FORESTRY IDEAS, 2020, vol. 26, No 1 (59): 262–269

FOREST ( NITEDULA, RODENTIA, GLIRIDAE) – A HIGHLY CONTAGIOUS IN RELATION TO ZOONOTIC DISEASES

Alexey Andreychev1* and Ekaterina Boyarova2 1Department of Zoology, National Research Mordovia State University, Saransk 430005, . *E-mail: [email protected] 2Center for Hygiene and Epidemiology in the Republic of Mordovia, Saransk 430030, 1a Dal’naya Str., Russia.

Received: 22 March 2020 Accepted: 23 May 2020

Abstract Republic of Mordovia in Russia is a historical focus for hemorrhagic fever with renal syndrome and tularemia. This study aimed at assessing the current status of these foci by studying their rodent reservoirs. Among the small in Mordovia, the red bank vole, the common vole and the house mouse play an important role as carriers of zoonotic diseases. However, it is neces- sary to take into account the role of such а small species as (Dryomys nitedula), which has a high percentage of infection. Of all examined dormice, 66.7 % were found to have antigens of hemorrhagic fever with renal syndrome viral pathogen, and 33.3 % - to have antigens of tularemia pathogen. Only one specimen (16.7 %) was found to have no antigens of zoonotic diseases. Our study concluded that the forest dormouse in the Republic of Mordovia was incrim- inated as a pathogen reservoir causing infectious diseases in human. Key words: hemorrhagic fever, Mordovia, rodents, tularemia.

