Prevalence of Yersinia pestis in rodents and fleas associated with black-tailed prairie dogs (Cynomys ludovicianus) at Thunder Basin National Grassland, Wyoming

Rodents (and their fleas) that are associated with prairie dogs are considered important for the maintenance and transmission of the bacterium (Yersinia pestis) that causes plague. Our goal was to identify rodent and flea species that were potentially involved in a plague epizootic in black-tailed prairie dogs at Thunder Basin National Grassland. We collected blood samples and ectoparasites from rodents trapped at off- and on-colony grids at Thunder Basin National Grassland between 2002 and 2004. Blood samples were tested for antibodies to Y. pestis F-1 antigen by a passive hemagglutination assay, and fleas were tested by a multiplex polymerase chain reaction, for the presence of the plague bacterium. Only one of 1,421 fleas, an Oropsylla hirsuta collected in 2002 from a deer mouse, Peromyscus maniculatus, tested positive for Y. pestis. Blood samples collected in summer 2004 from two northern grasshopper mice, Onychomys leucogaster, tested positive for Y. pestis antibodies. All three positive samples were collected from on-colony grids shortly after a plague epizootic occurred. This study confirms that plague is difficult to detect in rodents and fleas associated with prairie dog colonies, unless samples are collected immediately after a prairie dog die-off.     

Experimental study of the infecting ability of the flea Coptopsylla lamellifer rostrata in the Kyzylkum natural focus of plague

Experimental infecting of the fleas Coptopsylla lamellifer rostrata by plague was carried out. The fleas were infected by feeding through biomembrane (skin of a white mouse) with a mixture of defibrinated blood of guinea-pig and plague microbes. Under concentration 2-3 milliard of the microbes in 1 millilitre, from 60 to 100% of the fleas were infected. Forming of the block of proventriculus was observed in 9-13 day. Mean percent of blocking for all experiments was less than 1%. Maximal rate of blocking (2.8%) was observed in the experiment under everyday 3-hour feeding. After planting of the fleas with blocks on great gerbil (2 fleas on one gerbil) 20% of the gerbils were infected. The conclusion had been made that C. lamellifer rostrata has only insignificant effectiveness as a vector of plague agent in Kyzylkum. Probably it is caused by some specific features of this subspecies.     

No evidence of persistent Yersina pestis infection at prairie dog colonies in north-central Montana

Sylvatic plague is a flea-borne zoonotic disease caused by the bacterium Yersinia pestis, which can cause extensive mortality among prairie dogs (Cynomys) in western North America. It is unclear whether the plague organism persists locally among resistant host species or elsewhere following epizootics. From June to August 2002 and 2003 we collected blood and flea samples from small mammals at prairie dog colonies with a history of plague, at prairie dog colonies with no history of plague, and from off-colony sites where plague history was unknown. Blood was screened for antibody to Y. pestis by means of enzyme-linked immunosorbent assay or passive hemagglutination assay and fleas were screened for Y. pestis DNA by polymerase chain reaction. All material was negative for Y. pestis including 156 blood samples and 553 fleas from colonies with a known history of plague. This and other studies provide evidence that Y. pestis may not persist at prairie dog colonies following an epizootic.     

Ecological characteristics of flea species relate to their suitability as plague vectors

The ability of vector-borne diseases to persist and spread is closely linked to the ecological characteristics of the vector species they use. Yet there have been no investigations of how species used as vectors by pathogens such as the plague bacterium differ from closely related species that are not used as vectors. The plague bacterium uses mammals as reservoir hosts and fleas as vectors. The ability of different fleas to serve as vectors is assumed to depend on how likely they are to experience gut blockage following bacterial multiplication; the blockage causes fleas to regurgitate blood into a wound and thus inject bacteria into new hosts. Beyond these physiological differences, it is unclear whether there exist fundamental ecological differences between fleas that are effective vectors and those that are not. Here, using a comparative analysis, we identify clear associations between the ability of flea species to transmit plague and their ecological characteristics. First, there is a positive relationship between the abundance of flea species on their hosts and their potential as vectors. Second, although the number of host species exploited by a flea is not associated with its potential as a vector, there is a negative relationship between the ability of fleas to transmit plague and the taxonomic diversity of their host spectrum. This suggests a correlation between some ecological characteristics of fleas and their ability to develop the plague blockage. The plague pathogen thus uses mainly abundant fleas specialized on a narrow taxonomic range of mammals, features that should maximize the persistence of the disease in the face of high flea mortality, and its transmission to suitable hosts only. This previously unrecognized pattern of vector use is of importance for the persistence and transmission of the disease.Electronic Supplementary Material Supplementary material is available to authorised users in the online version of this article at .     

