Wood mice of the genus Apodemus are an essential component of small mammal communities throughout Europe. Molecular data suggest the postglacial colonization of current ranges from south European glacial refugia, different in particular species. Yet, details on the course of colonization and Holocene history of particular species are not available, partly because of a lack of reliable criteria for species identification in the fossil record. Using a sample of extant species, we analyzed variation patterns and between-species overlaps for a large set of metric and non-metric dental variables and established the criteria enabling the reliable species identification of fragmentary fossil material. The corresponding biometrical analyses were undertaken with fossil material of the genus (2528 items, 747 MNI) from 22 continuous sedimentary series in the Czech Republic and Slovakia, from LGM to Recent. In Central Europe, the genus is invariantly absent in LGM assemblages but regularly appears during the Late Vistulian. All the earliest records belong to A. flavicollis, the species clearly predominating in the fossil record until the Late Holocene. A. uralensis accompanied it in all regions until the late Boreal when disappeared from the fossil record (except for Pannonia). A few items identified as A. sylvaticus had already appeared in the early Holocene assemblages, first in the western part of the region, yet the regular appearance of the species is mostly in the post-Neolithic age. A. agrarius appeared sparsely from the Boreal with a maximum frequency during the post-Neolithic period. The results conform well to the picture suggested by molecular phylogeography but demonstrate considerable differences among particular species in dynamic of the range colonization. Further details concerning Holocene paleobiogeography of individual species in the medium latitude Europe are discussed.

Department of Zoology Charles University Viničná 7 Praha 2 Czech Republic

Zobrazit více v PubMed

Niethammer J. Apodemus flavicollis–Gelbhalsmaus, Apodemus sylvaticus–Waldmaus In: Niethammer J, Krapp F, editors. Handbuch der Säugetiere Europas. Vol. 1 Wiesbaden: Akademische Verlagsgessellschaft; 1978. pp. 325–358.

Martín-Suárez E, Mein P. Revision of the genera Parapodemus, Apodemus, Rhagamys and Rhagapodemus (Rodentia, Mammalia). Geobios 1998; 31: 87–97.

Freudenthal M, Martín-Suárez E. Family Muridae In: Rössner GE, Heissig K, editors. The Miocene land mammals of Europe. München: Verlag Dr. Friedrich Pfeil; 1999. pp. 401–409.

Musser GG, Brothers EM, Carleton MD, Hutterer R. Taxonomy and distributional records of Oriental and European Apodemus, with a review of the Apodemus—Sylvaemus problem. Bonn Zool Beitr. 1996; 46: 143–190.

Musser GG, Carleton MD. Superfamily Muroidea In: Wilson DE, Reeder DM, editors. Mammal species of the world: a taxonomic and geographic reference. 3rd ed. Baltimore: Johns Hopkins University Press; 2005. pp. 894–1531.

Serizawa K, Suzuki H, Tsuchiya K. A phylogenetic view on species radiation in Apodemus inferred from variation of nuclear and mitochondrial genes. Biochem Genet. 2000; 38: 27–40. PubMed

Suzuki H, Sato JJ, Tsuchiya K, Luo J, Zhang YP, Wang YX, Jiang XL. Molecular phylogeny of wood mice (Apodemus, Muridae) in East Asia. Biol J Linn Soc Lond. 2003; 80: 469–481.

Suzuki H, Filipucci MG, Chelomina GN, Sato JJ, Serizawa K, Nevo E. A biogeographic view of Apodemus in Asia and Europe inferred from nuclear and mitochondrial gene sequence. Biochem Genet. 2008; 46: 329–346. 10.1007/s10528-008-9149-7 PubMed DOI

Liu X, Wei F, Li M, Jiang X, Feng Z, Hu J. Molecular phylogeny and taxonomy of wood mice (genus Apodemus Kaup, 1829) based on complete mt DNA cytochrome b sequences, with emphasis on Chinese species. Mol Phylogenet Evo. 2004; 33: 1–15. PubMed

Dam JA van (1997) The small mammals from the upper Miocene of the Teruel-Alfambra region (Spain): paleobiology and paleoclimatic recontructions. Geol Ultraiectina. 1997; 156: 1–204.

