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Parasites, Bacteria and Viruses of Glis glis
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This entry is adapted from the peer-reviewed paper 10.3390/d14070562

Rodents (Rodentia), due to their number and species diversity, are important elements of natural ecosystems. Some species of rodents are widely distributed. Glis glis (Linnaeus, 1766) (Rodentia, Gliridae) is one such species. An overview of the parasites, bacteria and viruses of G. glis inhabiting the Western Palearctic is given.

ectoparasites Glis glis helminths overview protozoans viruses Western Palaearctic

1. Introduction

Rodents (Rodentia), due to their number and species diversity, are important elements of natural ecosystems. Some species of rodents are widely distributed [1][2][3][4][5][6][7]. The European edible dormouse, Glis glis (Linnaeus, 1766) is one such species and is widespread across western Eurasia. This rodent species is found in most European countries and regions of western Asia: through northern Turkey to the Caucasus, northern Iran and Turkmenistan [8][9][10][11]. Glis glis is the largest member of the family Gliridae, arboreal rodent with a nocturnal lifestyle. This rodent has the longest period of hibernation among the mammals of Europe, up to 9 months [12].
It is known that small wild rodents play an important role in the life cycles of the helminths of carnivorous mammals and birds of prey in higher trophic levels. Small rodents are involved in maintaining natural foci of zoonoses—diseases dangerous to humans and animals [4][13][14][15][16][17][18][19][20][21]. In this regard, the study of the parasite fauna of G. glis is of great scientific (biodiversity monitoring) and practical importance (study of the dormouse’s role in the spread and preservation of zoonoses).
The literature on parasites, viruses and protozoans of G. glis currently contains about 180 references, covering an approximately 200-year period. The first attempts to bring together data about the viruses, parasites and protozoans of G. glis were undertaken in the reviews by Rossolimo [22] and Kryštufek [23][24], which contained data on 64 species of ecto- and endoparasites found in the dormouse. Unfortunately, these reviews did not include most papers not indexed in electronic databases, so they are still inaccessible to most researchers.

2. Parasites, Bacteria and Viruses of Glis glis in the Western Palaearctic

At the present stage of research, 104 species (with subspecies) of viruses, protozoans, ectoparasites and helminths were recorded in G. glis: 4 viruses, 8 Protozoa, 6 Cestoda, 6 Trematoda, 4 Nematoda, 1 Heteroptera, 2 Anoplura, 39 Siphonaptera and 34 Acari.

2.1. Viruses of Glis glis

The study of viruses in G. glis has a short history spanning only the last decades. Four viruses of three families were found in the edible dormouse (Table 1).
Table 1. Viruses of Glis glis in Western Palaearctic.
Table

Species

Distribution

Host Range

Medical & Veterinary Significance

Country

References

Family Picornoviridae

Encephalocarditis virus (EMCV)

E

small rodents

cause myocarditis, diabetes mellitus, reproductive disorders and nervous system damage

Italy

[25][26]

family Polyomaviridae

Polyomavirus

E

Glis glis

—

Germany

[27]

Family Bunyaviridae

Hantaan orthohantavirus (HTNV)

E

small rodents

main causative agent of Korean hemorrhagic fever in humans

Slovenia

[28]

Dobrava-Belgrade orthohantavirus (DOBV)

E

Apodemus mice

cause hemorrhagic fever with renal syndrome

Serbia

[29]
Note: E—Europe.
Encephalocarditis virus (EMCV) is found in many species of wild and domestic animals in various regions of the world [30]. The host-specific Polyomavirus found in G. glis belongs to a group of DNA viruses that infect mammals, birds and fish [31][32]. Hantaan orthohantavirus (formerly known as Hantaan virus) is a negative-sense RNA virus species. The edible dormouse is a reservoir host for the Hantaan orthohantavirus (HTNV). Dobrava-Belgrade virus (also known as Dobrava virus), found in the edible dormouse, is common in the former Yugoslavia, Germany, Estonia, Slovakia, European Russia and other Eastern European countries [33]. All viruses have a European range (Table 1).

