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A review of plague persistence with special emphasis on fleas

Sylvatic plague is highly prevalent during infrequent epizootics that ravage the landscape of western North America. During these periods, plague dissemination is very efficient. Epizootics end when rodent and flea populations are decimated and vectored transmission declines. A second phase (enzootic plague) ensues when plague is difficult to detect from fleas, hosts or the environment, and presents less of a threat to public health. Recently, researchers have hypothesized that the bacterium (Yersinia pestis) responsible for plague maintains a continuous state of high virulence and thus only changes in transmission efficiency explain the shift between alternating enzootic and epizootic phases. However, if virulent transmission becomes too inefficient, strong selection might favor an alternate survival strategy. Another plausible non-exclusive hypothesis, best supported from Asian field studies, is that Y. pestis persists (locally) at foci by maintaining a more benign relationship within adapted rodents during the long expanses of time between outbreaks. From this vantage, it can revert to the epizootic (transmission efficient) form. Similarly, in the United States (US), enzootic plague persistence has been proposed to develop sequestered within New World rodent carriers. However, the absence of clear support for rodent carriers in North America has encouraged a broader search for alternative explanations. A telluric plague existence has been proposed. However, the availability of flea life stages and their hosts could critically supplement environmental plague sources, or fleas might directly represent a lowlevel plague reservoir. Here, we note a potentially pivotal role for fleas. These epizootic plague vectors should be closely studied with newer more exacting methods to determine their potential to serve as participants in or accomplices to a plague persistence reservoir.

Journal of Vector Borne Diseases

Serologic survey of selected arthropod-borne pathogens in free-ranging snowshoe hares (Lepus americanus) captured in Northern Michigan, USA

Snowshoe hares ( Lepus americanus ) in the Upper Peninsula (UP) of Michigan, USA, occupy the southern periphery of the species' range and are vulnerable to climate change. In the eastern UP, hares are isolated by the Great Lakes, potentially exacerbating exposure to climate-change-induced habitat alterations. Climate change is also measurably affecting distribution and prevalence of vector-borne pathogens in North America, and increases in disease occurrence and prevalence can be one signal of climate-stressed wildlife populations. We conducted a serosurvey for vector-borne pathogens in snowshoe hares that were captured in the Hiawatha National Forest in the eastern UP of Michigan, USA, 2016-2017. The most commonly detected antibody response was to the mosquito-borne California serogroup snowshoe hare virus (SSHV). Overall, 24 (51%) hares screened positive for SSHV antibodies and of these, 23 (96%) were confirmed positive by plaque reduction neutralization test. We found a positive association between seroprevalence of SSHV and live weight of snowshoe hares. Additionally, we detected a significant effect of ecological land type group on seroprevalence of SSHV, with strong positive support for a group representing areas that tend to support high numbers of hares (i.e., acidic mineral containing soils with cedar, mixed swamp conifers, tamarack and balsam fir as common overstory vegetation). We also detected and confirmed antibodies for Jamestown Canyon virus and Silverwater virus in a single hare each. We did not detect antibodies to other zoonotic vector-borne pathogens, including Lacrosse encephalitis virus, West Nile virus, Borrelia burgdorferi, Powassan virus, and Francisella tularensis. These results provide a baseline for future serological studies of vector-transmitted diseases that may increase climate vulnerability of snowshoe hares in the UP of Michigan, as well as pose a climate-related zoonotic risk.

Michigan

Environmental management of mosquito-borne viruses in Rhode Island

West Nile Virus (WNV) and Eastern Equine Encephalitis Virus (EEEV) are both primarily bird viruses, which can be transmitted by several mosquito species. Differences in larval habitats, flight, and biting patterns of the primary vector species result in substantial differences in epidemiology, with WNV more common, primarily occurring in urban areas, and EEEV relatively rare, typically occurring near swamp habitats. The complex transmission ecology of these viruses complicates prediction of disease outbreaks. The Rhode Island Department of Environmental Management (DEM) and Department of Health (DoH) provide prevention assistance to towns and maintain a mosquito surveillance program to identify potential disease risk. Responses to potential outbreaks follow a protocol based on surveillance results, assessment of human risk, and technical consultation.

