Occurrences of Sinolagomys (Lagomorpha) from the Valley of Lakes (Mongolia)

The genus Sinolagomys is an early representative of the family Ochotonidae, appearing first in the late early Oligocene of Central Asia. It is known in China from Shargaltein Tal, Taben Buluk, Ulan Tatal, and northern Junggaria, and a few specimens from Tatal Gol, Mongolia have been published. For most occurrences, the genus is not represented by many specimens. Extensive studies in the Valley of Lakes, Central Mongolia, have produced a large number of sinolagomyin fossils spanning at least 10 million years and belonging to five species: Sinolagomys kansuensis, Sinolagomys major, Sinolagomys gracilis, Sinolagomys ulungurensis, and Sinolagomys badamae sp. nov. Descriptions of these are given, as well as definition of the new species. Sinolagomyins flourished during the late Oligocene and early Miocene and came to occupy vast territories from China through Mongolia and Kazakhstan. The evolution of this ochotonid group is characterized by increasing taxonomic diversity and progressive development of rootless cheek teeth.

Desmatolagus from the Hsanda Gol Formation. However, they did not mention the existence of a different form (later known as Sinolagomys) among a thousand desmatolagin fossils. The genus Sinolagomys stored at the AMNH (New York) is represented by a single jaw fragment with p3-m1 under collection number BAMNH FM: 56648.L ater, based on material collected by the joint Soviet-Mongolian Paleontological expeditions, Gureev (1960) described from the Tatal Gol locality ten different lagomorph taxa, mostly desmatolagins, among which three fragments of ochotonid lower jaw with variable structure of p3 were discovered. One of them was described as new, under the species name Sinolagomys tatalgolicus.
The genus Sinolagomys had been recognised for the first time by Bohlin (1937) from the Oligocene localities of Shargaltein Tal, in Northern China. Early studies of Sinolagomys led to the recognition of three species: Sinolagomys kansuensis, Sinolagomys major, and Sinolagomys minor, the latter renamed by Bohlin as Sinolagomys gracilis (Bohlin 1942).
On the basis of the Tatal Gol specimens and revision of other Chinese ochotonid species, Gureev was of the opinion that Sinolagomys, although unusual, belongs to family Ochotonidae (=Lagomyidae), at that time including surviving species of the Holarctic genus Ochotona. The genus Sinolagomys differs from typical Ochotona in the simple structure of the main diagnostic teeth (p3 and P4-M2) and by retaining reduced cheek teeth roots.
These data allowed Gureev to refer Sinolagomys to an independent group for which he created the new subfamily Sinolagomyinae Gureev 1960. Later some specimens of S. kansuensis were discovered in Oligocene faunas of China (Huang 1987;Wang and Qiu 2000). Also, new species were defined for Miocene faunas of the region; Sinolagomys pachygnathus Li et Qiu and Sinolagomys ulungurensis Tong (Li and Qiu 1980;Tong 1989). This demonstrated that the genus Sinolagomys survived the Oligocene-Miocene transition.
During the last decades comprehensive investigations of the joint Austrian-Mongolian Expeditions were conducted in the Valley of Lakes, Central Mongolia. Field work resulted in the collection of a great number of mammal fossils including lagomorphs in the region (Daxner-Höck et al. 2017, this issue), in particular an impressive number of ochotonid specimens of the genus Sinolagomys now stored in the NHMW (Vienna, Austria) and in the MPC/L (Ulaabaatar, Mongolia). Only fossils of the NHMW collection are considered in this study.
The present paper describes for the first time abundant fossil sinolagomyins collected from more than 50 localities of the Valley of Lakes, spanning in age the early late Oligocene to early Miocene. It is believed that the first archaic ochotonids represented by the genus Sinolagomys appeared by the latest early Oligocene. However, these are poorly preserved and uncommon, in contrast to other late Oligocene lagomorphs. Later, the genus flourished, with significant diversification and increasing abundance. Five Oligocene taxa are known in this region in addition to S. tatalgolicus. Among the ochotonid remains, there are several lower jaw fragments that differ from each other by structure of the valuable diagnostic tooth (p3) and can be recognised as different morphospecies, given the scarce materials. In the future with more material, these may be referred to independent taxa.
