The European Ruminants during the “Microbunodon Event” (MP28, Latest Oligocene): Impact of Climate Changes and Faunal Event on the Ruminant Evolution

The Earth already experienced numerous episodes of global warming and cooling. One of the latest impressive events of temperature rising was the Late Oligocene Warming that occurred around 25 Mya. An increase of the marine temperature of 2 to 4°C has been observed in a short time interval. In Europe, this major climatic event can be correlated to the continental faunal turnover “Microbunodon Event”. This event is marked by a huge faunal turnover (40% of the ungulate fauna during the first 500k years) and environmental changes. Drier conditions associated to the appearance of the seasonality lead to new environmental conditions dominated by wooded savannahs. This is correlated to a major arrival of Asiatic immigrants. Moreover, from a homogenous fauna during the main part of the Oligocene, local climatic variations between the European Western coast and the more central Europe could have provided faunal regionalism during the latest Oligocene and earliest Miocene. Considering the ruminants, this event is the major ever known for this group in Europe. A total renewal at the family level occurred. Thanks to a precise stratigraphic succession, major evolutionary elements are highlighted. Typical Oligocene species, mainly Tragulina, were adapted to wooded environments and were leaves/fruits eaters. They disappeared at the end of MP27 or the early MP28. This corresponds to the appearance of the Asiatic immigrants. The Tragulina (Lophiomerycidae, Bachitheriidae) and stem Pecora gave way to more derived stem and maybe crown Pecora (e.g. “Amphitragulus”, Babameryx, Dremotherium). These newcomers were adapted to more open environments and mixed feeding. The disappearance of the Tragulina is probably linked to environmental and vegetation changes, and competition. They give way to more derived ruminants having a more efficient metabolism in drier conditions and a better assimilation of less energetic food.


Introduction
Ruminants from two Swiss localities already mentioned in Mennecart 2012 [8], have been integrated in this study (Fig. 1). Balstahl Bännli belongs to the Knauermolasse Formation (synonym of the Aarwangen Molasse and lateral equivalent of the Molasse Alsacienne Formation within the eastern Jura Molasse and the distal Plateau Molasse; [43][44][45]). Following the preliminary analysis of the small mammals (manuscript note in the collection of the Natural History Museum of Basel), this locality has been dated to MP28.
The studied ruminant material only belongs to localities dated to MP28, as this time period corresponds to one of the main faunal turnover with the "Grande Coupure" during the Paleogene. Even if all described ruminants species are already known by several publications (e.g. [17], [20], [50], [51]), new anatomical features are presented here (mandible, teeth and postcranial bones). Prodremotherium elongatum specimens have been the topic of a recent article [52]. Thus they have not been redescribed and reassessed in this work. The main part of the present specimens is unpublished. The ruminants from Gaimersheim1 are for the first time labelled and described. The ruminants from Mailhat were only known by two specimens numbered Br.12 (two upper dentitions: P4-M2 and M2-M3). Unfortunately, only one fossil has been found. Its reinterpretation leads to the description of the tooth row D4-M2 of Lophiomeryx chalaniati. The other ruminant specimens from Mailhat were unpublished. The Swiss specimens were already mentioned in previous works [6], [49], but not firmly described. The ruminants from Pech Desse and Pech du Fraysse have been observed and described, when new characteristics (mandible shape for example) were not included in Blondel [17]. This article presents for the first time the pictures and additional unpublished views of the holotypes of Bachitherium lavocati and "Amphitragulus" quercyi.

Methods
The dental terminology follows Bärmann & Rössner [53] (see Fig. 2) and that of the mandible Mennecart et al. [54]. First, second, and third lower molars are designated as m1, m2, and m3, respectively, and first, second, and third upper molars as M1, M2, and M3. Similarly, upper and lower permanent premolars are respectively designated as p1, p2, p3, p4, and P2, P3, P4, and upper and lower decidual premolars as d1, d2, d3, d4, and D2, D3, D4. The lower canine is named as c and the metatarsal bones as Mt. The astragalus morphology and measurements follow Martinez & Sudre [21]. Uncertain generic attribution for "Amphitragulus"quercyi is expressed with quotation marks. Cranial material of Bachitherium lavocati and "Amphitragulus" quercyi is not described in detail in this article and will be the subject of a separate study. Sizes are given in mm with a precision of 0.2 mm. The first data is the length; the second one is the width.
