The skull and endocranium of a Lower Jurassic ichthyosaur based on digital reconstructions

Even after 200 years of study, some details of the cranial anatomy of ichthyosaurs, one of the most successful groups of marine vertebrates in the Mesozoic, are still unclear. New information on the braincase, palate and occiput are provided from three‐dimensional scans of an exceptionally preserved ichthyosaur (‘Hauffiopteryx’ typicus) skull from the Toarcian (183–174 Ma, Lower Jurassic) of Strawberry Bank, England. This ichthyosaur has unusual, hollow, tubular hyoid bars. The occipital and braincase region is fully reconstructed, creating the first digital cranial endocast of an ichthyosaur. Enlarged optic lobes and an enlarged cerebellum suggest neuroanatomical adaptations that allowed it to be a highly mobile, visual predator. The olfactory region also appears to be enlarged, suggesting that olfaction was more important for ichthyosaurs than has been assumed. Phylogenetic analysis suggests this ichthyosaur is closely related to, but distinct from, Hauffiopteryx, and positioned within Thunnosauria, a more derived position than previously recovered. These results further our knowledge of ichthyosaur cranial anatomy in three dimensions and provide a platform in which to study the anatomical adaptations that allowed ichthyosaurs to dominate the marine realm during the Mesozoic.     

A small ichthyosaur from the Clearwater Formation (Alberta,Canada) and a discussion of the taxonomic utility of the pectoral girdle

Albian sedimentary successions of northwestern Canada have yielded a diverse assemblage of Mesozoic marine vertebrates, and ichthyosaurs form an important component of these faunas. Here, we describe a partial postcranial skeleton of a small (estimated at less than 3 m total body length) ichthyosaur from the Wabiskaw Member of the Clearwater Formation (lowermost Albian). The semi-articulated specimen includes much of the presacral vertebral column, dorsal ribs and gastralia. Most significantly, it possesses an articulated pectoral girdle and humerus, and also preserves the pelvic girdle, allowing new insights into girdle evolution in ichthyosaurs. Whereas both sets of girdles are thought to exhibit large amounts of intraspecific variation, the pectoral girdle of ophthalmosaurids appears to evolve very slowly, remaining essentially unchanged from the Middle Jurassic onwards. In contrast, the pelvic girdle shows taxonomically informative changes within Ophthalmosauridae. The variable and poorly known nature of girdle morphology in Cretaceous ichthyosaurs precludes generic referral of the specimen.     

Unusual gut contents in a Cretaceous ichthyosaur

Despite ichthyosaurs being one of the most extensively studied Mesozoic marine reptile groups, there is little documented direct evidence of dietary habits in most taxa. Here, we report the discovery of hatchling-sized marine protostegid turtle remains and an enantiornithine bird (in association with actinopterygian fish and phosphatic nodules) within the body cavity of a gravid female ichthyosaur (Platypterygius longmani) from the Lower Cretaceous of Australia; this is the first evidence, to our knowledge, of feeding by ichthyosaurs upon both turtles and birds. The exceptionally preserved gut contents show little evidence of digestion, suggesting consumption shortly before the ichthyosaur's death. Poor swimming ability may have made hatchling turtles easy prey that could have been either swallowed whole or processed by shake feeding. Ingestion of bird remains probably occurred through scavenging. Opportunistic feeding on vertebrates is at odds with existing interpretations of dietary habits in Cretaceous ichthyosaurs, which favour predation primarily upon cephalopods. Such specialization is considered a contributing factor in the group's ultimate extinction. However, the evidence here that at least some forms were able to use a wide range of available food types suggests that the decline of ichthyosaurs in the mid-Cretaceous may be linked to other factors such as competition with ecologically analogous pursuit predators.     

