Abstract
Plague, caused by Yersinia pestis, is an exotic disease in North America circulating predominantly in wild populations of rodents and their fleas. Black-tailed prairie dogs (Cynomys ludovicianus) are highly susceptible to infection, often experiencing mortality of nearly all individuals in a town as a result of plague. The fleas of black-tailed prairie dogs are Oropsylla tuberculata cynomuris and Oropsylla hirsuta. We tested the efficiency of O. tuberculata cynomuris to transmit Y. pestis daily from 24 to 96 h postinfection and compared it to previously collected data for O. hirsuta. We found that O. tuberculata cynomuris has over threefold greater transmission efficiency (0.18 infected fleas transmit Y. pestis at 24 h postinfection) than O. hirsuta (0.05 fleas transmit). Using a simple model of flea-borne transmission, we combine these laboratory measurements with field data on monthly flea loads to compare the seasonal vectorial capacity of these two flea species. Coinciding with seasonal patterns of flea abundance, we find a peak in potential for flea-borne transmission in March, during high O. tuberculata cynomuris abundance, and in September–October when O. hirsuta is common. Our findings may be useful in determining the timing of insecticidal dusting to slow plague transmission in black-tailed prairie dogs.
Similar content being viewed by others
References
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. In: Transactions of the 67th North American Wildlife and Natural Resources Conference
Bacot AW, Martin CJ (1914) Observations on the mechanism of the transmission of plague by fleas. Journal of Hygiene 13(Suppl 3):423–439
Barnes AM (1993) A review of plague and its relevance to prairie dog populations and the black-footed ferret. Washington, DC: United States Fish and Wildlife Service
Bibikova VA (1977) Contemporary views on the interrelationships between fleas and the pathogens of human and animal diseases. Annual Review of Entomology 22:23–32
Biggerstaff BJ (2006) PooledInfRate, Version 3.0: a Microsoft Excel Add-In to compute prevalence estimates from pooled samples. Fort Collins, CO: Centers for Disease Control and Prevention
Biggins DE, Kosoy MY (2001) Influences of introduced plague on North American mammals: implications from ecology of plague in Asia. Journal of Mammology 82:906–916
Bossard RL, Hinkle NC, Rust MK (1998) Review of insecticide resistance in cat fleas (Siphonaptera: Pulicidae). Journal of Medical Entomology 35:415–422
Brinkerhoff JA, Markeson AB, Knouft JH, Gage KL, Montenieri JA (2006) Abundance patterns of two Oropsylla (Ceratophyllidae: Siphonaptera) species on black-tailed prairie dog (Cynomys ludovicianus) hosts. Journal of Vector Ecology 31:355–363
Burroughs AL (1947) Sylvatic plague studies: the vector efficiency of nine species of fleas compared with Xenopsylla cheopis. Journal of Hygiene 42:371–396
Chu MC (2000) Laboratory manual of plague diagnostic tests. Geneva, Atlanta: Centers for Disease Control and Prevention, 129 pp
Crawley MJ (2007) The R Book. Hoboken, NJ
Cully JF, Williams ES (2001) Interspecific comparisons of sylvatic plague in prairie dogs. Journal of Mammology 82:894–905
Degtyareva LV, Labunets NF, Osipova SP, Shchedrin VL (1990) The ability of flea species on common vole from mountainous Dagestan to transmit and preserve the causative agent of plague. Parazitologiya 24:106–112
Dunn OJ (1964) Multiple comparisons using rank sums. Technometrics 6:241–252
Ecke DH, Johnson CW (1952) Plague in Colorado and Texas. Public Health Monographs 6:1–53
Eisen RJ, Bearden SW, Wilder AP, Montenieri JA, Antolin MF, Gage KL (2006) Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proceedings of the National Academy of Sciences of the United States of America 103:15380–15385
Eisen RJ, Lowell JL, Montenieri JA, Bearden SW, Gage KL (2007a) Temporal dynamics of early-phase transmission of Yersinia pestis by unblocked fleas: secondary infectious feeds prolong efficient transmission by Oropsylla montana (Siphonaptera: Ceratophyllidae). Journal of Medical Entomology 44:672–677
Eisen RJ, Wilder AP, Bearden SW, Montenieri JA, Gage KL (2007b) Early-phase transmission of the plague agent, Yersinia pestis, by unblocked oriental rat fleas, Xenopsylla cheopis, is as efficient as transmission by blocked fleas. Journal of Medical Entomology 44:678–682
Engelthaler DM, Hinnebusch BJ, Rittner CM, Gage KL (2000) Quantitative-competitive PCR as a technique for exploring flea-Yersinia dynamics. American Journal of Tropical Medicine and Hygiene 62:552–560
Eskey CR, Haas VH (1940) Plague in the Western part of the United States. Washington, DC: US Government Printing Office
Fitzgerald JP (1970) The ecology of plague in prairie dogs and associated small mammals in South Park, Colorado. Thesis, Fort Collins, CO: Colorado State University
Fitzgerald JP (1993) The ecology of plague in Gunnison’s prairie dogs and suggestions for the recovery of black-footed ferrets. United States Fish and Wildlife Service Biological Report, Washington, DC
Gage KL, Kosoy MY (2005) Natural history of plague: perspectives from more than a century of research. Annual Review of Entomology 50:505–528
Gan NV, Voronova GA, Yuzvik LN, Belyaeva VA (1990) The capability of Rhadinopsylla rothschildi and R. dahurica fleas as vectors of plague pathogen in Transbaikal natural focus. Parazitologiya 24:151–154
