A new Mammutidae (Proboscidea, Mammalia) from the Late Miocene of Gansu Province, China

The “Yanghecun specimen”, a proboscidean specimen represented by a mandible from Miocene of China and previously described as Gomphotheriidae, is here reviewed and described as a new genus and species of Mammutidae: Sinomammut tobieni. This taxon is a longirostrine mastodon, lacking lower tusks, and bearing a wide last molar with oblique and non-inflated lophids, broad transverse interlophids, and yoke-like wear figures. Phylogenetic analysis of Mammutidae based on dental and mandibular features recovered S. tobieni as sister group of the mastodon Mammut. The longirostrine condition and the well-developed lower incisors seem to be primitive for Mammutidae, while the brevirostry is the derived condition, probably emerged during the middle Miocene (12-11 Mya). However, two derived conditions are recognized to the lower tusks: the absence of lower tusks (S. tobieni) and the occasional presence of vestigial lower tusks (Mammut).


INTRODUCTION
The fossil record of the Proboscidea in China is abundant, however, its diversity is still being discovered, as the temporal distribution range of several genera (Tobien et al. 1986, 1988, Wang and Deng 2011, Wang et al. 2012, 2013).Recently, a very fragmentary fossil of a proboscidean with longirostrine and a tuskless lower jaw from the Miocene of China (GIOTC 0982-9-178, the "Yanghecun specimen" of Wang et al. 2014) was recognized (but not named) as a new genus and species of the family Gomphotheriidae.Also, the authors related this unnamed new taxon to the Asian trilophodont brevirostrine gomphothere Sinomastodon, and proposed to include them both in the subfamily Sinomastodontinae (Wang et al. 2014).DIMILA MOTHÉ, LEONARDO S. AVILLA, DESI ZHAO, GUANGPU XIE and BOYANG SUN Two decades ago, an almost complete proboscidean mandible was discovered in a fi eld work, the "Yanghecun specimen".The specimen is from the Yanghecun locality, Changdao Township, Xihe County, China, probably from the Upper Miocene strata (see Wang et al. 2014 for detailed discussion).Unfortunately, most part of the specimen has been lost and only the right mandibular ramus, bearing m2 (second lower molar) and m3 (third lower molar), as well as a photo of the specimen in situ (Fig. 1a), were preserved.However, a detailed analysis of the "Yanghecun specimen" revealed several morphological features that preclude its recognition as a member of Gomphotheriidae.Instead, these features suggest that the "Yanghecun specimen" is probably a new taxon of Mammutidae.
In this way, the objective of this study is to redescribe the "Yanghecun specimen", providing a formal description and diagnosis for a new genus and species, and presenting its phylogenetic position within the Mammutidae.

MATERIALS AND METHODS
Morphological comparisons were conducted for dental and mandibular specimens of Gomphotheriidae and Mammutidae housed at the collections of the American Museum of Natural History (AMNH), United States; Florida Museum of Natural History (FLMNH), United States; and Gansu Industrial Occupational Technology College (GIOTC), China.
The Mammutidae analyzed here includes all genera described and recognized in the current literature: Zygolophodon (Tobien 1975, Janis et al. 1998, Markov 2004, Codrea et al. 2005, Göhlich 2010), Mammut (Barbour 1931, Shoshani and Tassy 1996, Janis et al. 1998, Markov 2004) and Eozygodon (Tassy and Pickford 1983).We did not include the African taxon Losodokodon losodokius (Rasmussen and Gutierrez 2009) in the phylogenetic analysis, because it is known only by two upper molars (none mandibular, lower molars and/or tusks specimens), and so it is not comparable to the "Yanghecun specimen".Furthermore, some authors suggested that the Eurasian Mammut is polyphyletic (see Markov 2004, Garevski et al. 2012).The taxonomy of Mammut is not the scope of this study.Thus, this genus is represented in our phylogenetic analysis by Mammut americanum (including the temporal distribution from late Miocene to late Pleistocene, from North and Central Americas, see Janis et al.A NEW MASTODON FROM CHINA 67 1998).The Gomphotheriidae specimens analyzed included the taxa Gomphotherium, Tetralophodon, Sinomastodon and Anancus.The molars structures studied here followed the anatomical nomenclature of Tobien (1975).The length and height of the third lower molars (m3) were used to compare Mammutidae and Gomphotheriidae specimens.We performed a phylogenetic analysis with the help of the TNT software (Goloboff et al. 2008) using exact search (Implicit enumeration) in order to elucidate the relationships of the new taxon within the Mammutidae.All characters were unordered and equally weighted (value=1).Additionally to the new taxon here described, the ingroup is composed by all Mammutidae genera (the "Yanghecun specimen", Zygolophodon, Mammut and Eozygodon).We are proposing a new data matrix including thirteen dental and mandibular characters (Table I).In accordance to their relationships to the Mammutidae in Gheerbrant and Tassy (2009), the selected outgroup is represented by the genera Eritreum and Phiomia.