Lebensspuren von Meersauriern und ihren Beutetieren im mittleren Jura (Callovien) von Liesberg, Schweiz

Summary Numerous gutter-like furrows, up to 60 cm wide and up to 9 m long are preserved at the interface “Macrocephalus Beds”/“Callovian Marl” over a surface of 20 by 200 m. They are interpreted as feeding traces made by large marine vertebrates, most likely plesiosaurs and ichthyosaurs searching for food in the lime mud of the shallow Middle Jurassic sea floor. Possible prey animals were infaunal invertebrates (crustaceans) which produced an intricate meshwork of burrows (mainlyRhizocorallium irregulare andThalassinoides) in the bottom sediments, as well as infaunal bivalves. Evidence from cololites of predatory pelagic reptiles (ichthyosaurs, plesiosaurs) as well as reptile regurgitalites indicate that these animals fed not only on fast-swimming vertebrates and cephalopods but also on epi- and endobenthic invertebrates. In addition, the cololites show that the predators ingested considerable amounts of bottom sediment. Different sizes and shapes of the traces suggest that the gutters were produced by different reptiles or age groups. Candidates for the widest gutters are pliosaurs. Of the marine vertebrates known from Jurassic time, only the snout of adult pliosaurs of the genusLiopleurodon was broad enough to produce gutters more than 40 cm wide. Smaller, less than 15 cm wide gutters, could have been made by plesiosauroids or by the narrow pointed snouts of ichthyosaurs. Almost identical traces described from the Oxfordian of Spain and similar but smaller traces from the Lower Devonian of Prague are equally interpreted as feeding traces on the sea floor. Feeding traces of vertebrates in bottom sediments may give detailed information on the hunting behaviour of the predators. However, the attribution of the traces to definite vertebrate taxa remains uncertain.

     

Absence of Suction Feeding Ichthyosaurs and Its Implications for Triassic Mesopelagic Paleoecology

Mesozoic marine reptiles and modern marine mammals are often considered ecological analogs, but the extent of their similarity is largely unknown. Particularly important is the presence/absence of deep-diving suction feeders among Mesozoic marine reptiles because this would indicate the establishment of mesopelagic cephalopod and fish communities in the Mesozoic. A recent study suggested that diverse suction feeders, resembling the extant beaked whales, evolved among ichthyosaurs in the Triassic. However, this hypothesis has not been tested quantitatively. We examined four osteological features of jawed vertebrates that are closely linked to the mechanism of suction feeding, namely hyoid corpus ossification/calcification, hyobranchial apparatus robustness, mandibular bluntness, and mandibular pressure concentration index. Measurements were taken from 18 species of Triassic and Early Jurassic ichthyosaurs, including the presumed suction feeders. Statistical comparisons with extant sharks and marine mammals of known diets suggest that ichthyosaurian hyobranchial bones are significantly more slender than in suction-feeding sharks or cetaceans but similar to those of ram-feeding sharks. Most importantly, an ossified hyoid corpus to which hyoid retractor muscles attach is unknown in all but one ichthyosaur, whereas a strong integration of the ossified corpus and cornua of the hyobranchial apparatus has been identified in the literature as an important feature of suction feeders. Also, ichthyosaurian mandibles do not narrow rapidly to allow high suction pressure concentration within the oral cavity, unlike in beaked whales or sperm whales. In conclusion, it is most likely that Triassic and Early Jurassic ichthyosaurs were ‘ram-feeders’, without any beaked-whale-like suction feeder among them. When combined with the inferred inability for dim-light vision in relevant Triassic ichthyosaurs, the fossil record of ichthyosaurs does not suggest the establishment of modern-style mesopelagic animal communities in the Triassic. This new interpretation matches the fossil record of coleoids, which indicates the absence of soft-bodied deepwater species in the Triassic.     

The fossil record of ichthyosaurs,completeness metrics and sampling biases

Ichthyosaurs were highly successful marine reptiles with an abundant and well‐studied fossil record. However, their occurrences through geological time and space are sporadic, and it is important to understand whether times of apparent species richness and rarity are real or the result of sampling bias. Here, we explore the skeletal completeness of 351 dated and identified ichthyosaur specimens, belonging to all 102 species, the first time that such a study has been carried out on vertebrates from the marine realm. No correlations were found between time series of different skeletal metrics and ichthyosaur diversity. There is a significant geographical variation in completeness, with the well‐studied northern hemisphere producing fossils of much higher quality than the southern hemisphere. Medium‐sized ichthyosaurs are significantly more complete than small or large taxa: the incompleteness of small specimens was expected, but it was a surprise that larger specimens were also relatively incomplete. Completeness varies greatly between facies, with fine‐grained, siliciclastic sediments preserving the most complete specimens. These findings may explain why the ichthyosaur diversity record is low at times, corresponding to facies of poor preservation potential, such as in the Early Cretaceous. Unexpectedly, we find a strong negative correlation between skeletal completeness and sea level, meaning the most complete specimens occurred at times of global low sea level, and vice versa. Completeness metrics, however, do not replicate the sampling signal and have limited use as a global‐scale sampling proxy.     

