The Palaeobiology of the False Mako Shark, Parotodus benedenii (Le Hon, 1871): A View from the Pliocene Mediterranean Sea

Abstract

The extinct “false mako” shark, Parotodus benedenii (Lamniformes: Otodontidae), is essentially known from large, robust teeth that are widespread but overall rare in Oligocene to Pliocene deposits worldwide. More than 150 years after its description, this species still represents a palaeontological conundrum, as very little is known about its body aspect and palaeoecology. Here, we describe new specimens of P. benedenii from the Pliocene of Tuscany, central Italy. These new finds comprise some of the geologically youngest finds of P. benedenii worldwide, witnessing to the survival of false makos until the Late Pliocene at least, which in turn suggests that P. benedenii may have been the latest surviving member of the family Otodontidae. Building upon a thorough literature review, we provide an updated synthesis of the palaeobiology of P. benedenii. In light of the morphological evidence, and considering previously published suggestions, P. benedenii may be reconstructed as a large-sized, carnivorous shark that dwelt in pelagic settings and fed primarily on large, soft prey and scavenging items. Thus, some ecological partitioning did likely exist between P. benedenii and other elasmobranch apex predators of the Neogene mid-latitude seas (including, in Pliocene times, the extant species Carcharodon carcharias, Carcharhinus leucas and Galeocerdo cuvier).

1. Introduction

Teeth assigned to the extinct lamniform genus Parotodus are geographically widespread but uncommon in lower Eocene to Pliocene marine deposits [1]. These massive dental specimens are characterised by crowns with smooth cutting edges and a broad base, as well as by roots that bear a strongly developed lingual protuberance and a U-shaped basal edge [2]. Owing to their rarity and highly atypical shape, the remains of Parotodus have risen to almost mythical status among fossil collectors [3].

Ranging chronostratigraphically between the Oligocene (Rupelian) and the Pliocene, Parotodus benedenii is the geologically youngest representative of Parotodus [1,4]. Originally described as one of the many nominal species of Agassiz’s genus Oxyrhina [5], the benedenii morphology has long been considered to represent a close relative of the extant mako sharks in the genus Isurus [6,7,8]. Eventually, Oxyrhina benedenii came to be chosen as the type species of the then-new genus Parotodus by Cappetta [9], hence its vernacular name, “false mako” shark [3,10,11]. Parotodus benedenii and its congeners are mostly regarded as phylogenetically close to the extinct mega-toothed sharks (Otodus and kin), and as such, Parotodus is often referred, more or less confidently, to the family Otodontidae [12]. However, alternative attributions to Alopiidae, Cardabiodontidae and Lamnidae have also been proposed [13,14,15], and some works list Parotodus as incertae sedis [16].

Teeth of P. benedenii have been reported from world regions as disparate as Europe (Belgium, Germany, Hungary, Italy, Malta, the Netherlands, Portugal, Slovakia and Switzerland), Africa (Angola and South Africa), Macaronesia (the Azores and the Canary Islands), North America (USA, along both the eastern and western coasts of the country, and Mexico), South America (Ecuador and Peru), Indonesia (Sumatra) and the western Pacific (South Korea, Japan, New Caledonia; Australia and New Zealand) [3,4,17,18,19,20,21], as well as from the floor of the Indian and Pacific oceans, where this otherwise uncommon taxon appears to be surprisingly abundant [22,23]. As regards the peri-Mediterranean area, finds of P. benedenii come from the Miocene of Malta [24], southern Spain [25] and southern Italy [6,26], as well as from the Pliocene of the Balearic Islands [17] and many Italian localities [27]. In particular, the Pliocene marine deposits of Tuscany (central Italy) have yielded teeth of P. benedenii for a very long time. For instance, the celebrated 19th century palaeoichthyologist Roberto Lawley (b. 1818–d. 1881) [28] described and figured false mako teeth from the historical localities of Orciano Pisano, Siena and Volterra under five different species-level names (namely, Otodus sulcatus, Oxyrhina quadrans, Oxyrhina crassa, Oxyrhina gibbosissima and Oxyrhina Forestii) [29] (Figure 1).

More than 150 years after its description, Parotodus benedenii still represents a palaeontological conundrum, as very little is known about its body aspect and palaeoecology. Herein, we report on the discovery of new specimens of P. benedenii from Pliocene deposits of the Valdelsa Basin of Tuscany. We also provide an updated synthesis of the palaeobiology of P. benedenii based on a thorough literature review and first-hand observations.

