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Macropredatory Ichthyosaur from the Middle Triassic and the Origin of Modern Trophic Networks

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Macropredatory Ichthyosaur from the Middle Triassic and the Origin of Modern Trophic Networks Macropredatory ichthyosaur from the Middle Triassic and the origin of modern trophic networks Nadia B. Fröbischa,1, Jörg Fröbischa,1, P. Martin Sanderb,1,2, Lars Schmitzc,1,2,3, and Olivier Rieppeld aMuseum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung an der Humboldt-Universität zu Berlin, 10115 Berlin, Germany; bSteinmann Institute of Geology, Mineralogy, and Paleontology, Division of Paleontology, University of Bonn, 53115 Bonn, Germany; cDepartment of Evolution and Ecology, University of California, Davis, CA 95616; and dDepartment of Geology, The Field Museum of Natural History, Chicago, IL 60605 Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved December 5, 2012 (received for review October 8, 2012) The biotic recovery from Earth’s most severe extinction event at the Holotype and Only Specimen. The Field Museum of Natural His- Permian-Triassic boundary largely reestablished the preextinction tory (FMNH) contains specimen PR 3032, a partial skeleton structure of marine trophic networks, with marine reptiles assuming including most of the skull (Fig. 1) and axial skeleton, parts of the predator roles. However, the highest trophic level of today’s the pelvic girdle, and parts of the hind fins. marine ecosystems, i.e., macropredatory tetrapods that forage on prey of similar size to their own, was thus far lacking in the Paleozoic Horizon and Locality. FMNH PR 3032 was collected in 2008 from the and early Mesozoic. Here we report a top-tier tetrapod predator, middle Anisian Taylori Zone of the Fossil Hill Member of the Favret a very large (>8.6 m) ichthyosaur from the early Middle Triassic Formation at Favret Canyon, Augusta Mountains, Pershing County, (244 Ma), of Nevada. This ichthyosaur had a massive skull and large Nevada. The minimum geological age of the find is 244.6 ± 0.36 Ma labiolingually flattened teeth with two cutting edges indicative of (SI Methods). The exact locality data are on file at the FMNH. a macropredatory feeding style. Its presence documents the rapid evolution of modern marine ecosystems in the Triassic where the Diagnosis. This predator is a very large ichthyosaur >8.6 m (SI same level of complexity as observed in today’s marine ecosystems Length Estimate and Proportions) with autapomorphic very large, is reached within 8 My after the Permian-Triassic mass extinction and labiolingually flattened teeth (Fig. 1 E–H) bearing two cutting edges within 4 My of the time reptiles first invaded the sea. This find also (bicarinate) (Table S3). Additionally, the described taxon can be indicates that the biotic recovery in the marine realm may have oc- diagnosed by six unambiguous but equivocal synapomorphies: EVOLUTION curred faster compared with terrestrial ecosystems, where the first a postfrontal that does not participate in the upper temporal fe- apex predators may not have evolved before the Carnian. nestra, a postorbital that adopts a triradiate shape, an anterior terrace of the upper temporal fenestra that reaches the nasal, macropredator | macroevolution a supratemporal that lacks a ventral process, teeth that are laterally compressed, and a tibia that is wider than long. The described taxon he structure of modern marine trophic networks originated in differs from Cymbospondylus, the only other known large Middle Tthe Cambrian (1), but pre-Mesozoic ecosystems lacked con- Triassic ichthyosaur, in having a skull nearly twice as large for the spicuous macrophagous tetrapod apex predators feeding on other given total body length (SI Length Estimate and Proportions), in the large vertebrates (macropredators). Such predators became an in- lack of a deep lower temporal embayment, in that the upper tooth tegral component of food webs during the recovery from the row extends back nearly to the anterior margin of the orbit (Figs. 1 Permian-Triassic (P/T) mass extinction (2, 3), succeeding a long list and 2), in that the rib articular facets are not truncated by the an- of Paleozoic predators that gradually evolved larger, faster, and terior margin of the centrum, and in that the posterior dorsals and more mobile forms (4). From the Jurassic to the present, the mac- anterior caudals are bicipital. It differs from the Upper Triassic ropredator role in the sea has been assumed by a variety of sec- Himalayasaurus tibetensis, the only other Triassic ichthyosaur with ondarily marine tetrapods (2, 5) and, since the Late Cretaceous, also laterally compressed bicarinate cutting teeth, in the conical, evenly by sharks. For example, the macropredators in today’smarine tapering tooth crowns that lack longitudinal fluting (Fig. 1 E–H). ecosystems, the great white shark and the orca, are both capable of hunting, seizing, and dismembering prey of equal or even larger Phylogenetic Relationships. Phylogenetic analyses on the basis of body size than their own (6, 