Horáček I, Knitlová M, Wagner J, Kordos L, Nadachowski A. Late Cenozoic history of the genus Micromys (Mammalia, Rodentia) in Central Europe. PLoS ONE. 2013; 8: e62498 10.1371/journal.pone.0062498 PubMed DOI PMC

Bellinvia E, Munclinger P, Flegr J. Application of the RAPD technique for a study of the phylogenetic relationships among eight species of the genus Apodemus. Folia Zool. 1999; 48: 241–248.

Filippucci MG, Macholán M, Michaux JR. Genetic variation and evolution in the genus Apodemus (Muridae: Rodentia). Biol J Linn Soc Lond. 2002; 75: 395–419.

Michaux JR, Chevret P, Filippucci MG, Macholán M. Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12S rRNA. Mol Phylogenet Evol. 2002; 23: 123–136. 10.1016/S1055-7903(02)00007-6 PubMed DOI

Bellinvia E. A phylogenetic study of the genus Apodemus by sequencing the mitochondrial DNA control region. J Zool Syst Evol Res. 2004; 42: 1–9.

Zachos J, Pagani M, Sloan L, Thomas E, Billups K. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science. 2001; 292: 686–693. 10.1126/science.1059412 PubMed DOI

Kowalski K. Pleistocene rodents of Europe. Folia Quarternaria. 2001; 72: 1–389.

Horáček I, Ložek V. Palaeozoology and the Mid-European Quaternary past: scope of the approach and selected results. Rozpravy ČSAV, řada MPV. 1988; 98: 1–106.

Filippucci MG, Storch G, Macholán M. Taxonomy of the genus Sylvaemus in western Anatolia—morphological and electrophoretic evidence (Mammalia: Rodentia: Muridae). Senckenb Biol. 1996; 75: 1–14.

Reutter BA, Hausser J, Vogel P. Discriminant analysis of skull morphometric characters in Apodemus sylvaticus, A. flavicollis, and A. alpicola (Mammalia; Rodentia) from the Alps. Acta Theriol. 1999; 44: 299–308.

Frynta D, Mikulová P (2001) Discriminant analysis of morphometric characters in four species of Apodemus (Muridae: Rodentia) from Eastern Turkey and Iran. Isr J Zool. 2001; 47: 243–258.

Spitzenberger F. Die Säugetierfauna Österreichs. Bundesministerium für Land- und Forstwirtschaft. Wien: Umwelt und Wasserwirtschaft; 2001.

Barčiová L, Macholán M. Morphometric key for the discrimination of two wood mice species, Apodemus sylvaticus and A. flavicollis. Acta Zool Academ Sci Hung. 2009; 55: 31–38.

Jojic V, Blagojevic J, Vujosevic M. Two-module organization of the mandible in the yellow-necked mouse: a comparison between two different morphometric approaches. J Evol Biol. 2012; 25: 2489–2500. 10.1111/j.1420-9101.2012.02612.x PubMed DOI

Ancillotto L, Mori E, Sozio G, Solano E, Bertolino S, Russo D (2016) A novel approach to field identification of cryptic Apodemus wood mice: calls differ more than morphology. Mamm Rev. 2016;

Heinrich WD, Maul L. Skelettreste von Nagetieren (Rodentia, Mammalia) aus dem fossilen Tierbautensystem vin Piesede bei Malchin. Teil 1. Taxonomische und biometriche Kennzeichung des Fundgutes. Wiss Z Humboldt Univ Berl Math Naturwiss. 1983. a; 32: 729–743.

Heinrich WD, Maul L. Skelettreste von Nagetieren (Rodentia, Mammalia) aus dem fossilen Tierbautensystem vin Piesede bei Malchin. Teil 2. Paläoökologische und faunengeschichtliche Auswertung des Fundgutes. Wiss Z Humboldt Univ Berl Math Naturwiss. 1983b; 32: 45–752.