The chronostratigraphical framework is based on geological time scales for the Paleogene [4], [55]. Classically, European Land Mammal Ages (ELMA) have been described has a succession of reference levels defined by type localities. These localities have been chosen according to their mammal diversity and their geographical location [56]. This relative dating method was first applied to avoid the problem of diachronism among boundaries of various area [56]. Moreover, it was not possible to associate dating that you need using biozones, because "the resolution power of absolute dating was too weak given the fact that much too few calibrations were available for the European Paleogene and their inaccuracy was of the same order of magnitude as the intervals to be measured" [56]. However, Hooker noted that "In practice, because of referral of a fauna other than the reference fauna to a given reference level, a temporal range is spanned and a reference level is thus used in much the same way as a standard assemblage biozone" [4]. Moreover, new data, based on magnetostratigraphy and 40 Ar/ 39 Ar radiometric dating, improve the dating of these Paleogene biozones [57], [58]. Thus, numerous authors use biozones instead of reference levels in the Paleogene of Europe (e.g. [23], [47], [59]). To facilitate the reading and the comprehension of this article, biozones will be used instead of reference levels. Successions and durations of Oligocene mammal zones are established after Vandenberghe et al. [4]. The chosen time period encompasses the faunal transition occurring during the "Microbunodon Event ". To highlight the significance of the ruminant faunal changes during this period, comparisons with older and younger localities is done thanks to recently published data. The poly-cohort analysis follows Scherler et al. [9]. However, contrary to Scherler et al. [9], a focus on ruminant at the species level is done, integrating the new data presented here.

Description
Upper deciduous dentition. All crowns are broken. However, we can observe that D2 is biradiculate and D3 possesses three roots. The D3 is very anteroposteriorly elongated (~12x7mm) with a metaconule relatively salient with a rounded base. The D4 is well-molarized being square in occlusal view. The labial cusps are missing. The protocone is enlarged having the postprotocrista posteriorly oriented and reaching the premetaconulecrista at its middle. The metaconule is narrow and v-shaped in occlusal view with a straight premetaconulecrista. The lingual cingulum is strong and surrounds the entire protocone.
Upper permanent dentition. The upper molars have relatively square outline M2 being larger than M1. The cusps are very selenomorph. The fossae have flat lingual surfaces. The protocone is widely distally open and larger than the metaconule. The preprotocrista is straight and labially oriented reaching the prominent but broken parastyle. The postprotocrista is oblique and joins the premetaconulecrista at its middle part, at a slightly lower height. The premetaconulecrista is elongated, thin, straight, and oblique. It finishes at the level of the mesostyle, located side by side to the labial wall. The postmetaconulecrista is slightly concave and joins the postmetacrista. The metaconule is V-shaped in occlusal view. The paracone and the metacone are aligned labially. The weak paracone labial rib is stronger than that of the labially concave metacone, whereas both possess relatively short and straight cristae. The mesostyle and the parastyle, even if broken, are strong, salient and off-centred from the axis of the labial part of the paracone and the metacone. A metastyle is absent. The anterior cingulum is very strong surrounding the protocone. There is a weaker posterior cingulum, which stops at the end of the metaconule.
Metatarsals. The metatarsal II and III are partly broken. Due to preparation, neither the anterior view can be studied on the MtII nor the plantar view of the MtIII. Both are straight and keep the same size all along the diaphysis. Both bones are fully separated and with a similar thickness of the diaphysis. The better preserved (MtII) has the plantar part broken. The proximal articulation is triangular in shape, with a small depression on its plantar view. A distal rugosity is well marked. The proximal half of the MtIII is missing and the distal keel is worn.