2.2. Protozoa of Glis glis

Eight protozoan species from the five families are known in the edible dormouse (Table 2).
Table 2. Protozoa of Glis glis in Western Palaearctic.
Table

Species

Distribution

Host Range

Medical & Veterinary

Significance

Country

References

Family Borreliaceae

Borrelia afzelii Canica et al. 1994

E

rodents,

causative agent of Lime disease (LD)

Croatia

[34]

dormice

Germany

[35][36][37][38]

Borrelia garinii Baranton et al., 1992

E

birds

causative agent of LD

Germany

[36]

Borrelia bavariensis Margos et al., 2009

E

rodents, dormice

causative agent of LD

Germany

[36]

Borrelia miyamotoi Fukunaga et al., 1995

E

dormice

—

Germany

[36]

Family Rickettsiaceae

Rickettsia typhi (Wolbach and Todd, 1920)

C

rodents

causative agent of murine typhus, an endemic human typhus

Slovenia

[39]

Family Yersiniaceae

Yersinia pestis (Lehmann and Neumann, 1896)

C

wild and domestic animals (mainly rodents)

plague pathogen

Europe

[40]

Family Eimeriidae

Eimeria gliris Musaev and Veysov, 1961

E

Glis glis

—

Azerbaijan

[41]

Family Francisellaceae

Francisella tularensis (McCoy and Chapin 1912)

H

rodents, humans

pathogen of gram-negative coccobacillus, causative agent of tularemia

Switzerland

[42]
Note: E—Europe, C—Cosmopolitan, H—Holarctic.
Among the protozoa found in G. glis, Borellia spp. (family Spirochaetaceae) are most represented (four species). They belong to the Borrelia burgdorferi (Johnson et al., 1984) sensu lato species complex. The natural reservoir hosts of Borrelia are wild animals (rodents, birds and deer). Borrelia afzelii and B. bavariensis are associated with rodents [43][36][44]. Borrelia garinii is better adapted to birds [45].
The obligate intracellular bacteria Rickettsia typhi (Wolbach and Todd, 1920) is best known as the causative agent of an endemic human typhus that occurs worldwide [46]. This protozoan species can be transmitted to a mammalian host by the bite of an infected flea or louse [47].

2.3. Helminths of Glis glis

In total, 16 species of parasitic worms were recorded in G. glis: 6 Cestoda, 6 Trematoda and 4 Nematoda (Table 3). Most of the helminth species parasitise the edible dormouse at the mature stage (14 species). Only two species of helminths were noted at the larval stage: the trematode Alaria alata (Goeze, 1782) and the cestode Mesocestoides lineatus (Goeze, 1782), for which the dormice serve as paratenic hosts. The finding of a small number of larval stages of parasitic worms indicates an insignificant role of G. glis in the life cycles of helminths of vertebrates of high trophic levels.
Table 3. Helminths of Glis glis in Western Palaearctic.
Table

Species

Distribution

Host Range

Medical & Veterinary

Significance

Country

References

Family Dicrocoeliidae

Dicrocoelium dendriticum (Rudolphi, 1819)

C

mammals (mainly ungulates)

causative agent of dicroceliosis of livestock

Belarus

[48]

Lyperosomum armenicum (Stcherbakova, 1942)

E

Glis glis

—

Armenia

[49]

Belarus

[48][50][51]

Family Brachylaimidae

Brachylaima recurva (Dujardin, 1845)

P

small rodents

—

Russia

[52]

Family Plagiorchiidae

Plagiorchis elegans (Rudolphi, 1802)

H

birds, small mammals, reptiles

—

Belarus

[48][50]

Family Lecithodendriidae

Lecithodendrium semen (Kirschenblatt, 1941)

E

Glis glis

—

Belarus

[48][50][53]

Family Diplostomidae

Alaria alata (Goeze, 1782), msc.

C

amphibians, reptiles, small mammals

causative agent of alariasis of farmed fur animals

Belarus

[54]

Family Hymenolepididae

Armadolepis myoxi (sensu stricto) (Rudolphi, 1819) (syn.: Hymenolepis sulcata (von Linstow, 1879))

E

Glis glis

—

Switzerland

[55] reported as H. sulcata

Slovakia

[56][57][58][59][60] reported as H. sulcata

Croatia

[61] reported as H. sulcata, [62]

Hungary

[63] reported as H. sulcata

Spain

[64][65] reported as H. sulcata

Germany

[66][67] reported as H. sulcata

Armadolepis longisoma Makarikov, Stakheev and Tkach, 2018

E

Glis glis

—

Russia

[68] reported as Armadolepis sp. 1, [69][70]

Armadolepis genovi Makarikov and Georgiev, 2020

E

Glis glis

—

Bulgaria

[71] reported as H. myoxi, [72]

Armadolepis sp.

