Macropredatory ichthyosaur from the Middle Triassic and the origin of modern trophic networks

Abstract

The biotic recovery from Earth’s most severe extinction event at the Permian-Triassic boundary largely reestablished the preextinction structure of marine trophic networks, with marine reptiles assuming the predator roles. However, the highest trophic level of today's marine ecosystems, i.e., macropredatory tetrapods that forage on prey of similar size to their own, was thus far lacking in the Paleozoic and 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 large labiolingually flattened teeth with two cutting edges indicative of a macropredatory feeding style. Its presence documents the rapid evolution of modern marine ecosystems in the Triassic where the same level of complexity as observed in today’s marine ecosystems is reached within 8 My after the Permian-Triassic mass extinction and within 4 My of the time reptiles first invaded the sea. This find also indicates that the biotic recovery in the marine realm may have occurred faster compared with terrestrial ecosystems, where the first apex predators may not have evolved before the Carnian.

The structure of modern marine trophic networks originated in the Cambrian (1), but pre-Mesozoic ecosystems lacked conspicuous macrophagous tetrapod apex predators feeding on other large vertebrates (macropredators). Such predators became an integral component of food webs during the recovery from the Permian-Triassic (P/T) mass extinction (2, 3), succeeding a long list of Paleozoic predators that gradually evolved larger, faster, and more mobile forms (4). From the Jurassic to the present, the macropredator role in the sea has been assumed by a variety of secondarily marine tetrapods (2, 5) and, since the Late Cretaceous, also by sharks. For example, the macropredators in today's marine ecosystems, the great white shark and the orca, are both capable of hunting, seizing, and dismembering prey of equal or even larger body size than their own (6, 7). In the Jurassic and Cretaceous such macrophagous apex predators were marine reptiles, including pliosaurs, marine crocodiles, mosasaurs, ichthyosaurs, and sharks (2, 5). Throughout most of the Triassic, large macrophagous apex predators were unknown, suggesting that an essential component of extant marine food webs was absent. However, we now describe a very large ichthyosaur, Thalattoarchon saurophagis gen. et sp. nov., that places the evolution of such top predators at most 8 My after the P/T mass extinction and only 4 My after the first marine reptiles appeared in the fossil record.

Systematic Paleontology

• Ichthyosauria Blainville 1835

• Merriamosauria Motani 1999

• Thalattoarchon 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- from Greek (reptile, lizard) and phagis from Greek (eating).

Holotype and Only Specimen.

The Field Museum of Natural History (FMNH) contains specimen PR 3032, a partial skeleton including most of the skull (Fig. 1) and axial skeleton, parts of the pelvic girdle, and parts of the hind fins.

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) 10 mm.]

Horizon and Locality.

FMNH PR 3032 was collected in 2008 from the middle Anisian Taylori Zone of the Fossil Hill Member of the Favret Formation at Favret Canyon, Augusta Mountains, Pershing County, Nevada. The minimum geological age of the find is 244.6 ± 0.36 Ma (SI Methods). The exact locality data are on file at the FMNH.

Diagnosis.

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

Fig. 2.

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

Phylogenetic Relationships.

Phylogenetic analyses on the basis of parsimony and Bayesian methods indicate that the described taxon is more derived than Mixosauridae and Cymbospondylus and represents a basal member of Merriamosauria. In the Bayesian analysis, it falls out as more derived than Californosaurus, Toretocnemus, and Besanosaurus but is basal to more derived merriamosaurs (Fig. 3). This phylogenetic position is consistent with the stratigraphic occurrence of Thalattoarchon in the middle Anisian (Fig. 3).

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.

Brief Anatomical Description.

The skull of Thalattoarchon was strongly dorsoventrally flattened by sediment compaction (Fig. 1 A and D), but it was not crushed. Weathering removed all evidence of the premaxillae, external nares, and anterior parts of the lower jaw. The orbits are elongate, the left measuring 29 cm in length, 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 embayment is very shallow. The maxilla extends well below the orbits and 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 with total body length (SI Length Estimate and Proportions). Only the posterior maxillary teeth are preserved, yet it is safe to assume that tooth size increased toward the middle of the jaw. Such a 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 minimum of 12 cm tall (the full extent of the root is not exposed), with the crown being 5 cm high. The tooth crown is labiolingually flattened, lingually recurved, and bears sharp anterior and posterior cutting edges. There is no evidence of serration on the two cutting edges, and the labial and lingual surfaces of the crown are smooth (Fig. 1, E–H). One isolated tooth is only preserved as the fill of the pulp cavity. Even this pulp cavity fill shows the two cutting edges, which would have been much more pronounced on the enamel cap (13, 14). The teeth have massive roots with round cross sections and dentine infolding but are not swollen compared with the crown. The lateral margin of the dental lamina of the maxilla shows the remains of the resorbed teeth. On the basis of tooth shape and size and the presence of distinct cutting edges, the teeth can be assigned to the “cut” feeding guild among marine reptiles (15) (SI Anatomical Descriptions).

