Plague originated in Asia as a flea-borne zoonosis of mammalian hosts. Today, the disease is distributed nearly worldwide. In western United States of America, plague is maintained, transmitted, and amplified in diverse communities of rodents and fleas. We examined flea diversity on three species of prairie dogs (Cynomys spp., PDs) and six species of sympatric small rodents in Montana and Utah, United States of America. Among 2896 fleas, 19 species were identified; 13 were found on PDs and 9 were found on small rodents. In Montana, three flea species were found on PDs; the three species parasitize PDs and mice. In Utah, 12 flea species were found on PDs; the 12 species parasitize PDs, mice, voles, chipmunks, ground squirrels, rock squirrels, and marmots. Diverse flea communities and their willingness to parasitize many types of hosts, across multiple seasons and habitats, may favor plague maintenance and transmission. Flea parasitism on Peromyscus deer mice varied directly with elevation. Fleas are prone to desiccation, and might prosper at higher, mesic elevations; in addition, Peromyscus nest characteristics may vary with elevation. Effective management of plague is critical. Plague management is probably most effective when encompassing communities of rodents and fleas. Treatment of PD burrows with 0.05% deltamethrin dust, which suppressed fleas on PDs for >365 days, suppressed fleas on small rodents for at least 58 days. At one site, deltamethrin suppressed fleas on small rodents for at least 383 days. By simultaneously suppressing fleas on PDs and small rodents, deltamethrin should promote ecosystem resilience and One Health objectives.
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References
1.
AchtmanM, ZurthK, MorelliG, TorreaG, et al.Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci USA, 1999; 96:14043–14048.
2.
AntolinMF, GageKL, LowellJ. What is a plague focus?. Vector Borne Zoonot Dis, 2010; 10:S2.
3.
AntolinMF, GoberP, LuceB, BigginsDE, 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. In: RahmJ, ed. Transactions of the Sixty-Seventh North American Wildlife and Natural Resources Conference, April 3–7. Washington, D.C.: U.S. Fish and Wildlife Service, 2002:105–127.
4.
ArjoWM, GeseEM, BromleyC, KozlowskiA, et al.Serologic survey for diseases in free-ranging coyotes (Canis latrans) from two ecologically distinct areas of Utah. J Wild Dis, 2003; 39:449–455.
5.
BaltazardM. The conservation of plague in invertebrate foci. J Hyg Epidemiol Microbiol Immunol, 1964; 8:409–421.
6.
BarnesAM. Surveillance and control of bubonic plague in the United States. Symp Zool Soc Lond, 1982; 50:237–270.
7.
BigginsDE, EadsDA. Prairie dogs, persistent plague, flocking fleas, and pernicious positive feedback. Front Vet Sci Parasitol, 2019; [Epub ahead of print]; DOI: 10.3389/fvets.2019.00075.
8.
BigginsDE, GodbeyJL, GageKL, CarterLG, et al.Vector control improves survival of three species of prairie dogs (Cynomys) in areas considered enzootic for plague. Vector Borne Zoonot Dis, 2010; 10:17–26.
9.
BigginsDE, KosoyMY. Influences of introduced plague on North American mammals: Implications from ecology of plague in Asia. J Mamm, 2001; 82:906–916.
10.
BrinkheroffRJ. Mammal and flea occurrence in association with black-tailed prairie dog (Cynomys ludovicianus) colonies: Implications for interspecific plague transmission. PhD dissertation, University of Colorado, Boulder, CO, 2008.
11.
BronGM. The role of short-lived rodents and their fleas in plague ecology on prairie dog colonies. PhD dissertation, University of Wisconsin-Madison, Madison, WI, 2017.
12.
BronGM, RichgelsKL, SamuelMD, PojeJE, et al.Impact of sylvatic plague vaccine on non-target small rodents in grassland ecosystems. EcoHealth, 2018; 15:555–565.
13.
D'ortenzioE, LemaîtreN, BrouatC, LoubetP, et al.Plague: Bridging gaps towards better disease control. Med Maladies Infect, 2018; 48:307–317.
14.
EadsDA. Swabbing prairie dog burrows for fleas that transmit Yersinia pestis: Influences on efficiency. J Med Entomol, 2017; 54:1273–1277.
15.
EadsDA. Data on the efficacy of deltamethrin flea control with small rodents on prairie dog colonies in Montana and Utah, 2001–2004. USGS ScienceBase, 2021; U.S. Geological Survey data release, https://doi.org/10.5066/P9OFMMCC.
16.
EadsDA, BigginsDE. Plague bacterium as a transformer species in prairie dogs and the grasslands of western North America. Conserv Biol, 2015; 29:1086–1093.
17.