E

Glis glis

—

Russia

[52] reported as H. myoxi

Hymenolepididae sp.

E

—

—

Moldova

[73][74] reported as Hymenolepis horrida (Linstow, 1901)

Belarus

[50] reported as H. horrida and Rodentolepis straminea (Goeze, 1782)

Azerbaijan

[75] reported as Hymenolepis diminuta (Rudolphi, 1819)

Ukraine

[76] reported as R. straminea

Slovakia

[59] reported as Rodentolepis sp.

Family Mesocestoididae

Mesocestoides lineatus (Goeze, 1782), tetrathyridia

P

reptiles, small mammals

cause mesocestidosis in humans, carnivores

Italy

[77]

Family Capillariidae

Pterothominx sadovskoi (Morozov, 1956) (syn.: Thominx sadovskoi Morozov, 1956; Armocapillaria sadovskoi (Morozov, 1956))

P

small rodents

—

Belarus

[48][50][51]

Family Heligmonellidae

Paraheligmonina gracilis (Leuckart, 1842) (syn.: Heligmosomum gracile (Leuckart, 1842); Longistriata schulzi Schachnasarova, 1949; Longistriata elpatievskii Schachnasarova, 1949)

WP

Glis glis

—

Russia

[52][68][70]

Belarus

[48][50][51][54]

Germany

[78][79]

Bulgaria

[71]

Ukraine

[76][80][81]

Azerbaijan

[75][82]

Armenia

[83][84]

Croatia

[61][62]

Spain

[64]

Italy, France

[79]

Slovakia

[56][57]

Family Rictulariidae

Rictularia cristata (Frölich, 1802)

E

small rodents

—

Central Europe

[85][86][87]

Rictularia amurensis Schulz, 1927

P

small rodents

—

Belarus

[48][50]

Note: E—Europe, C—Cosmopolitan, H—Holarctic, P—Palaearctic, WP—Western Palaearctic.

2.4. Ectoparasites of Glis glis

In total, 76 species of ectoparasites were found on G. glis, belonging to Anoplura (2 species), Heteroptera (1), Siphonaptera (39) and Acari (34) (Table 4). Only eight species of ectoparasites are host-specific parasites of the edible dormouse: the lice Schizophthirus gliris (Blagoveshtchensky, 1965) and Schizophthirus pleurophaeus (Burmeister, 1839); the fleas Myoxopsylla jordani (Ioff and Argyropoulo, 1934) and Myoxopsylla laverani (Rothschild, 1911); and the mites Hirstionyssus gliricolus (Masan and Ambros, 2010), Hirstionyssus paulisimilis (Masan and Fenda, 2010), Gliricoptes glirinus (Canestrini, 1895) and Radfordia gliricola (Vesmanis and Lukoschus, 1978). Three species of ectopatasites are common parasites of arboreal rodents (squirrels and dormice): the fleas Ceratophyllus sciurorum (Schrank, 1803) and Leptopsylla sciurobia (Wagner, 1934) and the mite Hirstionyssus sciurinus (Hirst, 1921). The other 65 species of ectoparasites are accidental and facultative dormouse parasites, which parasitise many species of mammals and birds.
Table 4. Ectoparasites of Glis glis in the Western Palaearctic.
Table

Species

Distribution

Host Range

Medical & Veterinary

Significance

Country

References

Family Hoplopleuridae

Schizophthirus gliris Blagoveshtchensky, 1965

E

Glis glis

—

Poland, Bulgaria, North Makedonia

[88][89]

Schizophthirus pleurophaeus (Burmeister 1839)

WP

dormice

—

West Europe, Belarus

[88][89]

Hungary

[90]

Family Cimicidae

Oeciacus hirundinis (Lamarck, 1816)

P

birds (mainly swallows)

—

Slovenia

[91]

Slovakia

[92]

