Annales de Paléontologie 96 (2010) 25–32

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Original article

Albertona balkanica from Early Miocene of Snegotin(Serbia) – implications for the distribution and evolution

of Miocene Ochotonidae

Albertona balkanica du Miocène inférieur de Snegotin(Serbie) – implications pour la distribution géographique et l’évolution

des Ochotonidae du Miocène

Zoran MarkovicNatural History Museum, Njegoseva 51, P.O. Box 501, 11000 Belgrade, Serbia

Received 8 July 2010; accepted 15 October 2010

Abstract

Remains of Albertona balkanica from the Early Miocene clays of eastern Serbia have shifted the rangeboundary of this species in direction of Central Europe. The peculiarities in tooth morphology were usedfor comparison and defining of the possible evolutionary connection with other representatives of fossilOchotonidae. Due to the similarity with fauna of Aliveri in Greece, the association of small mammals ofSnegotin (which includes Albertona) was included in the MN4 zone.© 2010 Elsevier Masson SAS. All rights reserved.

Keywords: Lagomorpha; Ochotonidae; Miocene; Distribution; Serbia

Résumé

Des vestiges d’Albertona balkanica du Miocène inférieur des argiles de l’est de la Serbie ont permis dedéplacer la frontière de l’aire géographique de cette espèce en direction de l’Europe centrale. Les particu-larités de sa morphologie dentaire ont été utilisées pour la comparaison avec d’autres représentants fossilesd’Ochotonidae afin d’établir des connexions entre l’évolution de ces différentes espèces. En raison de lasimilitude avec la faune de Aliveri en Grèce, l’association des petits mammifères de Snegotin (qui comprendAlbertona) a été incluse dans la zone MN4.© 2010 Elsevier Masson SAS. Tous droits réservés.

Mots clés : Lagomorpha ; Ochotonidae ; Miocène ; Distribution ; Serbie

E-mail address: zoran.markovic@nhmbeo.rs

0753-3969/$ – see front matter © 2010 Elsevier Masson SAS. All rights reserved.doi:10.1016/j.annpal.2010.10.003

26 Z. Markovic / Annales de Paléontologie 96 (2010) 25–32

1. Introduction

Remains of fossil small mammals were discovered in sediment at the banks of Blatni Potok(44◦34’58“N; 21◦35’19”E), 250 m upstream from the bridge, at the local road Golubac – Klenje(Fig. 1).

The Miocene sediments at Blatni Potok belong to the isolated Tertiary freshwater basinSnegotin-Vukovic. This locality was already well-known due to its fossil flora (Mihajlovic andLazarevic, 2003). The vertebrate remains were collected from the grayish-green clays with tracesof coal, which are overlaid by marl with plant remains. Besides the remains of micromammaliathere were also numerous remains of fishes, amphibians, reptiles and birds. These are the firstrecords of Miocene small mammals in eastern Serbia.

The mammal material includes odontological and osteological remains. According to theamount of odontological remains – over 120, the dominant species was the only representative ofochotonids in this locality, Albertona balkanica, presented with 33 isolated teeth. As this is only thesecond record of this species in the Balkans, the paleontological part of this paper includes morpho-logical characteristics and tooth dimensions, while the discussion chapter includes comparisonswith the comparative specimens of this and other species of genus Albertona.

Repository abbreviation: NHMBEO/TVSM - Natural History Museum Belgrade TertiaryVertebrate Small Mammals Collection.

Conventions: The nomenclature of molar parts and methods of measurement were adaptedfrom Lopez-Martinez (1986) and Angelone (2007). Measurements were taken by using the mov-able ruler on the binoculars and given in 0.01 mm units. The juvenile premolars and incisiveswere not included in the chart of tooth dimensions.

2. Systematic paleontology

Order: LAGOMORPHA Brandt, 1855Family: OCHOTONIDAE Thomas, 1897Genus: Albertona Lopez-Martinez, 1986Type species: Albertona balkanica Lopez-Martinez, 1986Albertona balkanica Lopez-Martinez, 1986Material: 1 I, 3 p3, 2 p4, 3 m1, 1 m2, 4 I, 2 P2, 3 P3, 2 P4, 3 M1, 2 M2, 2 d3, 1 d4, 2 D2, 2 D3.

