Mammalia: Lagomorpha: Ochotonidae) from Three Late Miocene Localities in Ukraine

Palaeontologia Electronica palaeo-electronica.org

Dental enamel ultrastructure in Ochotona and Prolagus (Mammalia: Lagomorpha: Ochotonidae) from three late Miocene localities in Ukraine

Emilia Rabiniak, Leonid Rekovets, and Dariusz Nowakowski

ABSTRACT

The comparison of the dental enamel of late Miocene ochotonids from the Ukraine shows only very subtle differences. The ultrastructure of premolars, molars, and incisors of pikas: Ochotona and Prolagus (Lagomorpha, Ochotonidae) from three localities (Popovo 3, MN 11; Verkhnya Krynytsya 2, MN 12; Lobkove, MN 12/13) is mainly multilayered. In cheek teeth it is composed of a radial (up to 60% of total enamel thickness) and an irregular layer (up to 40%). There is almost no difference in the enamel ultrastructure between remains of different geological age and tooth position (premolars, molars). However, the lower incisor of Ochotona differs from the upper one in having a radial enamel and a HSB layer, whereas the upper have a radial and a tangential enamel. Minor differences between the various species of Ochotona and Prola- gus could be recognised in the arrangement of the prisms.

Emilia Rabiniak. Wroclaw University of Environmental and Life Sciences, Department of Biology and Animal Breeding, 51-630, Wroclaw, Chelmonskiego 38c, Poland. [email protected] Leonid Rekovets. Wroclaw University of Environmental and Life Sciences, Department of Biology and Animal Breeding, 51-630, Wroclaw, Chelmonskiego 38c, Poland. [email protected] Dariusz Nowakowski (corresponding author). Department of Anthropology, Institute of Biology, Wrocław University of Environmental and Life Sciences , ul. Kożuchowska 5, 51-631 Wrocław, Poland. [email protected]

Keywords: Lagomorpha; tooth; enamel; ultrastructure; Miocene

Submission: 25 July 2015 Acceptance: 4 September 2017

Rabiniak, Emilia, Rekovets, Leonid, and Nowakowski, Dariusz. 2017. Dental enamel ultrastructure in Ochotona and Prolagus (Mammalia: Lagomorpha: Ochotonidae) from three late Miocene localities in Ukraine. Palaeontologia Electronica 20.3.46A: 1-12 palaeo-electronica.org/content/2017/1998-enamel-ochotona-and-prolagus

Copyright: September 2017 Palaeontology Association. This is an open access article distributed under the terms of Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0), which permits users to copy and redistribute the material in any medium or format, provided it is not used for commercial purposes and the original author and source are credited, with indications if any changes are made. creativecommons.org/licenses/by-nc-sa/4.0/creativecommons.org/licenses/by-nc-sa/4.0/ RABINIAK, REKOVETS, & NOWAKOWSKI: ENAMEL OCHOTONA AND PROLAGUS