Family Pulicidae

Pulex irritans Linnaeus, 1758

C

mammals (including humans), birds

vector of plague bacteria Yersinia pestis;

intermediate host of the cucumber tapeworm Dipylidium caninum (Linnaeus, 1758), which cause helminthiasis in dogs and cats

Slovenia

[93][94]

Family Ceratophyllidae

Amalareus penicilliger (Grube, 1851)

P

forest rodents

—

Ukraine

[95]

Leptopsylla taschenbergi (Wagner, 1898)

P

forest rodents, insectivores

—

Armenia

[96]

Russia

[97]

Leptopsylla segnis (Schönherr, 1811)

C

house mice, rats

vector of plague and tularemia

Croatia

[93][94]

Leptopsylla sciurobia (Wagner, 1934)

P

squirrels, dormice, Apodemus mice

—

Serbia

[93][94]

Peromyscopsylla bidentata (Kolenati, 1863)

P

forest rodents

—

Ukraine

[95][98]

Ceratophyllus sciurorum (Schrank, 1803)

P

squirrels, dormice

vector of tularemia

Russia

[13][15][52][97][99][100][101][102][103]

Italy

[77][104][105]

Germany

[78][106][107]

Lithuania

[108]

Serbia, Croatia,

Montenegro,

Slovenia, North

Macedonia

[39][93][94]

Bosnia and

Herzegovina

[39][93][94][109]

Ukraine

[95][110]

Armenia

[96][111]

Belarus

[112]

Moldova

[73][74]

Hungary

[113]

Poland

[114]

Bulgaria

[115]

Ceratophyllus sciurorum sciurorum (Schrank, 1803)

P

squirrels, dormice

—

Slovenia

[39]

Germany

[116]

Ceratophyllus rusticus Wagner, 1903

E

birds

—

Slovenia

[93][94]

Ceratophyllus carniolicus Brelih and Trilar, 2001

E

Glis glis

—

Slovenia

[117]

Ceratophyllus hirundinis (Curtis, 1826)

P

birds

—

Slovenia

[93][94]

Ceratophyllus gallinae (Schrank, 1803)

C

birds

—

Slovenia

[94]

Germany

[116]

Lithuania

[108]

Ceratophyllus borealis Rothschild, 1907

P, G

birds

—

Russia

[52]

Ceratophyllus (Monopsyllus) sp.

E

—

—

Slovenia

[94]

Dasypsyllus gallinulae gallinulae (Dale, 1878)

C

birds

—

Slovenia

[94]

Megabothris turbidus (Rothschild, 1909)

P

forest rodents

vector of viral hemorrhagic fever and tularemia

Ukraine

[95][98][110]

Germany

[116]

Russia

[13][101]

Lithuania

[108]

Megabothris walkeri (Rothschild, 1902)

P

forest rodents

vector of tularemia

Russia

[13][101]

Myoxopsylla jordani Ioff and Argyropoulo, 1934

E, I

dormice

—

Armenia

[111]

Russia

[52][99][102][103]

Georgia

[118]

Myoxopsylla laverani (Rothschild, 1911)

WP

dormice

—

Germany

[106][107][116]

France

[119]

Nosopsyllus consimilis (Wagner, 1898)

P

forest rodents

vector of plague and tularemia

Armenia

[96]

Russia

[13][101]

Nosopsyllus fasciatus (Bosc d’Antic, 1800)

C

house mice, rats

vector of the rat tapeworm H. diminuta

Serbia

[109]

Orchopeas howardi (Baker, 1895) (syn.: Orchopeas wickhami (Baker, 1895))

N

Sciurus carolinensis Gmelin, 1788

—

UK

[120]

Family Ctenophthalmidae

Ctenophthalmus wagneri Tiflov, 1927

P

voles

vector of tularemia

Russia

[13][101]

Ctenophthalmus monticola (Kohaut, 1904)

E

insectivores

—

Serbia

[93][94]

Ctenophthalmus agyrtes (Heller, 1896)

E

Apodemus mice

vector of tularemia

Ukraine

[95][98]

Germany

[116]

Ctenophthalmus agyrtes ohridanus Wagner, 1939

E

small mammals

—

Croatia

[93][94]

Ctenophthalmus agyrtes wagnerianus Peus, 1950

E

small mammals

—

Slovenia

[93][94]

