Ichthyosaurs reference thread

[Life]

1. Diversity across time and space

Figure 3 in (Fröbisch et al., 2013) for reference:



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2. Swimming adaptations

2.1. Ichthyosaurs are the FIRST to represent tuna-shaped amniotes as a group but with variations in body plans and swimming modes.

Publication for reference: Structural, functional, and physiological signals in ichthyosaur vertebral centrum microanatomy and histology

ABSTRACT

The first tuna-shaped amniotes evolved among ichthyosaurs, but this group exhibits in fact a wide diversity of morphologies and swimming modes. The histology and microanatomical features of vertebral centra of a diversity of ichthyosaur taxa from most basal to highly derived illustrating this variability were analyzed. The occurrence of unusual parallel fibered bone with platings of true parallel-fibered bone confirms high growth rate in all these taxa. Ichthyosaur vertebrae, which are deeply amphicoelous, show a limited endosteal territory associated with a limited growth in length. No bone mass increase nor decrease occurs. The vertebral centrum is spongious, and two microtypes are observed in the periosteal territory, with different degrees of organization of the trabecular network. The microtypes appear to be associated with the shape of the vertebral centrum, the organization of the spongiosa becoming homogeneous in the disk-shaped centra of cymbospondylids and Neoichthyosauria, rather than much more heterogeneous in spool-shaped centra of primitive Triassic forms. As opposed to what was previously suggested in other amniotes, the main switch in microanatomical organization appears thus to be correlated to the acquisition of deeply amphicoelous disk-like vertebral centra rather than to a shift in swimming mode from long and slender-bodied anguilliform swimmers to thunniform swimmers.

Citation: Houssaye, A., Nakajima, Y., & Sander, P. M. (2018). Structural, functional, and physiological signals in ichthyosaur vertebral centrum microanatomy and histology. Geodiversitas, 40(2), 161-170.

LINK: bioone.org/journals/geodiversitas/volume-40/issue-2/geodiversitas2018v40a7/Structural-functional-and-physiological-signals-in-ichthyosaur-vertebral-centrum-microanatomy/10.5252/geodiversitas2018v40a7.short

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Figure 1 in (Houssaye et al., 2018) for reference:



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2.2. Ichthyosaurs had cartilage in articular and non-articular surfaces (with exception of the dorsal and ventral surfaces) independently of ontogenetic stage and shape to facilitate maneuverability during swimming.

Publication for reference: Microanatomy and histology of the distal limb elements of ophthalmosaurids from the Middle Jurassic to the Lower Cretaceous of the Neuquén Basin, Patagonia, Argentina

ABSTRACT

One of the most significant morphological modifications in numerous tetrapod lineages in their secondary adaptation to life in open marine environment is the transformation of the limb into fins. The loss of perichondral bone has been pointed out as the mechanism through which this transformation was achieved. Advanced ichthyosaurs, including ophthalmosaurids, are characterized by the zeugopodium and autopodium not clearly differentiated, and bones dorsoventrally flattened and nodular. In the case of distal limb elements, particularly phalanges, two main arrangements can be recognized in dorsal and ventral views: one is characterized by spaced and quite rounded elements, whereas in the other phalanges tightly packed arrangement is observed, showing almost straight articular surfaces which result in polygonal outlines. Previously only distal limb elements of non-ophthalmosaurids, were described. In this study, we describe and interpret the microstructure of distal limb elements of six specimens of ichthyosaur, five ophthalmosaurids and one non-ophthalmosaurid. Our result shows persistence of abundant cartilage in articular and non-articular surfaces (with exception of the dorsal and ventral surfaces) independently of ontogenetic stage and shape. The coat layer of calcified cartilage is thicker in juvenile than adult specimens and this could be related to the bone remodeling. It is probable that the persistence of significant amount of cartilage in the joint surfaces of the distal limb elements of ichthyosaurs would be linked to more evenly distribute forces through the limb, the increase in the number of articulations and the increase maneuverability during swimming.

Citation: Marianella, T., Lisandro, C., & Fernández, M. S. (2021). Microanatomy and histology of the distal limb elements of ophthalmosaurids from the Middle Jurassic to the Lower Cretaceous of the Neuquén Basin, Patagonia, Argentina. Cretaceous Research, 121, 104737.

LINK: www.sciencedirect.com/science/article/abs/pii/S0195667120304249

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3. Gigantism

3.1. Ichthyosaurs are the FIRST to attain gigantism in marine environments.

Geological Period and Location	Identity	Specimen	Estimated TL	Reference
The Norian Late Triassic; British Columbia	Shonisaurus sikanniensis sp. nov.	TMP 1994.378.02	21 m	Nicholls and Manabe (2004); Lomax et al (2018)
The Rhaetian Late Triassic; England	The Aust specimen (Shastasaurid; similarity to Shonisaurus sikanniensis)	BRSMG Cb3869		Redelstorff et al (2012); Lomax et al (2018)
The Rhaetian Late Triassic; England	The Aust specimen (Shastasaurid; similarity to Shonisaurus sikanniensis)	BRSMG Cb3870		Redelstorff et al (2012); Lomax et al (2018)
The Rhaetian Late Triassic; France	The Cuers specimen (Shastasaurid; similarity to Shonisaurus sikanniensis)	MHNTV PAL2/2010		Fischer et al (2014); Lomax et al (2018)
The Rhaetian Late Triassic; England	The Lilstock specimen (Shastasaurid; similarity to Shonisaurus sikanniensis)	BRSMG Cg2488	20 - 26 m	Lomax et al (2018)

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3.2. Ichthyosaurs are believed to have attained gigantism at a faster rate than marine mammals.

Publication reference: Early giant reveals faster evolution of large body size in ichthyosaurs than in cetaceans

Structured Abstract

INTRODUCTION

The iterative evolution of secondarily marine tetrapods since the Paleozoic offers the promise of better understanding how the anatomy and ecology of animals change when returning to the sea. Recurring patterns of convergence in the geological past may suggest predictability of evolution when transitioning from full-time life on land to full-time life in the ocean. Ichthyosaurs (fish-shaped marine reptiles of the Mesozoic) and today’s cetaceans (whales, dolphins, and porpoises) are two of the most informative lineages to exemplify secondary returns to the sea. The notable resemblance in body shape and lifestyle of ichthyosaurs and cetaceans contrasts with their separation in time by nearly 200 million years, providing an often-cited example of convergent evolution. Ichthyosaurs arose 249 million years ago and populated the oceans for the next 150 million years. Cetaceans did not evolve until about 56 million years ago. As tail-propelled swimmers, ichthyosaurs and cetaceans evolved not only convergent body shapes but also large body sizes.

RATIONALE

The integration of fossil and extant data can improve understanding of aquatic adaptation and gigantism as patterns of convergent evolution, particularly when interpreted in an ecological context. Our paleontological fieldwork in the Fossil Hill Member (Middle Triassic, Nevada, USA) provided the basis for the marine reptile data and resulted in finds of giant ichthyosaurs as part of the pelagic Fossil Hill Fauna. We compiled data for both fossil and living whales from the extensive literature. Together, these data provide the basis for computational analyses of maximum body size and its evolution over time. Modeling of energy flux in the Fossil Hill Fauna helps in understanding how the Fossil Hill ecosystem could have supported several large to giant tetrapod ocean consumers so early in ichthyosaur evolutionary history.

RESULTS

We describe an ichthyosaur with a 2-m-long skull from the Fossil Hill Fauna as a new species of Cymbospondylus. At present, this is the largest known tetrapod of its time, on land or in the sea, and is the first in a series of ocean giants. The Fossil Hill Fauna includes several other large-bodied ichthyosaurs in the Cymbospondylus radiation. The body-size range in this Triassic fauna rivals the range seen in modern whale faunas, from a total length of about 2 m in Phalarodon to more than 17 m in the new species. As preserved in the fossil record, the Fossil Hill Fauna represents a stable trophic network and could even have supported another large ichthyosaur if it bulk fed on small, but abundant, prey such as ammonoids. In absolute time, the new ocean giant lived 246 million years ago, only about 3 million years after the appearance of the first ichthyosaurs. Our research suggests that ichthyosaurs evolved large body size very early on in the clade’s history, comparatively earlier than whales.

CONCLUSION

Ichthyosaurs and cetaceans both evolved very large body sizes, yet their respective evolutionary pathways toward gigantism were different. Ichthyosaurs seem to have benefited from the abundance of pelagic conodonts and ammonoids after the recovery from the end-Permian mass extinction, even in the absence of modern primary producers. Cetaceans took different routes, but all appear to be related to trophic specialization, including the loss of teeth in baleen whales (Mysticeti) and the evolution of raptorial feeding and deep diving in toothed whales (Odontoceti).