2. Stratigraphic Framework

The Valdelsa Basin is a 25 × 60 km, NW–SE trending extensional basin of central-western Tuscany. Its sedimentary infill accounts for some 1000 m of continental and marine deposits that range chronostratigraphically from the Upper Miocene to the Lower Pleistocene [32]. A detailed sequence stratigraphic framework exists for the Valdelsa Basin, which allows for dividing its sedimentary infill into seven different synthems, namely, S1–S7 from older to younger [32].

Abundant remains of both marine and nonmarine vertebrates have been collected from several localities of the Valdelsa Basin [33,34,35,36,37,38,39,40,41,42,43,44,45,46,47]. In particular, the specimens discussed herein have been collected by one of us (SC) at two different Pliocene outcrops.

The first such outcrop consists of an abandoned quarry located in the Castelfiorentino municipality (indicative geographic coordinates: 43°35′57″ N, 10°58′51″ E) (Figure 2). Here, a 30 m thick mudstone succession is exposed, which belongs to the upper part of the upper Zanclean to lower Piacenzian S3 synthem and represents deposition during the normal-polarity Gauss chron [40]. These strata have been interpreted as representing a lower Piacenzian highstand [40].

Another tooth of P. benedenii was collected loose from the ground at a cultivated field in the Montespertoli municipality (indicative geographic coordinates: 43°37′01″ N, 11°01′12″ E) (Figure 2). According to the schematic geological map provided by Benvenuti et al. ([32]: figure 1), both the S3 synthem and the mid-Piacenzian S5 synthem occur in this area. Thus, the P. benedenii tooth from Montespertoli is either roughly coeval or slightly geologically younger than the material from Castelfiorentino.

3. Materials and Methods

3.1. Repository

The specimens discussed herein consist of two teeth that are stored in the Museo Geopaleontologico Scienze della Terra—Gruppo AVIS Mineralogia e Paleontologia Scandicci (=GAMPS; Badia a Settimo, Scandicci, Florence Province) with accession numbers GAMPS-00876a and GAMPS-00876b, respectively.

3.2. Specimen Documentation

Photographs of the studied material were taken with a Nikon D850 camera equipped with a Nikon Micro Nikkor AF-S 60 mm f/2.8 G ED macro lens.

4. Systematics

Otodontidae Glikman, 1964 [48]

Parotodus Cappetta, 1980 [9]

Parotodus benedenii (Le Hon, 1871) [5]

(Figure 3)

Synonymy: See Kent ([4]: 96).

Nomenclatural caveat: Le Hon [5] described Oxyrhina Benedenii based on a tooth from deposits of the alleged Pliocene age of the Antwerp area ([3]; but see also [49] for a different chronostratigraphic assignment of this and other finds by Le Hon). As the species name was clearly meant to honour the Belgian zoologist and palaeontologist van Pierre-Joseph Van Beneden [3], a rigorous application of the genitive case would have led to obtaining “[van]benedeni”, rather than “[van]benedenii”, as the correct epithet. It is likely for this reason that several subsequent works have considered either Isurus benedeni or Parotodus benedeni as the correct binomial name for this species [6,8,17,50]. One of the authors of the present paper (AC) has also taken this position in some earlier papers of his [51]. However, Le Hon’s [5] seemingly erroneous Latinisation must be treated under the ICZN [52] Code’s Article 32.5.1, which means that it cannot be considered as an inadvertent error, and as such cannot be corrected in a later contribution (see also [53,54]). That said, it is also possible that Le Hon [5] derived the epithet “benedenii” from some Latinised version of Van Beneden’s surname such as “Benedenius”, which would make this species name to conform perfectly to the Code’s Article 31.1.1. Circumstantial support for this interpretation may come from Le Hon’s [5] concomitant description of Anatodus Agassizii, whose species name was clearly meant to honour the French polymath Louis Agassiz, the latter being sometimes referred to as “Agassizius” in earlier scientific works [55].

Referred material and occurrence: GAMPS-00876a, one partial tooth from Upper Pliocene deposits cropping out at an abandoned quarry in the vicinity of Castelfiorentino, and GAMPS-00876b, one essentially complete tooth from ?Upper Pliocene deposits cropping out at a cultivated field in the vicinity of Montespertoli (Florence Province, Tuscany, Italy).