The genus continued to flourish through the late Oligoceneearly Miocene demonstrating an exceptional transition of the Paleogene-Neogene boundary. The stratigraphic ranges of Sinolagomys species from Mongolia are shown in Table 1.
By then ochotonids (Ochotonidae) had dispersed over the huge territory of Asia from China and Mongolia in the east through Kazakhstan and beyond in the west (Li and Qiu 1980;Huang 1987;Tong 1989;Erbajeva 1988Erbajeva , 1994Erbajeva , 2007Lopatin 1998;Wang and Qiu 2000;Meng et al. 2006Meng et al. , 2013Bendukidze et al. 2009;Erbajeva and Daxner-Höck 2014;Erbajeva et al. 2016). Sinolagomyinae are a characteristic element of small mammalian assemblages of Central Mongolia (Valley of Lakes). They are a species-rich group playing an important role for palaeoenvironmental reconstruction in the region and they facilitate interregional correlations.

Material and methods
New material is stored in the collection of the Natural History Museum of Vienna, Vienna, Austria. A second rich lagomorph collection from the same fossil sites is housed in the Mongolian Paleontological Center, Academy of Sciences, Ulaanbaatar. Fossils were collected during eight field seasons since 1995 by teams of the Joint Austrian-Mongolian Projects (FWF: P-10505-GEO, P-15724-N06, and P-23061-N19) through screen washing and as surface finds on exposed deposits.
Type specimens and fossils of the genus Sinolagomys from the localities Shargaltein Tal, Taben Buluk, and Ulan Tatal were examined in the collections of the Institute of the Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China. Type specimens of S. tatalgolicus from Tatal Gol and Sinolagomys sp. from Hsanda Gol were studied in the collections of the Paleontological Institute, Moscow, and American Museum of Natural History, New York, respectively.
Lingual borders of upper teeth (P4, M1, M2) slightly rounded; protocone larger than hypocone; enamel band is well developed across perimeter of tooth, but its thickness is variable. P2: not known in our materials. However, Bohlin (1942, p. 92, T.b. 586a, fig. 27c) illustrates P2 with one anterior fold. P3: oval-trapezoidal outline, tooth slightly longer on lingual part than labially, its anterior width significantly less than posterior width; paraflexus moderately deep; anteroloph extends to half of tooth width; internal hypostria short with little cement (Figs. 1a and 2a) P4: in contrast to P3 tooth much wider anteriorly than posteriorly. No basic changes in P4 structure occur in Sinolagomys major from the late early Oligocene to early Miocene; all known specimens of P4 with the distinctive, characteristic significantly greater anterior width. Hypostria relatively short, extending across half of tooth width, with little cement; the type specimen from Shargaltein Tal (P3-M1, Sh. 830, fig. 58, Bohlin 1937, p. 34) is characteristic, with rather short hypostria (Figs. 1b and 2c). M1: smaller than preceding tooth, anterior width of tooth slightly broader than, or equal to posterior width; enamel band well developed on the anterior and lingual margins of tooth; hypostria relatively deep, extends across half of tooth width or slightly more, filled with cement (Figs. 1a and 2d) M2: small, anterior width of tooth exceeds posterior one; internal side of tooth inclined much towards postero-internal corner; hypostria deep, extends almost external to border of tooth ( Fig. 2a) M3: small, rounded, but usually lacking. The unique P3-M3 from the site HTE-008 (NHMW 2011/0389/0089) contains this tooth (Fig. 2a, Table 2).
Mandible relatively high, slightly robust (depth below p4 7.0-7.3 mm; width 5 mm), root of lower incisor extending to below the talonid of m2 forms marked convexity on both labial and lingual surface of mandible. Anterior foramen mentale located in front of p3 on the level of mid-height of mandible, the other two mental foramina are under p4. Enamel band well developed in all borders of lower teeth (p4-m2) except the anterior margin. p3: rectangular shape with rounded margins; anterior border flat or with shallow depression with little or no cement; antero-external fold filled with little cement (Fig. 2b) p4-m2: trigonids wider than talonids (Table 3) having oval shape, enamel band is thick on the posterior margin of conids. m3: small oval conid, however in one specimen it is tiny (m2-m3, NHMW 2013/0194/0004). Similar small m3 was found in lower jaw of Sinolagomys major from Ulan Tatal (Huang 1987, fig. 12) and in one mandible of Eurolagus from La Grive, France. Discussion: S. major from the Valley of Lakes resembles the type specimen from the locality Shargaltein Tal (Bohlin 1937, fig. 58;Sh. 830) in size and general structure of teeth, but differs by deeper hypostria of upper teeth; however, the ratio of the trigonid and talonid width in p4-m2 (Sh. 270, paratype) is similar.
