Carcharomodus escheri (Agassiz, 1843) Kriwet & Mewis & Hampe, 2015

Kriwet, Jürgen, Mewis, Heike & Hampe, Oliver, 2015, A partial skeleton of a new lamniform mackerel shark from the Miocene of Europe, Acta Palaeontologica Polonica 60 (4), pp. 857-875 : 861-870

Carcharomodus escheri (Agassiz, 1843) comb. nov.

Figs. 2 , 5–11 .

1843 Carcharodon escheri ; Agassiz 1843: 260, pl. 36: 16–21.

1926 Oxyrhina hastalis Agassiz var. escheri Agassiz ; Leriche 1926: 409, pl. 33: 1–8. 1927 Oxyrhina hastalis Agassiz var. escheri Agassiz ; Leriche 1927: 74. 1961 Isurus hastalis escheri (Agassiz) ; Kruckow 1961: 44, table 1

(name only). 1969 Isurus (Oxyrhina) escheri (Agassiz) ; van den Bosch 1969: 30,

figs. 27–39, 53, 55, 58–59. 1975 Isurus escheri (Agassiz) ; Bosch et al. 1975: 99, pl. 23, figs. 5–7. 1983 Isurus escheri ; Bendix-Almgreen 1983: 2, 22 (name only). 1987 Isurus escheri Agassiz ; Cappetta 1987: 96. 1988 Isurus escheri (Agassiz, 1843) ; Nolf 1988: 34, 162. 2006 Carcharodon escheri (Agassiz, 1843) ; Cappetta 2006: 78. 2008 Cosmopolitodus escheri ; Wijnker et al. 2008: 174 (name only). 2010 “ Carcharodon ” escheri (Agassiz, 1844) ; Mollen 2010: 66, 67. 2012 Isurus escheri ; Ehret et al. 2012: 1144, 1145, 1150. Holotype: ETZ 0000000001750 (barcode number, previous collection number is ETZ P144), upper lateral tooth ( Fig. 4 ). Type locality: Switzerland (exact locality unknown). Type horizon: “Kalkschiefer”, Upper Marine Molasse, Burdigalian– Ottnangian, early Miocene.

Material.—Single incomplete and disarticulates specimen, MNU 071-20.

Diagnosis.—Same as for genus.

Description.—The skeleton of sharks is primarily cartilaginous but in certain places where strength is particularly important, shark cartilage secondarily ossifies, forming calcified hydroxyapatite bone ( Ridewood 1921; Goodrich 1930; Applegate 1967; Moss 1977; Compagno 1999). In particular, the jaws and the vertebral centra undergo secondary calcification during ontogeny, as the spinal column has to resist the powerful compressional forces of the surrounding water (e.g., Ridewood 1921; Dean and Summer 2006; Porter et al. 2014). Additionally, shark vertebrae grow through the incremental addition of calcified concentric rings (annuli). Centra are much more often preserved than other parts of the skeleton, but are most often found disassociated from the dentitions.

The partial skeleton presented herein comprises disarticulated teeth of all jaw quadrants and vertebral centra ( Fig. 2 ). Unfortunately, no remains of the jaws and fin skeleton are preserved or were recovered during excavation. Along with the dentition, 49 calcified vertebral centra ( Figs. 5–7 ) of Carcharomodus escheri are more or less well preserved. Most are damaged or only partly preserved; some were too imperfect for study or even being measured. When possible, three measurements were taken: height, width, and depth ( Table 1). The recovered vertebral centra range from 1.26 to 7.77 cm in width. Although the vertebral centra were all disarticulated, their gradual decrease in size proves evidence that they once belonged to one vertebral column of a single individual ( Fig. 8 ).