EadsDA, BigginsDE. Plague management on prairie dog colonies: Degree and duration of deltamethrin flea control. J Vector Ecol, 2019; [Epub ahead of print]; DOI: 10.1111/jvec.12327.
18.
EadsDA, BigginsDE, LongDH, GageKL, et al.Droughts may increase the susceptibility of prairie dogs to fleas: Incongruity with hypothesized mechanisms of plague cycles in rodents. J Mamm, 2015; 97:1044–1053.
19.
EasterdayWR, KausrudKL, StarB, HeierL, et al.An additional step in the transmission of Yersinia pestis?. ISME J, 2012; 6:231–236.
20.
EisenRJ, BorchertJN, MpangaJT, AtikuLA, et al.Flea diversity as an element for persistence of plague bacteria in an east African plague focus. PLoS One, 2012; 7:e35598.
21.
EisenRJ, EisenL, GageKL. Studies of vector competency and efficiency of North American fleas for Yersinia pestis: State of the field and future research needs. J Med Entomol, 2009; 46:737–744.
22.
EisenRJ, HolmesJL, SchotthoeferAM, VetterSM, et al.Demonstration of early-phase transmission of Yersinia pestis by the mouse flea, Aetheca wagneri (Siphonaptera: Ceratophyllidae), and implications for the role of deer mice as enzootic reservoirs. J Med Entomol, 2008; 45:1160–1164.
23.
EisenRJ, LowellJL, MontenieriJA, BeardenSW, et al.Temporal dynamics of early-phase transmission of Yersinia pestis by unblocked fleas: Secondary infectious feeds prolong efficient transmission by Oropsylla montana (Siphonaptera: Ceratophyllidae). J Med Entomol, 2007; 44:672–677.
24.
FoleyP, RothT, FoleyJ, RayC. Rodent-pika parasite spillover in western North America. J Med Entomol, 2017; 54:1251–1257.
25.
FranklinHA, StappP, CohenA. Polymerase chain reaction (PCR) identification of rodent blood meals confirms host sharing by flea vectors of plague. J Vector Ecol, 2010; 35:363–371.
26.
GageKL, KosoyMY. Recent trends in plague ecology. In: Roelle JE, Miller BJ, Godbey JL, Biggins DE, eds. U.S. Geological Survey Scientific Investigations Report 2005-5293. U.S. Geological Survey, Reston, VA,, 2006:213–231.
GoldbergAR. Diet, disease, and hibernation behavior of Northern Idaho Ground Squirrels. PhD dissertation, University of Idaho, Moscow, Idaho, 2018.
29.
GoldbergAR, ConwayCJ, BigginsDE. Flea sharing among sympatric rodent hosts: Implications for potential plague effects on a threatened sciurid. Ecosphere, 2020; 11:e03033.
30.
GrahamCB, WoodsME, VetterSM, PetersenJM, et al.Evaluation of the effect of host immune status on short-term Yersinia pestis infection in fleas with implications for the enzootic host model for maintenance of Y. pestis during interepizootic periods. J Med Entomol, 2014; 51:1079–1086.
31.
HawlenaH, AbramskyZ, KrasnovBR. Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia, 2005; 146:200–208.
32.
HoldenriedR, QuanSF. Susceptibility of New Mexico rodents to experimental plague. Public Health Rep, 1956; 71:979–984.
33.
HoplaCE. A study of the host associations and zoogeography of Pulex. In: TraubR, StarckeH, eds. Fleas: Proceedings of the International Conference on Fleas. Peterborough, United Kingdom: Ashton Wold, June 21–25, 1977; 1980:185–207.
34.
JachowskiDS, BrownNL, WehtjeM, TrippDW, et al.Mitigating plague risk in Utah prairie dogs: Evaluation of a systemic flea-control product. Wild Soc Bull, 2012; 36:167–175.
35.
JamesWB, BoothES. Biology and Life History of the Sagebrush Vole. Department of Biological Sciences of Walla Walla College and the Biological Station, Department of Biological Sciences, College Place, WA, 1952.
36.
KalabukhovNI. The structure and dynamics of natural foci of plague. J Hyg Epidemiol Microbiol Immunol, 1965; 9:147–159.
37.
KeimPS, WagnerDM. Humans and evolutionary and ecological forces shaped the phylogeography of recently emerged diseases. Nat Rev Microbiol, 2009; 7:813–821.
38.
KosoyM, ReynoldsP, BaiY, SheffK, et al.Small-scale die-offs in woodrats support long-term maintenance of plague in the US southwest. Vector Borne Zoonot Dis, 2017; 17:635–644.
39.
KraftJP, StappP. Movements and burrow use by northern grasshopper mice as a possible mechanism of plague spread in prairie dog colonies. J Mamm, 2013; 94:1087–1093.
