Flea abundance on black-tailed prairie dogs (cynomys ludovicianus) increases during plague epizootics

Vector-Borne and Zoonotic Diseases

Volumn 9, Issue 3, 2009, Pages 313-321

  Tripp, Daniel W ^a   Gage, Kenneth L ^b   Montenieri, John A ^b   Antolin, Michael F ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

Black tailed prairie dog; Cynomys ludovicianus; Plague; Yersinia

Indexed keywords

ARTICLE; CYNOMYS LUDOVICIANUS; DISEASE CARRIER; DISEASE TRANSMISSION; DOG; EPIZOOTIOLOGY; FEMALE; FLEA; HOST; INFESTATION; MALE; MAMMAL; MORTALITY; NONHUMAN; PLAGUE; PRAIRIE; PRIORITY JOURNAL; PULEX SIMULANS; SPRING; UNITED STATES; YERSINIA; YERSINIA PEPTIS;

ANIMALS; COLORADO; DISEASE OUTBREAKS; ECTOPARASITIC INFESTATIONS; FEMALE; FLEAS; MALE; PLAGUE; SCIURIDAE; YERSINIA PESTIS;

ANIMALIA; BACTERIA (MICROORGANISMS); CYNOMYS; CYNOMYS LUDOVICIANUS; MAMMALIA; OROPSYLLA; PULEX SIMULANS; SIPHONAPTERA (FLEAS); YERSINIA; YERSINIA PESTIS;

EID: 68149183777     PISSN: 15303667     EISSN: None     Source Type: Journal    
DOI: 10.1089/vbz.2008.0194     Document Type: Article

References (52)