The amphicoelous centra are of typical lamniform appearance, being slightly compressed dorso-ventrally and with deeply concave anterior and posterior faces. The largest vertebral centra are situated close to unidentifiable cranial remains decreasing continuously posteriorly in diameter size. The centra bear distinctive small circular perforations running through their centres representing the passage for the notochord. The better-preserved vertebral centra still show prominent paired dorsal and ventral depressions for articulation with the corresponding neural (basidorsal) and haemal (basiventral) arches. It is possible to determine the orientation of the vertebrae with the help of the distance of these depressions, because the basidorsal depressions are placed closer together than the basiventrals. Unfortunately, it was impossible to identify the attachment depressions for ribs because the larger centra, which are considered thoracic vertebrae, are less well preserved, being crushed. The calcification pattern of the vertebral centra of Carcharomodus escheri corresponds to the radial asterospondylic type ( Hasse 1879), which is characteristic for lamniform sharks ( Fig. 9 ).

Contrary to the vertebrae, fossil shark teeth possess high potential to provide information about taxonomic identities, phylogenetic relationships, life-history traits (e.g., ontogenetic changes, sexual variations, etc.) and diet preferences. The preserved tooth set of the specimen studied here thus is of major interest. It consists of 42 associated teeth from all four jaw quadrants ( Fig. 2 ) ranging in size from ca. 1.5 to 4.2 cm in total height ( Table 2). The marked dignathic and monognathic heterodonty patterns simplify the determination of each tooth position within the jaws. The 13 dental measurements taken from each tooth, which assisted in reconstructing the dental pattern of the studied sharks, are depicted in Table 2.

In addition to fully mineralised teeth with crown and root, some teeth are preserved only as thin enamel shells, which are often broken basally and which lack roots. These incomplete teeth represent replacement teeth, some of which are probably separated by two or more teeth from the functional tooth position of their corresponding file.

The symmetry of the principal cusp was used to divide teeth into two groups. The first sample comprises highly asymmetrical teeth with a distally inclined cusp with less well marked lateral cusplets of the upper jaw ( Fig. 10 ), whereas the second sample consists of more or less symmetrical teeth with small but distinct lateral cusplets of the lower jaw ( Fig. 11 ). Teeth of the upper and lower jaws were divided into right and left teeth after measuring the length of the mesial and distal cutting edges. The mesial cutting edges are always longer than the distal ones giving the teeth an asymmetric appearance in upper teeth. Teeth that are virtually identical in size and shape, and which provide similar measurements, are interpreted to come from the same tooth row and are thus lumped together. Furthermore, teeth of each identified jaw quadrant were sequentially assembled from larger, more erect principal cusps to smaller, more inclined principal cusps. All fully developed teeth present a more or less labio-lingually flattened crown, a triangular principal cusp, and most teeth have at least one pair of small, triangular lateral cusplets.

A B E F G C D H I J K L M N O P Q 10 mm R S T U V

The lingual neck separating the crown and the root is rather narrow and almost horizontal with only a faint medial concavity. The bilobed root is well developed but rather low, with generally one, rarely two small nutritive foramina on the salient lingual root protuberance. The root lobes are separated by a broad and shallow concavity, which is slightly more pronounced in anterior lower teeth. The principal cusp generally possesses a razor-like, irregularly crenulated cutting edge, whereas the lateral cusplets are devoid of any crenulations or serrations. This crenulation is stronger than the weak crenulation found in some teeth from the late Miocene Pacific, which previously were associated with Cosmopolitodus hastalis , but which certainly represents a different taxon. It is, however, not as strong as the saw-like serration of the cutting edges of Carcharodon carcharias teeth, which show clearly developed sharp points. The cutting edges of the teeth of Carcharomodus escheri are comparable

10

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cm

(

Width

1 0 5 10 15 20 25 Number of centra to emery paper, which consists of tiny little grains that produce an irregular serration.

Teeth of the upper jaw ( Fig. 10 ) are broader than the teeth of the lower jaw with distally inclined or curved main cusps, whereas the main cusps of lower jaw teeth are nearly erect. The lateral cusplets are less developed and greatly reduced at least in anterior and anterolateral files, and generally become slightly more distinct in posterolateral files. However, these lateral cusplets are never as distinct as those of lateral teeth. In all upper teeth, the principal cusp height is greater than its basal width.

