The trophic responses of two different rodent–vector–plague systems to climate change

Plague, the causative agent of three devastating pandemics in history, is currently a re-emerging disease, probably due to climate change and other anthropogenic changes. Without understanding the response of plague systems to anthropogenic or climate changes in their trophic web, it is unfeasible to effectively predict years with high risks of plague outbreak, hampering our ability for effective prevention and control of the disease. Here, by using surveillance data, we apply structural equation modelling to reveal the drivers of plague prevalence in two very different rodent systems: those of the solitary Daurian ground squirrel and the social Mongolian gerbil. We show that plague prevalence in the Daurian ground squirrel is not detectably related to its trophic web, and that therefore surveillance efforts should focus on detecting plague directly in this ecosystem. On the other hand, plague in the Mongolian gerbil is strongly embedded in a complex, yet understandable trophic web of climate, vegetation, and rodent and flea densities, making the ecosystem suitable for more sophisticated low-cost surveillance practices, such as remote sensing. As for the trophic webs of the two rodent species, we find that increased vegetation is positively associated with higher temperatures and precipitation for both ecosystems. We furthermore find a positive association between vegetation and ground squirrel density, yet a negative association between vegetation and gerbil density. Our study thus shows how past surveillance records can be used to design and improve existing plague prevention and control measures, by tailoring them to individual plague foci. Such measures are indeed highly needed under present conditions with prevailing climate change.     

Persistence of plague outbreaks among great gerbils in Kazakhstan: effects of host population dynamics

Outbreaks of plague (Yersinia pestis) among great gerbils (Rhombomys opimus) generally require a high host abundance to be initiated. The duration of an outbreak is expected to depend on the subsequent development of this abundance; however, prediction is nontrivial due to the complexity of the gerbil–plague system. The aim of this study was to investigate how the duration of outbreaks depends on different types of host population dynamics generated from: a cyclic model; an autoregressive model giving irregular fluctuations; and a simple model with uncorrelated fluctuations. For each model, outbreak duration was studied under various levels of mean and variability of host abundance. Its focus on the effect of different gerbil dynamics sets this study apart from the few published studies on diseases in dynamic host populations. Plague outbreaks were simulated in a cellular automaton model based on statistical analysis of archived records of plague and host abundance. Temporal autocorrelation was found to make outbreak duration less sensitive to changes in mean abundance than uncorrelated fluctuations. Cyclicity had little effect on the mean duration of outbreaks, but resulted in a multimodal distribution. For all three types of gerbil dynamics, increased variability in gerbil abundance reduced the duration of outbreaks when the mean abundance was high (paralleling results on the risk of species extinction in fluctuating environments), but increased their duration when the mean abundance was lower. Spatial heterogeneity was briefly tested and produced longer outbreaks than the homogenous case. The results are relevant to predicting plague activity in populations of great gerbils.     

Modeling the epidemiological history of plague in Central Asia: Palaeoclimatic forcing on a disease system over the past millennium

Background

Human cases of plague (Yersinia pestis) infection originate, ultimately, in the bacterium's wildlife host populations. The epidemiological dynamics of the wildlife reservoir therefore determine the abundance, distribution and evolution of the pathogen, which in turn shape the frequency, distribution and virulence of human cases. Earlier studies have shown clear evidence of climatic forcing on contemporary plague abundance in rodents and humans.

Results

We find that high-resolution palaeoclimatic indices correlate with plague prevalence and population density in a major plague host species, the great gerbil (Rhombomys opimus), over 1949-1995. Climate-driven models trained on these data predict independent data on human plague cases in early 20th-century Kazakhstan from 1904-1948, suggesting a consistent impact of climate on large-scale wildlife reservoir dynamics influencing human epidemics. Extending the models further back in time, we also find correspondence between their predictions and qualitative records of plague epidemics over the past 1500 years.