The specimen MNHN LIM148 is very interesting in completing the description of the central metacarpals attributed to a European Lophiomeryx, made by Brunet & Sudre ([29], USTL ACQ 328 from the old collection of Quercy) and by Schlosser ([65], Pl.2, Figs 13 & 14). MNHN LIM148 differs from the Early Oligocene from Mongolia Lophiomeryx gobiae described by Trofimov [66] in having shorter external metapodials II and V. However, Métais & Vislobokova [63] do not consider that Lophiomeryx gobiae belong to the genus Lophiomeryx and Vislobokova [67] proposed that this species is a Hypertragulidae. Nevertheless, the reduction of the lateral digits into bonny stylus appeared several times during the evolution of the ruminants [68].

Description
Mandibles. The mandible is massive with a straight ventral outline in lateral view. The corpus mandibularis becomes regularly larger toward m3. There is no well-preserved angular process. However, the incisura vasorum is not preserved, but does not seem to be pronounced. The angular process and the ramus are very enlarged with a caudal concavity of the ramus edge. The condylar process is high with a very small mandibular incisure. The coronoid process is enlarged and curved. In lateral view, the mandible high abruptly reduces at the beginning of the elongated diastema between p2 and p1. There is a well-developed crest on the dorsal part of the diastema. The caudal edge of the symphysis is at the middle of the diastema. The mandibular foramen is large and located just behind the p1. The European Ruminants during the "Microbunodon Event" Lower deciduous dentition. The d2 is double rooted. The d3 is anteroposteriorly elongated and narrow, very similar in shape to p4. The anterior conid is slightly tilted and enlarged. The mesolabial conid is high and central. It is as wide as the tooth with two relatively long posterior parallel crests. The posterolabial conid is large and forms the posterolabial edge of the tooth. There is no mesolingual conid. The transverse cristid is elongated joining the posterolingual corner of the tooth. The posterior valley is anteroposteriorly oriented. The posterior stylid is extremely reduced. The d4 possesses a flat lingual wall, without metastylid or mesostylid. The lingual cuspids are laterally compressed. They possess small and straight cristids. Anterior and posterior cingulids are absent. The ectostylids are present but very weak. The hypoconid and the protoconid are of the same size. However, the posthypocristid is longer than the postprotocristid. The posthypocristid is oblique and joins the postentocristid. The prehypocristid is oblique and leans on the external postprotocristid. The internal postprotocristid is oblique and joins the postmetacristid. The preprotocristid is anteriorly oriented and short. It ends at the base of the anterior fossa. The anterolabial conid and the anterolingual conid are anteriorly oriented and fused at the anterior edge of the tooth.
Lower permanent dentition. p1 is conical, tusk-like, and slightly curved. The three other premolars are relatively similar. They are laterally compressed. The anterior conid get larger from p2 to p4 and more and more oblique, enlarging the tooth. The mesolabial conid is high and triangular in occlusal view, as wide as the tooth. Three cristids join on the apex of this cuspid. Labially, the anterolingual cristid is oriented to anterior and reaches the base of the anterior conid. The mesolingual conid is absent. The transverse cristid is very elongated reaching the posterolingual edge of the tooth. The posterlabial cristid, on the labial edge of the tooth, joins the posterolabial conid on the three premolars. This cuspid is increasingly developed from p2 to p4. Thus the posterior valley is anterioposteriorly oriented and deep, posteriorly opened on p2 and p3. The posterior stylid encloses this valley on p4. The p2 shows an unexpected feature in having the back valley closed by a conid (maybe homologous to the posterolingual conid), clearly absent on p3 and p4. On p3, an internal ridge can be observed in the back valley or even a small neocrista also observed in some cases on p4. This neocrista seems to be highly variable. An anterior cingulid is present.
