Eurhinosaurus merits a separate discussion because of its uniquely low MPCI value. There is an anatomical reason why this taxon exhibits an anomalous value in this index. The genus is known for extreme shortening of the mandible, leading to an extensive overbite that is analogous to that seen in swordfish [6] . A large part of its upper dentition is anterior to the mandible, which starts to widen immediately posterior to the tip but is still not very wide at the point where the dentition ends. Apart from the overall shortening, the mandibular morphology is not unusual for an ichthyosaur. For example, the jaw symphysis is short, unlike in suction-feeding cetaceans that have low MPCI values. Given that the CB1 of Eurhinosaurus is slender as in other ichthyosaurs and that its hyoid corpus is unossified, it lacked the ‘equipment’ to generate suction. Therefore, it was most likely a ‘ram feeder’ as with other ichthyosaurs.

A part of the reason why suction feeding did not evolve in ichthyosaurs may be the basic skull design of the Ichthyosauria, which is a clade within the Ichthyopterygia [6] . In comparison with cetaceans, the jaw joint of this clade tends to be located much more posteriorly relative to the snout, at or behind the occiput that is often inclined to contribute to the posterior displacement of the joint as in Guanlingsaurus. Because of this posterior location, ichthyosaurs are destined to have more elongated mandibles than cetaceans even when the snout lengths are similar. Also, this design leads to posterior location of the coronoid region in ichthyosaurs, which is usually found at the level of the occipital condyle. Thus, the region is too far away from the snout to function as the gape-shortening apparatus–note that the precoronoid crest of beaked whales is located at the posterior part of the snout. This apparent constraint from the jaw-joint location is not applicable to basal Ichthyopterygia, so it may be possible to find a suction feeder among basal members of the clade in the future.

A previous study [10] mentioned the presence of dorsally convex coronoid region in Guanlingsaurus. This feature, however, is not well exposed in the specimens that they described. The newer specimen reported in [16] has a complete exposure of the mandible, where no special structure analogous to the precoronoid crest of beaked whales exists. Mandibular morphology of Guanlingsaurus is not very different from those of some deep-jawed ichthyosaurs of the Middle and Upper Triassic except its relative shortness. Also, even if a special structure existed in the region, it probably could not shorten the gape and narrow the mouth opening effectively because of its location (see below).

The ‘ram-feeding’ hypothesis for ichthyosaurs is further strengthened by two independent pieces of morphological evidence that are rooted in the mechanics of suction feeding. First, as evident from MPCI values, syringe-like suction pressure concentration that occurs between the throat and mouth opening was not very high in ichthyosaurs, unlike in suction-feeding cetaceans. The MPCI values of ichthyosaurs are similar to those of ‘ram-feeding’ marine mammals, again suggesting that ichthyosaurs were ‘ram feeders’. One exception is Eurhinosaurus that is discussed later. Second, ichthyosaurian mandibles are much more elongated than those of odontocete cetaceans on average ( Figs. 2 and 5B ). The most elongated mandibles among suction-feeding cetaceans are found in beaked whales, which are about as acute as the least elongated mandible of ichthyosaurs. Despite the unusually elongated mandibles for a suction feeder, beaked whales are able to suction feed thanks to the presence of superficial tissues around the corners of the gape, which in effect shorten the span of gape, while allowing a more rounded opening that is suitable for concentrating pressure projection [50] . This effective decrease in gape also has an osteological basis: beaked whales have the precoronoid crest of the mandible, a unique structure that enables the mandible to overlap the upper jaw far anterior to the jaw joint. There is no evidence for such soft- or hard-tissues in ichthyosaurs.

Lack of variation in the slenderness of the CB1 in ichthyosaurs is noteworthy. The ceratohyals of sharks show a broad range of slenderness depending on their prey capture ecology ( Fig. 3B ). The contrasting absence of such variation among ichthyosaurs seems to indicate that the use of the hyobranchial apparatus during feeding did not vary much among different types of ichthyosaurs, whether small or large, long- or short-snouted. We infer that the hyobranchial apparatus played a similar role during feeding across ichthyosaurian species.

