Microtus agrestis
Microtus agrestis (Linnaeus, 1761) Field Vole Mus agrestis Linnaeus, 1761:11. Type locality “Svecia [= Sweden],” Uppsala. Mus gregarius Linnaeus, 1766:84. Type locality “ Germania, Svecia [= Germany and Sweden],” East Prussia. Mus arvalis nigricans Kerr, 1792:239. Replacement name for Mus agrestis L...
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| Summary: | Microtus agrestis (Linnaeus, 1761) Field Vole Mus agrestis Linnaeus, 1761:11. Type locality “Svecia [= Sweden],” Uppsala. Mus gregarius Linnaeus, 1766:84. Type locality “ Germania, Svecia [= Germany and Sweden],” East Prussia. Mus arvalis nigricans Kerr, 1792:239. Replacement name for Mus agrestis Linnaeus, 1761. Arvicola hirta Bellamy, 1839:373. Type locality “Yealmpton,” Devonshire, England. Arv. [ icola ] Bailloni de Sélys Longchamps, 1841:225. Type locality “Abita il Nord della Francia e della Svizzera [=Inhabits the North of France and Switzerland.” Arvicola neglecta Jenyns, 1841:270. Type locality “Megarnie Castle in Perthshire,” Scotland. Arvicola levernedii Crespon, 1844:73. Type locality “entre St-Gilles et Aiguesmortes [= between St. Gilles and Aiguesmortes],” Gard, France. Lemmus insularis Nilsson, 1844:34. Type locality “Ostgötha, skärgård,” Sweden. A. [ rvicola ] britannicus de Sélys Longchamps, 1847:307. Type locality “L’Angleterre et l’Écosse [= England and Scotland].” Arvicola rozianus Bocage, 1865:7. Type locality “ Coimbra, no sitio da Geria,[= Coimbra, county of Geria],” Portugal. Arvicola agrestis var. nigra Fatio, 1869:241. Type locality “près d’Engstlen [= vicinity of Engstlen],” Berne, Switzerland. [ Arvicola agrestis var. ] rufa Fatio, 1900:472. Type locality “dans les Alpes savoisiennes, frontière du Valais, et dans les Alpes vaudoises (aux plans de Frenières),” Geneva, Switzerland. Arvicola agrestis angustifrons Fatio, 1905:191. Type locality “près de Zermatt, entre 1620 et 1700 m. s/m., en Valais [= near Zermatt between 1,620 and 1,700 meters in Valais],” Switzerland. Arvicola agrestis latifrons Fatio, 1905:194. Type locality “sur quelques points en Suisse, dans les bois de Veyrier, près de Geneve; entre autres et dans les environs de Lucerne [= at some points in Switzerland, in the woods of Veyrier near Geneva; including in and around Lucerne].” Microtus agrestis exsul Miller, 1908:201. Type locality “North Uist, Hebrides,” Scotland. Microtus agrestis insul Lydekker, 1909:74. Incorrect subsequent spelling of Lemmus insularis Nilsson, 1844. Microtus agrestis mongol Thomas, 1911:759. Type locality “Kemtchik Valley, Tannu-ola Mts., N.W. Mongolia.” Microtus agrestis arcturus Thomas, 1912:398. Type locality “Barlik Mts. S., N.W. Dzungaria,” China. Microtus agrestis mial Barrett-Hamilton and Hinton, 1913a:364. Type locality “Eigg, Inner Hebrides,” Scotland. Microtus agrestis luch Barrett-Hamilton and Hinton, 1913a:366. Type locality “Muck, Inner Hebrides,” Scotland. Microtus agrestis macgillivrayii Barrett-Hamilton and Hinton, 1913b:831. Type locality “Islay,” Inner Hebrides, Scotland. Microtus agrestis fiona Montagu, 1922:940. Type locality “Gigha,” Inner Hebrides, Scotland. Microtus agrestis punctus Montagu, 1923:868. Type locality “ Bled, Slovenia.” Microtus hirtus orioecus Cabrera, 1924:8. Type locality “Molins, Montseny, Prov. Gerona,” Spain. Microtus agrestis pannonicus Ehik, 1924:76. Type locality “Orman, near Komarviros County Zala, Hungary.” Microtus agrestis tridentinus Dal Piaz, 1924:10. Type locality “Brennero, Alto Adige, 1400 m s/m,” Italy. Microtus agrestis estiae Reinwaldt, 1927:13. Type locality “Inseln Villsandi und Abruka, [= Villsandi and Abruka Islands],” Estonia. Microtus agrestis Wettsteini