Description and taxonomic identification: GAMPS-00876a (Figure 3a–c) is an incomplete tooth whose crown was partly reconstructed with grey plasticine. Its maximum height, including the reconstructed crown part, is 55.5 mm. What is preserved of the crown is robust and greatly thickened labiolingually. The cutting edges are smooth. The lingual crown surface is strongly convex and smooth throughout, and features a broad neck at its base. The labial crown surface is concave in its median part above the crown–root junction, being gently convex elsewhere. In the same depressed area, longitudinal enameloid folds are present. The root is very thick, U-shaped, with long, arched root lobes. The mesial root lobe is bluntly pointed, whereas the distal root lobe is incompletely preserved. The lingual protuberance is conspicuous and shaped as a dome-like torus. Here, the root surface is damaged, and no nutrient foramina could be observed.

GAMPS-00876b (Figure 3d–f) is a complete, 60 mm high tooth. In labial/lingual view, the 44 mm high crown is broadly triangular, its tip being only gently bent distally. It is provided with smooth, complete cutting edges as well as with long shoulders that line the proximal portions of both root lobes and display no cusplets. As for GAMPS-00876a, the crown of GAMPS-00876b is robust and greatly thickened labiolingually; in profile view, it is distinctly curved labially. The lingual crown surface is strongly convex and smooth throughout, and features a broad neck at its base. The labial crown surface is strongly concave in its median part above the crown–root junction, being gently convex elsewhere. Longitudinal enameloid folds mark the basal portion of the labial crown surface, being particularly long and salient in the aforementioned depressed area. The labial crown surface distinctly overhangs the U-shaped root, which is very thick, even more so than in GAMPS-00876a. The root lobes are long and arched, and asymmetrically developed. The mesial root lobe is slender and bluntly pointed, whereas the distal root lobe is shorter and stouter. The lingual protuberance is extremely massive and shaped as a bulging torus. No nutrient foramina are clearly observable in this region of the lingual root surface.

Both GAMPS-00876a and GAMPS-00876b are referred to Parotodus benedenii because they are readily distinguished from other lamniform sharks by the following combination of characteristics: large size, crown and root robust and labiolingually thickened, absence of serrated cutting edges, absence of lateral cusplets, presence of a broad neck, basal edge of the root U-shaped, and development of a conspicuous lingual protuberance of the root [1,2,3,15,27,56].

Given the observation of a crown apex that is only slightly bent distally, a very prominent torus, and a mesial root lobe that is longer than the distal root lobe, GAMPS-00876b can be identified as a right lower anterior tooth [15,56]. The incomplete nature of GAMPS-00876a prevents from drawing definitive conclusions on its position in the dentition.

GAMPS-00876b is larger than many other Italian Pliocene false mako teeth and matches the figure reported by Cappetta [1] for the largest dental specimens of P. benedenii (though larger teeth do exist; [57]). Therefore, it is here interpreted as originating from a remarkably large-sized adult individual of P. benedenii.

Stratigraphic remarks: Marsili [27,58] regarded Parotodus benedenii as occurring in both the Lower and Upper Pliocene of the Mediterranean region. Conversely, Cappetta [1], Kent [4] and Everaert [59] listed this extinct lamniform species as making its last global appearance in Early Pliocene times. Our discovery of GAMPS-00876a in lower Upper Pliocene deposits confirms that the chronostratigraphic range of P. benedenii extends into the Piacenzian. Other Upper Pliocene records of P. benedenii appear to exist elsewhere, e.g., in Japan [2].

If the otodontid affinities of the false mako are accepted, then the extinction of P. benedenii not earlier than the Late Pliocene could also mean that this species represents the latest surviving member of the family Otodontidae. In fact, the extinction of Carcharocles megalodon (which at present is often regarded as a member of the genus Otodus) is now believed to have occurred around the Zanclean–Piacenzian transition ([60]; but see also [61] for an alternative extinction age of about 2.6 Ma). As for the Mediterranean region in particular, the disappearance of C. megalodon appears to have occurred during the Zanclean [27].

5. The Palaeobiology of Parotodus benedenii: An Updated Review

5.1. Body Size

Information about Parotodus benedenii is essentially limited to its dental remains, though some dermal denticles have also been mentioned in the literature [62]. Such a paucity of fossil materials leaves tooth sets as the sole source of data for reconstructing the body size of this impressive extinct lamniform species.