Conclusions

Central Asian climate fluctuations appear to have had significant influences on regional human plague frequency in the first part of the 20th century, and probably over the past 1500 years. This first attempt at ecoepidemiological reconstruction of historical disease activity may shed some light on how long-term plague epidemiology interacts with human activity. As plague activity in Central Asia seems to have followed climate fluctuations over the past centuries, we may expect global warming to have an impact upon future plague epidemiology, probably sustaining or increasing plague activity in the region, at least in the rodent reservoirs, in the coming decades. See commentary: http://www.biomedcentral.com/1741-7007/8/108     

Dynamics of Yersinia pestis and Its Antibody Response in Great Gerbils (Rhombomys opimus) by Subcutaneous Infection

Background

Rhombomys opimus (great gerbil) is a reservoir of Yersinia pestis in the natural plague foci of Central Asia. Great gerbils are highly resistant to Y. pestis infection. The coevolution of great gerbils and Y. pestis is believed to play an important role in the plague epidemics in Central Asia plague foci. However, the dynamics of Y. pestis infection and the corresponding antibody response in great gerbils have not been evaluated. In this report, animal experiments were employed to investigate the bacterial load in both the liver and spleen of infected great gerbils. The dynamics of the antibody response to the F1 capsule antigen of Y. pestis was also determined.

Methodology

Captured great gerbils that tested negative for both anti-F1 antibodies and bacterial isolation were infected subcutaneously with different doses (10⁵ to 10¹¹ CFU) of a Y. pestis strain isolated from a live great gerbil during routine plague surveillance in the Junggar Basin, Xinjiang, China. The clinical manifestations, changes in body weight, anal temperature, and gross anatomy of the infected animals were observed. The blood cell count, bacterial load, and anti-F1 antibody titers were determined at different time points after infection using a blood analyzer, plate counts, and an indirect hemagglutination assay, respectively.

Conclusions/Significance

The dynamics of bacterial load and the anti-F1 antibody concentration in great gerbils are highly variable among individuals. The Y. pestis infection in great gerbils could persist as long as 15 days. They act as an appropriate reservoir for plague in the Junggar Basin, which is part of the natural plague foci in Central Asia. The dynamics of the Y. pestis susceptibility of great gerbil will improve the understanding of its variable resistance, which would facilitate the development of more effective countermeasures for controlling plague epidemics in this focus.     

Zoonotic Echinostome Infections in Free-Grazing Ducks in Thailand

Free-grazing ducks play a major role in the rural economy of Eastern Asia in the form of egg and meat production. In Thailand, the geographical location, tropical climate conditions and wetland areas of the country are suitable for their husbandry. These environmental factors also favor growth, multiplication, development, survival, and spread of duck parasites. In this study, a total of 90 free-grazing ducks from northern, central, and northeastern regions of Thailand were examined for intestinal helminth parasites, with special emphasis on zoonotic echinostomes. Of these, 51 (56.7%) were infected by one or more species of zoonotic echinostomes, Echinostoma revolutum, Echinoparyphium recurvatum, and Hypoderaeum conoideum. Echinostomes found were identified using morphological criteria when possible. ITS2 sequences were used to identify juvenile and incomplete worms. The prevalence of infection was relatively high in each region, namely, north, central, and northeast region was 63.2%, 54.5%, and 55.3%, respectively. The intensity of infection ranged up to 49 worms/infected duck. Free-grazing ducks clearly play an important role in the life cycle maintenance, spread, and transmission of these medically important echinostomes in Thailand.     

Plague and climate: scales matter

Plague is enzootic in wildlife populations of small mammals in central and eastern Asia, Africa, South and North America, and has been recognized recently as a reemerging threat to humans. Its causative agent Yersinia pestis relies on wild rodent hosts and flea vectors for its maintenance in nature. Climate influences all three components (i.e., bacteria, vectors, and hosts) of the plague system and is a likely factor to explain some of plague's variability from small and regional to large scales. Here, we review effects of climate variables on plague hosts and vectors from individual or population scales to studies on the whole plague system at a large scale. Upscaled versions of small-scale processes are often invoked to explain plague variability in time and space at larger scales, presumably because similar scale-independent mechanisms underlie these relationships. This linearity assumption is discussed in the light of recent research that suggests some of its limitations.     

