Histology of sculptured cranial dermal bones of the stem salamander Kokartus honorarius (Amphibia: Caudata) from the Middle Jurassic of Kyrgyzstan

Kokartus honorarius from the Middle Jurassic (Bathonian) of Kyrgyzstan is one of the oldest and basalmost salamanders in the fossil record, and this taxon is useful for documenting a primitive caudate condition and patterns of character state transformations within Caudata. Here, we provide a histological analysis of its dermal bones based on two thin sections of a fragment of a sculptured dermal skull roof bone (squamosal?). The dermal bone histology of Kokartus is similar to that of basal crown-group tetrapods (e.g. temnospondyls, lepospondyls and seymouriamorphs) in the following features: the presence of basic pattern of organisation of dermal bones (diploë structure); the cancellous middle region occupies larger space than the compact cortices; active remodelling with the formation of numerous erosion bays and secondary osteons; high number of vascular canals with the formation a dense vascular network (= ‘rete vasculosum’); and parallel-fibred bone is a dominant type of primary bone matrix. Crown-group salamanders retained the diploë structure, but demonstrate features of simplification (in comparison with Kokartus): absence of pronounced sculpture, lower degree of vascularisation and lower degree of remodelling. The simplification of the histological structure is a derived feature for the Caudata which appeared during the transition from stem-group to crown-group salamanders.     

Bone microanatomy and lifestyle: A descriptive approach

Starting in 2004, our lab has published several studies on the relationship between bone microanatomy, lifestyle (aquatic to terrestrial), and the phylogeny of tetrapods. These studies emphasized quantitative and statistical analyses. Therefore, the raw data used in these studies were never published. This is unfortunate because no model captures all information in biological data. This paper remedies this situation by providing the detailed anatomical drawings used in our previous studies. These constitute the largest set of standardized cross-section images of appendicular long bones (tibiae, radii, and humeri) ever published, at least as far as the number of represented species (over one hundred) is concerned. All major aquatic to terrestrial extant tetrapod clades are represented (lissamphibians, mammals, turtles, squamates, and crocodilians). The comparative figures show that aquatic tetrapods differ most from the others, whereas amphibious taxa differ much less from their terrestrial relatives.     

Adaptive radiation in sauropod dinosaurs: bone histology indicates rapid evolution of giant body size through acceleration

The well-preserved histology of the geologically oldest sauropod dinosaur from the Late Triassic allows new insights into the timing and mechanism of the evolution of the gigantic body size of the sauropod dinosaurs. The oldest sauropods were already very large and show the same long-bone histology, laminar fibro-lamellar bone lacking growth marks, as the well-known Jurassic sauropods. This bone histology is unequivocal evidence for very fast growth. Our histologic study of growth series of the Norian Plateosaurus indicates that the sauropod sistergroup, the Late Triassic and early Jurassic Prosauropoda, reached a much more modest body size in a not much shorter ontogeny. Increase in growth rate compared to the ancestor (acceleration) is thus the underlying process in the phylogenetic size increase of sauropods. Compared to all other dinosaur lineages, sauropods were not only much larger but evolved very large body size much faster. The prerequisite for this increase in growth rate must have been a considerable increase in metabolic rate, and we speculate that a bird-like lung was important in this regard.     

A Mid-Upper Palaeolithic human humerus from Eel Point, South Wales, UK

We report here on a human humerus directly dated to 24,470 +/- 110 BP, placing it within the Gravettian, or Mid-Upper Palaeolithic. The partial humerus is an isolated find and can be attributed (with some caution) to the Pleistocene 'bone cave' of Eel Point on Caldey Island, Wales (UK). The humerus is probably male, similar in robusticity to other Gravettian right humeri. The apparent absence of stone tools and presence of hyaena bone and coprolites suggest that the element may not derive from an intentional burial. After a maxilla from Kent's Cavern and the Gravettian Paviland 1, Eel Point represents the third oldest anatomically modern human known from Britain. Stable carbon and nitrogen isotope measurements do not support certain use of marine foods but highlight the need for more research on contemporary faunal remains in order to better interpret human values from this period.     

