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Helminths in Myomorph Rodents (Rodentia, Myomorpha) from the National Park “Smolny” and Its Surroundings (European Russia)

: The National Park “Smolny” is a large forest area, located in the center of European Russia. The helminth fauna of myomorph rodents was studied for the ﬁrst time within the National Park in 2018–2020. Rodents were examined by the method of complete helminthological dissection. A total of 30 species of parasites were recorded in 11 rodent species: 6 trematodes, 11 cestodes and 13 nematodes. The trematode Plagiorchis maculosus (Rudolphi, 1802) was found in Clethrionomys glareolus (Schreber, 1780) from the Russian fauna for the ﬁrst time. Clethrionomys glareolus and Microtus arvalis (Pallas, 1779) are new hosts for P. maculosus and metacestode Versteria mustelae (Gmelin, 1790), respectively. The most widespread and eurybiont rodent species have the most diverse and rich helminth fauna, such as C/ glareolus (14 species), Apodemus agrarius (Pallas, 1771) (12) and Sylvaemus uralensis (Pallas, 1811) (10). The helminth fauna is less diverse in Sylvaemus ﬂavicollis (Melchior, 1834), M. arvalis (7 species each), Microtus agrestis (Linnaeus, 1761) (5), Microtus subterraneus (de Selys-Longchamps, 1836) (3), Sicista betulina (Pallas, 1779) (2) and Arvicola amphibius (Linnaeus, 1758) (1). Comparative analysis the helminth fauna of small rodents from the National Park “Smolny” with micromammals from other regions of European Russia revealed that the high similarity with other areas reaches the helminth fauna of M. subterraneus , S. ﬂavicollis , S. uralensis , S. betulina , A. amphibius and M. agrestis .


Introduction
Parasitic organisms are an integral part of natural biocenoses. They play an important role in the biosphere and act as one of the factors of biodiversity formation [1][2][3][4][5][6][7]. Helminths live in all vertebrates, including small rodents. Their species composition, age and seasonal infection rates serve to understand the changes that may occur in ecosystems [8][9][10].
The study of helminths of wild mammals in protected areas is of particular interest, because, the species diversity of both animal hosts and their parasites is most fully preserved here as a result of the special regime. In the context of global anthropogenic transformations of natural ecosystems, only protected areas are the most favorable places for animals to live in [11][12][13][14][15], the purpose of which is to preserve the biodiversity of forest ecosystems [16][17][18][19][20][21].
There are more than 300 protected areas of federal significance located in the territory of European Russia. Most of them are territories with large forest areas with rich biodiversity. Despite the long history of flora and fauna research in the Russian protected areas, the inventory of biodiversity in their territories is still one of the most actual purposes [22][23][24][25][26].
In forest ecosystems, the most representative and widespread mammal group is small wild rodents. Despite the wide distribution and high number of myomorph rodents, a long Within the National Park, trapping sessions of small rodents took place in May-August 2018-2020. Myomorph rodents were captured using spring metal snap traps (120 × 55 mm). Trap lines of 20 snap traps, separated by 10-m intervals, were located along the banks of small rivers and streams, forest edges, in fields and meadows. Snap traps baited with rye bread fried in sunflower seed oil. Trapping was conducted for five consecutive days in each locality.
The material for parasitological research was obtained as a result of work on accounting for the number of small rodents. They are regularly counted according to the research topics of the Federal State Budgetary Institution "Reserved Mordovia" ("Zapovednaya Mordovia") in 2018-2020. The research theme, trapping and handling procedures were approved by the Ministry of Natural Resources and Ecology of Russia.
Our research was conducted in compliance with the ethical standards of humane treatment of animals in accordance with the recommended standards described by the Directive of the European Parliament and of the Council of the European Union of 22 September 2010 "On the protection of animals used for scientific purposes" (EU Directive 2010/63/EU) [43]. Trapped rodents were killed by percussive blow to the head. Then the species, sex and age of the animals were identified.