The hyobranchial apparatus of Triassic and Early Jurassic ichthyosaurs strongly suggests that these marine reptiles were incapable of suction feeding. All but one species (Hauffiopteryx typicus) lacked an ossified hyoid corpus, whereas robust integration between ossified hyoid corpus and cornua has been identified as essential for amniote suction feeders as pointed out earlier. Even in H. typicus, such a robust integration is questionable ( Fig. 4D ). Also, the CB1 of ichthyosaurs, including H. typicus, is not very robust compared to suspensory hyobranchial elements of suction-feeding turtles (CB1), whales (stylohyals), and sharks (ceratohyals) ( Figs. 2 , 3 , and 5 ). Therefore, it seems reasonable to conclude that all ichthyosaurs examined were ‘ram feeders’ because they lacked hyobranchial adaptation toward suction feeding. Notably, two of the presumed suction feeders [11] have the most slender CB1 among ichthyosaurs examined; this makes them the least likely candidates for suction feeders among ichthyosaurs.

Paleoecological Implications

Suction feeders among extant air-breathing marine vertebrates have a limited range of feeding ecology. This is partly because suction is only effective over a short distance [39], which is usually less than 6 cm in the cetaceans measured so far [35], [44]. These air-breathing suction feeders almost exclusively feed on stationary or slow-moving prey and capture them with limited pursuit. For example, suction-feeding pinnipeds and sharks feed from the sea floor [57]. With the exception of Delphinapterus, which use suction feeding during shallower benthic foraging [35], ‘true’ suction feeders among cetaceans feed in the mesopelagic and bathypelagic zones [58]–[60]) to catch squid and fish [61]–[63]). Most mesopelagic and bathypelagic squid and fish are considered to be slow moving [64], with the exception of some large squids [65]–[67]. Beaked whales and sperm whales tend to swim through concentrations of these prey items in the lower DSL (Deep Scattering Layer) and benthopelagic layers during feeding dives [60], [68], although sperm whales reportedly pursue large squids from time to time [68]. If some shastasaurid ichthyosaurs were suction feeders resembling beaked whales as once suggested [10], then they would have needed concentrations of slow-moving, soft-bodied prey, most likely coleoid cephalopods, as in the modern mesopelagic/bathypelagic zones. None of the benthic feeders among suction-feeding, air-breathing marine predators is edentulous except the gray whale that uses side-suction [55], so benthic feeding is probably inappropriate for these ichthyosaurs.

Evidence for the presence of deep-water coleoid communities in the Triassic is scant, although its possibility cannot be completely excluded. The time period predates the common ancestor of extant decabrachian coleoids in the Late Jurassic or Early Cretaceous [69], [70]–this clade has extant members that are vertical migrants [69]. The oldest belemnites are known from the Carnian of Sichuan, China [71], [72], although they did not spread worldwide until the Early Jurassic [73], [74]. This clade has evidence for vertical migration reaching at least below the mixed surface layers in the Jurassic, while most belemnites are considered epipelagic organisms [75]–[77]. The habitat depth of the only Triassic belemnites is unknown; however they appear to be shallow water forms as with most belemnites, judging from published cross-section photographs [71] (pls.III and IV) and the premises of [75]. The Triassic saw two other lineages of coleoids (Fig. 6). Aulacocerids, which spread worldwide in the Late Triassic, especially along the Tethys Sea [78], may have inhabited deepwater [75]. It has even been suggested that they were not very active [78], as expected for deepwater organisms [64], [65]. The other coleoid lineage in the Triassic, namely phragmoteuthids, had a limited geographic distribution [78] and, judging from the phragmocone angle [79] and generalization by [75], probably lived in shallower waters. Thus, aulacocerids would have been the only possible prey coleoid group for deep-diving air-breathers. At his point, it is not known if the biomass of this group was sufficiently large to support deep-diving, air-breathing predators. Moreover, aulacocerids are considered to have had an extensive shell with a ‘living chamber’ as in nautiloids but unlike modern coleoids or belemnites [80]; thus, they may not have been suitable prey of suction feeders, and certainly were not analogous to modern deepwater coleoids in terms of their characteristics as prey.