S. major is known from the locality UlanTatal, China (Huang 1987). It is close to the population from the Valley of Lakes in size, the morphological structure of teeth, and lack of roots. This species is mentioned as well in the late Oligocene fauna of the northern Junggar basin, China (Meng et al. 2006).
Lower jaw is relatively robust; the incisor extends posteriorly along the ventral border of the mandible to the end of m1. The first foramen mentale is located slightly anteriorly to p3 and the second below m1. p3: rectangular shape; anterior border of tooth is smooth or with shallow depression, without cement; antero-external fold filled with cement; the enamel band is missing on the external and posterior borders of tooth, whereas it is quite thick along anterior and lingual margins.
In lower teeth (p4-m2), trigonid is wider than oval shaped talonid (Figs. 3b and 4a). Discussion: Sinolagomys kansuensis from the Valley of Lakes resembles the type species from the locality Shargaltein Tal, China, by the general structure of teeth, but differs significantly by lack of roots and by slightly larger size (Tables 4 and 5). Moreover, it differs by ratio of the trigonid and talonid width in p4-m2: in Mongolian specimens, the breadth of the trigonid is slightly larger than that of the talonid in contrast to the nominative species from China in which the trigonid is much wider than the talonid. The studied sample is similar to S. kansuensis from the locality UlanTatal, China, in size, in lack of roots and general morphological structure of teeth (Huang 1987, fig. 11).
Late Oligocene to early Miocene S. kansuensis dispersed westwards over the Northern Junggar Basin, China, and reached the Aral region in Kazakhstan. In the Junggar Basin, S. kansuensis is listed in the Teersihabahe and Suosuoquan Mammal assemblages (Meng et al. 2006(Meng et al. , 2013. In Kazakhstan, the species is mentioned by Bendukidze et al. (2009) from localities Altyn Schokysu and Akotau. The Kazakh form resembles the Mongolian sample in similar structure of teeth and size, but differs in retaining rudimentary roots.
Lingual borders of upper teeth (P4, M1, M2) slightly rounded; protocone and hypocone are almost equal in size; enamel band is well-developed across perimeter of tooth, but its thickness is variable-relatively thick in the anterior margin of upper teeth and posterior borders of lower teeth and thin respectively in posterior border of upper and anterior border of lower teeth. P2: oval shape, with shallow or absent anterior groove, lacks cement (NHMW 2013/0376/0001 and NHMW 2013/0376/ 0121) P3: with moderately deep paraflexus; anteroloph extends to mid-width of tooth; internal hypostria with little cement; protocone and hypocone of identical size; hypostria in upper teeth (P4-M2) filled with cement; depth of hypostria is variable: in P4 it reaches the middle of the tooth, and in M1 and M2 it is much deeper, may reach the external border of teeth (Fig. 5a, b).
Lower jaw relatively low, not robust; root of lower incisor extends to the talonid of m1; anterior foramen mentale located in front of p3 or below it at midlevel of mandible p3: small, rectangular shape with rounded margins; anterior border with shallow depression without cement or with relatively deep and filled with cement. Antero-external fold with little cement. In p4-m2 trigonids wider than talonids, which are of oval shape (Figs. 5c-f and 6c) m3: a small rounded, oval conid Discussion: This small Mongolian ochotonid resembles the type series of Sinolagomys ulungurensis in general dental features and size of the teeth and undoubtedly belongs to this species. As in the type material, the Mongolian form is characterized by highly variable morphological structure of p3, in particular by the groove on the anterior margin of tooth which varies from shallow without cement to relatively deep and filled with cement.
