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

We evaluated the invasion of plague bacteria Yersinia pestis into a population of black-tailed prairie dogs (Cynomys ludovicianus; BTPDs) in South Dakota. We aimed to ascertain if Y. pestis invaded slowly or rapidly, and to determine if vector (flea) control or vaccination of BTPDs assisted in increasing survival rates. We sampled BTPDs in 2007 (before Y. pestis documentation), 2008 (year of confirmed invasion), and 2009 (after invasion). We estimated annual BTPD re-encounter rates on three 9-ha plots treated annually with deltamethrin dust for flea control and three 9-ha plots lacking dust. In 2007 and 2008, approximately half the adult BTPDs live-trapped were injected subcutaneously with either an experimental plague vaccine (F1-V fusion protein) or placebo formulation; the remaining individuals were not inoculated. From 2007 to 2009, we sampled 1559 BTPDs on 2542 occasions. During 2007-2008, the prevalence and intensity of fleas on BTPDs were 69-97% lower on the dusted vs. no dust plots. From 2007 to 2008, the annual re-encounter rate of non-inoculated BTPDs was 150% higher on the dusted vs. no dust plots. During the same interval on the dusted plots, the re-encounter rate was 55% higher for vaccinated adult female BTPDs vs. nonvaccinated adult females, but the annual re-encounter rate was 19% lower for vaccinated adult males. By late August 2008, BTPDs were nearly extirpated from the no dust plots. During 2007-2008 and 2008-2009 on the dusted plots, which persisted, the BTPD re-encounter rate was 41% higher for vaccinated vs. non-vaccinated adult females but 35% lower for vaccinated adult males. Yersinia pestis erupted with vigor as it invaded. Flea control enhanced BTPD survival but did not offer full protection. Flea control and F1-V vaccination seemed to have additive, positive effects on adult females. Annual re-encounter rates were reduced for vaccinated adult males; additional experimentation is needed to further evaluate this trend.

Plague mitigation for prairie dog and black-footed ferret conservation: Degree and duration of flea control with 0.005% fipronil grain bait.

Sylvatic plague, a primarily flea-borne zoonosis, is a significant threat to prairie dogs (Cynomys spp., PDs) and their specialized predators, endangered black-footed ferrets (Mustela nigripes, BFFs). Host-fed fipronil baits have proven effective in controlling fleas on PDs for the purposes of plague mitigation and BFF conservation. Currently, annual treatments are the norm. We tested the long-term efficacy of fipronil bait treatments with black-tailed PDs (C. ludovicianus, BTPDs) and BFFs in South Dakota, USA. During 2018-2020, we provided BTPDs on 21 sites with grain bait formula, laced with 0.005% fipronil (50 â€‹mg/kg); 18 non-treated sites functioned as baselines. In 2020-2022, we live-trapped, anesthetized, and combed BTPDs for fleas. Flea control was significant for at least 639-885 days. Flea abundance on the treated sites was < 0.5 fleas/BTPD for ∼750 days. During 2020-2022, we sampled BFFs for fleas on 4 BTPD colonies treated with fipronil grain bait and 8 non-treated colonies. Flea control was significant with BFFs, but flea abundance began to rebound within ∼240 days post-treatment. When feasible, the combination of insecticide treatments, such as fipronil baits, and BFF vaccination against plague provide a "two-pronged" protection approach for these endangered carnivores. If fipronil bait treatments are less effective with predatory BFFs than PDs, as found herein, the "two-pronged" approach might be used to protect BFFs and biennial fipronil bait treatments might be used to protect PDs. If BFF vaccination is not possible, or few BFFs can be vaccinated, annual fipronil bait treatments might be used as a precaution to protect BFFs. Flea densities might be surveyed to determine when/where more frequent treatments seem useful.

Estimating parasite infrapopulation size given imperfect detection: Proof-of-concept with ectoparasitic fleas on prairie dogs.