An updated paleontological timetree of lissamphibians,with comments on the anatomy of Jurassic crown-group salamanders (Urodela)

We present an update of our time-calibrated supertree of extant and extinct lissamphibians (Marjanovi? D, Laurin M. 2007. Fossils, molecules, divergence times, and the origin of lissamphibians. Syst Biol 56(3):369–388) and of the divergence dates that can be inferred from it. The present version contains 319 extinct species or possible species of lissamphibians, compared to 223 previously. Discoveries of new fossiliferous sites, advances in phylogeny and recently obtained radiometric dates have offered opportunities to test our results, including the conclusion that the fossil record of Lissamphibia is dense enough to provide reliable calibration constraints for molecular divergence dating. By and large, the results are upheld. Some of the divergence dates we infer from the tree are up to 15 Ma younger than we previously published, some are up to 15 Ma older, some have had their range of uncertainty drastically reduced and the maximum age for the origin of Urodela (the salamander crown group) is no longer well constrained. The dermal bone plates in the gill region of the Jurassic urodeles Beiyanerpeton, Seminobatrachus and Chunerpeton and the grooves for the lateral line organ on the skull of the first require either unexpected reversals or several independent losses in other lissamphibians and indeed other urodeles.     

Long Bone Histology of Sauropterygia from the Lower Muschelkalk of the Germanic Basin Provides Unexpected Implications for Phylogeny

Background

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.

Methodology/Principal Findings

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.

Conclusions/Significance

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.     

A Tachyglossid-Like Humerus from the Early Cretaceous of South-Eastern Australia

A partial right humerus has been recovered from the Early Cretaceous (Albian) Eumeralla Formation at Dinosaur Cove in south-eastern Australia. General morphology, size and the presence of a single epicondylar foramen (the entepicondylar) suggest that the bone is from a mammal or an advanced therapsid reptile. The humerus is similar in size, shape and torsion to the equivalent bone of extant and late Neogene echidnas (Tachyglossidae) but, contrary to the situation in extant monotremes, in which the ulna and radius articulate with a single, largely bulbous condyle, it bears a shallow, pulley-shaped (i.e. trochlear-form) ulnar articulation that is confluent ventro-laterally with the bulbous radial condyle. This form of ulnar articulation distinguishes this bone from the humeri of most advanced therapsids and members of several major groups of Mesozoic mammals, which have a condylar ulnar articulation, but parallels the situation found in therian mammals and in some other lineages of Mesozoic mammals. As in extant monotremes the distal humerus is greatly expanded transversely and humeral torsion is strong. Transverse expansion of the distal humerus is evident in the humeri of the fossorial docodont Haldanodon, highly-fossorial talpids and some clearly fossorial dicynodont therapsids, but the fossil shows greatest overall similarity to extant monotremes and it is possible that the peculiar elbow joint of extant monotremes evolved from a condition approximating that of the fossil. On the basis of comparisons with Mesozoic and Cainozoic mammalian taxa in which humeral morphology is known, the Dinosaur Cove humerus is tentatively attributed to a monotreme. However, several apparently primitive features of the bone exclude the animal concerned from the extant families Tachyglossidae and Ornithorhynchidae and suggest that, if it is a monotreme, it is a stem-group monotreme. Whatever, the animal's true affinity, the gross morphology of its humerus indicates considerable capacity for rotation-thrust digging.     

The earliest known Salamanders (Amphibia,Caudata):A record from the Middle Jurassic of England

Marmorerpeton gen. nov. represented by M. kermackisp. nov. and M. freemani sp. nov., is the earliest known genus of fossil salamander from the Upper Bathonian, Middle Jurassic of Kirtlington, Oxfordshire, England. Marmorerpeton is more primitive than any other known salamander in the absence of intravertebral spinal nerve foramina in the atlantal centrum, but in other features it resembles members of the family Scapherpetontidae, neotenous salamanders otherwise known from the Upper Cretaceous and Palaeocene. The Kirtlington herpetofauna is a unique freshwater assemblage of Middle Jurassic small amphibians and reptiles, several of which represent the earliest known occurrences of their respective groups.     

Ontogeny of the hyobranchial apparatus in the salamanders Ambystoma talpoideum (Ambystomatidae) and Notophthalmus viridescens (Salamandridae): The ecological morphology of two neotenic strategies

Comparison of metamorphosis of skull and hyobranchial system in two species of neotenic salamanders reveals two different types of neoteny. Ambystoma talpoideum is completely neotenic owing to delayed metamorphosis. Notophthalmus viridescens exhibits limited neoteny as a result of incomplete metamorphosis. Morphological details of neoteny are compared to life history in both species in order to discuss the ecological morphology of the two neotenic strategies. Comparisons to Taricha granulosa, Triturus vulgaris, and Ambystoma gracile indicate that these two strategies are widely employed and may represent familial patterns.     

