Anura, Fischer, 1813

Villa, Andrea, Macaluso, Loredana & Mörs, Thomas, 2024, Miocene and Pliocene amphibians from Hambach (Germany): New evidence for a late Neogene refuge in northwestern Europe, Palaeontologia Electronica (a 3) 27 (1), pp. 1-56 : 33-43

Anura indet.

Material. Hambach 6C: four premaxillae (IPB-HaH 2268/2270, IPB-HaH 2299); 51 fragments of maxilla (IPB-HaH 2233/2265, IPB-HaH 2282/2298, IPB-HaH 2300); 17 trunk vertebrae (IPB-HaH 2089/2097, IPB-HaH 2144/2145, IPB-HaH 2157/ 2158, IPB-HaH 2181/2183, IPB-HaH 2192); seven sacral vertebrae (IPB-HaH 2087, IPB-HaH 2206/ 2208, IPB-HaH 2217/2218, IPB-HaH 2225); 12 urostyles (IPB-HaH 2088, IPB-HaH 2197/2198, IPB-HaH 2201/2205, IPB-HaH 2216, IPB-HaH 2226/2227, IPB-HaH 2306); three coracoids (IPB-HaH 2313/2314, IPB-HaH 2378); nine humeri (IPB-HaH 2063, IPB-HaH 2303/2304, IPB-HaH 2311/ 2312, IPB-HaH 2317/2318, IPB-HaH 2331); five radioulnae (IPB-HaH 2301/2302, IPB-HaH 2309, IPB-HaH 2330, IPB-HaH 2335); two ilia (IPB-HaH 2319/2320); one ischium (IPB-HaH 2322); one femur (IPB-HaH 2326); 14 tibiofibulae (IPB-HaH 2054, IPB-HaH 2062, IPB-HaH 2064/2068, IPB-HaH 2305, IPB-HaH 2310, IPB-HaH 2327, IPB-HaH 2332/2334, IPB-HaH 2400); four indeterminate elements (IPB-HaH 2308, IPB-HaH 2315, IPB-HaH 2328, IPB-HaH 2398). Hambach 11: 29 maxillae (IPB-HaR 2044/2070, IPB-HaR 2177/ 2178); one angular (IPB-HaR 2114); two atlases (IPB-HaR 2025, IPB-HaR 2035); five trunk vertebrae (IPB-HaR 2024; IPB-HaR 2027/2029; IPB-HaR 2037); two sacral vertebrae (IPB-HaR 2026, IPB-HaR 2036); three urostyles (IPB-HaR 2038/ 2040); two coracoids (IPB-HaR 2125/2126); two scapulae (IPB-HaR 2072/2073); 10 humeri (IPB-HaR 2089/2095, IPB-HaR 2108/2109, IPB-HaR 2153); 16 radioulnae (IPB-HaR 2074/2079, IPB-HaR 2107, IPB-HaR 2123/2124, IPB-HaR 2128, IPB-HaR 2155/2157, IPB-HaR 2180/2182); four ilia (IPB-HaR 2085/2086, IPB-HaR 2104/2105); one ischium (IPB-HaR 2106); three femurs (IPB-HaR 2133/2134, IPB-HaR 2141); 25 tibiofibulae (IPB-HaR 2080/2082, IPB-HaR 2118/2122, IPB-HaR 2135/2140, IPB-HaR 2158/2168); one indeterminate element (IPB-HaR 2169). Hambach 11C: three maxillae (IPB-HaR 2422/2424); one ornamented bone fragment (IPB-HaR 2430); four tibiofibulae (IPB-HaR 2410/2413); one indeterminate element (IPB-HaR 2409).

DISCUSSION

The Middle Miocene and Late Pliocene Amphibians from Hambach Compared

Deposition of the two fossiliferous levels in Hambach, stratum 6C (with site Hambach 6C) and stratum 11 (with sites Hambach 11 and 11C), is separated by about a dozen Myr and happened in very different global climatic contexts (the MCO vs a period of climate deterioration preceding the onset of Quaternary glacial cycles). This is clearly reflected in the faunal composition, with a far higher diversity in the Middle Miocene association compared to the Late Pliocene one and the presence of several taxa linked with subtropical conditions in the former (e.g., among amphibians and reptiles: cryptobranchids, Chelydropsis , Diplocynodon Pomel, 1847 , cobras). Based on our observations and identifications ( Table 1 ), the amphibian component of the Hambach faunas matches with this pattern, all in all. The Middle Miocene fossil assemblage from Hambach 6C includes at least six different urodeles and six anurans. The Hambach 11 and 11C combined assemblage, on the other hand, listed only half the number of urodeles, even though the total of recognized anurans amounts to the same value. The remains attributed to the indeterminate cryptobranchid and to Chelotriton stand as evidence of the already-mentioned “tropical” elements present during the Middle Miocene. In agreement with crocodylians ( Mörs et al., 2000; Mörs, 2002) and cobras ( Čerňanský et al., 2017), but in contrast with what happens with Chelydropsis turtles (which possibly persisted in the Upper Pliocene deposits; Mörs, 2002), the two urodeles are absent in younger sites at Hambach, hinting towards a likely extirpation between MN 5 and MN 16a. Other urodeles sharing the same pattern of a Miocene presence and Pliocene absence in Hambach include Euronecturus grogu and Triturus sp. It is interesting to note that the proteid E. grogu , of which Hambach 6C is the only occurrence known worldwide at the moment, seems to be replaced by Mioproteus , a member of a different “modern” lineage of Eurasian proteids ( Macaluso et al., 2022b). The ranid frogs Pelophylax sp. and Rana sp. are also recognized in Hambach 6C only, but the presence of ranids in the Upper Pliocene as well is attested by few remains from Hambach 11. At least one of these remains, the ilium IPB-HaR 2087, may even display green frog features, and thus the absence of either one or the two ranids from the younger assemblage may be artifactual.