RESULTS AND DISCUSSIONS
Although the specimen GIOTC 0982-9-178 was originally recognized as a member of Gompho-theriidae and more close related to the genus Sinomastodon (Wang et al. 2014), the presences of oblique and non-infl ated lophids, broad transverse valleys between lophids, and wide m3 with yokelike wear fi gures securely includes this specimen in family Mammutidae, which has the zygodont cheek dentition as one of its most important diagnostic feature (Tobien 1975).
The morphology of zygodont molars share some similarities with the bunodont molars of the Gomphotheriidae, as the subdivision of the transverse crests by a median sulcus in half lophs(lophids), which are built up by two or more small cones (the main cusp and the associated mesoconelet; see fi gure 3 of Tobien 1975), and the presence of a variable number of central conules and accessory conelets.
However, the central conules, or anterior and posterior crescentoids (ACr and PCr, respectively), in bunodont molars are pillar-like and markedly separated from the main cusp, while in the zygodont molars, these structures form enamel crests on posttrites (Po) and crest-like crescentoids on pretrites (Pr) (Tobien 1975, Tassy 2014).Furthermore, the wear fi gures in bunodont molars are usually shaped as a simple or double bounded   Although the Mammutidae had a worldwide distribution, absent only in South America, Australia and Antarctica (Shoshani and Tassy 1996), it was one of the less diversifi ed families within Elephantimorpha (Gheerbrant and Tassy 2009).Until now, the most geographically restricted genus was Eozygodon, which is recorded only in Africa (Tassy and Pickford 1983); the widespread genus Zygolophodon is recorded in Africa, Eurasia, North America; and Mammut is recorded in Eurasia, North and Central Americas (Tobien 1975).Notwithstanding, the morphological similarity with other Mammutidae taxa, the specimen GIOTC 0984-9-178 presents several unique features (these will be presented in the sequence).Thus, the specimen GIOTC Etymology-the genus name, Sino, from the latin Sinae, meaning Chinese, plus mammut, in reference to the type genus of the family Mammutidae; and, the species is named after Dr. Heinz Tobien, a great promotor of the research on Chinese Proboscidea.
Type Horizon-Upper Miocene strata, situated in the center of the Xihe-Lixian Basin in the West Qingling fold belt.It is composed of brownish-red silty mudstone and mudstone, partially intercalated with conglomerates, sandy conglomerates, and coarse sandstones.The Upper Miocene is distributed in a band in a gully, unconformity overlying the Xihanshui Group (Wang et al. 2014).
Diagnosis-a new monospecific genus of Mammutidae from China, known from a single robust and longirostrine mandible, with straight, thin and tuskless symphysis (the symphysis region was broken and lost during collection procedures).The zygodont cheek teeth include a trilophodont m2 and a tetralophodont m3.The m3 lophids are compressed anteroposteriorly and obliquely oriented (i.e., antero-lingual to postero-labial direction); its Prs have crest-like ACr and PCr (Pr1 and Pr2 have crest-like PCr and Pr2, Pr3 and Pr4 have crest-like ACr) and Po1 and Po2 have posterior zygodont crests (ZC).A small and weak posterior cingulum (PC) is present distal to the last Po; formed by six small cusps.
Description of material-the mandible has a robust body, with rounded labial portions; the longirostrine symphysis is relatively straight and thin.The original specimen presented a tuskless lower jaw (Fig. 1a).The ascending rami are fragmented and the condyles are not preserved (Fig. 1a).
The cheek teeth include both second (m2) and third (m3) molars (Fig. 2).The m2 is trilophodont, however, its broken at the protolophids level and totally worn; no diagnostic structures are observable on its crown (Fig. 2).The m3 is wide, tetralophodont and has a small PC; the lophids are compressed antero-posteriorly and oblique (i.e., antero-internal to postero-external direction), with clearly yoke-like crests (Fig. 2 and Fig. 3d).The lingual wall is vertical, while the labial wall is more oblique towards the tip of the cusps.The right m3 lophids are worn in different levels, with exposed dentine in all of them, except for the last one (Fig. 2a).The protolophid is completely worn out and its anterior region is obliterated.The metalophid is sorely worn, but the enamel fi gures on Prs and Pos are still visible and the exposed dentine surfaces are medially connected.The last two lophids are slightly worn, but very well preserved; the fourth lophid has reduced width in relation to the anterior lophids.
