A “preglacial” giant salamander from Europe: new record from the Late Pliocene of Caucasus

Disarticulated cranial

The oldest known cryptobranchids were reported from the Late Mesozoic of Asia, i.e., Chunerpeton tianyiensis Gao & Shubin, 2003, Eoscapherpeton asiaticum Nesov, 1981, and Eoscapherpeton gracilis Nesov, 1981(Skutschas 2009, 2013).Recent phylogenetic analyses recovered Chunerpeton Gao & Shubin, 2003, previously hypothesized to be a basal (stem) member of the Cryptobranchidae, as instead belonging in the stem-group Caudata (Rong et al. 2021;Jones et al. 2022).The position of Eoscapherpeton Nesov, 1981 as a basal Cryptobranchidae is supported by several features (midline contact of the dorsal [alary] processes of the premaxillae, frontal-maxillary contact, parietals strongly overlapped by the frontals, absence of a distinct medial process of the pterygoid and presence of pterygoid-parasphenoid contact; see Skutschas 2013), but its assignment to cryptobranchids has never been tested by a formal phylogenetic analysis.
The North American cryptobranchids are represented by Andrias matthewi (Cook, 1917) from the Miocene of the United States and Andrias (orig.Cryptobranchus) saskatchewanensis Naylor, 1981 from the late Paleocene of Canada and the early Eocene of United States (Meszoely 1966;Naylor 1981;Holman 2006).The taxonomic status and generic allocation of both species are unresolved because of the fragmentary nature of the fossil material (Dubois et al. 2022).Other cryptobranchid fossils come from the Pleistocene and are assigned to the modern hellbender, C. alleganiensis (Holman 2006).Cryptobranchus guildayi Holman, 1977, from the Pleistocene of the United States is considered conspecific with C. alleganiensis (Bredehoeft & Schubert 2015).
The European cryptobranchids include the widely distributed Andrias scheuchzeri (Holl, 1831), ranging from the late Oligocene to the Late Pliocene of Central Europe (Estes 1981), and the stem cryptobranchid Ukrainurus hypsognathus Vasilyan, Böhme, Chkhikvadze, Semenov, Joyce, 2013, described from the Late Miocene of Ukraine (Vasilyan et al. 2013).Additional records of the family (not identified below the family or genus levels) have been reported from several Cenozoic European and Asian localities (e.g.Shikama & Hasegawa 1962;Chkhikvadze 1982Chkhikvadze , 1984;;Vasilyan et al. 2017;Georgalis et al. 2019).The geologically youngest and easternmost European records came from Ruscinian (MN 14) of the Kuchurgan locality in Moldova and the Antipovka locality in Russia (Chkhikvadze 1981;Averianov 2001).These remains are important for documenting the distribution of cryptobranchids in Eastern Europe, but they are still undescribed.Recently, fossil bones of a giant salamander were discovered at Belorechensk, a new Eastern European locality yielding Late Pliocene vertebrates that are younger than those from the Kuchurgan and the Antipovka localities.Here we describe remains of the giant salamander from the Belorechensk locality, infer the individual age of this salamander, and discuss its paleoecological context.

MATERIAL AND METHODS
The cryptobranchid remains described below come from the Belorechensk locality, on the left bank of the Belaya River near the town of Belorechensk, Krasnodar Region of Russia (Fig. 1).The Belorechensk locality was discovered in 2021 by a joint expedition of the Geological Institute of RAS (Moscow, Russia) and the Southern Scientific Centre of RAS (Rostov-on-Don, Russia).The cryptobranchid remains were recovered during the field seasons of 2021 and 2022 from the bone-bearing clay layer of the Belorechensk Formation.The Belorechensk Formation overlays the Upper Miocene Gaverdovsky Formation along the Belaya River.The Belorechensk Formation is represented by pebbly deposits with interbedded layers of clays and sands and has a total thickness up to 100 m (Beluzhenko 2006)   desCription Frontal Both left and right frontals are almost completely preserved (Fig. 2).They match each other along the medial suture, which indicates they came from the same individual.The length of the complete specimen is 54.5 mm.The medial suture is markedly thickened dorsoventrally and interdigitated.The frontal is widest anteriorly and becomes narrower posteriorly, without a lateral constriction in the olfactory region.The dorsal surface is shallowly convex and smooth.The anteromedial portion of the bone is broad and forms a triangular facet for a nasal; the anterolateral portion is extended anteriorly and forms a narrow facet for a maxilla; and the lateral portion forms a facet for a prefrontal.Judging by the size of the facet on the frontals, the nasals overlapped the frontals for the anterior 30% of the length of the frontals.The ventral surface of the frontal is shallowly concave.The ventral surface bears the anterior portion of the roof of the cranial cavity and, posteriorly, an elongate facet for a parietal (Fig. 2E, H).The anterior portion of the cranial cavity is elongate and subtriangular in outline, narrowing posteriorly.Its anterior margin is straight and indistinctly bordered, whereas the lateral and posterior margins have sharp edges; the anterolateral margin has a bump.A shallow olfactory tract is visible in the olfactory region of the left frontal (Fig. 2E).