S. ulungurensis is close to S. gracilis and S. badamae n. sp. in its small size, but it differs from them by p3 having a groove or depression on the anterior margin of tooth. It differs from the species S. major, S. kansuensis, S. tatalgolicus, and S. pachygnathus by its relatively smaller size, by its more complicated p3 with well-developed anterior grove or depression. Moreover, it differs from S. kansuensis by having rootless teeth. Bohlin, 1942 (Figures 6a, b,   Description: Small-sized ochotonid, rootless, hypsodont teeth. P3 with relatively deep paraflexus; anteroloph moderately long, slightly exceeds half of tooth width; small internal hypostria with little cement; protocone slightly larger than hypocone. Metastyle small, follows from the occlusal surface downwards. Lower jaw relatively gracile (width below p4 is 2.7 mm), lower incisor extends to below the trigonid of m2, forming a moderate tuberosity on the lingual side of mandible. Below the tuberosity is a well-marked depression, which gradually shallows towards the ascending ramus; lateral surface of mandible smooth. Anterior foramen mentale located below p3, slightly above the ventral border of the mandible, posterior foramen under boundary of p4 and m1.

Sinolagomys gracilis
Enamel band of p3 well-developed along perimeter of tooth except at the anterior margin (Fig. 6a, b) Fossils of S. gracilis are not numerous in Mongolian faunas as is the pattern in China.
Discussion: A small ochotonid from Shargaltein Tal, Gansu, China, was described by Bohlin in 1937 as Sinolagomys minor (type Sh 96, P3-M1) on the basis of small size in comparison to S. kansuensis and S. major. Later, Bohlin (1942) revised all small ochotonid materials from Shargaltein Tal and Taben Buluk and he discovered that the type (Sh 96) cannot be distinguished from S. kansuensis by size. Given additional materials of small forms, he erected another new small-sized species S. gracilis based on another specimen (left p3-m2, Sh 434).
He wrote (Bohlin 1942, p. 100) B…the name gracilis was substituted for Bminor^as the species to which this latter name (minor) was attached was based on doubtful material^. The fossils of S. gracilis in contrast to the other species (S. kansuensis, S. major), although scarce, are known from both localities Shargaltein Tal and Taben Buluk.
S. gracilis from the Valley of Lakes is close to the type material in the general structure of teeth and in having a similar ratio of the trigonid to talonid width; however, it differs from the type specimen by slightly smaller size (Fig. 6a, b; Table 8). This species differs from S. kansuensis, S. major, S. tatalgolicus, and S. pachygnathus by its much smaller size and by having talonid width practically equal to trigonid width in p4-m2. In other species, the trigonid of p4-m2 is much wider than the talonid.
S. gracilis differs from S. badamae sp. nov. and S. ulungurensis by slightly smaller size and from the latter by lacking a depression on the anterior border of p3. S. badamae sp. nov. differs from S. gracilis by having prominent, rounded anterior margin of p3. In addition, S. kansuensis differs from S. gracilis in its rooted teeth.
Sinolagomys badamae sp. nov. (Figure 4b, Table 9) Derivatio nominis: In honor of D. Badamgarav †, Mongolian co-leader of the research team and outstanding Mongolian geologist  -From the largest species S. major, by much smaller size and prominent p3 -From S. kansuensis by smaller size and prominent p3, lack of roots in S. badamae -From S. pachygnathus by prominent p3, smaller size and by the much wider trigonid than talonid in S. badamae -From S. gracilis by slightly larger size, by greater breadth of trigonid relative to talonid (width of talonid in S. gracilis approaches that of the trigonid) -From S. ulungurensis by lack of depression on the anterior margin of p3, by much wider trigonid than talonid (trigonid only slightly wider in S. ulungurensis) -From S tatalgolicus by lack of deep depression on the anterior margin of p3 and smaller size Description Small-sized ochotonid (Table 9) P3: rootless, oval-trapezoidal outline, its anterior width relatively less than posterior width; paraflexus moderately deep; anteroloph extends to 1/3 of tooth width; internal hypostria short, with little cement. Along external border of the tooth, thin plate follows from the occlusal surface towards root. Mandible relatively high and robust (depth below p4 5.0-5.2 mm; width, 3.2-3.3 mm); the base of lower jaw is wide; the lower incisor extends to the talonid of m1 forming marked tuberosity on both lateral and medial surfaces of mandible. Anterior foramen mentale located anterior to p3 at mid-level of mandible. The thickness of enamel band in lower teeth (p3-m1) varies: it is well developed along the perimeter of teeth, except for the anterior margin of trigonid and lingual part of talonid. p3: rectangular shape with rounded borders; anterior margin of tooth prominent, lingual and posterior margins are practically straight; anteroconid elongated; enamel band is well developed on all borders of tooth; antero-external fold of tooth is relatively shallow, with little cement. p4-m1: trigonid significantly wider than talonid; in the holotype, both labial and lingual edges of trigonid in p4 and m1 are relatively sharpened to acute angles, but in the paratype, they are slightly rounded; in all specimens, the posterior margin of the trigonid has a short sharp projection and the structure of the talonid is the same; talonid is oval or egg-shaped, with rounded lingual and sharp labial edges, enamel band well developed along posterior border of talonids. Discussion: Sinolagomys badamae sp. nov. differs from all other species of the genus by the morphological structures of teeth and size as noted above. The species is characterized by advanced features such as lack of roots and the peculiar, prominent anterior portion of p3; however, some archaic characters are retained as well. Archaic features are much wider trigonid than talonid, lower incisor extending far posteriorly (to the talonid of m1), and mandible relatively robust despite the small size.