Fig. 1. Sketch map with the location of Snegotin site.Localisation géographique du site de Snegotin.

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Measurements:

Tooth Length N Width

Range Mean Mean Range

p3 1.56–1.69 1.63 3 1.80 1.68–1.88p4 1.65–1.66 – 2 – 1.82–1.92m1 1.62–1.68 1.66 3 1.71 1.65–1.78m2 x – 1 – 1.52P2 0.84–1.00 – 2 – 1.52–1.56P3 1.24–1.47 1.39 3 2.43 2.17–2.69P4 1.42–x – 2 – 2.61–2.76M1 1.40–1.52 1.46 3 2.70 2.67–2.72M2 1.37–1.41 – 2 – 2.45–2.47

2.1. Description

i: The cross section of the tooth is triangular with rounded lateral sides and a flattened anteriorsurface.

p3: The lingual edge is slightly convex. The flexids are filled with cement. The trigonid islinked with talonid by the proto- and metaisthmus. In one case the metaconid is not connectedwith the talonid. The anteroconid is ellipsoid in shape. The protoconid is triangular and relativelyshort. The metaconid is large, rounded, with a short protrusion on the labial side, decreasing thesize of centroflexid. The talonid bears a narrow hypoconid curved in anterolabial direction. Theentoconid is somewhat shorter. The centroflexid is slightly curved in anterolingual direction.

p4-m1-m2: The morphological structure of lower molariform teeth is almost uniform. Theyhave two rhomboid parts – the larger trigonid and the smaller talonid. They are connected withcement. The protoconid is always sharper than the metaconid. The protoflexid is slightly convex.The talonid is approximately of same width as the trigonid.

I: As in other ochotonids, it is separated into two parts by the anterior longitudinal furrow.There is no cement while the enamel is thin.

P2 – The anterior side of the tooth is convex, bearing three pronounced cusps. It is coveredwith a thin layer of cement. The protocone and the metacone are approximately same-sized. Theparaflexus is the dominant depression. The metaflexus is small, but still separates the metaconefrom the metastyle. The posterior and the lingual side of the tooth form a right angle.

P3: This tooth is slightly convex on the lingual side. The protoloph is well-developed and elon-gated. There is a small furrow at the anterolingual side. The paraflexus is narrow. The hypoflexusis small. The labial area of protoloph and the metastyle lack enamel.

P4-M1-M2: Molariform teeth with a long hypoflexus. The protocone and the hypocone havea similar degree of sharpness. The posterior wall of the hypoflexus is thickened (Fig. 2).

Deciduous teethd3: It includes three clearly differentiated parts connected with a centroisthmus and lagiloph.

The anteroconid is the smallest part, with rhomboid shape. The protoflexid lacks cement, whilethe other two flexids are partially filled. The metaconid is lingually protruding and exceeds thetooth width in the area of talonid. The protoconid occupies the central part of the tooth. Theprotoconid is smaller then the hypoconid.

d4: Similar to real molars, particularly p4. The roots are present.

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Fig. 2. Occlusal pattern of cheek teeth of Albertona balkanica from the Early Miocene of Snegotin, eastern Serbia: A.Left p3 (NHMBEO/TVSM 1196). B. Left p4 (NHMBEO/TVSM 1213). C. Right P2 (NHMBEO/TVSM 1211). D. LeftP3 (NHMBEO/TVSM 1201). E. Left P4 (NHMBEO/TVSM 1197). F. Left M2 (NHMBEO/TVSM 1199). G. Left d3(NHMBEO/TVSM 1202). H. Right D3 (NHMBEO/TVSM 1207).Surface occlusale des molaires de Albertona balkanica du Miocène inférieur de Snegotin, est de la Serbie : A. p3 gauche(NHMBEO/TVSM 1196). B. Gauche p4 (NHMBEO/TVSM 1213). C. P2 droite (NHMBEO/TVSM 1211). D. P3 gauche(NHMBEO/TVSM 1201). E. P4 gauche (NHMBEO/TVSM 1197). F. M2 gauche (NHMBEO/TVSM 1199). G. Gauche D3(NHMBEO/TVSM 1202). H. D3 droite (NHMBEO/TVSM 1207).