The molars are very selenodont. They become larger from m1 to m3. The trigonid and the talonid are relatively small, the trigonid being larger than the talonid. The preprotocristid is oblique and slightly curved enlarging the trigonid. It joins the well-developed premetacristid. Upper deciduous dentition. The D3 is massive. The labial wall is not flattened. The small anterior cone possesses a labial ridge. The globular paracone is in the centre of the labial wall. The anterolingual crista is connected to the posterior crista of the anterior cone. The protocone only forms a cingulum on the anterior edge of the large metaconule. The posterior fossa possesses a metaconule fold. The metacone possesses a big labial rib with an anterior ridge. The metastyle is well developed. The D4 has clearly a shape that prefigures those of upper molars. However, the protocone is smaller giving a shape more trapezoidal to the tooth. The postprotocrista and the premetaconulecrista do not fuse, the postprotocrista being highly elongated and curved. The parastyle is very enlarged. The paracone and the metacone are not labially in line, the metacone being a little oblique. The mesostyle is located on the metacone anterior extremity. The metastyle is small. No cingulum surrounds the D4.
Upper permanent dentition. P3 and P4 has similar lingual wall. The anterior style is globular, salient, and posterior. The anterolabial cone is slightly anterior position and high. The anterolabial cone rib is slightly bulged forming a small rib. The anterolabial crista is straight and aligned. The P3 is sickle shaped in occlusal view. It is slightly laterally compressed. The central lingual cone belongs to the lingual wall forming a small lingual discontinuity on its labial part. On P4, the lingual cone is very enlarged. The fossa is not obstructed by neocristae. The P4 bears well-marked anterolingual and posterolingual cingula, which are almost joining in the transverse axis of the tooth.
The upper molars become larger from M1 to M3. The protocone and the metaconule are similar in size. The preprotocrista joins the base of the straight preprotocrista. The postprotocrista is very elongated and curved ending in parallel of the long and curved premetaconulecrista. The latter is posteriorly forked. The straight postmetaconulecrista joins the base of the postmetacrista forming a smallmetastyle. The metacone and the paracone are not aligned, the metacone being a little oblique. Their cristae are short and straight. The metacone labial rib is weak whereas the paracone one is very prominent with an anterior groove. The mesostyle is large, salient, and prominent, forming a column. The parastyle is well developed at the level of the fusion of the preprotocrista and the preparacrista. There is no ectostyle. The upper molars do not possess cingulum. The fossae are not obstructed by neocristae.

Discussion
The peculiar shape of the p4, without mesolingual conid, is characteristic of the Tragulidae and Bachitheriidae [42], [54], [61]. The combination of a tusk like p1, a very elongated diastema between p1 and p2 and this structure of the p4 is unique among ruminants and indicate the Bachitheriidae [52], [61]. The differentiation between Bachitherium species is mainly based on size differences [20], [64]. Wehrli [69] considered that the size difference corresponds to a sexual dimorphism. But the diastema length [20], the proportions of the postcranial remains [50], [70], and differences in the general shape of the mandible [8], [54], [62], correspond to a species-specific ecomorphology. The p3 and p4 of Bachitherium specimens from Gaimer-sheim1 can possess neocrista within the back valley. Blondel [17] argues that this feature is unique among the Bachitheriidae and is an autapomorphy of the species B. lavocati. However, similar features have already been observed on B. curtum and B. insigne, even if it remains rare [8]. Aiglstorfer et al. [71] have already shown the huge variability in the shape of the traguline p4 within one species. The p4 of the Tragulidae Dorcatherium naui can lack the cristid forming the lingual edge of the tooth with the entire intermediary possible [71]. The size of the teeth studied here is very similar to those of Bachitherium curtum and B. lavocati [8], [17], [20], [64] (see S1 Annex). However, the diastema length of the specimens from Gaimersheim is longer than those of the small B. curtum, what clearly corresponds to the diagnosis of B. lavocati proposed by Sudre [20]. Until now, Bachitherium lavocati was only known in the Pech Desse locality [17], [20].