Libois R, Michaux JR, Ramalhinho MG, Maurois C, Sara M. On the origin and systematics of the northern African wood mouse (Apodemus sylvaticus) populations: a comparative study of mtDNA restriction patterns. Can J Zool. 2001; 79: 1503–1511.

Michaux JR, Magnanou E, Paradis E, Nieberding C, Libois R. Mitochondrial phylogeography of the woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Mol Ecol. 2003; 12: 685–697. PubMed

Michaux JR, Libois R, Paradis E, Filippucci MG. Phylogeographic history of the yellow-necked fieldmouse (Apodemus flavicollis) in Europe and in the Near and Middle East. Mol Phylogenet Evol. 2004; 32: 788–789. 10.1016/j.ympev.2004.02.018 PubMed DOI

Michaux JR, Libois R, Filippucci MG. So close and so different: comparative phylogeography of two small mammal species, the yellow-necked fieldmouse (Apodemus flavicollis) and the woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Heredity (Edinb). 2005; 94: 52–63. PubMed

Kryštufek B, Vohralík V. Distribution of field mice (Apodemus) (Mammalia: Rodentia) in Anatolia. Zool Middle East. 2007; 42: 25–36.

Kryštufek B, Vohralík V. Mammals of Turkey and Cyprus. Rodentia II: Cricetinae, Muridae, Spalacidae, Calomyscidae, Capromyidae, Hystricidae, Castoridae. Koper: University of Primorska, Science and Research Centre Koper; 2009.

Vohralík V (2002) Distribution, skull morphometrics and systematic status of an isolated population of Apodemus microps (Mammalia: Rodentia) in NW Bohemia, Czech Republic. Acta Soc Zool Bohem. 2002; 66: 67–80.

Ložek V. Quartärmollusken der Tschechoslowakei. Rozpravy ústředního ústavu geologického. 1964; 31: 1–374.

Ložek V. Faunengeschichtliche Grundlinien zur spät- und nacheiszeitlichen Entwicklung der Molluskenbestände in Mitteleuropa. Rozpr Ces Akad Ved Umeni Trida II Mat Prirodoved. 1982; 92: 1–106.

Walker MJC, Berkelhammer M, Björck S, Cwynar LC, Fisher DA, Long AJ et al. Formal subdivision of the Holocene Series/Epoch: a Discussion Paper by a Working Group of INTIMATE (Integration of ice-core, marine and terrestrial records) and the Subcommission on Quaternary Stratigraphy (International Commission on Stratigraphy). J Quat Sci. 2012; 27: 649–659

Horáček I, Ložek V, Svoboda J, Šajnerová A. Environment and the settlement of karst in the Late Palaeolithic and Mesolithic In: Svoboda J, editor. Praehistoric Caves: Catalogues, Documents, Studies. Brno: Institute of Archaeology of the Czech Academy of Sciences; 2002. pp. 313–354. (in Czech, with an abstract in English).

Horáček I. Holocene history of the mammalian fauna in the Northern Bohemian sandstone region (Czech Republic) In: Cílek V, Härtel H, Herben T, Jackson A, Rendel W, editors. Sandstone Landscapes. Prague: Academia; 2007. pp. 265–272.

Horáčková J, Ložek V, Juřičková L. List of malacologically treated Holocene sites with brief review of palaeomalacological research in the Czech and Slovak Republics. Quat Int. 2014; 357: 207–211.

Jánossy D, Kordos L. Pleistocene-Holocene mollusc and vertebrate fauna of two caves in Hungary. Annls hist-nat Mus natn hung. 1976; 68: 5–29.

Kordos L. A sketch of the vertebrate biostratigraphy of the Hungarian Holocene. Földr Közl. 1977; 25: 144–160.

Jánossy D. Pleistocene vertebrate faunas of Hungary Amsterdam: Elsevier; 1986.

Pazonyi P. Mammalian ecosystem dynamics in the Carpathian Basin during the last 27,000 years. Palaeogeogr Palaeoclimatol Palaeoecol. 2004; 212: 295–314.