Local factors associated with on‐host flea distributions on prairie dog colonies

Outbreaks of plague, a flea‐vectored bacterial disease, occur periodically in prairie dog populations in the western United States. In order to understand the conditions that are conducive to plague outbreaks and potentially predict spatial and temporal variations in risk, it is important to understand the factors associated with flea abundance and distribution that may lead to plague outbreaks. We collected and identified 20,041 fleas from 6,542 individual prairie dogs of four different species over a 4‐year period along a latitudinal gradient from Texas to Montana. We assessed local climate and other factors associated with flea prevalence and abundance, as well as the incidence of plague outbreaks. Oropsylla hirsuta, a prairie dog specialist flea, and Pulex simulans, a generalist flea species, were the most common fleas found on our pairs. High elevation pairs in Wyoming and Utah had distinct flea communities compared with the rest of the study pairs. The incidence of prairie dogs with Yersinia pestis detections in fleas was low (n = 64 prairie dogs with positive fleas out of 5,024 samples from 4,218 individual prairie dogs). The results of our regression models indicate that many factors are associated with the presence of fleas. In general, flea abundance (number of fleas on hosts) is higher during plague outbreaks, lower when prairie dogs are more abundant, and reaches peak levels when climate and weather variables are at intermediate levels. Changing climate conditions will likely affect aspects of both flea and host communities, including population densities and species composition, which may lead to changes in plague dynamics. Our results support the hypothesis that local conditions, including host, vector, and environmental factors, influence the likelihood of plague outbreaks, and that predicting changes to plague dynamics under climate change scenarios will have to consider both host and vector responses to local factors.     

The ability of flea species on the common vole from mountainous Dagestan to transmit and preserve the causative agent of plague

The infection ability and terms of preservation of plague microbe in fleas of common vole from Dagestan high-mountain plague focus (Frontopsylla causasica, Megabothris turbidus, Ctenophthalmus intermedius and Amphipsylla rossica) was studied experimentally. Block formation and transmission of the infection by F. caucasica and M. turbidus was observed. The transmission of plague microbe by Ct. intermedius fleas was first carried out. These species of fleas preserve the infection for a long time. Experiments with fleas of A. rossica yielded negative results.     

Paradoxopsyllus scorodumovi (Aphaniptera) flea, an effective vector of plague in a Gorno-Altai natural focus

A study was conducted on the fleas of P. scorodumovi and five local strains of the plague microbe, one of which is typical of the strains of the Altai subspecies and four are non-typical of this nidus. The fleas of this species are capable to transmit not only the plague agent of the strains typical of this nidus but also non-typical ones which differ in some biological properties and are avirulent for most carriers but Pallas's pika. Biological peculiarities of fleas of P. scorodumovi in addition to their high efficiency as vectors of the plague microbe enable us to associate the more active autumn epizooty with fleas of this species.     

The efficiency of Rhadinopsylla rothschildi and R. dahurica fleas as vectors of the causative agent of plague in a Transbaikal natural focus

Experiments have shown that a block of proventriculus arises in 2.1 to 12.5% of infected fleas of R. rothschildi and in 7.2 to 10.5% of R. dahurica. These fleas transmit the plague agent to different animals (Brandt's vole, narrow-skulled vole, Dahurian suslik). The plague microbe is preserved in the organism of infected insects till the end of the experiment, 74 and 24 days respectively. Therefore, the fleas can play a part in the maintenance of plague epizootics in the Transbaikal natural nidus.     

New records of sylvatic plague in Kansas

Sylvatic plague, or plague of wild rodents is caused by Yersinia pestis and entered California (USA) from Asia about 1899. Extensive sampling during the 1930's and 1940's documented the spread of plague to approximately its current distribution in North America. Records from the Centers for Disease Control and Prevention document plague in Kansas (USA) between 1945 and 1950, but since then there has been no documentation of plague in the state. Following a die-off of a black-tailed prairie dog (Cynomys ludovicianus) colony on the Cimarron National Grassland, in the southwestern corner of Kansas (3710'N, 10145'W), we sampled fleas from burrows in June 1997, and tested them for Yersinia pestis. Twelve of 13 pools of Oropsyla hirsuta and one of two Pulex sp. were positive. A similar sample of fleas, from another colony where black-tailed prairie dogs were active at the time, yielded no positive fleas.     