Sander, P. M., Griebeler, E. M., Klein, N., Juarbe, J. V., Wintrich, T., Revell, L. J., & Schmitz, L. (2021). Early giant reveals faster evolution of large body size in ichthyosaurs than in cetaceans. Science, 374(6575), eabf5787.

Link: www.science.org/doi/abs/10.1126/science.abf5787

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4. Raptorial Ichthyosaurs?

There is evidence of raptorial adaptations in following Ichthyosaurs:

Geological Period and Location	Identity	Specimen	Estimated TL	Reference
The Upper Triassic - the Lower Jurassic; Nottinghamshire; Chile	Temnodontosaurus sp.	LEICT: G463.1972	>10 m	(Lomax & Gibson, 2015; Otero & Sepúlveda, 2020)
The Norian Late Triassic; Tibet	Himalayasaurus tibetensis	IVPP V4003	>14 m	(Motani et al., 1999)
The Ladinian Middle Triassic; Nevada	Thalattoarchon saurophagis gen. et sp. nov	FMNHPR3032	>8.6 m	(Fröbisch et al., 2013)
The Ladinian Middle Triassic; Guizhou	Guizhouichthyosaurus	XNGM-WS-50-R4	~7 m	(Jiang et al., 2020)

Visuals

Footage:

Trophic interactions on record

Predator	Prey	Reference
ichthyosaur Guizhouichthyosaurus (specimen (XNGM-WS-50-R4); TL = ~5 m)	Thalattosaur Xinpusaurus xingyiensis (TL = ~4 m)	Jiang et al (2020)

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[Life]

Trophic interaction case # 1: Evidence Supporting Predation of 4-m Marine Reptile by Triassic Megapredator

Graphical Abstract



Summary

Air-breathing marine predators have been essential components of the marine ecosystem since the Triassic. Many of them are considered the apex predators but without direct evidence—dietary inferences are usually based on circumstantial evidence, such as tooth shape. Here we report a fossil that likely represents the oldest evidence for predation on megafauna, i.e., animals equal to or larger than humans, by marine tetrapods—a thalattosaur (∼4 m in total length) in the stomach of a Middle Triassic ichthyosaur (∼5 m). The predator has grasping teeth yet swallowed the body trunk of the prey in one to several pieces. There were many more Mesozoic marine reptiles with similar grasping teeth, so megafaunal predation was likely more widespread than presently conceived. Megafaunal predation probably started nearly simultaneously in multiple lineages of marine reptiles in the Illyrian (about 242–243 million years ago).

Citation: Jiang, D. Y., Motani, R., Tintori, A., Rieppel, O., Ji, C., Zhou, M., ... & Li, Z. G. (2020). Evidence Supporting Predation of 4-m Marine Reptile by Triassic Megapredator. Iscience, 23(9), 101347.

LINK: www.sciencedirect.com/science/article/pii/S2589004220305344

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Introduction

Land vertebrates started recolonizing the sea after the end-Permian mass extinction and diversified into many ecomorphs including apex predators (Kelley and Pyenson, 2015; Motani, 2009; Vermeij and Motani, 2018). Such predators are found among cetaceans and pinnipeds in the modern ecosystem but belonged to marine reptiles, such as plesiosaurs, mosasaurs, and ichthyosaurs, in the Mesozoic (Massare, 1987). However, direct evidence supporting the inference that some fossil marine reptiles preyed on marine megafauna is rare (Massare, 1987)—only five genera of Mesozoic marine reptiles have so far been reported with remains of other tetrapods in the stomach (Table 1), namely, three mosasaurs (Tylosaurus, Everhart, 2004; Konishi et al., 2014; Massare, 1987; Hainosaurus, Konishi et al., 2014; Russell, 1967; Prognathodon, Konishi et al., 2011) and two ichthyosaurs (Temnodontosaurus, Böttcher, 1989; McGowan, 1974; and Platypterygius, Kear et al., 2003). Even in these exceptional cases, only up to several bones of the prey, disarticulated and usually fragmentary, are preserved, and some of these prey tetrapods may not be large enough to be considered megafaunal species.



In the absence of direct evidence, circumstantial evidence, such as body size and tooth shape, has been used to infer the diet of fossil marine reptiles (Massare, 1987). If a large species has large teeth with carinae (cutting edges), it is usually considered the apex predator of its ecosystem even in the absence of a direct record of its diet (Frobisch et al., 2013; Massare, 1987). However, it is also known that not all marine apex predators have teeth with carinae (Böttcher, 1989; Massare, 1987), e.g., the killer whale (Orcinus orca) and Temnodontosaurus trigonodon. Moreover, the largest marine vertebrate of a given ecosystem is often not the apex predator—the largest whales are filter feeders, and so were the largest Mesozoic fishes (Friedman et al., 2010). The largest Mesozoic marine reptile, belonging to ichthyosaurs, was edentulous (Nicholls and Manabe, 2004), suggesting it did not feed on large bony prey. Modern marine apex predators, such as the killer whale and great white shark (Carcharodon carcharias) are typically in the size range of 5–8 m (Mikhalev et al., 1981; Ralls and Mesnick, 2018) and 3–6 m (Boldrocchi et al., 2017; French et al., 2018), respectively, although the largest individuals of O. orca reach 9 m. There are larger whales, such as baleen whales (up to about 30 m), sperm whale (up to about 18 m), and beaked whales (up to about 12 m) (Jefferson et al., 1993), but they are not apex predators.

Ichthyosaurs are a group of Mesozoic marine reptiles that gave rise to a fish-shaped body profile. They belong to Ichthyosauromorpha (Chen et al., 2014; Jiang et al., 2016; Motani et al., 2015b), a clade that emerged in the late Early Triassic, approximately coinciding with the marine invertebrate diversification in the late Early Triassic (Fan et al., 2020; Fu et al., 2016; Motani et al., 2017). They radiated in the latest Early to Middle Triassic and became air-breathing top predators during the process of reconstruction of the Triassic marine ecosystem after the end-Permian extinction. The lineage gave rise to the oceanic clade Euichthyosauria, which later “dominated” the Mesozoic oceans in the Jurassic and Cretaceous. The evolution of their diet and feeding functions has previously been studied to some extent (McGowan and Motani, 2003; Motani et al., 2013; Scheyer et al., 2014). However, many questions remain as to which species of ichthyosaurs were truly apex predators.

Guizhouichthyosaurus is a genus of ichthyosaur that would not be considered an apex predator based on the traditional criteria. Its typical size range is about 4–6 m in total length, being smaller than the killer whale (O. orca), although some individuals reached about 7 m. Its teeth lacked carinae and were not very large for the body size. However, in 2010, a nearly complete skeleton of Guizhouichthyosaurus that directly contradicts this interpretation was excavated from the Ladinian (Middle Triassic) Zhuganpo Member of the Falang Formation in Xingyi, Guizhou, southwestern China. The specimen, spanning 4.8 m, was subsequently prepared in the laboratory of the Xingyi National Geopark Museum. In the abdominal region of this specimen, an obvious block of packed bones bulges above the bedding plane. After a detailed preparation, it can be discerned that the bones inside of this bulging block are not ichthyosaurian but originated from a thalattosaur, which was most likely hunted by the ichthyosaur. The prey remains are partially articulated and represent the trunk region without the skull or tail. The purpose of this article is to report the stomach contents and discuss their implications for the early evolution of megafaunal predation by marine tetrapods.

There is confusion in the literature regarding the term “macropredator.” There has been a recent tendency in the fossil marine vertebrate literature to call predators that feed on large vertebrates “macropredators” (Benson et al., 2013; Frobisch et al., 2013; Konishi et al., 2014). However, the same term has historically been used in the ecological literature to indicate macroscopic predators, many of which are not large. We therefore call the predators that feed on megafauna “megapredators”—the word megafauna traditionally refers to animals of adult human size (arbitrarily set at 44 kg) or larger (Stuart, 1991), although the threshold value may be as low as 10 kg in some studies (Wroe et al., 2004).

Results

Bromalite Features
The main specimen studied (XNGM-WS-50-R4) is of an ichthyosaur identified as Guizhouichthyosaurus (Methods), containing a dense concentration of many bones inside the ribs and gastralia in the abdominal region (Figure 1). These bones are considered a bromalite, a term that refers to all trace fossils representing food items that entered the oral cavity or gastrointestinal tract in life, whether or not they were expelled subsequently (Hunt and Lucas, 2012). These bones do not pertain to the skeleton of the ichthyosaur—they are morphologically different from those of the ichthyosaur, whereas the ichthyosaur postcranial skeleton is well-articulated, without any obvious lack of bones.



Figure 1. The Skeleton of Guizhouichthyosaurus (XNGM-WS-50-R4) and Its Stomach Contents

(A) The skeleton.

(B) Close-up of the stomach area, highlighted by red rectangle in (A).