Dentary
The dentaries are represented by a complete right ramus and the anterior part of the left ramus (Fig. 3).They are long, slender, and slightly compressed labiolingually.The length of the complete specimen is 109.5 mm in straight line distance between its posterior and anterior tips and 120.2 mm along the curvature of its labial surface.The height of the dentary is 9.2 mm at the symphysis and 14.4 mm at the middle part of the tooth row.The symphysis is wide, convex, and roughly rhomboid in outline.The symphyseal surface is slightly rugose, mostly in its medial part, which suggests high mobility of the mandibular symphysis (Cundall et al. 1987).In lingual view, the dental lamina is of the same height throughout its length.The subdental lamina is half as high as the dental lamina or lower.The sulcus dentalis (subdental shelf ) is wide and slightly concave along its anterior portion, but flat and narrow along its middle and posterior portions.It bears several small foramina.The margin of the sulcus dentalis is clear and rounded in PIN 5882/3, but acute along its anterior part in PIN 5882/4.The Meckelian groove is deep and extends anteriorly to a point below the 26-28 tooth positions (as counted from the anterior end).The corpus dentalis is smooth and flattened anterior to the Meckelian groove.Ventrally, it becomes thinner and ends with a ventral keel.In labial view, the surface of the dentary is only slightly rugose.The eminentia longitudinalis is clearly developed throughout the bone.A few small neurovascular foramina extend below the eminentia longitudinalis.The tooth row contains 80 small and closely spaced pleurodont teeth.The tooth crowns are completely missing, but the pedicellar portions show that the teeth were narrow, as in other cryptobranchids.Internally, the dentary is compact and encloses a few small and medium-sized neurovascular cavities and canals (Fig. 3D).In the region containing the anterior part of the tooth row, the cavities are mostly located below the subdental shelf.In the regions containing the middle and the posterior parts of the tooth row, the cavities are located above and below the Meckelian groove.There are no cavities in the area of the Meckelian groove and the ventral keel.

Prearticular
The prearticular is represented by the right element lacking its anterior and posterior tips (Fig. 4).It is low anteriorly and posteriorly and highest in the area of the coronoid process.The coronoid process is large, but short anteroposteriorly, nearly triangular, and tilted posterolingually.The articular facet is narrow and smooth.The dental facet widens posteriorly and has a sharp dorsal border that forms the lingual border of the coronoid process.It occupies about half of the length of the coronoid process.

Vertebrae
The vertebrae are represented by five nearly complete specimens from the trunk region (Fig. 5).The centrum is deeply amphicoelous, antero-posteriorly short and hourglass-shaped in lateral view, and circular in anterior and posterior views.which are most visible across the distal portions (Fig. 5M).Most of the observed articular zygapophyseal surfaces have six or seven growth ridges.The interzygapophyseal ridges are not developed.

Femur
The femur is represented by its distal portion only (Fig. 6A-G).
It is asymmetrically rounded, being convex dorsally and concave ventrally.Cross-sections of the femur (Fig. 6E) show a thick cortex with a few vascular canals and/or erosion cavities in the proximal part of the preserved fragment, i.e., near the diaphyseal region, and a dense vascular network of canals in its distal part.The vascular canals open into grooves on the bone surface.

Rib
The rib is represented by a single proximal fragment (Fig. 6H-L).
It is anteroposteriorly flattened and medially slightly concave.The articulation surface is hourglass-shaped with narrow upper and wide lower portions.Ridges extend along the upper and lower margins of the rib.

