Macropredatory ichthyosaur from the Middle Triassicand the origin of modern trophic networksNadia 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 ofEvolution 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 thePermian-Triassic boundary largely reestablished the preextinctionstructure of marine trophic networks, with marine reptiles assumingthe predator roles. However, the highest trophic level of today’smarine ecosystems, i.e., macropredatory tetrapods that forage onprey of similar size to their own,was thus far lacking in the Paleozoicand early Mesozoic. Here we report a top-tier tetrapod predator,a very large (>8.6 m) ichthyosaur from the early Middle Triassic(244 Ma), of Nevada. This ichthyosaur had a massive skull and largelabiolingually flattened teeth with two cutting edges indicative ofa macropredatory feeding style. Its presence documents the rapidevolution of modern marine ecosystems in the Triassic where thesame level of complexity as observed in today’s marine ecosystemsis reachedwithin 8My after the Permian-Triassic mass extinction andwithin 4 My of the time reptiles first invaded the sea. This find alsoindicates that the biotic recovery in the marine realm may have oc-curred faster compared with terrestrial ecosystems, where the firstapex predators may not have evolved before the Carnian.

macropredator | macroevolution

The structure of modern marine trophic networks originated inthe Cambrian (1), but pre-Mesozoic ecosystems lacked con-spicuous macrophagous tetrapod apex predators feeding on otherlarge vertebrates (macropredators). Such predators became an in-tegral component of food webs during the recovery from thePermian-Triassic (P/T) mass extinction (2, 3), succeeding a long listof Paleozoic predators that gradually evolved larger, faster, andmore mobile forms (4). From the Jurassic to the present, the mac-ropredator role in the sea has been assumed by a variety of sec-ondarily marine tetrapods (2, 5) and, since the Late Cretaceous, alsoby sharks. For example, the macropredators in today’s marineecosystems, the great white shark and the orca, are both capable ofhunting, seizing, and dismembering prey of equal or even largerbody size than their own (6, 7). In the Jurassic and Cretaceous suchmacrophagous apex predators were marine reptiles, includingpliosaurs, marine crocodiles, mosasaurs, ichthyosaurs, and sharks (2,5). Throughout most of the Triassic, large macrophagous apexpredators were unknown, suggesting that an essential component ofextant marine food webs was absent. However, we now describea very large ichthyosaur, Thalattoarchon saurophagis gen. et sp. nov.,that places the evolution of such top predators atmost 8My after theP/T mass extinction and only 4 My after the first marine reptilesappeared in the fossil record.

Systematic Paleontology

Ichthyosauria Blainville 1835Merriamosauria Motani 1999Thalattoarchon saurophagis gen. et sp. nov

Etymology. The origin of the name is Thalatto- from Greek (sea,ocean) and archon (ruler); the specific name is sauro- fromGreek (reptile, lizard) and phagis from Greek (eating).

Holotype and Only Specimen. The Field Museum of Natural His-tory (FMNH) contains specimen PR 3032, a partial skeletonincluding most of the skull (Fig. 1) and axial skeleton, parts ofthe pelvic girdle, and parts of the hind fins.

Horizon and Locality. FMNHPR3032was collected in 2008 from themiddleAnisianTayloriZoneof the FossilHillMember of the FavretFormation at Favret Canyon,AugustaMountains, PershingCounty,Nevada. The minimum geological age of the find is 244.6± 0.36Ma(SI Methods). The exact locality data are on file at the FMNH.

Diagnosis. This predator is a very large ichthyosaur >8.6 m (SILength Estimate and Proportions) with autapomorphic very large,labiolingually flattened teeth (Fig. 1E–H) bearing two cutting edges(bicarinate) (Table S3). Additionally, the described taxon can bediagnosed by six unambiguous but equivocal synapomorphies:a postfrontal that does not participate in the upper temporal fe-nestra, a postorbital that adopts a triradiate shape, an anteriorterrace of the upper temporal fenestra that reaches the nasal,a supratemporal that lacks a ventral process, teeth that are laterallycompressed, and a tibia that is wider than long. The described taxondiffers from Cymbospondylus, the only other known large MiddleTriassic ichthyosaur, in having a skull nearly twice as large for thegiven total body length (SI Length Estimate and Proportions), in thelack of a deep lower temporal embayment, in that the upper toothrow extends back nearly to the anterior margin of the orbit (Figs. 1and 2), in that the rib articular facets are not truncated by the an-terior margin of the centrum, and in that the posterior dorsals andanterior caudals are bicipital. It differs from the Upper TriassicHimalayasaurus tibetensis, the only other Triassic ichthyosaur withlaterally compressed bicarinate cutting teeth, in the conical, evenlytapering tooth crowns that lack longitudinal fluting (Fig. 1 E–H).