Parasite infrapopulation size - the population of parasites affecting a single host - is a central metric in parasitology. However, parasites are small and elusive such that imperfect detection is expected. Repeated sampling of parasites during primary sampling occasions (e.g., each host capture) informs the detection process. Here, we estimate flea (Siphonaptera) infrapopulation size on black-tailed prairie dogs (Cynomys ludovicianus, BTPDs) as a proof-of-concept for estimating parasite infrapopulations given imperfect detection. From Jun-Aug 2011, we live-trapped 299 BTPDs for a total of 573 captures on 20 plots distributed among 13 colonies at the Vermejo Park Ranch, New Mexico, USA. During each capture, an anesthetized BTPD was combed 3 times consecutively, 15 s each, to remove and count fleas. Each flea (n = 4846) was linked to the BTPD from which it was collected and assigned an encounter history ('100', '010', '001'). We analyzed the encounter histories using Huggins closed captures models, setting recapture probabilities to 0, thereby accounting for flea removal from hosts. The probability of detecting an individual flea (p) increased with Julian date; field personnel may have become more efficient at combing fleas as the field season progressed. Combined p across 3 combings equaled 0.99. Estimates of flea infrapopulation size were reasonable and followed the negative binomial distribution. Our general approach may be broadly applicable to estimating infrapopulation sizes for parasites. The utility of this approach increases as p declines but, if p is very low, inference is likely limited.

LETHAL EFFECTS ON FLEA LARVAE OF FIPRONIL IN HOST FECES: POTENTIAL BENEFITS FOR PLAGUE MITIGATION.

Plague, caused by the bacterium Yersinia pestis, is a zoonotic disease of mammalian hosts and flea vectors. Fipronil baits have been used to suppress adult fleas for plague mitigation. The degree and duration of flea control may increase if fipronil also kills other stages in the flea life cycle. We fed grain treated with 0.005% fipronil by weight, or nontreated grain, to black-tailed prairie dogs (Cynomys ludovicianus), which excrete fipronil and metabolites in their feces after consuming fipronil in their diet. We presented prairie dog feces to 331 larval Oropsylla montana (Siphonaptera: Ceratophyllidae). When exposed to feces lacking fipronil or metabolites, 84% of larvae survived for 24 h. In contrast, survival declined to 42% for larvae contacting feces from fipronil-treated prairie dogs. Just 7% of larvae consuming feces from fipronil-treated prairie dogs survived. Fipronil and metabolites may persist in host feces for several months or longer in prairie dog burrows where flea larvae dwell and forage. The lethal effects of fipronil on adult and larval fleas (and perhaps other life stages) may help to explain why fipronil baits are capable of suppressing fleas on prairie dogs for ≥12 mo.

FLEA CONTROL ON PRAIRIE DOGS (CYNOMYS SPP.) WITH FIPRONIL BAIT PELLETS: POTENTIAL PLAGUE MITIGATION TOOL FOR RAPID FIELD APPLICATION AND WILDLIFE CONSERVATION.

Sylvatic plague is a widespread, primarily flea-vectored disease in western North America. Because plague is highly lethal to endangered black-footed ferrets (Mustela nigripes, BFFs) and the prairie dogs (Cynomys spp., PDs) on which BFFs depend for habitat and prey, minimizing the impacts of plague is a priority at BFF reintroduction sites. We developed a new, flour-based bait pellet containing 0.84 mg of fipronil and weighing ∼1.25 g (FipBits). We measured the degree and duration of flea control on black-tailed PDs (C. ludovicianus) in Montana and on Gunnison's PDs (C. gunnisoni) in Arizona, USA from 2018-2020. FipBits were distributed on treated plots one time at a rate of 125/ha. Fleas were virtually eliminated in Montana from 1 mo posttreatment to 1 yr later and remained substantially depressed 2 yr posttreatment. With the split colony design, we probably underestimated the degree of flea control achieved with FipBits due to crossover edge effects along the arbitrary line dividing the plots. Flea control in Arizona was significant from 1 mo posttreatment to 1 yr later, but flea abundance had recovered by 2 yr posttreatment. Flea control was evaluated from 2020-2021 in South Dakota, USA on four plots treated with three concentrations of fipronil in FipBits (0.68, 0.71, and 0.83 mg/FipBit). Fleas were essentially eliminated for 10 mo on the 0.83-mg plot and were substantially reduced on the two 0.71-mg plots. Fleas were reduced on the 0.68-mg plot, but the degree of control was less than observed on other treated plots. Impacts of plague on PDs and BFFs would probably be greatly reduced by the levels of flea control observed with FipBits. Options for expanded FipBit evaluations are being pursued for what may become a highly practical, affordable, and effective plague mitigation tool.

