Macropredatory from the Middle 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 event at the Holotype and Only Specimen. The Field Museum of Natural His- -Triassic boundary largely reestablished the preextinction tory (FMNH) contains specimen PR 3032, a partial skeleton structure of marine trophic networks, with marine 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 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 predator, middle Taylori Zone of the Fossil Hill Member of the Favret a very large (>8.6 m) ichthyosaur from the early 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 . 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 , the only other known large Middle Tthe (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 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 , 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 , , , 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, , 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, ) 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 26, 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 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 26, 2021 such large bicarinate cutting teeth (tooth crown height >5cm)did not evolve. Although the 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 plesiosaur Pliosaurus (16), Late Jurassic thalattosuchians such as (11, 18), and in large 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 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: , , 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). Intriguingly, the rst (B) Dorsal view. Rostrum length is a conservative estimate. Tooth size is taxonomic diversity peak of marine tetrapods is already reached reconstructed as increasing anteriorly beyond the preserved part because in the Anisian (Middle Triassic) (21, 22) and coincides with great the preserved posterior and middle maxillary teeth are unlikely to have been variation in dentitions, body shape, and body size. This mor- the largest teeth. (Scale bar: 100 mm.) phological disparity suggests that this first radiation of marine reptiles had already diversified broadly into a variety of trophic strategies including feeding on fish, squid, and shelled inverte- with total body length (SI Length Estimate and Proportions). Only brates (2, 15, 21–23). Among these, only ichthyosaurs rapidly EVOLUTION the posterior maxillary teeth are preserved, yet it is safe to assume evolved to large body size, for which a high basal metabolic rate that tooth size increased toward the middle of the jaw. Such (24) may have been a prerequisite (25). a trend is seen in many ichthyosaurs (9) and other marine reptiles: The discovery of Thalattoarchon in the Anisian Fossil Hill for example, mosasaurs (10), thalattosuchians (11), and pliosaurs Member of Nevada indicates that the Early and Middle Triassic (12). The largest fully preserved tooth of Thalattoarchon is a mini- ichthyosaur radiation culminated in a large macrophagous apex mum of 12 cm tall (the full extent of the root is not exposed), with predator already in the early Middle Triassic, at most 8 My after the crown being 5 cm high. The tooth crown is labiolingually the P/T crisis. Thalattoarchon was the top tier (Fig. S2) within flattened, lingually recurved, and bears sharp anterior and pos- a complex and taxonomically as well as ecologically diverse terior cutting edges. There is no evidence of serration on the two marine and fish fauna (SI Fauna and Food Web of the cutting edges, and the labial and lingual surfaces of the crown are Fossil Hill Member). The tetrapod fauna of the Fossil Hill Member smooth (Fig. 1, E–H). One isolated tooth is only preserved as the lacks any indication of the proximity of a shoreline and is over- fill of the pulp cavity. Even this pulp cavity fill shows the two whelmingly dominated by ichthyosaurs, despite the great diversity of cutting edges, which would have been much more pronounced on other lineages occurring in the Triassic (2). The only the enamel cap (13, 14). The teeth have massive roots with round unequivocal nonichthyosaur is the sauropterygian cross sections and dentine infolding but are not swollen compared (26, 27). The ichthyosaur fauna is dominated by two large-bodied with the crown. The lateral margin of the dental lamina of the Cymbospondylus species(28,29),towhichthemajorityofallfinds maxilla shows the remains of the resorbed teeth. On the basis of pertain. Small ichthyosaurs of the genus Phalarodon (P. callawayi tooth shape and size and the presence of distinct cutting edges, the and P. fraasi) are rare (30–32) but are more common in the eastern teeth can be assigned to the “cut” feeding guild among marine outcrop, possible reflecting greater proximity to the paleo-shoreline reptiles (15) (SI Anatomical Descriptions). (33). Previous analyses of rich fossil lagerstätten in South had documented the evolution of diverse marine reptile faunas by the Discussion Anisian as well (3, 34), yet a large macrophagous apex predator At a conservative length estimate of 8.6 m, Thalattoarchon is one remains unknown there. of the largest Early and Middle Triassic ichthyosaurs known and Much research effort has focused on the tempo of the recovery is about the same size as the generalist-feeder Cymbospondylus after the P/T mass extinction and what factors influenced the re- (SI Length Estimate and Proportions) and the largest modern covery process. Biotic interactions are frequently considered to shallow water macropredator, the orca. This overall large size, the have a strong influence and in the P/T aftermath may have slowed large and massive skull, and the presence of very large, labiolin- the overall recovery (35). Hoewever, extrinsic factors, i.e., poor gually flattened teeth are consistent with the macropredator role of environmental conditions such as extremely high temperatures, Thalattoarchon. Large bicarinate cutting teeth suggest that large heightened CO2 levels, and acid rain, could have delayed recovery vertebrate prey (marine tetrapods and fishes) were part of the diet as well (35–37). It is often assumed that trophic networks rebuild of Thalattoarchon, similar to that of extant orcas (7). Among ich- from the bottom up, starting with the primary producers with thyosaurs, bicarinate teeth similar in shape and size are seen only in a stepwise addition of further trophic levels (35). The discovery of the Himalayasasaurus, which lived at least 13 My later the top predator Thalattoarchon indicates full ecosystem recovery than Thalattoarchon and is known from very fragmentary material soon after the stabilization of the marine ecosystems following (16). Himalayasasaurus must have been larger than Thalattoarchon, a period of large environmental perturbations (36). Although but the published estimate of a body length of 15 m (16) is poorly large predators such as the rauisuchians Erythrosuchus and Tici- constrained. With a crown height of close to 6 cm, the teeth of nosuchus appear in the terrestrial rock record in the Anisian (38), Himalayasaurus are only slightly taller than those of Thalattoarchon it has been suggested that full recovery on land was not reached with a body length of >8.6 m. Among post-Triassic ichthyosaurs, until the Late Triassic, 30 My after the P/T extinction (39). It