Introduction gion of Middle (Ulyanovsk region) (Nafeev et al. 2009). Small are Hemorrhagic fever with renal syndrome the most incriminated reservoirs for viral (HFRS) is the most common natural ro- pathogen agents causing human HFRS dent borne disease of viral etiology in the in the natural environments (Tsvirko and Republic of Mordovia. The intensive rate Kozlov 2012). of morbidity per 100,000 population of the In addition to HFRS, small rodents in Mordovia Republic during the period from this region are reservoirs in the circulation 2001 to 2006, varied from 10.5 to 18.0, and the transmission of widespread hu- and the average long-term rate for this man infectious diseases like tularemia and period was 14.4±1.1, which exceeded the leptospirosis. In the natural foci of HFRS, same value in the Russian Federation by epizootics occur periodically. Thus, small 2.8 times. Broad-leaved forests and agri- rodents perform one of the main roles in cultural lands are predominant in all areas the spread of the zoonotic diseases. of HFRS infection (Churbanova 2008). A The red bank vole (Myodes glareolus) similar situation is shown for another re- has been considered the main reservoir Forest Dormouse (Dryomys Nitedula, Rodentia, Gliridae) – a Highly Contagious ... 263 among rodents in the zoonotic circulation The report on the presence of tu- in Mordovia and throughout Volga region laremia in forest dormouse in Mordovia (Trankvilevsky et al. 2015, Andreychev is of interest, since previously in the do- et al. 2019). The yellow-necked mouse mestic and international literature it was ( flavicollis), the striped field not detected in this species, for example mouse (Apodemus agrarius), and the red in (Pavlov et al. 1978). The re- bank vole (M. glareolus) play an important sults of standard tube agglutination test in role in zoonotic circulation of HFRS in the Western showed seropositive cases Balkan Peninsula (Stanko et al. 2004, Ro- among 4.8 % of the rodents, including D. gozi et al. 2013, Papa et al. 2016). nitedula (Mostafavi et al. 2017). Positive Ergeshbayev (2018), in the Kyrgyz Re- results on tularemia in the Republic of public mentioned the high degree of ec- Moldova were recorded in the following toparasite infestation of forest dormouse species: M. glareolus, Apodemus uralen- Dryomys nitedula (Pallas, 1778) (18 spe- sis, A. sylvaticus, A. flavicollis, M. muscu- cies), as well as its contact with numerous lus, M. spicilegus, and Crocidura suaveo- representatives of the rodent order. The lens (Chicu et al. 2010). researcher noted that it carried only one The forest dormice has not been re- species-specific parasite and 17 species ported infected with tularemia and HFRS, peculiar to marmots, voles, mice, gray for example in (Laakkonen et al. hamster, Turkestan rat and other rodents. 2006), and (Demchyshyna et al. Among them, five flea’s speciesCallopsyl - 2020). la caspia, Amphipsylla phaiomydis, A. an- The dynamics of identifying the causa- ceps, A. asiatica and Leptopsylla nemoro- tive agent of tularemia in Mordovia should sa were identified. Cultures of the plague be noted in 2015, 2017 and 2018, which pathogen from these flea’s species were are characterized by peak values (Andrey- isolated for this territory. This causes an chev, Boyarova and Kuznetsov 2016). important epizootological significance of Mostly, the tularemia microbe antigen was this rodent species. The importance of most often detected in areas along the forest dormice as carrier of parasites was middle rivers (Sura, Alatyr), rather than in also reported in Russia. In Central Russia, areas that do not have such water arter- ectoparasites were found in 90–95 % of ies. In pellets of prey birds, the causative forest dormice, and endoparasites were agent of tularemia was detected in the found in 50–70 % of small (Ros- districts more often than in the biomate- solimo et al. 2001). rial from rodents. This circumstance can Some small mammals are breeding be explained from the position that the in the grounds among other species. In remains of the hunted preys can contain particular, such reports about the yel- several prey species at once. This is ev- low-necked mouse are known. Dobra- idenced by the results of studies of oste- va-Belgrade virus strain (DOBV), causing ological material (Andreychev et al. 2014, in humans HFRS has been reported to be Andreychev, Lapshin and Kuznetsov originated by A. flavicollis, A. sylvaticus 2016, Andreychev and Lapshin 2017). and M. musculus (Weidmann et al. 2005). Therefore, the probability of detecting A previous study in Greece showed that tularemia microbe antigen here is higher approximately 10 % of A. flavicollis carried (Andreychev et al. 2019). DOBV (Papa et al. 2000). The purpose of this article is to study 264 A. Andreychev and E. Boyarova the role of the forest dormouse as carri- the region. This is due to the peculiarities er or reservoir of rodent-borne diseases. of its distribution. Forest dormouse occurs In addition to the red bank vole, there is from Western across Asia Minor, a high probability in the circulation of zo- Caucasus, reaching to Central Russia onotic diseases in the forest dormouse. and . In this extensive area, the species is rare in many parts of its na- tive range, especially in Western Europe Material and Methods and Russia (Batsaikhan et al. 2008, Mark- ov et al. 2017). Small mammals capturing and testing for All carcasses were used as a different possible pathogen agents, are result of basic research on population ge- the material for this study in the territory of netics (Grigoryeva et al. 2015) and hom- the Republic of Mordovia (53º38’–55º11’N ing (Andreychev and Kiyaykina 2020). and 42º11’–46º45’ E) (Fig. 1) for epizo- During the research period of 2009-2019, otological research purposes. Coniferous a total of 1995 individuals of the following forest, broad-leaved forests, shrub steppe rodent species were trapped: red bank and meadow steppe compose the ro- vole (M. glareolus) – 30.9 %, common dents’ habitat structure in the territory of vole (M. arvalis) – 23.8 %, Ural field mouse Mordovia. The main forests are composed (A. uralensis) – 18.7 %, yellow-necked by pine Pinus sylvestris (L.), spruce Picea mouse (A. flavicollis) – 11.5 %, striped abies (L.) Karst., European larch Larix de- field mouse A.( agrarius) – 10.4 %, house cidua (Mill.), oak Quercus robur (L.), com- mouse (M. musculus) – 4.4 %, and for- mon ash Fraxinus excelsior (L.), Norway est dormouse (D. nitedula) – 0.3 %. The maple Acer platanoides (L.), European captured rodents were transported to the white elm Ulmus laevis (Pall.), silver birch laboratory of the Center for Hygiene and Betula pendula (Roth.), white birch Betu- Epidemiology in the Republic of Mordovia. la pubescens (Ehrh.), common alder Al- Enzyme-linked immune sorbent assay nus glutinosa (L.), small-leaved lime Tilia (ELISA), using the ‘Huntagnost’ test sys- cordata (Mill.), black poplar Populus nigra tem for the presence of the pathogen, was (L.). the main method used to detect the HFRS The research was conducted in June antibodies in homogenized rodent’s lungs. and July 2018 and 2019. The live traps Studies on tularemia were performed us- were set in the typical habitats of the for- ing serological and bacteriological meth- est dormouse for several days and then ods. For leptospirosis and yersiniosis, transferred to the next site. We used four studies were conducted by serological trap lines. The number of traps in each method (Methodical Instructions 2012). line was 25. Snap traps were set for no more than 1 or 2 days. Salami and apple were used as baits. Traps were set main- Results and Discussion ly in mixed and broad-leaved forests. The latter biotope is a favourite habitat (Grig- Of the six examined dormice, four individ- oryeva et al. 2015, Andreychev and Ki- uals (66.7 %) were found to have antigens yaykina 2020). The material of the forest of the pathogen causing HFRS, and two dormouse (dead animals) was obtained in individuals (33.3 %) were found to have small quantities, since this rare species in antigens of tularemia pathogen. Only one Forest Dormouse (Dryomys Nitedula, Rodentia, Gliridae) – a Highly Contagious ... 265