Plague and Trace Metals in Natural Systems.

All pathogenic organisms are exposed to abiotic influences such as the microclimates and chemical constituents of their environments. Even those pathogens that exist primarily within their hosts or vectors can be influenced directly or indirectly. Yersinia pestis, the flea-borne bacterium causing plague, is influenced by climate and its survival in soil suggests a potentially strong influence of soil chemistry. We summarize a series of controlled studies conducted over four decades in Russia by Dr. Evgeny Rotshild and his colleagues that investigated correlations between trace metals in soils, plants, and insects, and the detection of plague in free-ranging small mammals. Trace metal concentrations in plots where plague was detected were up to 20-fold higher or lower compared to associated control plots, and these differences were >2-fold in 22 of 38 comparisons. The results were statistically supported in eight studies involving seven host species in three families and two orders of small mammals. Plague tended to be positively associated with manganese and cobalt, and the plague association was negative for copper, zinc, and molybdenum. In additional studies, these investigators detected similar connections between pasturellosis and concentrations of some chemical elements. A One Health narrative should recognize that the chemistry of soil and water may facilitate or impede epidemics in humans and epizootics in non-human animals.

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

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.

Reevaluation of the Role of Blocked Oropsylla hirsuta Prairie Dog Fleas (Siphonaptera: Ceratophyllidae) in Yersinia pestis (Enterobacterales: Enterobacteriaceae) Transmission.

Prairie dogs in the western United States experience periodic epizootics of plague, caused by the flea-borne bacterial pathogen Yersinia pestis. An early study indicated that Oropsylla hirsuta (Baker), often the most abundant prairie dog flea vector of plague, seldom transmits Y. pestis by the classic blocked flea mechanism. More recently, an alternative early-phase mode of transmission has been proposed as the driving force behind prairie dog epizootics. In this study, using the same flea infection protocol used previously to evaluate early-phase transmission, we assessed the vector competence of O. hirsuta for both modes of transmission. Proventricular blockage was evident during the first two weeks after infection and transmission during this time was at least as efficient as early-phase transmission 2 d after infection. Thus, both modes of transmission likely contribute to plague epizootics in prairie dogs.

Oral Sylvatic Plague Vaccine Does Not Adequately Protect Prairie Dogs (Cynomys spp.) for Endangered Black-Footed Ferret (Mustela nigripes) Conservation.

The plague bacterium Yersinia pestis is lethal to endangered black-footed ferrets (Mustela nigripes, BFF) and the prairie dogs (Cynomys spp., PD) on which they depend for habitat and prey. We assessed the effectiveness of an oral sylvatic plague vaccine delivered in baits to black-tailed PD (Cynomys ludovicianus, BTPD) from 2013 to 2017 on the Charles M. Russell National Wildlife Refuge (CMR) in northcentral Montana. We permanently marked BTPD on four paired vaccine (N = 1,349 individuals) and placebo plots (N = 926; 7,027 total captures). We analyzed capture-recapture data under a Cormack-Jolly-Seber model to estimate annual apparent survival. Overall, survival averaged 0.05 lower on vaccine plots than on paired placebo plots. Immediately before noticeable die-offs and detecting plague on pairs CMR1 and CMR2, 89% of BTPD sampled on vaccine plots had consumed at least one bait and the immune systems (pleural) of 40% were likely boosted by consuming baits over multiple years. Survival to the following year was 0.16 and 0.05 on the vaccine plots and 0.19 and 0.06 on the placebo plots for pairs CMR1 and CMR2, respectively. These rates were markedly lower than 0.63, the overall average estimate on those same plots during the previous 3 years. PD populations subjected to such large die-offs would not be expected to sustain a BFF population. An overriding limitation to achieving sufficient protection rests with vaccine delivery constraints. Late summer/fall bait distribution results in the highest bait uptake rates. However, the PD birth pulse each spring can double the size of populations in most years, greatly reducing the proportion of vaccinates in populations and diminishing potential herd immunity benefits. In addition to nonvaccinated juveniles and PD that do not consume bait, incomplete vaccine protection and time required for immunity to develop leaves a large majority of PD populations vulnerable to plague for 6-7 months or more each year.