Remarks. Numerous fossil elements can be assigned to anurans, but are either too poorly preserved or not taxonomically significant enough for a more refined identification.

Reptiles

While studying the amphibian material, we chanced upon a few remains of reptiles that were accidentally not included in Čerňanský et al.’s (2017) work. Most of these are fragments of poorly diagnostic bones, but at least two specimens are worth mentioning and figuring. IPB-HaH 2340 ( Figure 23 A-B), from Hambach 6C, is probably a fragment of the posterodorsal process of a right jugal. The ornamentation recalls Chamaeleo andrusovi Čerňanský, 2010 , even though the topotypic jugals of this species show two rows of protuberances instead of just one as in the case of the specimen from Hambach. It is here attributed to Chamaeleo aff. andrusovi , similar to the squamosal fragment described by Čerňanský et al. (2017) from the same site. IPB-HaR 2171 ( Figure 23 C-D), from Hambach 11, can be associated to the same taxon as the nasal assigned by Čerňanský et al. (2017) to Pseudopus cf. pannonicus ( Kormos, 1911) , because they share a similar dermal sculpturing.

Nevertheless, there are also amphibians clearly persisting in Hambach in both Middle Miocene and Late Pliocene times. These include at least two urodeles, Palaeoproteus cf. miocenicus and Lissotriton sp. , and two anurans, Latonia sp. and Hyla sp. As mentioned, ranids can also be added to this list, even though detailed identification of the Pliocene remains at specific rank is prevented. Among frogs, palaeobatrachids and pelobatids show the reverse situation, with Late Pliocene remains that can be identified at species ( P. eurydices ) or, possibly, genus (cf. Eopelobates sp. and? Eopelobates sp. ) ranks respectively, whereas only the general presence of the families can be reported for the Middle Miocene (even in a tentative way in the case of palaeobatrachids). On the opposed side, the toad Bufo gr. bufo is the only anuran whose presence is certified just for the Late Pliocene in Hambach. Therefore, considering the uncertainty surrounding the possible persistence of some taxa from the Middle Miocene, the composition of the Late Pliocene Hambach 11 and 11C amphibian assemblage is certainly impoverished compared to the older one from Hambach 6C, apparently mainly as far as the urodele component is concerned, but it appears to exhibit an overall similarity and continuity. This differs from other tetrapod groups, which are sporadically represented by the same or related taxa in both Miocene and Pliocene levels (e.g., some petauristid rodents and possibly the already-mentioned Chelydropsis turtles; Mörs et al., 2000; Mörs, 2002; Van Laere and Mörs, 2023).

In terms of abundance, the highest numbers of remains identified per taxon in the Miocene assemblage are those referred to Chelotriton sp. (57 remains) and Latonia sp. (37 remains). These are, therefore, the taxa dominating the oldest Hambach oryctocenosis. Latonia persisted as dominant also in the Pliocene with 22 remains (18 from Hambach 11 and six from Hambach 11C), following P. eurydices represented by 27 remains (23 and four from Hambach 11 and 11C, respectively). As already mentioned, Chelotriton is not present in the Pliocene 11 and 11C sites, in agreement with a general European trend of extinction of this newt. The only Pliocene remains referred to this genus come in fact from the Upper Pliocene of southern France ( Bailon, 1989; Macaluso et al., 2022a). The most-represented urodele in the Upper Pliocene of Hambach is Mioproteus cf. wezei , represented by 15 remains (nine and six, respectively, from Hambach 11 and 11C). Other taxa from both the Miocene and Pliocene assemblages are only represented by very few, less than 10 remains each (except for Triturus sp. , with 12). Thus, these represent only very minor components of the fossil associations.

Palaeobiogeographical Significance of the Hambach Amphibian Assemblages

The amphibian fossil record from Hambach already proved to host unexpected surprises with the discovery of Euronecturus grogu , an enigmatic proteid (see Macaluso et al., 2022b) that is only known from its type locality of Hambach 6C at the moment. The extended study of the whole amphibian record revealed that this is not the only noteworthy taxon preserved in the site, and that significant findings were hidden in both the Miocene and Pliocene assemblages.