Kent and Powell [56] described an associated tooth set of P. benedenii from the Lower Pliocene of the Yorktown Formation in the Lee Creek Mine, Aurora, North Carolina, USA. Consisting of 114 teeth, the largest of which is slightly shorter than 60 mm (viz the height of GAMPS-00876b), this tooth set allowed Kent and Powell [56] to reconstruct the dentition of P. benedenii with 14 upper files (including a reduced intermediate) and 13 lower files. Emendations to this scheme focusing on the identification of symphyseal and intermediate teeth have been proposed by Purdy et al. [15], Ward and Bonavia [24] and Kent [4]. The same North Carolinian tooth set was used by Kent [57] to extrapolate a total body length of 7.6 m based on the reconstructed upper jaw perimeter. Considering the largest size values of isolated teeth of P. benedenii, some of which reach 72 mm in height, Kent [57] estimated that this extinct shark species may have grown up to 20% longer, that is, about 9.2 m total body length. Even if false makos did not exceed the more conservative 7.6 m total length estimate, this figure would make the largest individuals of P. benedenii much larger than any modern or fossil specimen of white shark (Carcharodon carcharias) for which a total body length has been reliably measured/estimated (up to ca. 7 m or slightly more; [63,64]).

Interestingly, P. benedenii may have reached its maximum size values during the Pliocene [4]. Thus, for some time, C. carcharias and P. benedenii persisted side-by-side as two of the largest macrophagous sharks of at least some quarters of the global ocean, including the Mediterranean Sea, though the latter—and larger—taxon appears to have been consistently rarer than the former.

5.2. Body Shape

Inferring the body shape of an extinct animal whose taxonomically informative remains are essentially limited to overall rare fossil teeth may look as a wild-goose chase. Nonetheless, some insightful guesses on the body aspect of false makos were provided by Kent [57] based on Otodontidae and Lamnidae being regarded as the most derived lineages of Lamniformes as well as being sister groups to each other. Parotodus benedenii was thus reconstructed as characterized by a stiff and fusiform body, with a restricted jaw protrusion, long pectoral fins, an elevated first dorsal fin, reduced second dorsal and anal fins with pivoting bases, a slightly depressed caudal peduncle, caudal keels and a lunate tail, as well as by gigantothermy. Furthermore, considering the alleged open-sea palaeoenvironmental preferences of P. benedenii (see Section 5.3 below), Kent [57] hypothesised that false makos may have displayed long, wing-like pectoral fins like those of extant pelagic sharks such as Alopias superciliosus, Isurus paucus, Carcharhinus longimanus and Prionace glauca.

Kent’s [57] painstaking reconstruction of the body shape of P. benedenii is partly dependent on what is currently known as the “Lamnoidea hypothesis”, that is, the existence of a sister group relationship between otodontids and lamnids [65]. Such a hypothesis, however, is hotly debated [66,67], which suggests that alternative body shapes should also be considered. Among the aspects of Kent’s [57] reconstruction that may merit some rethinking is thermoregulation, whose role in P. benedenii could be reappraised in light of the recent discovery that regionally endothermic traits are commoner than hitherto known across Lamniformes ([68]; but see also [69] for an assessment of P. benedenii as an ectothermic species).

5.3. Habitat Preferences

That the false mako was a pelagic shark with a predilection for open-sea settings is widely recognised in the literature. Based on the common occurrence of teeth of Parotodus benedenii in nodules of the Central Pacific seafloor [22,23,70] hypothesised an offshore lifestyle for this extinct mackerel shark species. Cappetta [1] pointed out that the members of the genus Parotodus were essentially pelagic forms whose presence in neritic fossil-bearing localities should be regarded as exceptional. Ward et al. [2] also noted that teeth of Parotodus spp. occur most typically in mid- and outer shelf settings. Canevet [3] and Everaert [59] followed on the same lines, supporting a preference for pelagic, farshore habitats for P. benedenii.

With regard to the new Tuscan Pliocene records, the one with the best stratigraphic control (i.e., GAMPS-00876a) also originates from open shelf deposits [40]. We may be content to suggest that P. benedenii was an open-sea shark that frequented the marginal-marine waters much less commonly than the eurytrophic littoral forms (sensu [71]) such as the bull shark (Carcharhinus leucas) and tiger shark (Galeocerdo cuvier), which were also present in the Mediterranean Basin in Pliocene times [27]. In all likelihood, P. benedenii was also less coastal than C. carcharias, which nonetheless has recently been demonstrated to be more pelagic than was previously thought [72]. All things considered, significant differences in habitat preferences suggest that some degree of ecological partitioning existed between P. benedenii and other elasmobranch apex predators of the Pliocene mid-latitude seas, including C. carcharias, C. leucas and G. cuvier.