(C) Line drawing to show selected bone elements of prey in (B).

(D) 3D rendering showing the ventral side view of the bromalite, revealing two strings of vertebrae. Red triangles point at the vertebrae that can been seen from the top surface, and white triangles with red outlines mark three vertebrae that are hidden by the humerus. Yellow triangles point to the vertebrae of the second string. Abbreviations: cl, clavicle, color in dark orange; co, coracoid, in light orange; fe, femur, in tan; fi, fibula, in goldenrod; h, humerus, in blue; icl, interclavicle, in yellow; il, ilium, in dark green; isc, ischium, in purple; mt, metacarpal, and all possible digit elements in light purple; ns, neural spine, in light yellow; pu, pubis, in light green; r, radius, in light green; ti, tibia, in khaki; u, ulna, in light blue; v, vertebral centrum, in dark gold. Bones in dark gray and gray, ribs of thalattosaur Xinpusaurus xingyiensis. Bones in black, ribs, and gastralia of ichthyosaur Guizhouichthyosaurus (XNGM-WS-50-R4). Scale bars, 25 cm in (A), 10 cm in (B and C), and 5 cm in (D).

The entire bromalite is about 74 cm long anteroposteriorly and contains a central part that bulges beyond the bedding plane by about 15 cm. The bulge is approximately 47 cm long anteroposteriorly and 19 cm wide dorsoventrally. These anatomical orientations are based on the ichthyosaur that contains the bromalite, not the prey. Bones in the bromalite show little indication of etching by the stomach acid (see Discussion), whereas those exposed along the left wall have been physically damaged, together with the surrounding matrix, probably by a taphonomic cause.

The bromalite contains two vertebral strings with 10 and 9 vertebrae, respectively (Figures 1B–1D). Some neural arch elements are found disarticulated and scattered on the dorsal side of the bulge, and some ribs are preserved in an approximate series along the vertebral column. At least 13 types of appendicular bones are identified in the bromalite with confidence: the clavicle, coracoid, humerus, ulna, radius, metacarpal, manual phalanges, ilium, ischium, pubis, femur, tibia, and fibula (Figures 1B and 1C). In addition, a suspected interclavicle is also present. Some manual elements are preserved in partial articulation (Figures 1B and 1C). Most of the bones are found in pairs of the right and left elements with matching shapes and sizes.

Prey Identity, Size, and Orientation

The prey is identified as the thalattosaur Xinpusaurus xingyiensis (Figure 2) based on close similarities of appendicular skeletal elements in both shape and size. The similarity is most characteristically seen in humeral morphology—it is a robust bone with a limited shaft constriction, and with an expanded proximal extremity (Figure 3A). The same morphology is found in the holotype of X. xingyiensis (Li et al., 2016) (Figure 3B) but not in any other marine reptiles of comparable sizes from the same locality or coeval localities nearby: the thalattosaur Anshunsaurus wushaensis has a humerus with a strongly constricted shaft and remarkable distal expansion (Figure 3C); eosauropterygians, such as Lariosaurus (Figure 3E) (Lin et al., 2017), Nothosaurus (Figure 3F) (Ji et al., 2014), and Yunguisaurus (Figure 3G) (Wang et al., 2019) have curved humeral shafts; the placodont Glyphoderma has a strongly constricted humerus (Figure 3D); and ichthyosaurs, such as Qianichthyosaurus (Figure 3H) (Yang et al., 2013) and Guizhouichthyosaurus (the present specimen), have humeri that are short and robust, with an anterior flange. Other bones also conform with the species identification. The femur is approximately rectangular and has a nearly straight distal end, as in X. xingyiensis (Li et al., 2016). The radius has an anterior flange, which is a character only seen in some thalattosauroids among thalattosaurs (Nicholls, 1999), including X. xingyiensis (Li et al., 2016). None of the bones in the bromalite shows features that contradict the species identification.



Figure 2. Body Configurations of the Predator and Prey in XNGM-WS-50-R4, when compared with XNGM-WS-53-R3

(A) Skeletal reconstruction of the predator, Guizhouichthyosaurus, in XNGM-WS-50-R4.

(B) Approximate skeletal map of the prey, Xinpusaurus xingyiensis, in XNGM-WS-50-R4.

(C) Skeletal reconstruction of the holotype of X. xingyiensis (XNGM-WS-53-R3).

(D) Photographic view of X. xingyiensis (XNGM-WS-53-R3) with distortion removed by orthographic stitching.

(E) A natural mold of an isolated tail of Xinpusaurus (XNGM-WS2011-50-R6) found 23 m away from XNGM-WS-50-R4, with the dorsal side facing below. Scale bars, 1 m for (A–C), 10 cm in (D), and 25 cm in (E).



Figure 3. The Humerus of the Prey in XNGM-WS-50-R4, when compared with Those of Marine Reptiles from the Same Locality, as well as Coeval Localities in the Vicinity

(A) Prey in XNGM-WS-50-R4.

(B) Xinpusaurus xingyiensis (XNGM-WS-53-R3).

(C) Anshunsaurus wushaensis (XNGM XY-2013-R2).

(D) Glyphoderma kangi (XNGM XY-2016-R2).

(E) Lariosaurus xingyiensis (XNGM-WS-30-R19).

(F) Nothosaurus youngi (XNGM-WS-30-R24).

(G) Yunguisaurus liae (XNGMXY-2013-R1).

(H) Qianichthyosaurus xingyiensis (XNGM-WS-46-R1). Scale bars in black are 2 cm.

The appendicular bones of the prey are about 1.34 times longer than corresponding elements of the holotype of X. xingyiensis (XNGM-WS-53-R3) based on the geometric means of bone lengths (Table 1). The holotype has a preserved length of 2.1 m, excluding half of the tail that is missing (Figure 2D). Using the body proportion of the holotype of Xinpusaurus suni, a congeneric species that is slightly younger than X. xingyiensis, the total length including the missing half of the tail was estimated to be greater than 3 m (Li et al., 2016) (Figure 2C). When multiplying this value by 1.34, the prey thalattosaur is estimated to be about 4 m in total length (Figure 2B). Unfortunately, the sample size of authentic congeneric skeletons is too limited to allow incorporation of allometry to this estimation process.

There is no evidence to suggest that more than one individual prey is in the stomach of the predator: the bromalite does not contain excess bones beyond the number expected in a reptile, while the right and left bones have nearly identical sizes. The bones preserve the original skeletal association, with pectoral elements found posteriorly in the bromalite, and pelvic elements anteriorly, with only two pectoral bones displaced anteriorly. Thus, the posterior side of the bromalite is craniad for the prey. The orientation of the ribs also matches this prey orientation.

The skull, mandible, and tail of the prey are unlikely to be present in the bromalite, given that no isolated elements from these body regions are mixed in with what is preserved. Also, there is insufficient space in the bromalite to hide these parts—for example, the skull of the holotype of X. xingyiensis, which is smaller than the prey individual, would occupy most of the bromalite volume.

Predator Morphology and Diet Suggested by Teeth

The body length of the predator skeleton along the vertebral column is about 4.80 m, after excluding the taphonomic gap in the neck. Although this is only 1.2 times that of the prey, body mass is expected to be roughly seven times greater in the predator because the body trunk diameter relative to body length is about 2.5 times greater—the prey is slender and elongated, whereas the predator is spindle shaped (Figure 2). It is an adult or at least young adult individual based on the degree of ossification of the humeral head (Johnson, 1977).

The teeth are well preserved in the closed mouth (Figure 4A). When considering that the gum reached the boundary between the crown and root of fully erupted teeth, parts of the teeth that were exposed in life were not tightly packed (Figure 4B). All teeth are almost uniformly conical and bluntly pointed, without cutting edges. The largest teeth are found in the posterior-most premaxillary and anterior-most maxillary regions (Figure 4B), among which the largest is 28.0 mm long and 15.8 mm wide at the base (crown height 15.6 mm, base width 9.4 mm). The relative tooth size index based on the tooth crown height relative to the skull width (about 20.4 cm) is about 0.086, and the tooth shape index is 1.51 based on the tooth crown height relative to the width.



Figure 4. Skull and Dentition of the Predator in XNGM-WS-50-R4

(A) The skull.

(B) Close-up of the dentition from the area with the red rectangle in (A) White broken line in (B) indicates an approximate position of the gum line for the upper jaw. Note that the tooth parts that are exposed beyond the gum line are small and not densely packed. Scale bars are 5 cm in (A) and 7 cm in (B).

