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Measured values for all seven osteohistological features, on humeri obtained from new specimens sampled for this study.
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The study of bone growth rate and metabolic rate evolution in archosaurs (crocodiles, dinosaurs including birds, and pterosaurs) and close outgroups has become a subject of major interest among paleontologists in recent years. In this paper, we estimate the bone growth rate of Euparkeria using a new statistical inference model for the humerus. We m...
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... orientation of these cav- ities was computed as the angle between the major axis of each ellipse and a vector at a tangent to the bone periphery; thus, vascu- lar canals extending parallel to the bone periphery have angles ap- proaching 0 • and those extending parallel to the radius of the bone cross-section have angles approaching 90 • (de Boef and Larsson, 2007). Vascular canal orientation is a continuously varying trait; to incorporate this trait in our character matrix, we categorized this continuous variation into three orientation classes (see Table 1). These types of standard vascular canal orientation were defined in our transverse sections as follows: circular canals (C), which run roughly parallel to the bone periphery (0 • + 22.5 • ; 180 • − 22.5 • ); radial canals (R), which run roughly orthogonal to the bone pe- riphery (90 • ± 22.5 • ); and oblique canals (O), i.e., those canals excluded from the intervals corresponding to radial canals and to circular ones (see de Margerie et al., 2002de Margerie et al., , 2004de Boef and Larsson, 2007) R + O]). ...
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... Generally, low metabolic rates would be expected for heavily armored, herbivorous aetosaurs and for ambush-predatory phytosaurs and crocodylians. In contrast, high rates of bone growth have been found in Triassic terrestrial nonarchosaurian archosauromorphs, including Prolacerta, Proterosuchus, Erythrosuchus, Chanaresuchus, and Euparkeria, which is thought to be consistent with endothermy (Legendre et al. 2013). Bone histology and growth rates have been used to quantify metabolic rates between extinct and extant vertebrates, showing that Prolacerta, Garjainia, Euparkeria, Postosuchus, and ...
... Therefore, it is not possible to test whether the assumption of cylindricality has been met and whether the method can be considered at all reliable. Even with more-or-less cylindrical canals (aspect ratio 1:1.25), the estimation of radial angle could be quite inaccurate and therefore reduce the validity of any studies using radial orientations to estimate, for example, growth rates [70,109,143] or bone loading [21]. The results of any studies applying these methods should therefore be taken with caution. ...
Accurately estimating developmental age and life history traits in fossils is crucial for identifying and classifying extinct species and understanding how biological attributes evolved. The evolution of life history traits such as growth pattern is far from clear in birds, and development has been studied in only a handful of modern species. The exceptionally rapid growth of modern birds means ageing methods based on annual incremental growth lines, used in other vertebrates, are inapplicable to birds and robust alternative methods remain to be established. Analysis of avian intracortical bone microstructure, which varies both with age and tissue deposition rate, is a promising approach already used in palaeobiology. However, current thin section-based histological methods are destructive. Moreover, to date, most microstructural studies in avian bone are qualitative, 2D, and involve a limited range of extant species. The objective of this study was to investigate cortical bone microstructure and developmental age and life history traits in living birds, to identify phenotypes which can then be applied to examination of the fossil record, using minimally-destructive high-resolution 3D imaging. First, the necessity of 3D measurement was tested: a combination of idealised, simulated datasets and real synchrotron-based computed tomography (SR CT) datasets were used to compare published methods for measuring key microstructural traits based on 2D sections and 3D volumes. Next, SR CT imaging and quantitative measurements were used to characterise age-related changes in bone microstructure in a range of extant bird species: growth series ducks and pheasants, and a smaller sample size in starlings, rock doves, partridges, and ostrich. The methods tested in modern material were applied to fossils as a proof-of concept. It was found that 3D quantification methods are required for measuring vascular canal orientation and osteocyte lacunar shape and volume, though 2D sections could be used to measure traits such as bone volume fraction (BV/TV) and osteocyte lacunar volume. In all species studied, juvenile, subadult, and adult species could be distinguished by their values of BV/TV, and further information could be added using measured values of vascular canal diameter as well as qualitative assessment. Using a synchrotron-based CT system, high-resolution 3D datasets comparable to modern bone samples were obtained from fossils, and preliminary estimates of developmental age can be made. Further work may reveal more changes within juvenile age stages, and better characterise the variation within extant birds, allowing more accurate interpretation of the fossil record. Therefore developmental studies in a greater number of extant bird species are required using larger sample sizes, to support and add to the results presented in this thesis.