Comparison of Flea Sampling Methods and Yersinia pestis Detection on Prairie Dog Colonies.

Scientists collect fleas (Siphonaptera) to survey for Yersinia pestis, the bacterial agent of plague. When studying fleas parasitizing prairie dogs (Cynomys spp.), two primary methods are used: (1) combing fleas from live-trapped prairie dogs and (2) swabbing fleas from burrows with cloth swabs attached to metal cables. Ideally, burrow swabbing, the cheaper and easier method, would explain flea burdens on prairie dogs and provide reliable information on plague prevalence. In a linear regression analysis of data from 1-month intervals (June-August 2010-2011) on 13 colonies of black-tailed prairie dogs (Cynomys ludovicianus, BTPDs) in New Mexico, flea abundance on swabs explained 0-26% of variation in BTPD flea burdens. In an analysis of data (May-August 2016) from six colonies of BTPDs in Montana, flea abundance on swabs explained 2% of variation in BTPD flea burdens. In an analysis of data from a short-term interval (July 23-27, 2019) on four colonies of BTPDs in Montana, flea abundance on swabs explained 0.1% of variation in BTPD flea burdens. In an analysis of data from 1-week intervals (August-October 2000) on four colonies of white-tailed prairie dogs (Cynomys leucurus, WTPD) in Utah, swabbing data explained 0.1% of variation in WTPD flea burdens. Pools of fleas from two WTPD colonies were tested for Y. pestis by mouse inoculation and isolation; 65% from WTPDs tested positive, whereas 4% from burrows tested positive. Data herein also show that results from burrow swabbing can misrepresent flea species composition and phenology on prairie dogs. Burrow swabbing is useful for some purposes, but limitations should be acknowledged, and accumulated data should be interpreted with caution.

Plague transforms positive effects of precipitation on prairie dogs to negative effects.

Rodents characteristically benefit from increased precipitation, especially in typically dry habitats; "good years" of high precipitation improve their forage and water balance. However, Yersinia pestis (plague), a flea-borne pathogen of mammals that was introduced to western North America, has the greatest negative impact on at least some species of rodents during years of above-average precipitation. In the absence of plague mitigation, negative effects of plague in wet years might overwhelm the otherwise beneficial effects of increased moisture. In Montana and Utah, USA, where plague now occurs enzootically, we investigated the influence of precipitation on finite rates of annual population change (2000-2005) for 3 species of prairie dogs (Cynomys spp.) in replicated plots treated with deltamethrin dust and in non-treated plots for paired comparisons. There was a significant interaction between precipitation and treatment. When we reduced plague vector fleas, prairie dog visual counts tended to increase with increasing precipitation. Simultaneously, there was a negative relationship between counts and precipitation on paired plots where plague was not managed, suggesting that plague transformed and reversed the otherwise beneficial effect of increased precipitation. Are the good years gone for prairie dogs? Even if the good years are not gone, they are perhaps relatively scarce compared to historic times prior to the invasion of plague. This scenario might apply to other ecosystems and may pose broad conservation challenges in western North America.

Fipronil Pellets Reduce Flea Abundance on Black-Tailed Prairie Dogs: Potential Tool for Plague Management and Black-Footed Ferret Conservation.

In western North America, sylvatic plague (a flea-borne disease) poses a significant risk to endangered black-footed ferrets (Mustela nigripes) and their primary prey, prairie dogs (Cynomys spp.). Pulicides (flea-killing agents) can be used to suppress fleas and thereby manage plague. In South Dakota, US, we tested edible "FipBit" pellets, each containing 0.84 mg fipronil, on free-living black-tailed prairie dogs (Cynomys ludivicianus). FipBits were applied along transects at 125 per ha and nearly eliminated fleas for 2 mo. From 9-14 mo post-treatment, we found only 10 fleas on FipBit sites versus 1,266 fleas on nontreated sites. This degree and duration of flea control should suppress plague transmission. FipBits are effective, inexpensive, and easily distributed but require federal approval for operational use.

Epizootic Plague in Prairie Dogs: Correlates and Control with Deltamethrin.

The plague bacterium, Yersinia pestis, is a generalist pathogen of flea (Siphonaptera) vectors and mammalian hosts. In colonies of prairie dogs (PDs, Cynomys spp.), Y. pestis causes occasional epizootics, killing ≥90% of PDs within weeks to several months. We evaluated the effectiveness of deltamethrin, a pyrethroid insecticide, as a tool for preventing plague epizootics among three PD species. Specifically, we studied PD population growth on paired plots treated with deltamethrin for flea control or left untreated as baselines. We also evaluated PD population growth relative to flea abundance and PD density. All epizootics occurred on nontreated plots. Epizootics occurred on plots with very low PD densities as well as high densities. Mean population change, assessed by comparing visual counts of PDs in years before and during epizootics, was +88% for treated plots and -97% for nontreated plots. For comparison, an experimental oral vaccine against plague had an average change in population index or estimate during epizootics of -69% on vaccine plots compared with -83% for associated nontreated (placebo) plots. In our study and on plots not treated with deltamethrin, PD population growth was negatively correlated with flea abundance in the year before the epizootic, lending support to the hypothesis that flea abundance plays a critical role in plague transmission under natural conditions. Generally speaking, deltamethrin is a highly effective tool for plague management on PD colonies. That said, continued study is needed to refine deltamethrin treatments and to develop a more integrated strategy for plague management.

Ecology and Management of Plague in Diverse Communities of Rodents and Fleas.

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.

Managing plague on prairie dog colonies: insecticides as ectoparasiticides.

Human health practitioners and wildlife biologists use insecticides to manage plague by suppressing fleas (Siphonaptera), but insecticides can also kill other ectoparasites. We investigated effects of deltamethrin and fipronil on ectoparasites from black-tailed prairie dogs (Cynomys ludovicianus, BTPDs). In late July, 2018, we treated three sites with 0.05% deltamethrin dust and 5 sites with host-fed 0.005% fipronil grain. Three non-treated sites functioned as experimental baselines. We collected ectoparasites before treatments (June-July, 2018) and after treatments (August-October, 2018, June-July, 2019). Both deltamethrin and fipronil suppressed fleas for at least 12 months. Deltamethrin had no detectable effect on mites (Arachnida). Fipronil suppressed mites for at least 12 months. Lice (Phthiraptera) were scarce on non-treated sites throughout the study, complicating interpretation. Concentrating on eight sites where all three ectoparasites where found in June-July, 2018 (before treatments), flea intensity was greatest on BTPDs carrying many lice and mites. These three ectoparasites co-occurred at high numbers, which might facilitate plague transmission in some cases. Lethal effects of insecticides on ectoparasite communities are potentially advantageous in the context of plague management.

FLEA PARASITISM AND HOST SURVIVAL IN A PLAGUE-RELEVANT SYSTEM: THEORETICAL AND CONSERVATION IMPLICATIONS.

Plague is a bacterial zoonosis of mammalian hosts and flea vectors. The disease is capable of ravaging rodent populations and transforming ecosystems. Because plague mortality is likely to be predicted by flea parasitism, it is critical to understand vector dynamics. It has been hypothesized that paltry precipitation and reduced vegetative production predispose herbivorous rodents to malnourishment and flea parasitism, and flea parasitism varies directly with plague mortality. We evaluated these hypotheses on five colonies of Utah prairie dogs (UPDs; Cynomys parvidens), on the Awapa Plateau, Utah, US, in 2013-16. Ten flea species were identified among 3,257 fleas from UPDs. These 10 flea species parasitize prairie dogs, mice, rats, voles, ground squirrels, chipmunks, and marmots, all known hosts of plague. The abundance of fleas on individual UPDs (1,198 observations) varied inversely with UPD body condition; fleas were most abundant on lightweight, malnourished UPDs. Flea abundance on UPDs was highest in dry years that were preceded by wet years. Increased precipitation and soil moisture in the prior year might generate humid microclimates in UPD burrows (that could facilitate flea survival and reproduction) and paltry precipitation in the current year could predispose UPDs to malnourishment and flea parasitism. Annual re-encounter rates for UPDs (1,072 observations) were reduced in wetter years preceded by drier years; reduced precipitation and vegetative production might kill UPDs, and increased flea densities in drier years could provide conditions for plague transmission (and UPD mortality) when moisture returns. Re-encounter rates were reduced for UPDs carrying at least one flea compared to UPDs with no detected fleas. These results support the hypothesis that reduced precipitation in the current year predisposes UPDs to flea parasitism. Our results also suggest a link between flea parasitism and UPD mortality. Given documented connections between flea parasitism and plague transmission, our results point toward an effect of flea parasitism on plague-related deaths for individual UPDs, a phenomenon rarely investigated in nature.

Plague management of prairie dog colonies: degree and duration of deltamethrin flea control.

Plague is a flea-borne disease of mammalian hosts. On the grasslands of western North America, plague stifles populations of Cynomys spp. prairie dogs (PDs). To manage plague, PD burrows are treated with 0.05% deltamethrin dust that can suppress flea numbers and plague transmission. Here, we evaluate the degree and duration of deltamethrin flea control with three PD species at six sites across four U.S. states. Data were simultaneously collected at paired plots. Burrows from one randomly assigned member of each pair were treated with deltamethrin; non-treated plots served as experimental baselines. Flea control was strong ≤two months after treatment, remained moderate one year later, and was statistically detectable for up to two years at some sites. Flea abundance was lower in plots with higher rates of deltamethrin application. After burrow treatments, flea abundance increased over time, reaching >one per PD within 255 to 352 days. Nevertheless, annual treatments of burrows with deltamethrin provided PDs with substantial protection against plague. Even so, deltamethrin should be further evaluated and combined with other tools under an integrated approach to plague management. Integrated plague management should help to conserve PDs and species that associate with them, including the endangered black-footed ferret (Mustela nigripes).

Prairie Dogs, Persistent Plague, Flocking Fleas, and Pernicious Positive Feedback.

Plague (caused by the bacterium Yersinia pestis) is a deadly flea-borne disease that remains a threat to public health nearly worldwide and is particularly disruptive ecologically where it has been introduced. We review hypotheses regarding maintenance and transmission of Y. pestis, emphasizing recent data from North America supporting maintenance by persistent transmission that results in sustained non-epizootic (but variable) rates of mortality in hosts. This maintenance mechanism may facilitate periodic epizootic eruptions "in place" because the need for repeated reinvasion from disjunct sources is eliminated. Resulting explosive outbreaks that spread rapidly in time and space are likely enhanced by synergistic positive feedback (PFB) cycles involving flea vectors, hosts, and the plague bacterium itself. Although PFB has been implied in plague literature for at least 50 years, we propose this mechanism, particularly with regard to flea responses, as central to epizootic plague rather than a phenomenon worthy of just peripheral mention. We also present new data on increases in flea:host ratios resulting from recreational shooting and poisoning as possible triggers for the transition from enzootic maintenance to PFB cycles and epizootic explosions. Although plague outbreaks have received much historic attention, PFB cycles that result in decimation of host populations lead to speculation that epizootic eruptions might not be part of the adaptive evolutionary strategy of Y. pestis but might instead be a tolerated intermittent cost of its modus operandi. We also speculate that there may be mammal communities where epizootics, as we define them, are rare or absent. Absence of plague epizootics might translate into reduced public health risk but does not necessarily equate to inconsequential ecologic impact.