Massare proposed that three characteristics of the dentition were correlated with prey preference of marine tetrapods, i.e., relative size to the skull width, crown aspect ratio, and tooth wear (Massare, 1987). The tooth size index places the present ichthyosaur in either the Crunch or Smash guild (collectively called grasping teeth). The crown shape index points to the Crunch guild, whereas the apices of the teeth, being unpolished and unbroken, suggest the Smash guild. In such cases of conflicting outcomes, Massare suggested that the relative tooth size and apex shape were more important than the crown shape index (Massare, 1987). Thus, the ichthyosaur belongs to the Smash guild. The teeth of this guild are “used for grasping fairly soft prey such as belemnoids and soft cephalopods” (Massare, 1987).

Isolated Tail

An isolated Xinpusaurus tail (XNGM-WS2011-50-R6) was found near the main specimen (XNGM-WS-50-R4). The generic identification is based on the morphology of mid-caudal centra—of the two thalattosaurs from coeval localities in the region, A. wushaensis has anteroposteriorly elongated mid-caudal centra, whereas these centra are slightly higher than long in X. xingyiensis, as in the present specimen. The tail is about 2 m long along the vertebral column, containing 96 to 97 vertebrae (Figure 2E). Given that Xinpusaurus has up to 100 caudal vertebrae (Liu, 2015), this caudal series should represent a nearly complete tail, probably missing the first few vertebrae. The centra are tightly articulated with each other, except the most anterior one that is preserved in an inclined posture.

Discussion

The main specimen (XNGM-WS-50-R4) likely represents the oldest direct record of megafaunal predation by marine tetrapods and also sets the record for the largest prey size of Mesozoic marine reptiles at 4 m (Table 2), which is larger than the previous record of 2.5 m (Everhart, 2004; Konishi et al., 2014). This statement disregards an uncertain estimation given in an unpublished dissertation, where a partial series of gastralia and a few vertebrae of a brachaucheniid pliosaur, presumably belonging to Kronosaurus based on its geologic setting (i.e., Lower Cretaceous of the Great Australian Basin), was reported in association with seven elasmosaurid vertebrae. The total length of this elasmosaurid was estimated to be 3.3 m based on the body proportion of an elasmosaurid species from the same basin but could be bloated up to 5.0 m if a longer-necked species from North America was used as the model. The fragmentary nature of the specimen obscures if the presumed prey was in the stomach of the postulated predator. Although fish prey are not included in Table 2, fish found in marine reptile bromalites have so far been smaller than 2.5 m in total length (Konishi et al., 2014). The comparisons here are limited to lengths because it is difficult to estimate body masses accurately based on flattened fossils.



Two questions arise concerning how the individual of Xinpusaurus found its way to the stomach of Guizhouichthyosaurus: was it by predation or scavenging, and, if the latter, were the head and tail detached by the scavenger or through postmortem decay? The answer to the second question is simpler than that for the first. Forensic taphonomy in the marine context has shown that hands and feet are the first to be detached through postmortem decay of human remains at sea, followed by the head and then more proximal parts of the limbs, whereas the vertebral column is the last to disintegrate, being strongly reinforced by extensive connective tissues that take time to decay (Haglund, 1993; Mason et al., 1996). This tendency is expected to have been exaggerated in Xinpusaurus, which likely used its body axis for propulsion, whereas its small limbs were used as rudders without a role of body support; appendicular connective tissues must have been limited relative to those along the axial skeleton, allowing faster decay. Then the presence of at least one manus and some pedal elements in the absence of the head and tail therefore cannot be explained very well by the decay hypothesis.

Possibilities of predation versus scavenging merit careful consideration. We conclude that predation is more likely than scavenging for the following reasons. First, marine carrion usually results from partial predation rather than deaths due to other causes (Barrett-Lennard et al., 2011; Britton and Morton, 2004). If a predator other than Guizhouichthyosaurus killed the thalattosaur in question, then it would be strange for the nutritious trunk and limbs to be left intact by the predator. Second, ingestion likely took place at the sea surface where Guizhouichthyosaurus was able to breathe because swallowing of a large food item would have taken a long time, whether the food was ingested in one or a few pieces. This would limit the possibilities of scavenging because marine scavenging usually occurs at the seafloor (Britton and Morton, 2004; Whitehead and Reeves, 2005)—marine carrion usually do not stay afloat at the surface (Haglund, 1993; Mason et al., 1996). In addition, the specimen is from the subtropical region of the warm Middle Triassic period, so the decomposition would have been rapid, further narrowing the window of time when carcass would have been available at the sea surface. Third, marine carrions are rare (Britton and Morton, 2004), especially that of megafauna available within the diving depth of typical air-breathing predators like killer whales (Whitehead and Reeves, 2005) and Guizhouichthyosaurus.

Even in the unlikely case of the present bromalite representing scavenged prey, X. xingyiensis would still be on the list of prey actively hunted by Guizhouichthyosaurus. Obligate scavenging by large animals is rare in modern marine ecosystems (Beasley et al., 2012; Wilson and Wolkovich, 2011), instead, marine scavenging is almost always facultative (Britton and Morton, 2004; Hammerschlag et al., 2016). Modern megapredators, such as the great white shark (Carcharodon carcharias) (Tucker et al., 2019), tiger shark (Galeocerado cuvier) (Hammerschlag et al., 2016), and killer whale (O. orca) (Whitehead and Reeves, 2005), are known to scavenge when given opportunities, but they tend to scavenge the carrion of the species that they also hunt. The carrion that they scavenge is derived from predation by the same or another individual, unless it is human caused (Britton and Morton, 2004).

The isolated tail specimen (XNGM-WS2011-50-R6) also supports the predation hypothesis. The specimen witnesses, whether it belonged to the prey individual in the bromalite or not, that there was a mechanism to detach the tail of a large thalattosaur while it was intact—decay was probably not involved because the distal part of the tail is still articulated, whereas decay would have detached that region first because there is less connective tissue there. The specimen instead shows that the most proximal vertebra, which would be the last to decay, is halfway detached (Figure 2E). External forces would be necessary to cause such detachment, and it is difficult to find a source outside of a predator. Thus, there was at least a predator that could hunt Xinpusaurus, whereas Guizhouichthyosaurus was the only species larger than the prey in this and coeval localities in the region.

Circumstantial evidence suggests that the isolated tail belongs to the prey individual in the bromalite. The tail was only 23 m away from the ichthyosaur specimen on the same rock surface and has a size and completeness that are expected for the lost tail of the prey in the bromalite. Also, as stated above, its preservation suggests that the tail was detached from the body while it was intact. If it is from the prey individual, the predator likely died soon after ingesting the prey, and that may explain the lack of etching of the bone in the bromalite by the stomach acid, as well as the strange detachment of the neck of the predator. Unfortunately, it is impossible to test this hypothesis directly so a clear conclusion cannot be drawn on this issue.

The mechanism that the ichthyosaur would have used to remove the head and tail of the thalattosaur before ingestion is not directly recorded in the fossil. However, it most likely employed the “grip and tear” strategy, which is the only method used by extant aquatic megapredators to separate the prey into pieces (Hocking et al., 2017). In this method, the prey is torn apart by a combination of the physical inertia of the prey's body and torsion applied by the predator's jaws through jerking and twisting while holding a part of the prey in the jaws. The method is used by the killer whale and leopard seal among marine mammals (Hocking et al., 2017), and crocodiles among reptiles (Ng and Mendyk, 2012; Pooley and Gans, 1976). Bottlenose dolphins are also known to use similar behaviors to tear prey (Sprogis et al., 2017), although they are not megapredators. None of these predators use cutting teeth when tearing the prey, i.e., the leopard seal uses the canine and peg-like incisors but not the carnassial, whereas others lack cutting teeth. The teeth of Guizhouichthyosaurus are robust and not especially large for the skull width, as in crocodiles that employ the “grip and tear” strategy. The ichthyosaur may have lacked the strong pterygoideus muscle typical of crocodiles, but its myology is too poorly understood to enable a fruitful discussion of muscular force that held down the prey. Also, the bite force of Guizhouichthyosaurus is expected to be large by virtue of size alone—simple isometric geometry suggests that the bite force would quadruple when the body length is doubled, and the observed increase of bite force with size in Alligator is even greater (Erickson et al., 2003). The fact that the prey vertebral column is broken into strings suggests that Guizhouichthyosaurus indeed had bite force needed for that task. About 40 vertebrae are expected be present in the bromalite, judging from the typical vertebral counts of Xinpusaurus (Liu, 2015). Given that the vertebrae in the bromalite are found in strings of about 10 each, it is likely that the prey was swallowed in one to about four pieces. It is possible that the prey's trunk was in one piece with the vertebral column broken into three to four strings inside because the distance between the overlapping parts of the two vertebral strings in Figure 1D is as short as 1.5 cm—it would be difficult to pack them that closely if the strings had been swallowed as parts of difference pieces, with each string surrounded by connective tissues that would prevent them from lying closely together. The observed arrangements may instead be reached by swallowing a single mass of connective tissues with the vertebral column broken into strings inside, the vertebral strings may shift and overlap partly as the mass was pushed into the digestive system. This would be especially the case if the time between ingestion and predator's death is short, not leaving much time for digestion.