Mikadocephalus gracilirostris n. gen., n. sp., a new ichthyosaur from the Grenzbitumenzone (Anisian-Ladinian) of Monte San Giorgio (Switzerland)

An almost complete skull of a new ichthyosaur from the Middle Triassic Grenzbitumenzone Beds of Monte San Giorgio (Kanton Tessin, Switzerland) represents one of the most complete and best preserved finds of a large Triassic ichthyosaur cranium. Its affinites with other Triassic ichthyosaur taxa are discussed and it is demonstrated to represent a new genus and species,Mikadocephalus gracilirostris, which does not fit into any of the currently recognized families of Triassic ichthyosaurs. Remarkable similarities in cranial structure exit to postTriassic ichthyosaurs, with which a number of important apomorphies are shared.     

Ichthyosauria from the Upper Lias of Strawberry Bank,England

Abstract: Eight remarkably preserved specimens of ichthyosaurs from the lower Toarcian (Lower Jurassic) of Strawberry Bank (Ilminster, Somerset, England) are described fully for the first time. Whereas previously these ichthyosaurs were assigned to one species, Stenopterygius hauffianus, our study shows there are two, Stenopterygius triscissus and Hauffiopteryx typicus. S. triscissus is a small‐ to medium‐sized ichthyosaur up to 3.5 m long, characterised by three apomorphies: long and slender rostrum, large elliptical supratemporal fenestra and bipartite pelvis. H. typicus is a small ichthyosaur up to 2.95 m long, with five apomorphies: short and extremely slender rostrum, very large orbit, small rounded supratemporal fenestra and tripartite pelvis, which is fused distally. Cladistic analysis is equivocal about their relationships, suggesting either that Hauffiopteryx and perhaps also Stenopterygius are members of a clade Eurhinosauria or that this clade does not exist, and both genera are members of a wider clade Thunnosauria. Further, the clade Stenopterygiidae, in which Hauffiopteryx had been located, is not identified. Most striking is that the specimens are all juveniles (five specimens) or infants (three specimens), ranging from one‐tenth to one‐half the normal adult length of the species.     

The Liassic ichthyosaur<Emphasis Type="Italic">Stenopterygius</Emphasis> cf.<Emphasis Type="Italic">quadriscissus</Emphasis> from the lower Toarcian of Dobbertin (northeastern Germany) and some considerations on lower Toarcian marine reptile palaeobiogeography

An incomplete skull of the lower Toarcian ichthyosaurStenopterygius cf.quadriscissus is described from the lower Toarcian of Dobbertin (Mecklenburg, northeastern Germany). It represents both the northeasternmost occurrence of this ichthyosaur genus and the first diagnostic specimen from East Germany. It therefore extends the palaeobiogeographic range ofStenopterygius considerably and demonstrates that this ichthyosaur also inhabited the Germanic Basin east of the Rhenish Massif by Early Jurassic times. A palaeobiogeographical pattern is evident within the genusStenopterygius, with the ubiquitous speciesS. longifrons andS. hauffianus on one hand, andS. megalorhinus andS. quadriscissus on the other hand, which appear not to have ranged northwest of the London-Brabant Massif. It is suggested that, whereas the Rhenish Massif was not an effective barrier for dispersal of ichthyosaurs in Western Europe during early Toarcian times, the London-Brabant Massif played a rather significant role, as is also shown by the fossil record of other marine reptile groups. A provincialism of early Toarcian marine reptiles is suggested for Western Europe, with a northwestern province which contains the British occurrences, an intermediate, Subgermanic province in France and the Benelux countries, and a southeastern province in the Germanic Basin. The British and Germanic provinces are each characterized by a typical assemblage of ichthyosaurs, plesiosaurs, and marine crocodiles, wheres the intermediate Subgermanic region shows an intermingling of faunal elements.      

