Nyctereutes donnezani (Deperet 1890)

Two rather complete skulls (MNHN. F. ACA 291, ACA 292) belonging to fully adult individuals; damaged right upper canine (ACA 300); right P 4 on a piece of bone (ACA 298); two isolated M 1 (ACA 296, ACA 297); a palate (unnumbered) at the Natural History Museum of Ankara bearing right and left P 4 - M 2 series; a left isolated M 1 (AKÇ- 136) at the same museum; right mandible with the alveolus of p 1 and p 2 - m 3 (ACA 549); fragment of right mandible with p 4 - m 2 (ACA 294); fragment of right mandible with c-p 3 (ACA 295); fragment of left mandible with m 1 - m 2 and alveolus of m 3 (ACA 387); fragment of left mandible with p 4 and alveoli of p 1 - p 3 (FSL- 212806); right m 1 on a piece of bone (ACA 548); left lower canine (ACA 299); fragment of left mandible with m 1 - m 2 (AKÇ- 134) and another fragment of left mandible with m 1 - m 2 (unnumbered) in the collections of the Natural History Museum of Ankara. In addition to the cranial remains, there are a few postcranial bones that Ginsburg (1998) described and measured. They are not used in the present study. DESCRIPTION AND COMPARISON Skull The description of the cranial and dental remains is largely inspired by Ginsburg (1998) who provided a detailed comparative description of the Çalta fossils with Vulpes vulpes (Linnaeus, 1758) and some species of Nyctereutes, in particular N. donnezani and N. megamastoides (Pomel, 1843). In dorsal view, the Çalta skulls are narrow, elongated, and the muzzle thins progressively forward like in Vulpes vulpes but unlike in the extant Nyctereutes procyonoides (Gray, 1834), N. sinensis from China and N. megamastoides from western Europe, which have a much more massive skull and short muzzle. In dorsal view, the narrowing of the muzzle is progressive on the Çalta skulls, while it is abrupt in N. sinensis and N. megamastoides. The nasal bones are thin and long like in all other species of Nyctereutes, and they reach the level of the orbital constriction, distal to the maxillary-frontal suture. The posterodorsal part of the maxillae is slightly inclined as in N. sinensis and more than in V. vulpes. The postorbital processes are thick and well developed. They present a dorsal depression as in V. vulpes, N. sinensis and N. megamastoides. The ridges issuing from the distal margin of the postorbital processes join the sagittal crest behind the postorbital constriction, similar to N. tingi Tedford & Qiu, 1991. In N. megamastoides, N. sinensis and N. procyonoides, the fusion of the postorbital ridges with the sagittal crest takes place in the middle of the braincase, i. e. much more caudally than in N. tingi and in the skulls of Çalta. The sagittal crest is stronger than in V. vulpes and N. megamastoides. The braincase is curved as in the other species of Nyctereutes and Vulpes. In lateral view, the jugal bone is larger in the specimens from Çalta than in N. sinensis and V. vulpes. The tympanic bullae are more rounded than in V. vulpes and Canis lupus (Linnaeus, 1758). The paroccipital process (or jugular process) is appressed to the tympanic bullae and descends ventrally the level or even below the level of the bullae. This process is much higher in V. vulpes, N. tingi, N. sinensis and N. megamastoides. The nuchal crest fully dominates the occipital surface. It is stronger than in V. vulpes and C. lupus, but is similar in thickness to that of N. megamastoides. Ginsburg (1998) did not note that the two skulls from Çalta are different in size, MNHN. F. ACA 291 being clearly larger than ACA 292. In particular, the former is more robust and has stronger sagittal and nuchal crests, better defined temporal line and occiput structures, thicker zygomatic process of the maxillary bone, elongated but less rounded braincase, and thicker postarticular process. An anecdote deserves to be mentioned here. When the second author (S. Sen) was cleaning and preparing the fossils from Çalta in 1974, Björn Kurtén (1924 - 1988), the famous Finnish vertebrate paleontologist, visited the Institute of Paleontology of the Museum in Paris. He came to see the Çalta fossils under preparation, and asked for carnivores. He took the two Nyctereutes skulls of Çalta in his hands, observed them for a while, and said only “ Monsieur et Madame ”, and he left. We agree with B. Kurtén