7). In the Jurassic and Cretaceous such parsimony and Bayesian methods indicate that the described macrophagous apex predators were marine reptiles, including taxon is more derived than Mixosauridae and Cymbospondylus pliosaurs, marine crocodiles, mosasaurs, ichthyosaurs, and sharks (2, and represents a basal member of Merriamosauria. In the 5). Throughout most of the Triassic, large macrophagous apex Bayesian analysis, it falls out as more derived than Cal- predators were unknown, suggesting that an essential component of ifornosaurus, Toretocnemus, and Besanosaurus but is basal to extant marine food webs was absent. However, we now describe more derived merriamosaurs (Fig. 3). This phylogenetic posi- a very large ichthyosaur, Thalattoarchon saurophagis gen. et sp. nov., tion is consistent with the stratigraphic occurrence of Tha- that places the evolution of such top predators at most 8 My after the lattoarchon in the middle Anisian (Fig. 3). P/T mass extinction and only 4 My after the first marine reptiles appeared in the fossil record. Author contributions: N.B.F., J.F., P.M.S., L.S., and O.R. designed research; N.B.F., J.F., P.M.S., and L.S. performed research; N.B.F., J.F., P.M.S., and L.S. analyzed data; and N.B.F., Systematic Paleontology J.F., P.M.S., and L.S. wrote the paper. The authors declare no conflict of interest. Ichthyosauria Blainville 1835 This article is a PNAS Direct Submission. Merriamosauria Motani 1999 1N.B.F., J.F., P.M.S., and L.S. contributed equally to this work. Thalattoarchon saurophagis gen. et sp. nov 2To whom correspondence may be addressed. E-mail: [email protected] or [email protected]. 3Presentaddress:W.M.KeckScienceDepartment, Claremont McKenna, Pitzer, and Etymology. The origin of the name is Thalatto- from Greek (sea, Scripps Colleges, 925 N. Mills Avenue, Claremont, CA 91711. fi ocean) and archon (ruler); the speci c name is sauro- from This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. Greek (reptile, lizard) and phagis from Greek (eating). 1073/pnas.1216750110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1216750110 PNAS Early Edition | 1of5 Downloaded by guest on September 25, 2021 Fig. 1. T. saurophagis gen. et sp. nov. FMNH PR 3032 from the middle Anisian (Middle Triassic) part of the Fossil Hill Member of the Favret Formation, Favret Canyon, Augusta Mountains, Nevada. (A) Photograph of the skull in dorsal view. (B) Drawing of same view. (C) Photograph of the skull in left lateral view. Note the flattening of the skull by sediment compaction. Arrow marks the maxillary tooth figured in E–I.(D) Drawing of same view. (E–I) Left maxillary tooth crown in (E) labial view, (F) lingual view, (G) apical view, (H) distal view, and (I) mesial view. Note the lingually recurved shape and the sharp but unserrated cutting edges. [Scale bars: (A–D) 100 and (E–I)10mm.] Brief Anatomical Description. The skull of Thalattoarchon was openings are large and oval, reminiscent of those of Shastasaurus strongly dorsoventrally flattened by sediment compaction (Fig. 1 (8). The postorbital region is long, and the lower temporal em- A and D), but it was not crushed. Weathering removed all evi- bayment is very shallow. The maxilla extends well below the orbits dence of the premaxillae, external nares, and anterior parts of the and bears large teeth to its posterior extremity. lower jaw. The orbits are elongate, the left measuring 29 cm in The very large bicarinate cutting teeth of Thalattoarchon are its length, with a well-preserved scleral ring. The upper temporal most remarkable feature, along with the large skull size compared 2of5 | www.pnas.org/cgi/doi/10.1073/pnas.1216750110 Fröbisch et al. Downloaded by guest on September 25, 2021 such large bicarinate cutting teeth (tooth crown height >5cm)did not evolve. Although the Early Jurassic Temnodontosaurus,which also reached an estimated total body length of 9 m (17), shows some bicarinate teeth in its dentition, these are much smaller (Fig. 3). Even the posteriormost teeth of Thalattoarchon are absolutely 45% larger than the largest documented teeth of Temno- dontosaurus (15, 17). Among other post-Triassic marine rep- tiles, cutting teeth indicative of a macrophagous apex predator role are found in the Late Jurassic plesiosaur Pliosaurus (16), Late Jurassic thalattosuchians such as Dakosaurus (11, 18), and in large Late Cretaceous mosasaurs (16). In the Cenozoic, large macropredators evolved among cetaceans (19) and sharks (20). Thalattoarchon thus precedes all other large, macrophagous apex predator among secondarily aquatic tetrapods. Beginning with the recovery from the P/T biotic crisis, many different amniote lineages independently invaded the marine realm at different times up to the present (2). The first of these secondarily aquatic groups are three major lineages of reptiles: Sauropterygia, Thalattosauria, and Ichthyosauria. They suddenly appear in the marine fossil record by the late Spathian (Early ∼ fi Fig. 2. Reconstruction of the skull of T. saurophagis.(A) Left lateral view. Triassic), 4 My after the P/T crisis (8).
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