Conclusion
Fossils of Sinolagomys are rather well-preserved across the Oligocene to Miocene informal biozones C1-D of the Valley of Lakes in Central Mongolia. First very rare occurrences are evidenced in biozone B (two specimens) and in biozone C (one specimen), but the main distribution of the genus was during the biozones C1, C1-D, and D. The comprehensive analysis of the entire collection shows that several Oligocene species were distributed from the northern part of China to Central Mongolia and Eastern Kazakhstan. The diversity and abundance of Sinolagomyinae is highest in Biozone C1, and they appear to be an endemic taxon of Central Asia. The Neogene record of Sinolagomys in Central Asia continues in the early Miocene with the appearance of S. ulungurensis alongside the Oligocene species S. major and S. kansuensis.
No significant morphological changes in tooth structure of S. major and S. kansuensis from the Valley of Lakes sites are observed during the early late Oligocene and Miocene. Possibly, these species were rather conservative forms that persisted on landscapes under environments that did not change greatly.
The fossil history of the Ochotonidae offers clues to the palaeoclimate of the mid-Cenozoic world, especially for the palaeoecology of eastern Asia. The diversity patterns observed among fossil representatives indicate the changing conditions of dominant climatic patterns. Heightened fossil diversity is slowly emerging and indicates an increasing component of open habitat in a mosaic of grasslands and woodlands during the middle Cenozoic in Asia. This led to the development of the main ochotonid adaptive type. Inhabiting open landscapes and taking grass as nourishment, sinolagomyins are distinguished by increasing hypsodonty of the teeth at the early stage of their evolutionary development. Well-developed roots were lost as crown height increased, and root closure occurred late in ontogeny, yielding Brudimentary roots^(closed pulp cavities at the base of teeth). Later, Brudimentary roots^were lost completely as the teeth became fully hypsodont with open pulp cavities. Erbajeva et al. (2015) summarized much of the known record of Neogene and late Paleogene ochotonids, especially Asian records. There are additional important records of early Ochotoninae, such as early Miocene Alloptox (Mizuhoptox) from Japan (Tomida 2012). Apparently, the Neogene was the time of diversification and increasing abundance of advanced ochotonids. Oligocene Sinolagomyinae, rather than Ochotoninae, characterized late Paleogene assemblages of Asia. Now it is clearer that Sinolagomyinae were actually rather abundant in the late Oligocene and early Miocene of Asia. A hypothetical scenario for ochotonid evolution may be proposed.
A long, sustained period of global cooling characterized the late Eocene, leading to climatic oscillations during the Oligocene Epoch (BZoogeography of Paleogene Asia^1974; Berggren and Prothero 1992;Zachos et al. 2001). Until the late Oligocene, early ochotonids were uncommon elements in terrestrial communities. With global cooling and growing seasonality of precipitation, habitats changed, becoming more open, and primitive ochotonids of the subfamily Sinolagomyinae flourished. Locally they became common, as in the Valley of Lakes, Mongolia (Tab. 1). The genus Sinolagomys is the earliest species-rich form of the subfamily, and it flourished during the late Oligocene and early Miocene. We hypothesize Sinolagomys as a characteristic element of small mammal assemblages of eastern Asia in which subtropical forests had been replaced by landscapes with open woodlands and xerophytic vegetation.