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.     

Prominent role of volcanism in Common Era climate variability and human history

Climate reconstructions for the Common Era are compromised by the paucity of annually-resolved and absolutely-dated proxy records prior to medieval times. Where reconstructions are based on combinations of different climate archive types (of varying spatiotemporal resolution, dating uncertainty, record length and predictive skill), it is challenging to estimate past amplitude ranges, disentangle the relative roles of natural and anthropogenic forcing, or probe deeper interrelationships between climate variability and human history. Here, we compile and analyse updated versions of all the existing summer temperature sensitive tree-ring width chronologies from the Northern Hemisphere that span the entire Common Era. We apply a novel ensemble approach to reconstruct extra-tropical summer temperatures from 1 to 2010 CE, and calculate uncertainties at continental to hemispheric scales. Peak warming in the 280s, 990s and 1020s, when volcanic forcing was low, was comparable to modern conditions until 2010 CE. The lowest June–August temperature anomaly in 536 not only marks the beginning of the coldest decade, but also defines the onset of the Late Antique Little Ice Age (LALIA). While prolonged warmth during Roman and medieval times roughly coincides with the tendency towards societal prosperity across much of the North Atlantic/European sector and East Asia, major episodes of volcanically-forced summer cooling often presaged widespread famines, plague outbreaks and political upheavals. Our study reveals a larger amplitude of spatially synchronized summer temperature variation during the first millennium of the Common Era than previously recognised.     

A Non-Stationary Relationship between Global Climate Phenomena and Human Plague Incidence in Madagascar

Background

Plague, a zoonosis caused by Yersinia pestis, is found in Asia and the Americas, but predominantly in Africa, with the island of Madagascar reporting almost one third of human cases worldwide. Plague''s occurrence is affected by local climate factors which in turn are influenced by large-scale climate phenomena such as the El Niño Southern Oscillation (ENSO). The effects of ENSO on regional climate are often enhanced or reduced by a second large-scale climate phenomenon, the Indian Ocean Dipole (IOD). It is known that ENSO and the IOD interact as drivers of disease. Yet the impacts of these phenomena in driving plague dynamics via their effect on regional climate, and specifically contributing to the foci of transmission on Madagascar, are unknown. Here we present the first analysis of the effects of ENSO and IOD on plague in Madagascar.

Methodology/principal findings

We use a forty-eight year monthly time-series of reported human plague cases from 1960 to 2008. Using wavelet analysis, we show that over the last fifty years there have been complex non-stationary associations between ENSO/IOD and the dynamics of plague in Madagascar. We demonstrate that ENSO and IOD influence temperature in Madagascar and that temperature and plague cycles are associated. The effects on plague appear to be mediated more by temperature, but precipitation also undoubtedly influences plague in Madagascar. Our results confirm a relationship between plague anomalies and an increase in the intensity of ENSO events and precipitation.

Conclusions/significance

This work widens the understanding of how climate factors acting over different temporal scales can combine to drive local disease dynamics. Given the association of increasing ENSO strength and plague anomalies in Madagascar it may in future be possible to forecast plague outbreaks in Madagascar. The study gives insight into the complex and changing relationship between climate factors and plague in Madagascar.     