Ehik, 1928:197. Type locality “Ob. Trixen, Karintia [= Carinthia],” Austria. Microtus agrestis ognevi Skalon, 1935:11. Type locality “Церковенское на р. Таз [=Tserkovenskoe on Taz River],” northwestern Siberia. Microtus agrestis pallida Melander, 1938:74. Type locality “Смоленская обл, Ельнинский р- н. [= Elninsky department of Smolensk province, near vill. Miloje],” Russia. Microtus agrestis argyropoli Ognev, 1944:179. Type locality “South Urals, Valley of Inzer River,” Russia. Microtus agrestis scaloni Heptner, 1948:710. Replacement name for Microtus agrestis ognevi Skalon, 1935. Microtus agrestis argyropuli Ognev, 1950: Replacement name for Microtus agrestis argyropoli Ognev, 1944. Microtus agrestis carinthiacus Kretzoi, 1958:57. Replacement name for M. a. wettsteini Ehik, 1928. Microtus agrestis enez-groezi Heim de Balsac and de Beaufort, 1966:638. Type locality “Groix (= Morbihan),” France. Microtus agrestis armoricanus Heim de Balsac and de Beaufort, 1966:638. Type locality “environs de Quimper (= Finistère),” France. CONTEXT AND CONTENT. Order Rodentia, suborder Myomorpha, superfamily Muroidea, family Cricetidae, subfamilyArvicolinae, genus Microtus , subgenus Microtus . There remains some uncertainty concerning valid subspecies. Musser and Carleton (2005) list the above 39 named forms of Microtus agrestis without reference to subspecies. NOMENCLATURAL NOTES. Microtus agrestis and the Nearctic M. pennsylvanicus are similar morphologically (Klimkiewicz 1970). However, this similarity represents convergence, not a phylogenetic relationship (Krapp and Niethammer 1982; Musser and Carleton 2005). Phylogenetic analyses based both on karyotypes (Modi 1987) and DNA sequences of the entire cytochrome -b gene (Conroy and Cook 2000; Jaarola et al. 2004) clearly show that M. agrestis and M. pennsylvanicus are separate species. The European populations of M. agrestis are differentiated as 3 evolutionary units that may represent cryptic species (Kryštufek et al. 2008; Paupério et al. 2012). The generic name Microtus is a combination of 2 Greek words, micros for small and ous for ear, and the specific epithet agrestis is a Latin word meaning “of the field.” Vernacular names assigned to M. agrestis include common field vole, grass mouse, short-tailed vole, dark vole, blackish meadow mouse, and shorttailed field mouse (Alibhai and Gipps 1991; MacDonald and Barrett 1993; Kryštufek et al. 2008). DIAGNOSIS Juvenile Microtus agrestis , the common vole ( M. arvalis ), the root vole ( M. oeconomus ), and the East European vole ( M. levis —formerly M. rossiaermeridonalis ) are virtually indistinguishable by gross morphology (Nekrutenko et al. 2000). Representational difference analysis was used to isolate species-specific markers—Mag3 for M. agrestis and Moe1 for M. oeconomus (Nekrutenko et al. 2000). Using these sequences, species-specific polymerase chain reaction (PCR) primers produced unique amplification products that were able to distinguish between these 2 species. Microtus agrestis (Fig. 1) can be characterized by its pelage, rather long, shaggy, grayish brown, often tinged with russet and by its bicolored tail with dark dorsal fur. Tail length is about one-third the length of head and body. Only M. duodecimcostatus and M. lusitanicus have shorter tail lengths. These characters of M. agrestis combined with some or all (depending on which comparison is being made) of the following are diagnostic of the species: skull moderately broad, with width> one-half the length; width of interorbital constriction> 3.3 mm; M2 with 3 inner ridges ≤ 5 fields: an anterior loop, 2 outer and 1 inner closed triangles, a character absent in other