Parasite Examination
Rodents were examined by the method of complete helminthological dissection [44,45]. Helminths were collected and fixed in 70% ethanol. Trematodes and cestodes were stained with aceto-carmine, cleared in clove oil, and mounted in Canada balsam. Nematodes were translutened in lactic acid and mounted in Glycerin-Jelly [44,45]. The helminth identification was carried out in the Laboratory of Population Ecology of the Institute of Ecology of the Volga Basin of the Russian Academy of Sciences (Togliatti).

Data Analysis
To characterize the infestation of rodents with parasites, the following indices were used: the prevalence of invasion (P, %), the intensity range (IR, specimen.) and the mean abundance (MA). For parasites, the following features are given: Latin name, the general geographical distribution, the detection sites, host species in the studied territory.
The Shannon index (H') was calculated to determine the species diversity of helminths of myomorph rodents. The validity of the differences between the Shannon index value was evaluated using the Student's t-test [58]. The differences were considered significant at p < 0.05. The dominance of individual species in the helminth fauna was determined using the Palia-Kovnatsky index of dominance (D) [59]: where P is the prevalence of invasion, %; n i is the number of specimens of the i species. The parasite dominance groups were considered as following: 10-100-dominants, 1-10subdominants, 0.001-1.000-adominants.

Helminth Fauna of Small Rodents
In total, 30 species of parasitic worms were identified in the studied species of small rodents from the National Park "Smolny": 11 cestodes, 6 trematodes and 13 nematodes ( Table 2). We did not find any parasites in single specimens of M. musculus and M. minutus. In the vicinity of Semenovka village ( Figure 1, site 4), only one individual of A. amphibious was caught, which turned out to have no helminths.
Most of the parasites registered in micromammals are represented by adult forms-26 species. At the larval stage, only four cestode species are parasitized. For the metacestodes Taenia martis Zeder, 1803, Hydatigera taeniaeformis (Batsch, 1786) s. l. and Versteria mustelae (Gmelin, 1790), small rodents serve as intermediate hosts. For the cestode larva of Dilepis undula (Schrank, 1788) rodents are paratenic hosts.  In C. glareolus, 14 species of parasites belonging to the following systematic groups were found: 2 trematodes, 7 cestodes and 5 nematodes ( Table 2). Two of those species are host-specific parasites of C. glareolus (Heligmosomoides glareoli (Baylis, 1928) and Syphacia petrusewiczi Bernard, 1966). Four helminth species belong to specific rodent parasites of the subfamily Arvicolinae (Anoplocephaloides dentata Arvicola amphibius had one helminth species-the nematode H. laevis (Table 2). It is a host-generalist parasite of voles. Out of seven studied individuals of A. amphibius, only one was infected.
The helminth fauna in S. uralensis includes 10 species: 3 trematodes, 3 cestodes and 5 nematodes ( Table 2) (Table 3).  Nematodes that dominate in the helminth fauna of myomorph rodents from the National Park "Smolny" belong to five families ( Table 2). The most represented families are Oxyuridae (5 species) and Heligmosomidae (4). The Trichuridae family includes two species. The smallest number of species is in the families Spirocercidae and Heterakidae (one each).
Cestodes are also represented by five families, and parasites of the families Catenotaeniidae (4 species) and Taeniidae (3) dominate. The family Anoplocephalidae includes two cestode species. The families Dilepididae and Hymenolepididae include 1 species each ( Table 2).
Trematodes (6 species) are less represented in the helminth fauna of myomorph rodents from the National Park "Smolny" and belong to four families ( Table 2). The families Plagiorchiidae and Dicrocoeliidae include two trematode species; the families Brachylaimidae and Echinostomatidae include one species each.
The nematode S. stroma is widely distributed in myomorph rodents and registered in 13 of the 15 localities (Table 2 and Figure 1). The nematodes H. polygyrus, H. mixtum and S. obvelata were recorded in 12 studied sites. The cestode P. omphalodes was found in micromammals in nine localities. The cestodes C. henttoneni, S. lobata and the nematode S. petrusewiczii were found each in 7 studied places. The nematode S. agraria was registered in 6 stations. The trematode P. elegans, the nematode H. spumosa and the metacestode H. taeniaeformis s. l. were noted in five localities. The metacestode V. mustelae was found in rodents in four localities. The cestodes H. apodemi and the nematodes H. glareoli, H. laevis, T. arvicolae, T. muris were each registered in three studied places. The remaining 13 parasite species were observed only in one or two research sites (Table 2 and Figure 1).
There were no common helminths in the all studied rodent species. Five rodent hosts had one common metacestode H. taeniaeformis s. l. (Table 2). Four hosts had the cestode A. dentata and nematodes H. laevis and M. muris. Three rodent hosts are noted for six helminth species (P. omphalodes, H. apodemi, V. mustelae, larva, P. elegans, T. arvicolae, H. polygyrus). The nematodes S. nigeriana, S. obvelata, S. stroma and the cestode Catenotaenia sp. 1, were recorded in two host species. The remaining 16 parasite species each had one host ( Table 2).
Two out of 30 species of helminths (the metacestode H. taeniaeformis s. l. and the nematode S. obvelata) found in the myomorph rodents from the National Park "Smolny" have medical and veterinary significance as potential pathogens of dangerous helminthiasis.