Cryptobranchids are in general poorly represented in the fossil record, even though a particular concentration of Neogene cryptobranchid-bearing sites is found in central Europe, and more specifically in Southern Germany ( Böhme et al., 2012). Still, they are almost unknown from the European early Middle Miocene, even though their presence in Lower, upper Middle and Upper Miocene sites ( Westphal, 1958, 1970; Böttcher, 1987; Miklas, 2002; Böhme, 2003; Kvaček et al., 2004; Tempfer, 2004; Böhme et al., 2012; Vasilyan et al., 2013; Sach, 2016; Georgalis et al., 2019b; Szentesi et al., 2020) suggests their continuous persistence in the continent. As a matter of fact, Hambach 6C is currently the only known occurrence of a cryptobranchid from the early Middle Miocene time frame in Europe, and even adds to a limited Eurasian Langhian record that further includes only few localities in Kazakhstan ( Chkhikvadze, 1982; Böhme et al., 2012). Cryptobranchids later declined in Europe during the Pliocene, with their last occurrence at Willershausen, in central Germany ( Westphal, 1967; Böhme et al., 2012). The age of Willershausen was reported as Zanclean by Böhme et al. (2012, table 1), but it is now considered as Piacenzian ( Kolibáč et al., 2016, and reference therein). Adding to being the only data currently available on European early Middle Miocene cryptobranchids, Hambach 6C represents also the westernmost point ever reached by these urodeles in Eurasia, based on our current knowledge. Only the late Oligocene occurrence at Rott ( Westphal, 1958; Mörs, 2002; Böhme et al., 2012), close but located slightly eastward to Hambach, further supports the past existence of cryptobranchid populations west of the Rhine Graben.

One of the most unexpected findings from Hambach is the batrachosauroidid Palaeoproteus . Batrachosauroidids are enigmatic urodeles, which are mainly known from the Cretaceous and Palaeogene of North America ( Gardner and DeMar, 2013, and reference therein). They persisted in the USA throughout the Miocene, with a handful of occurrences in California ( Naylor, 1981), Delaware ( Weems and George, 2013), Florida ( Estes, 1963; Bryant, 1991), Louisiana ( Williams, 2009), and Texas ( Taylor and Hesse, 1943; Auffenberg, 1958; Hinderstein and Boyce, 1977; Holman, 1977; Albright, 1994). They are also known from Europe, even though their record on this continent is far poorer. They were possibly present already during the Cretaceous ( Duffaud, 1995; Evans and Milner, 1996; Evans and McGowan, 2002), and then are seldomly recovered in the Palaeocene ( Estes et al., 1967; Groessens-Van Dyck, 1981), Eocene ( Herre, 1935), and Upper Miocene ( Vasilyan and Yanenko, 2020). A single record from the Lower Miocene is also reported ( Böhme, 2003; Kvaček et al., 2004), but detailed descriptions and identification of these fossils remain unpublished so far. Similar to the cryptobranchids, the Hambach 6C Palaeoproteus remains are the only batrachosauroidid fossils currently known from the Middle Miocene in Europe. Adding to this, those coming from Hambach 11 and 11C further stand out as the youngest occurrence of this clade worldwide, as well as the only one postdating the Miocene/Pliocene transition. Moreover, Hambach lists among the northernmost sites reached by these urodeles in post-Palaeogene times, being located even slightly more northward than Hrytsiv in Ukraine ( Vasilyan and Yanenko, 2020) and Ahníkov/Merkur North in Czech Republic (where the presence of these amphibians can be seen as unconfirmed, for the time being; Böhme, 2003; Kvaček et al., 2004). Both the Miocene and Pliocene Hambach material is here referred to the European genus Palaeoproteus , and even to a taxon related to the species P. miocenicus . Even though a confident identification of the fossils with this Late Miocene species is currently prevented, Hambach is evidence that either one or two morphologically similar forms (depending on whether occurrences from Hambach 6C and Hambach 11 and 11C are conspecific or not) were already present in Europe several Myr before the oldest occurrence reported by Vasilyan and Yanenko (2020) and successively persisted at least up to slightly before the Plio-Pleistocene boundary.

Euronecturus is not the only proteid found in Hambach: Mioproteus , a possible representative of a modern European clade including also the extant Proteus ( Macaluso et al., 2022b) , actually replaced it in the youngest level. Several other occurrences of Mioproteus are known from Germany throughout the Miocene ( Schleich, 1985; Böhme, 2003; Böttcher et al., 2009; Prieto et al., 2009; Abdul Aziz et al., 2010; Sach, 2016; Macaluso et al., 2022a, 2022b), including fossils referred to both M. caucasicus and indeterminate species (even though most of these were never properly published). Its absence in Hambach 6C, thus, appears puzzling per se, especially when paired with the presence of Euronecturus . Some sort of competitive exclusion cannot be discounted, even though only treated as speculative at the moment due to the very poor information we have about the latter. Later on, Mioproteus survived up to the late Early Pleistocene ( Młynarski and Szyndlar, 1989; Averianov, 2001; Ivanov, 2007), but all findings postdating the Miocene/Pliocene transition are either unassigned to species ( Averianov, 2001; Ratnikov, 2010; Vasilyan et al., 2017) or referred to M. wezei ( Młynarski et al., 1984; Młynarski and Szyndlar, 1989; Bailon, 1995; Averianov, 2001; Ivanov, 2007; Syromyatnikova et al., 2021, Macaluso et al., 2022a). If our identification is correct, the Upper Pliocene occurrence of Mioproteus cf. wezei in Hambach would agree with this pattern. Furthermore, this is currently one of the westernmost records of Mioproteus , with only M. wezei from Balaruc II, in France ( Bailon, 1995), located in an even more western position (even though in a far more southern, Mediterranean area).