... Postosuchus likely had a similar BMR to Poposaurus. Histology shows an elevated rate of growth compared to modern crocodilians, but less so than seen in dinosauriforms or even the fastest growing loricatans [104,105]. BMR and target core temperature (35 °C) were the same as used as for Poposaurus. Osteoderms are known for Postosuchus, so it can be unambiguously assigned to a skin type similar to living crocodilians [103]. ...
The biogeography of terrestrial amniotes is controlled by historical contingency interacting with paleoclimate, morphology and physiological constraints to dispersal. Thermal tolerance is the intersection between organismal requirements and climate conditions which constrains modern organisms to specific locations and was likely a major control on ancient tetrapods. Here, we test the extent of controls exerted by thermal tolerance on the biogeography of 13 Late Triassic tetrapods using a mechanistic modeling program, Niche Mapper. This program accounts for heat and mass transfer into and out of organisms within microclimates. We model our 13 tetrapods in four different climates (cool and warm at low and high latitudes) using environmental conditions that are set using geochemical proxy-based general circulation models. Organismal conditions for the taxa are from proxy-based physiological values and phylogenetic bracketing. We find that thermal tolerances are a sufficient predictor for the latitudinal distribution of our 13 test taxa in the Late Triassic. Our modeled small mammaliamorph can persist at high latitudes with nocturnal activity and daytime burrowing but large pseudosuchians are excluded because they cannot seek nighttime shelter in burrows to retain elevated body temperatures. Our work demonstrates physiological modeling is useful for quantitative testing of the thermal exclusion hypothesis for tetrapods in deep time.
... Considering that bone growth rates are significantly related to RMR in amniotes (Montes et al. 2007), the former was used by Cubo et al. (2012) as a proxy to infer the thermometabolic status of extinct archosaurs. This method was used by Legendre et al. (2013) to infer the bone growth rate and the thermometabolic status of Euparkeria. In a second step, Legendre et al. (2016) adapted Guénard et al.'s (2013) PEMs to perform paleobiological inferences of RMR. ...
Notosuchia is a group of mostly terrestrial crocodyliforms. The presence of a prominent crest over-hanging the acetabulum, slender straight-shafted long bones with muscular insertions close to the joints, and a stable knee joint suggests that they had an erect posture. This stance has been proposed to be linked to endo-thermy, because it is present in mammals and birds and contributes to the efficiency of their respiratory systems. However, a bone paleohistological study unexpectedly suggested that Notosuchia were ectothermic organisms. The thermophysiological status of Notosuchia deserves further analysis, because the methodology of the previous study can be improved. First, it was based on a relationship between red blood cell size and bone vascular canal diameter tested using 14 extant tetrapod species. Here we present evidence for this relationship using a more comprehensive sample of extant tetrapods (31 species). Moreover, contrary to previous results, bone cross-sectional area appears to be a significant explanatory variable (in addition to vascular canal diameter). Second, red blood cell size estimations were performed using phylogenetic eigen-vector maps, and this method excludes a fraction of the phylogenetic information. This is because it generates a high number of eigenvectors requiring a selection procedure to compile a subset of them to avoid model overfitting. Here we inferred the thermophysiology of Notosuchia using phylogenetic logistic regressions, a method that overcomes this problem by including all of the phylogenetic information and a sample of 46 tetrapods. These analyses suggest that Araripesuchus wegeneri, Armadillosuchus arrudai, Baurusuchus sp., Iber-osuchus macrodon, and Stratiotosuchus maxhechti were ectothermic organisms.