Rhode Island

Potential effects of climate change on tick-borne diseases in Rhode Island

Human cases of tick-borne diseases have been increasing in the United States. In particular, the incidence of Lyme disease, the major vector-borne disease in Rhode Island, has risen, along with cases of babesiosis and anaplasmosis, all vectored by the blacklegged tick. These increases might relate, in part, to climate change, although other environmental changes in the northeast (land use as it relates to habitat; vertebrate host populations for tick reproduction and enzootic cycling) also contribute. Lone star ticks, formerly southern in distribution, have been spreading northward, including expanded distributions in Rhode Island. Illnesses associated with this species include ehrlichiosis and alpha-gal syndrome, which are expected to increase. Ranges of other tick species have also been expanding in southern New England, including the Gulf Coast tick and the introduced Asian longhorned tick. These ticks can carry human pathogens, but the implications for human disease in Rhode Island are unclear.

Rhode Island

Integrated pest management and allocation of control efforts for vector-borne diseases

Applications of various control methods were evaluated to determine how to integrate methods so as to minimize the number of human cases of vector-borne diseases. These diseases can be controlled by lowering the number of vector-human contacts (e.g., by pesticide applications or use of repellents), or by lowering the proportion of vectors infected with pathogens (e.g., by lowering or vaccinating reservoir host populations). Control methods should be combined in such a way as to most efficiently lower the probability of human encounter with an infected vector. Simulations using a simple probabilistic model of pathogen transmission suggest that the most efficient way to integrate different control methods is to combine methods that have the same effect (e.g., combine treatments that lower the vector population; or combine treatments that lower pathogen prevalence in vectors). Combining techniques that have different effects (e.g., a technique that lowers vector populations with a technique that lowers pathogen prevalence in vectors) will be less efficient than combining two techniques that both lower vector populations or combining two techniques that both lower pathogen prevalence, costs being the same. Costs of alternative control methods generally differ, so the efficiency of various combinations at lowering human contact with infected vectors should be estimated at available funding levels. Data should be collected from initial trials to improve the effects of subsequent interventions on the number of human cases.

Journal of Vector Ecology

Differences in mosquito communities in six cities in Oklahoma

Vector-borne diseases in the United States have recently increased as a result of the changing nature of vectors, hosts, reservoirs, pathogens, and the ecological and environmental conditions. Current information on vector habitats and how mosquito community composition varies across space and time is vital to successful vector-borne disease management. This study characterizes mosquito communities in urban areas of Oklahoma, United States, an ecologically diverse region in the southern Great Plains. Between May and September 2016, 11,996 female mosquitoes of 34 species were collected over 798 trap nights using three different trap types in six Oklahoma cities. The most abundant species trapped were Culex pipiens L. complex (32.4%) and Aedes albopictus (Skuse) (Diptera: Culicidae) (12.0%). Significant differences among mosquito communities were detected using analysis of similarities (ANOSIM) between the early (May–July) and late (August–September) season. Canonical correlation analysis (CCA) further highlighted the cities of Altus and Idabel as relatively unique mosquito communities, mostly due to the presence of Aedes aegypti (L.) and salt-marsh species and absence of Aedes triseriatus (Say) in Altus and an abundance of Ae. albopictus in Idabel. These data underscore the importance of assessing mosquito communities in urban environments found in multiple ecoregions of Oklahoma to allow customized vector management targeting the unique assemblage of species found in each city.

Oklahoma

Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawai'i

More than half of the Hawaiian honeycreepers (Drepanidinae) known from historical records are now extinct. Introduced mosquito-borne disease, in particular the avian malaria Plasmodium relictum , has been incriminated as a leading cause of extinction during the 20th century and a major limiting factor in the recovery of remaining species populations. Today, most native Hawaiian bird species reach their highest densities and diversity in high elevation (>1,800 m above sea level) forests. We determined the thermal requirements for sporogonic development of P. relictum in the natural vector, Culex quinquefasciatus , and assessed the current distribution of native bird species in light of this information. Sporogonic development was completed at constant laboratory and mean field temperatures between 30 and 17 C, but development, prevalence, and intensity decreased significantly below 21 C. Using a degree-day (DD) model, we estimated a minimum threshold temperature of 12.97 C and a thermal requirement of 86.2 DD as necessary to complete development. Predicted (adiabatic lapse-rate) and observed summer threshold isotherm (13 C) correspond to the elevation of high forest refuges on the islands of Maui and Hawai'i. Our data support the hypothesis that avian malaria currently restricts the altitudinal distribution of Hawaiian honeycreeper populations and provide an ecological explanation for the absence of disease at high elevation.

