Skip to main content

Advertisement

Log in

Testing the Generality of a Trophic-cascade Model for Plague

  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

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.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Agnew WD, Uresk W, Hansen RM (1986) Flora and fauna associated with prairie dog colonies and adjacent ungrazed mixed-grass prairie in western South Dakota. Journal of Range Management 39:135–139

    Google Scholar 

  • Antolin MF, Gober P, Luce B, Biggins DE, Van Pelt WE, Seery DB, et al. (2002) The influence of sylvatic plague on North American wildlife at the landscape level, with special emphasis on black-footed ferret and prairie dog conservation. Transactions of the 67 th North American Wildlife and Natural Resources Conference 104–127

  • Barnes AM, (1982) Surveillance and control of plague in the United States. In: Edwards MA, McDonnell U (eds). Animal Disease in relation to animal conservation. New York: Academic Press, pp 237–270

    Google Scholar 

  • Bennett BC (1997) Vegetation on the City of Boulder Open Space grasslands. PhD dissertation, University of Colorado

  • Benning TL, LaPointe D, Atkinson CT, Vitousek PM (2002) Interactions of climate change with biological invasions and land use in the Hawaiian Islands: modeling the fate of endemic birds using a geographic information system. Proceedings of the National Academy of Science 99:14246–14249

    Article  Google Scholar 

  • Bock CE, Vierling KT, Haire SL, Boone JD, Merkle WW (2002) Patterns of rodent abundance on open-space grasslands in relation to suburban edges. Conservation Biology 16:1653–1658

    Article  Google Scholar 

  • Brown JH, Morgan Ernest SK (2002) Rain and rodents: complex dynamics of desert consumers. BioScience 52:979–987

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model Selection and Inference: A Practical Information-Theoretic Approach, 2nd ed., New York: Springer-Verlag

    Google Scholar 

  • City of Boulder Open Space and Mountain Parks Department (1996) Black-tailed prairie dog habitat conservation plan. Available: http://www.ci.boulder.co.us/openspace/planning/pdogplan/pdogmain.htm [accessed September 30, 2004]

  • Collinge SK (2000) Effects of grassland fragmentation on insect species loss, recolonization, and movement patterns. Ecology 81:2211–2226

    Google Scholar 

  • Collinge SK, Johnson WC, Ray C, et al. Landscape structure and plague occurrence in black-tailed prairie dogs on grasslands of the western USA. Landscape Ecology, in press

  • Cully JF Jr (1997) Growth and life history changes in Gunnison’s prairie dogs after a plague epizootic. Journal of Mammalogy 78:146–157

    Google Scholar 

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

    Article  Google Scholar 

  • Enscore RE, Biggerstaff BJ, Brown TL, Fulgham RF, Reynolds PJ, Engelthaler DM, et al. (2002) Modeling relationships between climate and the frequency of human plague cases in the southwestern United States, 1960–1997. American Journal of Tropical Medicine and Hygiene 66:186–196

    PubMed  Google Scholar 

  • Franke CF, Ziller M, Staubach C, Latif M (2002) Impact of the El Niño/Southern Oscillation on visceral leishmaniasis, Brazil. Emerging Infectious Diseases 8:914–917

    PubMed  Google Scholar 

  • Gage KL, Ostfeld RS, Olson JG (1995) Nonviral vector-borne zoonoses associated with mammals in the United States. Journal of Mammalogy 76:695–715

    Google Scholar 

  • Gober P (2000) 12-month administrative finding, black-tailed prairie dog. Federal Register 65:5476–5488

    Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, et al. (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

    Article  PubMed  Google Scholar 

  • Hjelle B, Glass GE (2001) Outbreak of hantavirus infection in the four corners region of the United States in the wake of the 1997–1998 El Nino-Southern Oscillation. The Journal of Infectious Diseases 181:1569–1573

    Article  Google Scholar 

  • Hoogland JL (1995) The Black-Tailed Prairie Dog, Social Life of a Burrowing Mammal, Chicago: University of Chicago Press

    Google Scholar 

  • Johnson WC (2002) Landscape and community characteristics of black-tailed prairie dog colonies. MA thesis, University of Colorado, Boulder

  • Koford CB (1958) Prairie dogs, whitefaces, and blue grama. Wildlife Monographs 3:1–78

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Langlois JP, Fahrig L, Merriam G, Artsob H (2001) Landscape structure influences continental distribution of Hantavirus in deer mice. Landscape Ecology 16:255–266

    Article  Google Scholar 

  • Miller B, Wemmer C, Biggins D, Reading R (1990) A proposal to conserve black-footed ferrets and the prairie dog ecosystem. Environmental Management 14:763–769

    Google Scholar 

  • Miller B, Ceballos G, Reading R (1994) The prairie dog and biotic diversity. Conservation Biology 8:667–681

    Google Scholar 

  • Parmenter RR, Yadav EP, Parmenter CA, Ettestad P, Gage KL (1999) Incidence of plague associated with increased winter-spring precipitation in New Mexico. American Journal of Tropical Medicine and Hygiene 61:814–821

    PubMed  Google Scholar 

  • Perry RD, Fetherson JD (1997) Yersinia pestis: etiologic agent of plague. Clinical Microbiology Reviews 10:35–66

    PubMed  Google Scholar 

  • Reading RP, Matchett R (1997) Attributes of black-tailed prairie dog colonies in northcentral Montana. Journal of Wildlife Management 61:664–673

    Google Scholar 

  • Riebsame WE (editor) (1997) Atlas of the New West, New York: WW Norton and Company

    Google Scholar 

  • SAS Institute Inc (2001) SAS version 8.2, Cary, NC: SAS Institute

    Google Scholar 

  • Stafford JD, Strickland BK (2003) Potential inconsistencies when calculating Akaike’s Information Criterion. Bulletin of the Ecological Society of America 84:68–69

    Google Scholar 

  • Stapp P, Antolin MF, Ball M (2004) Patterns of extinction in prairie dog metapopulations: plague outbreaks follow El Niño events. Frontiers in Ecology and the Environment 2:235–240

    Google Scholar 

  • US Bureau of the Census (2000) Statistical Abstract of the United States. Washington, DC: US Government Printing Office

  • Yates TL, Mills JN, Parmenter CA, Ksiazek TG, Parmenter RR, Vande Castle JR, et al. (2002) The ecology and evolutionary history of an emergent disease: Hantavirus Pulmonary Syndrome. BioScience 52:989–998

    Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the City of Boulder Open Space Department, and Boulder County Parks and Open Space Department, particularly Mark Gershman, Cary Richardson, Bryan Pritchett, Lynn Riedel, Mark Brennan, Ann Wickman, and Jeanne Scholl for providing data on plague occurrence and information on prairie dog colonies in Boulder County. Brian Holmes helped assemble plague occurrence and prairie dog colony data in Phillips County, Montana. Sue Rodriguez-Pastor helped gather plague data from Boulder land management agencies. This research was supported by a grant (R-82909101-0) from the National Center for Environmental Research (NCER) STAR program of the US-EPA, and a grant from the NSF/NIH joint program in Ecology of Infectious Diseases (DEB-0224328).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sharon K. Collinge.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Collinge, S.K., Johnson, W.C., Ray, C. et al. Testing the Generality of a Trophic-cascade Model for Plague. EcoHealth 2, 102–112 (2005). https://doi.org/10.1007/s10393-005-3877-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-005-3877-5

Key words

Navigation