Ingestion of the prey may have been aided by a combination of inertial feeding and placement of the prey above the water to utilize gravity with least counteraction from buoyancy (Gans, 1969; Hocking et al., 2017). The use of gravity to aid ingestion is known among marine mammals (Hocking et al., 2017), as well as terrestrial ingestion of large prey by Varanus (Editorial, 2018). The throat and neck muscles of ichthyosaurs are poorly understood, so it is difficult to judge how these muscles could aid in ingestion of large prey pieces. Ichthyosaurs lack cranial and mandibular kinesis that allows some modern reptiles to swallow large prey, but it is evident from the bromalite contents that the ichthyosaur predator could let the prey pass through the intermandibular space even without such kinesis. The shoulder girdle of Guizhouichthyosaurus is small relative to the body, unlike in basal ichthyopterygians or mixosaurs, leaving the front side of the rib cage widely open without bony obstruction. This may have helped allow passage of large prey pieces into the digestive system.

As described earlier, three characteristics of the dentition suggest that the Guizhouichthyosaurus specimen belonged to the Smash feeding guild, whose members prey on soft cephalopods (Massare, 1987). In contrast, the bromalite reveals that its diet included large marine reptiles. The widely used tooth-based diet estimation scheme (Massare, 1987) captures the majority trend well, but taxa that are not fully accounted for have been noted before (Konishi et al., 2011; Motani, 1997, 1996; Pierce et al., 2009). Two of these counterexamples concerned taxa with grasping teeth, and the present case adds to the list. Therefore, the tooth-based scheme may underestimate the extent of megafaunal predation by marine tetrapods as suspected before.

Although grasping by teeth is typically thought to be effective when feeding on cephalopods and fish, it also constitutes an effective mechanism when feeding on air-breathing prey in water. The predator can grasp the prey in the mouth and hold it underwater until it weakens through the lack of oxygen, as seen in the hunting strategy of some crocodiles (Ng and Mendyk, 2012). The prey runs out of oxygen before the predator because it struggles to escape while the predator stays still. Moreover, scaling effects help the predator because heavier tetrapods tend to be able to hold their breath longer (Stephens et al., 2008). Once the prey weakens, the predator can start the process of prey size reduction and ingestion without much resistance from the prey, taking advantage of the gravity above water and inertia in water (Gans, 1969; Hocking et al., 2017). Therefore, there may have been more megapredators with grasping teeth than currently recognized. Candidates include two ichthyosaur genera from the Illyrian (Anisian, Middle Triassic) with grasping teeth and slightly larger body sizes than Guizhouichthyosaurus: Besanosaurus (Dal Sasso and Pinna, 1996), a monotypic genus that belongs to Shastasauridae (as does Guizhouichthyosaurus, Ji et al., 2016), and Cymbospondylus (Merriam, 1908).

Besanosaurus has a small skull and teeth for the body with a slender snout and has hitherto been considered a cephalopod feeder (Dal Sasso and Pinna, 1996). However, its skull is large enough to hold a coeval ichthyosaur, such as Mixosaurus cornalianus Type B (Brinkmann, 1998a, 1998b) and Mixosaurus. kuhnschnyderi (Brinkmann, 1998a, 1998b). The type specimen contains isolated ichthyosaur vertebrae that were originally interpreted as embryonic remains (Dal Sasso and Pinna, 1996). Although this interpretation may be correct, it is possible that the vertebrae represent parts of a prey Mixosaurus because the vertebral centra are too well developed for an embryo of the developmental stage indicated by their size: the centra are fully developed without a notochordal pit in the middle, whereas they are between 55% and 75% of the expected terminal size (i.e., the longest vertebrae are about 13% of the longest adult vertebrae, when newborn ichthyosaurs are about 18%–23% of adult lengths, Motani et al., 2014; O'Keefe and Chiappe, 2011).

Currently, the cymbospondylid Thalattoarchon from the Illyrian (about 243–242 million years ago), known only from a partial skull, is considered the first marine tetrapod megapredator based on tooth morphology and an estimated body size (Frobisch et al., 2013). However, it is now likely that megafaunal predation by marine tetrapods started almost simultaneously at least among three genera within Cymbospondylidae and Shastasauridae during the Illyrian. Starting from small predators with a variety of diet and feeding styles (Cheng et al., 2019; Motani et al., 2015a, 2015b; Rieppel, 1998) in the Olenekian (Motani et al., 2017), Mesozoic marine tetrapods gave rise to multiple megapredators in about 7 million years, as rebuilding of biodiversity after the end-Permian mass extinction neared its completion (Chen and Benton, 2012).

Limitations of the Study

The data for the present study are limited to what have been preserved in fossils. Inferences were made by interpreting such data in the context of modern anatomy, ecology, and taphonomy. As such, whereas the conclusions given represent most likely interpretations, they are not definitive.

Resource Availability

Lead Contact
Further information and requests for resources should be directed to and will be fulfilled by the Lead Contact, Ryosuke Motani ([e-mail]).

Materials Availability
The specimen studied is accessioned at the Xingyi National Geopark Museum, Xingyi City, Guizhou Province, China, with an accession number XNGM-WS-53-R4. It is presently on display for public viewing.

Data and Code Availability
All data used in the study are included in this publication. The present research did not use any new codes.

Methods
All methods can be found in the accompanying Transparent Methods supplemental file.

Supplemental Information

Document S1. Transparent Methods

REFERENCES

Check LINK above.

[Life]

Research article: 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.

Citation: Fröbisch, N. B., Fröbisch, J., Sander, P. M., Schmitz, L., & Rieppel, O. (2013). Macropredatory ichthyosaur from the Middle Triassic and the origin of modern trophic networks. Proceedings of the National Academy of Sciences, 110(4), 1393-1397.

LINK: www.pnas.org/content/110/4/1393.short

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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 8My 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. Horizon and Locality. FMNHPR3032 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 ± 0.36Ma (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).

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. 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.]

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).



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.)

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 13My 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.



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.

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.

ACKNOWLEDGMENTS. Jim Holstein discovered the fossil during a field expedition led by Martin Sander and Olivier Rieppel in 1997. Nicole Klein and Olaf Dülfer helped excavate the fossil. Akiko Shinya, Deborah Wagner, Constance van Beek, Jim Holstein, and Lisa Herzog prepared the fossil together with Field Museum volunteers. John Weinberg took the photographs of the fossil, and Georg Oleschinski contributed to the illustrations. Philipp Gingerich, Ryosuke Motani, and Johannes Müller read earlier versions of the manuscript, and Geerat Vermeij provided insightful comments in discussions with L.S. Two anonymous reviewers and the editor provided useful suggestions. 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 for Research and Exploration) Grants 6039-97 and 8385-08, The Field Museum of Natural History, and the University of Bonn.

Data supplements

Supporting Information

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[Life]

Research article: The status of Himalayasaurus tibetensis (Ichthyopterygia)

Abstract

A reexamination of the type specimen of Himalayasaurus tibetewis reveals that the bone previously identified as a coracoid is more likely a radius. This bone clearly shows a synapomorphy of the Shastasaurinae, which confirms a shastasaurid affinity previously proposed for the species. H. tibetensis is diagnostic for having remarkable cutting-edges on its flattened tooth crowns, which is otherwise unknown for ichthyopterygians. Himalayasaurus is among the largest ichthyopterygians known, rivaling the closely related Shonisaurus.

Citation: Motani, R., Manabe, M., & Dong, Z. M. (1999). The status of Himalayasaurus tibetensis (Ichthyopterygia). Paludicola, 2(2), 174-181.

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INTRODUCTION

Himalayasaurus tibetensis was originally described based on a partial skull and some associated postcranial elements (Dong, 1972). This Norian (Upper Triassic) species is comparable in size to the slightly older Shonisaurus from the Carnian (Upper Triassic) of Nevada, which is one of the largest ichthyopterygians thus far reported (Camp, 1980; Kosch, 1990; McGowan, 1991, 1996; McGowan and Montani, 1999). This is the youngest of the three ichthyopterygian genera reported from China (Young, 1965; Young and Dong, 1972; Callaway and Massare, 1989a; Montani and You, 1998). Dong (1972) suggested a shastasaurid affinity for H. tibetensis, but poor preservation prevented further testing of this hypothesis. Also, the relationships among various ichthyopterygians were poorly understood at that time, which made a phylogenetic study of H. tibetensis difficult.

