Monthly Occurrence of Vectors and Reservoir Rodents of Scrub Typhus in an Endemic Area of Jeollanam-do, Korea

Monthly surveys were conducted to investigate the occurrence of chigger mites and seroprevalence of scrub typhus among small mammals in Jeollanam-do, the southwestern part of Korea, from November 2006 through October 2007. Fifty-eight small mammals, including 57 Apodemus agrarius (98.3%) and 1 Crocidura lasiura (1.7%), were captured, and a total of 4,675 chigger mites representing 4 genera and 8 species were collected from them. The chigger infestation rate among small mammals was 69.0%. The most predominant species in A. agrarius was Leptotrombidium scutellare (54.0%), followed by Leptotrombidium pallidum (39.4%), Leptotrombidium orientale (4.4%), Leptotrombidium palpale (1.1%), Neotrombicula tamiyai (0.6%), Eushoengastia koreaensis (0.3%), Neotrombicula gardellai (0.3%), and Cheladonta ikaoensis (<0.1%). The chigger index of A. agrarius was the highest in October (740.0), followed by November (242.0), September (134.6), March (98.3), February (38.2), January (35.3), December (34.5), April (30.8), and May (1.7). The average antibody positive rate of scrub typhus in wild rodents was 50.0%. The seropositive rates were high in October (100.0%) and November (83.3%), whereas those in other months were relatively low (28.6-57.1%). The chigger index of L. scutellare rapidly increased in September to form an acuminate peak in October, followed by a gradual decline. These results suggest that the outbreak of scrub typhus in the southwestern part of Korean peninsula is mostly due to L. scutellare.     

Hantaan Virus Surveillance Targeting Small Mammals at Nightmare Range,a High Elevation Military Training Area,Gyeonggi Province,Republic of Korea

Rodent-borne disease surveillance was conducted at Nightmare Range (NM-R), near the demilitarized zone in northeast Gyeonggi Province, Republic of Korea, to identify hemorrhagic fever with renal syndrome (HFRS) risks for a mountainous high-elevation (500 m) military training site. Monthly surveys were conducted from January 2008-December 2009. A total of 1,720 small mammals were captured belonging to the Orders Rodentia [Families, Sciuridae (1 species) and Muridae (7 species)] and Soricomorpha [Family, Soricidae (1species)]. Apodemus agrarius, the primary reservoir for Hantaan virus (HTNV), accounted for 89.9% (1,546) of all small mammals captured, followed by Myodes regulus (4.0%), Crocidura lasiura (3.9%), Micromys minutus (1.4%), Mus musculus (0.3%), Microtus fortis (0.2%), Apodemus peninsulae (0.2%), Tamias sibiricus (0.1%), and Rattus norvegicus (<0.1%). Three species were antibody-positive (Ab+) for hantaviruses: A. agrarius (8.2%), M. minutus (4.2%), and C. lasiura (1.5%). HTNV specific RNA was detected in 93/127 Ab+ A. agrarius, while Imjin virus specific RNA was detected in 1/1 Ab+ C. lasiura. Overall, hantavirus Ab+ rates for A. agrarius increased with weight (age) and were significantly higher among males (10.9%) than females (5.1%) (P<0.0001). High A. agrarius gravid rates during the fall (August-September) were associated with peak numbers of HFRS cases in Korea that followed high gravid rates. From 79 RT-PCR positive A. agrarius, 12 HTNV RNA samples were sequenced and compared phylogenetically based on a 320 nt sequence from the G_C glycoprotein-encoding M segment. These results demonstrate that the HTNV isolates from NM-R are distinctly separated from HTNV isolated from the People’s Republic of China. These studies provide for improved disease risk assessments that identify military activities, rodent HTNV rates, and other factors associated with the transmission of hantaviruses during field training exercises.     

