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Classic flea-borne transmission does not drive plague epizootics in prairie dogs.

ABSTRACT: We lack a clear understanding of the enzootic maintenance of the bacterium (Yersinia pestis) that causes plague and the sporadic epizootics that occur in its natural rodent hosts. A key to elucidating these epidemiological dynamics is determining the dominant transmission routes of plague. Plague can be acquired from the bites of infectious fleas (which is generally considered to occur via a blocked flea vector), inhalation of infectious respiratory droplets, or contact with a short-term infectious reservoir. We present results from a plague modeling approach that includes transmission from all three sources of infection simultaneously and uses sensitivity analysis to determine their relative importance. Our model is completely parameterized by using data from the literature and our own field studies of plague in the black-tailed prairie dog (Cynomys ludovicianus). Results of the model are qualitatively and quantitatively consistent with independent data from our field sites. Although infectious fleas might be an important source of infection and transmission via blocked fleas is a dominant paradigm in the literature, our model clearly predicts that this form of transmission cannot drive epizootics in prairie dogs. Rather, a short-term reservoir is required for epizootic dynamics. Several short-term reservoirs have the potential to affect the prairie dog system. Our model predictions of the residence time of the short-term reservoir suggest that other small mammals, infectious prairie dog carcasses, fleas that transmit plague without blockage of the digestive tract, or some combination of these three are the most likely of the candidate infectious reservoirs.

SUBMITTER: Webb CT

PROVIDER: S-EPMC1434514 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundPlague, a widely distributed zoonotic disease of mammalian hosts and flea vectors, poses a significant risk to ecosystems throughout much of Earth. Conservation biologists use insecticides for flea control and plague mitigation. Here, we evaluate the use of an insecticide grain bait, laced with 0.005% fipronil (FIP) by weight, with black-tailed prairie dogs (BTPDs, Cynomys ludovicianus). We consider safety measures, flea control, BTPD body condition, BTPD survival, efficacy of plague mitigation, and the speed of FIP grain application vs. infusing BTPD burrows with insecticide dusts. We also explore conservation implications for endangered black-footed ferrets (Mustela nigripes), which are specialized predators of Cynomys.Principal findingsDuring 5- and 10-day laboratory trials in Colorado, USA, 2016-2017, FIP grain had no detectable acute toxic effect on 20 BTPDs that readily consumed the grain. During field experiments in South Dakota, USA, 2016-2020, FIP grain suppressed fleas on BTPDs for at least 12 months and up to 24 months in many cases; short-term flea control on a few sites was poor for unknown reasons. In an area of South Dakota where plague circulation appeared low or absent, FIP grain had no detectable effect, positive or negative, on BTPD survival. Experimental results suggest FIP grain may have improved BTPD body condition (mass:foot) and reproduction (juveniles:adults). During a 2019 plague epizootic in Colorado, BTPDs on 238 ha habitat were protected by FIP grain, whereas BTPDs were nearly eliminated on non-treated habitat. Applications of FIP grain were 2-4 times faster than dusting BTPD burrows.SignificanceDeltamethrin dust is the most commonly used insecticide for plague mitigation on Cynomys colonies. Fleas on BTPD colonies exhibit the ability to evolve resistance to deltamethrin after repeated annual treatments. Thus, more tools are needed. Accumulating data show orally-delivered FIP is safe and usually effective for flea control with BTPDs, though potential acute toxic effects cannot be ruled out. With continued study and refinement, FIP might be used in rotation with, or even replace deltamethrin, and serve an important role in Cynomys and black-footed ferret conservation. More broadly, our stepwise approach to research on FIP may function as a template or guide for evaluations of insecticides in the context of wildlife conservation.

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Classic flea-borne transmission does not drive plague epizootics in prairie dogs.

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