Comparative Analysis of the Helminth Fauna in Rodents
We have carried out a comparative analysis of the helminth fauna in myomorph rodents from different regions of European Russia. Figure 2 shows the dendrogram of the similarity of the helminth fauna in myomorph rodents. The cophenetic correlation coefficient is 0.811, which confirms the validity of the cluster. During clustering, all the considered species of micromammals were divided into 10 groups that include species with the most similar helminth fauna.
The first group is formed by the helminth fauna of M. minutus from the Central Chernozem Nature Biosphere Reserve (Kursk region) and Samarskaya Luka (Samara region). It differs as much as possible from the helminth fauna in other studied micromammal species on the territory of European Russia (Figure 2

Discussion
The analysis of the helminth fauna in myomorph rodents from the National Park "Smolny" showed that the species composition of parasites is qualitatively rich in C. glareolus (14 species), A. agrarius (12) and S. uralensis (10). It is less diverse in S. flavicollis, M. arvalis (7 species each) and M. agrestis (5). The helminth fauna in M. subterraneus (3), S. betulina (2) and A. amphibius (1) is very poor. Parasites were not detected in the studied single specimens of M. musculus and M. minutus, which is due to the small number of studied rodents.
The diversity of the helminth fauna in individual species of myomorph rodents is determined by the size of the ecological niche that the animal occupies in the biocenosis. The most diverse and rich helminth fauna is possessed by the most abundant and eurybiont rodent species such as C. glareolus, A. agrarius, S. uralensis and S. flavicollis.
For the majority of helminths (26 species), rodents serve as obligate hosts. They are facultative hosts for trematodes P. elegans, P. maculosus, E. miyagawai and cestode D. undula.
The finding of cestode larvae in myomorph rodents indicates the important role of these micromammals in the circulation of animal parasites at higher trophic levels. Adult forms of H. taeniaeformis s. l., T. martis and V. mustelae parasitize predatory mammals of the families Mustelidae and Canidae. On the other hand, the records of metacestodes in small rodents indicates a wide distribution of the final hosts of these parasites in biocenoses of the National Park. The invasion of rodents by these cestode species occurs by oral penetration of helminth eggs into the host along with food [45,47]. According to recent molecular genetic studies, the cestode of H. taeniaformis s. l. is a species complex and contains at least two or three cryptic species forming three clearly differentiated clades A (H. taeniaformis s. str.), B (Hydatigera kamiyai Iwaki 2016) and C (Hydatigera sp.) [61,62].
Invasion of C. glareolus with the cestode D. undula probably occurred while eating the intermediate hosts of the cestode which are oligochaete worms [45]. In our opinion, the findings of immature cestodes D. undula in the small intestine of rodents are cases of transit parasitism.
Invasion of rodents with the cestodes A. dentata, P. omphalodes, S. lobata and Catenotaenia spp. is carried out by accidental ingestion along with plant food (or by digging burrows) of intermediate hosts of these parasites which are oribatid and tyroglyphid mites and Onchiurus springtails [46,48]. Molecular genetic studies have shown that the cestode A. dentata is a species complex and includes at least five species common in the Holarctic [63]. The cestode P. omphalodes, which is widely distributed among the voles of Eurasia, also includes several species [64,65]. Recent studies have shown that Catenotaenia cestodes possess a high degree of specificity. Catenotaenia cricetorum Kirshenblat, 1949, previously observed in a large number of rodent species from the European fauna [51], is a combined species. New species were described for mice (Catenotaenia . Catenotaenia henttoneni is host-specific parasite for Clethrionomys voles [51]. The development of cestodes of the genus Hymenolepis Weinland, 1858 proceeds with the involvement of millipedes and insects of the orders Coleoptera, Lepidoptera and Orthoptera [46,48]. Rodents become infected with H. apodemi by eating insects and millipedes. Recent studies have revealed that the genus Hymenolepis includes several complex species, which may include a number of yet undescribed hymenolepidids. Thus, the rat parasite Hymenolepis diminuta (Rudolphi, 1819), described from R. norvegicus, was indicated for many rodent species of different families, including Apodemus and Sylvaemus mice [46]. Recently it has been established that H. diminuta is a complex of cryptic species [66]. Hymenolepis hibernia Montgomery, Montgomery et Dunn, 1987 and H. apodemi parasitise mice of Eurasia [49,67].