Rhombomys opimus contribution to the “fertile island” effect of tamarisk mounds in Junggar Basin

Fertile islands are created and maintained by a combination of physical and biologically mediated processes. Plants have been shown to be very important in the formation of fertile islands, and recent research indicates that the activities of burrowing animals have a significant influence on the physiochemical properties of soil that can promote the development of fertile islands. In this paper, we chose tamarisk (Tamarix spp.)??a constructive species that grows in the oasis-desert ecotone, and the great gerbil (Rhombomys opimus)??a widely distributed rodent in Central Asia to study the influence of great gerbils on soil nutrient dynamics in tamarisk mounds. Results indicate that fertile islands exist in tamarisk mounds without burrows of the great gerbil. However, the great gerbil??s burrowing activities promote the fertile island effect in tamarisk mounds: soil nutrients under shrubs with great gerbil activity were significantly higher than inter-mound areas in both surface soil and deep soil from 15 to 50?cm. Available nitrogen in mounds with rodent burrows was over twice as high as in tamarisk mounds without burrows at the same depth. The great gerbil??s burrowing activities promote the concentration of soil nutrients in the tamarisk mounds.     

气候变化对柴胡与狭叶柴胡适生分布的影响

研究气候变化下物种适生区的分布格局与变迁,对于物种的保护和资源的可持续利用具有重要的理论和实践意义。选取柴胡(Bupleurum chinense)与狭叶柴胡(Bupleurum scorzonerifolium)在中国地域内的381个有效分布点和36个环境因子,利用MaxEnt模型模拟当前以及未来(2050和2070年)两种气候情景下(RCP4.5和RCP8.5)其适生区的分布格局,并分析了制约其适生区分布的主导环境因子。结果表明：(1)影响柴胡适生区分布的主导环境因子为最湿月份降水量、最干季度平均温度以及海拔。影响狭叶柴胡适生区分布的主导环境因子为最湿月份降水量、温度季节性变化标准差以及海拔;(2)当前气候条件下,柴胡适生区总面积为1.4755×10⁶km²,约占我国国土面积的15.37%,中、高度适生区主要分布在陕西南部、山西东部、甘肃东南部、山东中部、河北中西部等地;狭叶柴胡适生区总面积为1.8034×10⁶km²,约占我国国土面积的18.78%,中、高度适生区主要分布在黑龙江西部和东部、内...     

Climate change promotes transitions to tall evergreen vegetation in tropical Asia

Vegetation in tropical Asia is highly diverse due to large environmental gradients and heterogeneity of landscapes. This biodiversity is threatened by intense land use and climate change. However, despite the rich biodiversity and the dense human population, tropical Asia is often underrepresented in global biodiversity assessments. Understanding how climate change influences the remaining areas of natural vegetation is therefore highly important for conservation planning. Here, we used the adaptive Dynamic Global Vegetation Model version 2 (aDGVM2) to simulate impacts of climate change and elevated CO₂ on vegetation formations in tropical Asia for an ensemble of climate change scenarios. We used climate forcing from five different climate models for representative concentration pathways RCP4.5 and RCP8.5. We found that vegetation in tropical Asia will remain a carbon sink until 2099, and that vegetation biomass increases of up to 28% by 2099 are associated with transitions from small to tall woody vegetation and from deciduous to evergreen vegetation. Patterns of phenology were less responsive to climate change and elevated CO₂ than biomes and biomass, indicating that the selection of variables and methods used to detect vegetation changes is crucial. Model simulations revealed substantial variation within the ensemble, both in biomass increases and in distributions of different biome types. Our results have important implications for management policy, because they suggest that large ensembles of climate models and scenarios are required to assess a wide range of potential future trajectories of vegetation change and to develop robust management plans. Furthermore, our results highlight open ecosystems with low tree cover as most threatened by climate change, indicating potential conflicts of interest between biodiversity conservation in open ecosystems and active afforestation to enhance carbon sequestration.     

A case of experimental transmission of the causative agent of plague from Ornithodoros tartakovskyi ticks to fleas of the great gerbil

Biological interrelations between ectoparasites from the colonies of great gerbil were studied experimentally. Hungry fleas Coptopsylla lamellifer are able to feed on the ticks Ornithodoros tartakovskyi infected with plague and in so doing be infected with plague agent. Such feeding is identified as "heterovampirism".     

Empiric physiology in epidemiologic doctrines of the 18th century, Hungarian General Norm of Health in 1770

According to standard textbooks, the last episode of European New Age plague pandemic died out by 1720 in Marseilles. Despite this allegation, the pandemic continued in well-documented new outbreaks, which attacked and devastated Central and Eastern Europe throughout the first half of the 18th century. At the beginning, military campaigns spread the infection out of the Ottoman Empire. Later on commercial goods took over this role via land or sea from Asia or out of the eastern Mediterranean region. Finally, the plague in Europe--except Russia and the Ottoman Empire--"died out" virtually by the end of the 18th century. Explaining this, there many scientific reasons were suggested: 1. Oriental rat fleas as main vectors of infection could not tolerate any more the European weather conditions (although there were no virtual climate changes in the last 300 years). 2. Black rats that lived in close proximity to man, were being outplayed by brown rats living rather outside of human habitats; 3. There emerged less virulent Yersinia strains that caused natural human immunisation. In spite of these suggestions, which may have contributed to the success, joint civil and military health authorities blocked the plague indeed, as a result of disciplined and relentless law enforcement. In Hungary, respectively in the Hapsburg Empire, well-advised health legislation backed up the effectiveness of local authorities. Following the last great devastation in 1738-1740, the General Norm of Health Service--a voluminous decree--summed up by 1770 all the time honoured empiric rules of foregoing centuries. It can be excellently demonstrated, how exactly the empiric rules discovered a century later met scientific facts of physiology and microbiology.     

Preventing desert locust plagues: optimizing management interventions

Solitarious desert locusts, Schistocerca gregaria (Forskål) (Orthoptera: Acrididae), inhabit the central, arid, and semi‐arid parts of the species’ invasion area in Africa, the Middle East, and South‐West Asia. Their annual migration circuit takes them downwind to breed sequentially where winter, spring, and summer rains fall. In many years, sparse and erratic seasonal rains support phase change and local outbreaks at only a few sites. Less frequently, seasonal rains are widespread, frequent, heavy, and long lasting, and many contemporaneous outbreaks occur. When such seasonal rains fall sequentially, populations develop into an upsurge and eventually into a plague unless checked by drought, migration to hostile habitats, or effective control. Increases in the proportion of gregarious populations as the plague develops alter the effectiveness of control. As an upsurge starts, only a minority of locusts is aggregated into treatable targets and spraying them leaves sufficient unsprayed individuals to continue the upsurge. Spraying all individuals scattered within an entire infested zone is arguably both financially and environmentally unacceptable. More of the population gregarizes and forms sprayable targets after each successive season of good rains and successful breeding. Eventually, unless the rains fail, the entire upsurge population becomes aggregated at high densities so that the infested area diminishes and a plague begins. These populations must continue to increase numerically and spread geographically to achieve peak plague levels, a stage last reached in the 1950s. Effective control, aided by poor rains, accompanied each subsequent late upsurge and early plague stage and all declined rapidly. The control strategy aims to reduce populations to prevent plagues and damage to crops and grazing. Differing opinions on the optimum stage to interrupt pre‐plague breeding sequences are reviewed.     

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.     

Draft Genome Sequence of Yersinia pestis Strain 2501, an Isolate from the Great Gerbil Plague Focus in Xinjiang, China

We deciphered the genome of Yersinia pestis strain 2501, isolated from the Junggar Basin, a newly discovered great gerbil plague focus in Xinjiang, China. The total length of assembly was 4,597,322 bp, and 4,265 coding sequences were predicted within the genome. It is the first Y. pestis genome from this plague focus.     