Callaway (1989) ws the first to propose a phylogenetic hypothesis that included Himalayasaurus. A generally accepted assumption of the time was that the so-called "Shastasauridae", which always contained Shastasaurus, Californosaurus, and Merriamia (now considered Toretocnemus; see Montani, in press), formed a natural group. This view, initiated by Merriam (1902, 1908), was followed by most reviewers (e.g., Kuhn, 1934; von Huene, 1951,1956; Mazin, 1982; Kirton, 1983; Callaway, 1989; Dal Sasso and Pinna, 1996), although they variously included some or all of the following taxa in the Shastasauridae in addition to the three core genera listed above: Pessosaurus, Cymbospondylus, Besanosaurus, Shonisaurus, and Himalayasaurus. With this assumed monophyly, Callaway (1989) analyzed a data matrix with 33 characters coded for seven "Shastasauridae", plus Grippia and Petrolacosaurus as the outgroup. He found a single most parsimonious tree in which Himalayasaurus was the basal taxon of the subclade Shastasaurinae (Figure 1A), whose sister taxon was Shonisaurus (Callaway, 1989). Dal Sasso and Pinna (1996) reanalyzed Callaway's (1989) data matrix by adding Besanosaurus and obtained six most parsimonious trees. They figured one of the six, which suggested that Himalayasaurus and Shonisaurus might form a clade of their own (Figure IB). Montani (in press) recently proposed a more comprehensive phylogenetic hypothesis for ichthyopterygians by analyzing a data matrix with 104 characters coded for 27 better known ichthyopterygians and five outgroups. Based on the strict consensus of 12 most parsimonious trees, he found that the "Shastasauridae" was not monophyletic as traditionally assumed (Motani, in press); Californosaurus and Toretocnemus, two of the three core taxa, were more closely related to parvipelvians than to Shastasaurus (Figure 1C). Motani (in press) did not include Himalayasaurus in his analysis because the genus was too poorly known at the time.

A recent reexamination of the type specimen of Himalayasaurus tibetensis revealed several anatomical features that are phylogenetically informative. The purpose of the present contribution is to reevaluate the phylogenetic relationships of this species based on the new knowledge.



FIGURE 1. A, Phylogenetic hypothesis proposed by Callaway (1989) for the traditional Shastasauridae. B, Phylogenetic hypothesis proposed by Dal Sasso and Pinna (1996) for the traditional Shastasauridae. C, Simplified phylogeny of the Ichthyopterygia based on Motani (in press). Black dots indicate node groups, and brackets stem groups. Three of the clades are represented by reversed triangle to save space, with the name of a typical constituent genus attached to each. Taxa with asterisks had been included in the Shastasauridae by at least one author, and those with double asterisks are the three core taxa of the traditional Shastasauridae mentioned in the text. Himalayasaurus is connected to the cladogram by a dotted line because the genus is poorly known. See text for the discussion of the phylogenetic position of the genus.

MATERIALS AND METHODS

The type and only specimen of Himalayasaurus tibetensis is stored at the Institute of Vertebrate Paleontology and Palaeoanthropology, Academia Sinica, China (IVPP V4003). The specimen comprises of five parts: IVPP V4003-1 (a slab with a partial skull and vertebrae), V4003-2 (fin element), V4003-3 and -4 (caudal vertebrae?) and V4003-5 (radius). It was not possible to examine V4003-3 and -4 in the present study. Comparisons were made with shastasaurian specimens stored at Berlin Ichthyosaur State Park, Nevada (BISP); the Marjorie Barrick Museum of Natural History, University of Nevada at Las Vegas (FZVE); the Royal Ontario Museum, Toronto, Canada (ROM); and the University of California Museum of Paleontology, Berkeley (UCMP).

Measurements less than 145 mm were taken using dial calipers and recorded to the nearest 0.1 mm. A plastic tape measure was used for larger measurements for Himalayasaurus, which were recorded to the nearest 10 mm. Larger measurements for Shonisaurus were made with large Vernier calipers and recorded to the nearest millimeter.

The range for the relative length of cervical vertebral centra was obtained in the following manner. Triassic ichthyosaurians has long necks (Massare ad Callaway, 1990), so the ratio between the maximum diameter of each centrum and its length was calculated for the first ten centra of each specimen, and the range of this MD/L ratio was listed. However, all ten centra were not always measurable with confidence, in which case the range was given based on a subset of the ten centra (those that were measurable).

Higher taxonomic names within the Ichthyopterygia follow Motani (in press). A phylogenetic tree with these names is provided as Figure 1. It should be noted that the names Shastasauridae and Shastasaurinae are differently defined from the traditional usage mentioned in the introduction.

SYSTEMATIC PALEONTOLOGY

Subclass Diapsida Osborn, 1903
OrdeC|?hthyosamia Je Blainville, 182S> ^ >
Suborderichthyopterygia Owen, 1840 ^
Family Shastasauridae Merriam, 1902
Subfamily Shastasaurinae Merriam, 1908
Genus Himalayasaurus Dong, 1972

Type and Only Species-Himalayasaurus tibetensis Dong, 1972.

Diagnosis—Large shastasaurian probably exceeding 15 m in total length; tooth crowns labiolingually flattened, with remarkable cutting edges on mesial and distal sides giving swollen outline in labiolingual view; radial shaft not reduced posteriorly and absent anteriorly; cervical vetebral centra short, with Width/Length ratio near 3.0.

Locality and Horizon—Upper Triassic (Norian) of Tibet.

Himalayasaurus tibetensis Dong, 1972.

Type and Only Specimen-IVPP V4003.

Diagnosis—As for genus.

Description-Radius: IVPP V4003-5 (Figure 2A), previously identified as a coracoid (Dong, 1972), is herein identified as a radius, because the outline of the bone is very similar to those of the shastasaurine radii (Figure 2) than to any ichthyopterygian coracoids. The bone is thicker proximally (87.2 mm) than distally (76.4 mm), and the decrease of the thickness is gradual between the two ends, as in most fin elements of Shonisaurus (McGowan and Motani, 1999). The distal margin of the bone is posteriorly curved (Figure 2A, bracket), where it forms a second, small facet. This area is much thinner (44.8 mm) than the main part of the distal end (76.4 mm), so the second facet is remarkably smaller than the distal facet. Such a small posterodistal facet is known for shastasaurine radii, in which it articulates with the ulna (Figure 2D-F).

The anterior margin is thin (26.0 mm), smooth, and convex without a notch. There is a wedge-shaped incision near the position where notches would occur in merriamosaurian radii (Figure 2A, arrow), but this is clearly a break: there is no thickening of the area that is usually associated with true notches. Surface striations are radial anteriorly, suggesting the loss of the plesiomorphic shaft in this area. The posterior margin is concave and the surface striations are parallel to the margin, so the plesiomorphic shaft is probably retained on this side of the bone. The co-occurrence of the complete loss of the radial shaft anteriorly and the complete retention posteriorly is unique to some shastasaurines, such as Shonisaurus and Shastasaurus neoscapularis (McGowan, 1994; Motani, 1999).

IVPP V4003-5 is wider (295 mm) than long (275 mm), as in most shastasaurine radii (one of the radii referred to Shonisaurus is longer than wide, probably because of distortion; Figure 2). It is also larger than any of the measured Shonisaurus radii (Table 1), but the difference is not remarkable.

Although the outline of IVPP V4003-5 may resemble those of some euichthyosaurian coracoids, the bone lacks a typical feature of those coracoids: the presence of both scapular and glenoid facets. The above mentioned posterodiastal facet is too small to be either of the facets.



FIGURE 2. Radius and other forefin elements of shastasaurines. A, radius of Himalayasaurus tibetensis (TVPP V4003-5). Bracket indicates a smallposterodistal facet Vertical stripes indicate the break mentioned in text B-C, radii of Shonisaurus (modified from Camp, 1980). D, forefin of Shonisaurus (after McGowan and Motani, 1999). E, forefin of Shastasaurus (modified from Callaway and Massare, 1989b). F, forefin of Shastasaurus neoscapularis (modified from McGowan, 1994). Scale bar in A is 10 cm. B-F are laterally inverted for ease of comparison, and are not to scale.

Fin element: IVPP V4003-2 (Figure 3) was previously identified as a vertebral centrum. The outline of the bone is indeed very similar to that of a typical euichthyosaurian caudal centrum, which seems to support this identification. However, two features of the bone suggest otherwise. First of all, the bone is not amphiceolous, unlike ichthyopterygian vertebral centra. Second, the thickness distribution suggests that the supposed bilateral symmetry (Figure 3D) does not exist: the axis of bilateral symmetry, if any, should be as in Figure 3C. Moreover, a close inspection reveals that a slightly concave profile of the supposed dorsal margin of the bone is formed by unprepared matrix (Figure 3D, white area). Therefore, the interpretation given in Figure 3C is more reasonable than the one in Figure 3D. The thickness decreases gradually from the top of Figure 3B to the bottom (Figure 3 A), and such a uniform decrease in thickness it typical of fin elements (McGowan and Motani, 1999). We conclude that IVPP V4003-2 is more likely a fin element than a vertebral centrum.