TWO NEW PARROTS (PSITTACIFORMES) FROM THE LOWER EOCENE FUR FORMATION OF DENMARK

Abstract:  Two new fossil psittaciform birds from the Lower Eocene 'Mo Clay' (Fur Formation) of Denmark ( c . 54 Ma) are described. An unnamed specimen is assigned to the extinct avian family of stem-group parrots, Pseudasturidae (genus and species incertae sedis ), while a second ( Mopsitta tanta gen. et sp. nov.) is the largest fossil parrot yet known. Both specimens are the first fossil records of these birds from Denmark. Although the phylogenetic position of Mopsitta is unclear (it is classified as family incertae sedis ), this form is phylogenetically closer to Recent Pstittacidae than to other known Palaeogene psittaciforms and may, therefore, represent the oldest known crown-group parrot.     

Microanatomical diversity of the humerus and lifestyle in lissamphibians

A study of body size and the compactness profile parameters of the humerus of 37 species of lissamphibians demonstrates a relationship between lifestyle (aquatic, amphibious or terrestrial) and bone microstructure. Multiple linear regressions and variance partitioning with Phylogenetic eigenVector Regressions reveal an ecological and a phylogenetic signal in some body size and compactness profile parameters. Linear discriminant analyses segregate the various lifestyles (aquatic vs. amphibious or terrestrial) with a success rate of up to 89.2%. The models built from data on the humerus discriminate aquatic taxa relatively well from the other taxa. However, like previous models built from data on the radius of amniotes or on the femur of lissamphibians, the new models do not discriminate amphibious taxa from terrestrial taxa on the basis of body size or compactness profile data. To make our inference method accessible, spreadsheets (see supplementary material on the website), which allow anyone to infer a lissamphibian lifestyle solely from body size and bone compactness parameters, were produced. No such easy implementation of habitat inference models is found in earlier papers on this topic.     

Long bone histology of Chersina angulata : Interelement variation and life history data

The current study deduced the growth pattern and lifestyle habits of Chersina angulata based on bone histology and cross-sectional geometry of limb bones. Femora, humeri, and tibiae of seven different-sized individuals representing different ontogenetic stages were assessed to determine the interelement and intraskeletal histological variation within and among the tortoises. The bone histology of adult propodials consists of a highly vascularized, uninterrupted fibrolamellar bone tissue with a woven texture in the perimedullary and midcortical regions suggesting overall fast early growth. However, later in ontogeny, growth was slow and even ceased periodically as suggested by slowly formed parallel-fibered bone tissue and several growth marks in the pericortical region. In juvenile individuals, fibrolamellar bone tissue is restricted to the perimedullary regions of propodials as remnants of bone formed during the earliest stages of ontogeny. The epipodials are characterized by having parallel-fibered bone tissue present in their cortices; however, periodic arrests in growth are recorded at various times. Remnants of fibrolamellar bone tissue formed during early ontogeny occur in the epipodials of only a few individuals. Interelement variation is evident, in terms of variation in the orientation of vascular canals between individuals and within the same diaphyseal cross-sections. Different elements show varying cross-sectional geometry, which appear to be correlated with the fossorial behavior of the species. Our results show that of all the long bones, the tibia is least remodeled during ontogeny and it is therefore the best element for skeletochronology.     

Histological skeletochronology indicates developmental plasticity in the early Permian stem lissamphibian Doleserpeton annectens

Doleserpeton annectens is a small‐bodied early Permian amphibamiform, a clade of temnospondyl amphibians regarded by many workers to be on the lissamphibian stem. Most studies of this taxon have focused solely on its anatomy, but further exploration of other aspects of its paleobiology, such as developmental patterns, is critical for a better understanding of the early evolutionary history of lissamphibians. Here, we present a histological analysis of growth patterns in D. annectens that utilizes 60 femora, the largest sample size for any Paleozoic tetrapod. We identified pervasive pairs of closely spaced lines of arrested growth (LAGs), a pattern that indicates a marked degree of climatic harshness and that would result in two cessations of growth within a presumed single year. We documented a wide degree of variation compared to previous temnospondyl skeletochronological studies, reflected in the poor correlation between size and inferred age, but this observation aligns closely with patterns observed in extant lissamphibians. Furthermore, sensitivity analyses conducted by subsampling our dataset at more typical sample sizes for paleontological studies produced a wide range of results. This includes biologically improbable results and exceptionally well‐fit curves that demonstrate that low sample size can produce potentially misleading artifacts. We propose that the weak correlation between age and size represents developmental plasticity in D. annectens that typifies extant lissamphibians. Detection of these patterns is likely only possible with large sample sizes in extinct taxa, and low sample sizes can produce false, misleading results that warrant caution in drawing paleobiological interpretations from such samples.     