Fröbisch et al. PNAS Early Edition | 3of5 Downloaded by guest on September 26, 2021 Fig. 3. Time-calibrated phylogeny of Ichthyosauria based on a Bayesian analysis. See ref. 8 for details of the phylogenetic analysis. Stratigraphic ranges of taxa are based on ref. 24. Note the very early appearance of Thalattoarchon.(Inset) Relative tooth size in ichthyosaurs. Thalattoarchon has the relatively largest teeth compared with body length in any ichthyosaur together with two smaller forms with crushing dentitions. The solid line represents the ordinary least square regression line, which is flanked by 95% confidence belts (dashed lines). See Table S1 for data.

therefore seems possible that ecological recovery in the marine taxa were interpreted as uncertainty. The reference taxon of the analysis realm was faster compared with terrestrial environments, but fur- was . The search mode was heuristic and used exactly the same ther investigations are necessary to better understand this pattern. settings as in the original analyses. The analysis found 44 most parsimonious trees (MPTs) 279 steps in length, which were optimized both under DELTRAN Methods and ACCTRAN character optimization. The strict consensus of the MPTs has The Bayesian analysis was conducted using Mr. Bayes 3.2.1 under application a consistency index of 0.514, a rescaled consistency index of 0.401, and a of the Mk model. The analysis was performed with four chains in two in- retention index of 0.792. For details of all methods please see SI Methods. dependent runs with 10 million generations and tree sampling at every 100 generations. A 25% burn-in was disregarded for subsequent analysis. It was ACKNOWLEDGMENTS. Jim Holstein discovered the fossil during a field tested whether the Markov Chain Monte Carlo (MCMC) chains have reached expedition led by Martin Sander and Olivier Rieppel in 1997. Nicole Klein stationarity by plotting log-likelihood values against numbers of generations and Olaf Dülfer helped excavate the fossil. Akiko Shinya, Deborah Wagner, Constance van Beek, Jim Holstein, and Lisa Herzog prepared the fossil to- and evaluation of the SD of split frequencies. The analysis was run twice, once gether with Field Museum volunteers. John Weinberg took the photographs with and once without gamma shape distribution. The Bayes factor supports of the fossil, and Georg Oleschinski contributed to the illustrations. Philipp the analysis without gamma shape distribution, and the results of this analysis Gingerich, Ryosuke Motani, and Johannes Müller read earlier versions of the with associated posterior probability values are presented in Fig. 3. Please note manuscript, and Geerat Vermeij provided insightful comments in discussions that the resulting tree topology of both analyses was identical. with L.S. Two anonymous reviewers and the editor provided useful sugges- The parsimony-based analysis was conducted with PAUP 4.0b10 on tions. The fossil was collected under Bureau of Land Management (BLM) a MacIntosh computer. Five taxa were assigned outgroup status (Petrola- Permit N-85047 and with the support of the BLM Winnemucca field office. cosaurus, Thadeosaurus, , , and ). All Fieldwork was funded by National Geographic Society (Committee for characters were treated as unordered, assigned equal weight, and were Research and Exploration) Grants 6039-97 and 8385-08, The Field Museum parsimony informative. Gaps were treated as missing data, and multistate of Natural History, and the University of Bonn.

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