Evidence Pareiasaurs had a Lifestyle Very Different From Modern Megafauna

Bone microstructure of pareiasaurs (Parareptilia) from the Karoo Basin, South Africa: implications for growth strategies and lifestyle habits

Authors:

Canoville et al

Abstract:

Numerous morphological studies have been carried out on pareiasaurs; yet their taxonomy and biology remain incompletely understood. Earlier works have suggested that these herbivorous parareptiles had a short juvenile period as compared to the duration of adulthood. Several studies further suggested an (semi-) aquatic lifestyle for these animals, but more recent investigations have proposed a rather terrestrial habitat.

Bone paleohistology is regarded as a powerful tool to assess aspects of tetrapod paleobiology, but few studies have been conducted on pareiasaurs. The present study assesses intra and inter-specific histovariability of pareiasaurs and provides fresh insights into their paleobiology, thereby permitting a re-evaluation of earlier hypotheses. Our sample comprises various skeletal elements and several specimens covering most of the taxonomic and stratigraphic spectrum of South African pareiasaurs, including large and basal forms from the Middle Permian, as well as smaller and more derived forms from the Late Permian.

Our results concerning size of elements and histological tissues show that for pareiasaurs, element size is not a good indicator of ontogenetic age, and furthermore, suggest that the specific diversity of the Middle Permian pareiasaurs may have been underestimated. The bone histology of these animals shows that they experienced a relatively rapid growth early in ontogeny. The periosteal growth later slowed down, but seems to have been protracted for several years during adulthood. Pareiasaur bone microanatomy is unusual for continental tetrapods, in having spongious stylopod diaphyses and thin compact cortices. Rigorous paleoecological interpretations are thus limited since no modern analogue exists for these animals.

Evidence of a High Metabolic Rate in Archosaurs

Palaeohistological Evidence for Ancestral High Metabolic Rate in Archosaurs

Authors:

Legendre et al

Abstract:

Metabolic heat production in archosaurs has played an important role in their evolutionary radiation during the Mesozoic, and their ancestral metabolic condition has long been a matter of debate in systematics and palaeontology. The study of fossil bone histology provides crucial information on bone growth rate, which has been used to indirectly investigate the evolution of thermometabolism in archosaurs. However, no quantitative estimation of metabolic rate has ever been performed on fossils using bone histological features. Moreover, to date, no inference model has included phylogenetic information in the form of predictive variables. Here we performed statistical predictive modelling using the new method of phylogenetic eigenvector maps on a set of bone histological features for a sample of extant and extinct vertebrates, in order to estimate metabolic rates of fossil archosauromorphs. This modelling procedure serves as a case study for eigenvector-based predictive modelling in a phylogenetic context, as well as an investigation of the poorly known evolutionary patterns of metabolic rate in archosaurs. Our results show that Mesozoic theropod dinosaurs exhibit metabolic rates very close to those found in modern birds, that archosaurs share an higher ancestral metabolic rate than that of extant ectotherms, and that this derived high metabolic rate was acquired at a much more inclusive level of the phylogenetic tree, among non-archosaurian archosauromorphs. These results also highlight the difficulties of assigning a given heat production strategy (i.e. endothermy, ectothermy) to an estimated metabolic rate value, and confirm findings of previous studies that the definition of the endotherm/ectotherm dichotomy may be ambiguous.

Anisian Triassic Dinosauriform Asilisaurus kongwe Just Complicated Dinosauriform Ontogeny

The femoral ontogeny and long bone histology of the Middle Triassic (?late Anisian) dinosauriform Asilisaurus kongwe and implications for the growth of early dinosaurs

Authors:

Griffin et al

Abstract:

The ontogeny of early-diverging dinosauromorphs is poorly understood because few ontogenetic series from the same species-level taxon are known and what is available has not been extensively documented. The large numbers of skeletal elements of the silesaurid Asilisaurus kongwe recently recovered from Tanzania provide an opportunity to examine the ontogenetic trajectory of the earliest known member of Ornithodira and one of the closest relatives to Dinosauria. We examined the ontogeny of the femur and the histology of a series of long bone elements. We observed bone scar variation in a series of femora (n = 27) of different lengths (73.8–177.2 mm). We hypothesize that most femora follow a similar developmental trajectory; however, we observed sequence polymorphism in the order of appearance and shape of bone scars, and we quantified this polymorphism using ontogenetic sequence analysis (OSA). Additionally, five femora, three tibiae, a fibula, and a humerus were thin-sectioned to examine osteological tissues. No lines of arrested growth (LAGs) are present in any specimen, and there is little histological information about the ontogenetic stage of femora, although none have slowed or ceased growth. The woven-fibered bone present in the cortex of elements sectioned is similar to that of the earliest dinosaurs. This sequence polymorphism provides an alternate hypothesis for the robust/gracile dichotomy found in early dinosaurs often interpreted as sexual dimorphism. The shared femoral features found in Asilisaurus and early dinosaurs suggest that this ontogenetic pattern is plesiomorphic for Dinosauria, and that size is a poor predictor of maturity in early dinosauriforms.

Appears Dimetrodon Relative Ophiacodon was Warm Blooded

Most people know that ‘warm-bloodedness’ is a characteristic of mammals. This trait actually encompasses a suite of physiological processes that help to maintain a relatively high, constant body temperature using heat generated internally. A new study by Christen Don Shelton of the University of Cape Town, South Africa and his colleague, Martin Sander at the University of Bonn, Germany, presented at this year’s Society of Vertebrate Paleontology meeting, shows that this character may have shown up in the ancestors of modern mammals far earlier than was previously thought.

One associated effect of being ‘warm-blooded’ is a relatively fast growth-rate. Mammals (and birds, who are also ‘warm-blooded’) tend to grow much faster than ‘cold-blooded’ vertebrates, like fish and reptiles. This fast growth rate is in turn associated with a particular type of bone growth pattern, called fibrolamellar bone (FLB). Both mammals and birds have FLB, and Shelton and his colleague investigated its presence in an early fossil relative of mammals, Ophiacodon.

Ophiacodon is distantly related to the large sail-back reptile, Dimetrodon, that people may be familiar with, and lived in North America around 280-300 million years ago. Although it didn’t look particularly mammal-like (you could be forgiven for calling it a ‘lizard’), it has many characters that link it with mammals. The highly vascularized tissue had previously been observed in Ophiacodon, but its presence had been written off to ecological factors, like its aquatic lifestyle, rather than to its fundamental physiology. Shelton looked at a number of bones of Ophiacodon of individuals of different ages, and found that the more likely explanation is that Ophiacodon was at least partly ‘warm-blooded’

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Paleohistology of Temnospondyls Micropholis stowi and Lydekkerina huxleyi

Paleohistology of Micropholis stowi (Dissorophoidea) and Lydekkerina huxleyi (Lydekkerinidae) humeri from the Karoo Basin of South Africa, and implications for bone microstructure evolution in temnospondyl amphibians

Author:

McHugh

Abstract:

Temnospondyl amphibians are a large and diverse group of early tetrapods, whose paleohistology has been incompletely studied. Here, humeri of Micropholis stowi and Lydekkerina huxleyi from the Karoo Basin of South Africa (Katberg Formation) were thin–sectioned for paleohistological analysis. Diaphyseal bone histology of both taxa exhibits a convergence to fibrolamellar tissue and an absence of lines of arrested growth; additionally, medullary cavities free of trabeculae support terrestrial lifestyles in both Micropholis and Lydekkerina. The presence of azonal tissue in Micropholis is unlike that of other dissorophoids or extant caudatans, suggesting an adaptation to local conditions in the Early Triassic of the Karoo Basin, as well as a complicated and incompletely studied pattern of histological evolution in dissorophoids. Additionally, the propodial histology of these and 12 other taxa were assessed through different broad–scale phylogenetic hypotheses for Temnospondyli. Results reveal convergence towards sustained, non–cyclical growth and an absence of lines of arrested growth in the diaphyses of Early Triassic temnospondyls. The optimization of histological traits on to existing phylogenetic hypotheses is equally parsimonious between the different topologies. Homoplasy among histological characters suggests that evolutionary history in this group is overshadowed by developmental plasticity in bone microstructure, potentially due to environmental and biomechanical constraints. However, the interpretation of these data is limited by small sample size, and increased sampling is required to validate the patterns revealed in this study.