Among salamandrids, Chelotriton is the most represented in Hambach 6C and also very common in Europe, and even in Germany, during the Miocene. Hambach lists among the northernmost Miocene occurrences reached by the genus on the continent, together with the slightly more southern remains from Echzell ( Vasilyan et al., 2022). These large salamandrids apparently decreased after the Messinian Salinity Crisis. They are reported from the post-evaporitic succession of Moncucco Torinese in Italy ( Colombero et al., 2017), and subsequently the only published occurrence is from the Upper Pliocene of Balaruc II in France ( Bailon, 1989). Their absence in Hambach 11 and 11C agrees with this observed pattern of extirpation from northern Europe possibly somewhen in the Late Miocene, and in any case before the Late Pliocene ( Macaluso et al., 2022a). Triturus newts also are represented in Hambach 6C only in our material, even though, in contrast with Chelotriton , their presence as far north as central Germany ( Holman, 1998; Böhme, 2000, 2020) and The Netherlands ( Villa et al., 2018c) in northwestern Europe is known up to the Quaternary. The genus still persists nowadays in the area of Hambach with the species T. cristatus ( Sillero et al., 2014; Speybroeck et al., 2016). Few published Triturus dated back to MN 5 are also reported in Europe only from southern Germany ( Böttcher et al., 2009), but other occurrences from Czech Republic and Germany were mentioned by Böhme (2003) without figures or detailed descriptions. The Hambach specimens add, thus, to the rather poor knowledge of these newts at the Early/Middle Miocene transition. Further significance can be given to the Miocene Lissotriton remains from Hambach 6C, given that these stand out among the oldest occurrences of the genus. Older remains were found in two upper Oligocene sites in southern France ( Macaluso et al., 2022a) and southern Germany ( Böhme 2008), as well as in the Lower Miocene of southern France (two sites; Rage and Hossini, 2000; Rage and Bailon, 2005), western Germany (one site; Vasilyan et al., 2022), and southern Germany (two sites; Böttcher et al., 2009; Böhme, 2010). Macaluso et al. (2022a) further mentioned possible Lissotriton identity for lower Eocene vertebrae from France ( Augé et al., 1997), but this has yet to be confirmed. Several other localities yielding Early and Middle Miocene Lissotriton remains in Germany (possibly going back even to the Oligocene/ Miocene transition) were listed by Böhme (2003), but these fossils still await proper publication. On the other hand, the very few vertebrae from Hambach 11 represent the first Pliocene Lissotriton remains found in Germany, where otherwise occurrences in the country date to either Miocene or Quaternary. Very few further Late Pliocene remains come from Poland ( Sanchiz and Młynarski, 1979b; Młynarski and Szyndlar, 1989) and Spain ( Gómez de Soler et al., 2012).

Anurans from Hambach also include very common taxa in Europe during corresponding time frames, as well as unexpected occurrences. The most abundant anuran in Hambach, Latonia , is very common all over Europe, including Germany, during most of the Neogene ( Roček, 1994b, 2013, and reference therein). It is far less distributed on the continent during the Late Pliocene, when only few occurrences in southern France ( Bailon, 1991), central Germany ( Böhme, 2000), northern Italy ( Vergnaud-Grazzini, 1970), and southern Ukraine ( Ratnikov, 2001) are known. In the Pleistocene, relict occurrences of this alytid genus in Europe are only reported from northern Hungary ( Szentesi, 2019) and central Italy ( Sorbelli et al., 2021). Early Pleistocene Latonia remains were also found in Turkey ( Vasilyan et al., 2014), but late Quaternary occurrences are limited to Israel ( Biton et al., 2016), where the last survivors of these frogs were recently rediscovered ( Biton et al., 2013; Perl et al., 2017). After the Miocene/Pliocene boundary, the German site of Kaltensundheim is the only place where Latonia was reported ( Böhme 2000) that reaches comparable northern latitudes with Hambach. However, Böhme (2002) found no trace of Latonia among the fossil material from this Thuringian site and recommended its removal from the taxon list of the assemblage. Thus, Hambach currently stands as the northernmost confirmed occurrence of Latonia from the late Neogene onwards.