European vole species, and a 5th field in a postero-internal position; M3 with 5 fields: an anterior loop, 3 closed triangles, and a long terminal loop rarely simplex; m1 with ≥ 7 fields and 4 outer ridges on the outer side; m3 with 3 transverse fields; length of upper molar toothrow never> 7 mm; foramen mandibulare usually lying over protuberance of lower incisor (Miller 1912; Ellerman 1940; Reichstein 1959; Saint-Girons 1973; Corbet 1978; Krapp and Niethammer 1982). Microtus agrestis is very similar to M. arvalis , but the latter can be distinguished by its pelage that is more yellowishbrown and its slightly smaller size (body length of M . arvalis 90–120 mm, body weight 14–40 g—Krapp and Niethammer 1982; MacDonald and Barrett 1993). Hairs inserted near the base of the ear are shorter in M. arvalis than M. agrestis (Dienske 1969). The asynaptic X and Y chromosomes of M. agrestis contain additional, nonobligatory heterochromatic blocks not found in another species of asynaptic vole, the Mediterranean pine vole ( M. duodecimcostatus ) as addressed by Borodin et al. (1995). GENERAL CHARACTERS General form of Microtus agrestis is robust with a large head (broad posteriorly), short and rounded ears, small eyes with diameter of 3.1–3.8 mm (Krapp and Niethammer 1982), and blunt snout. Mouth is small with upper incisors projecting very slightly. Tail is scantily covered with hair and has as many as 20 visible rings per cm near middle (Miller 1912; Krapp and Niethammer 1982). Ears are mostly covered by fur; meatal lobe (length) is frequently> l mm though <2 mm (Dienske 1969). General color of dorsum varies from dark gray-brown to chestnut-brown, with underparts pure gray or pale brown (Corbet and Harris 1991; MacDonald and Barrett 1993; Mathias 1999). Juveniles are darker than adults. M. agrestis has 2 pairs of pectoral and 2 pairs of inguinal mammae. Hind feet have 6 plantar pads, whereas forefeet have 5 palmar pads and inner digit is reduced to a minute tubercle (Miller 1912). Dorsal profile of skull is moderately convex. Condyles are visible in dorsal view due to forward projection of occiput (Fig. 2). In older animals, outer edges of parietals have welldeveloped longitudinal ridges that are continuous posteriorly with lambdoidal crest and which come together abruptly anteriorly to join interorbital ridge (Miller 1912). Auditory bullae are large and evenly inflated. Interorbital region is narrow, subcylindrical, and has distinct temporal ridges, which can unite to form a definite median crest extending well forward to nasals (Magalhães and Madureira 1980). Nasals are broad anteriorly and abruptly narrow at middle; posterior end is pointed, blunt, or angular. Incisive foramen is long and narrow, extending approximately to molar alveoli. Well-developed postorbital processes are present (Magalhães and Madureira 1980). Posterior edge of foramen mandibulare is about 0.5 mm from posterior edge of mandible (Dienske 1969; Fedyk and Ruprecht 1971). Mandible is robust and masseteric ridge is well developed. Lower incisors are much less strongly curved than upper incisors. Molar teeth are open-rooted throughout life, decreasing in size posteriorly. A postero-internal loop is present in M1, similar to that in M2; this is a frequent character in some populations (morphotype exsul — Miller 1912; Ognev 1950; Niethammer 1964; Reichstein and Reise 1965; Reichstein 1966; Meylan 1967; Almaça 1993; Yalden 1999). An 8th field in an anterior position can also occur in M1 (Dienske 1969; Magalhães and Madureira 1980). Marked geographical variation is found in size and color patterns of M. agrestis . M . agrestis from northern Europe (Scotland, Scandinavia, northern Russia), the Alps, and Camargue (France) are larger than those from central Europe (Krapp and Niethammer 1982). In England (Alibhai and Gipps 1991) and Sweden (Hansson and Jaarola 1989) size increases from south to north. Size also varies with elevation; larger M . agrestis are present at higher elevations in the area that was formerly Czechoslovakia (Krapp and Niethammer 1982) and in France and Portugal (Almaça 1993). Individuals with darker dorsal pelage occur in Scandinavia and Scotland, and individuals with lighter pelage are found in central Europe, southern England, and northernmost Scandinavia (Corbet and Southern 1977; Krapp and Niethammer 1982). Microtus agrestis males average slightly larger than females in external and cranial measurements in some populations (Reichstein 1959; Krapp and Niethammer 1982), but exhibit little or no secondary sexual variation in size in other populations (Wasilewski 1956; Gebczynska 1964; Saint-Girons 1973; Alibhai and Gipps 1991). Selected ranges of external and cranial measurements (mm; sexes combined) for adult M. agrestis from England (E, n = 38–46), France (F, n = 51–93), the Netherlands (N, n = 58), Switzerland (S, n = 17), and Portugal (P, n = 3–33) were: length of body, 115.0–121.0 (E), 85.0–130.0 (F), 78.0– 123.0 (S); length of tail, 25.0–46.0 (F), 29.5–46.0 (S); length of hind foot, 17.0–17.4 (E), 15.0–21.0 (F), 17.0–20.0 (S); length of ear, 9.0–14.0 (F), 10.0–13.0 (S); condylobasal length, 25.2–26.1 (E), 22.8–27.9 (F), 24.1–27.4 (S), 24.7–25.9 (P); zygomatic breadth, 12.1–15.7 (F), 12.1–16.1 (S), 12.6–14.1 (P); width of interorbital constriction, 3.1–3.9 (F), 3.3–3.8 (S), 2.3–3.2 (P); length of nasals, 5.5–7.8 (S), 5.9–7.0 (P); palatal length, 10.6– 15.0 (N); length of maxillary toothrow, 5.3–6.9 (F), 4.5–6.9 (N), 5.4–6.7 (S), 5.0–6.3 (P); length of mandibular toothrow, 5.2–6.7 (F), 5.4–6.6 (S), 5.0–5.8 (P); length of mandible, 12.4–17.0 (N), 14.0–17.3 (S), 13.6–15.9 (P—Dienske 1969; Saint-Girons 1973; Magalhães and Madureira 1980; Krapp and Niethammer 1982; Alibhai and Gipps 1991). Ranges of cranial measurements (mm; sexes combined) of 26 M. a. levernedii (l) from Switzerland and France (Madureira 1983), 13 M. a. agrestis (a) from Norway and Sweden (Miller 1912), and 3 M. a. neglectus (n) from Scotland (Miller 1912) were: condylobasal length, 26.6–28.4 (a), 25.0–25.4 (n); zygomatic breadth, 15.2–16.8 (a), 14.4–14.4 (n); width of interorbital constriction, 2.6–3.3 (l), 3.4–4.0 (a), 3.2–3.4 (n); width of postorbital constriction, 3.3–3.7 (l); nasal length, 7.2–8.0 (a), 6.8– 7.0 (n); palatal width, 1.5–1.8 (l); length of maxillary toothrow, 6.4–7.0 (a), 6.4–6.6 (n); length of mandibular toothrow, 6.2–6.8 (a), 6.2–6.4 (n); length of mandible, 14.9–17.6 (l), 16.8–18.0 (a), 15.4–16.2.(n). Cranial measurements (mm) of the type specimens of M. a. levernedii from Gard, France (female), and M. a. nigra (or niger ) from Berne (Geneva), Switzerland (male), respectively, were: condylobasal length, 28.0, 26.0; zygomatic breadth, 16.0, 14.8; width of interorbital constriction, 3.6, 3.4; nasal length, 8.0, 7.2; length of maxillary toothrow, 7.2, 6.4; length of mandibular toothrow, 7.0, 6.4; mandible length, 18.0, 16.6 (Miller 1912). Ranges of body and cranial measurements from specimens collected in Europe were: length of head and body, 78–135 mm; length of tail, 18–49 mm (ca. 30% head-body length); length of hind foot, 16–20.5 mm, body mass 14–50 g (birth mass ca. 2 g); condylobasal length, 23–29 mm (sample sizes not given—MacDonald and Barrett 1993). Ranges of body measurements for individuals collected in Spain were: head and body length, 95–123 mm; length of