CoMpArison And reMArks
We suggest that all listed bones come from a single individual because they were found close to each other, correspond well to each other in size and type of preservation, and there is no duplication of elements.
The giant salamander from Belorechensk can be assigned to Cryptobranchoidea and Cryptobranchidae (e.g.Gao & Shubin 2012) in having large body size, frontals strongly overlapped onto parietals, anterolateral extension of frontal, absence of the spinal nerve foramina, and unicapitate trunk ribs.
According to the criteria of Gubin (1991), the giant salamander from Belorechensk can be assigned to Cryptobranchinae based on its relatively small size, tooth bases situated directly above sulcus dentalis, and prezygapophyses situated above the base of the neural spine.However, 80 teeth in the dentary are too many for Cryptobranchinae, which are supposed to have 60-75 teeth (Gubin 1991).On the other hand, the cryptobranchine Andrias scheuchzeri has been reported to have as many as 82 teeth (Böttcher 1987).Therefore, it seems that the distinction between Cryptobranchinae and Aviturinae (sensu Gubin 1991) has to be revised with respect to this, and possibly to other, characters.The lack of consistent differences in other characters has been mentioned earlier (Vasilyan et al. 2013).
The cryptobranchid from Belorechensk clearly differs from the Paleogene species Aviturus exsecratus (Gubin 1991;Vasilyan & Böhme 2012) in a number of characters, i.e., its smaller overall size, markedly slender bones, different shapes of the frontals and the cranial cavity, a narrower and deeper sulcus dentalis of the dentary, a lower subdental lamina, absence of developed presymphyseal sulcus, fewer teeth, a markedly vaulted neural arch of the vertebrae, the absence of interzygapophyseal ridges, a poorly developed accessory alar process, and the presence of a depression on the posterior surface of the transverse process.It differs from another Paleogene cryptobranchid, Zaissanurus beliajevae (Chkhikvadze 1982), in having lower subdental laminae.
The cryptobranchid from Belorechensk differs from Ukrainurus hypsognathus from the Late Miocene of Ukraine in having its dentary slender and lower, the corpus dentalis and the subdental lamina both lower, the subdental shelf anteriorly concave, the lingual crista absent, the neurovascular foramina smaller, the labial side of the dentary nearly smooth, and the dentary facet of the prearticular situated more posteriorly (Vasilyan et al. 2013).It shares with U. hypsognathus the short and broad shape of the coronoid process of the prearticular and may have extremely elongated, elliptical prezygapophyseal articulation surfaces (Fig. 5L).
Among the Recent genera, the cryptobranchid from Belorechensk can be assigned to Andrias based on the frontals excluded from the narial opening (not excluded in Cryptobranchus) and a larger angle (about 40 degrees) between the neural spine and the axis of the vertebral centrum (19-37 degrees in Andrias vs 15-20 degrees in Cryptobranchus) (Estes 1981).Westphal (1958) could not diagnose modern Andrias species based solely on osteology.Some relevant characters were mentioned by Meszoely (1966): the shape of the orbit and the separation between the pterygoid and the maxilla.Unfortunately, neither of these features can be observed in the cryptobranchid from Belorechensk.Finally, Estes (1981) could not find any differences between A. scheuchzeri and A. davidianus, and he placed the latter within A. scheuchzeri.Comparisons between the cryptobranchid from Belorechensk with Andrias japonicus and Andrias davidianus are difficult, because we are not aware of any publications listing osteological characters diagnostic  of these modern species.Nevertheless, it seems possible to differentiate the cryptobranchid from Belorechensk from modern species of Andrias by its frontal not being laterally constricted in the olfactory region and having a longer contact with the nasals (Fig. 7A-C) and by the coronoid process of its prearticular being broad and long (Fig. 4).The cryptobranchid from Belorechensk seems closer to A. davidianus in having the cranial cavity of the frontals subtriangular, widest anteriorly and narrowing posteriorly (Fig. 7D, E), whereas in A. japonicus it is rhomboid (Fig. 7F).However, until reliable data on the comparative osteology of the modern species of Andrias become available and/or new material on the cryptobranchid from Belorechensk appears, we provisionally can assign the latter only to Andrias sp.