The skull of a large Lower Triassic ichthyosaur from Spitzbergen and its implications for the origin of the Ichthyosauria

An incomplete ichthyosaur skull from the Lower Triassic (Spathian) Sticky Keep Formation of Spitzbergen is one of the earliest ichthyosaurs known and by far the largest of the most basal ichthyosaurs. The specimen shows an extremely plesiomorphic cheek region of the skull and allows for the first time a confident reconstruction of the grundplan condition of the lower cheek region of ichthyosaurs. It unequivocally demonstrates the presence of a deep emargination of the lower cheek, which is bordered dorsally by the quadratojugal, squamosal and jugal, and therefore a plesiomorphic lack of contact between jugal and quadratojugal. The specimen also allows an evaluation of recent skull reconstructions of several Lower Triassic taxa which probably contain severe misinterpretations. The structure of the temporal and cheek region of the specimen can be most parsimoniously explained by the initial presence of a lower temporal fenestra. This provides important new evidence that the ancestry of ichthyosaurs might have lain within the Diapsida or their stem-group.     

The palaeohistology of the basal ichthyosaur Mixosaurus (Ichthyopterygia,Mixosauridae) from the Middle Triassic: Palaeobiological implications

Here, we provide the first bone histological examination of an ontogenetic series of the basal ichthyosaur Mixosaurus encompassing postnatal to large adult specimens. Growth marks are present in sampled humeri, a femur, a fibula, as well as in other skeletal elements (gastral ribs). Ontogenetic changes are traceable throughout stylo- and zeugopodial development, but interior remodelling and resorption deleted part of the internal growth record in the primary cortex. Mixosaurus humeri started as flat structures consisting of a core of endochondral woven bone and residual calcified cartilage, whereas growth continued by deposition of periosteal fibrolamellar and parallel-fibred bone. Unlike the fast-growing post-Triassic ichthyosaurs that lack growth marks, microstructural and life history data are now becoming available for a basal ichthyosaur. The high growth rate of Mixosaurus may indicate that higher metabolic rates characterised small, non-thunniform ichthyosaurs, as had been suggested already for post-Triassic, cruising forms.     

High Diversity in Cretaceous Ichthyosaurs from Europe Prior to Their Extinction

Background

Ichthyosaurs are reptiles that inhabited the marine realm during most of the Mesozoic. Their Cretaceous representatives have traditionally been considered as the last survivors of a group declining since the Jurassic. Recently, however, an unexpected diversity has been described in Upper Jurassic–Lower Cretaceous deposits, but is widely spread across time and space, giving small clues on the adaptive potential and ecosystem control of the last ichthyosaurs. The famous but little studied English Gault Formation and ‘greensands’ deposits (the Upper Greensand Formation and the Cambridge Greensand Member of the Lower Chalk Formation) offer an unprecedented opportunity to investigate this topic, containing thousands of ichthyosaur remains spanning the Early–Late Cretaceous boundary.

Methodology/Principal Findings

To assess the diversity of the ichthyosaur assemblage from these sedimentary bodies, we recognized morphotypes within each type of bones. We grouped these morphotypes together, when possible, by using articulated specimens from the same formations and from new localities in the Vocontian Basin (France); a revised taxonomic scheme is proposed. We recognize the following taxa in the ‘greensands’: the platypterygiines ‘Platypterygius’ sp. and Sisteronia seeleyi gen. et sp. nov., indeterminate ophthalmosaurines and the rare incertae sedis Cetarthrosaurus walkeri. The taxonomic diversity of late Albian ichthyosaurs now matches that of older, well-known intervals such as the Toarcian or the Tithonian. Contrasting tooth shapes and wear patterns suggest that these ichthyosaurs colonized three distinct feeding guilds, despite the presence of numerous plesiosaur taxa.