tail, 25–44 mm; length of hind foot, 16–21 mm, mass 21–41 g (sample sizes not given— Gosalbez and Luque-Larena 2002). Mean measurements (mm ± SD ) for footprints of 25 M. agrestis were: forefoot print, 7.0 ± 0.7 in width and 7.6 ± 0.5 in length; hind foot print, 7.0 ± 1.0 in width and 9.1 ± 0.8 in length (van Apeldoorn et al. 1993). Baculae (os penis) measurements (mm) of 2 adult males were: corpus length, 3.5, 3.2; basal width, 0.5, 0.4 (Didier 1954). DISTRIBUTION Distribution of Microtus agrestis (Fig. 3) in northern and central Europe extends from Scandinavia to the Alps, Pyrenees, Galicia, and northern Portugal and from England, Scotland, and nearby small islands eastward to former Yugoslavia, southern Urals, Altai Mountains (Mongolia), northwest China, and Lake Baikal (Russia) regions (Miller 1912; Ognev 1944; Corbet 1978; Krapp and Niethammer 1982; Brunet-Lecomte 1991; Gromov and Plyakov 1992; Mitchell-Jones et al. 1999; Musser and Carleton 2005). The species is absent from Iceland and Ireland (Kryštufek et al. 2008). The morphotype M. a. exsul comprises over 50% of specimens taken from the northern area of Russia, Scandinavia, and Scotland. In central Europe, the M. a. exsul type decreases to about 5%, and in southern Europe and the Alps, it never exceeds 20% of specimens collected (Krapp and Niethammer 1982). FOSSIL RECORD The 1st known fossil remains of Microtus agrestis are from the Upper Pleistocene of Europe (Kurtén 1968). Earlier records are mostly presented as the “ arvalis-agrestis ” group because these 2 species are only differentiated by M2, missing in most of the materials found. In the British Isles, M. agrestis is present from the Cromerian interglacial and Wolstonian period (penultimate glaciation) but never reached Ireland (Alibhai and Gipps 1991; Yalden 1999). Subfossil teeth collected from the island of Jura, Inner Hebrides, between 1,500 and 2,500 years ago, show a progressive simplification of the M1 pattern since that time (Corbet 1975). The M. agrestis group (including M. agrestoides ) was present in the Middle Terrace stage, then absent until the Iglitham stage of the Late Pleistocene (Hinton 1926). Two geochronological forms from France were M. agrestis jansoni with larger size measurements of M 1 in the Middle Pleistocene and M. agrestis aubinensis with smaller size measurement values of M 1 in the Upper Pleistocene (Chaline 1972). In Portugal, M. agrestis is found in Upper Pleistocene deposits of Caldeirão Cave in the center of the country (Póvoas et al. 1992). In southern Poland, fossil remains of M. agrestis indicate that the species was present during the entire late Quaternary, including the Last Glacial Maximum (Nadachowski 1984, 1989, 2001). Other fossils of M. agrestis are reported from Germany, Austria, Hungary, and Bulgaria (Chaline 1972, 1974; Krapp and Niethammer 1982; Nadachowski 1984; Kolfschoten 1994), Hungary (Jánossy 1986), southern Italy (Capasso-Barbato and Gliozzi 2001), and Eastern Europe including the : Published as part of Mathias, Maria Da Luz, Hart, E. Blake, Ramalhinho, Maria Da Graca & Jaarola, Maarit, 2017, Microtus agrestis (Rodentia: Cricetidae), pp. 23-39 in Mammalian Species 49 (944) on pages 23-34, DOI: 10.1093/mspecies/sex003, http://zenodo.org/record/4683692 : {"references": ["LINNAEUS, C. 1761. Fauna Suecica. 2 nd ed. Laurentii Salvii, Stockholm, Sweden.", "LINNAEUS, C. 1766. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Edition duodecima, reformata. Laurentii Salvii, Stockholm, Sweden.", "KERR, R. 1792. The animal kingdom, or zoological system, of the celebrated Sir Charles Linnaeus; Class I. 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