Phylogenetic Relationships. Phylogenetic analyses on the basis ofparsimony and Bayesian methods indicate that the describedtaxon is more derived than Mixosauridae and Cymbospondylusand represents a basal member of Merriamosauria. In theBayesian analysis, it falls out as more derived than Cal-ifornosaurus, Toretocnemus, and Besanosaurus but is basal tomore derived merriamosaurs (Fig. 3). This phylogenetic posi-tion is consistent with the stratigraphic occurrence of Tha-lattoarchon in the middle Anisian (Fig. 3).

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.,J.F., P.M.S., and L.S. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.1N.B.F., J.F., P.M.S., and L.S. contributed equally to this work.2To whom correspondence may be addressed. E-mail: martin.sander@uni-bonn.de orlschmitz@kecksci.claremont.edu.

3Present address: W. M. Keck Science Department, Claremont McKenna, Pitzer, andScripps Colleges, 925 N. Mills Avenue, Claremont, CA 91711.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1216750110/-/DCSupplemental.

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Brief Anatomical Description. The skull of Thalattoarchon wasstrongly dorsoventrally flattened by sediment compaction (Fig. 1A and D), but it was not crushed. Weathering removed all evi-dence of the premaxillae, external nares, and anterior parts of thelower jaw. The orbits are elongate, the left measuring 29 cm inlength, with a well-preserved scleral ring. The upper temporal

openings are large and oval, reminiscent of those of Shastasaurus(8). The postorbital region is long, and the lower temporal em-bayment is very shallow. The maxilla extends well below the orbitsand bears large teeth to its posterior extremity.The very large bicarinate cutting teeth of Thalattoarchon are its

most remarkable feature, along with the large skull size compared

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, FavretCanyon, 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 toothcrown 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 unserratedcutting edges. [Scale bars: (A–D) 100 and (E–I) 10 mm.]

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with total body length (SI Length Estimate and Proportions). Onlythe posterior maxillary teeth are preserved, yet it is safe to assumethat tooth size increased toward the middle of the jaw. Sucha trend is seen in many ichthyosaurs (9) and other marine reptiles:for example, mosasaurs (10), thalattosuchians (11), and pliosaurs(12). The largest fully preserved tooth of Thalattoarchon is a mini-mum of 12 cm tall (the full extent of the root is not exposed), withthe crown being 5 cm high. The tooth crown is labiolinguallyflattened, lingually recurved, and bears sharp anterior and pos-terior cutting edges. There is no evidence of serration on the twocutting edges, and the labial and lingual surfaces of the crown aresmooth (Fig. 1, E–H). One isolated tooth is only preserved as thefill of the pulp cavity. Even this pulp cavity fill shows the twocutting edges, which would have been much more pronounced onthe enamel cap (13, 14). The teeth have massive roots with roundcross sections and dentine infolding but are not swollen comparedwith the crown. The lateral margin of the dental lamina of themaxilla shows the remains of the resorbed teeth. On the basis oftooth shape and size and the presence of distinct cutting edges, theteeth can be assigned to the “cut” feeding guild among marinereptiles (15) (SI Anatomical Descriptions).