Fig. 1. Map of the Republic of Mordovia – oval – where animals were trapped. individual of the forest dormouse was Comparing the results obtained in Mor- found to have no antigens of zoonotic dis- dovia by the spectrum of mouse rodent eases. species infected with tularemia (Fig. 2) 266 A. Andreychev and E. Boyarova

Fig. 2. Rodents’ population structure involved as the reservoirs of tularemia and its circulation in 2019. with the data obtained for the entire Vol- the common vole was found positive as ga Federal district (Trankvilevsky et al. well (21.4 %). Our study showed that the 2015), a similar picture should be noted house mouse (41 %) was of primary im- in the primary role of the carrier of this dis- portance, while the red bank vole (23 %) ease, the red bank vole (M. glareolus) (in and the common vole (23 %) were highly Mordovia – 42 %, in Volga Federal district infected (Fig. 3). Perhaps the reason for – 56.2 %) and Ural field mouse (A. uralen- this is that a large number of animals were sis) (in Mordovia – 25 %, in Volga Federal captured near settlements. Our study district – 21.9 %). showed as well, that the field mouse was M. musculus, the house mouse, was not infected with the pathogen causing the third rodent species found positive for HFRS among common small mammals in the presence of tularemia bacteria (15 %); the region, although this species may be meanwhile, the field mouse, A. agrarius, active in the epizootic process in Russia was found positive for the same bacteria (Trankvilevsky et al. 2011). (15.6 %) in Volga Federal district area. The highest rate of infection with the Analyzing the results of infection of leptospirosis pathogen was observed in rodents with hantavirus for 1997–2001 the common vole. The field mouse was by Chumakov (2003) and 2007 by Chur- the second most infected (34 %). To a banova (2008), as well as the results ob- lesser extent, infection was detected in tained by our study a change in the role the house mouse. In other captured ro- of the main carrier of this disease could dents’ species, the pathogen was not de- be stated. Thus, in 1997-2001, a high tected. proportion of infected individuals were ob- Thus, among small mammals in Mor- served among the yellow-necked mouse, dovia, the red bank vole, the common vole field mouse, red bank vole and the com- and the house mouse have an important mon vole captured, meanwhile in 2007, role as carriers of zoonotic diseases. This Forest Dormouse (Dryomys Nitedula, Rodentia, Gliridae) – a Highly Contagious ... 267

Fig. 3. Rodents’ population structure involved as reservoirs of HFRS and its circulation in 2019. circumstance is due to the high number circulation of pathogens of natural focal of these species representing the rodent diseases in the Republic of Mordovia. Bul- fauna of each region. However, it is nec- letin Samara scientific center of Russian essary to take into account the role of Academy Sciences 5(2): 186–191 (in Rus- sian with English summary). such species like the forest dormouse, Andreychev A., Boyarova E., Lapshin A., which has a high percentage of the tu- Kuznetsov V. 2019. Detection of foci of tula- laremia and hantavirus pathogen. High remia using enzyme immunoassay for the diversity of small mammals’ species in predatory bird pellets. Periodico Tche Qui- Mordovia with positive infection results is mica 16(31): 632–641. ensuring the persistence and circulation Andreychev A.V., Kiyaykina O.S. 2020. Hom- of the tularemia agents in the natural foci, ing of the forest Dormouse (Dryomys which maintain a high risk of human dis- nitedula, Rodentia, Gliridae). Zoologich- ease cases. eskii Zhurnal 99(6): 698–705 (in Russian with English summary). DOI: 10.31857/ S0044513420060033 Andreychev A.V., Lapshin A.S. 2017. Quantita- Acknowledgement tive and Qualitative Composition of Diet of the Ural , Strix uralensi (Strigidae, Stri- We are grateful to E. A. Ilykaeva, A. V. Sa- giformes), in the Central Part of European laeva, E. O. Levtcova, S. A. Yutukova, M. Russia (the Example of the Republic of N. Suharnikova for support in carrying out Mordovia). Vestnik zoologii 51(5):421–428. of field studies. DOI: 10.1515/vzoo-2017-0050 Andreychev A.V., LapshIn A.S., Kuznetsov V.A. 2014. Food spectrum of the Eagle owl (Bubo bubo) in the Republic of Mordovia. References Zoologicheskii Zhurnal 93(2): 248–258 (in Russian with English summary). DOI: Andreychev A.V., Boyarova E.I., Kuznetsov V.A. 10.7868/S0044513414020032 2016. The role of mouse-like rodents in the Andreychev A.V., LapshIn A.S., Kuznetsov V.A. 268 A. Andreychev and E. Boyarova

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