Description & discussion
The specimen MNHN LIM157 presents a similar morphology to those of Bachitherium in having trochleas not in line. The edges are slightly different in size and high, the external one being bigger. The plantar crest is absent. There is a large plantar projection of the internal lib of the proximal trochlea. Considering the size provided by Martinez & Sudre [21], this fossil is larger Measurements. See S2 Annex.

Description
Mandibles. The corpus mandibulae is slender. The height below the check-teeth remains more or less the same. The ventral profile is very concave. The long diastema between c and p1 possesses a small constriction in its high. The incisura vasorum is weak, blurred, and relatively far from the m3. The ramus is slightly backward oriented and large. The condylar process is quite low.
Lower permanent dentition. Even if mandibles only possess the one tooth socket of a p1 added to p2 (both teeth being rarely separated, excepted for USTL PDS2134), neither p1 nor p2 is recorded. Blondel [17] described for the locality of Pech du Fraysse that the p1 of "Amphitragulus" quercyi is small without more details. The degree of molarization rises from p2 to p4. The mesolabial conid is high. It is placed on the anterior half on p2 and becomes larger on p4. The transverse is cristid backward oriented and becomes elongated from p2 to p4, on p4 it ends the mesolingual conid. This conid is high and strong. The presence of anterolingual and posterolingual cristids (on p4) seems variable. They are absent on the specimens of Pech Desse, but present on the specimens of Gaimersheim1 and Balsthal Bännli giving to the anterior valley a different shape. This latter is nearly closed when the anterolingual cristid is present and widely open when absent. The anterior conid on p4 can be absent (Pech Desse) or present (Gaimer-sheim1 and Balsthal Bännli) forming a forked anterolabial cristid. The posterior conid is becoming larger from p2 to p4, such as the posterior stylid, reaching the posterolingual edge of the p4. On p4, the back valley is ovoid and closed by the partial fusion of the posterolingual conid and the posterior stylid.
On the lower molars, the trigonid and the talonid are closed. The cuspids are bunoselenomorph. The preprotocristid is oblique and joins the premetacristid in the axis of the tooth. The premetacristid is longer on m3 than on m1. The anterior part of m1 is less bulged from m1 to m3, forming a pinched anterior part of the tooth. The internal postprotocristid is becoming longer from m1 to m3, forming a wider trigonid. The external postprotocristid is deep. The oblique prehypocristid is relatively thin and salient. It ends against the postprotocristid. The metastylid is small and salient. The ectostylid is present but becomes smaller from m1 to m3. The talonid is larger from m1 to m3 due to a longer posthypocristid. The posthypocristid is located side by side to the entoconid, but not fused. The lingual cuspids are relatively laterally compressed. They are not in exactly the same axis. As for the entocristids, the premetacristid is longer than the postmetacristid. All the lingual crests are straight. The postentocristid is very short and does not join the posthypocristid. The back fossa is elongated, narrow, and pinched. The hypoconulid forms the edge of this latter. The anterior cingulid is variable, from weak to very strong. The posterior cingulid is quite small.
Upper deciduous dentition. The D2 is anteroposteriorly elongated and laterally narrow. On D2 and D3, the small paracone and protocone are situated on the middle of the tooth. They are laterally compressed. On these teeth, the anterior cone has a large rib on its labial part. Instead of a posterior part formed by the mesostyle, the metacone, and a well-developed metaconule are present on D3 and D4. There is an enlarged posterior fossa. Due to the metaconule on D3 and D4, these teeth are enlarged compared to D2. The metaconule is larger on D4 than D3. On D4, the protocone is sickle-shaped in occlusal view with a postprotocrista transversally oriented. The posterior fossa is enlarged with a premetaconulecrista finishing between the paracone and metacone, and an elongated and curved postmetaconulecrista joins a small metastyle. Paracone and metacone are aligned on D4. On D3 and D4, the mesostyle forms a small column. The labial part of the metacone is relatively flat with a weak rib. The paracone on D4 possesses an enlarged labial rib, and anteriorly a globular parastyle, forming a small column. The cingula are weak and there is no entostyle.