Host associations and seasonal abundance of immatureIxodes persulcatus (Acari: Ixodidae) in a lyme-disease-endemic area in china

Ticks of nine small mammal species were studied in an area of endemic Lyme disease in Hailin County, Heilongjiang Province, from 1 May to 10 October 1986. The bulk (93%) total small mammal captures wereApodemus speciouss (45%),Clethrionomys rufocanus (31%),A. agrarius (11%) andEutamias sibiricus; (5%): these host species accounted for 97% of the 162 ticks collected.Ixodes persulcatus Schulze were most abundant onE. sibiricus (0.64 larvae and 0.08 nymphs/squirrel), and less abundant onA. agrarius (1.16 larvae/mouse),A. speciosus (0.38 larvae/mouse) andC. rufocanus (0.37 larvae and nymphs/vole). The seasonal abundance pattern of larvalI. persulcatus on four small mammal species appears as a bimodal peak (June and September), but nymphalI. persulcatus has a monomodal peak during spring. The prevalence of immatureI. persulcatus on four small mammal species may play an important role in the epidemiology of Lyme disease in Hailin County.     

Geographical Distribution and Molecular Identification of Larval. Trombiculid Mites in Korea (2005∼2007)

A surveillance of trombiculid mites was conducted by collecting wild small mammals twice a year (spring and autumn seasons) at 24 localities in Korea from 2005 to 2007 to clarify the nationwide distribution of scrub typhus vectors. Among 783 trapped rodents, Apodemus agrarius accounted for 87.4% and the trapping rate at riverside was recorded the highest. A total of 67,325 mites representing 4 genera and 14 species were collected and their chigger index (C. I.) was 86.0. The predominant species were Leptotrombidium pallidum (52.6%), L. scutellare (27.1%), L. palpale (8.2%), L. orientale (5.6%), and Neotrombicula tamiyai (1.7%). However, the portion of L. scutellare in southern area including endemic provinces such as Jeollabuk‐Do (34.3%), Jeollanam‐Do (49.0%), and Gyeongsangnam‐Do (88%) were relatively higher than middle areas where L. pallidum was predominant in. Additionally, in autumn season, the density of L. scutellare was increased up to 42.0% while that of L. pallidum was decrease to 37.6%. Now we are performing a periodic surveillance again (2011～2013) and trying to develop a method to identify these trombiculid mites using molecular markers.     

Ecology of <Emphasis Type="Italic">Hepaticola hepatica</Emphasis> infection in rodents in southern West Siberia

The paper analyzes data of the long-term monitoring of Hepaticola hepatica (Bancroft, 1893) Hall, 1916 prevalence in rodents in subtaiga small-leaf forests of the Northern Baraba lowland (the Severnyi raion of Novosibirsk oblast). The study found that the prevalence was (10.4 ± 1.02)% in Arvicola terrestris L., 1758; 4.5% in Microtus agrestis L., 1761; 3.4% in M. oeconomus Pall.,1776; 1.4% in Clethrionomys glareolus Schreb., 1780; 1.0% in C. rutilus Pall., 1779; and 0.2% in Apodemus agrarius Pall., 1771. A. terrestris was shown to become dominant in rodent communities during its outbreaks and play the main role in completing the life cycle of the parasite. During low density of A. terrestris, the H. hepatica reservoir in the biocenosis is maintained by other rodent species.     

Intestinal Parasites among Wild Rodents in Northern Gangwon-do,Korea

To determine geographical patterns of natural parasite infections among wild rodents, a total of 46 wild rodents from 3 different localities in northern Gangwon-do (Province), Korea were examined for intestinal parasite infections. Along with nematodes such as hookworms and Syphacia spp., Plagiorchis muris (2 specimens) (Trematoda) were collected from striped field mice, Apodemus agrarius. In a Korean wood mouse, Apodemus peninsulae, the overall nematode infections were similar to A. agrarius, but an adult worm of Echinostoma hortense (Trematoda) was collected. In addition, 2 species of cestodes, i.e., Hymenolepis nana and Hymenolepis diminuta, were collected from A. agrarius. Through this survey, A. agrarius and A. peninsule were confirmed as the natural definite hosts for zoonotic intestinal helminths, i.e., P. muris, E. hortense, H. nana, and H. diminuta, in northern Gangwon-do, Korea. Considering increased leisure activities around these areas, seasonal and further comprehensive surveys on wild rodents seem to be needed to prevent zoonotic parasite infections.     

Movements of field mice Apodemus agrarius (Pallas) in a suburban mosaic of habitats

Summary Movements of field mice (Apodemus agrarius) were studied using snap traps and coloured bait. The presence of coloured bait was recorded in 35% of field mice captured. Of animals with coloured bait, 60% had moved further than 100 m. The longest distances traversed by field mice exceeded 1000 m. It is suggested that live-trapping on a grid of several hectares is not an adequate method of studying small-mammal movements.     

Geographical Distribution and Relative Abundance of Vectors of Scrub Typhus in the Republic of Korea

A survey to determine the geographical distribution and relative abundance of potential vectors of scrub typhus was conducted from October to November 2006 at 13 localities throughout the Republic of Korea. Apodemus agrarius accounted for 97.6% (80/82) of all rodents, while only 2 Myodes regulus (2/82) were collected. A total of 10,860 chiggers were collected from A. agrarius belonging to 4 genera and 8 species, while only Walchia fragilis (40) was collected from Myodes regulus. Leptotrombidium pallidum (8,137; 74.9%), a vector of scrub typhus, was the predominant species collected from A. agrarius followed by Leptotrombidium scutellare (2,057, 18.9%), Leptotrombidium palpale (279; 2.7%), Leptotrombidium orientale (232; 2.1%), and Leptotrombidium zetum (79; 0.7%), Neotrombicula tamiyai (58; 0.5%), Euschoengastica koreaensis (16; 0.1%), and Cheladonta ikaoensis (2; < 0.1%). L. pallidum was the predominant chigger collected at collection sites in Gangwon (100%), Gyeonggi (87.2%), Chungnam (100%), Chungbuk (100%), Jeonbuk (73.9%), Jeonnam (77.0%), and Gyeongbuk (66.1%) provinces, whereas L. scutellare was the predominant chigger collected in Gyeongnam province (77.9%) and Jeju Island (62.3%). Data suggest a correlation between chigger population abundance and human cases of scrub typhus in Korea.     

Echinostome Infections in the Striped-Field Mouse, Apodemus agrarius, and the Ussuri White-Toothed Shrew, Crocidura lasiura, Caught Near the Demilitarized Zone, Gyeonggi-do (Province), Republic of Korea

A total of 1,498 small mammals (rodents and insectivores), including Apodemus agrarius (n = 1,366), Crocidura lasiura (54), Mus musculus (32), Micronytus fortis (28), Eothenomys regulus (9), Micronys minutes (6), and Cricetulus triton (3), were live-trapped in Gyeonggi-do (Province) (Paju-si, Pocheon-gun, and Yeoncheon-gun) near the demilitarized zone (DMZ) from December 2004 to September 2005. A. agrarius was found to be infected with 3 species of echinostomes (Echinostoma hortense, Echinostoma cinetorchis, and Euparyphium murinum), while C. lasiura was infected with 1 species (Echinochasmus japonicas) of echinostome. Other mammals were free from echinostome infections. Total 16 E. hortense were detected in 7 (0.5%) mice, 9 E. cinetorchis from 5 (0.4%), and 3 E. murinum from 2 (0.1%) out of 1.366 A. agrarius examined. E. japonicus was found only in 1 (1.9%; total 3 specimens) C. lasiura. These results demonstrate that A. agrarius and C. lasiura, inhabiting near the DMZ of Gyeonggi-do serve as the natural definitive hosts for several species of echinostomes, although their infection rates are low. This is the first record of natural infections of A. agrarius with E. cinetorchis and C. lasiura with E. japonicus in the Republic of Korea.     

Ecological surveillance of small mammals at Dagmar North Training Area,Gyeonggi Province,Republic of Korea, 2001–2005

A seasonal rodent‐borne disease surveillance program was established at Dagmar North Training Area located near the demilitarized zone, Republic of Korea, from 2001 through 2005. Selected habitats surveyed included earthen banks separating rice paddies, fighting positions along a 5 m rock‐faced earthen berm, and extensive tall grasses with various degrees of herbaceous and scrub vegetation associated with dirt roads, rice paddies, ditches, ponds, or the Imjin River. Of the nine species of small mammals captured, the striped field mouse (Apodemus agrarius), the primary reservoir for Hantaan virus, was the most frequently collected, representing 92.5% of the 1,848 small mammals captured. Males were captured similarly to females during the spring and summer seasons but were captured less frequently during the fall and winter seasons. Gravid rates were highest in the fall (25.5–57.3%) with the lowest rates during the summer (0.0–2.2%). Capture rates were the lowest along earthen banks separating rice paddies (5.5%) and highest in unmanaged tall grasses and crawling vegetation (15.3–43.5%). An increased knowledge of ecological factors that impact the abundance and distribution of small mammals and the associated ectoparasites and pathogens they harbor is critical for developing accurate disease risk assessments and mitigation strategies for preventing vector‐ and rodent‐borne diseases among soldiers training in field environments.     

Occurrence of the Stripe Field Mouse lineage (Apodemus agrarius Pallas 1771; Rodentia; Mammalia) in the Late Pleistocene of southwestern France

The Stripe Field Mouse lineage (Apodemus agrarius) was present in the Late Pleistocene in southwestern France (locality of Bouziès-Q, Quercy), according to the age of ca. 17,417–17,044 BC of the collected sample (AMS ¹⁴C dating of collagen extracted from small mammal bones). This occurrence demonstrates that a much western expansion of the Stripe Field Mouse lineage than believed occurred at the end of the last cold phase of the Pleistocene, the few fossil populations up to now known being both younger and located inside the present-day distribution area of the lineage. The AMS ¹⁴C date supports the hypothesis of the late migration of this species into Europe. If tooth morphology indicates clear differences with respect to Apodemus sylvaticus or A. flavicollis, there are appreciable ones between the Bouziès-Q population and the present-day Apodemus agrarius of western Europe, likely indicating evolution at the sub-specific level despite the short time period involved.     

A Biogeographic View of Apodemus in Asia and Europe Inferred From Nuclear and Mitochondrial Gene Sequences

Sequences of the mitochondrial cyt b gene and nuclear IRBP, RAGI, I7, and vWF genes were used to assess the evolutionary history of major lineages of Apodemus, in particular to better understand dispersal between Asia and Europe. Our data show eight extant lineages of Late Tertiary origin: Apodemus agrarius, A. semotus, A. peninsulae, A. speciosus, A. argenteus, A. gurkha, A. mystacinus, and A. sylvaticus. Monophyly of two European lineages (A. mystacinus and A. sylvaticus) and four Asian lineages (A. agrarius, A. semotus, A. peninsulae, and A. speciosus) was confirmed with high bootstrap support. Together with literature data, the available molecular data depict three crucial evolutionary events: (1) initial wide dispersal and subsequent radiation around 6 million years ago, (2) region-specific radiations in Europe and southern China around 2 million years ago, and (3) westward dispersal of A. agrarius to Europe in the Late Quaternary.     

Morphological and genetic variability in small island populations of the striped field mouse <Emphasis Type="Italic">Apodemus agrarius</Emphasis> Pallas, 1771

Morphological (craniometrical characteristics and variations of cusp t3 on the second upper molar (M²)) and genetic (polymorphism of chromosomes and blood proteins) variability was analyzed in small island populations of the striped field mouse Apodemus agrarius Pallas, 1771 from the Peter the Great Bay (Sea of Japan). It was found that the absence of t3 on M² is not a specific trait for A. agrarius. It was demonstrated that the population of field mice on the Bolshoy Pelis Island significantly differs from the populations from other islands and from the mainland according to the craniometrical parameters, teeth phenes, and variants of blood transferrin. The possible age of establishment of the island populations of the striped field mouse is discussed.     

