A newly discovered behavior (‘tail-belting’) among wild rodents in sub zero conditions

Rodents are among the most successful mammals because they have the ability to adapt to a broad range of environmental conditions. Here, we present the first record of a previously unknown thermal adaptation to cold stress that repeatedly occurred in two species of non-commensal rodents (Apodemus flavicollis and Apodemus agrarius). The classic rodent literature implies that rodents prevent heat loss via a broad range of behavioral adaptations including sheltering, sitting on their tails, curling into a ball, or huddling with conspecifics. Here, we have repeatedly observed an undescribed behavior which we refer to as “tail-belting”. This behavior was performed under cold stress, whereby animals lift and curl the tail medially, before resting it on the dorsal, medial rump while feeding or resting. We documented 115 instances of the tail-belting behavior; 38 in Apodemus agrarius, and 77 in Apodemus flavicollis. Thermal imaging data show the tails remained near ambient temperature even when temperatures were below 0 °C. Since the tail-belting occurred only when the temperature dropped below − 6.9 °C (for A. flavicollis) and − 9.5 °C (for A. agrarius), we surmise that frostbite prevention may be the primary reason for this adaptation. It is likely that tail-belting has not previously been documented because free-ranging mice are rarely-recorded in the wild under extreme cold conditions. Given that these animals are so closely-related to laboratory rodents, this knowledge could potentially be relevant to researchers in various disciplines. We conclude by setting several directions for future research in this area.

First report of Borrelia burgdorferi sensu stricto detection in a commune genospecies in Apodemus agrarius in Gwangju, South Korea

Lyme disease is a tick-borne infectious disease caused by the Borrelia burgdorferi sensu lato complex. However, the distribution of Borrelia genospecies and the tissue detection rate of Borrelia in wild rodents have rarely been investigated. Here, we studied 27 wild rodents (Apodemus agrarius) captured in October and November 2016 in Gwangju, South Korea, and performed nested polymerase chain reaction targeting pyrG and ospA to confirm Borrelia infection. Eight rodents (29.6%) tested positive for Borrelia infection. The heart showed the highest infection rate (7/27; 25.9%), followed by the spleen (4/27; 14.8%), kidney (2/27; 7.4%), and lungs (1/27; 3.7%). The B. afzelii infection rate was 25.9%, with the highest rate observed in the heart (7/27; 25.9%), followed by that in the kidney and spleen (both 2/27; 7.4%). B. garinii and B. burgdorferi sensu stricto were detected only in the spleen (1/27; 3.7%). This is the first report of B. burgdorferi sensu stricto infection in wild rodents in South Korea. The rodent hearts showed a high B. afzelii infection rate, whereas the rodent spleens showed high B. garinii and B. burgdorferi sensu stricto infection rates. Besides B. garinii and B. afzelii, B. burgdorferi sensu stricto may cause Lyme disease in South Korea.

Aggregated occurrence records of the invasive alien striped field mouse (Apodemus agrarius Pall.) in the former USSR

Open access to occurrence records of the most dangerous invasive species in a standardised format have important potential applications for ecological research and management, including the assessment of invasion risks, formulation of preventative and management plans in the context of global climate and land use changes in the short and long perspective. The striped field mouse (Apodemus agrarius Pallas, 1771) is a common species in the temperate latitudes of the Palaearctic. Due to land use and global climate changes, several waves of expansion of the range of this species have been observed or inferred. By intrusion into new regions, the striped field mouse has become an alien species there. Apodemus agrarius causes significant harm to agriculture and is one of the most important pests of grain crops. In tree nurseries, A. agrarius destroys seeds of valuable tree species and gnaws at the bark of saplings of broadleaf species and berry bushes. It is one of the most epidemiologically important rodents, involved in the circulation of the causative agents of haemorrhagic fever with renal syndrome (HFRS) and many other zoonotic infections. The foregoing allows us to classify the striped field mouse as a dangerous invasive alien species in the expanding part of the range. A lot of data accumulated for this species are of interest from both ecological and applied points of view. The accumulation and aggregation of data on the occurrence records of A. agrarius is relevant for the study of ecology, biogeography and construction of the spatial distribution and ecological niche models in the context of global climate change. We have created a dataset of 1603 occurrence records of this species, collected from 1936 to December 2020 by various zoologists, previously published or original. These records relate to a significant part of the striped field mouse’s range in Russia (1264 records) and neighbouring countries (339 records). The dataset shows the position of the northern and central parts of A. agrarius range, the disjunction of the range in Transbaikalia and isolated populations in the north of the range. The data were obtained in different formats from literature, indicating different degrees of accuracy of geographic coordinates and with several variations of the species' name. In the process of aggregating and fixing errors, we created a set of georeferenced occurrence records, adopted a controlled vocabulary, removed duplicates and standardised the format of records using unified data structure. We examined the dataset for inconsistencies with the taxonomic position of A. agrarius and removed the incorrect records. This paper presents the resulting dataset of A. agrarius occurrence records in the territory of Russia and neighbouring countries in a standardised format. This is a validated and comprehensive dataset of occurrence records of A. agrarius, including both our own observations and records from literature. This dataset is available for extension by other researchers using a standard format in accordance with Darwin Core standards. In different countries, there are a lot of occurrence records for the striped field mouse, but the overwhelming part of them is presented in separate literary sources, stored in the form of maps and in zoological collections. Prior to this project, such information was not available to a wide range of researchers and did not allow the use of these spatial data for further processing by modern methods of analysis, based on geographic information systems (GIS technologies). The created dataset combines species occurrence records of many Soviet zoologists who studied the distribution of the striped field mouse over a significant part of its recent range, in Russia and neighbouring countries (within the former USSR). The final set of records was created by combining the species occurrence records using a uniform data structure, checking geographic coordinates and removing duplicate and erroneous records. The dataset expands the available information on the spatial and temporal distribution of the dangerous invasive species in Russia and neighbouring countries of the former USSR (Estonia, Latvia, Lithuania, Belarus, Ukraine, Moldova, Georgia, Azerbaijan, Kazakhstan and Kyrgyzstan).

