MIDDLE PLEISTOCENE SMALL MAMMAL fAUNAS Of EUROPE : EVOLUTION , BIOSTRATIGRAPHY , CORRELATIONS

The paper is concerned with the small mammal fauna evolution in Europe in the Middle Pleistocene. The information on the faunas of the end of the Early Pleistocene has been also taken into consideration. The data available made possible identifying several stages in the small mammal evolution. Not all intervals within the Middle Pleistocene are provided with sufficient information for recognizing individual stages; that is particularly true for the cold periods of the Middle Pleistocene – the Donian and the Okian glaciations (=Elsterian, =Anglian). Based on the studies of small mammal localities, the biostratigraphic scheme has been developed, the principal phylogenetic lineages of Arvicolinae were traced, and maps of the Middle Pleistocene small mammal localities have been compiled kEY wORDS: Middle Pleistocene, small mammals, Europe, biostratigraphy, evolution,


MIDDLE PLEISTOCENE SMALL MAMMAL fAUNAS Of EUROPE: EVOLUTION, BIOSTRATIGRAPHY, CORRELATIONS INTRODUCTION
Problems of evolution of the Middle Pleistocene small mammals and the synchronization of the principal stages of their evolution with geological and climatic events have been examined in many previous publications (Agadjanian 2009;Alexandrova 1976;Chaline 1972;Cuenca-Bescόs et al. 2013;Heinrich 1990;Fejfar and Horaček 1990;Markova 1982Markova , 2005Markova , 2006Markova , 2007Markova , 2014;;Markova and Kolfschoten 2012;Markova and Puzachenko 2016;Markova and Vislobokova 2016;Masini and Sala 2011;Maul 2001;Maul and Markova 2007;Maul et al. 2000Maul et al. , 2007;;Nadachowski 1990;Rekovets 1994;Schreve 2004 a,b,c; Vislobokova and Tesakov 2013; van der Meulen 1973; van Kolfschoten 2014; von Koenigswald and van Kolfschoten 1996 and many others).In this paper we try to analyze generally the main stages in the evolution of the European small mammal faunas referring to the period from the Jaramillo paleomagnetic event (the end of the Early Pleistocene 1.07 -0.99 Ma, ~MIS 26-30) till the end of the Middle Pleistocene -the end of Saalian (=Walstonian, =Dnieper) glaciation (MIS 6).The ages of the temporal intervals were given according to oxygen isotope curve (Lisiecki and Raymo 2005).A significant number of global climatic events, glaciations and interglacials, correspond to this period.We tried to recognize the response of the small mammal faunas to the different climatic events during the Middle Pleistocene, to synchronize the faunas of Eastern Europe with those of Western Europe, to examine the principal evolutional changes in the different phylogenetic lineages of Arvicolinae during the Middle Pleistocene.

PRINCIPAL STAGES Of THE MIDDLE PLEISTOCENE SMALL MAMMAL fAUNAS
The end of the Early Pleistocene -the beginning of the Middle Pleistocene  The analysis of small mammal faunal data from Eastern and Western Europe dated to the interval from the Jaramillo paleomagnetic event to the beginning of the early Middle Pleistocene (1.06-0.7 Ma) provided evidence for several phases in the small mammal evolution recognizable within this interval.It is established that the boundary between large mammal fauna stages corresponds to those of Tamanian and Tiraspolian mammal assemblages in Eastern Europe, Early/Late Galerian in Italy, and MNQ 20/MNQ 21 zones.A more detailed picture was revealed in the evolution of small mammal faunas during the regarded interval; the phases are distinguishable by changes in the species composition, first occurrences of new species, and evolutionary changes in a several phylogenetic lineages of Arvicolidae.
On the Russian Plain most of localities are found in great geological sequences studied not only paleontologically, but also by several methods including paleomagnetic stratigraphy.Those supplementary data help to determine the stratigraphic position of mammal faunas.Many localities in the region of the Black Sea coasts include, along with mammals, shells of brackish-water mollusks differing in their evolutionary level.The mollusk assemblages permit to correlate the mammal faunas directly with the Black Sea transgressions and paleogeographic events in the Eastern Mediterranean.
A relatively large part of localities in Western Europe are related to karst caves and fissures.In such localities faunal remains of different age are often found to be mixed, and paleomagnetic analysis data are also not quite reliable.There are, however, a number of multilayered localities (Kärlich, Shöningen, Sima del Elephante, Grand Dolina, Colle Curti, Castagnone, the localities related to the different Themes River terraces, and some others) where multidisciplinary studies (including paleomagnetic analysis and absolute dating) were performed.
Every phase in the evolution of small mammals is identifiable not only by appearance of new taxa, but also by the prevalence of certain morphotypes within a taxon.The main evolutionary transformations within the phylogenetic lineages resulted from anagenesis; several "paleontological" species were identified on the basis of the dominant tooth morphotypes.In the Prolagurus -Lagurus lineage, for example, we never found a single tooth morphotype in a certain time interval; there is always a considerable variability recorded.At the level of faunas correlatable with the Jaramillo event there are some steppe lemmings with morphotypes typical of Prolagurus ternopolitanus (= P. praepannonicus) against the background of prevailing tooth morphotypes characteristic of P. pannonicus.Faunas dated to the very end of the Matuyama reversed polarity epoch (the Karai-Dubina locality) include steppe lemmings with tooth morphotypes of P. pannonicus, P. posterius, L. transiens.More than 90% of the teeth feature morphotypes characteristic of P. pannonicus, while L. transiens is represented by a single specimen displaying the extreme variant of the morphological variability (Markova 1982).Therefore, it is easy to make a mistake in attributing a locality to another evolutionary stage (faunal assemblage) if the species list of the locality is considered formally in the absence of other datable materials.All these phenomena require a careful investigation of fossil materials.(Markova 1990(Markova , 2007;;Shik 2014) (Fig. 1).
The other opinion exists also that more advanced voles of Allophaiomys -Microtus linage (for example, Microtus thenii) also existed during Jaramillo event (Maul et al. 2007) (Fig. 2).For our opinion it is necessary to carry out the additional studies to resolve this problem.Those faunas were identified as the Morozovkian small mammal assemblage (Alexandrova 1976;Markova 1990) and fall within the Matuyama reversed polarity zone.It is possible that those East European faunas may be correlated with the faunas with Microtus thenii from Untermassfeld (Germany) (Maul 2001) (Fig. 1, 2, 5).