in considering the differences noted here above as due to sexual dimorphism. We will see that such differences also exist on the mandibles. Mandible The ascending ramus is broken in all of the seven fragments of mandible from Çalta, which all represent parts of the corpus and bear various numbers of teeth. The corpus is quite long and moderately thick, and its depth increases progressively backward, more so on specimen MNHN. F. ACA 549 than on ACA 294 and FSL- 212806. The ventral margin is slightly convex, mainly below the p 4 and the molars. The symphyseal process is well defined under the p 2, interrupting the ventral profile of the body (Fig. 3). This process is apparently absent in the extant species, but variably present in fossil species of Nyctereutes. One of the diagnostic features of Nyctereutes is the presence of the subangular lobe, which is the insertion ridge of the digastric muscle. This muscle links the corpus of the mandible to the paroccipital process. The digastric muscle is involved in all complex jaw action, mainly by pulling the lower jaw backward and pivoting it at the jaw joint to open the mouth. The subangular lobe is strong on the specimen MNHN. F. ACA 549, similar in importance to that of N. donnezani from Perpignan and N. tingi from the Yushe Basin (Depéret 1890; Tedford & Qiu 1991), but weak on specimen ACA 294 (Fig. 3). The lobe is stronger and placed distally in N. megamastoides, N. sinensis and N. abdeslami (Boule 1889; Depéret 1890; Teilhard de Chardin & Piveteau 1930; Viret 1954; Martin 1971; Tedford & Qiu 1991; Koufos 1993; Geraads 1997; De Vos et al. 2002; Rook et al. 2017), as well as in the extant species N. procyonoides (Hidaka et al. 1998). The degree of development of this lobe, which is weak in the species from late the Miocene / early Pliocene (N. donnezani and N. tingi), but strong in the younger species (N. megamastoides, N. sinensis, N. abdeslami and N. procyonoides), is used to distinguish species. However, as shown by the specimens from Çalta, the robustness of this lobe may also be due to sexual dimorphism. To quantify the importance of the subangular lobe, we calculated the index (depth of the body behind m 2 / depth of the body in front of p 4) × 100. This index is 148 on the mandible with a strong subangular lobe (ACA 549), and 130 on the mandible with a weak subangular lobe ACA 294. We hypothesize that this difference in the development of the subangular lobe is due to sexual dimorphism, a strong subangular lobe being characteristic of male individuals. This value is 147 for the type mandible of N. donnezani from Perpignan, 133 for the mandible of Layna, Spain, 123 for the type mandible of N. tingi, but 142 for the other mandible referred to this species from the Upper Gaozhuang Formation (Tedford & Qiu 1991: fig. 1 G). In other words, all these specimens are similar in the robustness of the subangular lobe if we consider that the large values indicate male individuals and the small values female individuals. This index cannot be applied to N. megamastoides, N. sinensis, N. abdeslami and N. procyonoides because in these species the subangular lobe is situated in a different position, as we will see below. Another character of the subangular lobe is its position and shape. On specimen MNHN. F. ACA 549 it extends from beneath the distal half of m 1 to behind m 3, and its distal margin is curved. The mandibles of N. donnezani from Perpignan and N. tingi from the Yushe Basin have a similar shape and position of the subangular lobe (Depéret 1890; Tedford & Qiu 1991). On the fragment of mandible from Layna (Soria & Aguirre 1976: pl. 2, fig. 1; Bartolini Lucenti et al. 2018: fig. 4 A-C), the subangular lobe is weaker and starts a little more distally than on the type mandible from Perpignan. We suggest that the Layna hemimandible may represent a female individual of N. donnezani. Koufos (1997) referred to N. tingi a well-preserved skull from Megalo Emvolon, Greece, but its mandible is unknown. In N. megamastoides from Perrier (France) and from many other localities in Europe, N. vulpinus from St Vallier, N. abdeslami from Morocco, as well as in the extant species N. procyonoides, the ventral margin of the body is almost flat and the subangular lobe is situated more posteriorly, its maximum development being