Earliest vertebrate embryos in the fossil record (Middle Devonian,Givetian)

Serial sectioning of a nodule encapsulating an adult specimen of the arthrodire placoderm Watsonosteus fletti from the Eday Flagstone Formation (Givetian) in the Orcadian Basin of northern Scotland has revealed the presence of a number of embryos within the adult. This specimen represents the oldest known record of fossilized vertebrate embryos. Thin sections of two of the slices have revealed the detailed histological structure of embryonic plates in placoderms, showing that as previously deduced from visual examination, the outer and inner layers were the first to form. Gut contents preserved near the embryos show that the species had a varied diet, with dermal bone fragments from sarcopterygians and placoderms.     

What humeri are suitable for comparative testing of suture anchors? An ultrastructural bone analysis and biomechanical study of ovine,bovine and human humeri and four different anchor types

For testing of fixation devices such as suture anchors used in rotator cuff repair often animal bones are used. They are easily obtained, inexpensive and some have been found to be similar to human bone. But can we rely on the results drawn from these studies in our daily surgical practice?The purpose of this study was to compare the trabecular bone mineral density, the trabecular bone volume fraction and the cortical layer thickness in the greater tubercle in different species to evaluate their influence on primary stability of suture anchors under a cyclic loading protocol representing the physiologic forces placed on rotator cuff repairs in vivo.Bovine and ovine humeri are not suitable for suture anchor testing. The statistical significances for pullout forces between the anchors varied from species to species. Therefore, no very applicable information can be obtained from testing suture anchors in ovine or bovine humeri with regard to ultimate failure loads in human humeri. The ultimate failure load seems to depend mainly on the cortical thickness and on the subcortical trabecular bone quality.     

THE GEOLOGICALLY YOUNGEST ALBANERPETONTID AMPHIBIAN, FROM THE LOWER PLIOCENE OF HUNGARY

Abstract:  The Albanerpetontidae are salamander-like, Middle Jurassic to Neogene lissamphibians from Laurasia and North Africa. Extensive series of albanerpetontid bones recently identified in collections from the Csarnóta 2 locality, south-central Hungary, extend the temporal range of the clade forward about seven million years from the middle Miocene to the early Pliocene. The Hungarian material is diagnostic for the Euramerican type genus Albanerpeton and pertains to a new species, A. pannonicus sp. nov., which differs from the seven previously reported congeners (Early Cretaceous–Miocene) in a distinctive combination of primitive and derived character states of the jaws and frontals, including a unique ventromedian keel on the azygous frontals. Some of the Hungarian specimens are articulated sets of skull bones, including ones containing the first three-dimensional examples of a nasal and jugals known for albanerpetontids, that help clarify some details of cranial osteology in these amphibians. Cladistic analysis nests A. pannonicus within the robust-snouted clade, as the sister taxon to an unnamed late Palaeocene species from Canada and A. inexpectatum from early–middle Miocene deposits in France, Austria and Germany. This phylogeny and recent reports of diagnostic Albanerpeton material from the Campanian of France and Maastrichtian of Romania suggest the evolutionary history of Albanerpeton was more complex than previously hypothesized, with Europe having played a larger role. The 25 fossiliferous layers at Csarnóta 2 record a shift from forest to grassland palaeoenvironments. Fossils of A. pannonicus are present in all layers, implying that this species was not adversely affected by the change in palaeoenvironments.     