All m3 Prs and Pos are composed by a developed primary connelet (PCo) and secondary connelet (SCo), which are smaller and weaker than the associated PCo.All right m3 Prs present developed crest-like ACr (Pr1 crest-like ACr is absent or worn out), and the fi rst two also present crest-like PCr (Fig. 3d).The Po3 and Po4 anterior and posterior ZC are absent.The PC of right m3 is small and weak, formed by six small cusps, more developed on the Po side (Fig. 3).There is a small accessory connelet (ACo) on labial side of third interlophid area (IA).The IA is broad and well delineated (Fig. 3d).The crest-like PCr of Pr1 and Pr2 make contact with the crest-like ACr of Pr2 and Pr3, which intersect the fi rst and second IA.The crest-like ACr of Pr4 is slightly worn and do not connect with Pr3 (Fig. 3d).
Differential diagnosis-Sinomammut differs from Gomphotherium and other Gomphotheriidae taxa by having slender and oblique lophids on m3, which is inflated and more parallel in gomphotheres (Fig. 3d and e); by having ZC on m3 Po and ACr and PCr on Pr, which are absent in Gomphotheriidae; and by having proportionally wider m3 teeth (Fig. 4).The combination of a longirostrine and tuskless lower jaw (Fig. 1) differs Sinomammut from all other Mammutidae taxa, which have longirostrine mandible with lower tusks (Zygolophodon and Eozygodon) or brevirostrine mandible with variable presence of vestigial lower tusks (Mammut; see Table II).The presence of a complete ZC only on the Po1 and Po2 differ Sinomammut from Zygolophodon, which has developed ZC on all Pos, and from Mammut and Eozygodon, which have vestigial crests.The poorly  The phylogenetic analysis performed here resulted in only one most parsimonious tree, with 15 steps, the topology as follows: (Eozygodon (Zygolophodon (Sinomammut tobieni, Mammut))) (see Fig. 5).A closest relationship between Sinomammut tobieni and Mammut is supported by one unambiguous synapomorphy: the emergence of the pronounced crest-like lophs/lophids (character 13, state 1; see Fig. 3a to d).The clade (Zygolophodon (Sinomammut tobieni, Mammut)) is supported by two synapomorphies: the straight shape (character 7, state 1) and rounded/oval cross section of the lower tusks (character 8, state 1).The lower tusks in Eozygodon are well developed, elongated and dorsoventrally flattened, with two strong  Tobien (1975), Tassy and Pickford (1983), Shoshani and Tassy (1996) and Wang et al. (2014).The calibrated phylogeny of Mammutidae (following the previously cited literature for temporal range data) allowed the recognition of the diversifi cation of the clade Sinomammut plus Mammut occurred during the late Early-Middle Miocene (17 to 11.6 Mya; Fig. 5).Although features related to mandibular symphysis length (brevirostrine/longirostrine condition) and to lower tusks (presence/absence) did not appear as synapomorphies, we recognize their importance to Mammutidae evolution.The longirostrine condition seems to be primitive for Mammutidae, and this condition is present in the earliest mastodon, Eozygodon, and also in Zygolophodon and Sinomammut.Thus, the brevirostrine condition of Mammut is the derived condition, and it probably emerged during the Middle to Late Miocene (17-12 Mya, see Fig. 5).
Concerning the lower tusks, the primitive condition for the Mammutidae is well-developed incisors, which is present in Eozygodon (see figure 15 of Tassy and Pickford 1983: 64) and Zygolophodon (see figure 39 in Tobien et al. 1988: 150).However, two derived conditions are recognized in the Mammutidae: the absence of lower tusks, as recorded for Sinomammut; and, the occasional presence of vestigial lower tusks or its absence, as seen in Mammut (Barbour 1931, Haynes 1991).The uniqueness of the longirostrine and tuskless mandible of Sinomammut can clearly differ this new taxon and Mammut -the latter is brevirostrine, but occasionally present small lower tusks (Barbour 1931), usually interpreted as sexual dimorphism.In fact, the loss of the lower tusks and the shortening of mandibular symphysis are evolutionary trends observed in parallel to other Proboscidea families (Shoshani and Tassy 1996), such as Gomphotheriidae and Elephantidae, from the late Miocene to Pliocene.Except for the gomphothere Rhynchotherium, which kept the lower tusks during all life span (Lucas and Morgan 2008), and Cuvieronius, which had deciduous lower tusks at immature stage (Ferretti 2008, D. Mothé, unpublished data), all Pleistocene/ Holocene proboscidean lineages (including the two extant elephants genera) are brevirostrine and dibelodont (presence of upper tusks and absence of lower tusks).These evolutionary trends in the mandible of Proboscidea are probably related to the several global climatic and environmental changes, which occurred from the late Middle Miocene on, causing modifications on feeding habits of those proboscideans (mastication mechanics, also modifi cation in skull and molars morphology; see Maglio 1972), and probably included more abrasive vegetation, as C4 grasses, on diet (Janis 1988).