It is difficult to specify the position of this element within a fin, or whether it belongs to a forefin or hindfin. The element is not notched as in the leading-edge elements of the forefin of the Shastasaurinae, or widened as in digit-IV elements. It is possibly a digit-V element for these reasons, but too little is known about digit V of the Shastasaurinae to test this identification further. The relative size of the element with respect to the radius suggests that the element was not very distal within a fin, judging from the only articulated forefin of the Shastasaurinae, Shastasaurus neoscapularis (ROM 41993; Figure 2F).

Skull and mandible—A, very fragmentary and unprepared skull and mandible are preserved in IVPP V4003-1 (Figure 4C). At least two jaw rami are preserved, but it is difficult to judge (with confidence) whether they are derived from the upper or lower jaws. Therefore, the description will be given according to a tentative identification given in Figure 4C, which is based on the general distribution of bones. At least two vertebral centra are preserved near the dentigerous bones (Figure 4C), so it is likely that the specimen underwent disturbance during preservation.

The dentary is far from complete: only a part of dentigerous region is preserved. Fourteen better-preserved tooth positions can be confirmed over 680 mm, with less conspicuous ones preserved both anteriorly and posteriorly, making the total preserved count of 16. The ninth position is associated with a nearly complete tooth (Figure 4), but others are empty. There is a structure that appears to be a coronoid process in the posterior part of the bone, but this is probably unprepared matrix (Figure 4C, matrix): if this were a bony process, it would dorsally close the last four tooth positions.

There is a partially exposed tooth crown that points in the opposite direction to the one on the dentary, so the bone associated with this tooth crown is tentatively identified as a part of the upper jaw, rather than the other mandibular ramus. The upper jaw is less well preserved than the lower one. Nine tooth positions can be seen posteriorly (Figure 4C), but this jaw ramus is not well exposed anteriorly where the tooth just mentioned is located.



FIGURE 3. A fin element of Himalayasaurus tibetensis (TVPP V4003-2). A, horizontal view from the diredtion indicated by arrow in B. White area on theleft is plaster. B, planar view. C-D, two competing interpretations for the bilateral symmetry of the elements, with distribution of the thickness of the bone for four corners. The element was previously identified as a caudal vertebra. See text for explanation. Scale bar is 10 cm.

Dentition: Most characteristic of Himalayasaurus tibetensis is its dentition, especially the tooth crowns. Only one tooth that is well exposed in IVPP V4003-1, in association with the dentary. The crown looks like a thick dagger blade; it is labiolingually compressed and its cutting edges are remarkably well developed both mesially and distally (Figure 4A, B). Coarse and deep longitudinal striations run along the surface of the crown especially proximally. The pattern of enamel crystals can be observed with the naked eye on the surface, and these are elongated nearly perpendicular to the mesial and distal margins of the crown. The root is also coarsely striated, but it is not possible to judge whether this is because of folding of the dentine wall. The boundary between the crown and root is located at the level of the dentigerous margin of the dentary, so the gumline was probably not very high above this margin (only basal ichthyopterygians have high gum lines).

The entire tooth is 133.0 mm long, of which 59.7 mm is the crown. The crown appears more prominent than the root in labiolingual view: the maximum distomesial width of the tooth is 39.5 mm, for the swollen part of the crown, whereas the minimum for the constricted part of the root is 33.4 mm. This is unlike any other ichthyopterygians (see Massare, 1987): crowns are never larger than the roots. A labiolingaully compressed crown is not unique to Himalayasaurus. For example, Temnodontosaurus is occasionally known to have labiolingually compressed tooth crowns (thus the name of the type species T. platyodori), although such teeth are not necessarily persent in all individuals (McGowan, 1974; 1979; Massare, 1987).

Tooth implantation is difficult to establish. A bony fixation between the root and dentigerous bone cannot be established with confidence. Tooth positions are separated by ridges developed on dentigerous bones (Figure 4C), as in aulacodont ichthyosaurs such as Leptonectes tenuirostris. However, because of the incompleteness of the specimen, it is possible that these ridges may actually represent the remains of bony septa of thecodont or ankylothecodont tooth implantation that has been broken during preservation. In Shonisaurus, the teeth are set in separate sockets but the septa between sockets are thin (FZVE-C; reported as unnumbered by McGowan and Motani, 1999). Such thin walls of bone, even if they existed in life, are unlikely to be preserved in IVPP V4003-1, considering that dentigerous bones are halfway eroded in this specimen. It is also possible that the tooth implantation was subthecodont: it is inevitable that the dentary of Utatsusaurus would show similar interdental ridges once the teeth were removed (see Montani, 1996:fig. 3C). In short, the tooth implantation in Himalayasaurus could be any of the four types known for ichthyopterygians (Motani, 1997).



TABLE 1. Size comparison between Himalayasaurus and Shonisaurus. The width of the radius was measured at the distal part of the bone. The widths of the vertebral centra do not include parapophyses or diapophyses. The diameter of the tooth root in Shonisaurus is based on the maximum diameter of four dental sockets, which should be an overestimation of the true value. The same for Himalayasaurus is based on the narrowest part of the root of the only exposed tooth, which should be a slight underestimation of the thickest part. McGowan and Motani (1999) refer BISP 1 to Camp's (1980) Specimen D, but this was a mistake made by RM. Asterisks indicate derivation from Camp (1980).



FIGURE 4. The main slab of the holotype of Himalayasaurus tibetensis (IVPP V4003-1). A, only complete tooth in the specimen in labio-lingual view. Compare with B to see that the cutting edges are extremely well developed for an ichthyopterygian. B, same from slightly anterior direction. C, middle part of the slab. Anterior to the left. Unlabeled bones are not identifiable. Scale bars are 10 cm.

(Figure 4C), as in aulacodont ichthyosaurs such as Leptonectes tenuirostris. However, because of the incompleteness of the specimen, it is possible that these ridges may actually represent the remains of bony septa of thecodont or ankylothecodont tooth implantation that has been broken during preservation. In Shonisaurus, the teeth are set in separate sockets but the septa between sockets are thin (FZVE-C; reported as unnumbered by McGowan and Motani, 1999). Such thin walls of bone, even if they existed in life, are unlikely to be preserved in IVPP V4003-1, considering that dentigerous bones are halfway eroded in this specimen. It is also possible that the tooth implantation was subthecodont: it is inevitable that the dentary of Utatsusaurus would show similar interdental ridges once the teeth were removed (see Montani, 1996:fig. 3C). In short, the tooth implantation in Himalayasaurus could be any of the four types known for ichthyopterygians (Motani, 1997).

Vertebrae: One of the vertebral centra preserved in IVPP V4003-1 is sufficiently exposed. It has been removed from its life position, being associated wit the dentigerous part of the jaw. The centrum is 220 mm wide, 160 mm high, and 75 mm long. Because the centrum is wider than high, it is probably derived form the mid-cervical region. Preservation is too poor to elaborate on the identification.

DISCUSSION

Lucas and Gonzales-Leon (1995:fig. 4) and Lucas (1997:fig. 3) considered Himalayasaurus tibetensis a nomen dubium. Although they provided no discussion of this designation, their views are understandable considering the incompleteness of the type and only specimen (IVPP 4003). However, the species is unique among ichthyopterygians in having teeth with remarkably well developed crowns. Furthermore, diagnostic features of the postcranial elements enable the phylogenetic discussion of the species as given below. In light of the new knowledge provided in the present contribution, we conclude that the species is diagnostic and valid.

It is most likely that Himalayasaurus is closely related to shastasaurines, judging from the shape of the radius. Three features of the bone are particularly important: (1) the plesiomorphic shaft of the radius is completely lost or extremely reduced anteriorly (apomorphic within ichthyopterygians); (2) the plesiomorphic shaft is not reduced posteriorly (plesiomorphic for ichthyopterygians); and (3) the radius is wider than long (apomorphic within ichthyopterygians). Features 1 and 3 convergently occur in the Shastasaurinae and Parvipelvia (Figure 1), but feature 2 is primitively lost in the latter group (Motani, 1999, in press). Therefore, it is most likely that Himalayasaurus is closely related to the Shastasaurinae.