中国云南人间鼠疫流行区蚤类宿主特异性及宿主选择(英文)

应用生态学中的生态位宽度及生态位重叠研究方法,对中国云南人间鼠疫流行区１１种蚤的宿主特异性及宿主选择进行了研究。宿主特异性用Ｌｅｖｉｎｓ生态位宽度进行测定。宿主选择用夹角余弦生态位重叠进行测定。结果表明：长形病蚤普洱亚种及印鼠客蚤的生态位宽度最窄、宿主特异性最高,近端远棒蚤二刺亚种及斯氏新蚤滇川亚种的生态位最宽、宿主特异性最低。印鼠客蚤（云南人间鼠疫流行区的主要鼠疫媒介）的优势宿主是黄胸鼠。印鼠客蚤较高的宿主特异性意味着该蚤可能主要在其优势宿主的不同个体间保存或传播鼠疫病原体。短突栉眼蚤及端凹栉眼蚤在宿主选择上较接近,而其它蚤种在宿主选择上差异较大。     

Changes in Flea (Siphonaptera) Vector Activity in the Siberian Natural Plague Foci

Comparative analysis of vector activity of fleas in the Siberian natural plague foci was carried out during two long-term periods of experimental studies: 1967–1980 and 1983–2007. The data on block formation frequency in adult fleas infected with Yersinia pestis were analyzed for 127 experiments with 15 flea species and subspecies. The vector activity of fleas in all the Siberian plague foci (Altai, Tuva, and Transbaikalia) has increased over a rather short time period of 30–40 years. The frequencies of flea blocking were significantly different (P < 0.001) between the analyzed periods in all the three plague foci.

     

Main traits of the annual cycles of the fleas (Aphaniptera) of the mountain suslik in the Baksan River valley

Data are given on the fleas of Citellus musicus from Central Caucasus. Ecological peculiarities of fleas from the above region were compared with data known for fleas from plain Precaucasus. Differences between annual cycles of fleas of the same species from two altitude belts of the Baksan valley are considered. Epizootological significance of ecological peculiarities of fleas in the Baksan plague nidus is discussed.     

Relationship of the flea Citellophilus tesquorum altaicus (Siphonaptera: Ceratophyllidae) with the plague agent

Some aspects of relationships of the flea Citellophilus tesquorum altaicus and bacterium Yersinia pestis of two strains isolated from different parts of the Tuva natural plague focus were studied. Peculiarities of elimination and blood meal activity of fleas infected with two strains of the plague agent were not revealed. Differences in mortality and alimentary activity are considerably determined by the sex of insects. The ability of examined strains to form a proventriculus block was not identical in the strains examined. This ability was expressed higher in the strain I-3428, which originated from the same part of the natural focus as the insectarium flea culture, than in the strain I-3327. During the spring and first half of summer, the proventriculus block appeared more frequently in females. The increasing of the fraction of blocked individuals was observed in both sexes from spring to summer. As for the ability to transmit the plague agent, similar seasonal increasing was noted in males, but in females, the ability to inoculate the plague microbe was always maintained at the same level.     

Transmission shifts underlie variability in population responses to Yersinia pestis infection

Host populations for the plague bacterium, Yersinia pestis, are highly variable in their response to plague ranging from near deterministic extinction (i.e., epizootic dynamics) to a low probability of extinction despite persistent infection (i.e., enzootic dynamics). Much of the work to understand this variability has focused on specific host characteristics, such as population size and resistance, and their role in determining plague dynamics. Here, however, we advance the idea that the relative importance of alternative transmission routes may vary causing shifts from epizootic to enzootic dynamics. We present a model that incorporates host and flea ecology with multiple transmission hypotheses to study how transmission shifts determine population responses to plague. Our results suggest enzootic persistence relies on infection of an off-host flea reservoir and epizootics rely on transiently maintained flea infection loads through repeated infectious feeds by fleas. In either case, early-phase transmission by fleas (i.e., transmission immediately following an infected blood meal) has been observed in laboratory studies, and we show that it is capable of driving plague dynamics at the population level. Sensitivity analysis of model parameters revealed that host characteristics (e.g., population size and resistance) vary in importance depending on transmission dynamics, suggesting that host ecology may scale differently through different transmission routes enabling prediction of population responses in a more robust way than using either host characteristics or transmission shifts alone.     