Myomorph rodents become infected with trematodes while eating invertebrates, which serve as the second intermediate hosts of these parasites. When visiting near-water stations, rodents eat aquatic and near-water insects which are the second intermediate hosts of Plagiorchis trematodes. As the result, they become infected with P. elegans and P. maculosus [46,48]. Also, near waterbodies, micromammals become infected with E. miyagawai, while eating freshwater gastropods that are the second intermediate hosts of the parasite. It has been experimentally established that they may be the limneids Lymnaea stagnalis (Linnaeus, 1758) and Lymnaea truncatula (Muller, 1774) [68,69]. Or rodents eat tadpoles of Rana frogs which are also indicated as the second intermediate hosts of this trematode [46,48]. Freshwater gastropods Planorbis planorbis (Linnaeus, 1758), Anisus vortex (Linnaeus, 1758), Radix peregra (Muller, 1774), Galba corvus (Gmelin, 1791) and Gyraulus chinensis (Dunker, 1848) serve as the first intermediate hosts of E. miyagawai [70], they probably could also act as second intermediate hosts.
The life cycle of B. rodentini has not been studied, but, probably, like in other dicroceliid species, the second intermediate hosts of the trematodes are insects [46]. While eating them, rodents become infected with this parasite.
The absence of trematodes in the helminth fauna of M. arvalis, M. agrestis and M. subterraneus indicate the avoidance of near-water habitats by these rodents and a small quantity of near-water plants in the rodent diet. Invertebrate feeding is not typical for Microtus voles. The absence of trematodes in the helminth fauna of the water vole and birch mouse is mainly due to the small number of studied rodents of these species.
Infection of rodents with helminths that have a direct life cycle (nematodes) occurs as a result of close contact with the soil. When feeding on the green parts of plants, active burrowing, rodents accidentally swallow both eggs of nematodes (H. spumosa, genera Trichuris and Syphacia) and invasive larvae of parasites (genera Heligmosomum and Heligmosomoides) [47,71]. Recent studies of the morphological and genetic variability of Trichuris spp. have revealed that T. arvicolae parasitizes in rodents of the Arvicolinae subfamily, and T. muris parasitizes in mice [55,72,73].
The rodents become infected with the nematode M. muris, which has an indirect life cycle, by eating insects-intermediate hosts of the parasite (dung beetles of the genus Geotrupes Latreille, 1797, locusts, grasshoppers, crickets, earwigs and cockroaches) or, which is unlikely, paratenic hosts-amphibians [47,71,74].
The metacestode H. taeniaeformis s. l., which has veterinary significance, can cause hydatigerosis of wild and domestic carnivores [27,75,76]. The nematode S. obvelata is potentially dangerous to man and can cause human syphaciosis [27,76]. We have not found in small rodents of the National Park "Smolny" a dangerous parasite the metacestode Echinococcus multilocularis Leuckart, 1863, which causes echinococcosis of humans and animals [75,76]. Despite the widespread distribution of E. multilocularis in the northern and central regions of Eurasia in the final hosts-carnivores [48,75], single findings of the parasite in M. arvalis and A. agrarius from the Samarskaya Luka (Middle Volga region) were recorded in rodents of European Russia [27,28,77].
A comparison of the parasite fauna in the studied rodent species from the National Park "Smolny" showed that the helminth fauna of micromammals within the subfamilies Murinae and Arvicolinae is most similar in terms of the Morisita's overlap index ( Table 3). The revealed similarity of the helminth fauna of different rodent species is mainly due to the diet of herbaceous vegetation (voles), seeds of plants and fruits (mice), as well as the phylogenetic relationship of animals.
The analysis of the helminth species diversity in myomorph rodents showed that the helminth fauna of M. arvalis, M. subterraneus and S. uralensis is more diverse, despite the fact that A. agrarius (12 species) and C. glareolus (14) have a greater number of helminth species. The Shannon index values are lower in these rodent species due to the high abundance and dominance of Syphacia nematodes in their helminth fauna ( Table 2). This is also due to the presence of a larger number of single and random parasite species in A. agrarius and C. glareolus. As a result, Shannon index showed that the helminth fauna in M. arvalis (7 species), M. subterraneus (3) and S. uralensis (10) are more diverse than in A. agrarius and C. glareolus.
The helminth diversity in myomorph rodents in a particular locality is associated with different natural conditions of their habitats. The fauna of animal parasites is influenced by many factors: the diversity of the fauna of vertebrates and invertebrates in the biocenosis, which can serve as intermediate and final hosts of helminths, microclimatic conditions of animal habitats, host population density, diet features, etc. [2,[78][79][80][81][82][83][84][85].
There was a high degree of similarity, according to a comparative analysis of the helminth fauna of myomorph rodents from the National Park "Smolny" with the parasite fauna of small rodents from other territories of Russia. The degree of similarity of helminth fauna in rodents is determined by the presence of a larger or smaller number of hostspecific parasite species that are found throughout the range of the rodent host. Most of the recorded helminth species in micromammals (26 out of 30 registered) are obligate parasites of rodents that are widely distributed in Russia and Europe. This is due to the wide distribution of both final rodent hosts and intermediate hosts of their helminths.