Palaeobatrachids are almost completely absent from western Europe following the Miocene/Pliocene transition ( Wuttke et al., 2012; Roček, 2013; Roček et al., 2021), with the only notable exceptions being Tegelen, in The Netherlands ( Villa et al., 2016), and Hambach 11 and 11C. These localities share the same palaeobatrachid species, which is currently not known elsewhere, and are geographically close, even though the Dutch site is younger, being Lower Pleistocene (Gelasian) in age. Other Pliocene and Quaternary occurrences of palaeobatrachids are all located far eastward. The closest one in geographical terms to Tegelen and Hambach, and only other post-Miocene site with palaeobatrachids in Germany, is possibly Voigtstedt, a Chibanian locality in Thuringia, from which Palaeobatrachus langhae ( Fejérváry, 1917) was reported by Kretzoi (1965) and later mentioned as a tentative occurrence by Holman (1998), Sanchiz (1998), and Böhme (2000). There is no other Miocene occurrence of palaeobatrachids in the northwestern part of continental Europe surrounding Hambach and Tegelen ( Wuttke et al., 2012), and the estimated closest relatives to the Plio-Pleistocene species P. eurydices are to be found in the Lower Miocene of southern France and central Germany ( Palaeobatrachus robustus Hossini and Rage, 2000 ; Hossini and Rage, 2000; Roček, 2013; Villa et al., 2016; Roček et al., 2021; Vasilyan et al., 2022). In this context, the fragmentary maxilla from Hambach 6C testifies that these water-dwelling frogs likely inhabited the area during the early Neogene as well, even though the preservational status prevents both a confident attribution at family rank and even more any inference on the possible persistence of the lineage leading to P. eurydices . More Neogene palaeobatrachid fossils from countries such as Belgium, The Netherlands, and (northwestern) Germany are needed to shed light on the early evolution of this possibly relictual lineage.

A situation similar to that of palaeobatrachids arises for pelobatids from Hambach as well. Several pelobatids are reported from the Palaeogene and Neogene of Europe (e.g., Sanchiz, 1998; Roček, 2013; Vergilov and Tzankov, 2021; and reference therein), but only few of them come from the northwestern part of the continent, where Hambach is located. Miocene pelobatids found in the area come from only three localities placed slightly eastward to the latter site: an Aquitanian indeterminate member of the family from Budenheim, near Mainz, mentioned, but neither described nor figured, by Schleich (1988); several Burdigalian remains of Pelobates sanchizi Venczel, 2004 from Echzell ( Vasilyan et al., 2022); and a Middle Miocene premetamorphic tadpole from Climbach, near Allendorf, attributed to Eopelobates sp. (originally referred to Palaeobatrachus goldfussi Tschudi, 1838 by von Meyer, 1860, but later reidentified by Špinar, 1972; see Gardner, 2016). The two fossil bones from Hambach 6C are evidence that the range of pelobatids extended further west in this part of Europe in the Middle Miocene, but it is currently impossible to figure out whether or not they were related to either the taxa living in nearby areas in Palaeogene times (e.g., Eopelobates bayeri Špinar, 1952 from Belgium, Eopelobates wagneri ( Weitzel, 1938) from western Germany; Roček, 2013; Roček et al., 2014; Smith et al., 2018), the Early/Middle Miocene above-mentioned ones from western Germany, or even those from the youngest level in Hambach. If correctly identified, the Late Pliocene Eopelobates from Hambach 11 and 11C, on the other hand, shares potentially no relations with other pelobatids identified at genus rank in close-by post-Miocene sites. Known congeneric occurrences postdating the Miocene/ Pliocene transition are all located in Eastern Europe ( Młynarski 1962; Sanchiz and Młynarski, 1979a; Młynarski and Szyndlar, 1989; Ratnikov, 2001; Venczel, 2001; Roček, 2013; Roček et al., 2014; Vergilov and Tzankov, 2021), even though Rage and Roček (2003), Roček (2013), and Vergilov and Tzankov (2021) recommended caution on these occurrences due to the absence of the most diagnostic cranial elements in the respective material. Nevertheless, only Pelobates is recorded in the western part of the continent in the last 5 Myr. Apart from the fossils from Hambach, the other youngest published records of Eopelobates in western Europe are Middle Miocene in age ( Špinar, 1972; Böhme, 2010; Roček et al., 2014; Gardner, 2016). If our identification is correct, the possible Late Pliocene Hambach Eopelobates is, thus, another unexpected late survivor from the site. Available published evidence suggest that Eopelobates went extinct before the beginning of the Pleistocene (but see Rage and Roček, 2003, and Vergilov and Tzankov, 2021, for an older extinction date), which agrees with the fact that Quaternary sites in the area close to Hambach only yielded Pelobates ( Böttcher, 1991; Holman, 1998; Sanchiz, 1998; Schouten, 2016; Villa et al., 2018c).

Taking into account their rather fragile skeleton, tree frogs of the genus Hyla are rather common in European sites from the Miocene onwards, especially during the Quaternary. Earliest European representatives of the genus possibly entered the continent in the Early Miocene ( Sanchiz and Roček, 1996; Rage and Roček, 2003; Roček, 2013), together with several other amphibians and reptiles ( Szyndlar and Schleich, 1993; Ivanov, 2000; Delfino et al., 2003; Rage and Roček, 2003; Rage, 2013; Georgalis et al., 2016; Ivanov et al., 2018; Villa et al., 2018a; Villa and Delfino, 2019; Macaluso et al., 2022a). In this context, tree frogs from Hambach represent one of the oldest occurrences in Germany, together with Oggenhausen 2 in Baden-Württemberg ( Böttcher et al., 2009), but also the westernmost location reached in Europe by these frogs during the Neogene based on the current published knowledge (even though, again, bones of tree frogs are very fragile and maybe subject to a strong preservation bias). Hambach is also the first German site yielding Pliocene tree frog remains. Subsequently, tree frogs persisted in the area, as testified at least by the members of the H. arborea group found in Tegelen ( Villa et al., 2018c). They are widespread throughout northwestern Europe nowadays ( Sillero et al., 2014; Speybroeck et al., 2016).