The next question is whether Himalayasaurus is the sister group of the Shastasaurinae or is nested within it. Only one feature is available to assess this question: the relative length of cervical vertebral centra. The only measurable cervical centrum of Himalayasaurus is much shorter than wide, with the Maximum Diameter/Length ratio of 2.93. Such short cervical centra are typical of Shonisaurus (MD/L = 3.19-3.23 for BISP Specimen 1; see Materials and Methods of the calculation of the range), whereas Shastasaurus has much longer cervical centra (DM/L = 1.90-2.17 for UCMP 9076). Cervical centra are not short in the outgroup, including Mixosaurus (MD/L = 1.56-1.68) and Californosaurus (MD/L = 1.67-2.05), so the shortened cervical central seem to be apomorphic within the Shastasaurinae (measurements unavailable for Besanosaurus). Given the absence of any opposing features, we conclude that it is most reasonable to consider shortened cervical centra as a synapomorphy of Himalayasaurus and Shonisaurus. Therefore, Himalayasaurus is probably more closely related to Shonisaurus than to Shastasaurus, a suggested in Figure 1 (dotted line). This conclusion accords with that of Dal Sasso and Pinna (1996), and is very close to Callaway's (1989) phylogenetic hypothesis. Nevertheless, it is desirable to obtain more data on Himalayasaurus in the future to test the present hypothesis: the shortness of the cervical centra may be related to large body size of the two genera.

Himalayasaurus was probably comparable to Shonisaurus in size. McGowan and Motani (1999) gave an estimated total length of 14.5 m for the most complete skeleton of Shonisaurus (BISP 1) which is close to what was estimated by Camp (1980) and Kosch (1990). Individuals larger than BISP 1 are known for Shonisaurus, being represented by incomplete material (McGowan and Motani, 1999). Himalayasaurus (IVPP V4003) is larger than BISP 1 in vertebral measurement, but not by more than 10% (Table 1). Therefore, Himalayasaurus was probably within the size range of Shonisaurus, assuming similar body proportions for the two closely related genera. The large size and extensive cutting edges of the teeth in H. tibetensis suggest that large vertebrates were probably among its prey items, as McGowan (1974) and Massare (1987) suggested for some large Jurassic ichthyosaurs.

The similarities between Himalayasaurus tibetensis and Shonisaurus popularis, as pointed out above, raise the question whether the two, given the limited material of H. tibetensis, are congeneric. The only difference between the two is the shape of the tooth crown, but this features alone does not warrant a separate generic status. If the two species are considered congeneric, the name Himalayasaurus Dong, 1972 has priority over Shonisaurus Camp, 1976. However, it is also possible that the two species are considerably different in the region of the body that is unpreserved in H. tibetensis. Considering the poor preservation of H. tibetensis, we remain conservative and keep the two species in separate genera.

ACKNOWLEDGMENTS

We are grateful to J. Lu of assistance as IVPP. We thank E. L. Nicholls for discussions with RM at IVPP. C. McGowan gave permission to use the data on Shonisaurus collected by him and RM at UNLV an BISP. K. Padian and J. Massare read the earlier version of the manuscript and provided useful comments. This project was supported by an International Reserch Grant-in-aid to MM (No. 09041168) form the Ministry of Education of Japan, and a fellowship from the Miller Institute for Basic Research in Science, University of California, Berkeley to RM. Last but not least, we would like to express our admiration of Jack Callaway's contributions to the field, especially for reviving the study of Triassic ichthyosaurs. RM is very grateful to Jack for the kindness and friendship he showed to a young newcomer to the field of ichthyosaurian paleontology.

LITERATURE CITED

Blainville, H. M. D. de. 1835. Description de quelques especes de reptiles del la Californie. Nouvelles Annales du Museum d'Histoire Naturelle, Paris 4:233-296.

Callaway, J. M. 1989. Systematics, phylogeny, and ancestry of Triassic ichthyosaurs. Unpublished PhD dissertation, University of Rochester, 204 pp.

Callaway, J. M. and J. A. Massare. 1989a. Geographic and stratigraphic distribution of the Triassic Ichthyosauria (Reptilia; Diapsida). Neues Jahrbuch fur Geologic und Palaontologie, Abhandlungen 178:37-58.

Callaway, J. M. and J. A. Massare. 1989b. Shastasaurus altispinus (Ichthyosauria, Shastasauride) from the Upper Triassic of the El Antimonio district, northwestern Sonora, Mexico. Journal of Paleontology 63:930-939.

Camp, C. L. 1976. Vorlaufige Mittelung iiber grosse Ichthyosaurier aus der oberen Trias von Nevada. Osterische Akademie der Wissenschaften, Mathematisch-naturwissen schaftliche Klasse, Sitzungsberichte, Abteilung 1,185:125-134.

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Dong, Z.-M. 1972. An ichthyosaur fossil from the Qomolangma Feng region. Pp. 7-10 in C. C.

Young and Z.-M. Dong (eds.) Aquatic reptiles from the Triassic of China. Academia Sinica, Institute of Vertebrate Paleontology and Palaeoanthropology, Memoir 9, Peking. [in Chinese]

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Reconstruction of H. tibetensis

[Life]

Research Article: Giant Late Triassic ichthyosaurs from the Kössen Formation of the Swiss Alps and their paleobiological implications

ABSTRACT

The Late Triassic was populated by the largest ichthyosaurs known to date, reaching lengths of over 20 m. Recent discoveries include the remains of giant ichthyosaurs from the Austroalpine nappes of the eastern Swiss Alps. The finds come from the lower two members of the Kössen Formation (late Norian to Rhaetian). The material consists of a very large tooth lacking most of the crown from the Rhaetian Schesaplana Member, a postcranial bone association of one very large vertebra and ten rib fragments also from the Schesaplana Member, and an association of seven very large vertebral centra from the upper Norian to lower Rhaetian Alplihorn Member. These associations represent the only published partial skeletons of large to giant ichthyosaurs younger than middle Norian. We compare the material with the two largest ichthyosaurs known from partial skeletons, Shonisaurus popularis (15 m) and Shastasaurus sikkanniensis (21 m) from the late Carnian (ca. 230 Ma) of Nevada and the middle Norian (ca. 218 Ma) of British Columbia, respectively. The incomplete tooth confirms that at least some giant ichthyosaurs had teeth. Based on their proportional differences, the two bone associations may represent two different taxa of Shastasaurus-like ichthyosaurs. The larger and geologically younger specimen may have been nearly the size of S. sikkanniensis, and the smaller that of S. popularis. These giant ichthyosaurs from the eastern Swiss Alps indicate that such ichthyosaurs also colonized the western Tethys. The finds also unequivocally document that giant ichthyosaurs persisted to the latest Triassic.

Citation: Martin Sander, P., Pérez De Villar, P. R., Furrer, H., & Wintrich, T. (2022). Giant Late Triassic ichthyosaurs from the Kössen Formation of the Swiss Alps and their paleobiological implications. Journal of Vertebrate Paleontology, 41(6), e2046017.

Link: www.tandfonline.com/doi/abs/10.1080/02724634.2021.2046017

[Life]

Research article: Grouping behavior in a Triassic marine apex predator

Highlights

• Abundant fossils from Nevada reflect aggregations of a predatory marine reptile
  
• Nearly all individuals are large adults apart from multiple embryos or neonates
• No evidence for significant environmental perturbation is found

Summary

Marine tetrapods occupy important roles in modern marine ecosystems and often gather in large aggregations driven by patchy prey distribution,^1,2 social or reproductive behaviors,^3,4 or oceanographic factors.⁵ Here, we show that similar grouping behaviors evolved in an early marine tetrapod lineage, documented by dozens of specimens of the giant ichthyosaur Shonisaurus in the Luning Formation in West Union Canyon, Nevada, USA.^6,7 A concentration of at least seven skeletons closely preserved on a single bedding plane received the bulk of previous attention. However, many more specimens are preserved across ∼106 square meters and ∼200 stratigraphic meters of outcrop representing an estimated >105–6 years. Unlike other marine-tetrapod-rich deposits, this assemblage is essentially monotaxic; other vertebrate fossils are exceptionally scarce. Large individuals are disproportionately abundant, with the exception of multiple neonatal or embryonic specimens, indicating an unusual demographic composition apparently lacking intermediate-sized juveniles or subadults. Combined with geological evidence, our data suggest that dense aggregations of Shonisaurus inhabited this moderately deep, low-diversity, tropical marine environment for millennia during the latest Carnian Stage of the Late Triassic Period (237–227 Ma). Thus, philopatric grouping behavior in marine tetrapods, potentially linked to reproductive activity, has an antiquity of at least 230 million years.

Citation: Kelley, N. P., Irmis, R. B., dePolo, P. E., Noble, P. J., Montague-Judd, D., Little, H., ... & Pyenson, N. D. (2022). Grouping behavior in a Triassic marine apex predator. Current Biology, 32(24), 5398-5405.

Link: www.cell.com/current-biology/fulltext/S0960-9822(22)01761-4?_returnURL=https%3A%2F%2Flinkinghub.elsevier.com%2Fretrieve%2Fpii%2FS0960982222017614%3Fshowall%3Dtrue

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Link: nhmu.utah.edu/blog/2022/new-research-berlin-ichthyosaur-state-park

3D Modeling: 3d.si.edu/enter-sea-dragon