D2: They are much abraded so they lack the enamel coating that should close the inside ofmasticating surface. The roots are present.

D3: The anterior and the posterior parts of the tooth are of similar size. The hypoflexus isdeep, almost reaching the center of tooth width. The mesoflexus is only slightly marked, whilethe paraflexus is long, arched and penetrating the metacone. The protocone is smaller than thehypocone. The paracone is much pressed from the sides.

2.2. Comparisons

Teeth of adult individuals from site Snegotin are somewhat larger than the teeth from Aliv-eri (Lopez-Martinez, 1986). They are also larger than the comparative specimens of species A.

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Fig. 3. Localities where representatives of genus Albertona were recorded. Circles: Albertona balkanica; Squares:Albertona aegeensis and Albertona cf. aegeensis.Sites où le genre Albertona est représenté. Cercles : Albertona balkanica ; carrés : Albertona aegeensis et Albertona cf.aegeensis.

aegeensis and A. cf. aegeensis from Turkey (Ünay and Göktas, 1999). All permanent teeth lackroots.

P4 is molariform (Fig. 2, E). The specimens from Snegotin show the primitive characters ofa well-developed mesoflexid, lack of anteroconid and protoconulid in p3 (Fig. 2, A), and onlytwo flexa in P2 (Fig. 2, C). The cement is not as thick as in teeth from Aliveri, which is anotherprimitive characteristic. In P2 from Snegotin the metaflexus is shallower and the protocone lesspronounced than in the corresponding premolars in species A. aegeensis and A. cf. aegeensis fromTurkey.

3. Discussion

The genus Albertona lacks clearly defined phyletic connections and presently includes onlytwo species – balkanica and aegeensis (Fig. 3).

Albertona balkanica was identified at two sites: Aliveri in Greece (where it was describedfrom), and Snegotin in Serbia. The remains of ochotonids from Horlak (Sümengen et al., 1990),cited as Albertona cf. balkanica have never been described. Based on the similarity of availablespecies of small mammals at this site and others in Turkey, this remains most probably belong tospecies Albertona aegeensis. The remains of this species were also recorded in several other sitesin Turkey: Söke and Dededag (Ünay and Göktas, 1999), Mut (Atabey et al., 2000; Atabey et al.,2001) and Cankiri-Sülüklü göl (Özcan et al., 2007). The fauna from Söke is included in MN4(Ünay and Göktas, 1999) according to records by Megacricetodon cf. primitivus, Cricetodon aff.tobieni and Anomalomys cf. minor. However, the presence of representatives of genera Debruijnia,Spanocricetodon and Lartretomys has led Alcicek (2010) to assign this association to MN3-4.

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Fig. 4. Distribution of genera Lagopsis, Albertona and Alloptox in south Europe and Anatolia during Early/MiddleMiocene.Distribution des genres Lagopsis, Albertona et Alloptox dans le sud de l’Europe et l’Anatolie pendant la Miocèneinférieur/moyen.