Bufonids and ranids are also inhabitants of modern northwestern Europe, as well as common findings in Neogene and Quaternary fossil assemblages in the continent. Hambach stands out as one of the northernmost known occurrences of the common toad in Pliocene times, together with Kaltensundheim in Germany ( Böhme, 2002) and at least Węże 2 in Poland ( Młynarski et al., 1984). Both the common toad and the two ranids were found also in the Lower Pleistocene of the nearby Tegelen locality ( Villa et al., 2018c).

Palaeoenvironmental Insights and the Role of Northwestern Europe as a Late Neogene Refugial Area for Amphibians

The Hambach palaeofaunas, and especially their amphibian components, appear rather significant for their composition, with representatives of enigmatic and poorly known taxa and unexpected occurrences both in chronological and geographical terms. The palaeoenvironments in which these palaeofaunas lived were certainly humid ones. In addition to sedimentological and palaeobotanical evidence (see Geological setting), these humid conditions are testified by the rather high diversity of amphibians and the presence of other water-related animals (e.g., fish, pond turtles, Natrix Laurenti, 1768 snakes, dominant aquatic/semiaquatic forms among the insectivores, beavers; Mörs, 2002; Čerňanský et al., 2017). As far as amphibians are concerned, permanent water bodies are indicated by the occurrences of Palaeoproteus ( Herre, 1935; Vasilyan and Yanenko, 2020), palaeobatrachids, and, at least in the Pliocene level, Mioproteus (a fully aquatic taxon according to Venczel and Codrea, 2018). The extant Latonia nigriventer inhabits marshy areas in the Hula Valley, in Israel ( Biton et al., 2013, 2016; Perl et al., 2017), and the abundance of Latonia in both the Miocene and Pliocene of Hambach hints towards persistent preference for similar swampy environments in past members of the clade as well. Pelobatids are fossorial anurans that suggest the availability of sandy soils in Hambach. Forested areas nearby are supported by the rare tree frogs, as well as Pliopithecus Gervais, 1849 , and flying squirrel remains ( Mörs, 2002; Van Laere and Mörs, 2023) for the Miocene and Pliocene, respectively.

Humidity in Hambach was particularly high during the Middle Miocene, when cryptobranchids were living in the area. As a matter of fact, these urodeles are tied to high humidity and pluviometry according to Böhme et al. (2012). A certain influx of marine conditions in an estuarine setting is highlighted by the abundant marine fish and rare cetacean remains in Hambach 6C ( Mörs, 2002). This changed at the end of the Middle Miocene ( Schäfer et al., 2004), long before the deposition of remains found in Hambach 11 and 11C, which only include freshwater fish and is devoid of other marine animals. Fish remains in Hambach also mark another change from slow currents and larger channels in Hambach 6C to more oxygenated waters with higher energy in Hambach 11 and 11C ( Mörs, 2002). Moreover, another palaeoenvironmental differences highlighted by the faunal composition in the two Hambach levels lies in the temperature: the Miocene fauna is rich in thermophilic vertebrates, such as giant tortoises, crocodylians, chameleons, “Oriental vipers”, and possibly cobras ( Mörs, 2002; Čerňanský et al., 2017), whereas these are absent in the Pliocene one. This agrees with the climate reconstruction performed for Hambach 6C based on palaeobotanical data ( Utescher et al., 2000, 2002), and makes further sense when considering that the Middle Miocene fauna deposited in a greenhouse interval (the Miocene Climatic Optimum; Steinthorsdottir et al. 2021), whereas the Late Pliocene one in a period of climate deterioration.