Conclusion/Significance

Western Europe was a diversity hot-spot for ichthyosaurs a few million years prior to their final extinction. By contrast, the low diversity in Australia and U.S.A. suggests strong geographical disparities in the diversity pattern of Albian–early Cenomanian ichthyosaurs. This provides a whole new context to investigate the extinction of these successful marine reptiles, at the end of the Cenomanian.     

The mixosaurid ichthyosaur Contectopalatus from the Middle Triassic of the German Basin

The skull of the mixosaurid species Contectopalatus atavus (Quenstedt, 1851-52) is the most bizarre of any known ichthyosaur. It possesses a very high sagittal crest formed by the nasal, frontal and parietal bones which grows higher during ontogeny. This skull structure - found to a lesser extent in the other mixosaurid genera Mixosaurus and Phalarodon - is a synapomorphy of the family Mixosauridae. It is here interpreted as correlated with a unique arrangement of the jaw adductor musculature among tetrapods, with the internal jaw adductors extending over most of the skull roof up to the external narial opening. This reconstruction would increase the biting force considerably and the hypothesis is supported by peculiarities of the dentition and jaws of Contectopalatus. Contectopalatus probably reached a length of about 5 meters. It is therefore the largest known mixosaurid and one of the largest Triassic ichthyosaurs. The general text-book picture of mixosaurs as small, rather unspecialized, primitive ichthyosaurs is incorrect. Mixosaurs were a highly specialized, uniquely adapted and very diverse ichthyosaur family, some members of which rank among the marine top predators of their time.     

First record of live birth in Cretaceous ichthyosaurs: closing an 80 million year gap

New fossils of embryonic ichthyosaurs are both the geologically youngest and the physically smallest known ichthyosaur embryos. The embryos are articulated, though only partially preserved, and are located within the body cavity of an adult, presumably the mother. The embryos and adult were found in association with several other individuals of differing size classes, all of which appear to be a new taxon of Cretaceous ichthyosaur. The material was collected from units of the Loon River Formation, Hay River, Northwest Territories, Canada. The implications of this new material to ichthyosaurian reproductive biology are discussed.     

Convergent Evolution in Aquatic Tetrapods: Insights from an Exceptional Fossil Mosasaur

Mosasaurs (family Mosasauridae) are a diverse group of secondarily aquatic lizards that radiated into marine environments during the Late Cretaceous (98–65 million years ago). For the most part, they have been considered to be simple anguilliform swimmers – i.e., their propulsive force was generated by means of lateral undulations incorporating the greater part of the body – with unremarkable, dorsoventrally narrow tails and long, lizard-like bodies. Convergence with the specialized fusiform body shape and inferred carangiform locomotory style (in which only a portion of the posterior body participates in the thrust-producing flexure) of ichthyosaurs and metriorhynchid crocodyliform reptiles, along with cetaceans, has so far only been recognized in Plotosaurus, the most highly derived member of the Mosasauridae. Here we report on an exceptionally complete specimen (LACM 128319) of the moderately derived genus Platecarpus that preserves soft tissues and anatomical details (e.g., large portions of integument, a partial body outline, putative skin color markings, a downturned tail, branching bronchial tubes, and probable visceral traces) to an extent that has never been seen previously in any mosasaur. Our study demonstrates that a streamlined body plan and crescent-shaped caudal fin were already well established in Platecarpus, a taxon that preceded Plotosaurus by 20 million years. These new data expand our understanding of convergent evolution among marine reptiles, and provide insights into their evolution''s tempo and mode.     

A New Look at Ichthyosaur Long Bone Microanatomy and Histology: Implications for Their Adaptation to an Aquatic Life

Background

Ichthyosaurs are Mesozoic reptiles considered as active swimmers highly adapted to a fully open-marine life. They display a wide range of morphologies illustrating diverse ecological grades. Data concerning their bone microanatomical and histological features are rather limited and suggest that ichthyosaurs display a spongious, “osteoporotic-like” bone inner structure, like extant cetaceans. However, some taxa exhibit peculiar features, suggesting that the analysis of the microanatomical and histological characteristics of various ichthyosaur long bones should match the anatomical diversity and provide information about their diverse locomotor abilities and physiology.