Although the association from Dededag may look superficially similar, it has certain characteristicsmore similar to zone MN4. Anomalomys aliveriensis and Megacricetodon primitivus are clearlydefined in Dededag. The possible more advanced evolutionary form of species A. aegeensis(identified as A. cf. aegeensis) also indicates the decrease in size of mesoflexid and the morepronounced protoconulid. These characteristics were recorded in the representatives of genusAlloptox, which replaced Albertona in the Middle-Late Miocene of Serbia (unpublished materialfrom Natural History Museum in Belgrade collections), Greece and Turkey. Lopez-Martinez(1986), Sen (1990) and Vasileiadou and Koufos (2005) assume that Albertona is the ancestor ofthe first representative of genus Alloptox in Turkey – species Alloptox anatoliensis (Ünay andSen, 1976), as well as some other species identified in the Early and Middle Miocene of China(Liu and Zheng, 1997). However, the shape of protoloph in P3 of Albertona and its position on thetooth show greater similarity with representatives of genera Marcuinomys and Lagopsis, fittingwithin the phylogenetic picture presented by Erbajeva (1994). According to the morphologicalcharacteristics of teeth, this group might also include Bellatona. In Alloptox the protoloph is moreprotruding at the anterior side, leading to a triangular shape of tooth instead of the ellipsoid shapein Albertona. According to this characteristic, Albertona fits better within the line Marcuinomys– Lagopsis – Paludotona. Sen (2003) separated the evolutionary line Marcuinomys – Lagopsis– Paludotona from the line Albertona - Alloptox. However, it is more probable that the generaAlbertona, Alloptox and Lagopsis belong to separate lines, and that their ancestors should belooked for among the Oligocene ochotonids – most probable Sinolagomys or some close form(Tobien, 1978; Wu, 2003). This hypothesis is supported by the fact that the remains of Sinolagomysdiscovered in Oligocene-Miocene border sediments of the Western Balkans (unpublished materialfrom Natural History Museum in Belgrade and Utrecht University Faculty of Earth Sciencescollections). Adaptation to living conditions has caused different ranges of these three genera. Therecords of genus Lagopsis are connected with the western part of European continent, Albertonafor the Balkans and Anatolia, while Alloptox spread from the Balkans and extreme southeast partof Europe across Turkey to China and Africa (Fig. 4).

The existence of Albertona seems limited only to Early Miocene, while the records of repre-sentatives of other two genera were also found in the sediments of Middle Miocene.

Z. Markovic / Annales de Paléontologie 96 (2010) 25–32 31

The accompanying fauna of small mammals from sites Mut (Atabey et al., 2000; Atabeyet al., 2001; Ünay et al., 2001), Cankiri-Sülüklü göl (Özcan et al., 2007) and Horlak (Sümengenet al., 1990) shows no significant similarities with the association from Aliveri and Snegotin. Theelements such as Galerix uenayae and Cricetodon kasapligili, stratigraphically assigned by MN3zone (de Bruijn et al., 1993; Ostende et al., 2001a, 2001b), and Spanocricetodon sp., from MP30to MN2 in Anatolia (Theocharopoulos, 2000), additionally challenge the possibility of assigningthese localities in the same MN zone as Aliveri and Snegotin. The mismatch in composition ofthese faunas may be attributed to regional differences recorded both at Aliveri and at Karydia(Doukas, 2003), caused by migratory influences.

The record from Snegotin has defined the northernmost boundary of range of species Alber-tona balkanica. The fact that faunas of Aliveri and Snegotin show mixture of European andEastern elements indicates that the land connection of Balkans with the Central Europe and Ana-tolia was formed most probably already at middle-Early Miocene (end of MN3). This type ofpaleogeographic reconstruction was also presented by de Bruijn and Sarac (1991).

The results of identification so far indicate that the composition of small mammal fauna from thelocality of Snegotin is exceptionally similar to the site Aliveri in Greece. All identified species fromSnegotin - Galerix symeonidisi, Heterosorex ruemkeae, Myxomygale engesseri, Megacricetodonprimitivus, Cricetodon aliveriensis, Anomalomys aliveriensis, Gliridinus euryodon, Microdyromissp., Myodiromis sp. and Albertona balkanica are also represented in Aliveri (Doukas, 2003).

Therefore it may be concluded that this fauna also belongs to zone MN4.

4. Conclusion

Studies of fossil small mammals in central Balkans were started only in the late 20th century.Therefore the number of localities studied from this aspect is still modest (Markovic, 2003).However, each identified remain of this fossil presents a new picture on their distribution in spaceand time. The remains of Albertona from the Early Miocene of Snegotin are therefore openingthe issue of its evolutionary position. The new records of lagomorphs from Early and MiddleMiocene in the area of central Balkans would contribute not only to elucidation of this case butalso to the overall picture of migrations in European and Asian forms.

Acknowledgements

I am thankful to Engin Ünay and Sefket Sen for providing me the required literature. Specialthanks to Predrag Ilic for arranging the figures. I am very grateful to Milos Milivojevic forhis efficient help during fieldwork and preparing material in Natural History Museum Belgradelaboratory.

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