... This pattern of occurrences of both endothermy and ectothermy within closely related amniotic taxa through deep time has been described by Cubo & Jalil (2019, p. 327) as a "flickering on and off" of bradymetabolism and tachymetabolism. Other examples can be found in Botha-Brink & Smith (2011), Legendre, Segalen & Cubo (2013) and Appendix S1. ...
... Numerous recent studies have relied on the use of FLB as an indicator of high bone growth rate and, in turn, tachymetabolism (e.g. Padian, de Ricqlès & Horner, 2001;Montes et al., 2007;de Ricqlès et al., 2008;Cubo et al., 2012;Houssaye, 2013;Legendre et al., 2013;Padian & Lamm, 2013;Stein & Prondvai, 2014;Klein, Foth & Schoch, 2017). The timing of our survey is fortunate because it follows the emergence of improved quantitative techniques for analysing osteohistological attributes that allow inferences about the metabolic status of fossil samples by comparing them with equivalent attributes of extant ectotherms and endotherms whose metabolic rates are known (Legendre et al., 2016;Olivier et al., 2017;Fleischle, Wintrich & Sander, 2018;Cubo & Jalil, 2019). ...
The whole‐body (tachymetabolic) endothermy seen in modern birds and mammals is long held to have evolved independently in each group, a reasonable assumption when it was believed that its earliest appearances in birds and mammals arose many millions of years apart. That assumption is consistent with current acceptance that the non‐shivering thermogenesis (NST) component of regulatory body heat originates differently in each group: from skeletal muscle in birds and from brown adipose tissue (BAT) in mammals. However, BAT is absent in monotremes, marsupials, and many eutherians, all whole‐body endotherms. Indeed, recent research implies that BAT‐driven NST originated more recently and that the biochemical processes driving muscle NST in birds, many modern mammals and the ancestors of both may be similar, deriving from controlled ‘slippage’ of Ca2+ from the sarcoplasmic reticulum Ca2+‐ATPase (SERCA) in skeletal muscle, similar to a process seen in some fishes. This similarity prompted our realisation that the capacity for whole‐body endothermy could even have pre‐dated the divergence of Amniota into Synapsida and Sauropsida, leading us to hypothesise the homology of whole‐body endothermy in birds and mammals, in contrast to the current assumption of their independent (convergent) evolution. To explore the extent of similarity between muscle NST in mammals and birds we undertook a detailed review of these processes and their control in each group. We found considerable but not complete similarity between them: in extant mammals the ‘slippage’ is controlled by the protein sarcolipin (SLN), in birds the SLN is slightly different structurally and its role in NST is not yet proved. However, considering the multi‐millions of years since the separation of synapsids and diapsids, we consider that the similarity between NST production in birds and mammals is consistent with their whole‐body endothermy being homologous. If so, we should expect to find evidence for it much earlier and more widespread among extinct amniotes than is currently recognised. Accordingly, we conducted an extensive survey of the palaeontological literature using established proxies. Fossil bone histology reveals evidence of sustained rapid growth rates indicating tachymetabolism. Large body size and erect stature indicate high systemic arterial blood pressures and four‐chambered hearts, characteristic of tachymetabolism. Large nutrient foramina in long bones are indicative of high bone perfusion for rapid somatic growth and for repair of microfractures caused by intense locomotion. Obligate bipedality appeared early and only in whole‐body endotherms. Isotopic profiles of fossil material indicate endothermic levels of body temperature. These proxies led us to compelling evidence for the widespread occurrence of whole‐body endothermy among numerous extinct synapsids and sauropsids, and very early in each clade's family tree. These results are consistent with and support our hypothesis that tachymetabolic endothermy is plesiomorphic in Amniota. A hypothetical structure for the heart of the earliest endothermic amniotes is proposed. We conclude that there is strong evidence for whole‐body endothermy being ancient and widespread among amniotes and that the similarity of biochemical processes driving muscle NST in extant birds and mammals strengthens the case for its plesiomorphy.
... Later in life, these rates slowed dramatically (~7.6 mm 2 /year between LAGs 3 and 4 and 12.5 mm 2 /year between LAGs 4 and 5). These growth rates are similar to those reported for aetosaurs, but considerably slower than those reported for avemetatarsalian archosaurs (Cubo, Le Roy, Martinez-Maza, & Montes, 2012;Legendre, Segalen, & Cubo, 2013;Padian, de Ricqlès, & Horner, 2001). Independent of evolutionary changes in life history strategy among early archosaurs, the slower growth of Revueltosaurus is not a surprise because of its small body size (cf. ...
Once known solely from dental material and thought to represent an early ornithischian dinosaur, the early‐diverging pseudosuchian Revueltosaurus callenderi is described from a minimum of 12 skeletons from a monodominant bonebed in the upper part of the Chinle Formation of Arizona. This material includes nearly the entire skeleton and possesses a combination of plesiomorphic and derived character states that help clarify ingroup relationships within Pseudosuchia. A phylogenetic analysis recovers R. callenderi in a clade with Aetosauria and Acaenasuchus geoffreyi that is named Aetosauriformes. Key autapomorphies of R. callenderi include a skull that is longer than the femur, a complete carapace of dermal armor including paramedian and lateral rows, as well as ventral osteoderms, and a tail end sheathed in bone. Histology of the femur and associated osteoderms demonstrate that R. callenderi was slow growing and that the individuals from the bonebed were not young juveniles but had not ceased growing. A review of other material assigned to Revueltosaurus concludes that the genus cannot be adequately diagnosed based on the type materials of the three assigned species and that only R. callenderi can be confidently referred to Revueltosaurus.
... Such studies have focused mostly on quantitative osteohistological features in a phylogenetic context, encouraged by the rise of cladistics in paleontology (Cracraft 1981), followed by that of PCMs and associated automated procedures and software to correlate and model quantitative traits in an evolutionary context (Paradis 2012, Garamszegi 2014. The identification of a strong phylogenetic signal in several histological traits (see Chapter 30), as well as a significant relationship between those variables and bone growth rate (Montes et al. 2007) led to the building of predictive models for bone growth rate based on phylogenetic regressions that used those traits as independent variables (Cubo et al. 2012, Legendre et al. 2013). These models identified several nonarchosaurian archosauromorphs, as well as nonavian dinosaurs and fossil pseudosuchians, as presenting high bone growth rates similar to those of extant mammals, and thus compatible with endothermy. ...
... However, Werning (2013) reinterpreted the material of Chanaresuchus bonapartei Romer, 1971, described by de Ricqlès et al., 2008 as a low growth tissue. Both presence and absence of fibrolamellar bone have been reported in archosauriforms (such as Euparkeria capensis Broom, 1913;de Ricqlès et al., 2008;Botha-Brick & Smith, 2011;Legendre et al., 2013;Werning, 2013). Within pseudosuchian archosaurs, fibrolamellar bone or woven bone has been observed in early ontogenetic stages of phytosaurs (Rutiodon Emmons, 1856), aetosaurs (Stagonolepis Agassiz, 1844;Desmatosuchus Case, 1920;Cope, 1875) and ornithosuchids (de Ricqlès et al. 2003a,b;Werning 2013). ...