The specimen preserves only two teeth referable to upper anterior positions ( Fig. 10A ), which are also the largest of all preserved teeth. Both are identical in shape and probably come from the same tooth row. The root of the slightly larger tooth is better mineralised than the root of the other one, but it is broken and not completely preserved, similar to the condition found in replacement teeth. The labial face base of the crown very slightly overhangs the root. The root is low with sub-vertical, slightly converging lateral edges in labial and lingual views. The root lobes are not distinctly separated but broadly united forming an obtuse angle with a very broad and shallow median concavity. The lingual protuberance is weak. A nutritive foramen cannot be observed due to the state of preservation. Very diminutive lateral cusplets are preserved mesially and distally, which are not well separated from the main cusp. Their size is not more than 6.3% of the size of the main cusp. The main cusp is broad and shows a complete but irregularly crenulated cutting edge and is inclined distally forming an angle of about 19°. Both mesial and distal cutting edges are slightly concave in their lower half with the mesial cutting edge being significantly longer than the distal one. The tip of the crown points labially.

One of the preserved teeth could be identified as an intermediate tooth because it is differently shaped in comparison to all other upper lateral teeth ( Fig. 10B ). The angle between its root lobes is 160°, whereas the root lobes of the other upper lateral teeth of similar size form a more obtuse angle of 135° on average. As in the anterior teeth, the base of the labial face of the crown very slightly overhangs the root, and the lingual protuberance is weak. The lingual face of the root shows two nutritive foramina, with one of them being slightly smaller than the other. A multiple pair of lateral cusplets accompanies the main cusp with its irregularly crenulated cutting edges. The lateral cusplets are not symmetrical on both sides, but the mesial one is divided forming two incipient tips, whereas the distal one is divided into three very small tips. Though the lateral cusplets are minute in size (7.85% of the total crown height), they are more distinct than those of the anterior teeth. The principal cusp is almost hook-like with a quite long and in its upper part convexly curved mesial but distinctly concavely curved distal cutting edge forming an angle of about 12° with the basal face of the root. It is reduced in size with its crown height being only about 58% of the crown height of the second anterior tooth, and about 79% of the crown height of the first lateral tooth. The root of the upper intermediate tooth is almost rectangular with broadly united root lobes separated only by a very shallow concavity, massive and with subvertical, converging lateral edges similar to the condition seen in the second anterior upper tooth. Following Shimada’s (2002a) terminology, this tooth corresponds to the intrabullar intermediate tooth (or third upper anterior tooth).

Thirteen preserved teeth represent upper laterals ( Fig. 10C–L ). None of the lateral teeth has lateral cusplets that are equal in size on both mesial and distal sides but the presence of lateral cusplets in upper teeth seems to be very variable. The distal lateral cusplets generally are better developed and show more tips than those of the mesial side, but all are very minute. Even in the smallest preserved lateral tooth the height of the lateral cusplets does not exceed 8.28% of the total crown height. All teeth possess a main cusp that is distally inclined, with its tip being curved labially. The lingual protuberance is salient in all upper lateral teeth, and the lingual face of the root reveals one to two nutritive foramina, with one being smaller than the other.

One of the fully mineralised and best preserved teeth differs significantly from the others in having seemingly smooth cutting edges and a finer, more angular root with lobes forming an angle of about 150°, whereas the root lobes of the other lateral teeth form an angle of 135° on average ( Fig. 10B ). The mesial cutting edge is significantly concave, whereas the distal one is convex, giving the apex an anteriorly twisted appearance. Conversely, the mesial cutting edge is convex and the distal one more concave in all other teeth identified as upper laterals. The root is very low, with lobes that extend laterally more than 20% from the base of the crown, which is also distinct from other upper laterals. Only the mesial side shows a small heel that can be regarded as a very reduced lateral cusplet. It is also remarkable that this is the only tooth in the upper jaw where the base of the labial face of the crown does not overhang the labial face of the root. Nevertheless, based on its general size and appearance, we identify this tooth as being the first upper lateral tooth. This tooth clearly separates the new taxon from all other similar lamnid sharks. However, we refrain here from including this tooth in the diagnosis, because of its quite distinct morphology and hypothesised jaw position pending further studies of associated or completely articulated dentitions of this taxon.

Teeth of the lower jaw ( Fig. 11 ) are characterised by lateral cusplets that are more or less equal in size on both sides of the nearly erect and less blade-like main cusp. In almost all the teeth of the lower jaw the principal cusp height is only slightly greater than its width.

