An annotated checklist of arthropods associated with the root vole Microtus oeconomus

In the literature, 114 species of arthropods associated to Microtus oeconomus have been reported in the entire area of their occurrence. There are eight species of hard ticks, 52 species of gamasid and chigger mites, 47 species of fleas and seven species of sucking lice. In general, the dominant parasites of the Palearctic and Nearctic root vole populations are either western or entire Palearctic species. The analysis of the geographical range of their occurrence indicates that most of them occur both in Europe and Asia. Throughout Europe, Asia and America (Holarctic realm), root voles share 13 species of mites, seven species of fleas, and three species of sucking lice. Ectoparasite species split between two continents, most of them are found in both Europe and Asia (Palearctic region). Here belong three species of ixodid ticks, sixteen species of mites, seven species of fleas and two species of sucking lice. In Asia and the North American continents (Holarctic realm excluding Europe) populations of root voles share only one tick species, two species of mites, three species of fleas and one species of sucking lice. Of the parasitic species found only in Western Palearctic, excluding Asia, root voles are infested by three ixodid tick species, 14 mite species, and 13 flea species. Among the parasitic arthropods affecting root vole only in Eastern Palearctic, excluding Europe, one tick species, four mite species and seven flea species occur. There are only three mite species, ten flea and one sucking louse species on voles that inhabit North America (Nearctic region). Associated arthropods are obligate and facultative parasites or nidicolic and edaphic species. Seasonal changes in numbers of ticks, parasitic mites, sucking lice, fleas have also been observed.


Introduction
Root vole Microtus oeconomus (Pallas, 1776) is one of the most widespread members of the Cricetidae family.It is a boreal species; its continuous area in Europe does not extend south of the 50° latitude.It is found in the northern and central parts of Europe, from the Scandinavian Peninsula to the Pyrenees, Alps and Carpathian Mountains in of the root vole affects the large number and variety of associated ectoparasite arthropods.
This paper is an analytical review summarizing the available data on parasitic arthropods associated with M. oeconomus across their range of distribution.Papers were collected from websites including PubMed, Google Scholar, Web of Science, Scopus, ScienceDirect.Preliminary phrases or keywords, including root-vole and Microtus oeconomus names, and names of taxa of different levels of external parasites, were used to search for papers about infestation of the rodent species with ticks, mites, fleas and sucking lice.For the second step, new basic keywords were included in an additional search for supplementary papers, about infestation spectrum of biological stages of ticks and mesostigmated mites infesting root vole, the spectrum of other hosts of ticks, mites, fleas and sucking lice, the geografic distribution.The third stage was the analysis of the reference list in publications collected during the first and second stages.The aim was to find records not included in the world databases, that is, published before the spread of the Internet.For the evaluation of the quality of papers, the selected records required commonly used standards such as layout, properly described study methods, reliable results, correct conclusions, correct naming and terminology.
The review covers obligatory and facultative parasitic species.Commensals and arthropods otherwise associated with the rodent, although they are, for example, an important element of the nest fauna or interact in various ways with parasites, have been omitted.The attention was paid to the general abundance of parasitic species, their diversity, and differences in the composition of parasitofauna in particular zoogeographic regions.
The list includes 114 species of arthropods, associated with the root vole, which have been mentioned as parasites in the literature until the completion of the article (in 2022).The most important information is given -synonyms present in parasitological literature, geographical occurrence, range of hosts, place and authors of records of associations with M. oeconomus and, if possible, infestation prevalence or similar data.The classification and names of arthropod species are given after Wegner (1966), Skuratowicz (1967), Krasnov (2008), Krantz and Walter (2009), and Guglielmone et al. (2014).Species names are used according to the review papers by majority of European authors, though some of these might be treated as synonyms.
The short description of each species follows the same pattern: valid taxonomic name; the commonly used synonyms; distribution (and, if necessary, additional data affecting the spread); host range, with an indication of the most important host, if any; records on M. oeconomus; prevalence and intensity of infestation of M. oeconomus, if possible.