Ctenophthalmus proximus (Wagner, 1903)

E

small mammals

—

Russia

[97]

Ctenophthalmus assimilis (Taschenberg, 1880)

P

voles

—

Ukraine

[95]

Ctenophthalmus congener Rothschild, 1907

WP

small mammals

—

Slovenia

[93][94]

Ctenophthalmus nifetodes Wagner, 1933

E

Dinaromys bogdanovi (V. and E. Martino, 1922)

—

Bosnia &

Herzegovina,

Montenegro

[93][94][121]

Ctenophthalmus nifetodes brelihi Rosicky and Carnelutti, 1959

E

Dinaromys bogdanovi

—

Slovenia

[93][94][121][122]

Ctenophthalmus nifetodes tvrtkovici Brelih, 1986

E

Dinaromys bogdanovi

—

Croatia

[93][94][121]

Palaeopsylla soricis (Dale, 1878)

P

insectivores

vector and reservoir of tularemia

Germany

Russia

[116]

[13][101]

Doratopsylla dasycnema dasycnema (Rothschild, 1897)

P

insectivores

—

former Yugoslavia

[123]

Germany

[116]

Family Hystrichopsyllidae

Hystrichopsylla talpae (Curtis 1826)

P

Talpa europaea

vector and reservoir of tick-borne encephalitis

Lithuania

[108]

Russia

[13][101]

Hystrichopsylla orientalis Smit, 1956

E

small rodents, insectivores

—

Lithuania

[124]

Hystrichopsylla orientalis orientalis Smit, 1956

E

small rodents, insectivores

—

Bosnia &

Herzegovina

[93][94]

Family Ischnopsyllidae

Ischnopsyllus intermedius (Rothschild, 1898)

E

bats

—

Germany

[116]

Family Laelapidae

Androlaelaps casalis (Berlese, 1887) (syn.: Haemolaelaps casalis (Berlese, 1887)

C

birds

cause human dermatitis

Moldova

[73][74]

Ukraine

[98]

Belarus

[125]

Laelaps agilis C.L. Koch, 1836

P

forest mice, insectivores, carnivores

vector of plague, tularemia, hemorrhagic fever with renal syndrome (HFRS), tick-borne encephalitis, leptospirosis, brucellosis

Slovakia

[126]

Eulaelaps stabularis (C.L. Koch, 1836)

C

small mammals, birds

vector of tularemia, Q fever, tick-borne encephalitis, brucellosis, leptospirosis

Slovakia

[126]

Myonyssus gigas (Oudemans, 1912)

P

rodents, insectivores, carnivores

—

Slovakia

[126]

Haemogamasus horridus Michael, 1892

WP

rodents, insectivores, carnivores

—

Slovakia

[126]

Haemogamasus nidi Michael, 1892

H

rodents, insectivores, carnivores

vector of tularemia

Slovakia

[126]

Haemogamasus pontiger (Berlese, 1904)

C

rodents, insectivores, carnivores

—

Slovakia

[126]

Family Hirstionyssidae

Hirstionyssus sciurinus (Hirst, 1921)

P

Sciurus vulgaris, Glis glis

vector of tularemia, tick-borne encephalitis, brucellosis, leptospirosis

Russia

[13][101]

Slovakia

[126]

Hirstionyssus gliricolus Masan and Ambros, 2010

E

Glis glis

—

Slovakia

[126]

Hirstionyssus paulisimilis Masan and Fenda, 2010

E

Glis glis

—

Slovakia

[126]

Hirstionyssus sunci Wang, 1962

P

small rodents, insectivores

cause human dermatitis

Slovakia

[126]

Family Glycyphagidae

Labidophorus talpae Kramer, 1877

E

moles

—

Europe

[127]

Family Ixodidae

Ixodes (Ixodes) ricinus (Linnaeus, 1758)

P

mammals, birds

vector of louping-ill virus of sheep, Lyme disease, ehrlichiosis (tick-borne fever) of cattle; transmits Babesia spp., which causes Redwater fever in cattle and sheep

Russia

[52]

Moldova

[73]

Ukraine

[98][110]

Germany

[35][37][128][129]

Belarus

[125]