Small mammal faunas
More advanced faunas are identified by the first occurrence of Microtus ex gr.oeconomus (= M. protooeconomus, =M.ratticepoides).The bulk of the fauna is formed by Prolagurus pannonicus and Eolagurus argyropuloi; remains of Mimomys savini and Allophaiomys pliocaenicus nutiensis are present in small number.According to paleomagnetic data, these faunas are correlated to the end of the Matuyama epoch.The faunas at that stage of evolution are recognized as Petropavlovkian assemblage of small mammals in Eastern Europe (Alexandrova 1976;Markova 1998) (Fig. 1, 2, 5).
The faunas marked by the first appearance of Microtus arvalinus and Prolagurus posterius (Shamin locality, Don R. basin) occur in inversely magnetized deposits and are dated to the very end of the Matuyama epoch.The presence of the above named species makes the faunas closer to the Early Tiraspolian ones.In the localities pertaining to the beginning of the Brunhes epoch the rooted voles of Mimomys genus still persist.Steppe lemmings are represented mostly by Prolagurus posterius, though remains displaying the Prolagurus pannonicus morphotype were presented long enough (up to the end of the Don glacial epoch).The genus Microtus became more diversified at that time (Agadjanian 2009;Markova 1992Markova , 2007)).It should be noted, however, that correlations are often performed on small collections and on insufficiently representative remains recovered from different localities.In such cases, the comparison may lead to a false conclusion.On the whole, the analysis of small mammal remains dated to Early-Middle Pleistocene (and of Arvicolinae in particular) is a useful tool, as it enables the evolution process to be traced in various phylogenetic lineages, and the sediments from which they originate to be dated.This palaeontological dating is particularly important, as absolute dates are practically lacking for the interval under consideration; as to the paleomagnetic method in itself, unsupported by paleontological materials, it hardly can deliver a conclusive date.

first half of the Middle Pleistocene (MIS 18 -12)
The main intervals of the first half of the Middle Pleistocene include: Ilyinian complex interglacial (MIS 18 and 17), that apparently corresponds to the glacial A of the Cromerian complex and interglacial Cromer II; the Donian glaciation (MIS16)  5).In this paper, when dealing with the materials from Eastern Europe, the authors follow the last stratigraphic scheme, proposed by Shik (2014).The West European stratigraphic subdivisions are given according to Gibbard et al. (2004).
The analysis performed on the European small mammal faunas dated to the first part of the Middle Pleistocene gives ground for distinguishing several stages in their evolutionary development during ~0.76-0.42Ma BP.

Ilyinian complicated interglacial = glacial A of the Cromerian complex and Cromer II interglacial
The faunas of these intervals correspond to MIS 18 and MIS 17 (~0.Markova 1982Markova , 1992)).According to the material from West European localities, the first documented appearance of Microtus agrestis is dated to that time (Nadachowski 1985) (Fig. 1, 2, 5).

