Spatial and Temporal Distribution of Rodents During Active and Quiescent Periods in the Plague Focus in Exu, Northeastern Brazil

The plague caused by the Yersinia pestis bacterium is primarily a fleatransmitted zoonosis of rodents that can also be conveyed to humans and other mammals. In this work, we analyzed the spatial and temporal distribution of rodents’ populations during active and quiescent periods of the plague in the municipality of Exu, northeastern Brazil. The geospatial analyses had shown that all rodent species occurred through the whole territory of the municipality with different hotspots for the risk of occurrence of the different species. Important fluctuation in the rodent populations was observed with a reduction in the wild rodent fauna following the end of a plague epidemic period, mostly represented by Necromys lasiurus and increase of the commensally species Rattus rattus. A higher abundance of rats might lead to an increased exposure of humans populations, favoring spillovers of plague and other rodent-borne diseases. Our analysis contributed to further highlight the role of the wild rodent species as the amplifier hosts and of the commensally rats (Rattus rattus) as the preserver hosts on the quiescent period on that transmission infection area. Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 1 September 2021 doi:10.20944/preprints202109.0022.v1 © 2021 by the author(s). Distributed under a Creative Commons CC BY license. 2


Introduction
The plague caused by the Yersinia pestis bacterium is primarily a flea-transmitted zoonosis of rodents their main hosts, that can also be conveyed to humans and other mammals [1]. The rodents constitute the most diverse order (Rodentia) of mammals, with almost 2,600 species, representing 40% of the living mammal species [2]. Out of these, 279 species have already been found naturally infected by Y. pestis [3].
The plague caused three worldwide pandemics in the Christian era, claiming numerous lives, with major impact in the course of our history, scientific development and culture [4][5]. The infection reaches Brazil by sea route in 1899, during the third pandemic, through the port of Santos, São Paulo state. The infection afflicted initially the brown rat-population of Rattus norvegicus of seaports and in the rural zone of the Northeast, the commensally species (Rattus rattus). Finally, it encountered the susceptible autochthonous wild or sylvatic fauna and established several natural foci where the ecological conditions were suitable for its persistence [6][7]. These foci persist until nowadays spreading throughout several mountain ranges and plateaus across the states of Ceará, Piauí, Rio Grande do Norte, Paraíba, Pernambuco, Alagoas, Bahia, Minas Gerais and Rio de Janeiro [8][9].
By analyzing the records of human plague in the Brazilian plague foci, the municipality of Exu located in the Pernambuco State, Northern Brazil, was considered the epicenter of the focal area of the Chapada do Araripe focus [10]. Based on the concepts of a natural-permanent focus and the telluric conservation of the plague bacillus inside the rodent´s burrows, Baltazard [10] hypothesized that the plague activity would persist for longer there and gradually turn quiescent until reappearing in the same regions.
Indeed, the Kernel density analysis (KDE) of the number of cases reported in Pernambuco revealed that the municipality of Exu is at higher risk for the occurrence of plague. Exu appeared at the epicenter of the Kernel patch that radiates in decreasing intensity as it moves away from the plateau slope towards the plains and neighboring municipalities [11].
The studies on the Rodentia and Siphonaptera faunas have become an important part of the plague control program activities and several field and laboratory studies have been 3 carried out to understand the possible role of the different rodent and flea species in the maintenance, epizootization, and epidemization of plague in the Brazilian focal areas. It is worth noting that an important part of this work was the continuous trapping of rodents to detect plague activity among wild species, especially Necromys lasiurus [10,[12][13][14][15][16][17].
Here, we analyzed the spatial and temporal distribution of rodents' populations in the municipality of Exu, northeastern Brazil from 1966 to 2005, during active and quiescent periods of human plague in the region.

Study area
The study was performed in the municipality of Exu ( Figure 1C  Google Earth Engine (GEE) platform. All geospatial data were obtained from free access and use platforms.

Data analysis
The rodent species, the locality and the year of collection were compiled and   The R. rattus, the most abundant species in the period, was widely disseminated throughout the territory and occupied a higher number of localities ( Figure 3B). However, the areas with the highest density and considered hotspots for the occurrence of this species are in the boundaries of the villages Tabocas, Viração, Timorante and Zé Gomes ( Figure 4B). N. lasiurus was also found throughout the territory and presented several hotspots near the villages Tabocas and Viração and a hotspot near the village Zé Gomes