Methodology/Principal Findings

The material analyzed for this study essentially consists of mid-diaphyseal transverse sections from stylopod bones of various ichthyosaurs and of a few microtomographic (both conventional and synchrotron) data. The present contribution discusses the histological and microanatomical variation observed within ichthyosaurs and the peculiarities of some taxa (Mixosaurus, Pessopteryx). Four microanatomical types are described. If Mixosaurus sections differ from those of the other taxa analyzed, the other microanatomical types, characterized by the relative proportion of compact and loose spongiosa of periosteal and endochondral origin respectively, seem to rather especially illustrate variation along the diaphysis in taxa with similar microanatomical features. Our analysis also reveals that primary bone in all the ichthyosaur taxa sampled (to the possible exception of Mixosaurus) is spongy in origin, that cyclical growth is a common pattern among ichthyosaurs, and confirms the previous assumptions of high growth rates in ichthyosaurs.

Conclusions/Significance

The occurrence of two types of remodelling patterns along the diaphysis, characterized by bone mass decrease and increase respectively is described for the first time. It raises questions about the definition of the osseous microanatomical specializations bone mass increase and osteoporosis, notably based on the processes involved, and reveals the difficulty in determining the true occurrence of these osseous specializations in ichthyosaurs.     

Mechanical properties of pufferfish (Lagocephalus gloveri) skin and its collagen arrangement

Skin is a biological material the mechanical properties of which are dependent on the constituents from which it is assembled. Skin, the outer covering of animals is made up of collagen fibers arranged in more or less ordered arrays. Pufferfish skin provides a rigid framework to support the body contents and a flexible covering to allow whatever changes are necessary for the remarkable inflation mechanism. Here, we describe the structure and tensile properties of the dorsal and ventral skin of the pufferfish, Lagocephalus gloveri Abe and Tabeta, 1983. The ultimate tensile strength of ventral skin was found to be around two times higher than that of the dorsal skin. It was observed that the dorsal skin could resist more deformation than the ventral skin. The collagen fibers were arranged in different ordered arrays for ventral and dorsal skin and the concentration of fibers was found to be more in ventral than dorsal skin. This provides more stiffness to ventral skin. Scanning electron microscopy studies of the ventral skin showed a unidirectional arrangement of the collagen fibers, which provides more stretching capacity. Dorsal skin, on the other hand, has an orthogonal arrangement of fibers. The present study thus showed that the mechanical behavior of the skin of L. gloveri is strongly influenced by the concentration and arrangement of collagen fibers.     

Preservational modes of some ichthyosaur soft tissues (Reptilia,Ichthyopterygia) from the Jurassic Posidonia Shale of Germany

Konservat-Lagerstätten, such as the Toarcian (Early Jurassic) Posidonia Shale of southwestern Germany, are renowned for their spectacular fossils. Ichthyosaur skeletons recovered from this formation are frequently associated with soft tissues; however, the preserved material ranges from three-dimensional, predominantly phosphatized structures to dark films of mainly organic matter. We examined soft-tissue residues obtained from two ichthyosaur specimens using an integrated ultrastructural and geochemical approach. Our analyses revealed that the superficially-looking ‘films’ in fact comprise sections of densely aggregated melanosome (pigment) organelles sandwiched between phosphatized layers containing fibrous microstructures. We interpret this distinct layering as representing condensed and incompletely degraded integument from both sides of the animal. When compared against previously documented ichthyosaur fossils, it becomes readily apparent that a range of preservational modes exists between presumed ‘phosphatic’ and ‘carbonized’ soft-tissue remains. Some specimens show high structural fidelity (e.g. distinct integumentary layering), while others, including the fossils examined in this study, retain few original anatomical details. This diversity of soft-tissue preservational modes among Posidonia Shale ichthyosaurs offers a unique opportunity to examine different biostratinomic, taphonomic and diagenetic variables that potentially could affect the process of fossilization. It is likely that soft-tissue preservation in the Posidonia Shale was regulated by a multitude of factors, including decay efficiency and speed of phosphatic mineral nucleation; these in turn were governed by a seafloor with sustained microbial mat activity fuelled by high organic matter input and seasonally fluctuating oxygen levels.