Upper permanent dentition. The three premolars increase in molarization from P2 to P4. Their labial wall is relatively similar. The anterolabial cone is bulbous on P3, and forms a median rib on P4. The anterior style becomes less pronounced from P2 to P4. There is no posterior style. The lingual cone has a median position. It becomes larger from P2 to P4. On P2, it is small and low. On P4, it is as large as the tooth. The enlargement of this cusp leads to a change of the orientation of the lingual cristae from anteroposterior on P2 to transverse on P4.
The upper molar cusps are relatively bunoselenomorph. They have a short and straight postprotocrista labially oriented. The preprotocrista, relatively straight, joins a welldeveloped parastyle. The metaconule is slightly reduced and is larger on M3. The premetaconulecrista and the fossae are simple without neocrista. The posterior fossa is tilted, especially on M3. From straight on M1, the postmetaconulecrista becomes sigmoidal on M3, bypassing the metacone. The labial cusps are in the same axis with relatively straight cristae. The paracone labial rib is salient, but without anterior groove. There is no metacone labial rib. The para-, meso-, and metastyles are salient. The lingual cingulum is very weak to absent such as the entostyle.

Discussion
The recorded structure of the fourth lower premolar is typical for derived stem pecoran and crown pecoran in having a well-developed mesolingual conid and posterior cristid [52], [54]. Moreover, the presence of a tooth socket for the p1 excludes an attribution to Prodremotherium or Mosaicomeryx [52]. Even if the teeth are not as bunoselenodont as in Amphitragulus elegans, the referred specimens have quite primitive features, such as a highly reduced metastylid, a low crown, a small postentocristid, and although laterally compressed, bulged lingual cuspids on lower molars. All of these characteristics exclude an affiliation to either Dremotherium or Bedenomeryx [8], [74]. Furthermore, the extremely small size of "Amphitragulus" quercyi is a distinguishing feature for the latest Oligocene ruminants of Europe [16], [17], [72], [75].

Description
Lower permanent dentition. The lower molar is very badly preserved. However, this big ruminant possesses a fully selenomorph trigonid. The cristid are elongated and the cuspids are high with the enamel slightly pleated. The metastylid is well developed.
Upper permanent dentition. The P4 is badly preserved. All the lingual part is missing. The anterolabial cone possesses a weak labial rib. The anterior stylid is broken. The posterior one is small but present. No neocrista obstructs the fossa. The quadratic upper molars in occlusal view bear a well-developed metaconule slightly smaller than the protocone. The cusps are very selenomorph. The preprotocrista and the postmetaconulecrista are labially oriented and quite straight. The postprotocrista is long, highly curved, and labially oriented. It can be completely isolated (SNSB-BSPG 1952II4855) or fused (MNHN LIM154) to the premetaconulecrista. The latter ends at the axis of the mesostyle. The posterior basin can possess a small metaconule fold on M2, larger on M3. The paracone, possessing a paracone rib, and the metacone, labially flat and concave, are aligned. The mesostyle and parastyle are well developed. They form rounded small columns. The mesostyle is larger from M1 to M3. The entostyle is weak or absent. There is neither a lingual cingulum surrounding the protocone nor a metastyle forming a welldeveloped cuspid. However, small anterior and posterior cingula are present.