Five teeth represent lower anteriors in comparison with extant lamnid taxa. Three of the teeth are badly preserved and lack their roots. The two others are identical in size and shape, with one being completely developed with fully mineralised cusp and root, whereas the other is preserved as a thin enamel shell only, representing a replacement tooth. They thus represent two rearward positions and belong to the same tooth row and possess a slightly distally curved cusp with an anteriorly twisted apex. Labially, the main cusp distinctly juts out over the root. Lower anterior teeth are more slender than upper anteriors and superficially resemble those found in Isurus . Their roots are more massive, with one nutritive foramen, and display a more developed lingual protuberance. The asymmetrical root lobes are elongate and form an obtuse angle of 110° with the anterior root lobe, being more slender and longer than the distal one. Differences from Isurus and Cosmopolitodus include crenulated cutting edges and very incipient multiplied lateral cusplets with their height being only 6.4% of the total crown height.

The crown height of the third lower anterior, which also could be considered a lower intrabullar intermediate, is only 72.5% of that of the largest and most completely preserved lower anterior tooth. It is nevertheless larger than the following, first lateral tooth. It displays two symmetrical pairs of well-developed lateral cusplets, whose height is nearly 12% of the total crown height, escorting a nearly erect and straight main cusp with completely crenulated cutting edges. The main cusp reveals a lingual re-curvature and the apex point labially. The root shows a lingual protuberance and one nutritive foramen. The elongated root lobes are not symmetrical in shape, with the mesial one being more slender and elongated than the distal one similar to the condition found in lower anteriors. They form an obtuse angle and a V-shaped notch.

Thirteen teeth are identified as belonging to lower lateral files. Apart from the posterolateral teeth that display a slight inclination, the main cusps of lower lateral teeth are nearly vertical. All lateral teeth show two to three pairs of well developed, symmetrical lateral cusplets with heights between 14.3% and 23.8% of the total crown height, increasing from anterolateral to posterolateral files.

Body size estimates.—Only two teeth can be referred to upper anterior tooth rows, most probably from the second row. A definite, completely preserved first upper anterior is not available, as used in the work of Gottfried et al. (1996) to estimate the total body length. Gottfried et al. (1996) use a different terminology than Shimada (2002a). What Gottfried et al. (1996) call the second upper anterior [UA2] is the first upper anterior tooth [UA1] of Shimada (2002a). However, comparing the measurements of the tooth heights in extant Great White Sharks ( Hubbell 1996), the two upper anterior teeth hardly differ in size or are even of nearly the same height, and therefore the same is assumed for the two upper anterior teeth of Carcharomodus escheri . The total height (crown + root) of the inferred second upper anterior tooth of this taxon measures almost exactly 42 mm. Applying the formula of Gottfried et al. (1996), a total body length of 3.81 m is established.

Tovalidatethisbodysizeestimate,wealsousedShimada’s (2002d) method based on the second upper anterior tooth. The crown height of the second upper anterior is 31.76 mm, resulting in a total body length of 3.82 m, which is almost the same as derived from Gottfried et al’s (1996) equation. For comparison, we also used the equation for body size estimation of Isurus spp. established by Shimada (2002c) assuming that the new taxon represents a lamnid shark with similar dental patterns to living lamnid sharks. Based on this equation and using the second upper anterior, the body size amounts to 3.67 m, which is slightly smaller than those derived from comparisons with the living Great White Shark. It is important to note that the teeth of the specimen described herein are not the largest ever found of this species. Others can reach a height of up to 50 mm, which would imply a body length of almost 5.00 m.

For comparison, we also calculated the total body length of our specimen using the size of vertebral centra and employing Gottfried et al.’s (1996) method. Extant Great White Shark, Carcharodon carcharias , has a total of 172 to 187 vertebrae, with the largest in the mid-body region ( Gottfried et al. 1996), and very small ones that extend to the posterior tip of the caudal fin. Assuming that Carcharodon carcharias is closely related to Carcharomodus , it is likely that only 36% of the vertebrae are preserved in this specimen. Although the vertebral column thus is far from complete, it is still useful to estimate the total body size of this shark.

The largest preserved vertebral centrum has a diameter of 77.7 mm. This measure thus equals ca. 4.50 m total body length, which is significantly larger than the estimates derived from the teeth. This discrepancy might be related to the fact that the lamnid described here represents a different taxon. It is, however, reasonable to assume a total body length of this specimen of about 4.0 m based on all available evidence.

Age estimates.—Vertebral centra accumulate calcified growth material as they age, producing concentric layers, which can be used for age estimates of sharks both living and extinct ( Cailliet et al. 2006; MacFadden et al. 2004). These concentric layers include opaque and translucent bands, which are generally assumed to have been deposited seasonally ( Cailliet and Goldman 2004), and a pair of these layers forms a “ring” deposited annually (e.g., Gruber and Stout 1983; Natanson et al. 2002). However, various exceptions were documented for different sharks that cast some doubt on this model of annual ring periodicity (e.g., Stevens 1975; Natanson 1984; Cailliet et al. 1985; Branstetter and Musick 1994; Casey and Natanson 1992; Natanson 1993; Hamady et al. 2014). Nevertheless, the majority of studies indicate annual ring formation for most sharks, including lamniforms (e.g., Smith and Aseltine-Neilsen 2001; Campana et al. 2002). Although a detailed age analysis of the fossil lamniform shark using sophisticated methods such as bomb radiocarbon dating ( Campana 2001) is beyond the scope of this paper, it is important to provide a rough age determination for assessing whether it is a juvenile or already has reached maturity. Ring count was executed on the X-ray images and all additional preserved vertebral centra starting at the birth-mark. Accordingly, all vertebrae display more than 10 (12–14) pairs of rings ( Fig. 9 ). It is not possible to establish the exact number of bands because no thin sections of vertebral centra could be prepared. Nevertheless, our results suggest that this specimen of Carcharomodus escheri was more than 10 years old representing a late subadult to adult individual in comparison to living lamnid sharks(compare,e.g., Fowler et al.2005; Goldman and Musick 2006; Cassoff et al. 2007).

Remarks.—Agassiz(1843) erected the species “ Carcharodon escheri ” for isolated teeth from the early-middle Miocene (Upper Marine Molasse) of Switzerland and southern Germany, respectively. These are the only definite findings from the Miocene Molasse basins. The holotype is the first tooth figured by Agassiz (1843: pl. 36: 16–18) from Switzerland. The exact locality of this specimen is unknown. The second figured tooth from southern Germany represents the paratype (Agassiz 1843, pl. 36: 19–21). Lateral cusplets are not preserved in both teeth because the basal parts of the cutting edges and the mesial root lobe in the holotype are damaged. In their general morphology, nevertheless, both teeth represent upper laterals. The synonymy list given above is far from being complete and only lists the most important references. This species was assigned variously to the genera Carcharodon , Isurus , Macrorhizodus , and Oxyrhina (e.g., Glikman 1964; Cappetta 2012). Woodward (1889: 411) synonymised Carcharodon escheri with Carcharodon subserratus Agassiz, 1843 based on a single specimen from the Eocene of Sheppey. According to Ward in Cappetta (2012) the specimen on which Woodward (1889) based his assignment represents a heavily mineralized and slightly abraded specimen, which originated from the Antwerp area and was imported to Sheppey, where it was sold with local fossils in the 19 th century leading to the misinterpretation by Woodward (1889). Carcharodon subserratus represents a member of a distinct evolutionary lineage of very large macrophageous lamniforms of Carcharocles .

Stratigraphic and geographic range.—This species is quite common in the Mio-Pliocene of Europe (e.g., Leriche 1926; Kruckow 1960, 1965; Ceuster 1976; Bosch 1969, 1978, 1980; Bosch et al. 1975; Bendix-Almgreen 1983; Moths 1998). Its teeth, however, are very rare in the late early Miocene but become more abundant in the middle to late Miocene of the boreal realm (e.g., Priem 1912; Leriche 1926; Kruckow 1965; Brzobohatý and Schultz 1973; Cappetta 2012). The stratigraphic youngest remains are from the Zanclean–early Piacenzian (Pliocene) of, for instance, the Netherlands ( Wijnker et al. 2008). Teeth identified as Oxyrhina hastalis var. escheri from the early Miocene of the Antwerp region by Leriche (1926) were transferred to Isurus xiphodon and Isurus hastalis , respectively, by Purdy et al. (2001). Carcharomodus escheri seems to be extremely rare in the Miocene Molasse Basin with the two teeth described by Agassiz (1843) being the only definite records. So far, we were not able to identify any other unambiguous specimen of this peculiar species in any Miocene locality of the Miocene Molasse Basin.

The taxonomic assignments of teeth from the Miocene of Portugal and Spain identified to this species ( Antunes and Jonet 1970; Serralheiro 1954; García et al. 2009) are ambiguous and we currently consider these as belonging to another isurid species. Additional teeth assigned to “ Isurus escheri ” were reported from many Mio-Pliocene localities outside of Eurasia. For instance, Fitzgerald (2004) reported

Isurus escheri ” from the early Pliocene of Australia and Muizon and DeVries (1985) from the late Pliocene of Peru. However, we agree with Nyberg et al. (2006) and restrict the lamnid species Carcharomodus escheri to specimens occurring along the Atlantic coastline of Europe. All other specimens recovered outside Europe assigned to this species need to be transferred to a different taxon (e.g., Ehret et al. 2012). Consequently, Carcharomodus escheri seems to be a predominant element of Western and Central European elasmobranch faunas during the Miocene.

Figures

Fig. 2. Photograph (A) of mounted specimen MNU 071-20 of the mackerel shark Carcharomodus escheri (Agassiz,1843) in the museum and drawing (B) of its in situ finding position, in Gross Pampau, the middle–late Miocene, depicting preserved teeth and vertebral centra. The large anterior vertebrae were recovered from the sediment after the in situ drawing during the excavation was produced.

Fig. 5. Trunk vertebrae of the mackerel shark Carcharomodus escheri (Agassiz, 1843), MNU 071-20, from Gross Pampau, the middle–late Miocene, displaying the characteristic lamniform morphology and concentric growth bands from anterior (A) to posterior (P).

Fig. 4. Holotype of the mackerel shark Carcharomodus escheri (Agassiz, 1843) from the Upper Marine Molasse (Burdigalian-Ottnagian, early Miocene) of Switzerland. A. Original drawings of Agassiz (1843: pl. 36: 16–18), in labial (A1) and lingual (A3) views. B. Photographs of holotype (ETZ 0000000001750), in labial (B1) and lingual (B2) views.

Fig. 8. Graphic representation of vertebral size decrease in Carcharomodus escheri (Agassiz, 1843) from anterior to posterior. Steps at positions 10-11, 14-15 and 18-19 indicate missing portions due to collecting and/or taphonomic artefacts.

Fig. 9. Radiographs of vertebrae of the mackerel shark Carcharomodus escheri (Agassiz, 1843), MNU 071-20, from Gross Pampau, the middle– late Miocene. A. Precaudal vertebra, same as in Fig. 6Q. B. Caudal abdominal/caudal vertebra, same as in Fig. 7J.

Fig. 10. Upper teeth of the mackerel shark Carcharomodus escheri (Agassiz, 1843), MNU 071-20, from Gross Pampau, the middle–late Miocene. A. Second upper right anterior tooth. B. Right upper first lateral tooth. C–L. Left (C, D, G, I, K) and right (E, F, H, J, L) upper teeth. Labial (A1–L1) and lingual (A2–L2) views. For positions of lateral teeth within jaw see Fig. 12.

Fig. 11. Lower jaw teeth of the mackerel shark Carcharomodus escheri (Agassiz, 1843), MNU 071-20, from Gross Pampau, the middle–late Miocene. A. Lower left anterior tooth. B. Lower left intermediate tooth.C–H. Lower lateral teeth. Labial (A 1 –H 1) and lingual (A 2 –H 2) views. I. Incomplete anterior lower lateral tooth. J, K. Incompletely mineralized lower replacement teeth.