Muchkapian interglacial (=Cromer III)
The   (Grün and Schwartz 2000).More than ten localities of this age were found in Eastern Europe (Markova 2006).They are distributed from the Upper Volga basin to the northern Black Sea region.Studies of the loess-paleosol series on the Russian Plain permitted to identify a horizon of fossil soil -the Inzhavino paleosol -attributable to the Likhvinian Interglacial (Velichko et al. 1992;Shik 2014).
Several very important localities were found in Western Europe.Among them, there is the famous Barnfield Pit locality in Great Britain (Swanscombe, Kent) in the south of the Thames drainage basin.The bone-bearing layers lie on those dated to the Anglian glacial epoch.When describing particular faunas in the paper, we used the name of the taxon given by the author.An index designating the enamel surface ratio in the Arvicola teeth has been widely used in determination of the water vole evolutionary stage and the relative age of enclosing deposits (Markova 1975(Markova , 1981;;Heinrich 1978) (Fig. 4).

Borisoglebskian cooling (MIS 10)
The only locality with small mammals, Topka locality (the Don R. drainage basin), was discovered in the deposits overlying those of the Likhvinian Interglacial and in all probability belonging to the cold interval correlatable with the Borisoglebsk loess horizon (MIS 10) (Krasnenkov and Kazantseva, 1993).The locality yielded remains of Arvicola chosaricus, but no voles of the "Terricola= Pitymys" subgenus typical for Pre-Okian faunas have been found at the Topka (Fig. 1).
No small mammal localities of that age are known in Western Europe (Fig. 1, 2, 5).
The water vole teeth are distinct for more advanced morphology than have Arvicola from the Barnfield Pit locality with SDQ=130, but more archaic than those described in water vole remains from the localities correlatable with MIS 7 (Fig. 1, 2, 4, 5).Schreve (2001b) described this fauna as belonging to the Purfleet Mammal Assemblage-Zone -MAZ Purfleet.Unfortunately the lagurides are practically absent from Western European faunas.

Orchikian cooling (MIS 8)
The Kamenka (=Purfleet, =Reinsdorf ) interglacial was followed by a new cooling (MIS 8, 300-243 ka BP), which was named after the name of loess horizon distributed on the Russian Plain as the Orchikian one (Velichko et al. 1992) As follows from the enamel index of water vole teeth (SDQ = 100.65-107.12)(Fig. 4), the fauna may be dated to the second half of the Middle Pleistocene.

Romnian, = Schöningen, = Sandy Lane interglacial
The fauna found in the Matveevka locality on the Sula R. (the Dnieper R. drainage basin, Cherkassy Region, Ukraine, 49º31´ N, 32º41´ E) may be assigned to the end of the Romnian warming (MIS 7).The sequence includes a layer of sand and gravel with bone remains of small mammals.Upwards it is replaced with loess layer overlain in turn with the Dnieper till; still higher a loess-like loam occurs including a paleosol horizon (Krokhmal and Rekovets 2010;Rekovets, 1994) 2000].Judging by the water vole enamel index (SDQ) equal to 113.5 (Heinrich, 1990), it corresponds to MIS 7 (7e/7с).The U-series dates confirm the validity of the deposits attribution to MIS 7: >350,000-200,000 yr BP (Blackwell and Schwarcz 1986) Most of the localities in the region of the Black Sea coasts include, along with mammals, shells of brackish-water mollusks varying in their evolutionary level.The mollusk assemblages permit the mammal faunas to be directly correlated with the Black Sea transgressions and palaeogeographic events in the Eastern Mediterranean (Mikhailesku and Markova 1992).As is known, a significant part of localities in Western Europe are related to karst caves and fissures.In such localities faunal remains of different age are often found to be mixed, and data of palaeomagnetic analysis are also not quite reliable.There are, however, a number of multilayered localities (Kärlich, Shöningen, Sima del Elephante, Grand Dolina, Colle Curti, Castagnone, the localities from the fluvial sequences from the Thames R. terraces and some others) where multidisciplinary studies (including palaeomagnetic analysis and absolute dating) were performed.The correlation between the East European localities and those mentioned above are very realistic.
The relatively long time interval of the Middle Pleistocene is noted for several climatic events of global scale (glaciation -interglacial) that occurred during it.The biostratigraphic scheme of the Middle Pleistocene has been developed and maps of small mammal localities compiled (Fig. 1, 2, 5).Thus, faunas of small mammals related to the long Middle Pleistocene interval allow assessment of their taxonomy and evolutionary development.These data can also help us to divide the geological deposits by age and permit reconstruction of the palaeogeographic picture of the past.The results obtained may serve as an important component for compiling biostratigraphic schemes of the Middle Pleistocene and of the Pleistocene in general.
fig.1.Biostratigraphical scheme of the Middle Pleistocene by small mammal data from Western and Eastern Europe