The opportunistic pathogen Encephalitozoon cuniculi in wild living Murinae and Arvicolinae in Central Europe

Encephalitozoon spp. is an obligate intracellular microsporidian parasite that infects a wide range of mammalian hosts, including humans. This study was conducted to determine the prevalence of Encephalitozoon spp. in wild living rodents from Poland, the Czech Republic and Slovakia. Faecal and spleen samples were collected from individuals of Apodemus agrarius, Apodemus flavicollis, Apodemus sylvaticus, and Myodes glareolus (n = 465) and used for DNA extraction. PCR, targeting the ITS region of the rRNA gene was performed. The overall prevalence of microsporidia was 15.1%. The occurrence of Encephalitozoon cuniculi in the abovementioned host species of rodents has been presented for the first time, with the highest infection rate recorded for A. flavicollis. Sequence analysis showed that the most frequent species was E. cuniculi genotype II (92.5%). E. cuniculi genotypes I (1.5%) and III (6.0%) were also identified.     

Occurrence rates of wild rodent hosts and chigger mites and the infection rate of Orientia tsutsugamushi in the central region of South Korea from 2015 to 2018

Outbreaks of vector‐borne diseases are dramatically increasing because of climate change, consequently increasing the importance of surveillance of endemic disease vectors. In this study, we surveyed chigger mites, vectors for Orientia tsutsugamushi—the bacteria that causes Tsutsugamushi disease—, and their rodent hosts in Gimcheon, central South Korea, in 2015–2018. A total of 225 rodents were collected, with trap rate and percentage of rodents infected by chigger mites of 9.8 and 72.4%, respectively. Six species of rodents from five genera were collected, the most common rodent being Apodemus agrarius (n = 153, infection rate = 90.8%). The highest number of rodents was collected in spring (trap rate = 10.3), but the rate of infected rodents was higher in fall (81.5%) than in spring (61.3%). Trap rate was highest for bank near waterway (17.9), but the chigger index (CI) was highest in hill (224.1). A total of 20,534 (CI 126.0) chigger mite individuals from 10 species and three genera were found on the collected rodents. The most common species was Leptotrombidium pallidum (n = 7,982, 83.6%, CI 49.0), followed by L. palpale and L. scutellare. Chigger mites were most frequent at banks near waterway (n = 11,093, CI 152.0) and hill (n = 2,017, CI 224.1). To detect O. tsutsugamushi in chigger mites, 450 pools of chigger mites (n = 10,991) were analyzed; 24 pools were positive—23 of A. agrarius, the most frequently collected species in South Korea, 1 of Micromys minutus—and the minimum positive rate (MPR) was 0.22. The detected strain types included Boryong (dominant in all years, seasons, and habitats), Jecheon, 07–489, and IIOC1202.     

Evidence for co-invasion events: different chigger species (Actinotrichida,Trombidioidea: trombiculidae) share a host

Cases of co-invasion of various chigger species parasitizing murids and cricetids in various habitats were analysed using morphological and molecular approaches. Here we provide evidence for 25 new cases of co-parasitism of chigger mites on rodent hosts (Myodes glareolus, Apodemus flavicollis, Apodemus agrarius) accounting for 8.6% of all host-parasite associations observed in this study. The results confirm higher incidence of co-parasitism in vertebrate-associated Parasitengona mites compared to arthropod-associated ones. Among factors influencing the occurrence of co-parasitism in Trombiculidae the body constitution and year-round availability of hosts associated with lower host specificity of larvae should be considered.     

