No evidence for enzootic plague within black-tailed prairie dog (Cynomys ludovicianus) populations

Abstract

Yersinia pestis, causative agent of plague, occurs throughout the western United States in rodent populations and periodically causes epizootics in susceptible species, including black-tailed prairie dogs (Cynomys ludovicianus). How Y. pestis persists long-term in the environment between these epizootics is poorly understood but multiple mechanisms have been proposed, including, among others, a separate enzootic transmission cycle that maintains Y. pestis without involvement of epizootic hosts and persistence of Y. pestis within epizootic host populations without causing high mortality within those populations. We live-trapped and collected fleas from black-tailed prairie dogs and other mammal species from sites with and without black-tailed prairie dogs in 2004 and 2005 and tested all fleas for presence of Y. pestis. Y. pestis was not detected in 2126 fleas collected in 2004 but was detected in 294 fleas collected from multiple sites in 2005, before and during a widespread epizootic that drastically reduced black-tailed prairie dog populations in the affected colonies. Temporal and spatial patterns of Y. pestis occurrence in fleas and genotyping of Y. pestis present in some infected fleas suggest Y. pestis was introduced multiple times from sources outside the study area and once introduced, was dispersed between several sites. We conclude Y. pestis likely was not present in these black-tailed prairie dog colonies prior to epizootic activity in these colonies. Although we did not identify likely enzootic hosts, we found evidence that deer mice (Peromyscus maniculatus) may serve as bridging hosts for Y. pestis between unknown enzootic hosts and black-tailed prairie dogs.

Keywords: Cynomys ludovicianus; Yersinia pestis; black-tailed prairie dog; plague; prairie dogs.

Figure 1

Location of 14 black‐tailed prairie dog colonies and grassland sites in Boulder County, Colorado where fleas were collected from black‐tailed prairie dogs and small mammals in 2004 and/or 2005. Site abbreviations for sites added in 2005 start with a letter instead of a numeral. Circles and squares represent grassland sites and black‐tailed prairie dog colonies, respectively, and the colors of these shapes indicate presence (red) or absence (blue) of Y. pestis in individual fleas collected from these sites in 2005. The inset indicates the location of the study area within the state of Colorado in the United States.

Figure 2

Top: Specific dates in 2005 when black‐tailed prairie dogs and/or small mammals were trapped at 7 grassland sites (blue; just small mammal trapped) and 7 black‐tailed prairie dog colonies (orange; both black‐tailed prairie dogs and small mammals trapped) and fleas were collected from the trapped mammals. Bottom: Specific date that the first Y. pestis positive flea was collected at each of the 8 sites that yielded Y. pestis positive fleas. The species of the first Y. pestis positive flea from each site, as well as the rodent species that it was collected from (in parentheses), is indicated. “Swab” indicates the first Y. pestis positive flea was collected via a burrow swab.

Figure 3

Patterns of population structure in Y. pestis that was genotyped from DNA extracted from 78 individual fleas collected in 2005 from 6 sites, including 3 black‐tailed prairie dog colonies (BTPD) and 3 grassland sites (GRASS). (a) Midpoint rooted neighbor‐joining tree created using genetic distance data generated from amplicon size data for 43 Y. pestis VNTR loci. Length of branches indicates genetic distances between samples. (b) NMDS ordination plot of the same genetic distance data, with squares indicating black‐tailed prairie dog colonies, circles indicating grassland sites, and different colors representing different sites.