Summarising list of associated arthropods
The ectoparasites of M. oeconomus belong to the orders Acari (mites and ticks), Anoplura (sucking lice) and Siphonaptera (fleas).There are no records of parasites belonging to Coleoptera (beetles) and Diptera (flies), whose representatives can occur on other Microtus species (Timm 1985).The total list of related arthropods recorded in the entire area of root vole distribution includes eight species of ixodid ticks, 52 species of mites, 47 species of fleas and seven species of sucking lice; however, only 21 of them cover the whole occurrence range of the host.(Tables 1, 2, 3 and 4).Many of the on the list species are those which have only been recorded on M. oeconomus once, or are mentioned as parasites of this rodent without specifying the location.These are 30 species (two ticks, 12 mites, 11 fleas, three sucking lice), mostly specific to another rodent or with a wide range of hosts for which root vole may have been an accidental host.Their association with M. oeconomus needs confirmation.The exceptions are two species of Psorergates, described as ectoparasites of this rodent on the basis of a single observation, and never recorded again.
As typical parasites of rodents, associated with voles, arthropods are classified into four taxonomic groups.The list of associated arthropods varies geographically.These are ixodid ticks, gamasid and chigger mites, fleas and sucking lice.The lifestyle of root vole also influences the parasite community -the preferred habitats of this species are wet fields and meadows as well as wet forests.It digs burrows and is able to build nests above the ground in bushes and clumps of grass and sedges (Pucek 1981).
Most of the recorded ectoparasites are species with a broad host spectrum, although species that attack small mammals -rodents and insectivores predominate.Three flea species are specific to M. oeconomus -they are the most common and most abundant on this host.These are M. walkeri in Europe, P. ostsibirica in Asia and North America, and M. calcarifer in the entire Holarctic zone.In addition, Psorergates oeconomi and P. neerlandicus mites were found only on M. oeconomus, although this is only a single report, not confirmed by further observations.
The remaining groups of arthropods include parasites typical to the genus -common on M. oeconomus and other species of the genus Microtus; on other small mammals they occur in low numbers.These are the tick D. reticulatus in Western Palearctic, the mite H. transiliensis and the flea M. taiganus in Eastern Palearctic, three mites and three flea species throughout the Palearctic, two flea, four mite and two sucking lice species throughout the Holarctic realm.In addition, there are one nearctic mite and two flea species found in Asia and North America (Tables 1, 2, 3 and 4).(Zwolski 1960;Skuratowicz 1967;Karbowiak et al. 2022), Russia (Novozhilova 1967;Krasnov et al. 2010).Prevalence: accidental (Zwolski 1960;Karbowiak et al. 2022).
In general, the dominant parasites of Palearctic and Nearctic root vole populations are either cosmopolitan or Palearctic species.The analysis of the geographical range of their occurrence indicates that most of them occur both in Europe and Asia.In the whole Holarctic realm -across Europe, Asia and Northern America -root voles share 13 species of mites, seven species of fleas, and three species of sucking lice.The species that occur in two continents are found mainly in the Palearctic region -Europe and Asia.They include species that are found throughout Eurasia, from the Atlantic coast, or at least from Central Europe, to the Pacific coast of Asia, or at least their range extends to the Central Siberian Highlands.These are three tick species, 16 mite species, seven flea species and two sucking lice species.Ectoparasites of root vole, occurring in Asia and the North American continent are only one tick species, two gamasid mite species, three flea species and one sucking louse species.Among parasites that occur only in the Western Palearctic, root voles harbour three tick species, 14 mite species, and 13 flea species.As mentioned above, most of these species exceed the Urals range.Two species of gamasid mites and five species of fleas are recorded only in Europe.In the Eastern Palearctic one species of ticks, four species of mites, and seven flea species are found.Three mite species, ten flea species and one sucking louse species