DiscussionAt a conservative length estimate of 8.6 m, Thalattoarchon is oneof the largest Early and Middle Triassic ichthyosaurs known andis about the same size as the generalist-feeder Cymbospondylus(SI Length Estimate and Proportions) and the largest modernshallow water macropredator, the orca. This overall large size, thelarge and massive skull, and the presence of very large, labiolin-gually flattened teeth are consistent with the macropredator role ofThalattoarchon. Large bicarinate cutting teeth suggest that largevertebrate prey (marine tetrapods and fishes) were part of the dietof Thalattoarchon, similar to that of extant orcas (7). Among ich-thyosaurs, bicarinate teeth similar in shape and size are seen only inthe Late TriassicHimalayasasaurus, which lived at least 13 My laterthan Thalattoarchon and is known from very fragmentary material(16). Himalayasasaurusmust have been larger than Thalattoarchon,but the published estimate of a body length of 15 m (16) is poorlyconstrained. With a crown height of close to 6 cm, the teeth ofHimalayasaurus are only slightly taller than those of Thalattoarchonwith a body length of >8.6 m. Among post-Triassic ichthyosaurs,

such large bicarinate cutting teeth (tooth crown height >5 cm) didnot evolve. Although the Early Jurassic Temnodontosaurus, whichalso reached an estimated total body length of 9 m (17), showssome bicarinate teeth in its dentition, these are much smaller (Fig.3). Even the posteriormost teeth of Thalattoarchon are absolutely45% 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 predatorrole are found in the Late Jurassic plesiosaur Pliosaurus (16),Late Jurassic thalattosuchians such as Dakosaurus (11, 18), andin large Late Cretaceous mosasaurs (16). In the Cenozoic, largemacropredators evolved among cetaceans (19) and sharks (20).Thalattoarchon thus precedes all other large, macrophagous apexpredator among secondarily aquatic tetrapods.Beginning with the recovery from the P/T biotic crisis, many

different amniote lineages independently invaded the marinerealm at different times up to the present (2). The first of thesesecondarily aquatic groups are three major lineages of reptiles:Sauropterygia, Thalattosauria, and Ichthyosauria. They suddenlyappear in the marine fossil record by the late Spathian (EarlyTriassic), ∼4 My after the P/T crisis (8). Intriguingly, the firsttaxonomic diversity peak of marine tetrapods is already reachedin the Anisian (Middle Triassic) (21, 22) and coincides with greatvariation in dentitions, body shape, and body size. This mor-phological disparity suggests that this first radiation of marinereptiles had already diversified broadly into a variety of trophicstrategies including feeding on fish, squid, and shelled inverte-brates (2, 15, 21–23). Among these, only ichthyosaurs rapidlyevolved to large body size, for which a high basal metabolic rate(24) may have been a prerequisite (25).The discovery of Thalattoarchon in the Anisian Fossil Hill

Member of Nevada indicates that the Early and Middle Triassicichthyosaur radiation culminated in a large macrophagous apexpredator already in the early Middle Triassic, at most 8 My afterthe P/T crisis. Thalattoarchon was the top tier (Fig. S2) withina complex and taxonomically as well as ecologically diversemarine reptile and fish fauna (SI Fauna and Food Web of theFossil Hill Member). The tetrapod fauna of the Fossil Hill Memberlacks any indication of the proximity of a shoreline and is over-whelmingly dominated by ichthyosaurs, despite the great diversity ofother marine reptile lineages occurring in the Triassic (2). The onlyunequivocal nonichthyosaur is the sauropterygian Augustasaurus(26, 27). The ichthyosaur fauna is dominated by two large-bodiedCymbospondylus species (28, 29), to which the majority of all findspertain. Small ichthyosaurs of the genus Phalarodon (P. callawayiand P. fraasi) are rare (30–32) but are more common in the easternoutcrop, possible reflecting greater proximity to the paleo-shoreline(33). Previous analyses of rich fossil lagerstätten in South China haddocumented the evolution of diverse marine reptile faunas by theAnisian as well (3, 34), yet a large macrophagous apex predatorremains unknown there.Much research effort has focused on the tempo of the recovery

after the P/T mass extinction and what factors influenced the re-covery process. Biotic interactions are frequently considered tohave a strong influence and in the P/T aftermath may have slowedthe overall recovery (35). Hoewever, extrinsic factors, i.e., poorenvironmental conditions such as extremely high temperatures,heightened CO2 levels, and acid rain, could have delayed recoveryas well (35–37). It is often assumed that trophic networks rebuildfrom the bottom up, starting with the primary producers witha stepwise addition of further trophic levels (35). The discovery ofthe top predator Thalattoarchon indicates full ecosystem recoverysoon after the stabilization of the marine ecosystems followinga period of large environmental perturbations (36). Althoughlarge predators such as the rauisuchians Erythrosuchus and Tici-nosuchus appear in the terrestrial rock record in the Anisian (38),it has been suggested that full recovery on land was not reacheduntil the Late Triassic, 30 My after the P/T extinction (39). It