Possible vector dissemination by swift foxes following a plague epizootic in black-tailed prairie dogs in northwestern Texas

To determine whether swift foxes (Vulpes velox) could facilitate transmission of Yersinia pestis to uninfected black-tailed prairie dog (Cynomys ludovicianus) colonies by acquiring infected fleas, ectoparasite and serologic samples were collected from swift foxes living adjacent to prairie dog towns during a 2004 plague epizootic in northwestern Texas, USA. A previous study (1999-2001) indicated that these swift foxes were infested almost exclusively with the flea Pulex irritans. Black-tailed prairie dogs examined from the study area harbored only Pulex simulans and Oropsylla hirsuta. Although P. irritans was most common, P. simulans and O. hirsuta were collected from six swift foxes and a single coyote (Canis latrans) following the plague epizootic. Thus, both of these canids could act as transport hosts (at least temporarily) of prairie dog fleas following the loss of their normal hosts during a plague die-off. All six adult swift foxes tested positive for antibodies to Y. pestis. All 107 fleas from swift foxes tested negative for Y. pestis by mouse inoculation. Although swift foxes could potentially carry Y. pestis to un-infected prairie dog colonies, we believe they play only a minor role in plague epidemiology, considering that they harbored just a few uninfected prairie dog fleas (P. simulans and O. hirsuta).     

Uniquely insidious: Yersinia pestis biofilms

Bubonic plague, one of history's deadliest infections, is transmitted by fleas infected with Yersinia pestis. The bacteria can starve fleas by blocking their digestive tracts, which stimulates the insects to bite repeatedly and thereby infect new hosts. Direct examination of infected fleas, aided by in vitro studies and experiments with the nematode Caenorhabditis elegans, have established that Y. pestis forms a biofilm in the insect. The extracellular matrix of the biofilm seems to contain a homopolymer of N-acetyl-d-glucosamine, which is a constituent of many bacterial biofilms. A regulatory mechanism involved in Y. pestis biofilm formation, cyclic-di-GMP signaling, is also widespread in bacteria; yet only Y. pestis forms biofilms in fleas. Here, the historical background of bubonic plague is briefly described and recent studies investigating the mechanisms by which these unique and deadly biofilms are formed are discussed.     

Level of parasitic contact in colonies of the little suslik in the semideserts of western Kazakhstan

Field experiments were conducted during the settling of young animals of Citellus pygmaeus in four areas 4 to 13.6 hectares in size. From 3 to 6 animals were caught in each area and labeled by administering radioactive substance (0.5 micrograms of glycine 14C or methionine 35S) and colouring hair on the head. In a day or two labeled sousliks were caught again and in 6-7 days a total catching of animals and collection of ectoparasites from their hair and burrows done. In al, 942 sousliks were caught in the experimental areas and 2624 specimens of fleas of different species and 2305 ticks of R. schulzei collected. The average number of fleas which were labeled on one little souslik for a day was 0.1 to 2.3. The number of labeled fleas in the above areas coincided with the number of fleas infected with plague in the areas of epizootia. The level of parasitic contact in settlements of little souslik cannot provide the development of plague epizootia by transmission of the agent through fleas.     

Pathogenic action of the plague microbe on the flea Xenopsylla cheopis and the ultrastructure of the causative agent at various times of its stay in the vector

Pathology of gastro-intestinal tract of Xenopsylla cheopis fleas infected with plague microbe was determined by means of electron microscopy. Ultrastructure of plague microbe during different periods of its stay in the vector was studied.     

The experimental action of lindane on the vector capacity of plague-infected fleas]

Being fed on white mice, intoxicated with subtoxic doses of lindane, blocked fleas sharply decreased in number. The inhibition of the vector ability of fleas, infected with plague, under the systemic effect of lindane is shown.     

HOST-SPECIFICITY AND HOST-SELECTION OF FLEAS IN FOCI OF HUMAN PLAGUE IN YUNNAN CHINA*

Abstract The host-specificity and the host-selection of 11 species of fleas collected from 47 species of small mammals in foci of human plague in Yunnan, China, were studied by using methods in the evaluation of ecological niche breadth and overlap. Levins' niche breadth was used for the host-specificity. while clip angle niche overlap and a fuzzy clustering analysis were used for host-selection. Of the 11 species of fleas, the host-specificity of Nosopsyllus elongatus puerensis and Xenopsylla cheopis are the highest (narrow niche breadth), and those of Aviostivalis klossi bispiniformis and Neopsylla stevensi sichuanyunnana the lowest (wide niche breadth). Of 11 species of fleas, the dominant host of X. cheopis (a very high effective vector of plague in the foci of human plague in Yunnan Province. China) is Rattw flavipectus (the main animal host and infectious source of plague in the foci). A high host-specificity of X. cheopis implies that X. cheopis mainly maintains or transmits the pathogen of plague among the individuals of its dominant species of host, R. flavipectus. The result of niche overlap analysis reveals that Ctenophthalrnus In-evipre jiciens and Ctenophthaltnus parcus have a similar host-selection while other species of fleas are quite different in their host selection.