Alternative lifestyles: A plague persistence hypothesis Wimsatt, Jeffrey; Eads, David A.; Matchett, Marc R. ...
Ecosphere (Washington, D.C),
November 2023, 2023-11-00, 20231101, 2023-11-01, Letnik:
14, Številka:
11
Journal Article
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Several explanations have been posited for how the plague bacterium (Yersinia pestis) reemerges during sylvatic cycles within the same foci over many years, and often without direct evidence of host ...die‐offs. One prevalent view is that transmission‐optimized Y. pestis bacteria, exhibiting epizootic/enzootic behavior, almost continually replicate and survive through repeated, linked, host‐centered propagation events. These bacteria, we will refer to as “r‐pestis” type ecotype(s), represent a limited number of phenotypic lineages exhibiting optimal transmissibility and high rates of reproduction. These attributes, it is thought, assure their durability through time. For continuous r‐pestis type expansions to be successful, adequate numbers of fleas and hosts must become infected to produce massive numbers of bacteria. In the process, host and flea numbers decline as they succumb to plague. Here we hypothesize that r‐pestis population expansions seed the environment and confront a unique, highly competitive local milieu, where natural selection favors new ecotypes that incorporate a range of emergent adaptive survival strategies. These newly adapted survivors we recognize as a range of “K‐pestis” ecotypes with greater durability and lower reproduction rates. These emergent K‐pestis forms may arise in succession or coexist for varying periods of time with r‐pestis ecotypes, and with other K‐pestis ecotypes. Among K‐pestis ecotypes, we hypothesize that through adaptive radiations, some persist within flea life stages, soil, organic waste, amoebae, plants, carcasses, hosts, or within niches yet to be characterized. In some settings, after a long quiet period, when favorable, K‐pestis bacteria may trigger a singular event where an r‐pestis transmission stream emerges precipitating another enzootic/epizootic progression. If this hypothesis withstands rigorous testing, then Y. pestis might represent an even more formidable, enduring, and adaptable foe, where unforeseen local events could trigger new epidemic and epizootic/enzootic events threatening humans and populations of other mammals, including those of conservation concern.
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.
Mountain lions (Puma concolor) have historically experienced large‐scale range contractions, but are beginning to recolonize portions of their former range. To reach potential suitable habitats in ...eastern North America, mountain lions need to move across the grassland and agriculture‐dominated habitats of the Great Plains, which are different from the forested areas associated with mountain lions in western North America. To inform restoration planning in this area, it is important to understand differences in mountain lion habitat selection in this “nontraditional” grassland habitat. We tracked GPS‐collared mountain lions in the Northern Great Plains of Montana and identified movement states (localized or exploratory) using behavioral change point analysis and net‐squared displacement. We compared habitat selection between the different states using step‐selection functions that included several environmental covariates. Similar to elsewhere throughout their range, across both movement states, mountain lions tended to select forested environments that were farther from human development. In contrast to more traditionally occupied mountainous regions, mountain lions in the Great Plains selected areas of lower elevations. They selected areas both near and far from water, but avoided riparian areas and selected more rugged environments when in exploratory movement states. This suggests that mountain lions in the Northern Great Plains are utilizing river corridors, particularly those with rough or broken topography during exploratory phases. To enhance future recolonization and connectivity of mountain lions to the east of our study area, we encourage managers to maintain and restore forest fragments along river corridors in the Great Plains.
Scientists collect fleas (Siphonaptera) to survey for
, the bacterial agent of plague. When studying fleas parasitizing prairie dogs (
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 (
, 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 (
, WTPD) in Utah, swabbing data explained 0.1% of variation in WTPD flea burdens. Pools of fleas from two WTPD colonies were tested for
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.
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.
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.
Context
Resource selection functions are powerful tools for predicting habitat selection of animals. Recently, machine-learning methods such as random forest have gained popularity for predicting ...habitat selection due to their flexibility and strong predictive performance.
Objectives
We tested two methods for predicting continental-scale, second-order habitat selection of a wide-ranging large carnivore, the mountain lion (
Puma concolor
), to support continent-wide conservation management, including estimating abundance, and to predict habitat suitability for recolonizing or reintroduced animals.
Methods
We compared a generalized linear model (GLM) and a random forest model using GPS location data from 476 individuals across 20 study sites in the western USA and Canada and remotely-sensed landscape data. We internally validated models and examined their ability to correctly classify used and available points by calculating area under the receiver operating characteristics (AUC). We performed leave-one-out (LOO) out-of-sample tests of predictive strength on both models.
Results
Both models suggested that mountain lions select for steeper slopes, areas closer to water, and with higher normalized difference vegetation index (NDVI), and against variables associated with human impact. The random forest model (AUC = 0.94) demonstrated that mountain lion habitat can be accurately predicted at continental scales, outperforming the traditional GLM model (AUC = 0.68). Our LOO validation provided similar results (x̄ = 0.93 for the random forest and x̄ = 0.65 for the GLM).
Conclusions
We found that the added flexibility of the random forest model provided deeper insights into how individual covariates impacted habitat selection across diverse ecosystems. Our LOO analyses suggested that our model can predict mountain lion habitat selection in unoccupied areas or where local data are unavailable. Our model thus provides a tool to support discussions and analyses relevant to continent-wide mountain lion conservation and management including estimating metapopulation abundance.
Black-footed ferrets (Mustela nigripes) require extensive prairie dog colonies (Cynomys spp.) to provide habitat and prey. Epizootic plague kills both prairie dogs and ferrets and is a major factor ...limiting recovery of the highly endangered ferret. In addition to epizootics, we hypothesized that enzootic plague, that is, presence of disease-causing Yersinia pestis without any noticeable prairie dog die off, may also affect ferret survival. We reduced risk of plague on portions of two ferret reintroduction areas by conducting flea control for 3 years. Beginning in 2004, about half of the ferrets residing on dusted and nondusted colonies were vaccinated against plague with an experimental vaccine (F1-V fusion protein). We evaluated 6-month reencounter rates (percentage of animals observed at the end of an interval that were known alive at the beginning of the interval), an index to survival, for ferrets in four treatment groups involving all combinations of vaccination and flea control. For captive-reared ferrets (115 individuals observed across 156 time intervals), reencounter rates were higher for vaccinates (0.44) than for nonvaccinates (0.23, p = 0.044) on colonies without flea control, but vaccination had no detectable effect on colonies with flea control (vaccinates = 0.41, nonvaccinates = 0.42, p = 0.754). Flea control resulted in higher reencounter rates for nonvaccinates (p = 0.026), but not for vaccinates (p = 0.508). The enhancement of survival due to vaccination or flea control supports the hypothesis that enzootic plague reduces ferret survival, even when there was no noticeable decline in prairie dog abundance. The collective effects of vaccination and flea control compel a conclusion that fleas are required for maintenance, and probably transmission, of plague at enzootic levels. Other studies have demonstrated similar effects of flea control on several species of prairie dogs and, when combined with this study, suggest that the effects of enzootic plague are widespread. Finally, we demonstrated that the experimental F1-V fusion protein vaccine provides protection to ferrets in the wild.
Plague, caused by Yersinia pestis, is a widespread threat to endangered black-footed ferrets (Mustela nigripes) and their primary prey, prairie dogs (Cynomys spp.). Wildlife biologists most commonly ...manage plague using insecticides to control fleas, the primary vectors of Y. pestis. We tested edible baits containing the insecticides lufenuron and/or nitenpyram in prairie dogs. During a laboratory study, we treated 26 white-tailed prairie dogs (Cynomys leucurus) with lufenuron at 300 mg/kg body mass. All animals remained clinically healthy over the 9 wk monitoring period. Although serum lufenuron concentrations were >130 ppb in two treatment groups at week 1, concentrations declined to ≤60 ppb after 3 wk in non-torpid prairie dogs and after 7 wk in torpid prairie dogs. In a field experiment, we tested baits containing a combination of 75 mg lufenuron and 6 mg nitenpyram, respectively, in black-tailed prairie dogs (Cynomys ludovicianus). We uniformly distributed baits at 125 baits/ha on two plots (treated once) and 250 baits/ha on two plots (each treated twice 4.4 wk apart). Following treatments, flea abundance increased on prairie dogs and remained stable in burrows. Our findings indicate that baits containing lufenuron and nitenpyram, at the reported treatment rates, are ineffective tools for flea control on prairie dogs. Future experiments might evaluate efficacy of higher doses of lufenuron and nitenpyram, and repetitive treatments at differing intervals over time to evaluate potentially therapeutic treatments.
Sylvatic plague, caused by
Yersinia pestis
, frequently afflicts prairie dogs (
Cynomys
spp.), causing population declines and local extirpations. We tested the effectiveness of bait-delivered ...sylvatic plague vaccine (SPV) in prairie dog colonies on 29 paired placebo and treatment plots (1–59 ha in size; average 16.9 ha) in 7 western states from 2013 to 2015. We compared relative abundance (using catch per unit effort (CPUE) as an index) and apparent survival of prairie dogs on 26 of the 29 paired plots, 12 with confirmed or suspected plague (
Y. pestis
positive carcasses or fleas). Even though plague mortality occurred in prairie dogs on vaccine plots, SPV treatment had an overall positive effect on CPUE in all three years, regardless of plague status. Odds of capturing a unique animal were 1.10 (95% confidence interval C.I. 1.02–1.19) times higher per trap day on vaccine-treated plots than placebo plots in 2013, 1.47 (95% C.I. 1.41–1.52) times higher in 2014 and 1.19 (95% C.I. 1.13–1.25) times higher in 2015. On pairs where plague occurred, odds of apparent survival were 1.76 (95% Bayesian credible interval B.C.I. 1.28–2.43) times higher on vaccine plots than placebo plots for adults and 2.41 (95% B.C.I. 1.72–3.38) times higher for juveniles. Our results provide evidence that consumption of vaccine-laden baits can protect prairie dogs against plague; however, further evaluation and refinement are needed to optimize SPV use as a management tool.
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