INTRODUCTION several Late Miocene taxa of Prolagus and Ochot- ona (Ochotonidae) from Ukraine in order to com- The evolution of dental morphology of Euro- plement the current knowledge. pean ochotonids (pikas) is relatively well known due to many publications (e.g., Tobien, 1963; MATERIAL AND METHODS López-Martínez, 1974; Tobien, 1974, 1975; Agad- janian and Erbajeva, 1983; Erbaeva, 1988; López- The material included the third lower premo- Martínez, 1989, 2001; Tesakov and Averianov, lars (p3), molars, and incisors from the Upper Mio- 2002; López-Martínez, 2008; Angelone and Sesé, cene Ukrainian localities Popovo 3 (MN 11, Upper 2009; Čermák, 2010; Fostowicz-Frelik, 2010; Fos- Sarmatian), Verkhnya Krynytsya 2 (MN 12, Upper towicz-Frelik et al., 2010; Angelone and Čermák, Meotian), and Lobkove (MN 12/13). The general 2014; Lissovsky, 2014). However, only few papers information on the sites, and on the qualitative and deal with the enamel ultrastructure of this family. quantitative composition of their fauna can be von Koenigswald and Martin (1984) have pub- found in Rekovets and Pashkov (2009); Čermák lished a series of works on various aspects of mor- and Rekovets (2010); Rekovets et al. (2014). All phology, evolution, and function of enamel layers three sites hold alluvial deposits of the Dnieper in various Lagomorpha of different geological age River containing gravels and sands, and remains (von Koenigswald and Clemens, 1992;von Koenig- of small mammals (Table 1). The faunas indicate a swald, 1996; Martin, 1999, 2004; von Koenigswald dry climate with the prevalence of steppes. The et al., 2010). However, the enamel microstructure food of herbivores consisted of tough plants which of ochotonids from sites of south-eastern Europe should be reflected in the morphology of the teeth. has not been studied in detail. The region is rela- Samples of the following taxa were included tively well explored and plays an important role in in the analysis: Prolagus aff. crusafonti and Ochot- the history of faunal exchanges between Asia and ona sp. from Popovo 3, Ochotona cf. eximia from Europe, and in the formation of the extant species Verkhnya Krynytsya 2, and Ochotona sp. from ranges. Studies on the enamel ultrastructure of Lobkove. We cannot definitely exclude that all the Neogene and Pleistocene small mammals of this Ochotona specimens under consideration actually region have so far dealt with Castoridae only belong to the same species. However, in any case (Rekovets and Nowakowski, 2013). Ontogenetic the teeth are of different age. The preparation of changes of enamel have been investigated in teeth for the analysis followed von Koenigswald some late Neogene species of Spalax (Rekovets (1980), and improved in later works. The method et al., 2014). was slightly modified by omitting the cut with a dia- This work provides new data on the enamel mond saw (IsoMet® Low Speed Saw), which can microstructure of incisors, premolars and molars of cause teeth damage; the specimens were ground

TABLE 1. A list of specimens including species of lagomorphs, types of teeth, numbers of images, and excavation locations/age.

No. of microscope No. Taxon Tooth position Locality age images 1. Ochotona cf. eximia p3 Lobkove 9041- 9046 MN 12/13 (Upper Maeotian,Cherevychnian stage) 2. Ochotona cf. eximia p3 Verchnia Krynica 2 9026- 9037 m3 MN 12 9843 lower incisors (Lower Maeotian, Belkian stage) 9812 3. Ochotona sp. p3 Popovo 3 0248- 0261 (ex.gr. kalfense) m2 MN 11 9836 upper incisors (Upper Sarmatian, Beryslavian stage) 9768 4. Prolagus aff. crusafoni p3 Popovo 3 8995- 9006 m3 MN 11 9817-9820 (Upper Sarmatian, Beryslavian stage)

The following abbreviations were used, according to Koenigswald et al. (2010): EDJ - enamel dentine junction, HSB - Hunter-Schre- ger bands, IPM - interprismatic matrix, IRRE - irregular enamel (here: IR), OES – outer enamel surface, PLEX – prismless external layer, R – radial enamel, T– tangential enamel.

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immediately after embedding them in epoxy resin to von Koenigswald and Sander (1997) and our (Epoxy Embedding Medium kit - 45359 Sigma- research, the basic enamel layer types in lago- Aldrich GmbH). The quality of grinding was con- morphs are: trolled under stereomicroscope. The samples were 1) radial type – prisms directed radially away from the rinsed for 10 seconds in a 5% HCl solution fol- EDJ; in transverse section, the prisms are perpen- lowed by ethanol, and placed for 30 seconds in the dicular to the EDJ; in vertical section, the prisms ultrasonic apparatus to remove the dust. The cross display inclination angles from zero to nearly 90°; sections were standard for all samples and were 2) tangential type – prisms have a strong lateral devia- analysed in a scanning electron microscope (Zeiss tion and almost no inclination; all prisms are parallel EVO LS 15) in the Laboratory of Electron Micros- to each other but the IPM anastomoses are nearly copy, Faculty of Biology and Animal Sciences, orthogonal; this layer occurs in lagomorphs only in Wrocław University of Environmental and Life incisors; Sciences. Longitudinal sections were also made 3) irregular type – irregular decussation of individual for Ochotona sp. from Popovo 3. prisms or bundles of prisms; the descriptive term "irregular enamel" defines types of different evolu- The lower p3s were subject to the most tionary origin; in placentals, most of the irregular detailed examination, since they are the most enamel has evolved from HSB; in marsupials, irreg- diagnostic and functional teeth. Incisors were ular enamel is derived from a radial type; examined only in Ochotona. In Popovo 3 also Pro- 4) HSB – specific mode of prism decussation in layers, lagus occurred, but it was impossible to distinguish also called bands; layer bifurcations are always between the incisors of the two genera. The num- present; each set of layers bifurcates in only ber of examined tooth areas depended on the one direction; transitional zones may occur regions of interest and the quality of grinding. between bands; Approximately 10-12 images per tooth were taken, 5) PLEX – unstructured, thin layer next to the OES bor- which was sufficient for the analysis. As a rule, der. the detailed photographs of enamel were taken in corresponding tooth areas (anteroconid, metaco- RESULTS nid, hypoconid, protoconid). The nomenclature of tooth elements follows Čermák (2009) and von Prolagus aff. crusafonti from Popovo 3 (MN 11) Koenigswald et al. (2010). The images were taken (Figures 1, 2) at different magnifications (approximately 1000- The lower p3 enamel consists of a radial and times). Preparation, grinding, and photographing an irregular layer. The boundary between them is were carried out in the Department of Ecology and easily visible and relatively distinct. The morphol- Vertebrate Palaeontology, University of Environ- ogy of the enamel layers is similar to the situation mental, and Life Sciences in Wrocław. in Prolagus oeningensis (von Koenigswald, 1996, The stratigraphic subdivision for the Eastern figure 17) and Prolagus sardus (von Koenigswald Paratethys, used in this paper, follows Topachevski and Clemens, 1992, figure 22). In all three species et al. (1998) and Nesin and Nadachowski (2001). the two layers occur with almost 50% of the total Enamel Ultrastructure of Lagomorph Teeth thickness of the tooth enamel. Only in the area of the entoconid and the posterior part of anteroconid The tooth enamel is made of specific prisms, an irregular layer is present with up to 30% of the which resemble elongated crystals (hydroxyapa- thickness; in its structure it is similar to PLEX (Fig- tite crystallites) and are connected by IPM matrix. ure 1, N. 9003). T h e i rregular layer prisms The prisms may vary in their arrangement, shape, slightly interweave almost in the entire tooth length, and structure, but also in the relative incli- (except for a thinner enamel on the ento- and nation to each other. The lagomorph enamel was hypoconid). A similar structure was observed in initially divided into three basic types which were Prolagus sardus (von Koenigswald and Clemens, adopted from von Koenigswald’s (1980) descrip- 1992, figure 22) and Prolagus oeningensis (von tion of rodent enamel. Later, von Koenigswald and Koenigswald, 1996, figure 17). The arrangement of others (von Koenigswald, 1996; Martin, 2004; von the irregular layer prisms is tangential-like, but the Koenigswald et al., 2010) applied some descriptive tangential layer prisms are arranged mostly at par- terms in the analysis of lagomorph enamel. How- ticular angle to each other and to the vertical axis ever, the difference is that lamellar enamel occurs of the tooth. In Prolagus the arrangement of the only in rodents, whereas in lagomorphs this pattern prisms is quite chaotic (Figure 1, N. 9003, 9006). is included in irregular and HSB types. According

3 RABINIAK, REKOVETS, & NOWAKOWSKI: ENAMEL OCHOTONA AND PROLAGUS

FIGURE 1. Lower p3 enamel ultrastructure; Prolagus aff. crusafonti from Popovo 3, cross-section.

FIGURE 2. Posterior lobe of lower m2 enamel ultrastructure; Prolagus aff. crusafonti from Popovo 3, cross- section. 1- 4, Enamel structure details from four different tooth parts.

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The prisms of the radial layer are densely from that in Prolagus of similar geological age. In packed, gathered in tightly arranged bundles with Ochotona, the prisms are not gathered in bundles surrounding IPM matrix (Figure 1, N. 8999, 9003, like in Prolagus, but form a single structure on the 9006). The structure of the radial layer is constant IPM matrix and are sharpened. In cross section, throughout the tooth; the prism bundles are they are arranged linearly and in the vertical distri- arranged in parallel linear structures and slightly bution they are inclined to each other (the inclina- inclined towards the EDJ border (Figure 1, N. tion is directed to the OES and EDJ borders) 8995). However, there is variation in the thickness (Figure 3, N. 0259, 0260). A non-structured layer of the radial layer, which is thinnest inside the of the enamel type PLEX can be observed in the enamel folds (Figure 1). The linear arrangement of entoconid area next to the OES border (Figure 3, the radial layer prisms is also characteristic of the N. 0261). lower molars of the two compared Prolagus spe- The enamel of the lower m2 (Figure 4) has cies. also two layers – a radial (almost 60-70% of the The enamel of the posterior lobe of the lower total width of the enamel) and an irregular layer m2 of this species (Figure 2.1-4) consists also of (almost 30-40% of the width). The irregular layer two layers with a similar morphology to that of the prisms are inclined to the side and at an angle to p3. The only exception is that the posterior parts of the IPM. Next to the OES border, not very clearly the enamel bands on the posterolophid and anter- visible, we assume the presence of a PLEX layer. olophid (after Čermák, 2009) show 70% of enamel The prisms of the radial layer are arranged almost prisms of the irregular type, which is dominated by in the same way as in the posterior lobe of the vertically arranged prisms, as in the radial layer. lower m2 of Prolagus, but more irregularly. The Also the radial layer prisms are grouped more cha- IPM matrix is faintly visible. otically compared to the situation in p3 and do not The enamel of the upper incisor (Figure 5) of form distinct linear bands (Figure 2). Presumably, Ochotona sp. has also two layers – a radial and a these peculiarities of radial enamel arrangements tangential one. The r adial layer next to the EDJ are species-specific within the genus. The enamel border is made of vertical and inclined prisms, in Prolagus oeningensis (vonKoenigswald, 1996, arranged chaotically (Martin, 1997). The tangential figure 17) is quite similar. Particularly the structure layer consists of slightly intertwined prisms, and of the irregular layer is very similar in all compared occurs often also in the middle of the radial layer. taxa, with the exception of Prolagus aff. crusafonti, A similar situation was reported by v o n Koenig- where it is narrower and more chaotically arranged swald (1996, figure 2) for Ochotona. (not linearly as in Prolagus oeningensis). Next to The longitudinal section of the lower incisor the OES border a very thin layer of the unstruc- (Figures 6.1-2) shows a very well-developed HSB tured PLEX type occurs (Figure 2.1-4). layer with a distinct IPM matrix and a radial layer with weak single prisms (not bundles). HSB struc- Ochotona sp. from Popovo 3 (MN 11) (Figures tures are clearly visible. Such an arrangement of 3-6) the HSB layers distinguishes this form from the As in Prolagus, the enamel of the p3 is com- less structured enamel of Prolagus oeningensis posed of two layers: a radial layer next to the EDJ (von Koenigswald, 1996, figure 3). border and an irregular layer next to the OES bor- Ochotona cf. eximia from Verkhnya Krynytsya der. Parallel vertical prisms occur in the radial 2 (MN 12) (Figures 7-9) layer and somewhat intertwined prisms in the irregular layer. The width of these two layers is – in The enamel of the lower p3 is also double-lay- cross section of the tooth – almost equal, as it is in ered; the irregular layer covers usually less than Prolagus. However, the irregular layer is much thin- 50% of the enamel thickness, and the radial layer ner in the recessed parts of the tooth (up to 20% of more than 50%. The prisms of the radial layer the thickness). It is also thinner in the protoconid are arranged in bundles of linear structure (as in and the metaconid - mesoflexid areas (Figure 3, Prolagus and in the m2 of Ochotona from Popovo N. 0250). The interweaving of the prisms of the 3) (Figure 7, N. 9026, 9032). The irregular layer irregular layer is more structured in comparison to has a different structure from Ochotona sp.- Pop- Prolagus. The bands of this layer are arranged ovo 3, because it has virtually no prisms running irregularly and at different angles to each other vertically (more like tangential layer) and all of (Figure 3, N. 0248). The arrangement of the them are inclined towards the OES (one row) prisms in the radial layer in Ochotona sp. differs and EDJ (the row next to it) (Figure 7, N. 9027,

5 RABINIAK, REKOVETS, & NOWAKOWSKI: ENAMEL OCHOTONA AND PROLAGUS

FIGURE 3. Lower p3 enamel ultrastructure; Ochotona sp. from Popovo 3, cross-section.

FIGURE 4. Lower m2 enamel ultrastructure; Ochotona sp. from Popovo 3, cross-section.

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FIGURE 5. Upper incisor enamel ultrastructure; Ochotona sp. from Popovo 3 , cross-section.

FIGURE 6. Lower incisor enamel ultrastructure; Ochotona sp. from Popovo 3, longitudinal section. 1-2, Enamel structure details from two different tooth parts.

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FIGURE 7. Lower p3 enamel ultrastructure; Ochotona cf. eximia from Verkhnya Krynytsya 2, cross-section.

FIGURE 8. Posterior lobe of lower m2 enamel ultrastructure; Ochotona cf. eximia from Verkhnya Krynytsya 2, cross-section.

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9032). The irregular layer has randomly arranged between the layers is clearly visible, although structures, depending on the tooth region (Figure sometimes it is fuzzy and indistinct. Ultrastructur- 7). The structure of the irregular layer is similar to ally, the irregular enamel is composed of irregular that of the p3 of Ochotona from Popovo 3. How- bands with separate prisms. Such a structure can ever, the prisms of the radial layer are grouped in be classified as an enamel morphologically similar more distinct bundles in Ochotona cf. eximia (Fig- to the tangential type. ure 7, N. 9026). The boundary between the radial In the areas of the outer conids, the irregular and the irregular layer is visible, but quite fuzzy. layer is the thickest and forms more than 50% of The posterior lobe of the lower m2 of this spe- the total enamel thickness. In the tooth recesses cies (Figure 8) displays a similar enamel structure (flexids) this layer is thinner and builds up to 20% as the p3, with a clearly separated, typically struc- of the enamel thickness only. In these areas the tured irregular layer. The radial layer prisms are enamel is less structured, which is particularly grouped in bundles; the IPM matrix is clearly visible characteristic of Prolagus but not of Ochotona. and creates a kind of support for the pile bounds. The enamel is the thickest on the anteroconid The prisms are arranged in parallel IPM bands and the metaconid. It is much thinner on the back directed to the EDJ border. Next to this border side of the entoconid and rarely has only one practically no prisms occur. layer, a radial one. The variation of the thickness of The lower incisor enamel of Ochotona cf. exi- the layers and the arrangement of prisms is more mia shows a radial layer next to the EDJ boundary, pronounced in the irregular layer in Prolagus than with parallel and linearly arranged pile bands, and in Ochotona. For example, the posterior part of the a thin layer of curved HSB enamel prisms bands enamel in the anteroconid is similar to the enamel (Figure 9). The enamel structure is very similar to in the entoconid, with the dominance of the radial those of Prolagus oeningensis (von Koenigswald, layer (Figure 1, N. 8999, 9003). In Ochotona sp. 1996, figure 4) and Ochotona princeps (Martin, from Popovo 3 the prisms are single (Figure 3, 1999). N. 0259), except for the situation in the meta- and entoconid, where they are gathered in bundles OchotonaFIGURE 9. Lowersp. from incisor Lobkove enamel (MN ultrastructure 12/13) (Figure of Ochotona cf. eximia from Verkhnya Krynytsya 2, cross-section. (Figure 3, N. 0261). In Ochotona cf. eximia 10) (Verkhnya Krynytsya 2) and Ochotona sp. (Lob- The enamel of the p3 of Ochotona sp. from kove) the irregular layer is variable, and is more Lobkove is very similar to that of Ochotona cf. exi- primitive and not decussate on the meta- and ento- mia. It has two layers, and the thickness of the conid (Figure 7, N. 9027, Figure 10, N. 9046). The irregular enamel is smaller than the thickness of variation of the enamel thickness on p3 has been the radial enamel. The irregular enamel has a typi- explained in other studies as an indicator of func- cal structure (Figure 10, N. 9041, 9043), and the tional pressure on its different parts. Based on our radial enamel prisms are gathered in bundles (Fig- data and literature information, it can be concluded ure 10, N. 9042). Next to the EDJ border a thin that enamel with a thick and more structured irreg- layer of an indeterminate structure is sometimes ular layer experiences the greatest functional pres- visible (possibly PLEX) (Figure 10, N. 9046). Inter- sure of the tooth. This concerns primarily the estingly, the enamel on the base of the entoconid anteroconids and the outer conids of the p3. Addi- area is thin and consists mainly of a radial layer tionally, in Prolagus and Ochotona the irregular and an amorphous-prismatic structure, which has enamel in p3 is almost identically structured. In not been observed so far in other teeth (Figure 10, Ochotona sp. from Lobkove, this type of enamel N. 9045). has vertical and inclined piles, which may resemble the tangential enamel. The radial enamel is differ- DISCUSSION ent in grouping in bundles, which are arranged in parallel bands directed to the EDJ border. This In Prolagus and Ochotona from the Late Mio- concerns Prolagus and Ochotona, but not Ochot- cene localities of Ukraine the lower p3 enamel is ona sp. from Popovo 3, where similar bundles were composed of two layers - an outer one, consisting found only on the metaconid and entoconid. In of irregular enamel next to the OES border and contrast to Prolagus sardus, P. aff. crusafonti has a an inner one consisting of radial enamel next to less structured irregular layer. The boundary EDJ. In almost all sections of the p3 enamel, the between the layers is hardly visible, the radial layer two-layered structure can be recognised, with the piles are more distinctly gathered in bundles, but dominance of the radial layer occupying more than they are less distinctly arranged in parallel bands 50% of the total enamel thickness. The boundary

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FIGURE 10. Lower p3 enamel ultrastructure; Ochotona sp. from Lobkove, cross- section. towards the EDJ border (Koenigswald and Clem- Also the incisor enamel of Ochotona is made ens, 1992). of two layers - the radial and HSB type in the lower The enamel of the lower molars of Prolagus (Figures 6, 9), and the radial and tangential type in and Ochotona is similar to that of the p3. The the upper incisors (Figure 5). This enamel structure only difference is that the radial and irregular has been described in detail for Ochotona by von layers have a more amorphous structure, caused Koenigswald (1996, figure 1, 2, 5). The enamel by the arrangement of the prisms (Figures 2, 4). In structure of the upper incisors of Ochotona from contrast to the p3, the bundles of piles do not the Late Miocene of Ukraine is very similar to those form parallel linear bands directed to the EDJ bor- of the extant Ochotona princeps (Martin, 1999, fig- der. Particularly this structure is attributed to the ure 7A) and of O. pusilla (von Koenigswald, 1996, radial layer of Ochotona and Prolagus sp. from figure 5). One difference is that the tangential Popovo 3. However, in Ochotona cf. eximia these enamel in the extant Ochotona pusilla is located enamel layers, especially the radial type, are more directly next to the OES border, while in the recent structured (Figure 8). Prolagus aff. crusafonti from O. princeps and O. sp. from the Miocene of Pop- Popovo 3 (Figure 2) has a more primitive (amor- ovo 3 it occurs in the middle of the radial layer. phous) piles arrangement of the radial and irregu- The radial enamel in O. pusilla consists of prisms lar enamel than P. oeningensis: not very clear gathered in structured bundles, in contrast to the radial layer pile bands and a hardly visible bound- situation in fossil Ochotona, where this structure is ary between the layers (von Koenigswald, 1996, more amorphous (Figure 5). However, the lower figure 17). The enamel as a whole is more primitive incisors described by us (Figures 6, 9) have radial in Prolagus aff. crusafonti in comparison to P. and HSB layers, which are very similar to those oeningensis and P. s ardus. described by von Koenigswald (1996) and Martin (1999). The enamel of the lower incisor is also

10 PALAEO-ELECTRONICA.ORG rather similar in the extant O. princeps (Martin, ochotonid taxa from SE Europe like Pliolagomys, 1999, figure 7D). However, in O. cf. eximia from Ochotonoides will be required. Verkhnya Krynytsya 2 the radial layer prisms are collected in bundles and arranged in linear parallel REFERENCES structures (Figure 9) whereas in O. princeps they Agadjanian, A. and Erbajeva, M. 1983. Late Cenozoic are arranged in round-shaped IPM matrix. rodents and lagomorphs of the USSR. Nauka, Based on this investigation, we can conclude 1983:1-189. that the enamel ultrastructure of all the studied Angelone, C. and Čermák, S. 2014. Two new species of teeth of the late Miocene Prolagus and Ochotona Prolagus (Lagomorpha, Mammalia) from the Late are double-layered, consisting of a primitive irregu- Miocene of Hungary: taxonomy, biochronology, and lar type and a radial type. Basically, the two-layer palaeobiogeography. Paläontologische Zeitschrift, structure of the enamel is also specific for the 89:1023-1038. extant Ochotona species (von Koenigswald et al., Angelone, C. and Sesé, C. 2009. New characters for 2010). species discrimination within the genus Prolagus (Ochotonidae, Lagomorpha, Mammalia). Journal of CONCLUSIONS Paleontology, 83:80-88. Čermák, S. 2009. Lagomorpha (Mammalia) of the Plio- cene and Pleistocene of Europe: A revision of Summarizing, we can conclude that: selected taxa. Unpublished Ph.D. thesis, Charles University, Prague. 1 - The dental enamel ultrastructure of late Miocene Čermák, S. 2010. The Late Miocene and Pliocene ochotonids from the Ukraine shows only very subtle Ochotoninae (Lagomorpha, Mammalia) of Europe– differences. The enamel of both premolars and the present state of knowledge, p. 9-28. In Nowakow- molars of Ochotona and Prolagus is basically com- ski, D. (ed.), Morphology and Systematics of Fossil posed of two layers, a radial and an irregular one. Vertebrates. DN Publisher, Wrocław, Poland. The only difference between the two genera is a Čermák, S. and Rekovets, L.I. 2010. Early Pliocene slight difference in the arrangement of prisms. ochotonids (Mammalia, Lagomorpha) from Southern The prisms in the radial layers are arranged in bun- Ukraine. Geodiversitas, 32:107-120. dles except for Ochotona sp. from Popovo 3, where Erbaeva, M. 1988. Pishchukhi kainozoya (taksonomiya, they occur as single elements. The irregular layer is sistematika, filogeniya) (Cenozoic Pikas (Taxonomy, composed of intertwined structures (prisms and IPM Systematics, and Phylogeny). Nauka, Moscow. matrix). Fostowicz-Frelik, Ł. 2010. A new species of Pliocene 2 - In Ochotona sp. m2 from Popovo 3, the radial and Prolagus (Lagomorpha: Ochotonidae) from Poland is irregular enamel layers are more amorphous, which the northernmost record of the genus. Journal of Ver- may be (but not necessarily) related to the great tebrate Paleontology, 30:609-612. geological age of the finds (MN 11). Fostowicz-Frelik, L., Frelik, G.J., and Gasparik, M. 2010. 3 - The extension of the two enamel differs within the Morphological phylogeny of pikas (Lagomorpha: various dental elements (flexids and conids, i.e., Ochotona), with a description of a new species from particularly in anteroconid, metaconid, and entoco- the Pliocene/Pleistocene transition of Hungary. Pro- nid), as it has been shown in several p3s. ceedings of the Academy of Natural Sciences of Phil- 4 - No differences in the enamel layers have been adelphia, 159:97-118. observed between teeth of Ochotona from various Lissovsky, A.A. 2014. Taxonomic revision of pikas late Miocene (MN 11-13) Ukrainian sites. Ochotona (Lagomorpha, Mammalia) at the species level. Mammalia, 78:199-216. 5 - Vertical and horizontal cross sections of Ochotona López Martínez, N. 1974. Taux taxonomique d’évolution incisors are in accordance with data of Ochotona dans l’ordre des Lagomorphes (Mammalia). Bulletin from the literature, showing radial and tangential de la Société Géologique de France, 16:422-430. enamel in the upper, and radial and HSB in the López Martínez, N. 1989. Revision sistematica y biostra- lower incisors. This is probably associated with the tigrafica de los lagomorphos (Mammalia) del neog- different functional load on the two pairs of incisors. eno y cuaternario de España. Memorias del Museo 6 - Since the observed differences between cheek teeth Paleontológico de la Universidad de Zaragoza, of Ochotona of an age interval of almost 12 million Diputación General de Aragón, 1-350. years (MN 11 - Holocene) are very subtle, we López Martínez, N. 2001. Paleobiogeographical history assume that enamel ultrastructure may be taxo- of Prolagus, an European ochotonid (Lagomorpha). nomically useful only to distinguish between larger Lynx (Praha), 32:215-231. taxonomic units (above genus level) within the fam- López Martínez, N. 2008. The lagomorph fossil record ily Ochotonidae. In order to check this, additional and the origin of the European rabbit, p. 27-46. In research on the enamel ultrastructure of Pliocene Alves, P.C., Ferrand, N., and Hackländer, K. (eds.),

11 RABINIAK, REKOVETS, & NOWAKOWSKI: ENAMEL OCHOTONA AND PROLAGUS

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