Fig. 2. Reconstruction of the skull of T. saurophagis. (A) Left lateral view.(B) Dorsal view. Rostrum length is a conservative estimate. Tooth size isreconstructed as increasing anteriorly beyond the preserved part becausethe preserved posterior and middle maxillary teeth are unlikely to have beenthe largest teeth. (Scale bar: 100 mm.)

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therefore seems possible that ecological recovery in the marinerealm was faster compared with terrestrial environments, but fur-ther investigations are necessary to better understand this pattern.

MethodsThe Bayesian analysis was conducted using Mr. Bayes 3.2.1 under applicationof the Mk model. The analysis was performed with four chains in two in-dependent runs with 10 million generations and tree sampling at every 100generations. A 25% burn-in was disregarded for subsequent analysis. It wastested whether the Markov Chain Monte Carlo (MCMC) chains have reachedstationarity by plotting log-likelihood values against numbers of generationsand evaluation of the SD of split frequencies. The analysis was run twice, oncewith and once without gamma shape distribution. The Bayes factor supportsthe analysis without gamma shape distribution, and the results of this analysiswith associated posterior probability values are presented in Fig. 3. Please notethat the resulting tree topology of both analyses was identical.

The parsimony-based analysis was conducted with PAUP 4.0b10 ona MacIntosh computer. Five taxa were assigned outgroup status (Petrola-cosaurus, Thadeosaurus, Claudiosaurus, Hovasaurus, and Hupehsuchus). Allcharacters were treated as unordered, assigned equal weight, and wereparsimony informative. Gaps were treated as missing data, and multistate

taxa were interpreted as uncertainty. The reference taxon of the analysiswas Utatsusaurus. The search mode was heuristic and used exactly the samesettings as in the original analyses. The analysis found 44 most parsimonioustrees (MPTs) 279 steps in length, which were optimized both under DELTRANand ACCTRAN character optimization. The strict consensus of the MPTs hasa consistency index of 0.514, a rescaled consistency index of 0.401, and aretention index of 0.792. For details of all methods please see SI Methods.

ACKNOWLEDGMENTS. Jim Holstein discovered the fossil during a fieldexpedition led by Martin Sander and Olivier Rieppel in 1997. Nicole Kleinand Olaf Dülfer helped excavate the fossil. Akiko Shinya, Deborah Wagner,Constance van Beek, Jim Holstein, and Lisa Herzog prepared the fossil to-gether with Field Museum volunteers. John Weinberg took the photographsof the fossil, and Georg Oleschinski contributed to the illustrations. PhilippGingerich, Ryosuke Motani, and Johannes Müller read earlier versions of themanuscript, and Geerat Vermeij provided insightful comments in discussionswith L.S. Two anonymous reviewers and the editor provided useful sugges-tions. The fossil was collected under Bureau of Land Management (BLM)Permit N-85047 and with the support of the BLM Winnemucca field office.Fieldwork was funded by National Geographic Society (Committee forResearch and Exploration) Grants 6039-97 and 8385-08, The Field Museumof Natural History, and the University of Bonn.

1. Vannier J, Steiner M, Renvoisé E, Hu S-X, Casanova J-P (2007) Early Cambrian origin ofmodern food webs: Evidence from predator arrow worms. Proc Biol Sci 274(1610):627–633.

2. Motani R (2009) The evolution of marine reptiles. Evol Educ Outreach 2(2):224–235.3. Hu SX, et al. (2011) The Luoping biota: Exceptional preservation, and new evidence on the

Triassic recovery from end-Permian mass extinction. Proc Biol Sci 278(1716):2274–2282.4. Vermeij G (2002) Evolution in the consumer age: predators and the history of life. The

Fossil Record of Predation. Paleontological Society Special Papers 8, eds Kowalewski M,Kelley PH (Paleontological Society, Lawrence, KS), pp 375–393.