Hawaii

Dispersal of Culex quinquefasciatus (Diptera: Culicidae) in a Hawaiian rain forest

Introduced mosquito-borne pathogens avian malaria (Plasmodium relictum Grassi and Feletti) and avian pox virus (Avipoxvirus) have been implicated in the past extinctions and declines of Hawaiian avifauna and remain significant obstacles to the recovery and restoration of endemic Hawaiian birds. Effective management of avian disease will require extensive mosquito control efforts that are guided by the local ecology of the vector Culex quinquefasciatus Say (Diptera: Culicidae). During October and November 1997 and September through November 1998 five mark-release-recapture experiments with laboratory-reared Cx. quinquefasciatus were conducted in a native rain forest on Hawaii Island. Of the overall 66,047 fluorescent dye-marked and released females, 1,192 (1.8%) were recaptured in 43-52 CO2-baited traps operated for 10-12-d trapping periods. Recaptured mosquitoes were trapped in all directions and at distances up to 3 km from the release site. The cumulative mean distance traveled (MDTs) over the trapping period ranged from a high of 1.89 km after 11 d (September 1998) to a low of 0.81 km after 11 d (November 1998). Released mosquitoes moved predominately in a downwind direction and they seemed to use forestry roads as dispersal corridors. Applying an estimated MDT of 1.6 km to a geographical information system-generated map of the Hakalau Forest National Wildlife Refuge clearly demonstrated that the effective refuge area could be reduced 60% by mosquitoes infiltrating into managed refuge lands. These findings should have significant implications for the design of future refuges and development of effective mosquito-borne avian disease control strategies.

Journal of Medical Entomology

Droughts may increase susceptibility of prairie dogs to fleas: Incongruity with hypothesized mechanisms of plague cycles in rodents

Plague is a reemerging, rodent-associated zoonosis caused by the flea-borne bacterium Yersinia pestis . As a vector-borne disease, rates of plague transmission may increase when fleas are abundant. Fleas are highly susceptible to desiccation under hot-dry conditions; we posited that their densities decline during droughts. We evaluated this hypothesis with black-tailed prairie dogs ( Cynomys ludovicianus ) in New Mexico, June–August 2010–2012. Precipitation was relatively plentiful during 2010 and 2012 but scarce during 2011, the driest spring–summer on record for the northeastern grasslands of New Mexico. Unexpectedly, fleas were 200% more abundant in 2011 than in 2010 and 2012. Prairie dogs were in 27% better condition during 2010 and 2012, and they devoted 287% more time to grooming in 2012 than in 2011. During 2012, prairie dogs provided with supplemental food and water were in 23% better condition and carried 40% fewer fleas. Collectively, these results suggest that during dry years, prairie dogs are limited by food and water, and they exhibit weakened defenses against fleas. Long-term data are needed to evaluate the generality of whether droughts increase flea densities and how changes in flea abundance during sequences of dry and wet years might affect plague cycles in mammalian hosts.

Journal of Mammalogy

Modeling the geographic distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the contiguous United States

In addition to serving as vectors of several other human pathogens, the black-legged tick, Ixodes scapularis Say, and western black-legged tick, Ixodes pacificus Cooley and Kohls, are the primary vectors of the spirochete ( Borrelia burgdorferi ) that causes Lyme disease, the most common vector-borne disease in the United States. Over the past two decades, the geographic range of I. pacificus has changed modestly while, in contrast, the I. scapularis range has expanded substantially, which likely contributes to the concurrent expansion in the distribution of human Lyme disease cases in the Northeastern, North-Central and Mid-Atlantic states. Identifying counties that contain suitable habitat for these ticks that have not yet reported established vector populations can aid in targeting limited vector surveillance resources to areas where tick invasion and potential human risk are likely to occur. We used county-level vector distribution information and ensemble modeling to map the potential distribution of I. scapularis and I. pacificus in the contiguous United States as a function of climate, elevation, and forest cover. Results show that I. pacificus is currently present within much of the range classified by our model as suitable for establishment. In contrast, environmental conditions are suitable for I. scapularis to continue expanding its range into northwestern Minnesota, central and northern Michigan, within the Ohio River Valley, and inland from the southeastern and Gulf coasts. Overall, our ensemble models show suitable habitat for I. scapularis in 441 eastern counties and for I. pacificus in 11 western counties where surveillance records have not yet supported classification of the counties as established.