40.
KrasnovBR. Functional and Evolutionary Ecology of Fleas: A Model for Ecological Parasitology. Cambridge, United Kingdom: Cambridge University Press, 2008.
41.
KrasnovBR, ShenbrotGI, MouillotD, KhokhlovaIS, et al.Ecological characteristics of flea species relate to their suitability as plague vectors. Oecologia, 2006; 149:474–481.
42.
LehaneB. The Compleat Flea. New York: The Viking Press, 1969.
43.
LorangeEA, RaceBL, SebbaneF, HinnebuschBJ. Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. J Infect Dis, 2005; 191:1907–1912.
44.
MaestasLP, BrittenHB. Effects of deltamethrin treatment on small mammal and ectoparasite population dynamics and plague prevalence in a North American mixed-grass prairie system. Vector Borne Zoonot Dis, 2019; [Epub ahead of print]; DOI: 10.1089/vbz.2018.2332.
MullicanTR, KellerBL. Burrows of the sagebrush vole (Lemmiscus curtatus) in southeastern Idaho. Great Basin Naturalist, 1987; 47:276–279.
47.
NeerinckxSB, PetersonAT, GulinckH, DeckersJ, et al.Geographic distribution and ecological niche of plague in sub-Saharan Africa. Int J Health Geogr, 2008; 7:54.
48.
NelsonBC. Plague studies in California—the roles of various species of sylvatic rodents in plague ecology in California. Proceeding of the 9th Vertebrate Pest Conference. 1980:89–96. Available at http://digitalcommons.unl.edu, University of California, Davis, California, USA.
49.
RamakrishnanS. Impact of enzootic plague on Neotoma mexicana in Northern New Mexico. MS Thesis, New Mexico Highlands University, Las Vegas, New Mexico, 2018.
50.
ReidRA. A Field Guide to Mammals of North America North of Mexico. New York: Houghton Mifflin Company, 2006.
51.
RussellRE, AbbottRC, TrippDW, RockeTE. Local factors associated with on-host flea distributions on prairie dog colonies. Ecol Evol, 2018; 8:8951–8972.
52.
SalkeldDJ, Salathé M, Stapp P, Jones JH. Plague outbreaks in prairie dog populations explained by percolation thresholds of alternate host abundance. Proc Natl Acad Sci USA, 2010; 107:14247–14250.
53.
SalkeldDJ, StappP. No evidence of deer mouse involvement in plague (Yersinia pestis) epizootics in prairie dogs. Vector Borne Zoonot Dis, 2008; 8:331–338.
54.
SeeryDB, BigginsDE, MontenieriJA, EnscoreRE, 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.
55.
SmithGW, JohnsonDR. Demography of a Townsend ground squirrel population in southwestern Idaho. Ecology, 1985; 66:171–178.
56.
StappP, SalkeldDJ, EisenRJ, PappertR, et al.Exposure of small rodents to plague during epizootics in black-tailed prairie dogs. J Wildl Dis, 2008; 44:724–730.
57.
ThiagarajanB, BaiY, GageKL, CullyJFJr. Prevalence of Yersinia pestis in rodents and fleas associated with black-tailed prairie dogs (Cynomys ludovicianus) at Thunder Basin National Grassland, Wyoming. J Wild Dis, 2008; 44:731–736.
58.
ThomasRE. A review of flea collection records from Onychomys leucogaster with observations on the role of grasshopper mice in the epizoology of wild rodent plague. Great Basin Nat, 1988; 31:83–95.
59.
WhickerAD, DetlingJK. Ecological consequences of prairie dog disturbances. BioScience, 1988; 38:778–785.
60.
WilkeningJL, RayC, BeeverEA, BrussardPF. Modeling contemporary range retraction in Great Basin pikas (Ochotona princeps) using data on microclimate and microhabitat. Quat Int, 2011; 235:77–88.
61.
WilliamsSK, SchotthoeferAM, MontenieriJA, HolmesJL, et al.Effects of low-temperature flea maintenance on the transmission of Yersinia pestis by Oropsylla montana. Vector Borne Zoonot Dis, 2013; 13:468–478.
62.
WimsattJ, BigginsDE. A review of plague persistence with special emphasis on fleas. J Vector Borne Dis, 2009; 46:85–99.
63.
XuL, StigeLC, KausrudKL, AriTB, et al.Wet climate and transportation routes accelerate spread of human plague. Proc R Soc London Ser B, 2014; 281:20133159.
64.
ZeppeliniCG, de AlmeidaAMP, Cordeiro-EstrelaP. Zoonoses as ecological entities: A case review of plague. PLoS Negl Trop Dis, 2016; 10:e0004949.
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