Evaluation of Five Pulicides to Suppress Fleas on Black-Tailed Prairie Dogs: Encouraging Long-Term Results with Systemic 0.005% Fipronil.

Plague, a flea-borne disease, hampers efforts to restore populations of black-footed ferrets (Mustela nigripes), which occupy colonies of prairie dogs (Cynomys spp.) in North America. Plague is managed by infusing prairie dog burrows with DeltaDust® 0.05% deltamethrin, a pulicide that kills fleas. Experiments are needed to identify pulicides that can be used in rotation with DeltaDust for integrated plague management. In South Dakota, USA, we tested the efficacy of four pulicide dusts when applied at a rate of 8 g per burrow on colonies of black-tailed prairie dogs (Cynomys ludovicianus): Sevin® 5% carbaryl; Dusta-cide® 6% malathion; Alpine® 0.25% dinotefuran with 95% diatomaceous earth; and Tri-Die® 1% pyrethrum with 40% amorphous silica and 10% piperonyl butoxide. We also tested systemic 0.005% fipronil, which was distributed as ½ cup of laced grain per burrow. We sampled prairie dogs on 3294 occasions and detected 10,041 fleas. Sevin and Dusta-cide suppressed fleas but only for 1 month. Neither Alpine nor Tri-Die had any noticeable, consistent effect on fleas. Fipronil suppressed fleas by 97-100% for 3 months. The residual effect of fipronil persisted for ∼12 months. Efficacy of fipronil seems comparable with DeltaDust, which exhibited a residual effect for ∼10 months in prior studies. Continued research is needed to optimize fipronil treatments for plague management on prairie dog colonies.

RESISTANCE TO DELTAMETHRIN IN PRAIRIE DOG ( CYNOMYS LUDOVICIANUS) FLEAS IN THE FIELD AND IN THE LABORATORY.

Sylvatic plague poses a substantial risk to black-tailed prairie dogs ( Cynomys ludovicianus) and their obligate predator, the black-footed ferret ( Mustela nigripes). The effects of plague on prairie dogs and ferrets are mitigated using a deltamethrin pulicide dust that reduces the spread of plague by killing fleas, the vector for the plague bacterium. In portions of Conata Basin, Buffalo Gap National Grassland, and Badlands National Park, South Dakota, US, 0.05% deltamethrin has been infused into prairie dog burrows on an annual basis since 2005. We aimed to determine if fleas ( Oropsylla hirsuta) in portions of the Conata Basin and Badlands National Park have evolved resistance to deltamethrin. We assessed flea prevalence, obtained by combing prairie dogs for fleas, as an indirect measure of resistance. Dusting was ineffective in two colonies treated with deltamethrin for >8 yr; flea prevalence rebounded within 1 mo of dusting. We used a bioassay that exposed fleas to deltamethrin to directly evaluate resistance. Fleas from colonies with >8 yr of exposure to deltamethrin exhibited survival rates that were 15% to 83% higher than fleas from sites that had never been dusted. All fleas were paralyzed or dead after 55 min. After removal from deltamethrin, 30% of fleas from the dusted colonies recovered, compared with 1% of fleas from the not-dusted sites. Thus, deltamethrin paralyzed fleas from colonies with long-term exposure to deltamethrin, but a substantial number of those fleas was resistant and recovered. Flea collections from live-trapped prairie dogs in Thunder Basin National Grassland, Wyoming, US, suggest that, in some cases, fleas might begin to develop a moderate level of resistance to deltamethrin after 5-6 yr of annual treatments. Restoration of black-footed ferrets and prairie dogs will rely on an adaptive, integrative approach to plague management, for instance involving the use of vaccines and rotating applications of insecticidal products with different active ingredients.