1. Anderson, SH, Williams, ES. Plague in a complex of white-tailed prairie dogs and associated small mammals in Wyoming. J Wildl Dis 1997; 33:720-732.
2. Antolin, MF, Gober, P, Luce, B, Biggins, DE, et al. The influence of sylvatic plague on North American wildlife at the landscape level, with special emphasis on black-footed ferret and prairie dog conservation. Proceedings of the 67th North American Wildlife and Natural Resources Conference 2002; 67:104-127.
3. Brinkerhoff, JA, Markeson, AB, Knouft, JH, Gage, KL, et al. Abundance patterns of two Oropsylla (Ceratophyllidae: Siphonaptera) species on black-tailed prairie dog (Cynomys ludovicianus) hosts. J Vector Ecol 2006; 31:355-363.
4. Burroughs, AL. Sylvatic plague studies. The vector efficiency of nine species of fleas compared with Xenopsylla cheopis. J Hyg 1947; 45:371-396.
5. Cavanaugh, DC. Specific effect of temperature upon transmission of the plague bacillus by the oriental rat flea. Am J Trop Med Hyg 1971; 20:264-273.
6. Cavanaugh, DC, Marshall, JR. The influence of climate on the seasonal prevalence of plague in the Republic of Vietnam. J Wildl Dis 1972; 8:85-94.
7. Chu, MC. Laboratory Manual of Plague Diagnostic Tests. Fort Collins, CO: Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, 2000.
8. Collinge, SK, Johnson, WC, Ray, C, Matchett, R, et al. Testing the generality of a trophic cascade model for plague. EcoHealth 2005; 2:1-11.
9. Crawley, MJ. The R Book. New York: John Wiley, 2007.
10. Cully, JF, Carter, LG, Gage, KL. New records of sylvatic plague in Kansas. J Wildl Dis 2000; 36:389-392.
11. Cully, JF, Williams, ES. Interspecific comparisons of sylvatic plague in prairie dogs. J Mammal 2001; 82:894-905.
12. Ecke, DH, Johnson, CW. Plague in Colorado. In: Plague in Colorado and Texas. Washington, DC: Public Health Monograph No. 6. U.S. Government Printing Office, 1952:1-37.
13. Eisen, RJ, Bearden, SW, Wilder, AP, Montenieri, JA, et al. Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc Natl Acad Sci USA 2006; 103:15380-15385.
14. Eisen, RJ, Wilder, AP, Bearden, SW, Montenieri, JA, et al. Early-phase transmission of Yersinia pestis by unblocked Xenopsylla cheopis (Siphonaptera: Pulicidae) is as efficient as transmission by blocked fleas. J Med Entomol 2007; 44:678-682.
15. Enscore, RE, Biggerstaff, BJ, Brown, TL, Fulgham, RF, et al. Modeling relationships between climate and the frequency of human plague cases in the southwestern United States, 1960- 1997. Am J Trop Med Hyg 2002; 66:186-196.
16. Eskey, CR, Haas, VH. Plague in the Western Part of the United States. Washington DC: US Public Health Service Bulletin No. 254. US Government Printing Office, 1940:1-83.
17. Gage, KL, Montenieri, JA, Thomas, RE. The role of predators in the ecology, epidemiology, and surveillance of plague in the United States. In: Halverson, WS, Crabb, AC, eds. Proceedings of the 16th Vertebrate Pest Conference, University of California, Davis, 1994:201-206.
18. Gage, KL, Kosoy, MY. Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 2005; 50:505-528.
19. Hinnebusch, BJ, Perry, RD, Schwan, TG. Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 1996; 273:367-370.
20. Hinnebusch, BJ, Fischer, ER, Schwan, TG. Evaluation of the role of the Yersinia pestis plasminogen activator and other plasmid-encoded factors in temperature-dependant blockage of the flea. Am J Infect Dis 1998; 178:1406-1415.
21. Holmes, BE, Foresman, KR, Matchett, MR. No evidence of persistent Yersinia pestis infection at prairie dog colonies in north-central Montana. J Wildl Dis 2006; 42:164-169.
22. Hoogland, JL. The Black-Tailed Prairie Dog: Social Life of a Burrowing Mammal. Chicago: The University of Chicago Press, 1995.
23. Hoogland, JL, Davis, S, Benson-Amram, S, Labruna, D, et al. Pyraperm kills fleas and halts plague among Utah prairie dogs. Southwest Nat 2004; 49:376-383.
24. Hopla, CE. A study of the host associations and zoogeography of Pulex. In: Traub, R, Starcke, H, eds. Fleas. Proceedings of the International Conference on Fleas. Rotterdam, The Netherlands: AA Balkema Publishers, 1980:185-207.
25. Hubbard, CA. Fleas of Western North America. New York: Hafner Publishing Co., 1968.
26. Indian Plague Commission. On the seasonal prevalence of plague in India. J Hyg 1908; Plague Suppl 4:266-310.
27. Kartman, L, Prince, FM. Studies on Pasturella pestis in fleas. V. The experimental plague-vector efficiency of wild rodent fleas compared with Xenopsylla cheopis, together with observation on the influence of temperature. Am J Trop Med Hyg 1956; 5:1058-1070.