Herman JS, Jóhannesdóttir F, Jones EP, McDevitt AD, Michaux JR, White TA, et al. Post-glacial colonization of Europe by the wood mouse, Apodemus sylvaticus: evidence of a northern refugium and dispersal with humans. Biol J Linn Soc Lond. 2016;

Storch G. VI. Jungpleistozäne Kleinsäugerfunde (Mammalia: Insectivora, Chiroptera, Rodentia) aus der Brillenhöhle In: Riek G, editor) Das Paläolithikum der Brillenhöle bei Blaubeuren (Schwäbische Alb), Teil II: Die jungpleistozänen Tierknochenfunde aus der Brillenhöhle. Stuttgart: Verlag Müller and Graff; 1973. pp. 106–123.

Storch G. Die Pleistozän-Holozän-Grenze in der Kleinsäugerfauna Deutschlands. Z Saugetierkd. 1974; 39: 84–97.

Storch G. Kleinsäugerfunde (Mammalia) aus der mesolitischen Kulturschit unter dem Felsdach Inzigkofen im oberen Donautal. In: Taute W, editor. Das Mesolithikum in Süddeutschland. Teil 2: Naturwissenschafliche Untersuchungen, Tübinger Monographien zur Urgeschichte. 1978a; 5: 131–132.

Storch G. Paläolithische und mesolithische Kleinsäugerfunde (Mammalia) von den Fohlenhaus-Höhlen im Lonetal (Schwäbische Alb). In: Taute W, editor. Das Mesolithikum in Süddeutschland. Teil 2: Naturwissenschafliche Untersuchungen. Tübinger Monographien zur Urgeschichte. 1978b; 5: 133–138.

Storch G. Das spätglaziale und frühholozäne Kleinsäuger-Profil vom Felsdach Felsställe in Mühlen bei Ehingen, Alb-Donau-Kreis. In: Kind CJ, editor. Das Felsställe. Eine jungpaläolithisch-frühmesolithische Abri-Station bei Ehingen-Mühlen, Alb-Donau-Kreis. Die Grabungen 1975–1980. Forschungen und Berichte zur Vor- und Frühgeschichte in Baden-Württemberg. 1987; 23: 275–285.

Storch G. Local differentiation of faunal change at the Pleistocene-Holocene boundary. Cour Forsch-Inst Senckenberg. 1992; 153: 135–142.

Fahlke JM. Der Austausch der terrestrischen Säugetierfauna an der Pleistozän / Holozän-Grenze in Mitteleuropa. PhD. Thesis, Rheinischen Friedrich-Wilhelms-Universität Bonn. 2009. Available from: http://hss.ulb.uni-bonn.de/2009/1836/1836-1.pdf

Steiner HM. Untersuchen über die Variabilität und Bionomie der Gattung Apodemus (Muridae, Mammalia) der Donau-Auen von Stockerau (Niederösterreich). Z Wiss Zool. 1968; 177: 1–94.

Vogel P. Apodemus sylvaticus (L., 1758), Apodemus flavicollis (Melchior, 1834), Apodemus alpicola Heinrich, 1952 In: Hausser J, editor. Säugetiere der Schweiz—Verbreitung, Biologie und Ökologie, Basel: Birkhäuser Verlag; 1995. pp. 178–282.

Montgomery WI. Population structure and dynamics of sympatric Apodemus species (Rodentia: Muridae). J Zool. 1980; 192: 351–377.

Davis BA, Brewer S, Stevenson AC, Guiot J. The temperature of Europe during the Holocene reconstructed from pollen data. Quat Sci Rev. 2003; 22: 1701–1716.

Horáček I, Jahelková H. History of the Pipistrellus pipistrellus group in Central Europe in light of its fossil record. Acta Chiropt. 2005; 7: 189–204.

Kolfschoten T van. The smaller mammals from the Late Pleistocene sequence of the Sesselfelsgrotte (Neuessing, Lower Bavaria) In: Freund G, Reisch L, editors. Sesselfelsgrotte VI, Naturwissenschaftliche Untersuchungen, Wirbeltierfauna 1. Stuttgart: Franz Steiner Verlag Wiesbaden Gmbh; 2014. pp. 27–117.