Monitoring Chigger Mites for Orientia tsutsugamushi in Field Small Mammals in Hwaseong-si, Gyeonggi-do, Korea, 2019-2020

Incidence of tsutsugamushi disease (scrub typhus) caused by Orientia tsutsugamushi, is steadily increasing. It is a mite-borne disease transmitted by chigger mites. In this study, the chigger mites were collected from field small mammals in Hwaseong-si (city), Gyeonggi-do (province), Korea, 2019 and 2020. The field small mammals captured were 56 Apodemus agrarius (94.9%) and 3 Crocidura lasiura (5.1%). A total of 7,531 chigger mites were collected from the captured small mammals. Using PCR test, 153 chigger mite pools were examined and 17 pools were reported positive for O. tsutsugamushi. The O. tsutsugamushi were identified to 5 strains; Jecheon strain was most prevalent, followed by Boryong strain. The other strains were OI011, Taguchi, and Shimokoshi. Collectively, these results provide essential regional information on mite-borne tsutsugamushi disease in the Hwaseong-si, and further contribute to bring awareness and rapid diagnosis for the tsutsugamushi disease.

A novel genotype of Hantaan orthohantavirus harbored by Apodemus agrarius chejuensis as a potential etiologic agent of hemorrhagic fever with renal syndrome in Republic of Korea

Background Orthohantaviruses, causing hemorrhagic fever with renal syndrome (HFRS) and hantavirus cardiopulmonary syndrome, pose a significant public health threat worldwide. Despite the significant mortality and morbidity, effective antiviral therapeutics or vaccines for orthohantavirus infections are currently unavailable. This study aimed to investigate the prevalence of HFRS-associated orthohantaviruses and identify the etiological agent of orthohantavirus outbreaks in southern Republic of Korea (ROK). Methodology/Principal findings We collected small mammals on Jeju Island during 2018–2020. We detected the Hantaan virus (HTNV)-specific antibodies and RNA using an indirect immunofluorescence assay test and reverse transcription-polymerase chain reaction on Apodemus agrarius chejuensis (A. chejuensis). The prevalence of anti-HTNV antibodies among rodents was 14.1%. A total of six seropositive mice harbored HTNV RNA. The amplicon-based next-generation sequencing provided nearly full-length tripartite genomic sequences of six HTNV harbored by A. chejuensis. Phylogenetic and tanglegram analyses were conducted for inferring evolutionary relationships between orthohantaviruses with their reservoir hosts. Phylogenetic analyses identified a novel distinct HTNV genotype. The detected HTNV genomic sequences were phylogenetically related to a viral sequence derived from HFRS patient in southern ROK. Tanglegram analysis demonstrated the segregation of HTNV genotypes corresponding to Apodemus spp. divergence. Conclusions/Significance Our results suggest that A. chejuensis-borne HTNV may be a potential etiological agent of HFRS in southern ROK. Ancestral HTNV may infect A. chejuensis prior to geological isolation between the Korean peninsula and Jeju Island, supporting the co-evolution of orthohantaviruses and rodents. This study arises awareness among physicians for HFRS outbreaks in southern ROK.

Multiplex PCR-Based Nanopore Sequencing and Epidemiological Surveillance of Hantaan orthohantavirus in Apodemus agrarius, Republic of Korea

Whole-genome sequencing of infectious agents enables the identification and characterization of emerging viruses. The MinION device is a portable sequencer that allows real-time sequencing in fields or hospitals. Hantaan orthohantavirus (Hantaan virus, HTNV), harbored by Apodemus agrarius, causes hemorrhagic fever with renal syndrome (HFRS) and poses a critical public health threat worldwide. In this study, we aimed to evaluate the feasibility of using nanopore sequencing for whole-genome sequencing of HTNV from samples having different viral copy numbers. Amplicon-based next-generation sequencing was performed in A. agrarius lung tissues collected from the Republic of Korea. Genomic sequences of HTNV were analyzed based on the viral RNA copy numbers. Amplicon-based nanopore sequencing provided nearly full-length genomic sequences of HTNV and showed sufficient read depth for phylogenetic analysis after 8 h of sequencing. The average identity of the HTNV genome sequences for the nanopore sequencer compared to those of generated from Illumina MiSeq revealed 99.8% (L and M segments) and 99.7% (S segment) identities, respectively. This study highlights the potential of the portable nanopore sequencer for rapid generation of accurate genomic sequences of HTNV for quicker decision making in point-of-care testing of HFRS patients during a hantavirus outbreak.