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larger image TIFF original image Download: Figure 6. Stratigraphic ranges of major coleoid and key ichthyosaur groups being discussed. Divergence time and tree topology is based on [70]. Ranges of fossil coleoid groups are based on [79], [89]. The shastasaurid ichthyosaurs of the Late Triassic, which were previously interpreted as suction feeders resembling beaked whales [10], did not co-exist with slow-moving and soft-bodied coleoid prey suitable for such suction feeders. The deep-diving ichthyosaur Ophthalmosaurus was coeval with some soft-bodied coleoid vertical migrants. Dark blue indicates deep habitat (reaching the mesopelagic zone) and light blue shallow (epipelagic). The color gradation for vampyromorphs indicates uncertainty in habitat depths of early forms. The upper range of vertically migrating belemnites is extended to the level indicated by [90]. https://doi.org/10.1371/journal.pone.0066075.g006

Hypothetically, it may be possible that some slow moving, soft-bodied coleoids, comparable to today's deepwater forms, inhabited shallow waters in the Triassic and could have served as potential prey for suction feeding marine reptiles. However, such a form has not been recognized to date, despite the fact that the fossil record of shallow water cephalopods is much richer than that of their deepwater counterparts. Absence of such slow moving forms in shallow water may be reasonable because the slowness of extant deepwater coleoids has been linked to the relaxed visually mediated predator/prey interactions in light-limited environments [65].

Another question is whether Triassic ichthyosaurs were capable of deep diving. Deep diving ability has been suggested for ichthyosaurs in the past but only for more derived ichthyosaurs in the Jurassic [8], [15], which had large scleral ring apertures that enabled dim-light adapted vision and a thunniform body plan that facilitated cruising ability. It is unlikely that shastasaurid ichthyosaurs were thunniform, judging from complete skeletons from China. Also, their eyes were not particularly large for ichthyosaurs, with apertures that were small for the eye size, indicating a lack of dim-light adaptation. It is thus likely that these shastasaurids were not deep divers.

Hypothetically, it may be possible that some slow-moving, soft-bodied coleoids, comparable to today's deepwater forms, inhabited shallow waters in the Triassic, providing a viable prey source for suction feeders. However, such a form has not been recognized to date, even though shallow water fossils are far more abundant than their deepwater counterparts. Absence of such shallow water forms may be reasonable because the slowness of extant deepwater coleoids has been linked to the paucity of nutrients in deep sea layers [65].

A recent study suggested that ichthyosaurian eyes evolved in response to large predators rather than deep diving [81]. However, this suggestion is not well-supported optically [82] or by fossil evidence. First, the authors mainly discussed Temnodontosaurus and its possible predators, whereas deep diving was suggested for Ophthalmosaurus and possibly other thunnosaurs that are more derived than Temnodontosaurus [8]. Second, Temnodontosaurus, when it first appeared in the Hettangian (earliest Jurassic), was by far the largest of the coeval marine reptiles despite the claim of [81]. The very large Rhomaleosaurus that [81] mentioned, which was comparable in body length to Temnodontosaurus but was much smaller in gape size than the latter, is known from the Toarcian [83], some ten million years later. Predator-driven evolution has also been proposed for deep diving in ichthyosaurs [84]; however the discussion remains qualitative, especially concerning the involvement of predators. We suggest that the availability of deepwater prey (see below) can explain the data presented in [84] as well.

The appearance of deep-diving ichthyosaurs, such as Ophthalmosaurus, may predate that of the common ancestors of the Decabrachia [69] (Fig. 6). However, isotopic records suggest that belemnites that were coeval with Ophthalmosaurus included vertical migrants [77]. Also, one belemnite that co-occurs with Ophthalmosaurus, namely Cylindrotheuthis, is thought to have been capable of withstanding shallow mesopelagic water pressure [75]. The interpretation of [75] has been challenged in the past but the basic principle of his study remains justified [85]–[88]. Additionally, coleoids belonging to the lineage of vampyromorphs are known as early as the Toarcian of the Early Jurassic [88] (Fig. 6). Although the habitat depths of these early forms are debatable, the only extant member of the lineage, vampire squid Vampyroteuthis infernalis, is a mesopelagic inhabitant.