5. Walker SE, Brett CE (2002) Post-Paleozoic Patterns in Marine Predation: Was Therea Mesozoic and Cenozoic Marine Predatory Revolution? The Fossil Record of Pre-dation. Paleontological Society Special Papers 8, eds Kowalewski M, Kelley PH (Pa-leontological Society, Lawrence, KS), pp 119–193.

6. Motta PJ, Wilga CD (2001) Advances in the study of feeding behaviors, mechanisms,and mechanics of sharks. Environ Biol Fishes 60(1-3):131–156.

7. Jefferson TA, Stacey PJ, Baird RW (1991) A review of Killer Whale interactionswith other marine mammals:predation to co-existence. Mammal Rev 21(4):151–180.

Fig. 3. Time-calibrated phylogeny of Ichthyosauria based on a Bayesian analysis. See ref. 8 for details of the phylogenetic analysis. Stratigraphic ranges oftaxa are based on ref. 24. Note the very early appearance of Thalattoarchon. (Inset) Relative tooth size in ichthyosaurs. Thalattoarchon has the relativelylargest teeth compared with body length in any ichthyosaur together with two smaller forms with crushing dentitions. The solid line represents the ordinaryleast square regression line, which is flanked by 95% confidence belts (dashed lines). See Table S1 for data.

1396 | www.pnas.org/cgi/doi/10.1073/pnas.1216750110 Fröbisch et al.

Dow

nloa

ded

by g

uest

on

Apr

il 5,

202

1

http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1216750110/-/DCSupplemental/pnas.201216750SI.pdf?targetid=nameddest=STXThttp://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1216750110/-/DCSupplemental/st01.docwww.pnas.org/cgi/doi/10.1073/pnas.1216750110

8. Sander PM, Chen X, Cheng L, Wang X (2011) Short-snouted toothless ichthyosaurfrom China suggests Late Triassic diversification of suction feeding ichthyosaurs.PLoS One 6(5):e19480.

9. McGowan C, Motani R (2003) Handbook of Paleoherpetology. Part 8. Ichthyopterygia(Dr. Friedrich Pfeil Verlag, Munich), p 175.

10. Russell DA (1967) Systematics and morphology of American mosasaurs. Bull PeabodyMus Nat Hist Yale Univ 23:1–241.

11. Gasparini Z, Pol D, Spalletti LA (2006) An unusual marine crocodyliform from theJurassic-Cretaceous boundary of Patagonia. Science 311(5757):70–73.

12. Andrews CW (1913) A Descriptive Catalogue of the Marine Reptiles of the OxfordClay. Part II (The British Museum, London) p 206.

13. Sander PM (1999) The microstructure of reptilian tooth enamel: terminology, func-tion, and phylogeny. Münchner Geowissenschaftliche Abhandlungen 38:1–102.

14. Sander PM (2000) Prismless enamel in amniotes: Terminology, function, and evolu-tion. Development, Function and Evolution of Teeth, eds Teaford M, Ferguson MWJ,Smith MM (Cambridge Univ Press, New York), pp 92–106.

15. Massare JA (1987) Tooth morphology and prey preference of Mesozoic marine rep-tiles. J Vertebr Paleontol 7(2):121–137.

16. Motani R, Manabe M, Dong ZM (1999) The status of Himalayasaurus tibetensis (Ich-thyopterygia). Paludicola 2(2):174–181.

17. McGowan C (1996) Giant ichthyosaurs of the Early Jurassic. Can J Earth Sci 33(7):1011–1021.

18. Andrade MBD, Young MT, Desojo JB, Brusatte SL (2010) The evolution of extremehypercarnivory in Metriorhynchidae (Mesoeucrocodylia: Thalattosuchia) based onevidence frommicroscopic denticle morphology. J Vertebr Paleontol 30(5):1451–1465.