Geographical distribution of individual species of arthropods associated with root vole
The division of the world into zoogeographic regions largely reflects the distribution of species, but it does not exactly match them.For publication purposes, the Western Palearctic, the Eastern Palearctic, the Palearctic as a whole, and the Nearctic are included.However, it should be remembered that the division of the parasitic species mentioned in the paper between these regions is in some cases very coarse.Few are beyond doubt, such as the C. bisoctodentatus flea, found only in Europe, or the E. wenmanni flea, found only on the American continent.It is problematic to classify the species inhabiting western and eastern Eurasia to the appropriate part of the zoogeographic regions.The arbitrary border between the Western and Eastern Palearctic is the Ural mountain range.The mountain range is convenient in determining the boundaries of zones on the map, but it does not always render precisely into the occurrence and spread of animals.Most species begin their range in Central or Eastern Europe, spread throughout Asia to the Pacific coast, or possibly from the Atlantic coast throughout Europe to Western Siberia Plain.In these cases, species that occur in Europe, extending no further than Western Siberia Plain, were considered to belong to the Western Palearctic, species found in Eastern Europe, and further found throughout Asia all the way to the Pacific, are considered as fauna of the Eastern Palearctic.The decisive factor was whether most of the range of this species is to the west or east of the Ural Mountains.The question of the horizontal division of Asia into zoogeographical realms has been omitted; except     It should be noted that many species of ectoparasitic arthropods have a much wider range of distribution than their known records on the root vole.This applies, for example, to wide-ranging arthropods such as the D. reticulatus tick, the P. kraepelini, H. nidi, H. hirsutus mites, and the M. turbidus, M. walkeri, N. fasciatus and C. agyrtes fleas.Known reports of their finding on root voles concern only the western area of their occurrence.There are also species often collected from root voles only in the eastern part of their range such as H. nidiformes, H. liponyssoides, H. soricis, and H. amphibius mites and the M. rectangulatus flea.At the moment it is not possible to say whether this is only the result of a lack of sufficient studies or whether they actually prefer other species of hosts spread in the range of their occurrence.