Population coverage analysis of T-Cell epitopes of Neisseria meningitidis serogroup B from Iron acquisition proteins for vaccine design

Although the concept of Reverse Vaccinology was first pioneered for sepsis and meningococcal meningitidis causing bacterium, Neisseria meningitides, no broadly effective vaccine against serogroup B meningococcal disease is yet available. In the present investigation, HLA distribution analysis was undertaken to select three most promiscuous T-cell epitopes out of ten computationally validated epitopes of Iron acquisition proteins from Neisseria MC58 by using the population coverage tool of Immune Epitope Database (IEDB). These epitopes have been determined on the basis of their binding ability with maximum number of HLA alleles along with highest population coverage rate values for all the geographical areas studied. The comparative population coverage analysis of moderately immunogenic and high immunogenic peptides suggests that the former may activate T-cell response in a fairly large proportion of people in most geographical areas, thus indicating their potential for development of epitope-based vaccine.     

Large-scale phytogeographical patterns in East Asia in relation to latitudinal and climatic gradients

Aim This paper aims at determining how different floristic elements (e.g. cosmopolitan, tropical, and temperate) change with latitude and major climate factors, and how latitude affects the floristic relationships between East Asia and the other parts of the world. Location East Asia from the Arctic to tropical regions, an area crossing over 50° of latitudes and covering the eastern part of China, Korea, Japan and the eastern part of Russia. Methods East Asia is divided into forty‐five geographical regions. Based on the similarity of their world‐wide distributional patterns, a total of 2808 indigenous genera of seed plants found in East Asia were grouped into fourteen geographical elements, belonging to three major categories (cosmopolitan, tropical and temperate). The 50°‐long latitudinal gradient of East Asia was divided into five latitudinal zones, each of c. 10°. Phytogeographical relationships of East Asia to latitude and climatic variables were examined based on the forty‐five regional floras. Results Among all geographical and climatic variables considered, latitude showed the strongest relationship to phytogeographical composition. Tropical genera (with pantropical, amphi‐Pacific tropical, palaeotropical, tropical Asia–tropical Australia, tropical Asia–tropical Africa and tropical Asia geographical elements combined) accounted for c. 80% of the total genera at latitude 20°N and for c. 0% at latitude 55–60°N. In contrast, temperate genera (including holarctic, eastern Asia–North America, temperate Eurasia, temperate Asia, Mediterranean, western Asia to central Asia, central Asia and eastern Asia geographical elements) accounted for 15.5% in the southernmost latitude and for 80% at 55–60°N, from where northward the percentage tended to level off. The proportion of cosmopolitan genera increased gradually with latitude from 5% at the southernmost latitude to 21% at 55–60°N, where it levelled off northward. In general, the genera present in a more northerly flora are a subset of the genera present in a more southerly flora. Main conclusions The large‐scale patterns of phytogeography in East Asia are strongly related to latitude, which covaries with several climatic variables such as temperature. Evolutionary processes such as the adaptation of plants to cold climates and current and past land connections are likely responsible for the observed latitudinal patterns.     

中国鼠疫宿主鼠类丰富度格局及疫区环境因子分析

鼠疫等媒介疾病地理分布规律的认识对于疫病防控具有重要意义,分析影响疾病地理分布的因素进而预测疾病发生趋势已经成为目前研究的热点。本文在分析鼠间鼠疫及其宿主鼠类地理分布数据以及相关环境数据的基础上,探讨了鼠疫宿主丰富度与环境因子的关系以及影响鼠间鼠疫发生的主要环境因素。我国的鼠疫宿主鼠类在干旱区和季风区过渡带的县级行政单元中物种丰富度最高,物种丰富度与高度差正相关性最高。发生鼠间鼠疫的地区,宿主鼠类丰富度较高,未发生鼠间鼠疫的地区,宿主鼠类丰富度较低。影响鼠间鼠疫发生的主要环境因子包括蚤类物种数、年均气温、年降雨量、年均相对湿度和年日照时数和气候因子,其次是包括高度差、植被类型数、土壤类型数和地貌类型数的景观因子,以及反映海拔和宿主鼠类物种数的地形和宿主鼠类因子。在未来全国气候变干变暖条件下,我国鼠间鼠疫发病区可能随宿主鼠类的迁移而扩展。