The faunal change between Hambach 6C on one side and Hambach 11 and 11C on the other is, thus, evident in several of its components, but it seems to affect the amphibians to a lower extent. Some amphibian taxa indeed disappeared between the Middle Miocene and the Late Pliocene (i.e., cryptobranchids, the Euronecturus lineage, Chelotriton ), but others persisted to even be among the last known representatives of their clades in northern/northwestern Europe ( Latonia , palaeobatrachids) or worldwide ( Palaeoproteus ). The case of cryptobranchids is particularly interesting because their last reported occurrence in Europe is in Willershausen, an Upper Pliocene locality in Lower Saxony, central Germany. This makes it and Hambach 11 and 11C close or comparable in terms of both geographical position and age, leading to the question on why these urodeles are absent from the Upper Pliocene level in Hambach. The depositional environment in Willershausen was that of a large and deep lake in a sinkhole, surrounded by a hilly mesophytic woodland ( Kolibáč et al., 2016, and reference therein). The reconstructed palaeoclimate was cooler than what suggested for the Miocene Hambach, but with similar precipitations ( Thiel et al., 2012). Unlike other taxa present in Hambach 6C and absent in Hambach 11 and 11C, then, extirpation of cryptobranchids from there is likely not tied to a decrease in temperature, given their survival in the colder Willershausen. An alternative potential explanation may be the altitudinal distribution model proposed by Böhme et al. (2012): cryptobranchids appear generally limited to higher elevations in drier periods with low basinal relief and colonize lowland environments in hyperhumid moments with high basinal relief. Giant salamanders may have disappeared from the Lower Rhine Embayment in one of such drier periods after the Middle Miocene, whereas the more elevated area near the Willershausen lake (i.e., the Harz Mountains) was able to sustain populations of these amphibians up to at least the late Neogene.

Another locality that is worth comparing with Hambach is Tegelen, in The Netherlands ( Table 2 ). Sediments at Tegelen were also deposited by the Rhine-Meuse river system, even though in a slightly younger, Early Pleistocene, time ( van den Hoek Ostende, 2004; van den Hoek Ostende and de Vos, 2006). The Russel-Tiglia-Egypte pit at Tegelen is notable for being the type locality of P. eurydices , the palaeobatrachid species found in the Upper Pliocene level at Hambach, and for having yielded a rather diverse assemblage of amphibians and reptiles ( Villa et al., 2016, 2018c). Urodeles are much more diverse in Hambach, especially in the Miocene layers. Tegelen only yielded salamandrids ( Triturus and Lissotriton ), whereas Hambach has salamandrids, proteids, batrachosauroidids (both Miocene and Pliocene) and cryptobranchids (only Miocene). Among salamandrids, the presence of Chelotriton in the Miocene level of Hambach expands the ecomorphological adaptations represented by a member of this clade in this assemblage compared to Tegelen. As already mentioned, Triturus is missing in the Pliocene of Hambach, but it is present in the Pleistocene of Tegelen. Given the scarcity of the remains, it is not clear whether the absence of this newt may just be artifactual or not, though. For anurans, significant is the persistence of palaeobatrachids in all levels at Hambach and then in the Russel-Tiglia-Egypte pit at Tegelen, and especially the same species being shared between the Upper Pliocene of the former and the Lower Pleistocene of the latter. In general, the overall diversity of frog and toads appears comparable, but there are strong differences in composition of the assemblages. Latonia is the most abundant anuran in Hambach, but it is absent in Tegelen. Pelobatids are possibly represented by Eopelobates at least in the Pliocene of Hambach, whereas Pelobates is identified at Tegelen. On the other hand, the Hambach assemblages lack Bombina Oken, 1816 , and Pelodytes Bonaparte, 1838 , taxa otherwise present at Tegelen. Hyla , the common toad, and the ranids are shared by both the German and Dutch localities, even though less common in Hambach and restricted to specific levels as far as the toad and the ranids are concerned.

When looking at reptiles, crocodylians are absent in both the Pliocene of Hambach and at Tegelen, whereas several cranial and postcranial remains attributed to Diplocynodon were recovered in the Miocene level of the former ( Mörs et al., 2000; Mörs, 2002). Turtles from Tegelen only include Emys Duméril, 1806 , and Mauremys , moreover never found together in the same pit ( Schreuder, 1946; van den Hoek Ostende and de Vos, 2006; Villa et al., 2018c). Hambach displays a higher diversity in the Miocene, with several distinct lineages and both aquatic/semiaquatic and terrestrial animals, but only two taxa in the Pliocene ( Mörs, 2002; Klein and Mörs, 2003). Emys is shared between the Pliocene of Hambach (even though this occurrence still lacks a detailed publication, with description and figures of the remains, and should be treated with caution) and the Pleistocene of Tegelen, but Hambach misses Mauremys and Tegelen misses Chelydropsis (again, if its presence in Pliocene Hambach is confirmed). Squamate faunas from Hambach 6C and Tegelen are very different, with the former being far more diverse (especially in the snake component) and including several Palaeogene/Neogene lineages missing in Tegelen (i.e., chameleons, Eoanilius Rage, 1974 , Bavarioboa Szyndlar and Schleich, 1993 , cf. Falseryx Szyndlar and Rage, 2003 , cf. Naja Laurenti, 1768 , and the “Oriental vipers”; Čerňanský et al., 2017). A small viper is present in both, even though it is not clear if they may represent the same viper group. “Colubrine” snakes and Natrix are also shared between Tegelen and both Miocene and Pliocene levels in Hambach. However, Pleistocene and Pliocene “colubrines” remain unidentified at lower taxonomic ranks, whereas the Miocene ones include at least three different taxa (“ Coluber ” Linnaeus, 1758, Texasophis Holman, 1977 , and Telescopus Wagler, 1830 ). Not a lot can be said about lacertids, except for them being recovered both in the Middle Miocene of Hambach ( Čerňanský et al., 2017) and the Pleistocene of Tegelen ( Villa et al., 2018c). Diversity seems to be comparable (two taxa), but there seems to be no evidence in Hambach of a possible green lizard as in Tegelen. Pseudopus is present in all Hambach levels ( Čerňanský et al., 2017; this work) and tentatively even in Tegelen. However, Miocene and Pliocene assemblages in Hambach bear two different Pseudopus species, and it is not clear if the Tegelen one may be related to either one of the two.