The nature of the associations between arthropods and root voles
Arthropods associated with rodents and insectivores formed several ecological groups of parasites given by their feeding behavior and degree of association with mammals.The first are obligatory parasites (OP), specialized and having a strong trophic relationship with the mammal, in many cases with a specific genus or species.They live mainly in the hair (parasites that inhabit the host) or in nests (parasites that inhabit the nests).Representatives of this group are ixodid ticks, sucking lice, adult fleas and many gamasid mites (Hirstionyssus, Laelaps).Temporary parasites may be included in this group as well, which feed on the host but spend most of their time in the host's nest.Common examples are a few fleas and a few mesostigmatid mites.
Facultative parasites (FP) live independent of a host but may occasionally be parasitic.They can be found on the body of a mammal, but more often in their nests.This group includes species of mite genera such as Androlaelaps, Eulaelaps, Haemogamasus.
Obligate parasites are the most numerous group of parasitic arthropods associated with voles.These are all species of hard ticks -eight species, all sucking lice -seven species, fleas − 47 species and parasitic/facultative parasitic mites -about 40 species, most of which belong to Laelapidae, Trombiculidae, Myobiidae, Psorergatidae and Listrophoridae families.Most of the obligate parasites occur in the Palearctic region, the most numerous group of which are both in Asia and Europe.The range of a few parasites is limited to Western Palearctic (17 species, including 4 ticks, 9 mites, 13 fleas) or Asia (7 species including one tick, 2 mites, 3 fleas, one sucking louse species) only.Two flea species have have been found on root voles in Northern America only (Table 4).
It is obvious that throughout the wide range of M. oeconomus distribution, there is a large group of cosmopolitan ectoparasites, recorded from every place of occurrence of their host.This phenomenon can be linked to the late colonization of Northern America by the root vole around 55,000 years ago in the Pleistocene, while M. oeconomus fossils in Europe date back 125,000 years.Consequently, the allozymic, chromosomal and morphological variability between subspecies is less than on previous invaders (Lance and Cook 1998).The dominant parasites of the Palearctic and Nearctic vole populations are therefore cosmopolitan or Palearctic species.Many of the blood-sucking parasites that are characteristic of Nearctic rodents cannot be found anywhere outside this region.Holland (1963) emphasizes that many flea species are believed to have survived from the ancient Bering fauna, which apparently originated in the Palearctic.In general, nearctic forms are co-species with species found in Asia, and sometimes in Europe.
The most numerous group of M.oeconomus ectoparasites are species inhabiting the entire Palaearctic zone.The next numerous group are ectoparasites, the range of which covers the entire Holarctic realm -from Europe, through Asia to North America.Among them, there are cosmopolitan species, spread all over the world.The species belonging to the cosmopolitan group are the mites A. fahrenholzi, H. ambulans, E. stabularis, the fleas N. fasciatus, L. segnis, and the sucking louse P. serrata.These are polyxenic parasites, or species scattered all over the world with cosmopolitan hosts -especially rats and house mice.They comprise the L. segnis and N. fasciatus fleas, and the A. fahrenholzi mite.The mites H. amphibius and L. muris can be also included to this group; they are associated with A. terrestris, and spread to new areas with their host.They are not abundant on root voles, but due to low host specificity they attack them in the absence of suitable hosts.
Many of that group are boreal, boreo-montane or trans-Beringian species, not so much related to the typical environment of these landscapes, but to the polar climate: H. gudauricus, L. clethrionomydis, A. penicilliger, C. idius, C. indages, M. rectangulatus, A. marikovskii, A. sibirica, and C. birulai.The least numerous is the group shared between Asia and America.There are only seven species -I.angustus, H. mandschuricus, L. multispinosus, Amphipsylla marikovskii, P. ostsibirica, C. dacenkoi, and P. borealis.
It is noteworthy that one tick species -Haemaphysalis concinna -has only been recorded in an isolated population of the root vole in southern Slovakia.In analogy, the fleas Epitedia spp.unique to voles on the American continent and many distinct boreal species of the genera Catallagia, presence of the host, but also on some environmental factors, the dominant groups may be different in the European, Asian and American root vole populations.This is included in the literature records.The dominant external parasites of the root vole are hard ticks -larvae and nymphs.In Europe, such species are I. ricinus and D. reticulatus, their average prevalence is 11.0% and 14.0%, respectively (Karbowiak et al. 2022), but seasonally the prevalence can reach 75 to 100.0% (Kononova 1996;Karbowiak et al. 2022).In Asia, I. ricinus is absent and is replaced by I. persulcatus and I. pavlovskyi (Filippova 1977).
A common group of parasites are subdominants and their prevalence of infestation does not exceed 9.0%.Parasites with low host specificity and wide distribution mainly belong to this group.In Europe, such parasites are the M. turbidus flea, the H. nidi and H. ambulans mites (Karbowiak et al. 2022).The list of subdominant mites in the population of M. oeconomus in Belarus is provided by Savitsky and Kulnazarov (1988) -these are P. oudemansi, P. kraepelini, C. chiropterae, H. isabellinus, A. fahrenholzi, L. agilis, L. jettmari, and T. autumnalis.The dominant mite species inhabiting the nests of the root vole are H. ambulans and A. fahrenholzi (Edler and Mehl 1972;Whitaker et al. 2007;Krasnov et al. 2010;Bregetova 1956;Airoldi et al. 1989).In the Asiatic part of M. oeconomus occurrence range, the subdominants are fleas -C.uncinatus (Novozhilova 1967) a cosmopolitan range due to the wide distribution of their main hosts.Facultative parasites are a small group of 14 mite species belonging to Parasitidae and Laelapidae.They are species with a wide range, spanning the Palearctic and even the entire Northern Hemisphere.The large group of mites includes arthropods associated not with voles, but with their nests, as commensals or on the principle of synoikia -groups of nidicolous and edaphic species.The four species -Androlaelaps fahrenholzi, Eulaelaps stabularis, Nosopsyllus fasciatus, Leptopsylla segnis, have a cosmopolitan range.An interesting fact is the lack of recorded optional parasites and arthropods from the nidicolous and edaphic groups in the nearctic; however, it cannot be determined whether they do not actually exist, or whether they exist and have not been detected so far (Tables 1, 2 and 3).
In many cases it is difficult to classify several species or taxa into a particular ecologic group.Many mites have a wide spectrum of foraging behavior, they can be both predators and hematophages.Fleas, as adults, are obligatory blood feeding parasites, strongly associated with their hosts, while as larvae they are associated with nests, where they find favorable conditions for development, and at this stage of development they are saprobionts.
In the case of ticks and fleas, the nature of their parasitism usually follows the taxonomic order and their enumeration is not difficult.This is not the case for mites, as obligate and facultative hematophages or predators can be found in the same taxonomic group.An additional difficulty is the fact that some species are known only from the morphological description and nothing is known about their lifestyle, food, or the role they play in the root vole.Therefore, the classification of these species into the group of obligatory, facultative or commensal parasites is based on the principle of reference to related species -which of course carries the risk of error.