Journal of Medical Entomology

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 ).

Montana, South Dakota, Utah

Experimental infection of Hawai'i 'Amakihi (hemignathus virens) with West Nile virus and competence of a co-occurring vector, culex quinquefasciatus: potential impacts on endemic Hawaiian avifauna.

Introduced mosquito-borne avian disease is a major limiting factor in the recovery and restoration of native Hawaiian forest birds. Annual epizootics of avian pox (Avipoxvirus) and avian malaria (Plasmodium relictum) likely led to the extinction of some species and continue to impact populations of susceptible Hawaiian honeycreepers (Drepanidinae). The introduction of a novel pathogen, such as West Nile virus (WNV), could result in further population declines and extinctions. During September and October 2004, we infected Hawai'i' Amakihi (Hemignathus virens) with a North American isolate of WNV by needle inoculation and mosquito bite to observe susceptibility, mortality, and illness in this endemic passerine, and to determine the vector competence of the co-occurring, introduced mosquito Culex quinquefasciatus. All experimentally infected Hawai'i ;Amakihi became viremic, with a mean titer >10(5) plaque-forming units (PFU)/ml, and they experienced clinical signs ranging from anorexia and lethargy to ataxia. The fatality rate among needle-inoculated Hawai'i' Amakihi (n=16) was 31.3%, but mortality in free-ranging birds is likely to increase due to predation, starvation, thermal stress, and concomitant infections of avian malaria and pox. Surviving Hawai'i' Amakihi seem to clear WNV from the peripheral blood by 7-10 days postinfection (DPI), and neutralizing antibodies were detected from 9 to 46 DPI. In transmission trials, Hawaiian Cx. quinquefasciatus proved to be a competent vector and Hawai'i Amakihi an adequate amplification host of WNV, suggesting that epizootic WNV could readily become an additional limiting factor of some native Hawaiian bird populations.

Hawai'i

Landscape factors influencing the spatial distribution and abundance of mosquito vector Culex quinquefasciatus (Diptera: Culicidae) in a mixed residential-agricultural community in Hawai'i

Mosquito-borne avian diseases, principally avian malaria (Plasmodium relictum Grassi and Feletti) and avian pox (Avipoxvirus sp.) have been implicated as the key limiting factor associated with recent declines of endemic avifauna in the Hawaiian Island archipelago. We present data on the relative abundance, infection status, and spatial distribution of the primary mosquito vector Culex quinquefasciatus Say (Diptera: Culicidae) across a mixed, residential-agricultural community adjacent to Hawai'i Volcanoes National Park on Hawai'i Island. We modeled the effect of agriculture and forest fragmentation in determining relative abundance of adult Cx. quinquefasciatus in Volcano Village, and we implement our statistical model in a geographic information system to generate a probability of mosquito capture prediction surface for the study area. Our model was based on biweekly captures of adult mosquitoes from 20 locations within Volcano Village from October 2001 to April 2003. We used mixed effects logistic regression to model the probability of capturing a mosquito, and we developed a set of 17 competing models a priori to specifically evaluate the effect of agriculture and fragmentation (i.e., residential landscapes) at two spatial scales. In total, 2,126 mosquitoes were captured in CO 2-baited traps with an average probability of 0.27 (SE = 0.10) of capturing one or more mosquitoes per trap night. Twelve percent of mosquitoes captured were infected with P. relictum. Our data indicate that agricultural lands and forest fragmentation significantly increase the probability of mosquito capture. The prediction surface identified areas along the Hawai'i Volcanoes National Park boundary that may have high relative abundance of the vector. Our data document the potential of avian malaria transmission in residential-agricultural landscapes and support the need for vector management that extends beyond reserve boundaries and considers a reserve's spatial position in a highly heterogeneous landscape.

