Jack F. Cully

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 (Cynomysludovicianus) 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.

Disease Limits Populations: Plague and Black-Tailed Prairie Dogs

Plague is an exotic vector-borne disease caused by the bacterium Yersinia pestis that causes mortality rates approaching 100% in black-tailed prairie dogs (Cynomys ludovicianus). We mapped the perimeter of the active portions of black-tailed prairie dog colonies annually between 1999 and 2005 at four prairie dog colony complexes in areas with a history of plague, as well as at two complexes that were located outside the distribution of plague at the time of mapping and had therefore never been affected by the disease. We hypothesized that the presence of plague would significantly reduce overall black-tailed prairie dog colony area, reduce the sizes of colonies on these landscapes, and increase nearest-neighbor distances between colonies. Within the region historically affected by plague, individual colonies were smaller, nearest-neighbor distances were greater, and the proportion of potential habitat occupied by active prairie dog colonies was smaller than at plague-free sites. Populations that endured plague were composed of fewer large colonies (>100 ha) than populations that were historically plague free. We suggest that these differences among sites in colony size and isolation may slow recolonization after extirpation. At the same time, greater intercolony distances may also reduce intercolony transmission of pathogens. Reduced transmission among smaller and more distant colonies may ultimately enhance long-term prairie dog population persistence in areas where plague is present.

Spatiotemporal dynamics of black-tailed prairie dog colonies affected by plague

Black-tailed prairie dogs (Cynomys ludovicianus) are a key component of the disturbance regime in semi-arid grasslands of central North America. Many studies have compared community and ecosystem characteristics on prairie dog colonies to grasslands without prairie dogs, but little is known about landscape-scale patterns of disturbance that prairie dog colony complexes may impose on grasslands over long time periods. We examined spatiotemporal dynamics in two prairie dog colony complexes in southeastern Colorado (Comanche) and northcentral Montana (Phillips County) that have been strongly influenced by plague, and compared them to a complex unaffected by plague in northwestern Nebraska (Oglala). Both plague-affected complexes exhibited substantial spatiotemporal variability in the area occupied during a decade, in contrast to the stability of colonies in the Oglala complex. However, the plague-affected complexes differed in spatial patterns of colony movement. Colonies in the Comanche complex in shortgrass steppe shifted locations over a decade. Only 10% of the area occupied in 1995 was still occupied by prairie dogs in 2006. In 2005 and 2006 respectively, 74 and 83% of the total area of the Comanche complex occurred in locations that were not occupied in 1995, and only 1% of the complex was occupied continuously over a decade. In contrast, prairie dogs in the Phillips County complex in mixed-grass prairie and sagebrush steppe primarily recolonized previously occupied areas after plague-induced colony declines. In Phillips County, 62% of the area occupied in 1993 was also occupied by prairie dogs in 2004, and 12% of the complex was occupied continuously over a decade. Our results indicate that plague accelerates spatiotemporal movement of prairie dog colonies, and have significant implications for landscape-scale effects of prairie dog disturbance on grassland composition and productivity. These findings highlight the need to combine landscape-scale measures of habitat suitability with long-term measures of colony locations to understand the role of plague-affected prairie dogs as a grassland disturbance process.

ECOSYSTEM ENGINEERING BY A COLONIAL MAMMAL: HOW PRAIRIE DOGS STRUCTURE RODENT COMMUNITIES

As ecosystem engineers, prairie dogs (Cynomys spp.) physically alter their environment, but the mechanism by which these alterations affect associated faunal composition is not well known. We examined how rodent and vegetation communities responded to prairie dog colonies and landcover at the Cimarron National Grassland in southwest Kansas, USA. We trapped rodents and measured vegetation structure on and off colonies in 2000 and 2003. We plotted two separate ordinations of trapping grids: one based on rodent counts and a second based on vegetation variables. We regressed three factors on each ordination: (1) colony (on-colony and off-colony), (2) cover (shortgrass and sandsage), and (3) habitat (factorial cross of colony x cover). Rodent communities differed by colony but not cover. Vegetation differed across both gradients. Rodent responses to habitat reflected those of colony and cover, but vegetation was found to differ across cover only in the sandsage prairie. This interaction suggested that rodent composition responded to prairie dog colonies, but independently of vegetation differences. We conclude that burrowing and soil disturbance are more important than vegetation cropping in structuring rodent communities.