Ixodes (Ixodes) acuminatus Neumann, 1901 (syn. I. redikorzevi Olenev, 1927)

P

rodents, insectivores, carnivores

vector of LD, tularemia, Q fever

Europe

[130]

Ixodes (Ixodes) laguri Olenev, 1929 (syn.: I. laguri colchicus Pomerantzev, 1948)

P

small rodents, hedgehogs, small carnivores

vector of plague and tularemia

Russia

[52][131][132]

Ixodes (Exopalpiger) trianguliceps Birula, 1895

P

rodents, insectivores, carnivores

vector of LD

Ukraine

[98][110]

Germany

[129]

Family Amblyommidae

Dermacentor marginatus (Sulzer, 1776)

P

mammals, insectivores, small carnivores

vector of tick-borne Russian spring–summer encephalitis (TBRSSE), North Asian tick typhus

Croatia

[133]

Family Bdellidae

Bdella muscorum Ewing, 1909

H

small mammals

—

Bulgaria

[134]

Cyta latirostris (Hermann, 1804)

C

small mammals

—

Bulgaria

[134]

Cyta coerulipes (Duges, 1834)

C

small mammals

—

Bulgaria

[134]

Family Myocoptidae

Gliricoptes glirinus (Canestrini, 1895) (syn.: Myocoptes glirinus Can. 1895)

WP

Glis glis

—

Germany

[107][135]

Italy

[136][137]

France

[136][137]

Belgium

[138]

Armenia

[137][139]

Russia

[140]

UK

[135]

Family Myobiidae

Radfordia (Graphiurobia) gliricola Vesmanis and Lukoschus, 1978

WP

Glis glis

—

Germany

[141]

Russia

[142]

Family Trombiculidae

Ascoschoengastia latyshevi (Schluger, 1955)

P

rodents, insectivores, birds

—

Europe

[143]

Leptotrombidium europaeum (Daniel and Brelih, 1959) (syn.: Leptotrombidium intermedia europaea Daniel and Brelih, 1959

P

rodents, insectivores

vector of rickettsiosis tsutsugamushi

former Czechoslovakia, former Yugoslavia, Bulgaria, Albania, Spain

[144]

Leptotrombidium sylvaticum Hushcha and Schluger, 1967

P

rodents, insectivores

vector of rickettsiosis tsutsugamushi

Ukraine

[110][145]

Miyatrombicula muris (Oudemans, 1910)

E

rodents, insectivores

—

Central and South Europe, Russia

[143]

Neotrombicula vernalis (Willmann, 1942)

WP

rodents, insectivores

vector of rickettsiosis tsutsugamushi

Austria

[144]

Neotrombicula austriaca Kepka, 1964

E

rodents, insectivores

vector of rickettsiosis tsutsugamushi

Bulgaria, Moldova

[143]

Neotrombicula inopinata (Oudemans, 1909) (syn.: N. germanica Willmann, 1952; N. autumnalis germanica (Willmann, 1952)

WP

rodents, insectivores, birds

vector of rickettsiosis tsutsugamushi, cause human trombiculiasis

Germany

[107][143]

Ukraine

[143][145]

Neotrombicula japonica (Tanaka, Kaiwa, Teramura & Kagaya, 1930) (syn.: Trombicula dubinini Schluger, 1955)

P

rodents, insectivores

vector of rickettsiosis tsutsugamushi

Ukraine

[110][143]

Neotrombicula nagayoi Sasa, Hayashi, Sato, Miura and Asahima, 1950

P

rodents

vector of rickettsiosis tsutsugamushi

Moldova

[73][146]

Neotrombicula vulgaris (Schluger, 1955)

E

rodents

vector of rickettsiosis tsutsugamushi

Ukraine

[110]

Hirsutiella zachvatkini (Schluger, 1948) (syn.: Trombicula zachvatkini Schluger, 1948; Neotrombicula zachvatkini)

P

rodents

vector of diseases causes by Rickettsia spp.

Moldova

[73][74]

Ukraine

[110][143][145]

Russia

[13][101]

Schoutedenichia sp.

P

—

—

Moldova

[73]

Note: E—Europe, C—Cosmopolitan, H—Holarctic, P—Palaearctic, WP—Western Palaearctic, G—Greenland, I—Iran, N—Nearctic.

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