Rhynchosaurs Grew Like Archosaurs

Osteohistology of hyperodapedontine rhynchosaurs from the Upper Triassic of Southern Brazil

Authors:

Veiga et al

Abstract:

The first osteohistological study focused exclusively on rhynchosaurs (non-archosauriform archosauromorphs), based on the hyperodapedontines Teyumbaita sulcognathus and Hyperodapedon sp., from the Upper Triassic of Southern Brazil, indicates a relatively rapid growth rate in early ontogeny shown by the fibrolamellar complex, with a change to slow intermittent growth during late ontogeny represented by parallel-fibred bone with several growth marks. Contrary to previous studies, which described a typical non-archosaur reptilian bone tissue pattern for rhynchosaurs, with growth marks extending across the entire cortex, we demonstrate that, in both studied taxa, the initial growth rate was faster in comparison to the later. This suggests that the ability rapid growth at high rates was already present in basal non-archosauriform archosauromorphs.

Observing the Lilliput Effects in Therocephalians Across the Permian Triassic Mass Extinction

Bone microstructure and the evolution of growth patterns in Permo-Triassic therocephalians (Amniota, Therapsida) of South Africa

Authors:

Huttenlocker et al

Abstract:

Therocephalians were a speciose clade of nonmammalian therapsids whose ecological diversity and survivorship of the end-Permian mass extinction offer the potential to investigate the evolution of growth patterns across the clade and their underlying influences on post-extinction body size reductions, or ‘Lilliput effects’. We present a phylogenetic survey of limb bone histology and growth patterns in therocephalians from the Middle Permian through Middle Triassic of the Karoo Basin, South Africa. Histologic sections were prepared from 80 limb bones representing 11 genera of therocephalians. Histologic indicators of skeletal growth, including cortical vascularity (%CV) and mean primary osteon diameters (POD), were evaluated in a phylogenetic framework and assessed for correlations with other biologically significant variables (e.g., size and robusticity). Changes in %CV and POD correlated strongly with evolutionary changes in body size (i.e., smaller-bodied descendants tended to have lower %CV than their larger-bodied ancestors across the tree). Bone wall thickness tended to be high in early therocephalians and lower in the gracile-limbed baurioids, but showed no general correlation with cross-sectional area or degree of vascularity (and, thus, growth). Clade-level patterns, however, deviated from previously studied within-lineage patterns. For example, Moschorhinus, one of few therapsid genera to have survived the extinction boundary, demonstrated higher %CV in the Triassic than in the Permian despite its smaller size in the extinction aftermath. Results support a synergistic model of size reductions for Triassic therocephalians, influenced both by within-lineage heterochronic shifts in survivor taxa (as reported in Moschorhinus and the dicynodont Lystrosaurus) and phylogenetically inferred survival of small-bodied taxa that had evolved short growth durations (e.g., baurioids). These findings mirror the multi-causal Lilliput patterns described in marine faunas, but contrast with skeletochronologic studies that suggest slow, prolonged shell secretion over several years in marine benthos. Applications of phylogenetic comparative methods to new histologic data will continue to improve our understanding of the evolutionary dynamics of growth and body size shifts during mass extinctions and recoveries.

Hidden Pterosaur Diversity in Late Cretaceous Hungary

Does morphology reflect osteohistology-based ontogeny? A case study of Late Cretaceous pterosaur jaw symphyses from Hungary reveals hidden taxonomic diversity

Authors:

Prondvai et al

Abstract:

With a single complete mandible and 56 mandibular symphyseal fragments of various sizes, the Late Cretaceous Hungarian azhdarchid material has been considered one of the most extensive monospecific pterosaur assemblages in the world. Representing a broad size range, these elements have been thought to demonstrate a developmental series of Bakonydraco galaczi. As such, they were ideal to test whether absolute size and/or morphology reliably indicate relative ontogenetic stages in this pterosaur. Forty-five specimens were selected for multivariate morphometrics and classified into four size classes. After acquiring the morphometric data set, we thin-sectioned eight symphyses representing all size groups and classified them into relative ontogenetic stages based on qualitative microstructural inspection prior to quantitative histological analyses. Microstructural characters suggestive of developmental state were then quantified for intra- and interindividual uni- and multivariate analyses to test the correspondence among the results of qualitative and quantitative analyses. In contrast to our expectations, histological features identified the smallest specimen as an adult and not an early juvenile. The substantial size difference between this specimen and other adults, along with its distinct microanatomical and histological features, implies the presence of at least two pterosaur taxa in this symphysis assemblage. This hypothesis is further supported by multivariate morphometrics, which separate the smallest symphyses from all other specimens that form one continuous group. Although the latter group also shows considerable size variability in corresponding ontogenetic stages, this suggests developmental plasticity rather than the presence of even more taxa, and indicates that symphysis size and morphology are poor indicators of skeletal maturity in these animals. Hence, bone histology is an important independent test of the assessment of ontogenetic stage using size and morphology.

Permian Stereospondyl Rhinesuchus was a Long Lived Taxon

Paleohistology and histovariability of the Permian stereospondyl Rhinesuchus

Authors:

Julie McHugh

Abstract:

Rhinesuchids are a basal group of stereospondyls, one of the most successful groups of early amphibians. They are also the only group of stereospondyl amphibians present prior to the Permian–Triassic boundary. Here, Rhinesuchus postcranial material is sampled for paleohistological analysis for the first time and gives us a model for growth in basal stereospondyls. Bone microstructure confirms an aquatic lifestyle for Rhinesuchus, and indicates that it was a long-lived taxon (greater than 30 years), growing seasonally like other amphibians. The shaft of the iliac dorsal process preserves the largest number of rest lines, suggesting it as a preferred element to estimate minimum age in basal stereospondyls. Femoral diaphyseal sections are readily comparable to distal rib sections for skeletochronological purposes, but preserve fewer rest lines than the ilium. Narrowly banded annuli and rest lines in the inner cortex of Late Permian elements indicate a taxon that was able to weather successive seasons of harsh conditions, and perhaps indicates a reason for the success of Stereopsondyli through the Permo-Triassic mass extinction.

Bone Histology Hints at Mosasaur Paleobiology and Evolution

Microanatomical and Histological Features in the Long Bones of Mosasaurine Mosasaurs (Reptilia, Squamata) – Implications for Aquatic Adaptation and Growth Rates

Authors:

Alexandra Houssaye, Johan Lindgren, Rodrigo Pellegrini, Andrew H. Lee, Damien Germain and Michael J. Polcyn

Abstract:
Background

During their evolution in the Late Cretaceous, mosasauroids attained a worldwide distribution, accompanied by a marked increase in body size and open ocean adaptations. This transition from land-dwellers to highly marine-adapted forms is readily apparent not only at the gross anatomic level but also in their inner bone architecture, which underwent profound modifications.

Methodology/Principal Findings

The present contribution describes, both qualitatively and quantitatively, the internal organization (microanatomy) and tissue types and characteristics (histology) of propodial and epipodial bones in one lineage of mosasauroids; i.e., the subfamily Mosasaurinae. By using microanatomical and histological data from limb bones in combination with recently acquired knowledge on the inner structure of ribs and vertebrae, and through comparisons with extant squamates and semi-aquatic to fully marine amniotes, we infer possible implications on mosasaurine evolution, aquatic adaptation, growth rates, and basal metabolic rates. Notably, we observe the occurrence of an unusual type of parallel-fibered bone, with large and randomly shaped osteocyte lacunae (otherwise typical of fibrous bone) and particular microanatomical features in Dallasaurus, which displays, rather than a spongious inner organization, bone mass increase in its humeri and a tubular organization in its femora and ribs.

Conclusions/Significance

The dominance of an unusual type of parallel-fibered bone suggests growth rates and, by extension, basal metabolic rates intermediate between that of the extant leatherback turtle, Dermochelys, and those suggested for plesiosaur and ichthyosaur reptiles. Moreover, the microanatomical features of the relatively primitive genus Dallasaurus differ from those of more derived mosasaurines, indicating an intermediate stage of adaptation for a marine existence. The more complete image of the various microanatomical trends observed in mosasaurine skeletal elements supports the evolutionary convergence between this lineage of secondarily aquatically adapted squamates and cetaceans in the ecological transition from a coastal to a pelagic lifestyle.