under the coronoid process. In N. sinensis from China, the ventral margin of the mandible is irregularly curved, and the subangular lobe is situated a little more anteriorly than in N. megamastoides and N. abdeslami. Distal to the subangular lobe, MNHN. F. ACA 549 displays an open angle between the subangular lobe and the base of the ascending ramus; this part is not preserved on the other specimens of Çalta. In the mandibles of N. donnezani from Perpignan and Layna, this angle is also a rather open curve. In N. megamastoides, N. abdeslami and N. sinensis the distal margin of the subangular lobe is almost vertical, and the angle between this lobe and the angular process is sharp. For this character, N. vulpinus displays an intermediate position. The labial face has two mental foramina, the larger one is under the p 1 at the mid depth of the body, and the second smaller one is under p 3 and situated in the upper part of the body. In N. tingi, the second foramen is placed under the anterior root of the p 3. Although there are two mental foramina in all species, their position is somewhat variable between individuals. Judging by our reading of the literature, sexual dimorphism in fossil species of Nyctereutes is unknown. This may be partly explained by the limited number of specimens in most localities and their fragmentary nature, which is insufficient to demonstrate sexual dimorphism. However, some localities, such as Saint-Vallier (France, latest Pliocene) have yielded abundant remains of raccoon dog. The Saint-Vallier material has been studied by Viret (1954), Martin (1971) and Argant (2004) who referred it to N. megamastoides, by Soria & Aguirre (1976) who distinguished it as a new subspecies N. megamastoides vulpinus, and by Monguillon et al. On the other hand, Hidaka et al. (1998) and Kim et al. (2012) observed some features indicating sexual dimorphism in the extant species N. procyonoides, such as stronger canine width, longer m 3, thicker mandibular body and narrower postorbital constriction in male individuals, and a more globular braincase in female individuals. These observations partly overlap with the morphological differences that we noted as due to sexual dimorphism in the skulls and mandibles from Çalta. Dentition The only upper incisor preserved is an I 3 of MNHN. F. ACA 292, which has an asymmetric and rather sharp crown (Fig. 1). Its buccal face is slightly curved. The lingual face is curved mainly at the base of the crown. The morphology is quite similar to that of the I 3 of V. vulpes and N. procyonoides. The upper canine is long, sharp and barely curved. It is similar in size and thickness to that of N. donnezani of Perpignan (Fig. 2). In N. megamastoides from Dafnero in Greece and Kvabebi in Georgia (Vekua 1972; Koufos 1993; Rook et al. 2017), as well as in the extant N. procyonoides, the upper canine is rather gracile and curved distally, similar in that of N. tingi from China. The canines of V. vulpes are slightly more pointed than in the specimens of Çalta. The P 1, P 2 and P 3 are not preserved. There is a diastema of about 5 mm between the single alveolus of P 1 and the anterior alveolus of the P 2. The P 4 is robust compared to that of V. vulpes, but similar to that of N. donnezani from Perpignan and Layna (Figs 1; 2). The anterior depression between the protocone and paracone is moderately deep, similar to N. donnezani (Perpignan and Layna). In N. megamastoides of Perrier this depression is more lingual, as it is in N. tingi, while in other specimens of N. megamastoides (Montopoli, Dafnero, Sesklon, Kvabebi) and N. sinensis (Nihowan and Yushe Basin), the anterior face of the P 4 is almost straight. The latter two species differ in having the protocone strongly projected antero-lingually like in V. vulpes, while on the Çalta specimens, it does not exceed the level of the anterior margin of the paracone or is barely anterior to it. In N. tingi, the protocone is small, protrudes anterior to the paracone and is situated near it, thus shaping slender the outline of P 4. There is a sharp ridge descending from the tip of the paracone anteriorly. Bartolini Lucenti (2017) provided a detailed morphological analysis of P 4 in different species of Nyctereutes. He noted that the metastylar blade is short in N. donnezani from Perpignan and Layna, and