CONCLUSIONS
A new Mammutidae monospecific genus, Sinomammut tobieni, is described based on a longirostrine and tuskless partial lower jaw from

Figure 1 -
Figure 1 -The original record of "Yanghecun specimen".Note the longirostrine symphysis fragmented in two pieces (on the right).(a) Original photo of the complete specimen, an almost complete lower jaw; (b) Reconstructed sketch of Yanghecun specimen based on original picture in (a) by Pablo Lara.The region of the condyles (hachured area) was reconstructed based on Mammut americanum and may not correspond anatomically to Sinomammut.Scale bar: 10 cm.
I Character-taxon matrix used in the cladistic analysis of the Mammutidae, including the new taxon Sinomammut tobieni.Missing data (either due to non-preservation or because non-applicable) are coded as "?".Dental, cranial and mandibular characters are: 1) Antero-posterior compression of lophs/lophids on molars: (0) absent (1) present; 2
developed and lingually oriented PC (mainly behind last Po) differentiates Sinomammut from other Mammutidae taxa, in which the PC is well developed and lingually oriented (mainly behind last Po, as in Eozygodon), poorly developed and parallel to the last Po (Zygolophodon) or well developed and parallel to the last Po (Mammut).

Figure 4 -
Figure 4 -Scatter diagram of late Neogene and Pleistocene Mammutidae and Gomphotheriidae m3 width and length.Note the difference between the Mammutidae cloud (gray dots) and Gomphotheriidae (open dots).Key: Sinomammut tobieni is represented by the black star; the genus Mammut is represented by the gray circles; Zygolophodon is represented by gray squares; Eozygodon is represented by gray diamonds; Tetralophodon is represented by open circles; Sinomastodon is represented by open triangles; Anancus is represented by open squares; Gomphotherium is represented by open diamonds.Data was based onTobien (1975),Tassy and Pickford (1983),Shoshani and Tassy (1996) andWang et al. (2014).

Figure 5 -
Figure 5 -Phylogenetic hypothesis of the family Mammutidae including the new mastodon Sinomammut tobieni.Diagnostic characters and states are described on TableI.
Figure 5 -Phylogenetic hypothesis of the family Mammutidae including the new mastodon Sinomammut tobieni.Diagnostic characters and states are described on TableI.
The authors are grateful to all curators of the collections cited above for allowing the access to the Proboscidea specimens that supported this study; to Dr. ShiqiWang, Dr. Taissa  Rodrigues, Dr. Alexander Kellner, Dr. Marcelo Britto and Mrs. Sabrina Ferreira for improvements in content and English; to the two anonymous reviewers; Conselho Nacional de Desenvolvimento Científi co e Tecnológico (CNPq) and Fundação Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ) granted PhD scholarship funds to the author DM (process numbers 140453/2012-01, 201081/2014-8 and E-26/100.246/2014)and Conselho Nacional de Desenvolvimento Científi co e Tecnológico (CNPq) granted Post-Doctoral scholarship funds to the author LA (248772/2013-9).

TABLE II Sinomammut autapomorphies compared to Mammutidae taxa. Note that the set of features of Sinomammut is unique among the Mammutidae.
Zygodont crests absent.DIMILA MOTHÉ, LEONARDO S. AVILLA, DESI ZHAO, GUANGPU XIE and BOYANG SUN concavities (at the dorsal and ventral sides; Tassy and Pickford 1983).