Nicole Klein

Eosauropterygians consist of two major clades, the Nothosauroidea of the Tethysian Middle Triassic (e.g., Nothosaurus) and the Pistosauroidea. The Pistosauroidea include rare Triassic forms (Pistosauridae) and the Plesiosauria of the Jurassic and Cretaceous. Long bones of Nothosaurus and Pistosaurus from the Muschelkalk (Middle Triassic) of Germany and France and a femur of the Lower Jurassic Plesiosaurus dolichodeirus were studied histologically and microanatomically to understand the evolution of locomotory adaptations, patterns of growth and life history in these two lineages. We found that the cortex of adult Nothosaurus long bones consists of lamellar zonal bone. Large Upper Muschelkalk humeri of large-bodied Nothosaurus mirabilis and N. giganteus differ from the small Lower Muschelkalk (Nothosaurus marchicus/N. winterswijkensis) humeri by a striking microanatomical specialization for aquatic tetrapods: the medullary cavity is much enlarged and the cortex is reduced to a few millimeters in thickness. Unexpectedly, the humeri of Pistosaurus consist of continuously deposited, radially vascularized fibrolamellar bone tissue like in the Plesiosaurus sample. Plesiosaurus shows intense Haversian remodeling, which has never been described in Triassic sauropterygians. The generally lamellar zonal bone tissue of nothosaur long bones indicates a low growth rate and suggests a low basal metabolic rate. The large triangular cross section of large-bodied Nothosaurus from the Upper Muschelkalk with their large medullary region evolved to withstand high bending loads. Nothosaurus humerus morphology and microanatomy indicates the evolution of paraxial front limb propulsion in the Middle Triassic, well before its convergent evolution in the Plesiosauria in the latest Triassic. Fibrolamellar bone tissue, as found in Pistosaurus and Plesiosaurus, suggests a high growth rate and basal metabolic rate. The presence of fibrolamellar bone tissue in Pistosaurus suggests that these features had already evolved in the Pistosauroidea by the Middle Triassic, well before the plesiosaurs radiated. Together with a relatively large body size, a high basal metabolic rate probably was the key to the invasion of the Pistosauroidea of the pelagic habitat in the Middle Triassic and the success of the Plesiosauria in the Jurassic and Cretaceous.

The histology of cervical ribs of Sauropoda reveals a primary bone tissue, which largely consists of longitudinally oriented mineralized collagen fibres, essentially the same tissue as found in ossified tendons. The absence of regular periosteal bone and the dominance of longitudinal fibres contradict the ventral bracing hypothesis (VBH) postulated for sauropod necks. The VBH predicts histologically primary periosteal bone with fibres oriented perpendicular to the rib long axis, indicative of connective tissue between overlapping hyperelongated cervical ribs. The transformation of the cervical ribs into ossified tendons makes the neck more flexible and implies that tension forces acted mainly along the length of the neck. This is contrary to the VBH, which requires compressive forces along the neck. Tension forces would allow important neck muscles to shift back to the trunk region, making the neck much lighter.

Long bone histology of the most derived Sauropoda, the Titanosauria suggests that titanosaurian long bone histology differs from the uniform bone histology of basal Sauropoda. Here we describe the long bone histology of the titanosaur Ampelosaurus atacis and compare it to that of basal neosauropods and other titanosaurs to clarify if a special titanosaur bone histology exists. Ampelosaurus retains the laminar vascular organization of basal Sauropoda, but throughout most of cortical growth, the scaffolding of the fibrolamellar bone, which usually is laid down as matrix of woven bone, is laid down as parallel-fibered or lamellar bone matrix instead. The remodeling process by secondary osteons is very extensive and overruns the periosteal bone deposition before skeletal maturity is reached. Thus, no EFS is identifiable. Compared to the atypical bone histology of Ampelosaurus, the large titanosaur Alamosaurus shows typical laminar fibrolamellar bone. The titanosaurs Phuwiangosaurus, Lirainosaurus, and Magyarosaurus, although differing in certain features, all show this same low amount or absence of woven bone from the scaffolding of the fibrolamellar bone, indicating a clear reduction in growth rate resulting in a higher bone tissue organization. To describe the peculiar primary cortical bone tissue of Phuwiangosaurus, Ampelosaurus, Lirainosaurus, and Magyarosaurus, we here introduce a new term, “modified laminar bone” (MLB). Importantly, MLB is as yet not known from extant animals. At least in Lirainosaurus and Magyarosaurus the reduction of growth rate indicated by MLB is coupled with a drastic body size reduction and maybe also a reduction in metabolic rate, interpreted as a result of dwarfing on the European islands during the Late Cretaceous. Phuwiangosaurus and Ampelosaurus both show a similar reduction in growth rate but not in body size, possibly indicating also a reduced metabolic rate. The large titanosaur Alamosaurus, on the other hand, retained the plesiomorphic bone histology of basal neosauropods.

Sauropterygia is an abundant and successful group of Triassic marine reptiles. Phylogenetic relationships of Triassic Sauropterygia have always been unstable and recently questioned. Although specimens occur in high numbers, the main problems are rareness of diagnostic material from the Germanic Basin and uniformity of postcranial morphology of eosauropterygians. In the current paper, morphotypes of humeri along with their corresponding bone histologies for Lower to Middle Muschelkalk sauropterygians are described and interpreted for the first time in a phylogenetic context. Nothosaurus shows a typical plesiomorphic lamellar-zonal bone type, but varying growth patterns and the occurrence of a new humerus morphotype point to a higher taxonomic diversity than was known. In contrast to the enormous morphological variability of eosauropterygian humeri not assigned to Nothosaurus, their long bone histology is relatively uniform and can be divided into two histotypes. Unexpectedly, both of these histotypes reveal abundant fibrolamellar bone throughout the cortex. This pushes the origin of fibrolamellar bone in Sauropterygia back from the Cretaceous to the early Middle Triassic (early Anisian). Histotype A is assigned to Cymatosaurus, a basal member of the Pistosauroidea, which includes the plesiosaurs as derived members. Histotype B is related to the pachypleurosaur Anarosaurus. Contrary to these new finds, the stratigraphically younger pachypleurosaur Neusticosaurus shows the plesiomorphic lamellar-zonal bone type and an incomplete endochondral ossification, like Nothosaurus. Histological results hypothetically discussed in a phylogenetical context have a large impact on the current phylogenetic hypothesis of Sauropterygia, leaving the pachypleurosaurs polyphyletic. On the basis of histological data, Neusticosaurus would be related to Nothosaurus, whereas Anarosaurus would follow the pistosaur clade. Furthermore, the presence of fibrolamellar bone, which is accompanied with increased growth rates and presumably even with increased metabolic rates, already in Anarosaurus and Cymatosaurus can explain the success of the Pistosauroidea, the only sauropterygian group to survive into the Jurassic and give rise to the pelagic plesiosaur radiation.