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Bone profiler: A tool to quantify, model, and statistically compare bone-section compactness profiles
... In 2003, a computer program named Bone Profiler was produced to model bone tissue distribution in sections (Girondot and Laurin 2003). The main idea was to reduce bone section complexity to a limited number of variables that can be further compared using statistical tests. ...
... More recently, we were contacted by several researchers noting that the last available version of the software had stopped working on recent computers. They expressed concerns, because the method described in Girondot and Laurin (2003) has become a standard method in paleobiology, and it is important to continue to make it available for paleobiological and comparative studies. We produced a new enhanced version of the method and the software to fulfill this need. ...
... The center of the section is not generally a correct estimate of the center of the bone that should be used to model compactness, because bone deposition rate on the outer surface and bone resorption rate in the medullary cavity are usually anisotropic. The "ontogenetic" center corrects for this effect and should be the preferred center used for most analyses (Girondot and Laurin 2003). All the detected centers can be shown superimposed on the original image using the function plot() ( Figure 1A). ...
Bone sections have been widely used for over a century to assess life history traits of extant and extinct vertebrates, and they remain extremely useful. The charac- terization of their geometric and microanatomical properties forms the core of many descriptive and inferential studies. Bone compactness in particular has been associated with various attributes in individuals, such as habitat use or specific morphofunctional traits. A method implemented in software was published in 2003 to reduce the complexity of bone sections to facilitate quantitative analyses. We improve this method using better statistical tools (maximum likelihood and Bayesian analysis), a new func- tion to model compactness, and we propose new enhanced software, BoneProfileR, as an R package, along with an online version for users unfamiliar with this language. Application of the new method to the femur of an extant hedgehog (Erinaceus europaeus) and a Permian temnospondyl (Eryops megacephalus) allows us to quantitatively and objectively describe the cross-sectional microanatomy of these two taxa.
... We prepared thin sections to quantify the relative area (in percentages) occupied by bone tissue (global compactness, Cg), as well as the relative width of the transition zone between the medulla and the cortex (S), the distance of this transition zone from the center of the sections (P), and the minimum (Min) and maximum (Max) values of bone compactness. 11 In general, the limb bones of Paratethyan seals are uniformly compact in both transverse and longitudinal sections (Cg = 97%-100%), with no medullary cavity or extensive cancellous core (Figures 2H-2N and S2; Table S4). They typically show low values of S and small differences between Min and Max. ...
... Automated statistical calculations were made with the software Prism (GraphPad ed.). Microanatomical terminology follows Francillon-Vieillot et al. 44 and Prondvai et al. 45 For further details, see Girondot and Laurin 11 and GraphPad (http://www.graphpad.com/scientific-software/prism/). ...
... All (statistical) calculations were performed automatically by the software, cancelling the need for the authors to make assumptions of the statistical approach and, thus, canceling the need for the use of methods to determine whether the data met these assumptions. For further details, see Girondot and Laurin 11 and GraphPad (http://www.graphpad.com/scientific-software/ prism/). ...
Pachyosteosclerosis—a condition that creates dense, bulky bones—often characterizes the early evolution of secondarily aquatic tetrapods like whales and dolphins1, 2, 3 but then usually fades away as swimming efficiency increases.⁴ Here, we document a remarkable reversal of this pattern, namely the convergent re-emergence of bone densification in Miocene seals, dolphins, and whales from the epicontinental Paratethys Sea of eastern Europe and central Asia. This phenomenon was driven by imbalanced remodeling and inhibited resorption of primary trabeculae and coincided with hypersaline conditions—the Badenian salinity crisis—that affected the Central Paratethys between 13.8 and 13.4 Ma.⁵ Dense bones acting as ballast would have facilitated efficient swimming in the denser and more buoyant water and hence were likely adaptive in this setting. From the Central Paratethys, pachyosteosclerosis subsequently spread eastward, where it became a defining feature of the endemic late Miocene whale assemblage.