28. Krasnov, BR, Khokhlova, IS, Fielden, LJ, Burdelova, NI. Effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). J Med Entomol 2001; 38:629-637.
29. Krasnov, BR, Burdelova, NV, Shenbrot, GI, Khokhlova, IS. Annual cycles of four flea species in the central Negev desert. Med Vet Entomol 2002; 16:266-276.
30. Krasnov, BR, Shenbrot, GI, Mouillot, D, Khokhlova, IS, et al. Ecological characteristics of flea species relate to their suitability as plague vectors. Oecologia 2006; 149:474-481.
31. Maupin, GO. A survey of the siphonaptera and ectoparasite and inquiline acarina associated with the black-tailed prairie dog, Cynomys ludovicianus. Masters thesis. Colorado State University, Fort Collins, CO, 1970.
32. National Climate Data Center [Online]. 2007. Available at www.ncdc.noaa.gov. Accessed 2007 September 14.
33. Pauli, JN, Buskirk, SW, Williams, ES, Edwards, WH. A plague epizootic in the black-tailed prairie dog (Cynomys ludovicianus). J Wildl Dis 2006; 42:74-80.
34. Poland, JD, Barnes, AM. Plague. In: Steele, JF, ed. CRC Handbook Series in Zoonoses, Section A: Bacterial, Rickettsial, and Mycotic Diseases. Boca Raton: CRC Press, 1979:515-597.
35. Pollitzer, R. Plague. WHO Monogr Ser 1954; 22:1-698.
36. R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing, 2007.
37. Reichardt, TR, Galloway, TD. Seasonal occurrence and reproductive status of Opisocrostis bruneri (Siphonaptera: Ceratophyllidae), a flea on Franklin's ground squirrel, Spermophilus franklinii (Rodentia: Sciruridae) near Birds Hill Park, Manitoba. J Med Entomol 1994; 31:105-113.
38. Roelle, JE, Miller, BJ, Godbey, JL, Biggins, DE. Recovery of the black-footed ferret: progress and continuing challenges. In: Scientific Investigations Report 2005-5293. Proceedings of the Symposium on the Status of the Black-footed Ferret and Its Habitat, 2004 Jan 28-29, Fort Collins, CO. U.S Geological Survey, 2006:1-288.
39. Salkeld, DJ, Eisen, RJ, Stapp, P, Wilder, AP, et al. The potential role of swift foxes (Vulpes velox) and their fleas in prairie dog-plague (Yersinia pestis) outbreaks. J Wildl Dis 2007; 43: 425-431.
40. Salkeld, DJ, Stapp, P. Prevalence and abundance of fleas in black-tailed prairie dog burrows: implications for the transmission of plague (Yersinia pestis). J Parasitol 2008; 94:616-621.
41. Savage, LT. Population genetics, fragmentation and plague in black-tailed prairie dogs (Cynomys ludovicianus). Ph.D. dissertation. Colorado State University, Fort Collins, CO, 2007.
42. Seery, DB, Biggins, DE, Montenieri, JA, Enscore, RE, et al. Treatment of black-tailed prairie dog burrows with deltamethrin to control fleas (Insecta: Siphonaptera) and plague. J Med Entomol 2003; 40:718-722.
43. Silverman, J, Rust, MK, Reierson, DA. Influence of temperature and humidity on survival and development of the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). J Med Entomol 1981; 18:35-78.
44. Sokal, RR, Rohlf, FJ. Biometry: The Principals and Practice of Statistics in Biological Research, 3rd edition. New York: WH Freeman and Co., 1995.
45. Stapp, P, Antolin, MF, Ball, M. Patterns of extinction in prairie dog metapopulations: plague outbreaks follow El Nino events. Front Ecol Environ 2004; 2:235-240.
46. Stark, HE. The Siphonaptera of Utah; Their Taxonomy, Distribution, Host Relations, and Medical Importance. Atlanta: US Department of Health, Education, and Welfare, 1958.
47. Stevenson, HL, Bai, Y, Kosoy, MY, Montenieri, JA, et al. Detection of novel Bartonella strains and Yersinia pestis in prairie dogs and their fleas (Siphonaptera: ceratophyllidae and pulicidae) using multiplex polymerase chain reaction. J Med Entomol 2003; 40:329-337.
48. Venables, WN, Ripley, BD. Applied Statistics with S. 4th edition. New York: Springer, 2002.
49. Webb, CT, Brooks, CP, Gage, KL, Antolin, MF. Classic flea-borne transmission does not drive plague epizootics in prairie dogs. Proc Natl Acad Sci USA 2006; 103:6236-6241.
50. Wilcomb, MJ. A study of prairie dog burrow systems and the ecology of their arthropod inhabitants in central Oklahoma. Ph.D. dissertation. University of Oklahoma, Norman, OK, 1954.
51. Wilder, AP, Eisen, RJ, Bearden, SW, Montenieri, JA, et al. Transmission efficiency of two flea species (Oropsylla tuberculata cynomuris and Oropsylla hirsuta) involved in plague epizootics among prairie dogs. EcoHealth 2008; 5:205-212.
52. Wilson, K, Bjornstad, ON, Dobson, AP, Merler, S, et al. Heterogeneities in macroparasite infections: patterns and processes. In: Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H, et al. eds. The Ecology of Wildlife Diseases. Oxford: Oxford University Press, 2002:6-44.