19. Lambert O, et al. (2010) The giant bite of a new raptorial sperm whale from theMiocene epoch of Peru. Nature 466(7302):105–108.

20. Gottfried MD, Fordyce RE (2001) An associated specimen of Carcharodon angustidens(Chondrichtyes, Laminidae) from the late Oligocene of New Zealand, with commentson Carcharodon interrelationships. J Vertebr Paleontol 21(4):730–739.

21. Benson RBJ, Butler RJ, Lindgren J, Smith AS (2010) Mesozoic marine tetrapod di-versity: mass extinctions and temporal heterogeneity in geological megabiases af-fecting vertebrates. Proc Biol Sci 277(1683):829–834.

22. Kelley NP, Motani R, Jiang D-Y, Rieppel O, Schmitz L (2012) Selective extinction of Triassicmarine reptiles during long-term sea level changes illuminated by seawater strontiumisotopes. Palaeogeogr Palaeoclimatol, Palaeoecol, 10.1016/j.palaeo.2012.07.026.

23. Thorne PM, Ruta M, Benton MJ (2011) Resetting the evolution of marine reptiles atthe Triassic-Jurassic boundary. Proc Natl Acad Sci USA 108(20):8339–8344.

24. Bernard A, et al. (2010) Regulation of body temperature by some Mesozoic marinereptiles. Science 328(5984):1379–1382.

25. Sander PM, et al. (2011) Biology of the sauropod dinosaurs: The evolution of gigan-tism. Biol Rev Camb Philos Soc 86(1):117–155.

26. Sander PM, Rieppel OC, Bucher H (1997) A new pistosaurid (Reptilia: Sauropterygia)from the Middle Triassic of Nevada and its implications for the origin of plesiosaurs. JVertebr Paleontol 17(3):526–533.

27. Rieppel O, Sander PM, Storrs GW (2002) The skull of the pistosaur Augustasaurusfrom the Middle Triassic of northwestern Nevada. J Vertebr Paleontol 22(3):577–592.

28. Fröbisch N, Sander PM, Rieppel O (2006) A new species of Cymbospondylus (Diapsida,Ichthyosauria) from the Middle Triassic of Nevada and a re-evaluation of the skullosteology of the genus. Zool J Lin Soc Lond 147(4):515–538.

29. Merriam JC (1908) Triassic Ichthyosauria, with special reference to the Americanforms. Mem Univ Calif 1(1):1–155.

30. Schmitz L, Sander PM, Storrs GW, Rieppel O (2004) New Mixosauridae (Ichthyosauria)from the Middle Triassic of the Augusta Mountains (Nevada, USA) and their im-plications for mixosaur taxonomy. Palaentographica A 270(4-6):133–162.

31. Schmitz L (2005) The taxonomic status of Mixosaurus nordenskioeldii (Ichthyosauria).J Vertebr Paleontol 25(4):983–985.

32. Jiang D, Schmitz L, Hao W, Sun Y (2006) A new mixosaurid ichthyosaur from theMiddle Triassic of China. J Vertebr Paleontol 26(1):60–69.

33. Sander PM, Rieppel OC, Bucher H (1994) New marine vertebrate fauna from theMiddle Triassic of Nevada. J Paleontol 68(3):676–680.

34. Jiang DY, et al. (2009) Biodiversity and sequence of the Middle Triassic Panxian ma-rine reptile fauna, Guizhou Province, China. Acta Geol Sin 83:451–459.

35. Cheng Z-Q, Benton MJ (2012) The timing and pattern of biotic recovery following theend-Permian mass extinction. Nat Geosci, 10.1038/ngeo1475.

36. Payne JL, et al. (2004) Large perturbations of the carbon cycle during recovery fromthe end-permian extinction. Science 305(5683):506–509.

37. Sun Y, et al. (2012) Lethally hot temperatures during the Early Triassic greenhouse.Science 338(6105):366–370.

38. Nesbitt SJ (2011) The early evolution of archosaurs: Relationships and the origin ofmajor clades. Bull Am Mus Nat Hist 352:1–292.

39. Sahney S, Benton MJ (2008) Recovery from the most profound mass extinction of alltime. Proc Biol Sci 275(1636):759–765.

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