Description & discussion
The Babameryx engesseri specimen clearly differs from all other Gaimersheim1 ruminants' specimens. This specimen is much larger than "Amphitragulus" quercyi [8], [17], [75] (S2 Annex), and to a lesser extent bigger than Bachitherium lavocati [17], [20] (S1 Annex), but smaller than Dremotherium guthi [8], [76]. Its size and morphology are in accordance with other described Babameryx specimens. It possesses a regularly concave ventral outline of the mandible. In Bachitherium, the lower outline of the mandible is always straight [20], [42], [54], [62]. Moreover, the teeth of Babameryx are a little more bunodont than those of Bachitherium and Dremotherium [16] in having more bulged lingual cuspids. The trigonid and talonid are reduced due to transverse internal postprotocristid and posthypocristid. Contrary to Bachitherium, the postentocristid and the posthypocristid do not fuse together [16], [42]. The posthypocristid reaches the lingual part of the tooth. The lingual cristids are small in comparison to those of Dremotherium giving to the molars of Babameryx engesseri a sharper and more bunodont aspect [16], [76]. An external postprotocristid is present. The metastylid is very reduced. The anterior and posterior cingula are big and the ectostylid is well developed. This is the oldest occurrence of the species [16].
In conclusion, it is suitable to admit, if all specimens belong to a same fossiliferous layer, that the Mailhat fauna represents the biozone MP28. Considering the presence of non-Pecoran ruminants, absent in younger localities (such as Pech du Fraysse and Ebnat Kappel), Mailhat is older than Pech du Fraysse, but younger than Pech Desse.
There is an acceptance that Lophiomeryx is a member of Tragulina and Prodremotherium is a basal stem pecoran, whereas the phylogenetic position of Bachitherium within the Tragulina is still debated [52], [61]. The other latest Oligocene newcomers ("Amphitragulus" quercyi, Dremotherium guthi, Babameryx engesseri, and a little latter "Amphitragulus" feningrei and Bedenomeryx milloquensis; see Figs. 7 & 8) are considered to be more derived stem Pecora, or even crown Pecora [52], [62], [92]. They all possess a highly derived lower fourth premolar structure being massive and possessing a well-developed mesolingual conid. In Bachitherium, Lophiomeryx, and Prodremotherium this is not the case [52]. "Amphitragulus" quercyi is the first representative of this clade in Europe. It appeared at the same time as Bachitherium lavocati and Prodremotherium elongatum in Pech Desse. "A." quercyi has been listed in Boningen (type locality for MP27; [93]) this could be the oldest record for this species. However, the referred specimens of this locality are too badly preserved to be identified as Pecora ( [47], personal observation). "A." quercyi and Dremotherium guthi were already described from Asia [67], [90]. The immigration of this cohort continued until the beginning of the Miocene where a large diversity of ruminants occurred with no less than seven different genera (Amphitragulus, Andegameryx, Bedenomeryx, Dremotherium, Friburgomeryx, Oriomeryx, Pomelomeryx; [8], [9], [62], [80]. The appearance of derived Pecora in Europe coincides with the temporary disappearance of the Tragulina (Fig. 7).

Causes and consequences of the Ruminant fauna renewal
Environmental changes. The latest Oligocene corresponds to a major faunal renewal among the mammals, such as the rodents [15], the terrestrial cetartiodactyls [9], [17], [18], and the perissodactyls [9], [19], [49], but also among the reptiles, such as the booids [14], and the plants [12], [13]. This crisis is named "Microbunodon Event" [9]. Indeed, the time interval MP27-MP30 (ca. 24.3 and 22.9, [94]) is marked by huge global changes. It began with the Late Oligocene Warming and ended with the Mi1 glaciation [94], which characterizes the Oligocene-Miocene transition. The seawater temperature increased by 2 to 4°C and the temperature on continents by nearly 10°C [6], [10], [15]. This ecological turnover can also be correlated with environmental and sedimentological changes, well marked in the Swiss Molasse Basin. The USM1 deposits, characterised by flood plain deposits ("Molasse Rouge" and the "Untere Bunte Mergel"), change into the USM2 deposits (coal in La Rochette, and gypsum deposits in the Jura Molasse) [82], [86], [94], [95]. This peculiar configuration of wet and dry environment in close area is probably due to paleotopography [82]. The original altitude of the La Rochette mines is estimated at 500 m [82]. The Late Oligocene Warming, associated with the Alpine orogeny, gave birth to changes in the sedimentary processes (flood plain deposits to evaporitic processes) and probably changes in the climate (more arid, warmer, with seasonality) and vegetation cover [4], [12], [82].