N. vulpinus from Saint-Vallier, France, while it is long in the type material of N. megamastoides from Perrier, indicating a more carnivorous diet. We tried to calculate the ratio of the metastylar blade to the total buccal length (paracone + metastylar blade) in all available records of Nyctereutes from Eurasia. Our results are not conclusive. The metastylar blade represents 37 to 46 % of the total length, without, however, discriminating any species. For instance, on seven P 4 from Çalta, this ratio varies between 38.8 and 43.1 %. A continuous and thick lingual cingulum runs from the distal edge of the protocone to the distal base of the metacone. This cingulum is weak in M. megamastoides (Perrier, Montopoli, Dafnero, Sesklon, Kvabebi), N. vulpinus (St. - Vallier) and in the extant N. procyonoides, but similar in thickness to that of the Çalta specimens in N. donnezani (Perpignan, Layna) and N. sinensis (Nihowan). In summary, the P 4 from Çalta is almost identical in proportions and morphology to that of N. donnezani from Perpignan and Layna (Fig. 4). The M 1 is almost as long as it is wide (Fig. 4). However, the typical feature of this molar is the narrowness of its lingual part, which gives it an almost triangular outline, a character shared with W W W 7 9 9 5 7 7 3 5 5 1 3 3 681012145101520254681012 N. donnezani - Layna N. donnezani - Çalta N. tingi – Yushe N. donnezani - Perpignan N. donnezani, N tingi, and N. procyonoides. In N. megamastoides, N. abdeslami and N. sinensis, the lingual part is larger, and the molar has a trapezoidal outline. In addition, the occlusal outline of M 1 and M 2 in the first group of species is curved distally in their lingual parts, as in Vulpes and Canis, while in the second group the M 1 is not curved distally, but the M 2 is. The paracone and metacone are equally large on the M 1 of Çalta as in N. donnezani from Perpignan and Layna and N. megamastoides from Perrier, Dafnero, Sesklon and Kvabebi. In N. tingi, N. sinensis and N. procyonoides, the metacone is smaller than the paracone. The metaconule is well developed and slightly taller than the protocone. The M 1 is surrounded by thick buccal and lingual cingula and thin mesial and distal cingula. The development of the cingula displays intra and interspecific variation and is rarely used for species distinction. The M 2 is wider than long. The paracone is a little stronger than the metacone, and the metaconule is weaker than the protocone. These features are also found in N. donnezani, N. megamastoides, N. tingi and N. sinensis, but the latter two species have a metaconule that is even smaller. The hypocone is well developed and strongly raised, as in N. donnezani of Layna and Perpignan. It is different from that of N. sinensis, which has a much more massive hypocone (Teilhard de Chardin & Piveteau 1930). The labial and lingual cingula are present, well developed and continuous. The lingual part is curved distally as in other species of Nyctereutes, but this curvature is a little stronger in N. tingi, N. sinensis and N. procyonoides. The lower canine is sharp, a little shorter than in N. sinensis, N. procyonoides and V. vulpes, and in particular much less curved distally than in these species (Fig. 3). In these characters, it recalls N. donnezani from Layna, and N. tingi from the Yushe Basin. The p 1 is small and single-rooted, and its crown is narrow, sharp and, similar to that of N. donnezani and N. procyonoides asymmetric. In M. megamastoides, N. tingi and N. sinensis this tooth is strongly because of its tip is displaced mesially. asymmetric The other lower premolars are two-rooted, narrow, elongated and with a sharp tip (Fig. 3). Their length and width increase from p 2 to p 4. The mesial ridge is sharper than the distal one as in all other species of Nyctereutes. Only the p 4 has a distinct distal accessory cuspid. N. megamastoides and N. sinensis frequently also have a distal accessory cuspid on the p 3. The distal edge of the premolars is widened and only the p 4 has a distal cingulum, similar to N. donnezani and N. tingi. In other species, the distal edge of the premolars is much wider, in particular in p 4, and often surrounded by a cingulum. The m 1 is elongate and about twice as long as it is wide (Figs 3; 4). The anterior slope of the paraconid is almost