Royer A, Montuire S, Legendre S, Discamps E, Jeannet M, Lécuyer C. Investigating the Influence of Climate Changes on Rodent Communities at a Regional-Scale (MIS 1–3, Southwestern France). PloS ONE. 2016; 11: e0145600 10.1371/journal.pone.0145600 PubMed DOI PMC

Moncel MH, Ashton N, Lamotte A, Tuffreau A, Cliquet D, Despriée J. The Early Auchelian of north-western Europe. J Anthropol Archaeol. 2015; 40: 302–331.

Horáček I. Small vertebrates in the Weichselian series in Dzeravá skala cave: list of the samples and a brief summary In: Kaminska L, Kozlowski JK, Svoboda JA, editors. Pleistocene Environments and Archaelogy of the Dzerava skala Cave, Lesser Carpathians, Slovakia. Krakow: Polish Academy of Arts and Sciences; 2006. pp. 157–167.

Nadachowski A, Żarski M, Urbanowski M, Wojtal P, Miękina B, Lipecki G et al. Late Pleistocene Environment of the Czestochowa Upland (Poland) Reconstructed on the Basis of Faunistic Evidence from Archaeological Cave Sites. Krakow: Polish Academy of Sciences, Institute of Systematics and Evolution of Animals; 2009.

Socha P. Rodent palaeofaunas from Biśnik Cave (Kraków-Częstochowa Upland, Poland): Palaeoecological, palaeoclimatic and biostratigraphic reconstruction. Quat Int. 2014; 326–327: 64–81.

Haarsma A, Kaal R. Predation of wood mice (Apodemus sylvaticus) on hibernating bats. Popul Ecol. 2016;

Gromov IM. The fossil Late Pleistocene rodents of the Crimean foothills. Transaction Quaternary Comission. 1961; 17: 1–189. (in Russian).

Benecke N. The Evolution of the vertebrate fauna in the Crimean mountains from the Late Pleistocene to the mid-Holocene In: Benecke N, editor. The Holocene History of the European Vertebrate Fauna; Archäologie in Eurasien 6. Rahden: Verlag Marie Leidorf GmbH; 1999. pp. 43–58.

Krokhmal AI, Rekovets LI. Localities of the Pleistocene small mammals of Ukraine and neighbouring regions Kiev: LAT&K; 2010. (in Russian).

David AI, Chetraru NA. Fauna of Palaeolithic locality ʺDuruitorʺ and the Pleistocene natural setting of Moldavia In: Ganja JM, Negadjev KN, David AI, editors. Late Cenozoic fauna from the Dniestr-Prut interfluve. Kishinev: Schtinca; 1978. pp. 75–99. (in Russian).

David AI. Theriofauna formation in the Late Pleistocene and Holocene on the territory of the Republic of Moldavia In: Benecke N, editor. The Holocene History of the European Vertebrate Fauna; Archäologie in Eurasien 6. Rahden: Verlag Marie Leidorf GmbH; 1999. pp. 59–72.

David AI, Pascaru VN. Theriofauna of Paleolithic site Buzduzhen 1 (Moldova) In: Matishov GG, Kalmykov NP, Titov VV, editors. Problems of paleontology and archeology of the south of Russia and neighbouring territories. Rostov on Don: Southern Scientific Center of Russian Academy; 2005. pp. 21–22. (in Russian).

Popov VV. Quaternary small mammals from deposits in Temnata-Prohodna Cave system In: Kozlowski JK, Laville H, Ginter B, editors. Temnata Cave. Excavations in Karlukovo Karst Area, Bulgaria. Krakow: Jagiellonian University Press; 1994. pp. 11–53.

Spitzenberger F, Engelberger S. A new look at the dynamic western distribution border of Apodemus agrarius in Central Europe (Rodentia: Muridae). Lynx n.s. 2014; 45: 69–79.