Journal of Medical Entomology

Avian malaria in a boreal resident species: long-term temporal variability, and increased prevalence in birds with avian keratin disorder

The prevalence of vector-borne parasitic diseases is widely influenced by biological and ecological factors. Environmental conditions such as temperature and precipitation can have a marked effect on haemosporidian parasites ( Plasmodium spp.) that cause malaria and those that cause other malaria-like diseases in birds. However, there have been few long-term studies monitoring haemosporidian infections in birds in northern latitudes, where weather conditions can be highly variable and the effects of climate change are becoming more pronounced. We used molecular methods to screen more than 2,000 blood samples collected from black-capped chickadees ( Poecile atricapillus ), a resident passerine bird. Samples were collected over a 10 year period, mostly during the non-breeding season, at seven sites in Alaska, USA. We tested for associations between Plasmodium prevalence and local environmental conditions including temperature, precipitation, site, year and season. We also evaluated the relationship between parasite prevalence and individual host factors of age, sex and presence or absence of avian keratin disorder. This disease, which causes accelerated keratin growth in the beak, provided a natural study system in which to test the interaction between disease state and malaria prevalence. Prevalence of Plasmodium infection varied by year, site, age and individual disease status but there was no support for an effect of sex or seasonal period. Significantly, birds with avian keratin disorder were 2.6 times more likely to be infected by Plasmodium than birds without the disorder. Interannual variation in the prevalence of Plasmodium infection at different sites was positively correlated with summer temperatures at the local but not statewide scale. Sequence analysis of the parasite cytochrome b gene revealed a single Plasmodium spp. lineage, P43. Our results demonstrate associations between prevalence of avian malaria and a variety of biological and ecological factors. These results also provide important baseline data that will be informative for predicting future changes in Plasmodium prevalence in the subarctic.

Alaska

Studies on avian malaria in vectors and hosts of encephalitis in Kern County, California. I. Infections in avian hosts

An epizoological study of Plasmodium infections in wild birds of Kern County, California, in the years 1946 through 1951 greatly extended knowledge of the occurrence of these parasites and their behavior in nature. Examination of 10,459 blood smears from 8,674 birds representing 73 species resulted in the observation of Plasmodium spp. in 1,094 smears representing 888 individual birds of 27 species. Seven species of Plasmodium were found: relictum, elongatum, hexamerium, nucleophilum, polare, rouxi and vaughani. Plasmodium relictum was by far the most frequently observed species, occurring in at least 79 per cent of the infected birds. Twelve new host species are recorded for this parasite. Sufficient morphological variation was observed to indicate that two strains of this species probably exist in nature. Numerous new host records were made of plasmodia with elongate gametocytes. The finding of parasites believed to be P. rouxi in two new host species represents the first record of the occurrence of this Plasmodium outside of Algeria. Multiple smears were obtained from a number of individual birds over varying time periods. Evidence of prolonged parasitemia was unusual, but some individuals had parasitemia on consecutive months and even for three successive years. In most individuals, parasitemias were of short duration. The inoculation of blood from wild birds into canaries led to the demonstration of many infections not observed on blood smear examination of donors. Use of these two complementary techniques led to more complete host records and a truer picture of the prevalence of infection. Three age classes of birds were studied--nestling, immature (less than 1 year of age) and adult. Parasites were observed in all three groups but infections in the younger individuals were most susceptible to interpretation. As to time of onset, numerous records were obtained of infection in nestling birds. Prevalence rates in immature birds after a single season's exposure ranged from 64 to 100 per cent in the house finch and 17 to 68 per cent in the English sparrow in different areas and years. Marked differences were found in the prevalence rates in different summer months, years and areas. It is believed these differences reflect variation in a number of environmental factors. This study indicates the extensive distribution of Plasmodium infection in a wide range of wild avian hosts. The observations are of possible importance in epidemiological studies of other arthropod-borne diseases such as the viral encephalitides for which these birds serve as hosts.

California