Conclusions
Thus, the helminth fauna of 11 species of myomorph rodents from the National Park "Smolny" is represented by 30 species: 6 trematodes, 11 cestodes and 13 nematodes. No parasites were found in M. musculus and M. minutus.
The trematode P. maculosus was found in C. glareolus in the fauna of Russia for the first time. C. glareolus is indicated as a new host for the trematode. M. arvalis is noted as a new host for the metacestode V. mustelae.
The richness of the helminth fauna of different species of myomorph rodents is determined by the size of the ecological niche of micromammals that they occupy in the biocenosis. Among the small rodents from the National Park "Smolny", the most diverse helminth fauna is in numerous and widespread species: in rodents of the subfamily Arvicolinae-C. glareolus; in rodents of the subfamily Murinae-S. uralensis and A. agrarius. Species with low numbers and limited trophic and/or spatial niches are characterized by a poor helminth fauna (M. subterraneus, S. betulina and A. amphibius).
A comparative analysis of the helminth fauna in myomorph rodents showed that the parasite composition in M. subterraneus from the National Park "Smolny" reaches the maximum similarity with other regions of European Russia. High similarity with other regions of Russia was noted for the helminth fauna in S. flavicollis, S. uralensis, A. amphibious, S. betulina and M. agrestis. The fauna of the helminths in A. agrarius, C. glareolus and M. arvalis is less similar to other studied areas.
Two out of 30 helminth species found in myomorph rodents have medical and veterinary significance as potential pathogens of dangerous helminthiasis. These include the cestode H. taeniaeformis s. l. and the nematode S. obvelata.
Author Contributions: Conceptualization, A.R. and N.K.; methodology, A.K. and N.K.; formal analysis, A.K. and N.K.; investigation, A.K. and N.K.; writing-original draft preparation, A.K., N.K. and A.R.; writing-review and editing, A.K. and A.R.; project administration, A.R.; funding acquisition, A.R. All authors have read and agreed to the published version of the manuscript.

Data Availability Statement:
The data presented in this study are available on request from the corresponding author.