Stanko M. Apodemus agrarius (Pallas, 1771) (Rodentia, Muridae) in Slovakia. Košice: Equilibria s.r.o.; 2014. (in Slovakian with English summary).

Atopkin DM, Bogdanov AS, Chelomina GN. Genetic variation and differentiation in Apodemus agrarius interred from RAPD-PCR analysis. Russ J Genet. 2007; 43: 665–676. PubMed

Koh HS, Shaner PJ, Csorba G, Wang Y, Jang KH, Lee JH. Comparative genetics of Apodemus agrarius (Rodentia: Mammalia) from insular and continental Eurasian populations: cytochrome b sequence analyses. Acta Zool Acad Sci Hung. 2014; 60: 73–84.

Tatarinov KA. The fauna of the Neogene and Antropogene vertebrates of Podolna and Carpatian Mts. region; its history and recent composition. PhD. thesis, Academy of Sciences of the Ukrainian SSR. 1970. (in Russian).

Toškan B, Kryštufek B. Noteworthy rodent records from the Upper Pleistocene and Holocene of Slovenia. Mammalia. 2006; 70: 98–105.

Böhme W, Reichstein H. Zum Vorkommen und zur Verbreitung der Brandmaus, Apodemus agrarius (Pallas, 1771), am NW-Rande ihres europäische Areal. Zool Anz. 1966; 177: 319–329.

Aguilar JP, Pélissié T, Sigé B, Michaux J. Occurrence of the stripe field mouse lineage (Apodemus agrarius Pallar 1771; Rodentia; Mammalia) in the Late Pleistocene of southwestern France. C R Palevol. 2008; 7: 217–225.

Zimov SA, Zimov NS, Tikhonov AN, Chapin FS. Mammoth steppe: a high-productivity phenomenon. Quat Sci Rev. 2012; 57: 26–45.

Kolfschoten T van. The Saalian mammal fossils from Wageningen-Fransche Kamp. Meded Rijks Geol Dienst. 1991; 46: 37–53.

Kolfschoten T van. The Middle Pleistocene (Saalian) and Late Pleistocene (Weichselian) mammal fauna from Maastricht-Belvédere (Southern Limburg, the Netherlands). Meded Rijks Geol Dienst. 1985; 39: 45–74.

Storch G, Lütt O. Artstatus der Alpenwaldmaus, Apodemus alpicola Heinrich, 1952. Z Saugetierkd. 1989; 54: 337–346.

Spitzenberger F, Englisch H. Die Alpenwaldmaus (Apodemus alpicola Heinrich, 1952) in Österreich. Mammalia Austriaca 21. Bonn Zool Beitr. 1996; 46: 249–260.

Horáček I, Ložek V, Knitlová M. Juřičková L. Darkness under candlestick: glacial refugia on mountain glaciers In: Sázelová S, Novák M, Mizerová A, editors. Forgotten times and spaces: New perspectives in paleoanthropological, paleonethnological and archeological studies. Brno: Institute of Archaeology of the Czech Academy of Sciences; 2015. pp. 363–377.

Kaneko Y, Kryštufek B, Zagarondnyuk I, Vohralík V, Batsaikhan N, Avirmed D, Sukhchuluun G. Apodemus agrarius. The IUCN Red List of Threatened Species. 2008; e.T1888A8654207.

Schlitter D, Straeten E van der, Amori G, Hutterer R, Kryštufek, Yigit N, Mitsain G. Apodemus sylvaticus. The IUCN Red List of Threatened Species. 2008; e.T1904A8791394.

Amori G, Hutterer R, Kryštufek B, Yigit N, Mitsain G, Palomo LJ. Apodemus flavicollis. The IUCN Red List of Threatened Species. 2008; e.T1892A8699693.

Kryštufek B, Sozen M, Bukhnikashvili A. Apodemus uralensis. The IUCN Red List of Threatened Species. 2008; e.T1905A8801937.

Late Pleistocene Expansion of Small Murid Rodents across the Palearctic in Relation to the Past Environmental Changes