Regionalism intensification. The biostratigraphy proposed by the rodents indicates that Pech du Fraysse and Gaimersheim1 are contemporaneous [37]. However, the ruminants are different by the abundant presence of Dremotherium guthi in the French locality, and of Bachitherium lavocati in the German one. This difference could be linked to different paleoenvironments, D. guthi living in more open environment [16]. Considering the cenogram analyses, Southern France and Switzerland communities clearly define a wooded savannah environment [16], [96]. The area of Gaimersheim1 remained an environment relatively similar from the rest of the Arvenian [96]. Gaimersheim1 could have been a refuge area with more wooded environment in an active tectonic context (Fig. 8). Similar observations have been noticed during the latest Oligocene and earliest Miocene, using cenogram analysis [97] and the postcranial skeleton of ruminants [9], [98]. Moreover, different environmental conditions could explain the regionalism of Bedenomeryx, only located in the arid South-western France, and "Amphitragulus" feningrei only found in more central Europe (Fig. 8). "Amphitragulus" quercyi and Dremotherium guthi invaded the entire Europe from a precocious immigration since MP28.
Synecological changes. Considering our analysis, we observe, such as Blondel [17] and to a lesser extent Jehenne & Brunet [99] that the surviving taxa of the Early Oligocene first disappeared in Europe during the Late Oligocene Warming; they are replaced by species from the same family or closely related (Bachitherium and Prodremotherium; see Figs. 7 & 8). Then these taxa totally disappeared and more derived ruminants rose (see Figs. 7 & 8). The paleoecology of the other mammals also changed. Considering the postcranial remains, the mid-Oligocene species are characteristic of wooded environments (Bachitherium curtum, B. inigne, and Mosaicomeryx quercyi), contrary to the latest Oligocene ones (such as Prodremotherium elongatum, Bachitherium lavocati, Dremotherium guthi), which lived in more open habitats [9], [52], [62], [70]. Paleoecological changes have also been observed among other mammal groups. Looking at the rodents, the ratio of omnivorous, soft plant eaters, and very hypsodont burrowing the ground increase, whereas those probably adapted to arid environment disappeared in Quercy [15]. Considering the rhinoceros, the cursorial and mediportal locomotion types are dominating after the "Microbunodon Event", while cursorial type with rare graviportal occurred before [9].
The end of the Oligocene is marked by the appearance in Europe of a seasonality characterized by a dry season [13], [16]. Accordingly, these new environmental conditions led to a major faunal renewal between the primitive families and the more derived Pecora, which possessed a more efficient metabolism and were better adapted to dry habitats. By comparing the fossil Tragulina (Bachitheriidae and Lophiomerycidae) with the living Tragulidae, Janis [100] considered that the primitive European Tragulina are mainly distinguished by forestomach fermentation with a less efficient ruminating system during the Oligocene. Nowadays, the Tragulidae only live in the tropical forests of Africa and South-East Asia [101], [102]. The opening of the environment with fewer forests during the latest Oligocene and the appearance of the seasonality could have been fatal for these primitive ruminants and induced the total renewal of the ruminant fauna during a very short time interval (Figs. 7 & 8).

Conclusion
The latest Oligocene (between MP27 and MP30) is a period of tremendous diversity increase of ruminants in Europe with at least 12 different species from 10 different genera. During the middle Oligocene, only 3 different genera occurred with a maximum of 5 synchronous species. All the Late Oligocene species are only partly contemporaneous and thus their successive occurrence allows for a precise biostratigraphy of the latest Oligocene. For example, MP27 is the last appearance datum of Bachitherium curtum and B. insigne. MP28 is the last appearance datum of Lophiomeryx, the only occurrences of B. lavocati and Prodremotherium elongatum, and the first appearance datum of the more derived "Amphitragulus", Dremotherium, and