Bony‐toothed birds (Aves: Pelagornithidae) from the Middle Eocene of Belgium

Abstract: We describe well‐preserved remains of the Pelagornithidae (bony‐toothed birds) from the middle Eocene of Belgium, including a sternum, pectoral girdle bones and humeri of a single individual. The specimens are tentatively assigned to Macrodontopteryx oweni Harrison and Walker, 1976 , which has so far only been known from the holotype skull and a referred proximal ulna. Another species, about two times larger, is represented by an incomplete humerus and tentatively identified as Dasornis emuinus ( Bowerbank, 1854 ). The fossils provide critical new data on the osteology of the pectoral girdle of bony‐toothed birds. For the first time, the sternum of one of the smaller species is preserved, and this bone exhibits a more plesiomorphic morphology than the recently described sternum of the giant Miocene taxon Pelagornis. The coracoid resembles that of the Diomedeidae (albatrosses) in overall morphology, but because bony‐toothed birds lack apomorphies of the Procellariiformes, the similarities are almost certainly owing to convergence. Bony‐toothed birds were often compared with the ‘Pelecaniformes’ by previous authors, who especially made comparisons with the Sulidae (gannets and boobies). However, the coracoid distinctly differs from that of extant ‘pelecaniform’ birds, and the plesiomorphic presence of a foramen nervi supracoracoidei as well as the absence of a well‐delimited articulation facet for the furcula supports a position outside the Suloidea, the clade to which the Sulidae belong.     

Shell bone histology indicates terrestrial palaeoecology of basal turtles

The palaeoecology of basal turtles from the Late Triassic was classically viewed as being semi-aquatic, similar to the lifestyle of modern snapping turtles. Lately, this view was questioned based on limb bone proportions, and a terrestrial palaeoecology was suggested for the turtle stem. Here, we present independent shell bone microstructural evidence for a terrestrial habitat of the oldest and basal most well-known turtles, i.e. the Upper Triassic Proterochersis robusta and Proganochelys quenstedti. Comparison of their shell bone histology with that of extant turtles preferring either aquatic habitats or terrestrial habitats clearly reveals congruence with terrestrial turtle taxa. Similarities in the shell bones of these turtles are a diploe structure with well-developed external and internal cortices, weak vascularization of the compact bone layers and a dense nature of the interior cancellous bone with overall short trabeculae. On the other hand, 'aquatic' turtles tend to reduce cortical bone layers, while increasing overall vascularization of the bone tissue. In contrast to the study of limb bone proportions, the present study is independent from the uncommon preservation of appendicular skeletal elements in fossil turtles, enabling the palaeoecological study of a much broader range of incompletely known turtle taxa in the fossil record.     

Postcranial morphology and growth of the pachypleurosaur Anarosaurus heterodontus (Sauropterygia) from the Lower Muschelkalk of Winterswijk, The Netherlands

Sauropterygia from the Muschelkalk are only found in lag deposits known as bone beds, and most of the material consists of isolated bones. Alpha taxonomy of Sauropterygia from the Germanic Basin which include Pachypleurosauria is thus based mainly on skull morphology of a few specimens. Articulated or associated postcranial material of pachypleurosaurs, associated with diagnostic skull material, is very rare in the Germanic Basin and currently occurs in larger numbers only in the Lower Muschelkalk of Winterswijk (Gelderland Province, The Netherlands), which continuously produces new material. For the first time, the morphology of several partially articulated skeletons of the pachypleurosaur Anarosaurus heterodontus is described and compared. Some of those specimens have skull material attached; others were identified as pachypleurosaurs on the basis of their long bone histology. The current study revealed that postcranial bones of A.?heterodontus feature a diverse morphology reflecting differences during ontogeny. Thus, A.?heterodontus specimens could be assigned to size classes (I?CIII). However, on the basis of morphology, histology, and maximal known size of isolated skulls and humeri, none of these specimens represent fully grown individuals. Growth mark counts of midshaft-femur samples, morphologically assigned to size class?III, document that this size class was reached within the first year of life. Size class?III continued into the second year of life, and then afterwards skeletal maturity was reached. Thus, a juvenile A.?heterodontus grew very fast, which is also indicated by its bone tissue type, composed of a high number of radial vascular canals and a fast-deposited bone matrix. The assignment of isolated bones from Lower to Middle Muschelkalk localities to A.?heterodontus is now possible with an extensive amended diagnosis of this taxon. This largely contributes to the understanding of taxonomical diversity and distribution. Morphological comparison of the postcranial skeleton of A.?heterodontus with that of the two other valid pachypleurosaurs from the Germanic Basin, Anarosaurus pumilio and Dactylosaurus, supports their close phylogenetic relationship. Furthermore, the skeleton of A.?heterodontus has no morphological or histological aquatic adaptation such as pachyostosis or pachyosteosclerosis and thus represents the least degree of aquatic adaptation within Pachypleurosauria.