Suction Feeding Adaptations of <italic>Ocepechelon</italic>
Despite the tremendous diversity in form and function of the turtle skulls [4], [18], [19], the skull of Ocepechelon bouyai is one of the most unusual. Although the lower jaw and hyoid apparatus of this species remain unknown, the diet and feeding mechanics of Ocepechelon can be inferred from the architecture of its large and highly specialized skull (see Text S1 of Supporting Information S1 and Figures 2–5) [20]. The flattened, streamlined shape of the cranium, combined with the dorsal position and orientation of the orbits and external nares, suggest that Ocepechelon was an epipelagic turtle hunting close to the sea surface, as for example crocodilians. Its marine behaviour is supported by both the sedimentological context of the type locality and the chelonioid skull anatomy. As a Dermochelyoidae, Ocepechelon much likely possessed limbs modified into flippers, allowing an active swimming ecology in open-sea. Possibly referable postcranial material found in the same Maastrichtian Level III of the Oulad Abdoun Basin further supports this anatomical deduction (see Text S1, p 11–13, in Supporting Information S1).
The most intriguing feature of Ocepechelon is its pipette-like longirostrine bony snout. The thin, tubular snout of Ocepechelon was embedded ventro-laterally in a deep and non-triturating rhamphotheca, as indicated by an area covered by nutritive foramina and short longitudinal sulci. But the absence of cutting, shearing or triturating structures in the upper jaw precludes any use for direct capture or processing of food items.
Ocepechelon has a large head, an elongated upper jaw without food triturating structures, and a mouth aperture in a plan perpendicular to the forward movement, all morphological features characteristic of ram feeding tetrapods [21]. Nevertheless, ram feeders tend to have an oral orifice with a very large cross-sectional area. The snout of Ocepechelon, ending with a relatively small rounded forward-facing-mouth aperture, is reminiscent of the rostrum and mandible of the much smaller syngnathiform fishes (seahorses, pipefishes, and allies), which represent efficient designs for suction feeding [22]–[26].
Suction feeding is frequent in aquatic vertebrates (chondrichthyans, osteichthyans, amphibians, aquatic turtles and marine mammals) [21], [25], [27]–[34]. The aspiration tube of suction feeders is variably formed by the snout, independently from the presence of teeth. It is documented in living short-snouted freshwater turtles such as Chelus and Chelydra, and among extant marine mammals, in the long-snouted sperm whale Physeter and beaked whales (Odonteceti, Ziphiidae), as well as in more or less short-snouted species such as various delphinoids and walruses. In all these groups, the buccal tunnel is at least partly made of soft tissues; examples include the mucosa issued from an external adductor muscle in the freshwater turtle Chelus, the Mundplätte (figures in [33]), or the large gums, and extensive lower lips that line the mouth opening in beaked whales (diagrams for species of Mesoplodon, figs. 2 and 3 in [24], figures (partly) and diagrams in [34], including fig. 3 for a generalized odontocete). Because the tubular rostrum of Ocepechelon is made of bone, it is therefore unique among marine tetrapods.
Ocepechelon differs significantly from other suction feeding turtles [18], in its unique cranial architecture. It particularly shares some interesting resemblances with beaked whales. Ocepechelon and most beaked whales are large animals, and, as in all other extant cetaceans and Ocepechelon, the nostrils of beaked whales are posterodorsally shifted (Figures 2, 3, 6). They also share similarities on their feeding apparatus: elongated jaws (without triturating surfaces in Ocepechelon and toothless in most extant beaked whales, except for one or two pairs of apical teeth modified in tusks in adult males) and a small gape [24]. The mouth gape of Ocepechelon can be inferred from the diameter of the tube (about 6 cm). It is worth emphasizing the disproportion between the tiny size of the mouth opening and the large size of the skull (70 cm long). The snout diameter predicts that Ocepechelon was a small-prey hunter (e.g., small fishes, cephalopods and jellyfishes). In pipefishes the snout length is inversely related to the mouth cross-section and is considered as an evolutionary advantage since it reduces the time to reach the prey [23]. In Ocepechelon, the elongated rostrum and the round and small mouth much likely increased the velocity of the water influx [22].