vertical, while its posterior slope is inclined, similar like in N. donnezani. In other species, the distal slope of the paraconid is almost flat or slightly inclined near the protoconid. The protoconid is well developed, massive and greatly dominates the other cusps. The talonid is wide as, or even wider than the trigonid. This is also the case in other species of Nyctereutes, except in N. sinensis and N. donnezani from Perpignan, which have narrower talonids, while in the specimens of Layna, also referred to N. donnezani, the talonid is wider than the trigonid. The hypoconid is slightly more developed than the entoconid. In N. megamastoides, they are almost equal in volume whereas the hypoconid is much more developed than the entoconid in N. tingi and N. sinensis. The presence of a weak hypoconulid can be noted like in N. megamastoides and N. sinensis. The m 2 is elongate, and its talonid is a little narrower than the trigonid (Fig. 3). In N. megamastoides the m 2 is robust, almost rectangular in outline and more elongated. In N. tingi, N. sinensis and N. procyonoides the talonid of m 2 is reduced. This is also the case with the specimens of N. donnezani from Perpignan and a right hemimandible from Layna (LC- 3; Soria & Aguirre 1976: pl. 2, fig. 1), which have m 2 with a narrow and reduced talonid, while on another right mandible from Layna (unnumbered; Soria & Aguirre 1976: pl. 2, fig. 2), the distal part of m 2 is not reduced, and its shape is similar to that of the Çalta specimen. On the m 2 of Çalta, the cusps are well developed, the metaconid is larger than the other cusps like in N. sinensis and N. megamastoides. There is a strong anterolabial cingulum as in N. megamastoides and N. donnezani. This cingulum is reduced or vestigial on the m 2 of the Chinese species. The m 3 is small and ovoid in outline (Fig. 3). It has a welldeveloped protoconid and a weak metaconid. This tooth is different from m 3 of N. tingi in having two cusps instead of one. In other species, the m 3 has two or even three cusps of variable volume. Regarding the size of teeth (Table 2; Fig. 4), the Çalta raccoon dog displays intermediate values between the larger N. tingi from the Yushe Basin in China and N. donnezani from Perpignan and Layna in western Europe. Using size criteria, Bartolini Lucenti (2018) suggested excluding the Çalta raccoon dog from N. donnezani, and referred it to Nyctereutes sp. In detailed comparison, the p 4 and m 1 of N. tingi are larger than all specimens referred to N. donnezani, including Çalta, while this is not obvious for the upper cheek teeth and the m 3. The m 3 of N. tingi is smaller than that of Çalta, Perpignan and Layna. The upper cheek teeth of N. tingi are poorly documented, with only two specimens for each, one small, similar in size to that of N. donnezani, while the other is larger than those of N. donnezani and Çalta. The dimensions of P 4, M 1, M 2 and m 2 from Çalta are greater than those of N. donnezani from Perpignan and Layna, while the p 4 and m 1 are similar in size to the ones from these localities. In summary, the size of the cheek teeth from Çalta are intermediate between the smaller teeth from Perpignan and Layna (N. donnezani) and the larger teeth from the Yushe Basin (N. tingi). Regarding the lack of obvious size differences, one can wonder what is the effect of sexual dimorphism on the dentition of Nyctereutes. Kim et al. (2012: 1614) observed in N. procyonoides that “ sexual difference is more apparent from data relating to the skull than that relating to the teeth ”. Taking into consideration these results, the size of the cheek teeth alone seems not useful for species differentiation given the lack of statistically significant samples for each species. The skull, mandible and dentition of the Çalta raccoon dog have many morphological similarities with those of N. donnezani from its type locality Perpignan as well as from Layna. As noted above, they display several characters that are different from other species of the genus, in particular N. tingi, N. sinensis, N. megamastoides and N. abdeslami. In view of this, it is very likely that the specimens of Çalta belong to N. donnezani. This identification will be tested by the phylogenetic analysis of cranial and dental characters in various species of the genus Nyctereutes.