Age,growth and hatch dates of ingressing larvae and surviving juveniles of Atlantic menhaden Brevoortia tyrannus

Ages, growth and hatch dates of ingressing Brevoortia tyrannus larvae were determined in a 3 year sampling survey at the mouth of the Chesapeake Bay, U.S.A. To determine if otolith‐aged cohorts had variable relative survival, hatch dates of summer‐caught young‐of‐the‐year (YOY) juveniles collected throughout the Chesapeake Bay were compared with hatch dates of ingressing larvae. Modal total length of ingressing larvae was similar among years: 28 mm in 2005–2006 and 2007–2008, and 30 mm in 2006–2007. Ages of ingressing larvae ranged from 9 to 96 days post hatch (dph); mean ages were similar among years, but significantly older in 2006–2007 (50 dph) than in 2005–2006 (44 dph) and 2007–2008 (46 dph). Larval growth rates differed among years. Earliest growth, when larvae were offshore (0–20 dph), was faster in 2006–2007 (0·62 mm day^?1), than in 2005–2006 and 2007–2008 (0·55 mm day^?1 in these years). Subsequently, from 30 to 80 dph, growth was slowest in 2006–2007. Hatch dates of ingressing larvae occurred from September to March and 90% (2007–2008) to 98% (2006–2007) had hatched prior to 31 December. In contrast, most surviving YOY juvenile B. tyrannus had hatched in January to February, suggesting selective mortality of early‐hatched individuals, apparently during the overwinter, larval to juvenile transition period.     

The influence of spring floods on small mammal communities in the Nemunas River Delta, Lithuania

The influence of the annual spring floods on small mammal communities was studied in the Nemunas River Delta, SW Lithuania. The aim of the investigation was to compare the diversity of small mammals inhabiting spring-flooded meadows, meadows not subjected to flooding and spring-flooded forest in years characterized by differing heights and durations of spring flood. In the years of the high flood, the number of species and diversity index were higher, while index of dominance was less than in the years of low flood. Significantly, the highest proportions of Apodemus agrarius were recorded in spring-flooded meadows in years of high flood (41.7%), while Microtus oeconomus occurred in the highest proportions in spring-flooded meadows in years of low flood (66.8%) and in meadows not subjected to flooding (47.1%). In non-flooded areas, M. Oeconomus is not expelled by the floods and outcompetes other species. After high levels of flooding, during the process of re-population, the voles may be outcompeted by A. agrarius. In the absence of dominant species, greater opportunities existed for the establishment of more species (13 species in flooded meadows). Micromys minutus accounted for up to 19.5–30.1% in the years of high flood. We concluded that the annual spring floods in the Nemunas Delta had no long-term negative effects, the number of small mammal species and their abundance had been restored in just a few months. The worst consequences of the high flood were recorded in forest habitat. Spring floods, and especially the higher floods, are natural environmental agents, maintaining the high diversity of small mammals in meadows and reed-beds.     

Detection and Molecular Characterization of Cryptosporidium spp. from Wild Rodents and Insectivores in South Korea

In order to examine the prevalence of Cryptosporidium infection in wild rodents and insectivores of South Korea and to assess their potential role as a source of human cryptosporidiosis, a total of 199 wild rodents and insectivore specimens were collected from 10 regions of South Korea and screened for Cryptosporidium infection over a period of 2 years (2012-2013). A nested-PCR amplification of Cryptosporidium oocyst wall protein (COWP) gene fragment revealed an overall prevalence of 34.2% (68/199). The sequence analysis of 18S rRNA gene locus of Cryptosporidium was performed from the fecal and cecum samples that tested positive by COWP amplification PCR. As a result, we identified 4 species/genotypes; chipmunk genotype I, cervine genotype I, C. muris, and a new genotype which is closely related to the bear genotype. The new genotype isolated from 12 Apodemus agrarius and 2 Apodemus chejuensis was not previously identified as known species or genotype, and therefore, it is supposed to be a novel genotype. In addition, the host spectrum of Cryptosporidium was extended to A. agrarius and Crosidura lasiura, which had not been reported before. In this study, we found that the Korean wild rodents and insectivores were infected with various Cryptosporidium spp. with large intra-genotypic variationa, indicating that they may function as potential reservoirs transmitting zoonotic Cryptosporidium to livestock and humans.     

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.