Assembling a safe and effective toolbox for integrated flea control and plague mitigation: Fipronil experiments with prairie dogs

Abstract

Background Plague, 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 findings During 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. Significance Deltamethrin 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.

Prairie dog responses to vector control and vaccination during an initial Yersinia pestis invasion

“…In both flea analyses, we considered dust treatment, year of sampling (for the first year of each annual re-encounter interval, as described below, 2007 [2007–2008] and 2008 [2008–2009]), BTPD age, BTPD sex, and an interaction between treatment and year. Flea parasitism on BTPDs varies seasonally at Conata/Badlands ( Eads et al, 2019 , 2022b ), so we included a variable for Julian day.…”

“…As an index to BTPD annual survival, we used re-encounter rates (the proportion of marked BTPDs that were recaptured the following year; Tripp et al, 2017 ; Matchett et al, 2021 ; Eads et al, 2022b ) analyzed with binomial logistic regression. This approach does not account for imperfect capture probabilities or potential emigration from study plots.…”

“…For the purposes herein, we define plague epizootics within a given species as resulting in the deaths of >90% of individuals over a wide area within weeks to months ( Biggins and Eads, 2019 ). We define enzootic plague as affecting lesser proportions of individuals, while acknowledging that enzootic plague can have strong ecological impacts ( Zeppelini et al, 2016 ) with significant conservation implications ( Biggins et al, 2021b , Biggins et al, 2021a , Biggins et al, 2010 ; Matchett et al, 2010 ; Goldberg et al, 2021 , Goldberg et al, 2022 ; Eads et al, 2022a , Eads et al, 2022b ).…”

Characterization in Potent Modulation on Voltage-Gated Na+ Current Exerted by Deltamethrin, a Pyrethroid Insecticide

“…Deltamethrin (DLT, decamethrin) is a cyclopropanecarboxylate ester obtained by formal condensation between 3-(2,2-dibromovinyl)-2,2-dimethylcyclopanecarboxylic acid and cyano(3-phenoxyphenyl)methanol [ 1 , 2 ]. It is viewed to be the active insecticide of the proinsecticide tralomethrin [ 3 , 4 , 5 ]. Pyrethroids like DLT or tefluthrin (Tef) have been demonstrated to modify the gating characteristics of voltage-gated Na + (Na V ) channels [ 6 , 7 , 8 , 9 , 10 ].…”

“…Pyrethroids like DLT or tefluthrin (Tef) have been demonstrated to modify the gating characteristics of voltage-gated Na + (Na V ) channels [ 6 , 7 , 8 , 9 , 10 ]. Deltamethrin (DLT), a neurotoxic type-II pyrethroid ester insecticide [ 3 , 4 , 5 ], has been demonstrated previously to cause a reversible sequence of motor symptoms in rats involving hind limb rigidity and choreoathetosis [ 2 , 11 , 12 , 13 ]. Alternatively, DLT was also reported to decrease Cl − currents through voltage-dependent Cl − channels and this action probably contributes the most to the features of poisoning with DLT or other type II pyrethroids [ 14 , 15 , 16 ].…”