fig. 2 .
fig. 2. Arvicolinae phylogenetic lines during the Middle Pleistocene by the materials from European localities data reflect the drastic cooling and aridization during this glaciation (Fig. 1, 2, 5).The second half of the Middle Pleistocene (MIS 11 -MIS 6) Likhvinian (= Holsteinian, = Hoxnian) interglacial (MIS 11) Middle Pleistocene (or the beginning of the Middle Neopleistocene in Russian stratigraphical schemes) is recognized by a noticeable warming of interglacial order -the Likhvinian (Holsteinian, Hoxnian) interglacial.This interglacial is most close to the Holocene optimum in its climatic characteristics.The deposits attributed to the Likhvinian (Holsteinian, Hoxnian) interglacial overlie those of the preceding glaciation (Elsterian in Western Europe, Anglian in Great Britain, Oka glaciation in Eastern Europe).The deposits exposed in the Hoxne stratotype in Great Britain (Layer C) have been dated by uranium series and ESR at 404+33/-42 ka BP, which fits well enough into the time limits of MIS 11

Anastasia K .
Markova is specialist of Quaternary palaeontology and historical biogeography and works in the Laboratory of Biogeography of the Institute of Geography RAS.She is the Doctor of Geographical Sciences.Her main fields of interests focused on the evolutional peculiarities of Pleistocene small mammals, their taxonomy, geographical distribution in the past and palaeoecology.She leaded the intra-institutional scientific collective, which study the species composition, biodiversity and distribution of Late Pleistocene and Holocene mammals of Northern Eurasia.She is the member of Russian Quaternary Commission and the member of editorial board of the journal "Stratigraphy.Geological correlation".A.K. Markova published more than 250 scientific papers including 4 monographs, chapters in 8 collective monographs and chapters in 4 palaeogeographical atlases.Andrey Yu.Puzachenko is a specialist in vertebrate zoology and historical biogeography.He works in the Laboratory of Biogeography of the Institute of Geography RAS.He is the Doctor of biological Sciences.His main fields of interests focus on morphological diversity of recent and extinct mammal species and the evolution of the Pleistocene mammalian faunas in the Holarctic during the Middle and the Late Pleistocene.A. Yu.Puzachenko published 191 scientific articles in Russian and international journals, and chapters in 13 collective monographs.

3. Allophaiomys M 1 quotient by the materials from European localities Anastasia K. Markova, Andrey Yu. Puzachenko MIDDLE PLEISTOCENE SMALL MAMMAL ...
780 Ma -0.676 Ma).They are characterized by the presence of rhizodont voles Mimomys pusillus, M. savini, Pliomys episcopalis, steppe fig.These faunas differ from the earlier ones by the presence of cold-adapted species: Dicrostonyx ex gr.simplicior and Lemmus sp.Rhizodont voles of Mimomys (M.savini) and Pliomys genera are parts of these faunas.The steppe lemmings are represented by Prolagurus posterius and Lagurus transiens; the narrow-skulled voles -by Lasiopodomys (Stenocranius) gregaloides.M. (Terricola) arvalidens, M. arvalinus, M. oeconomus (= M. ratticepoides), and M. hyperboreus also are present in these faunas (Agadjanian 2009, (Stuart and Lister, 2001)vini was described (Pakefield site)(Stuart and Lister, 2001).In the second part of this interglacial.The first and M. oeconomus.The narrow skulled voles are represented by L. (Stenocranius) gregalis, though the morphotypes of the teeth, typical for L. (S.) gregaloides, still are present in small numbers.The first appearance of L. (S.) gregalis distinguishes these faunas from the previous ones.In Western Europe at the beginning of this interglacial.

4. Water vole Arvicola enamel thickness quotient SDQ by the materials from the Middle Pleistocene European localities
The fauna was described by D. Schreve under the name fig. or A. cantianus or A. terrestris cantianus.
(Zastrozhnov et al. 2017) however more younger age of Khozarian fauna from the Cherny Yar stratotype locality(Zastrozhnov et al. 2017).So, till now the position of the Khozarian faunas is discussed.
(Markova 1982)pared with A. cantianus and is an indicator species of the Khozarian faunas (Fig.2, 4).In steppe lemmings of the Lagurus genus the 'lagurus' morphotype is dominant in the faunas of the Khozarian type; more archaic 'transiens' morphotypes have been recorded in the steppe lemming remains, but their proportion is rater small(Markova 1982).
Apodemus sp., Clethrionomys sp.Microtus oeconomus, Microtus sp.(Fig.1, 2, 5).A unique multilayered cave site with artifacts of the . The faunas of this age are absent from Eastern Europe.A few localities of this age were found in Western Europe.The Harnham locality was discovered in the south of Great Britain, at the Avon and the Ebble interfluve.It was dated by OSL to approximately 250 ka BP and attributed to the end of MIS 8 (Bates et al. 2014).The locality yielded some mammal bones: