Exceptionally preserved shark fossils from Mexico elucidate the long-standing enigma of the Cretaceous elasmobranch Ptychodus

Abstract

The fossil fish Ptychodus Agassiz, 1834, characterized by a highly distinctive grinding dentition and an estimated gigantic body size (up to around 10 m), has remained one of the most enigmatic extinct elasmobranchs (i.e. sharks, skates and rays) for nearly two centuries. This widespread Cretaceous taxon is common in Albian to Campanian deposits from almost all continents. However, specimens mostly consist of isolated teeth or more or less complete dentitions, whereas cranial and post-cranial skeletal elements are very rare. Here we describe newly discovered material from the early Late Cretaceous of Mexico, including complete articulated specimens with preserved body outline, which reveals crucial information on the anatomy and systematic position of Ptychodus. Our phylogenetic and ecomorphological analyses indicate that ptychodontids were high-speed (tachypelagic) durophagous lamniforms (mackerel sharks), which occupied a specialized predatory niche previously unknown in fossil and extant elasmobranchs. Our results support the view that lamniforms were ecomorphologically highly diverse and represented the dominant group of sharks in Cretaceous marine ecosystems. Ptychodus may have fed predominantly on nektonic hard-shelled prey items such as ammonites and sea turtles rather than on benthic invertebrates, and its extinction during the Campanian, well before the end-Cretaceous crisis, might have been related to competition with emerging blunt-toothed globidensine and prognathodontine mosasaurs.

1. Introduction

Ptychodus Agassiz, 1834 (Elasmobranchii: Ptychodontidae) is a cosmopolitan group of fossil sharks occurring in Albian–Campanian (approx. 105 to 75 million years old) marine deposits of all continents except Antarctica (e.g. [1–10]). This diverse Cretaceous genus, including at least 16 species, is primarily known from isolated teeth and partial dentitions. Two species groups, which often co-occur with each other, can be distinguished: species with low-crowned (uncuspidate) teeth and species with high-crowned (cuspidate) teeth, such as Ptychodus decurrens and P. mammillaris, respectively (e.g. [8,10]). Teeth were arranged in a way that they formed large dental plates supported by elongated, V-shaped jaws [1,8,9,11–14]. It is generally accepted that ptychodontids had a durophagous predatory lifestyle, using their massive grinding dentitions to prey on shelled bottom-dwelling animals such as bivalves, brachiopods and crustaceans, but also to hunt ammonites and other pelagic animals in the open water column [8,9,12,14–21]. Although complete specimens of Ptychodus have not been reported so far, the body size of this extinct predator was estimated to have reached or even exceeded 10 m in total length based on jaw elements and dentitions (e.g. [12,13]), making Ptychodus the largest durophagous shark that ever roamed the oceans, being even bigger than modern apex shark predators.

Since its first report in the first half of the eighteenth century based on some isolated teeth from the English Chalk [22,23], numerous researchers attempted to identify the relationships of this fascinating predator resulting in sometimes very contradictory interpretations ranging from representing durophagous bony fishes such as porcupinefishes as well as various cartilaginous fishes [23]. Although Ptychodus has been unanimously acknowledged to be a chondrichthyan since the seminal work of Agassiz [24], its exact affinities remained dubious for decades, and it was assumed to belong either to extinct hybodont sharks, modern sharks, or even rays [1,5,12,23,25–33]. Closer relationships to living mackerel sharks were already proposed by Hamm [34], but without providing substantial information or figures. Later, the same author [35] placed the family Ptychodontidae (i.e. Ptychodus and Paraptychodus [36]) in its own order, Ptychodontiformes, with unresolved relationships to other sharks. The new complete skeletons described here help resolve the long-standing enigma of Ptychodus. This material allows detailed phylogenetic and morphological analyses, which were implemented to identify the systematic relationships of Ptychodus and characterize the predatory lifestyle of this peculiar durophagous shark.

2. Material and methods

(a) . Repository of specimens

The six Ptychodus specimens examined for this study are part of the Colección Paleontológica de Coahuila (CPC) and are permanently housed in two Mexican public museums: the Museo La Milarca, San Pedro Garza García, Nuevo León (MMSP) and the Museo del Desierto, Saltillo, Coahuila (MUDE).

(b) . Geological setting

All the specimens studied here come from the quarries near Vallecillo (26° 39.32′ N, 100° 00.82′ W), Nuevo León, northeastern Mexico. In this region, the uppermost Cenomanian–middle Turonian Vallecillo Member comprises approximately 8 m of pinkish platy limestone intercalated in the monotonous marl-limestone series of the Agua Nueva Formation [37]. These beds were deposited in an open marine shelf environment [37,38] and include a unit of thin laminated layers rich in inoceramid bivalves, ammonites and vertebrates (e.g. [17,39]). The latter are represented by exquisitely preserved fossils of fishes (elasmobranchs, actinopterygians and actinistians) and marine reptiles (protostegid turtles, mosasauroids and polycotylid plesiosaurs) (e.g. [39–42]) (see electronic supplementary material, figure S1).

(c) . Phylogenetic analysis

We explored the phylogenetic relationships of the genus Ptychodus Agassiz, 1834 within the elasmobranchs using a modified version of Jambura et al.'s [43] data matrix. In order to provide a broader context of these relations, several Palaeozoic, Mesozoic, Cenozoic and Recent chondrichthyan taxa were additionally included as outgroups, with Pucapampella and Doliodus serving as the root. To accommodate the inclusion of these groups, several modifications and additional characters from previous works were added to the present data matrix (e.g. [44–56]; see electronic supplementary material, for additional references). The resulting data matrix was assembled in Mesquite 3.81 [57] and includes 221 characters (see electronic supplementary material and [58]).

The parsimony analysis was carried out in TNT v.1.6 [59], under Goloboff et al.'s [60] protocol, considering the inclusion of inapplicable characters. A traditional parsimony search with step matrices ('smatrix &') was conducted with the command 'mult' using TBR (tree bisection and reconnection) as the algorithm for branch permutations for 10 000 iterations holding ten trees for each iteration. This protocol was repeated ten times using the command 'loop' with different random seeds to evaluate if the tree space was adequately explored by the parameters. All ten searches recovered a similar number of most parsimonious trees (MPTs) (633–636) and the same strict consensus (see electronic supplementary material), suggesting an adequate search in the tree space. All MPTs recovered in these ten searches were included in the same file, from which a global strict consensus was generated. Jackknife and Bremer analyses were used to estimate clade support using the ‘resample’ and ‘jak’ commands. For the support analysis under a regular jackknife analysis (i.e. with independent deletion), 10 000 replications were carried out, from which the absolute frequencies of the groups on the strict consensus tree were estimated, leaving the remaining parameters in the default settings. The Bremer support was calculated based on suboptimal topologies 50 steps larger than the ones found in the parsimony analysis, collapsing groups with support lower than one (see scripts in [58]).

(d) . Ecomorphological analysis

The measurement data (see electronic supplementary material) for the extant species used to assess the ecomorphotype of Ptychodus were assembled from the literature [61–64]. We followed Sternes & Shimada's [65] strategy by using illustrations of reference books (i.e. FAO publications, authored by internationally recognized experts) to determine some morphometric measurements sometimes not provided in the literature and thus not available for all species included in the present analysis. Sternes & Shimada [65] demonstrated the high degree of similarity between the book illustrations and actual shark samples, thus showing that such drawings can be reliably used for interspecific morphometric analyses. Measurements of specimen MMSP CPC 3063 (142 cm TL) were used to infer measurements of medium-, large- and giant-sized Ptychodus sp. with three distinct maximum TL (2, 5 and 10 m, respectively). All measurements were log-transformed in order to improve normality and homogeneity of variance.

Using 11 linear body measurements (PCL, P1H, D1H, D2H, CFL, PD1, PD2, PP1, PP2, CDM, CPV) (electronic supplementary material, figure S10), we compared Ptychodus sp. to 42 modern shark species belonging to the eight main ecomorphotypes (i.e. probenthic, leptobenthic, squatinobenthic, littoral, bathic, microceanic, macroceanic, tachypelagic) defined by Compagno [66]. For each ecomorphology, we selected several species (all with two dorsal fins) representative of the size range and body proportions of the category (see electronic supplementary material, table S3). Two non-parametric tests revealed statistically significant differences between the ecomorphotypes (ANOSIM: R = 0.463, p = 0.0001; PERMANOVA: F = 12.46, p = 0.0001) (see electronic supplementary material, tables S4 and S5 for pairwise comparisons). A linear discriminant analysis (LDA) was performed using Paleontological Statistics (PAST) software, v. 4.04 [67] to maximize differences among a priori groups and predict the ecomorphotype of Ptychodus sp. The LDA matrix consists of 11 quantitative variables (log-transformed linear body measurements) and one qualitative variable (ecomorphotype category, here used as grouping variable) scored for 42 living shark species (assigned to eight given groups) plus Ptychodus sp. (with no given group). As the ecomorphotype of the latter is unknown, a ‘?’ was scored in the group column; thus, Ptychodus sp. was not included in the discriminant analysis itself but was classified (see electronic supplementary material).

3. Systematic palaeontology

Class Chondrichthyes Huxley, 1880

Subclass Elasmobranchii Bonaparte, 1838

Infraclass Neoselachii Compagno, 1977

Clade Selachimorpha Nelson, 1984

Superorder Galeomorphii Compagno, 1973

Order Lamniformes Berg, 1937

Family Ptychodontidae Jaekel, 1898

Genus Ptychodus Agassiz, 1834

Type species. Ptychodus schlotheimii Agassiz, 1834 (nomen oblitum), a senior synonym of Ptychodus latissimus Agassiz, 1835 (nomen protectum).

(a) . Material examined

MMSP CPC 3063, Ptychodus sp., complete well-preserved specimen (1420 mm total length (TL)) exposed in right lateral view, showing almost all skeletal elements, dentition, phosphatized muscle remains and body outline displaying all fins (figure 1a,b; electronic supplementary material, figure S2). MMSP CPC 3064, P. sp., almost complete juvenile specimen (565 mm TL) exposed in right laterodorsal view, showing jaws, dentition, vertebral column, pectoral, first dorsal and caudal fins, and most of the body outline (except second dorsal and anal fins) (figure 1c,d; electronic supplementary material, S3). MUDE CPC 3065, P. sp., a partial skeleton exposed in right lateral view, showing part of the neurocranium, scleral capsule, jaws, teeth, branchial elements, anterior vertebral column, and some dorsal fin radials (figure 2a; electronic supplementary material, figure S4). MMSP CPC 3066, P. sp., incomplete skeleton missing tail in left lateral view, showing neurocranial remains, scleral capsule, jaws, teeth, vertebral column, branchial elements, pectoral and first dorsal fins, phosphatized muscle remains and most of the body outline (figure 2b; electronic supplementary material, figure S5). MMSP CPC 3067, P. sp., slightly disarticulated almost complete skeleton (approx. 890 mm TL) exposed in left lateral view, showing some jaw elements (Meckel's cartilages), teeth, most of the vertebral column, first dorsal and caudal fins, phosphatized muscle remains and most of the body outline (figure 2c; electronic supplementary material, figure S6). MMSP CPC 3068, P. decurrens, almost complete skeleton (approx. 2030 mm TL) in dorsal view, showing neurocranial remains, scleral capsule, jaws, dentition, pectoral and caudal fins, and vertebral column (figure 2d; electronic supplementary material, figure S7).

Figure 1.

Fully articulated Ptychodus specimens from the early Late Cretaceous (Turonian) of Vallecillo showing the general morphology and anatomy of the genus. (a,b) Photograph (a) and interpretative line drawing (b) of MMSP CPC 3063, adult specimen of Ptychodus sp. (c,d) Photograph (c) and interpretative line drawing (d) of MMSP CPC 3064, juvenile specimen of Ptychodus sp. All to the same scale.

Figure 2.

Additional, partially disarticulated Ptychodus specimens from the early Late Cretaceous (Turonian) of Vallecillo. (a) MUDE CPC 3065, Ptychodus sp., incomplete specimen mostly preserving the head. (b) MMSP CPC 3066, Ptychodus sp., incomplete specimen missing the tail. (c) MMSP CPC 3067, Ptychodus sp., nearly complete specimen. (d) MMSP CPC 3068, Ptychodus decurrens, nearly complete specimen. All to the same scale. ba, branchial arches; df, dorsal fin; hr, hypochordal rays; lcf, lower lobe of caudal fin; Mc, Meckel's cartilage; my, myomeres; nc, neurocranium; oh, occipital hemicentrum; pq, palatoquadrate; sca, scleral capsule; sco, scapulocoracoid; te, teeth; ucf, upper lobe of caudal fin; vc, vertebral column.

(b) . Locality and horizon

Vallecillo Lagerstätte (26°39.32′N, 100°00.82′W), Nuevo León, Mexico, lower Turonian (Pseudaspidoceras flexuosum Zone) platy limestone of the Vallecillo Member, Agua Nueva Formation, Upper Cretaceous.

(c) . Amended diagnosis of genus

Medium-sized to gigantic fusiform-bodied sharks with large and long head. Presence of two dorsal fins and an anal fin. Occipital region of the neurocranium with a prominent nuchal crest; occipital condyles extending posteriorly and surrounding at least two cervical vertebral centra. Scleral capsules with tesserae densely mineralized and organized. Palatoquadrate presenting a large otic process on the quadrate portion along with a large process articulating with the Meckel's cartilage. Meckel's cartilage presenting a well-developed facet with surface for articulation with the palatoquadrate process. Posterior part of the Meckel's cartilage with a slender, sigmoidal extension posterior to the articulation facet. Meckel's cartilage becoming progressively wider towards its posterior portion. Palatoquadrate–Meckel's cartilage articulation well posterior to the occiput. Pectoral fins large and semifalcate with narrowly rounded tips. Pectoral fins plesodic with long distal radial segments. Three pectoral basals, with metapterygial axis present. Pectoral girdle with a well-developed, dorsally directed scapular process. Pelvic fins small. First dorsal fin is rounded, with high semiplesodic fin skeleton, and significantly larger than the second dorsal fin. First dorsal fin origin is located slightly posterior to the pectoral fins origin, and second dorsal fin origin is located slightly anterior to anal fin origin. Segmented dorsal basals; no basal plates and spines. Anal fin small (similar in size to the second dorsal fin) and lacking any evidence of basal cartilages. Caudal fin lunate or semilunate with high heterocercal angle (up to 45°) (lower angle in juveniles). Hypochordal rays are well developed and directed ventrally (high hypochordal ray angle, lower in juveniles). Vertebral centra is strongly calcified and exhibiting concentric rings and numerous parallel lamellae, which run radially from the centre to the external margin. Dentition is composed of molariform teeth arranged in numerous (up to 23) anteroposteriorly directed files and forming convex dental plates. Dental plates are semi-elliptical in shape and narrow anteriorly. Occlusal crown surface showing transverse or radial ridges, granulations, wrinkles, and a possible single cusp. Dentition shows different degrees of heterodonty. Largest teeth of the dentition from the lower symphysial (medial) file. Lateral teeth gradually shrinking and losing bilateral symmetry across each dental plate mesiodistally. Anaulacorhize root is massive and always bilobate (i.e. basal face slightly concave in labial view) except in upper symphysial teeth.

(d) . General comparative description

The head is very large and long (approx. 34% of TL and 1.6 times the distance between pectoral and pelvic fin bases), with a subterminal mouth extending posteriorly behind the orbits (figure 1). A similar elongated head is known in the megamouth shark (Megachasma) [53,68]. In all Ptychodus specimens available, the neurocranium and rostral cartilages are crushed, and anatomical structures are not easily discernible. An occipital crest is present. The eyeballs were encapsulated by rigid scleral capsules showing an external surface covered by tessellated calcified cartilage (figure 3a). The jaws are well developed, with long palatoquadrates and Meckel's cartilages articulating with each other well posterior to the occiput (reaching the level of the tenth vertebra), like in most lamniforms [69,70] (figure 1). The Meckel's cartilage is a massive and deep element, with a markedly convex ventral border. The toothed portion of the jaws is restricted to about the anterior half of the palatoquadrates and Meckel's cartilages (figures 1 and 3b). The tooth morphology, characterized by a massive crown with several transverse ridges, is typical of the genus [5] and confirms the assignment of the specimens studied (figure 3c; electronic supplementary material, figure S9). Elements of the hyoid arch (hyomandibular and ceratohyal) cannot be identified with certainty. The branchial arches are well separated from each other, and some of their elements (epibranchials and ceratobranchials) are elongated, suggesting large gill openings like in many lamniforms [63].

Figure 3.

Anatomical details of Ptychodus. (a) Scleral capsule showing tesserae, specimen MUDE CPC 3065. (b) Portion of articulated dentition, specimen MMSP CPC 3063. (c) Close-up on two teeth of the lower dentition (box in (b)), specimen MMSP CPC 3063. (d) Precaudal vertebral centrum showing parallel lamellae (white arrow), specimen MMSP CPC 3067. (e) precaudal vertebral centra and muscle remains (well-preserved myomeres plus scattered isolated myofibres), specimen MMSP CPC 3067. (f) Close-up on muscle tissues (box in (e)) showing myospeta (white arrows) and myomeres composed of myofibres (black arrows), specimen MMSP CPC 3067. (g) First dorsal fin, specimen MMSP CPC 3063. (h) Pectoral fin, specimen MMSP CPC 3063. (i) Tail portion showing second dorsal fin (white arrow indicating its origin), anal fin (black arrow indicating its origin) and proximal caudal fin skeleton, specimen MMSP CPC 3063.

The total vertebral count is approximately 160, with precaudal vertebral count ranging from 89 to 92. The vertebral centra are circular and short, with a length/diameter ratio ranging from 0.52 (anterior precaudal) to 0.39 (posterior precaudal). This is similar to the range observed in other Cretaceous lamniform taxa [71]. The vertebral column is thick for its length, i.e. the maximum centrum diameter is 2.5% of the precaudal vertebral column length (as in Lamna [72]). They are strongly calcified and show concentric rings and numerous bands running radially from the centre to the external margin [1,8,73] (figure 3d).

The mesopterygium, which is subtriangular in shape, is the largest element of the three basal cartilages. The metapterygium is more elongated and extends posteriorly with a series of segments (metapterygial axis). The pectoral fins are well-developed, straight and relatively narrow-tipped. There are 16 longitudinal series of pectoral radials. The radials seem to be composed of two segments. Some distal radials bifurcate distally and reach the end of the pectoral fin (plesodic condition). The pelvic fins are markedly smaller than the pectoral fins.

There are two dorsal fins devoid of spines and basal plates. The first dorsal fin is relatively low (i.e. slightly longer than high) and apically rounded, and its origin is located slightly posterior to the origin of the pectoral fins. It is semiplesodic (sensu [53,74]) and shows segmented basals. There are at least 20 radials, some of them bifurcating distally. The second dorsal fin is much smaller, and its origin is located slightly anterior to the anal fin origin. The first dorsal fin shape and skeleton as well as the position and respective sizes of both dorsal fins resemble those observed in modern lamnid sharks (e.g. Lamna [63,69]). The anal fin is apically angular, slightly higher than long, and similar in size to the second dorsal fin. Its origin is located slightly posterior to the second dorsal fin origin.

The caudal fin shows a lunate or semilunate shape (heterocercal angle up to approx. 45°), with a moderately elongated dorsal lobe and a shorter subvertical ventral lobe (high hypocercal angle). The longest hypochordal rays, which are located in the anterior portion of the caudal fin, are robust, laterally flattened and ventrally directed, thus forming a high hypochordal ray angle (128°) similar to that observed in Lamna (up to 122°) and Cretoxyrhina (133°) [75]. Specimen REG 2544 P.F. 839 indicates that juveniles did not have a lunate caudal fin, with lower heterocercal and hypochordal ray angles (approx. 30° and approx. 90°, respectively) and a less vertical ventral lobe (lower hypocercal angle). This ontogenetic difference is known in some modern lamnid and cetorhinid lamniforms [76,77]. The caudal fin of Ptychodus corresponds in its proportions to the type 4 (type 2 in juveniles) defined for lamniform sharks [75]. Although not preserved in any specimen, a terminal lobe may have been present, as in all living lamniforms [63] and in Cretaceous lamniform specimens with well-preserved caudal fins [78].

The squamation consists of minute, densely arranged ridged dermal denticles (= placoid scales). Best preserved skin portions are located on the dorsal, anal and pectoral fins of specimen MMSP CPC 3063, where placoid scales are leaf-shaped (approx. 180 µm long and approx. 140 µm wide), with a slightly swollen apical crown surface showing five longitudinal ridges bounded by shallow grooves (inter-ridge distance = 40 µm) (electronic supplementary material, figure S8). Their morphology is consistent with that of some placoid scales previously described in Ptychodus rugosus [12,34] and similar in size and morphology to that described in the extant lamnid Isurus oxyrinchus [79].

Some portions of the lateral trunk musculature (i.e. myomeres and myospeta) are preserved in several specimens. Muscle fibres, composing each myomere, can be observed in situ or as scattered isolated elements (likely a result of the decay process) (figures 1 and 3e,f). In specimen MMSP CPC 3063, a brownish area located inside the abdominal cavity might represent remnants of the iron-rich liver tissues (figure 1).

4. Results and discussion

(a) . Phylogenetic relationships

The parsimony analysis recovered 6349 MPTs of 691 steps, a consistency index (CI) of 0.47 and a retention index (RI) of 1. The phylogenetic analysis conducted in the present study provides new insights into the long-standing debate of the systematic affiliation of Ptychodus, placing this taxon within Neoselachii (crown elasmobranchs), as a member of Lamniformes within Galeomorphii. In the following section, only the characters observed in the new Ptychodus specimens or accounted for the genus in the literature are considered (see electronic supplementary material and [58] for full synapomorphy list and character reconstructions).

The clade Neoselachii (crown elasmobranchs) (figure 4; Clade 119) is well supported in the present study with a jackknife value (JV) of 99% and a Bremer value (BV) of 10. Ptychodus affiliation within Neoselachii is supported by the following features (in specimens or in literature): the lack of an internasal plate separating the palatoquadrates (character 4:0), the reduced number of cartilages connecting the basipterygium and the clasper cartilage (character 149:1), the presence of an occipital hemicentrum (character 154:1), the presence of calcified vertebral centra in the different regions on the body (characters 155:1 and 158:1), and the presence of multilayered enameloid on the teeth [33,80] (character 209:1).

Figure 4.

Cladogram (strict consensus tree estimated from the 6349 most parsimonious trees) showing the placement of Ptychodus within Elasmobranchii. Numbers in nodes follow the arrangement ‘node number: jackknife support/Bremer support’. Clades of interest for the relations of Ptychodus are colour coded.

The clade Selachimorpha (figure 4; Clade 118) has relatively low support in the present analysis (JV of 55% and BV of 1). The placement of Ptychodus within Selachimorpha is supported by a suite of characters that include an enlarged and broad mesopterygium (character 134:2), the presence of a propterygium, which is reduced, not elongated anteriorly and containing radials (characters 135:1, 136:3 and 137:0).

The clade Galeomorphii (figure 4; Clade 131) presents high support (JV: 73% and BV: 3). The placement of Ptychodus within Galemorphii is based on the reduced or lack of supraneurals (character 169:0). Within Galeomorphii, the clade [Orectolobiformes + (Carcharhiniformes + Lamniformes)] (figure 4; Clade 135) has relatively low support of 59% (JV) and a BV of 2. The affiliation of Ptychodus to this clade is supported by the presence of secondary calcification in the vertebral centra and the presence of radii radiating from the notochordal sheath (characters 166:1 and 167:0), the lack of dorsal fin basal cartilages (basal plates) (segmented sensu [69]) (character 176:2) and the lack of dorsal fin spines (character 202:0). These features clearly separate Ptychodus from heterodontiforms, another group of durophagous galeomorph sharks.

The clade Lamniformes (figure 4; Clade 139) has high support (JV: 88% and BV: 4). The assignment of Ptychodus to Clade 139 is supported by the presence of an occipital crest (character 30:2), the presence of a large process on the otic region (quadrate portion) of the palatoquadrate (character 84:1), with a deep groove for the abductor mandibularis (character 83:1). Within Lamniformes, Ptychodus is included in a polytomic group (figure 4; Clade 140). This group has low support (JV: 51% and BV: 1) and is based on the presence of a plesodic dorsal fin (character 175:1) (some trees also recovered the presence of plesodic pectoral fins (character 121:0) and the presence of homocercal caudal fin (character 177:1) as additional characters for this clade). It is worth mentioning that all characters supporting the lamniform affiliation do not necessarily represent synapomorphies for the lamniforms as they are also present in other taxa. For instance, a large process in the quadrate portion of the palatoquadrate also occurs in Hexanchus, Heptranchias, Notorynchus and Orthacanthus among others (character 84:1), but in these taxa this process also forms part of the postorbital articulation (see [81]), which is not present in Lamniformes. However, those taxa do not present the same combination of shared features leading to the clade Lamniformes and placing Ptychodus as a member of this group.

(b) . Ecomorphological specializations

The LDA morphospace defined by the first three LD axes shows good discrimination among ecomorphological groups (figure 5). The living species were assigned to an ecomorphotype category with high accuracy (correct classification = 90.48%; electronic supplementary material, table S6). The positions of Ptychodus with distinct maximum TL are close to that of the tachypelagic group. This is confirmed by the LDA classifier, which assigns medium-, large- and giant-sized Ptychodus species to the tachypelagic group based on the minimal Mahalanobis distance to the group mean (electronic supplementary material, table S7).

Figure 5.

Plots of Linear Discriminant Analysis based on 11 log-transformed measurements for 42 living shark species belonging to eight ecomorphotypes, with Ptychodus specimen MMSP CPC 3063 (P. sp.) (grey star) and medium-, large- and giant-sized Ptychodus sp. (with the same proportions as MMSP CPC 3063) added (white stars). (a) LD1 versus LD2. (b) LD1 versus LD3. (c) LD2 versus LD3. See electronic supplementary material, table S8 for LDA scores.

Ptychodus shares several morphological features with tachypelagic lamnids (e.g. Carcharodon, Lamna), such as a first dorsal fin placed in a markedly anterior position, just posterior to the origin of the pectoral fins, a minute second dorsal fin, and a lunate caudal fin [66,63]. Additional features present in Ptychodus also characterize tachypelagic lamnids, such as high heterocercal and hypochordal ray angles [75], a vertebral column that is thick for its length [72], and scleral capsules that are covered by noticeably discrete and well-organized tesserae [82,83]. All these features are found in living fast-swimming species and are therefore consistent with the assignment of Ptychodus to the tachypelagic ecomorphotype.

Ptychodus, like all other lamniforms, exhibits a morphology and body proportions clearly different from those characterizing extant durophagous sharks, which are all demersal forms (e.g. Heterodontus and Nebrius in the probenthic and littoral ecomorphotype categories, respectively) [66]. However, the massive dentitions of Ptychodus, composed of numerous ornamented molariform teeth, unambiguously indicate a durophagous diet (see [8,9,14,32]). Another aspect of the anatomy of Ptychodus that clearly separates it from all other extinct and extant durophagous sharks is its gigantic size (e.g. [12,13,73]). Shimada et al. [12,13] estimated the size of various species of Ptychodus using the proportions between anteroposterior jaw length, symphysial tooth size and total body length (based on the assumption that jaw length is 7–8.5% of TL). For instance, Shimada et al. [13] found that P. mortoni could have reached 11.2 m TL. However, the jaw length is 18% and 21% of TL in specimens MMSP CPC 3063 and MMSP CPC 3068, respectively, indicating that the total lengths proposed by Shimada et al. [12,13] were overestimated. Here, we obtained the proportion between lower symphysial tooth length and TL from the dental and skeletal remains preserved in specimen MMSP CPC 3063. Assuming that these proportions are maintained across various species, different ontogenetic stages and between sexes, we propose revised body size estimates using the best-preserved known Ptychodus dentitions (electronic supplementary material, table S2). According to our results, the maximum TL for the genus would be 9.7 m based on an associated dentition of P. latissimus from Italy [20], with a corresponding jaw length of roughly 1.9 m. The maximum body length of roughly 2.5 m (possibly 3.5 m) so far documented for the largest living durophagous shark (Stegostoma fasciatum; see [63]) pales in comparison with the gigantic sizes reached by some uncuspidate species of Ptychodus such as P. latissimus, P. martini, P. mediterraneus and P. polygyrus (see also electronic supplementary material). Furthermore, such sizes have rarely been exceeded during the long and complex evolutionary history of sharks, with the few exceptions being restricted to apex predators and planktivorous forms (e.g. the extinct megatooth shark, Otodus megalodon, and the living whale shark, Rhincodon typus) [66]. Therefore, the lamnid-like morphology of Ptychodus combined with its massive pavement-like dentition and its large to gigantic size, make it a unique meso- to apex predator, as well as probably the largest durophagous shark that ever existed. The tachypelagic ecomorphotype revealed by the newly discovered material from Mexico challenges the widely held view that the durophagous genus Ptychodus was a group of bottom-dwelling sharks (e.g. [12,13]) feeding mainly on shelled benthic invertebrates such as inoceramid bivalves (e.g. [15,16,21]). New evidence indicates that Ptychodus was an open-water, fast-swimming predator that preyed on well-armoured pelagic organisms such as large ammonites and sea turtles (figure 6), thus confirming the more active nektonic lifestyle previously suggested based on morphological features of vertebral centra and placoid scales [33,34]. At Vallecillo, the presence of cracked shells of the spinose ammonite Pseudaspidoceras flexuosum may have resulted from predation Ptychodus, as previously hypothesized [17].

Figure 6.

Life reconstruction of the tachypelagic lamniform shark Ptychodus in the early Turonian open marine environment of Vallecillo. Two individuals are shown preying on nektonic shelled organisms (i.e. an ammonite and a sea turtle) in a trophic hotspot. Artwork by Frederik Spindler.

Lamniformes show a wide range of diets, especially when fossil taxa are taken into account [84]. While extant lamniform sharks are superpredators (Carcharodon), fish/cephalopod-eating predators (e.g. Alopias, Carcharias, Isurus, Lamna) or filter-feeders (Cetorhinus, Megachasma) [63], the systematic position of Ptychodus indicates that durophagy evolved within a Cretaceous lineage of lamniforms, making this order one of the most diverse in terms of feeding strategies. Hard-prey specialists were so far unknown among extant and extinct lamniform sharks, with the exception of Ptychocorax, a poorly known Late Cretaceous (Coniacian–Campanian) anacoracid genus characterized by a unique dentition consisting of anterior cutting teeth and lateroposterior grinding teeth [5]. Interestingly, this short-lived experimentation with durophagous habits, somewhat similar to that observed in ptychodontids, emphasizes the capacity for rapid acquisition of trophic specializations in lamniform sharks. Our study confirms that Cretaceous lamniforms exhibited particularly diverse ecomorphologies and diets, with ptychodontids adding to other highly specialized groups of the order such as anacoracids [5], johnlongines [85], haimirichiids [86] and aquilolamnids [87]. Our findings also show that the development of durophagous specializations within elasmobranchs occurred several times independently in most major extant groups (orders) and distinct ecomorphotype categories. Furthermore, the gigantic sizes reached by the last (Campanian) representatives of Ptychodus suggest that the availability of space and nektonic shelled prey items may have been a more important factor than previously assumed. During the Campanian, ptychodontid sharks would have been in direct competition with the members of mosasaur clades Globidensini and Prognathodontini (Squamata: Mosasauridae), two emerging groups of pelagic predators with powerful crushing dentitions and therefore probably targeting the same nektonic shelled prey items [88].

Ethics

All specimens examined for this study are part of the Colección Paleontológica de Coahuila (CPC) and are permanently housed in two Mexican public museums: the Museo La Milarca, San Pedro Garza García, Nuevo León (MMSP) and the Museo del Desierto, Saltillo, Coahuila (MUDE). As indicated above, the collection numbers of the six specimens are: MMSP CPC 3063; MMSP CPC 3064; MUDE CPC 3065; MMSP CPC 3066; MMSP CPC 3067; MMSP CPC 3068.

This work did not require approval from a human subject of animal welfare committee.

Data accessibility

All the data relevant to this study can be found in the electronic supplementary material [89] and downloaded from the Dryad Digital Repository: https://doi.org/10.5061/dryad.12jm63z5n [58].

Declaration of AI use

We have not used AI-assisted technologies in creating this article.

Authors' contributions

R.V.: conceptualization, data curation, formal analysis, investigation, methodology, writing—original draft, writing—review and editing; E.V.-S.: data curation, formal analysis, investigation, methodology, writing—original draft, writing—review and editing; M.A.: data curation, formal analysis, investigation, methodology, writing—original draft, writing—review and editing; J.K.: funding acquisition, investigation, writing—review and editing; E.F.: investigation, writing—review and editing; M.A.G.G.: investigation, writing—review and editing; J.M.P.G.: investigation, writing—review and editing; C.I.: investigation, writing—review and editing; E.S.S.: investigation, writing—review and editing; W.S.: conceptualization, funding acquisition, investigation, writing—review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Conflict of interest declaration

We declare we have no competing interests.

Funding

This research was funded in part by Géosciences Rennes, UMR CNRS 6118 to R.V. and by the Austrian Science Fund (FWF) [P33820] to J.K.