Skip to main content

Advertisement

SpringerLink
Log in

High prevalence of Yersinia pestis in black-tailed prairie dog colonies during an apparent enzootic phase of sylvatic plague

  • Original Paper
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Altizer A, Harvell D, Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol Evol 18:589–596

    Article  Google Scholar 

  • Anderson E, Forrest SC, Clark TW, Richardson L (1986) Paleobiology, biogeography, and systematics of the black-footed ferret, Mustela nigripes (Audubon and Bachman), 1851. Gr Basin Nat Mem 8:11–62

    Google Scholar 

  • Anderson SH, Williams ES (1997) Plague in a complex of white-tailed prairie dogs and associated small mammals in Wyoming. J Wildl Dis 33:720–732

    PubMed  CAS  Google Scholar 

  • Barnes AM (1982) Surveillance and control of bubonic plague in the United States. Symp Zool Soc Lond 50:237–270

    Google Scholar 

  • Burroughs AL (1947) Sylvatic plague studies. The vector efficiency of nine species of fleas compared to Xenopsylla cheopsis. J Hyg 45:371–396

    Article  Google Scholar 

  • Biggins DE, Kosoy MY (2001) Influences of introduced plague on North American mammals: implications from ecology of plague in Asia. J Mammal 82:906–916

    Article  Google Scholar 

  • Chesser RK (1983) Genetic variability within and among colonies of the black-tailed prairie dog. Evolution 37:320–331

    Article  Google Scholar 

  • Cully JF Jr, Williams ES (2001) Interspecific comparisons of sylvatic plague in prairie dogs. J Mammal 82:894–905

    Article  Google Scholar 

  • Cully JF Jr, Carter LG, Gage KL (2000) New records of sylvatic plague in Kansas. J Wildl Dis 36:389–392

    PubMed  Google Scholar 

  • Daley JG (1992) Population reductions and genetic variability in black-tailed prairie dogs. J Wildl Manage 56:212–220

    Article  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287:443–449

    Article  PubMed  CAS  Google Scholar 

  • Davis S, Begon M, De Bruyn L, Ageyev VS, Klassovskiy NL, Pole SB, Viljugrein H, Stenseth NC, Leirs H (2004) Predictive thresholds for plague in Kazakhstan. Science 304:736–738.

    Article  PubMed  CAS  Google Scholar 

  • Engelthaler DM, Gage KL, Montenieri JA, Chu M, Carter LG (1999) PCR detection of Yersinia pestis in fleas: comparison with mouse inoculation. J Clin Microbiol 37:1980–1984

    PubMed  CAS  Google Scholar 

  • Faunawest Wildlife Consultants (1999) Status of the black and white-tailed prairie dogs in Montana. Montana Fish, Wildlife, and Parks, Helena, pp 1–28

    Google Scholar 

  • Forrest S (2005) Getting the story right: a response to Vermeire and colleagues. BioScience 55:526–530

    Article  Google Scholar 

  • Gage KL, Kosoy MY (2005) Natural history of plague: perspectives from more than a century of research. Annu. Rev. Entomol., 50:505–528

    Article  PubMed  CAS  Google Scholar 

  • Geoscience Associates (2003) Fort Belknap Indian Reservation mapping project

  • Hinnebusch JB, Schwan TG (1993) New method for plague surveillance using polymerase chain reaction to detect Yersinia pestis in fleas. J Clin Microbiol 31:1511–1514

    PubMed  CAS  Google Scholar 

  • Hinnebusch JB, Gage KL, Schwan TG (1998) Estimation of vector infectivity rates for plague by means of a standard curve-based competitive polymerase chain reaction method to quantify Yersinia pestis in fleas. Am J Trop Med Hyg 58:562–569

    PubMed  CAS  Google Scholar 

  • Holdenried R (1952) Sylvatic plague studies. VII. Plague transmission potentials of the fleas Diamanus montanus and Polygenis gwyni compared with Xenopsylla cheopis. J Infect Dis 90:131–140

    PubMed  CAS  Google Scholar 

  • Kartman L (1970) Historical and oecological observations of plague in the United States. Trop Geog Med 22:257–275

    CAS  Google Scholar 

  • Keeling MJ, Gilligan CA (2000) Metapopulation dynamics of bubonic plague. Nature 407:903–906

    Article  PubMed  CAS  Google Scholar 

  • Knowles CJ, Stoner CJ, Gieb SP (1982) Selective use of black-tailed prairie dog towns by mountain plovers. Condor 84:71–74

    Article  Google Scholar 

  • Kotliar NB, Baker BW, Whicker AD, Plumb G (1999) A critical review of assumptions about the prairie dog as a keystone species. Env Mgmt 24:177–192

    Article  Google Scholar 

  • Lechleitner RR, Kartman L, Golderberg MI, Hudson BW (1968) An epizootic of plague in Gunnison’s prairie dogs (Cynomys gunnisoni) in south-central Colorado. Ecology 49:734–743