The prevalence of infestation and domination structure
The list of arthropod species associated with the root vole is quite extensive.Most of the reports, however, concern only finding the species on voles or in their nests.Compared to the species list, detailed data on the degree of ectoparasite infestation of voles are sparse and come from only a few sources.In many cases, authors noted the species as common or dominant parasite and give either detailed numbers nor the season of occurrence.
The dominant group of parasites is determined by the high frequency of infestation -usually above 10.0%, and the occurrence in all host populations in the geographical area.Since the occurrence of the parasite depends not only on the 1 3 period of their life than with the host.The temperate climate has strong influence on their biology, seasonal dynamics of occurrence and peaks of activity, different for larvae, nymphs and adults (Nowak-Chmura 2013).This renders into noticeable seasonal changes in the host invasion.

Conclusions
The fauna of the root vole ectoparasites includes forms typical for small rodents -mites, ticks, fleas and sucking lice.The wide range of root vole occurrence cause a large variety of ectoparasites.Among the ectoparasites, there are local species found in specific zoogeographical regions, as well as widespread species found throughout the Holarctic.There is also a group of cosmopolitan species found all over the world.
Funding There are currently no funding sources.

Declarations
Conflict of interest On behalf of all authors, the corresponding author states that there is no conflict of interest.
Ethical approval Not applicable.

Informed consent Not applicable.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material.If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.To view a copy of this licence, visit http://creativecommons. org/licenses/by/4.0/.and A. penicilliger, the prevalence of infestation was 9.8% (Nikulina 1980).
The variability of the parasitic fauna of different root vole populations is probably related to the differences in the historical development of the biotopes.These differences were also reflected in the different hydrological conditions, vegetation and level of diversity of small mammals.In addition, the contact and exchange of flea fauna with populations of small mammals living in various environmental conditions also plays an important role (Stanko 1994).
Seasonal variability is an issue to consider when describing the fauna of mammalian ectoparasites.Most species of ectoparasites change their population densities during the year or occur only seasonally, in certain months, and are absent in the rest of the year.An example of such a change in the seasonal abundance of ectoparasites is the population of root voles in the Baikal region described by Vershinin et al. (2019).In winter, gamasid mites dominate, and in summer, ixodid ticks.The fleas are most numerous in autumn, while sucking lice do not show any distinct fluctuations.In addition, seasonal changes in the number of parasitic mites are relatively rarely described, data can only be found in a few studies.For example, in Slovakia peak parasite numbers in Mus spicilegus Petényi, 1882 nests were found in December and declinen by April.In the group of nidicolous species, only a slight increase in numbers was observed in December, declining in April.Edaphic species had two population peaks, from December to February and in May (Várfalvyová et al. 2011).In Odessa, Ukraine, the peak number of gamasid mites on rodents was observed in autumn (Voljansky 1974).Some specific data were provided by Haitlinger (1988) for H. nidi and E. stabularis occurring on small mammals in Poland.Haemogamasus nidi has two population peaks -bigger in spring and smaller in autumn.Eulaelaps stabularis has one peak in summer.However, the dynamics may vary and depends on the host species.Sucking lice also tend to show seasonal dynamics in appearance.The average intensity of H. edentula infestation is low in spring and increase was observed in autumn (Haitlinger 1989).
Similar phenomena have also been described in the case of fleas.In the Białowieża Primeval Forest, C. agyrtes, M. turbidus and P. soricis are most abundant in summer, rarely in autumn, and absent in winter.Ctenophthalmus uncinatus is common in spring and summer, and declines in autumn.Peromyscopsylla bidentata occurs mainly in autumn and Rh.integella in winter (Lachmajer 1959).
Ticks are exhibiting the most rapid seasonal changes in incidence.On M. oeconomus, infestation by larvae and nymphs of ticks of the genera Ixodes and Dermacentor was observed (Karbowiak et al. 2022).Ticks are temporary parasites that are associated with the environment for a longer 1 3 .

Table 2
The world list of fleas associated with Microtus oeconomus.Classification afterKrasnov (2008)

Table 3
The world list of sucking lice associated with Microtus oeconomus

Table 4
Distribution of ectoparasitic arthropod species associated to M. oeconomus in zoogeographic regions Oropsylla and Corrodopsylla are not found in Asian and European vole populations.