DISCUSSION
individuAl Age of the beloreChensk giAnt sAlAMAnder The Andrias from Belorechensk has an internally compact dentary with a few small to middle-size cavities and canals (Fig. 3D), in contrast to the large cavities and canals observed inside the dentaries of most other cryptobranchids (i.e., Andrias scheuchzeri, Ukrainurus hypsognathus, Andrias davidianus, and Zaissanurus beliajevae; Vasilyan et al. 2013: fig.3).Although the amount of internal compactness of the dentary seems to be of taxonomic value (Vasilyan et al. 2013), its variation among the studied cryptobranchids can probably be explained by differences in the individual age.However, this hypothesis has to be tested with specimens of different ontogenetic stages.
Poor development of cavities and canals in the dentaries from Belorechensk may be a consequence of a younger age of this individual, in comparison to other studied cryptobranchids (Canoville et al. 2018;Skutschas et al. 2019).
Counting growth rings on the articular surfaces of the vertebral zygapophyseal processes is one of the methods for estimating the individual age of living and extinct tetrapods.It was recently applied to Aviturus (Skutschas et al. 2020;Grigoriev et al. 2022).The Andrias from Belorechensk shows six or seven zygapophyseal growth rings on most of its zygapophyseal articular surfaces, suggesting that the animal died approximately during its seventh year of life.Its zygapophyseal growth rings are still widely spaced, which indicates that it died during a stage of rapid growth.Meanwhile, the estimated (based on the length of the dentary) total length of the Andrias from Belorechensk is about 90-100 cm.Both modern species of Andrias undergo a rapid initial growth until reaching about 60% of their final total length at which point the growth rate freshwater stagnophilous mollusks, together with ferruginous plant remains, suggest the Belorechensk salamander inhabited a freshwater and slow-flowing reservoir, the banks of which were covered with forest and shrub vegetation (Fig. 8).

the eAst europeAn giAnt sAlAMAnders
The Andrias from Belorechensk greatly extends the known geographic range of giant salamanders in Europe.The most widespread species, A. scheuchzeri, is known from a number of Oligo-Miocene localities in Central Europe (Böhme et al. 2012).The geologically youngest locality for this species is Willershausen in Germany (Westphal 1967) and is dated to the Late Pliocene, Villanyian, MN 16 (Rietschel & Storch 1974;Manning et al. 2019).In Eastern Europe, an undescribed dentary fragment of a cryptobranchid salamander has been listed from the Antipovka locality (MN 14), Voronezh Region of Russia (Averianov 2001).A cryptobranchid record has been mentioned from the Kuchurgan locality (MN 14) in Moldova (Chkhikvadze 1981).A possible cryptobranchid fragment comes from the Uryv locality of Russia (Agadzhanyan pers. comm., 2022).The Uryv locality belongs to the Uryvian faunal complex, which is the same age (MN 16a) as the Belorechensk locality.Given that modern cryptobranchid salamanders occur in humid subtropical or temperate areas with temperatures of 8-25°C, their fossils can be useful palaeoclimatic and palaeoenvironmental indicators (Böhme et al. 2012).The cryptobranchid records of the Uryvian faunal complex suggest favorable conditions for these animals in Eastern Europe up to the Late Pliocene, i.e., warm humid to very humid climates with mean annual precipitation exceeding 900 mm (Böhme et al. 2012).This hypothesis is corroborated by the presence in the Eastern European localities of the Uryvian faunal complex of other "archaic" taxa, i.e., the amphibians Latonia, Palaeobatrachus, and Mioproteus at the Uryv locality and Mioproteus at the Veselovka and the Plevaka localities (Ratnikov 2009; Syromyatnikova 2022).A climatic cooling at the Pliocene-Early Pleistocene transition (MN 16/MN 17) at c. 2.6 Ma, certainly disrupted the faunal assemblages of Europe and particularly affected the herpetofaunal communities (Delfino et al. 2003).Both the Belorechensk and possible Uryv cryptobranchid specimens are among the geologically youngest and easternmost records of giant salamanders in Europe, from where they disappeared because of the Late Pliocene climatic deterioration (Fig. 9).
fig. 1. -Maps showing geographic location of the Belorechensk locality and a photo of the Upper Pliocene deposits of the Belorechensk Formation.

. Apart from the cryptobranchid remains, the recovered vertebrate material includes remains of teleosts (cf. Tinca, Rutilus sp., Silurus sp.,
Syromyatnikova E. V. et al.sidered within A. davidianus (Turvey et al. 2019; Chai et al.  2022).These three species are differentiated by soft features and molecular data, but no osteological data was provided.Because our study relies entirely on osteological features, in this paper we consider A. jiangxiensis and A. sligoi within A. davidianus.The fossil cryptobranchid material from Belorechensk is curated in the paleoherpetological collection of the Palaeontological Institute of the Russian Academy of Sciences (PIN) under collection no.5882.MAteriAl.-Two frontals, PIN 5882/1 and 5882/2; two dentaries, PIN 5882/3 and 5882/4; one prearticular, PIN 5882/5; five trunk vertebrae, PIN 5882/6-10; one femur, PIN 5882/11; one rib, PIN 5882/12; all from the Belorechensk locality, Northern Caucasus, Late Pliocene, and interpreted as belonging to a single individual.