscape. Our results suggest that prairie dog colonies retain some connectivity despite fragmentation by urbanization and agricultural development.     

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.     

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.     

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.     

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).     

Isolation and characterization of 11 microsatellite loci from Oropsylla hirsuta, a vector of sylvatic plague

The flea (Oropsylla hirsuta) is an important vector of the plague bacterium, Yersinia pestis, in black-tailed prairie dog (Cynomys ludovicianus) colonies. We developed 11 anonymous microsatellite primers for O. hirsuta using a subtractive hybridization procedure. All primers were polymorphic exhibiting 4-12 alleles.     

Mark-Resight Methodology for Estimating Population Densities for Prairie Dogs

Abstract: Accurate assessments of local population size of the black-tailed prairie dog (Cynomys ludovicianus) are essential because of their overall decline and importance to prairie ecosystems. We describe the use of mark-resight methodology to estimate black-tailed prairie dog population size and density. Study colonies include isolated urban habitat fragments in Denver, Colorado, USA, and unfragmented control colonies in the Pawnee National Grassland, USA. We compare results from various mark-resight estimators to those derived from linear transformations of visual counts of active prairie dogs. Our results suggest that mark-resight methods are feasible in both urban and rural systems, and reveal extremely high densities for isolated prairie dogs in urban sites. Our methodology can be used to obtain reliable, unbiased estimates of local population size and density.     

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.     

Local factors associated with on‐host flea distributions on prairie dog colonies

Outbreaks of plague, a flea‐vectored bacterial disease, occur periodically in prairie dog populations in the western United States. In order to understand the conditions that are conducive to plague outbreaks and potentially predict spatial and temporal variations in risk, it is important to understand the factors associated with flea abundance and distribution that may lead to plague outbreaks. We collected and identified 20,041 fleas from 6,542 individual prairie dogs of four different species over a 4‐year period along a latitudinal gradient from Texas to Montana. We assessed local climate and other factors associated with flea prevalence and abundance, as well as the incidence of plague outbreaks. Oropsylla hirsuta, a prairie dog specialist flea, and Pulex simulans, a generalist flea species, were the most common fleas found on our pairs. High elevation pairs in Wyoming and Utah had distinct flea communities compared with the rest of the study pairs. The incidence of prairie dogs with Yersinia pestis detections in fleas was low (n = 64 prairie dogs with positive fleas out of 5,024 samples from 4,218 individual prairie dogs). The results of our regression models indicate that many factors are associated with the presence of fleas. In general, flea abundance (number of fleas on hosts) is higher during plague outbreaks, lower when prairie dogs are more abundant, and reaches peak levels when climate and weather variables are at intermediate levels. Changing climate conditions will likely affect aspects of both flea and host communities, including population densities and species composition, which may lead to changes in plague dynamics. Our results support the hypothesis that local conditions, including host, vector, and environmental factors, influence the likelihood of plague outbreaks, and that predicting changes to plague dynamics under climate change scenarios will have to consider both host and vector responses to local factors.     

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.     

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.     

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.     

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.     

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.     

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.