    Article  Google Scholar 

  • McCallum H, Dobson A (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol Evol 10:190–194

    Article  Google Scholar 

  • Menkens GE Jr, Anderson SH (1991) Population dynamics of white-tailed prairie dogs during an epizootic of sylvatic plague. J Mammal 72:328–331

    Article  Google Scholar 

  • Miller B, Reading R, Hoogland J, Clark T, Ceballos G, List R, Forrest S, Hanebury L, Manzano P, Pacheco J, Uresk D (2000) The role of prairie dogs as a keystone species: response to Stapp. Conserv Biol 14:318–321

    Article  Google Scholar 

  • Miller B, Ceballos G, Reading R (1994) The prairie dog and biotic diversity. Conserv Biol 8:677–681

    Article  Google Scholar 

  • Pauli JN, Buskirk SW, Williams ES, Edwards WH (2006) A plague epizootic in the black-tailed prairie dog (Cynomys ludovicianus). J Wildl Dis 42:74–80

    PubMed  Google Scholar 

  • Perry RD, Fetherston JD (1997) Yersinia pestis- etiologic agent of plague. Clin Microbiol Rev 10:35–66

    PubMed  CAS  Google Scholar 

  • Rayor LS (1985) Dynamics of a plague outbreak in Gunnison’s prairie dog. J Mammal 66:194–196

    Article  Google Scholar 

  • Restani M, Rau LR, Flath DL (2001) Nesting ecology of burrowing owls occupying black-tailed prairie dog towns in southeastern Montana. J Raptor Res 35:296–303

    Google Scholar 

  • Seery DB, Matiatos DJ (2000) Response of wintering buteos to plague epizootics in prairie dogs. West North Am Nat 60:420–425

    Google Scholar 

  • Sodeinde OA, Goguen JD (1988) Genetic analysis of the 9.5-kilobase virulence plasmid of Yersinia pestis. Infec Immun 56:2743–2748

    CAS  Google Scholar 

  • Thorne TE, Williams ES (1988) Disease and endangered species: the black-footed ferret as a recent example. Conserv Biol 2:1988

    Article  Google Scholar 

  • Trudeau KM, Britten HB, Restani M (2004) Sylvatic plague reduces genetic variability in black-tailed prairie dogs. J Wildl Dis 40:205–211

    PubMed  Google Scholar 

  • Ubico SR, Maupin GO, Fagerstone KA, McLean RG (1988) Plague epizootic in the white-tailed prairie dogs (Cynomys leucurus) of Meeteetse, Wyoming. J Wildl Dis 24:399–406

    PubMed  CAS  Google Scholar 

  • Van Putten M, Miller SD (1999) Prairie dogs: the case for listing. Wildl Soc Bull 27:1110–1120

    Google Scholar 

  • Webb CT, Brooks CP, Gage KL, Antolin MF (2006) Classic Flea-borne transmission does not drive plague epizootics in prairie dogs. Proc Natl Acad Sci USA 103:6236–6241

    Article  PubMed  CAS  Google Scholar 

  • Williams ES, Mills K, Kwiatkowski DR, Thorne ET, Boerger-Fields A 1994. Plague in a black-footed ferret (Mustela nigripes). J Wildl Dis 30:581–585

    PubMed  CAS  Google Scholar 

  • Woodroffe R (1999) Managing disease threats to wild mammals. Anim Cons 2:185–193

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Assiniboine Tribal authorities for granting permission to conduct research on the Fort Belknap Indian Reservation, Montana. Our work received logistical support from G. Kaiser, U.S. Bureau of Indian Affairs. P. Young kindly shared unpublished data and insight on prairie dog ecology. J. Weigand generously allowed DH the use of his property as a field camp. We thank an anonymous reviewer and Associate Editor for their useful comments on the manuscript. Partial funding was provided by the Nelson Foundation and the University of South Dakota Office of Research. This material is based upon work supported by the National Science Foundation/EPSCoR Grant No. 0091948 and by the State of South Dakota.

Author information

Authors and Affiliations

  1. Department of Biology, University of South Dakota, Vermillion, SD, 57069, USA

    David A. Hanson & Hugh B. Britten

  2. Department of Biological Sciences, St. Cloud State University, St. Cloud, MN, 56301, USA

    Marco Restani

  3. Basic Biomedical Sciences, University of South Dakota, Vermillion, SD, 57069, USA

    Leigh R. Washburn

Authors
  1. David A. Hanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hugh B. Britten
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marco Restani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leigh R. Washburn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hugh B. Britten.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hanson, D.A., Britten, H.B., Restani, M. et al. High prevalence of Yersinia pestis in black-tailed prairie dog colonies during an apparent enzootic phase of sylvatic plague. Conserv Genet 8, 789–795 (2007). https://doi.org/10.1007/s10592-006-9226-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-006-9226-6

Keywords

Search

Navigation