Discussion
Practically since the arrival of the plague in Brazil in 1899, during the third pandemic, a surveillance and control program adjusted to the epidemiological situation, ecological and demographic characteristics and scientific and technological conditions has been carried out [7,10,17]. For several decades, the rodents were trapped for detection of the plague bacillus and/or antiplague antibodies [22][23][24]. The surveys among the rodents were discontinued in 2007 due to new evidences that serological survey of plague antibodies among roaming-dogs is a more efficient and cost effective tool for plague surveillance [17]. Rodent populations are well known to undergo significant fluctuations over both seasonal and multiannual cycles, which also impact the risk of zoonosis spillovers to humans [25]. Here, we observed 4 to 7 years intervals in the pendular N. lasiurus population spikes. However, from the last years of human cases of plague onwards, their abundance peaks were progressively decreasing both in frequency and abundance. From the 1995 peak until the end of the study period (2005) no N. lasiurus population growths were observed. The decline of these populations might be due to the important and continuous plague die offs of the susceptible species for many years [17]; climate change and environmental alterations promoted by agriculture [9].
From 1996 to 2005 no O. nigripes occurred and the species C. expulsus and W.
pyrrhorhinos were captured in small numbers (Figure 2A-B). The reduction or disappearance of these species does not qualify them as endangered species to extinction risks because this is just a local event [26]. It is noteworthy that some species may eventually show sudden and explosive multiplication popularly known as "ratadas". This As observed in Figure 3A and 4A, all species occurred in the whole territory of the municipality. The wild species live from agricultural products, which they consume in situ. Although occupying the same places (sitios or farms) dispersed throughout the territory, the different species do not occupy the same habitats. The species N. lasiurus, C. expulsus, C. langguthi, O. nigripes and W pyrrhorhinos usually shelter in sites covered by a low and dense vegetation, where they make their nests. Besides, C. langguthi, O.
nigripes and W. pyrrhorhinos can make nests in small threes or rock walls. Others (G. spixii, T. laurentius) shelter into chinks and crevices of rocks, further away from the humans [10,27].
The main economic activity in practically all the rural land of the municipality of Exu is dedicated to agricultural practiced in the "sitios" located mainly along the hydrographic network on the slopes of the Chapada do Araripe (seen in the satellite image - Figure 1C), where remnants of native vegetation (caatinga) are also found. The term "Sitio" means a rural land division usually including housing, functional buildings (barns, garages, storage areas) and a parcel for cultivating and/or raising stock. The human dwellings are generally unpaved or cemented or with brick floors, clay or brick walls and a roof of tile, zinc, grass or straw. They are often used as both housing and storage for crop products (maize, beans and cotton grains). Unlike the R. rattus, the wild rodents only exceptionally enter these dwellings.
The urbanization of some rural communities living with precarious sanitary infrastructure have set the ideal conditions for the expansion of the commensal rat [28].
Therefore, R. rattus were more abundant inside household captures ( Figure 5) or in the boundaries of the villages Tabocas, Viração, Timorante and Zé Gomes.
The high abundance of rats in those villages might lead to more contact between them and the inhabitants, favoring plague and other rodent-borne diseases [29].
Therefore, some preventive measures should be implemented in these villages including surveillance and rodent and insect control [20].
In a previous study in this same plague area [11], it was observed the transition of the infection from urban to rural areas. The plague reappeared in the rural area after six years of quiescence, and disseminated practically throughout the municipality territory among the wild fauna. According to the figures 3A-F, the dispersal area of the rodents in the present study overlaps the sites of the distribution of the human cases shown by Fernandes et al [11].
The plague disappeared suddenly in this focus since 1975 [11]. Purportedly it could be associated to the rarefaction of the susceptible species, mainly the population of N.
lasiurus, considered the amplifier host. In spite of the increasing in the R. rattus population, plague activity was no longer detected in rodents or humans [17]. The rats are relatively resistant to fatal plague infection and do not suffer from important die-offs that could lead to epizootization in the absence of susceptible species [10,15,[30][31]. On the other hand, the R. rattus might be a preserver host by maintaining the plague dormant until eventual flea re-infection might reactivate the epizootic cycle after restoration of the susceptible wild hosts populations [3,32].

Conclusion
The data presented in this work highlight that N. lasiurus might be the responsible for plague epidemics in this focal area of transmission in northeastern Brazil, since the reduction in the abundance of this species over time coincides with the period of disease quiescence. Besides, the increasing in the abundance of R. rattus is directly related to the urbanization process of small rural localities. In spite of their abundance they did not drive plague epidemics as could be expected especially considering their proximity to the humans. As the plague infection cycle can reactivate after several years of epidemiological silence a quiescence period must not be misled as extinguished [1,5].
Therefore, continuous surveillance is required and preventive measures focused in driving the rodents away from the houses and protection against flea bites should not be overlooked.