Absence of suction feeding ichthyosaurs and its implications for triassic mesopelagic paleoecology - PubMed (original) (raw)

Absence of suction feeding ichthyosaurs and its implications for triassic mesopelagic paleoecology

Ryosuke Motani et al. PLoS One. 2013.

Abstract

Mesozoic marine reptiles and modern marine mammals are often considered ecological analogs, but the extent of their similarity is largely unknown. Particularly important is the presence/absence of deep-diving suction feeders among Mesozoic marine reptiles because this would indicate the establishment of mesopelagic cephalopod and fish communities in the Mesozoic. A recent study suggested that diverse suction feeders, resembling the extant beaked whales, evolved among ichthyosaurs in the Triassic. However, this hypothesis has not been tested quantitatively. We examined four osteological features of jawed vertebrates that are closely linked to the mechanism of suction feeding, namely hyoid corpus ossification/calcification, hyobranchial apparatus robustness, mandibular bluntness, and mandibular pressure concentration index. Measurements were taken from 18 species of Triassic and Early Jurassic ichthyosaurs, including the presumed suction feeders. Statistical comparisons with extant sharks and marine mammals of known diets suggest that ichthyosaurian hyobranchial bones are significantly more slender than in suction-feeding sharks or cetaceans but similar to those of ram-feeding sharks. Most importantly, an ossified hyoid corpus to which hyoid retractor muscles attach is unknown in all but one ichthyosaur, whereas a strong integration of the ossified corpus and cornua of the hyobranchial apparatus has been identified in the literature as an important feature of suction feeders. Also, ichthyosaurian mandibles do not narrow rapidly to allow high suction pressure concentration within the oral cavity, unlike in beaked whales or sperm whales. In conclusion, it is most likely that Triassic and Early Jurassic ichthyosaurs were 'ram-feeders', without any beaked-whale-like suction feeder among them. When combined with the inferred inability for dim-light vision in relevant Triassic ichthyosaurs, the fossil record of ichthyosaurs does not suggest the establishment of modern-style mesopelagic animal communities in the Triassic. This new interpretation matches the fossil record of coleoids, which indicates the absence of soft-bodied deepwater species in the Triassic.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1

Figure 1. Measurements taken from ichthyopterygian specimens.

a, schematic drawing of mandible with a pair of ceratobranchial I. b, magnified view of a single ceratobranchial I. HL: hyobranchial rod length; HW, hyobranchial rod median width; ML, mandibular ramus length; MW, mandibular width; TW, mandibular width at the end of tooth row. Brown, mandible; orange, hyobranchial rod.

Figure 2

Figure 2. Mandible and hyobranchial apparatus of selected vertebrate groups.

Suction feeders are in the top row, and ‘ram’ feeders bottom row. Brown fill, mandible; green fill, hyoid corpus; orange fill , ossified/calcified hyobranchial rods that are discussed; white fill with real outline, other ossified hyobranchial elements; white fill with dotted outline: cartilaginous hyobranchial element. Taxa: a, Mata Mata Turtle Chelus fimbriatus; b, Japanese Angel Shark Squatina japonica; c, Pygmy Sperm Whale Kogia breviceps; d, Common Musk Turtle Sternotherus odoratus; e, Sharpnose Sevengill Shark Heptranchias perlo; f, Bottlenose Dolphin Tursiops truncatus; and g, Triassic Ichthyosaur Qianichthyosaurus zhoui. Derivations: a based ; b and e from CT data; c and f based on ; d based on ; and g based on IVPP 11838. Not to scale.

Figure 3

Figure 3. Bivariate SMA regression of features related to Mandibular Pressure Concentration Index and Hyobranchial Robustness.

a. Mandibular Pressure Concentration Index; b. Mandibular Robustness. Lower intercept values in a and b indicate: a, higher pressure concentration within the oral cavity; and b, less robust suspensory element of hyobranchial apparatus. Ichthyopterygians has limited pressure concentration (high intercept in a) and slender hyobranchial rod (low intercept in b). E, G, Sha, and Sho denote Eurhinosaurus, Guanlingsaurus, Shastasaurus, and Shonisaurus, respectively. Note that the latter three were considered suction feeders by .

Figure 4

Figure 4. Hyobranchial apparatus of selected ichthyopterygians.

a., Qianichthyosaurus zhoui (IVPP 11838); Guanlingsaurus liangae (GNG dq-50);c, Ichthyosaurus communis (OUM J10313); and d, Hauffiopteryx typicus (SMNS 81962). cbi, ceratobranchial I; hc, hyoid corpus; l, left; r, right. Scale bars are five centimeters.

Figure 5

Figure 5. Boxplots of two ratios across taxa and feeding types.

a, hyobranchial robustness; b, mandibular bluntness. The thick line in the center denotes the median, the box surrounding it contains the middle 50% of the data points, and the whiskers extend to the most extreme data point which is no more than 1.5 times the interquartile range from the box. The data outside the whisker are considered outliers, plotted as small circles.

Figure 6

Figure 6. Stratigraphic ranges of major coleoid and key ichthyosaur groups being discussed.

Divergence time and tree topology is based on . Ranges of fossil coleoid groups are based on , . The shastasaurid ichthyosaurs of the Late Triassic, which were previously interpreted as suction feeders resembling beaked whales , 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 .

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The specimen of Chaohusaurus was collected with funds from the National Geographic Society Committee for Research and Exploration (#8669-09) to RM and Project 40920124002 from the National Natural Science Foundation of China to DJ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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