Suction feeding does not require strong biting and is often associated with weakly developed jaw adductor muscles, as seen in edentulous odontocetes. According to the different suction feeding processes, the different parts of the jaw adductor muscles are not equally developed, as seen with the developed mucosa in Chelus [33], [35]. Dominant muscles in Ocepechelon were attached to the pterygoids, as suggested by the conspicuous large ventral pterygoid flanges of these bones, comparable in development to those of pleurodiran Podocnemididae. In these turtles, the pars ventralis of the muscle pterygoideus (anterior part of the Musculus adductor mandibulae internus), inserted between the developed flanges, has a special function of protraction of the lower jaw, acting in synergy with the rectracting component of the external adductor muscle [35]. Situated above the hyoid apparatus, this muscle couple could also have acted in combination with the piston function of the hyoid and tongue in the swallowing process. By deduction, the same system might have worked convergently in Ocepechelon. However, the muscular bauplan is basically identical for swallowing process in turtles, such as it is figured in the sharpening feeder pleurodire Podocnemis [35] (fig. 11) (which possesses pterygoid flanges) and the crushing feeder cryptodire Chelonia [35] (fig. 10).
Moreover, in Ocepechelon, the squamosals are exceptionally developed into broad posterolateral wings, providing large surfaces for visceral muscle attachment [35], much likely for an important hyoid and tongue musculature, as in other living turtles such as the leatherback Dermochelys [35], [36] and notably the suction feeder Chelus [32], [33]. The hyoid apparatus and associated musculature are also remarkably developed in cetaceans, especially in suction feeding beaked whales (diagrams and figs. in [24], [27], [37]).
The remarkable and unique anatomy of Ocepechelon, including a unique bony pipette-like longirostrine snout, exceptionnaly large pterygoid flanges and posteriorly developed squamosal wings, suggests a feeding strategy that was later paralleled by several cetaceans, including the beaked whales [24], [25], [34]. We hypothesize that it fed, as the latter, by generating a fast, large-amplitude depression within its buccopharyngeal cavity. Given the narrow tubular shape of its upper jaw, Ocepechelon probably performed small-gape suction (with minimally opened mouth), thereby enhancing the suction force for attracting and ingesting the prey (Figures 2, 3, 6, Video S1). In general, a small and circular mouth opening generates greater negative intraoral pressure than a laterally open and larger mouth. A part of the marine mammals, excluding beaked whales, perform a circular mouth opening through shortening and widening of the rostrum and jaws [24], [33] (e.g. odontocete mandibular bluntness studied in details in Werth [34]).
In aquatic turtles, the expansion of the buccal and pharyngeal cavities plays an important role, since the highly distensible oesophagus may serve as a water reservoir and entrap prey until the closure of the mouth, before swallowing the prey and finally expelling the water, a behaviour that we propose for Ocepechelon [29]–[33], [38] (Video S1). Many living turtles, including marine forms such as Dermochelys, have keratinized buccopharyngeal papillae that allow both filtering water and entrapping prey [39]. Beaked whales also possess lingual or palatal horny papillae that may help retaining the prey against the palate [24]. Ocepechelon could have possessed mouth papillae.
Conclusion
During the Mesozoic, large marine carnivorous reptiles such as ichthyopterygians, sauropterygians, mosasaurid squamates and crocodyliformes exhibited a wide range of feeding strategies based on their tooth morphologies, from benthic crushing feeders to huge open-sea generalist predators [40]. However, despite this considerable diversity in the Mesozoic marine reptile modes of predation [40], [41], as well as a broad overlap of their tooth morphospaces with those of Cenozoic marine mammals, indicating multiple feeding behavior convergences [42], suction feeding, though being a common feeding strategy in aquatic vertebrates [34] has been extremely rarely reported among Mesozoic marine reptiles. It has been hypothesized (but without any concrete argument) for Hupesuchus, a small marine reptile from the Middle Triassic of China [43] and recently postulated for Shonisaurus [44], [45] and Shastasaurus [46], both large toothless Triassic ichthyosaurs, interpreted as suction feeders also comparable to many extant odontocetes.
The unique anatomy and ecology of Ocepechelon suggest a prey capture behavior similar to that of several extant suction feeding odontocetes. Furthermore it is the only bony pipette-feeder ever reported among tetrapods. Irrespective of its feeding strategy, Ocepechelon dramatically illustrates the anatomical and taxonomic diversification of chelonioid turtles during the Late Cretaceous (Figures 6, 7). It combines turtle morphology with a feeding device that parallels the adaptation of modern pipefishes and some living odontocetes.
With its peculiar morphology, Ocepechelon likely occupied a different ecological niche compared to other coeval marine reptiles [3], [4], [8], [16]. Its specialization further emphasizes the tremendous diversity that prevailed among the fishes and reptiles in the shallow marine environments of the Late Maastrichian Phosphates of Morocco, shortly before the K/Pg mass extinction event [47], [48].