Notosuchian crocodyliforms represent an intriguing group since they are mainly terrestrial forms and therefore with completely different lifestyles than extant crocodylian, which is reflected in their particular skeletal anatomy. Although there are some inferences in the literature related to the palaeoecology of notosuchian, little is known about their biology (e.g. metabolism, growth dynamics). The palaeohistology allows us to perform interpretations about the growth dynamics and strategies of growth in these extinct forms. Here, we worked on specimens of Araripesuchus Price, 1959 (Notosuchia, Uruguaysuchidae), coming from La Buitrera Palaeontological Area, Río Negro Province (northern Patagonia, Argentina). We described for the first time the osteohistology of this taxon, based on thin sections of the stylopodium shaft (femur and humerus) of four specimens, providing an assumption of its growth dynamics. A general slow growth rate is inferred for Araripesuchus, based on the poorly vascularized parallel‐fibred/lamellar bone matrix. An unusual pattern of bone deposition was observed in two specimens; we consider this tissue as evidence of a rapid growth event at some point in the ontogeny of these individuals. Finally, it can be interpreted that in Araripesuchus, sexual maturity could be reached at least between eight to thirteen years old. This study is a first step to provide insight into the life history of these terrestrial notosuchids and to provide new empirical evidence for the osteohistological variability and palaeoecology of this peculiar group of extinct crocodyliforms.
... Such studies have focused mostly on quantitative osteohistological features in a phylogenetic context, encouraged by the rise of cladistics in paleontology (Cracraft 1981), followed by that of PCMs and associated automated procedures and software to correlate and model quantitative traits in an evolutionary context (Paradis 2012, Garamszegi 2014. The identification of a strong phylogenetic signal in several histological traits (see Chapter 30), as well as a significant relationship between those variables and bone growth rate (Montes et al. 2007) led to the building of predictive models for bone growth rate based on phylogenetic regressions that used those traits as independent variables (Cubo et al. 2012, Legendre et al. 2013). These models identified several nonarchosaurian archosauromorphs, as well as nonavian dinosaurs and fossil pseudosuchians, as presenting high bone growth rates similar to those of extant mammals, and thus compatible with endothermy. ...
... Therefore, it is not possible to test whether the assumption of cylindricality has been met and whether the 2D method can be considered reliable. Even with approximately cylindrical canals (aspect ratio 1:1.25), the estimation of the radial angle θ was not robust (r 2 = 0.61) and, therefore, reduces the validity of any studies using radial orientations to estimate, for example, growth rates (Cubo et al., 2012;Legendre et al., 2013Legendre et al., , 2014 or bone loading . ...
Describing and quantifying vascular canal orientation and volume of osteocyte lacunae in bone is important in studies of bone growth, mechanics, health and disease. It is also an important element in analysing fossil bone in palaeohistology, key to understanding the growth, life, and death of extinct animals. Often, bone microstructure is studied using two-dimensional (2D) sections, and three-dimensional (3D) shape and orientation of structures are estimated by modelling the structures using idealised geometries based on information from their cross sections. However, these methods rely on structures meeting strict geometric assumptions. Recently, 3D methods have been proposed which could provide a more accurate and robust approach to bone histology, but these have not been tested in direct comparison with their 2D counterparts in terms of accuracy and sensitivity to deviations from model assumptions. We compared 2D and 3D methodologies for estimating key microstructural traits using a combination of experimental and idealised test datasets. We generated populations of cylinders (canals) and ellipsoids (osteocyte lacunae), varying the cross-sectional aspect ratios of cylinders and orientation of ellipsoids to test sensitivity to deviations from cylindricality and longitudinal orientation, respectively. Using published methods, based on 2D sections and 3D datasets, we estimated cylinder orientation and ellipsoid volume. We applied the same methods to six CT datasets of duck cortical bone, using the full volumes for 3D measurements and single CT slices to represent 2D sections. Using in silico test datasets that did deviate from ideal cylinders and ellipsoids resulted in inaccurate estimates of cylinder or canal orientation, and reduced accuracy in estimates of ellipsoid and lacunar volume. These results highlight the importance of using appropriate 3D imaging and quantitative methods for quantifying volume and orientation of 3D structures and offer approaches to significantly enhance our understanding of bone physiology based on accurate measures for bone microstructures.