Discussion

At a conservative length estimate of 8.6 m, Thalattoarchon is one of the largest Early and Middle Triassic ichthyosaurs known and is about the same size as the generalist-feeder Cymbospondylus (SI Length Estimate and Proportions) and the largest modern shallow water macropredator, the orca. This overall large size, the large and massive skull, and the presence of very large, labiolingually flattened teeth are consistent with the macropredator role of Thalattoarchon. Large bicarinate cutting teeth suggest that large vertebrate prey (marine tetrapods and fishes) were part of the diet of Thalattoarchon, similar to that of extant orcas (7). Among ichthyosaurs, bicarinate teeth similar in shape and size are seen only in the Late Triassic Himalayasasaurus, which lived at least 13 My later than Thalattoarchon and is known from very fragmentary material (16). Himalayasasaurus must have been larger than Thalattoarchon, but the published estimate of a body length of 15 m (16) is poorly constrained. With a crown height of close to 6 cm, the teeth of Himalayasaurus are only slightly taller than those of Thalattoarchon with a body length of >8.6 m. Among post-Triassic ichthyosaurs, such large bicarinate cutting teeth (tooth crown height >5 cm) 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 Temnodontosaurus (15, 17). Among other post-Triassic marine reptiles, 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 Triassic), ∼4 My after the P/T crisis (8). Intriguingly, the first taxonomic diversity peak of marine tetrapods is already reached in the Anisian (Middle Triassic) (21, 22) and coincides with great variation in dentitions, body shape, and body size. This morphological 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 invertebrates (2, 15, 21–23). Among these, only ichthyosaurs rapidly evolved 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 Triassic ichthyosaur radiation culminated in a large macrophagous apex predator already in the early Middle Triassic, at most 8 My after the P/T crisis. Thalattoarchon was the top tier (Fig. S2) within a complex and taxonomically as well as ecologically diverse marine reptile and fish fauna (SI Fauna and Food Web of the Fossil Hill Member). The tetrapod fauna of the Fossil Hill Member lacks any indication of the proximity of a shoreline and is overwhelmingly dominated by ichthyosaurs, despite the great diversity of other marine reptile lineages occurring in the Triassic (2). The only unequivocal nonichthyosaur is the sauropterygian Augustasaurus (26, 27). The ichthyosaur fauna is dominated by two large-bodied Cymbospondylus species (28, 29), to which the majority of all finds pertain. Small ichthyosaurs of the genus Phalarodon (P. callawayi and P. fraasi) are rare (30–32) but are more common in the eastern outcrop, possible reflecting greater proximity to the paleo-shoreline (33). Previous analyses of rich fossil lagerstätten in South China had documented the evolution of diverse marine reptile faunas by the Anisian as well (3, 34), yet a large macrophagous apex predator remains unknown there.

Much research effort has focused on the tempo of the recovery after the P/T mass extinction and what factors influenced the recovery process. Biotic interactions are frequently considered to have a strong influence and in the P/T aftermath may have slowed the overall recovery (35). Hoewever, extrinsic factors, i.e., poor environmental conditions such as extremely high temperatures, heightened CO₂ levels, and acid rain, could have delayed recovery as well (35–37). It is often assumed that trophic networks rebuild from the bottom up, starting with the primary producers with a stepwise addition of further trophic levels (35). The discovery of the top predator Thalattoarchon indicates full ecosystem recovery soon after the stabilization of the marine ecosystems following a period of large environmental perturbations (36). Although large predators such as the rauisuchians Erythrosuchus and Ticinosuchus appear in the terrestrial rock record in the Anisian (38), it has been suggested that full recovery on land was not reached until the Late Triassic, 30 My after the P/T extinction (39). It therefore seems possible that ecological recovery in the marine realm was faster compared with terrestrial environments, but further investigations are necessary to better understand this pattern.

Methods

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

The parsimony-based analysis was conducted with PAUP 4.0b10 on a MacIntosh computer. Five taxa were assigned outgroup status (Petrolacosaurus, Thadeosaurus, Claudiosaurus, Hovasaurus, and Hupehsuchus). All characters were treated as unordered, assigned equal weight, and were parsimony informative. Gaps were treated as missing data, and multistate taxa were interpreted as uncertainty. The reference taxon of the analysis was Utatsusaurus. The search mode was heuristic and used exactly the same settings as in the original analyses. The analysis found 44 most parsimonious trees (MPTs) 279 steps in length, which were optimized both under DELTRAN and ACCTRAN character optimization. The strict consensus of the MPTs has a consistency index of 0.514, a rescaled consistency index of 0.401, and a retention index of 0.792. For details of all methods please see SI Methods.