Growth and Life-History Changes in Gunnison's Prairie Dogs after a Plague Epizootic

I measured rates of growth of individual Gunnisons prairie dogs ( Cynomys gunnisoni ) at three towns in the Moreno Valley, New Mexico; at an established prairie dog town (site 1) prior to a plague ( Yersinia pestis ) epizootic and at two towns reestablished after the epizootic (sites 2 and 3). Populations declined by >99% during the epizootic. After the epizootic, adults had greater mass, and juveniles grew faster than before. At sites 2 and 3, juveniles had high interyear survival (39%), whereas at site 1, prior to plague, survival of juveniles was 17%. At sites 2 and 3, yearlings bred, whereas they did not at site 1. Mean litter size near the end of lactation was 1.5 at site 1 and 5.0 at sites 2 and 3. Application of observed demographic parameters to Leslie-matrix analysis indicated that projected size of population was declining (λ = 0.829) at site 1 and was tripling annually (λ = 2.905) at sites 2 and 3. The difference in λ was mostly due to increased survivorship of juveniles and reproduction at an earlier age in the new towns.

Influence of Fire on Black-tailed Prairie Dog Colony Expansion in Shortgrass Steppe

Abstract Factors influencing the distribution and abundance of black-tailed prairie dog (Cynomys ludovicianus) colonies are of interest to rangeland managers because of the significant influence prairie dogs can exert on both livestock and biodiversity. We examined the influence of 4 prescribed burns and one wildfire on the rate and direction of prairie dog colony expansion in shortgrass steppe of southeastern Colorado. Our study was conducted during 2 years with below-average precipitation, when prairie dog colonies were expanding throughout the study area. Under these dry conditions, the rate of black-tailed prairie dog colony expansion into burned grassland (X ¯  =  2.6 ha · 100-m perimeter−1 · y−1; range  =  0.8–5.9 ha · 100-m perimeter−1 · y−1; N  =  5 colonies) was marginally greater than the expansion rate into unburned grassland (X ¯  =  1.3 ha · 100-m perimeter−1 · y−1; range  =  0.2–4.9 ha · 100-m perimeter−1 · y−1; N  =  23 colonies; P  =  0.066). For 3 colonies that were burned on only a portion of their perimeter, we documented consistently high rates of expansion into the adjacent burned grassland (38%–42% of available burned habitat colonized) but variable expansion rates into the adjacent unburned grassland (2%–39% of available unburned habitat colonized). While our results provide evidence that burning can increase colony expansion rate even under conditions of low vegetative structure, this effect was minor at the scale of the overall colony complex because some unburned colonies were also able to expand at high rates. This result highlights the need to evaluate effects of fire on colony expansion during above-average rainfall years, when expansion into unburned grassland may be considerably lower.

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

ABSTRACT 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 longterm 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.

Effects of rodent community diversity and composition on prevalence of an endemic bacterial pathogen - Bartonella

Abstract By studying Bartonella prevalence in rodent communities from 23 geographic sites in the western United States and one site in northern Mexico, the present study focused on the effects of rodent community diversity (measured by richness and Shannon index) and composition on prevalence of Bartonella infections. The analysis showed negative correlations of Bartonella prevalence with rodent richness and Shannon index. Further, Bartonella prevalence varied among rodent genera/species. Three models were applied to explain the observations. (1) Within-species/genus transmission: Bartonella strains usually are host-specific and adding non-host species would decrease Bartonella prevalence in its principal host through reduction of host contact (encounter reduction); (2) Frequency-dependence: Adding hosts would decrease the proportion of all infected individuals in the community, resulting in a reduction in the number of contacts between susceptible and infected individuals that usually leads to transmission (transmission reduction); and (3) Dominant species effect: Dominant species, if not susceptible to Bartonellae, can constrain the abundance of susceptible hosts (susceptible host regulation). These mechanisms work in concert; and the level of Bartonella prevalence is an outcome of regulation of all of these mechanisms on the entire system.

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.

Equilibrium and Extinction in a Trisexual Diploid Mating System: An Investigation

In order to study the dynamics of a three-sex (trisexual) mating system, we have chosen to extend the heterogametic sex-determining mechanism, used in many species, to include three sexes: XX, XY and YY. In this model, non-like types may mate, but like-types may not mate. Yeasts and fungi are known to have multiple mating types (sometimes numbering in the thousands), but the mechanics of these sex-determining systems are markedly different from the heterogametic system we are interested in studying [5]. Our motivation for using this scheme stems from the knowledge that in some species, such as most fish, XX is female, and XY is male [1]. Under certain conditions, a YY individual may be produced, and in the case of fish, this usually develops into a male. Our goal is to discover the emergent behavior of a hypothetical “diploid trisexual mating system” (DTMS) where the YY type is its own distinct “mating type”, in order to shed light on why such a system is not observed in nature today.