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.     

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.     

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     

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.     

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.     

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.     

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.     

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).     

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.     

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.     

Genetic variation and population structure in a threatened species,the Utah prairie dog Cynomys parvidens: the use of genetic data to inform conservation actions

The Utah prairie dog (Cynomys parvidens), listed as threatened under the United States Endangered Species Act, was the subject of an extensive eradication program throughout its range during the 20th century. Eradication campaigns, habitat destruction/fragmentation/conversion, and epizootic outbreaks (e.g., sylvatic plague) have reduced prairie dog numbers from an estimated 95,000 individuals in the 1920s to approximately 14,000 (estimated adult spring count) today. As a result of these anthropogenic actions, the species is now found in small isolated sets of subpopulations. We characterized the levels of genetic diversity and population genetic structure using 10 neutral nuclear microsatellite loci for twelve populations (native and transplanted) representative of the three management designated “recovery units,” found in three distinct biogeographic regions, sampled across the species' range. The results indicate (1) low levels of genetic diversity within colonies (H_e = 0.109–0.357; H_o = 0.106‐ 0.313), (2) high levels of genetic differentiation among colonies (global F_ST = 0.296), (3) very small genetic effective population sizes, and (4) evidence of genetic bottlenecks. The genetic data reveal additional subdivision such that colonies within recovery units do not form single genotype clusters consistent with recovery unit boundaries. Genotype cluster membership support historical gene flow among colonies in the easternmost West Desert Recovery Unit with the westernmost Pausaugunt colonies and among the eastern Pausaugunt colonies and the Awapa Recovery unit to the north. In order to maintain the long‐term viability of the species, there needs to be an increased focus on maintaining suitable habitat between groups of existing populations that can act as connective corridors. The location of future translocation sites should be located in areas that will maximize connectivity, leading to maintenance of genetic variation and evolutionary potential.     

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.     

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.     

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.     

Expected future plague levels in a wildlife host under different scenarios of climate change

We predicted future plague and black-tailed prairie dog dynamics in the North American prairies under different scenarios of climate change. A climate-driven model for the joint dynamic of the host–parasite system was used. Projections for the regional climate were obtained through empirical–statistical downscaling of global climate scenarios generated by an ensemble of global climate models for the recent Fourth Assessment Report by the IPCC. The study shows the uncertainties involved in predicting future regional climate and climate-driven population dynamics, but reveals that unchanged or lower levels of plague, leading to increased black-tailed prairie dog colonies, can be expected. Less plague is particularly expected for scenarios that assume the highest emission of greenhouse gases associated with the greatest projected future warming. Moreover, under high-emission scenarios, decreased probabilities of extremely high numbers of infected colonies are expected, along with decreased probabilities of extremely low total numbers of colonies. The assumed main underlying mechanism is an inhibiting effect of high temperatures on fleas (dispersal vector) and on flea-mediated transmission of the disease-causing bacterium. Our study highlights the importance of using dynamic ecological (here host–parasite) models together with ensembles of climate projections to investigate the responses of populations and parasites to a changed climate.     

Extreme plasticity in thermoregulatory behaviors of free-ranging black-tailed prairie dogs

In the natural environment, hibernating sciurids generally remain dormant during winter and enter numerous deep torpor bouts from the time of first immergence in fall until emergence in spring. In contrast, black-tailed prairie dogs (Cynomys ludovicianus) remain active throughout winter but periodically enter short and shallow bouts of torpor. While investigating body temperature (T(b)) patterns of black-tailed prairie dogs from six separate colonies in northern Colorado, we observed one population that displayed torpor patterns resembling those commonly seen in hibernators. Five individuals in this population experienced multiple torpor bouts in immediate succession that increased in length and depth as winter progressed, whereas 16 prairie dogs in five neighboring colonies remained euthermic for the majority of winter and entered shallow bouts of torpor infrequently. Our results suggest that these differences in torpor patterns did not result from differences in the physiological indicators that we measured because the prairie dogs monitored had similar body masses and concentrations of stored lipids across seasons. Likewise, our results did not support the idea that differences in overwinter T(b) patterns between prairie dogs in colonies with differing torpor patterns resulted from genetic differences between populations; genetic analyses of prairie dog colonies revealed high genetic similarity between the populations and implied that individuals regularly disperse between colonies. Local environmental conditions probably played a role in the unusual T(b) patterns experienced by prairie dogs in the colony where hibernation-like patterns were observed; this population received significantly less rainfall than neighboring colonies during the summer growing seasons before, during, and after the year of the winter in which they hibernated. Our study provides a rare example of extreme plasticity in thermoregulatory behaviors of free-ranging prairie dogs and provides evidence contrary to models that propose a clear delineation between homeothermy, facultative torpor, and hibernation.