Garrett-Jones C, Grab B (1964) The assessment of insecticidal impact on the malaria mosquito’s vectorial capacity, from data on the proportion of parous females. Bulletin of the World Health Organization 31:71–86
Hoogland JL (1995) The Black-tailed Prairie Dog: Social Life of a Burrowing Mammal. Chicago and London: The University of Chicago Press
Hoogland JL, Davis S, Benson-Amram S, Labruna D, Goossens B, Hoogland MA (2004) Pyraperm kills fleas and halts plague among Utah prairie dogs. The Southwestern Naturalist 49:376–383
Hubbard CA (1968) Fleas of Western North America. New York: Hafner Publishing
Jirakanjanakit N, Rongnoparut P, Saengtharatip S, Chareonviriyaphap T, Duchn S, Bellec C, et al. (2007) Insecticide susceptible/resistance status in Aedes (Stegomyia) aegypti and Aedes (Stegomyia) albopictus (Diptera: Culicidae) in Thailand during 2003–2005. Journal of Economic Entomology 100:545–550
Juneau P (2003) Using SAS to perform a single-stage multiple comparison procedure for all pair-wise comparisons in a one-way layout with unequal variances. In: Proceedings of the PharmaSUG 2003 Annual Conference May 4–7, 2003, Miami, Florida
MacDonald G (1957) The Epidemiology and Control of Malaria. London: Oxford University Press
Matambo TS, Abdalla H, Brooke BD, Koekemoer LL, Mnzava A, Hunt RH, et al. (2007) Insecticide resistance in the malarial mosquito Anopheles arabiensis and association with the kdr mutation. Medical and Veterinary Entomology 21:97–102
Maupin GO (1970) A survey of the siphonaptera and ectoparasite and inquiline acarina associated with the black-tailed prairie dog, Cynomys ludovicianus. Thesis, Fort Collins, CO: Colorado State University
R Development Core Team (2007) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing
Romero A, Potter MF, Potter DA, Haynes KF (2007) Insecticide resistance in the bed bug: a factor in the pest’s sudden resurgence? Journal of Medical Entomology 44:175–178
Salkeld DJ, Eisen RJ, Stapp P, Wilder AP, Lowell J, Tripp DW, et al. (2007) The potential role of swift foxes (Vulpes velox) and their fleas in prairie dog-plague (Yersinia pestis) outbreaks. Journal of Wildlife Diseases 43:425–431
Seery DB, Biggins DE, Montenieri JA, Enscore RE, Tanda DT, Gage KL (2003) Treatment of black-tailed prairie dog burrows with deltamethrin to control fleas (Insecta: Siphonaptera) and plague. Journal of Medical Entomology 40:718–722
Stapp P, Antolin MF, Ball M (2004) Patterns of extinction in prairie dog metapopulations: plague outbreaks follow El Nino events. Frontiers in Ecology and the Environment 2:235–240
Stevenson HL, Bai Y, Kosoy MY, Montenieri JA, Lowell JL, Chu MC, et al. (2003) Detection of novel Bartonella strains and Yersinia pestis in prairie dogs and their fleas (Siphonaptera: ceratophyllidae and pulicidae) using multiplex polymerase chain reaction. Journal of Medical Entomology 40:329–337
Tan WB, Sun LX, Zhang DH, Sun J, Qian J, Hu XB, et al. (2007) Cloning and overexpression of ribosomal protein L39 gene from deltamethrin-resistant Culex pipiens pipiens. Experimental Parasitology 115:369–378
Ubico SR, Maupin GO, Fagerstone KA, McLean RG (1988) A plague epizootic in the white-tailed prairie dogs (Cynomys leucurus) of Meeteetsee, Wyoming. Journal of Wildlife Diseases 24:399–406
United States Fish and Wildlife Service (2000) Endangered and threatened wildlife and plants; 12-month finding for a petition to list the black-tailed prairie dog as threatened. Federal Register 65:5476–5488
Webb CT, Brooks CP, Gage KL, Antolin MF (2006) Classic flea-borne transmission does not drive plague epizootics in prairie dogs. Proceedings of the National Academy of Sciences of the United States of America 103:6236–6241
Wilder AP (2007) Transmission of the plague bacterium Yersinia pestis by the prairie dog fleas Oropsylla hirsuta and Oropsylla tuberculata cynomuris (Siphonaptera: Ceratophyllidae). Thesis, Fort Collins, CO: Colorado State University
Wilder AP, Eisen RJ, Bearden SW, Montenieri JA, Gage KL, Antolin MF (in press) Oropsylla hirsuta (Siphonaptera: Ceratophyllidae) can support plague epizootics in black-tailed prairie dogs (Cynomys ludovicianus) by early-phase transmission of Yersinia pestis. Vector-Borne and Zoonotic Diseases
Acknowledgments
We thank C.T. Webb, W.C. Black IV, A.M. Meyer, and D.J. Salkeld for helpful discussions and comments on the manuscript, and A.B. Markeson for collection of flea load data. S.K. Collinge and C. Ray provided valuable methodological advice regarding prairie dog trapping and flea collection. Transmission studies were supported by the Centers for Disease Control and Prevention. Flea load data collection was supported by the National Science Foundation Ecology of Infectious Diseases program (EID 0327052) to M.F.A. and K.L.G., and Shortgrass Steppe Long Term Ecological Research (DEB 0217631) to Colorado State University. Funding to R.J.B. was provided by the National Center for Environmental Research (NCER) STAR program of the US-EPA (R-82909101-0) and the NSF/NIH joint program in Ecology of Infectious Diseases (DEB-0224328).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wilder, A.P., Eisen, R.J., Bearden, S.W. et al. Transmission Efficiency of Two Flea Species (Oropsylla tuberculata cynomuris and Oropsylla hirsuta) Involved in Plague Epizootics among Prairie Dogs. EcoHealth 5, 205–212 (2008). https://doi.org/10.1007/s10393-008-0165-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-008-0165-1