It seems, thus, that a major change in the reptilian palaeofauna happened already at some point in the Middle Miocene-Late Pliocene interval, with less significant differences between the Upper Pliocene assemblage of Hambach 11 and 11C and the Lower Pleistocene ones of the Tegelen pits (and in particular the Russel-Tiglia-Egypte pit). On the other hand, differences in the batrachofauna are more marked between Hambach 11 and 11C and Tegelen compared to the two levels in Hambach. Whilst the faunal change affecting reptiles agrees with the well-recognized pattern of extirpation of thermophilic taxa from northern Europe characterizing the late Neogene and Quaternary (e.g., Delfino et al., 2007; Rage, 2013; Blain et al., 2016; Villa and Delfino, 2019), amphibians here appear to be less affected by this trend. The differences between Hambach and Tegelen in the amphibian palaeocommunity may be simply explained by different palaeoenvironments (swamp vs floodplain, respectively), but the peculiarity of the batrachofauna in Hambach 11 and 11C (with several taxa otherwise unknown from northwestern Europe in contemporary times) and its similarities with the Hambach 6C one suggest that other factors may be also at play. Reconstructed palaeoclimate at Tegelen based on the herpetofaunistic association recovered from the Russel-Tiglia-Egypte pit ( Villa et al., 2018c) indicate a humid subtropical climate, but with MAT and MAP significantly lower than those at Hambach during the Middle Miocene (quantitative climate reconstructions are not available for the Upper Pliocene Hambach sites). A light degree of aridity was also suggested by the same reconstruction. No evidence of a similar dryness is available for the Upper Pliocene level in Hambach. Increased aridization was proposed as a possible cause for the disappearance of some amphibians (i.e., palaeobatrachids; Wuttke et al., 2012) from Western Europe in the late Neogene, but it is evident that areas suitable for these animals persisted at least in the northwestern part of the continent (i.e., in the Lower Rhine Embayment and the Rhine-Meuse delta system) up to the Late Pliocene and, maybe to a lower extent, the Early Pleistocene. High humidity may have allowed the Lower Rhine Embayment to act as a refuge for amphibians during this time, while they were disappearing from other parts of Western Europe. Later, a combination of increasing aridity and potentially the onset of the Quaternary glaciation may have led to the ultimate loss of the refugial conditions and to a faunistic change towards the early Quaternary and subsequent modern batrachofauna of the area. As a matter of fact, various evidence points out to different trends shown by temperatures and precipitations in the Lower Rhine Embayment during the late Neogene, with MATs showing a clear decreasing trend after the early Middle Miocene and MAPs maintaining high values (> 1000 mm) well into the Pliocene ( Utescher et al., 2000, 2009, 2012; van Dam, 2006; Crampton-Flood et al., 2018). Utescher et al. (2012) further observed that cool events in the Zanclean of northwestern Europe are related to, or start with, wetter conditions, in contrast with the correlation of warmer and wetter periods in the Miocene. This may have favoured the survival of amphibians in this area. In a somehow similar way, a persistent humid climate allowed the Italian Peninsula to act as a preferential refuge for amphibians during the Quaternary glacial cycles, versus the role of reptile refuges that was played by the more arid Balkan and Iberian peninsulae ( Macaluso et al., 2021, 2023a). A comparable role may be advocated for the Lower Rhine Embayment as well during the late Neogene and maybe the Early Pleistocene.

Figures

FIGURE 23. Reptiles from Hambach: right squamosal (IPB-HaH 2340) of Chamaeleo aff. andrusovi in lateral (A) and medial (B) views; left frontal (IPB-HaR 2171) of Pseudopus cf. pannonicus in dorsal (C) and ventral (D) views. Scale bars equal 1 mm.

Tables

TABLE 1. Distribution of amphibian taxa identified in the fossiliferous localities within the Hambach mine.

	Middle Miocene	Late Pliocene
	Hambach 6C	Hambach 11	Hambach 11C
Cryptobranchidae indet.	x
Palaeoproteus cf. miocenicus	x	x	x
? Palaeoproteus cf. miocenicus	x
Euronecturus grogu	x
Mioproteus cf. wezei		x	x
Chelotriton sp.	x
? Chelotriton sp.	x
Lissotriton sp.	x	x
Triturus sp.	x
Urodela indet.	x
Latonia sp.	x	x	x
Palaeobatrachus eurydices		x	x
? Palaeobatrachidae indet.	x
cf. Eopelobates sp.		x
? Eopelobates sp.			x
Pelobatidae indet.	x
Hyla sp.	x	x
Bufo gr. bufo		x
Pelophylax sp.	x
Rana sp.	x
Ranidae indet.	x	x
Anura indet.	x	x	x