5.4. Trophic Ecology

In order to propose a comprehensive reconstruction of the palaeobiology of P. benedenii, its feeding habits should also be discussed. Given the highly unusual shape of its teeth, as well as the little that is positively known about its anatomy beyond the dentition, the trophic ecology of Parotodus benedenii remains quite a conundrum, though most authors agree that P. benedenii was a formidable carnivore [2,27,56]. Kent and Powell [56] astutely noted that the “P. benedeni [sic] teeth are adapted for piercing and rending fibrous, compliant tissues [...] such as the skin and muscles of vertebrate prey [...]. Functionally, the teeth and dentition of P. benedeni more closely resemble those of the extinct mosasaurs and the extant killer whales [Orcinus orca], than those of other sharks. With a piercing-lacerating dentition of large, robust teeth attached to equally robust jaws, P. benedeni could have produced gaping wounds and massive soft tissue trauma in their prey”. Compagno (in [15]) suggested that P. benedenii “fed by grabbing prey, such as seabirds, porpoises, and seals, with its teeth and swallowing it whole”. Ward et al. [2] further observed that all the nominal species of Parotodus display relatively little damage to the apex of their tooth crowns, particularly compression fractures caused by impacts on bone, which in turn may suggest that this predator used to eat relatively soft-bodied prey such as sharks. All things considered, the sturdy, smooth-edged teeth of P. benedenii appear to be less fit than the strongly compressed, serrated teeth of, e.g., Carcharodon carcharias for slicing flesh [56], as well as for dealing with somewhat coriaceous food items such as sea turtles (especially the hard-shelled cheloniids).

In our opinion, comparisons between the dental design of the false mako and those of the living taxa of Lamniformes are of somewhat limited usefulness for the purposes of clarifying the trophic ecology of P. benedenii. Though similarities with the extant species Isurus oxyrinchus (aka the shortfin mako, a member of Lamnidae) and Alopias vulpinus (aka the common thresher shark, a member of Alopiidae) have long been highlighted [4], differences are so considerable that whether functional and dietary convergence exist between P. benedenii and the aforementioned mackerel shark species remains uncertain at best. Teeth of P. benedenii are also similar to those of some Cretaceous lamniforms such as Cardabiodon [14], whose feeding habits are similarly uncertain.

Further considerations on the trophic ecology of P. benedenii may be made by considering the alleged habitat preferences of this extinct taxon. Unlike what is known for C. carcharias, a predilection for farshore, essentially pelagic settings would have made coastal animals such as seals only rarely available as potential prey items for P. benedenii [73]. In turn, it is reasonable to hypothesise that large vertebrate carcasses drifting in the open sea would have provided the piercing-lacerating dentition of the essentially pelagic P. benedenii with relatively soft carrion to dismember and forage on, especially in the cetacean-rich Pliocene Mediterranean palaeobiotopes [64,74]. All things considered, significant differences in tooth design and dentition, which we interpret as witnessing to an only partial overlap of dietary spectra, suggest that a certain degree of trophic partitioning existed between P. benedenii and other elasmobranch apex predators of the Mediterranean Basin and other Neogene mid-latitude seas, including, in Pliocene times, the extant species C. carcharias, Carcharhinus leucas and Galeocerdo cuvier.

However well-reasoned these arguments may be, it should be noted that no taphonomic evidence exists of the trophic ecology of Parotodus benedenii. As a possible reflection of its farshore habitats, as well as of the alleged “overrepresentation” of shelfal palaeoenvironments in the Cenozoic fossil record of marine vertebrates such as whales [75], no fossil skeletons appear to exist at present preserving associated teeth or even bite marks that would compare favourably with the false mako. That said, the possibility that some of the widespread unserrated bite marks that are often assigned to commoner shark species such as Cosmopolitodus spp. [76,77,78] do rather belong to P. benedenii should also be taken into account.

6. Conclusions

We reported on the discovery of new specimens of Parotodus benedenii from Pliocene deposits of the Valdelsa Basin (Tuscany, central Italy). These new records comprise some of the geologically youngest finds of P. benedenii worldwide, witnessing to the survival of false makos until the Late Pliocene at least. Thus, for some time, the white shark and P. benedenii persisted side by side as two of the largest macrophagous sharks of at least some quarters of the global ocean, including the Mediterranean Sea.

Building upon a thorough literature review, an updated synthesis of the palaeobiology of P. benedenii was also provided herein. In light of the morphological evidence, and considering previously published suggestions, P. benedenii may be reconstructed as a large-sized (up to more than 7 m total body length), carnivorous shark that dwelt in pelagic settings and fed primarily on large, soft prey and scavenging items. Open-sea habits and a trophic spectrum that was likely poor in coriaceous prey items suggest that some ecological partitioning existed between P. benedenii and other elasmobranch apex predators of the Neogene mid-latitude seas (including, in Pliocene times, the extant species C. carcharias, Carcharhinus leucas and Galeocerdo cuvier).