... b Compactness profile indices for rib and humerus (Cg, Cc, Cp, S and P). Measured using Bone Profiler [25]. Each cross-section picture was converted to a binary image using Adobe Photoshop CS6 attenuate), Chinese white dolphin (Sousa chinensis), baiji (Lipotes vexillifer), finless porpoise (Neophocaena asiaeorientalis), common bottlenose dolphin (Tursiops truncatus), cow (Bos taurus), pig (Sus scrofa), sheep (Ovis aries), and dog (Canis lupus familiaris). ...
... Bone sections were prepared as outlined by Canoville et al. and by Hayashi and colleagues [12,19] (Fig. 1a). (2) To improve the sample size, sample images and information of more species was retrieved from previous various studies [2,6,12,13,19,25]. ...
... We employed binary images of thin sections and assessed bone density using Bone Profiler [25], to obtain the variables S (relative width of the transition zone between the medullary and the cortical regions) and P (proportional to the size of the medullary cavity) for each section. The compactness of the center/periphery/ whole of bone sections was calculated using Image-Pro Plus, to obtain the variables Cg (globe compactness, ranging from 0~1), Cc (compactness in the center of the section. ...
Background:
The transition from land to sea by the ancestor of cetaceans approximately 50 million years ago was an incredible evolutionary event that led to a series of morphological, physiological, and behavioral adaptations. During this transition, bone microstructure evolved from the typical terrestrial form to the specialized structure found in modern cetaceans. While the bone microstructure of mammals has been documented before, investigations of its genetic basis lag behind. The increasing number of cetaceans with whole-genome sequences available may shed light on the mechanism underlying bone microstructure evolution as a result of land to water transitions.
Results:
Cetacean bone microstructure is consistent with their diverse ecological behaviors. Molecular evolution was assessed by correlating bone microstructure and gene substitution rates in terrestrial and aquatic species, and by detecting genes under positive selection along ancestral branches of cetaceans. We found that: 1) Genes involved in osteoclast function are under accelerated evolution in cetaceans, suggestive of important roles in bone remodeling during the adaptation to an aquatic environment; 2) Genes in the Wnt pathway critical for bone development and homeostasis show evidence of divergent evolution in cetaceans; 3) Several genes encoding bone collagens are under selective pressure in cetaceans.
Conclusions:
Our results suggest that evolutionary pressures have shaped the bone microstructure of cetaceans, to facilitate life in diverse aquatic environments.
... Bone compactness parameters were calculated using Bone Profiler (Girondot & Laurin, 2003). To prepare the dataset for this approach the images were segmented into binary images in Photoshop CC 2023 (Adobe Systems). ...
... CDI is the ratio of the section that is taken up by the cortex: CDI = external diameter-internal diameter/external diameter (Castanet et al., 2000). 4S is the slope at point P (p = 1-CDI) and it is roughly the extent of the cortical transition zone (Girondot & Laurin, 2003). C g is the compactness of the entire section. ...
Orthosuchus stormbergi was a small‐bodied crocodyliform, representative of a diverse assemblage of Early Jurassic, early branching crocodylomorph taxa from the upper Elliot Formation of South Africa. The life history of these early branching taxa remains poorly understood, with only sparse investigations into their osteohistology, yet species like Orthosuchus have potential to inform about the macroevolution of growth strategies on the stem leading to crown crocodilians. In order to elucidate the growth patterns of Orthosuchus , we used propagation phase contrast X‐ray synchrotron micro‐computed tomography to virtually image the osteohistology of the postcrania of two specimens, including multiple elements from the type (SAM‐PK‐K409), and the femur of a referred specimen (BP/1/4242). In total, we scanned nine mid‐diaphyseal sections of the humerus, radius, ulna, radiale, femur, tibia, fibula, and a rib. We then compared our results to osteohistological sections of crocodylomorph taxa from the published literature. Our results show that the most predominant bone tissue type in Orthosuchus is lamellar, with a few patches of woven and parallel‐fibred bone. The type specimen contains four to five lines of arrested growth and the hindlimb elements present outer circumferential lamellae, whereas the referred specimen contains six to seven. Both specimens grew at similar rates, reaching adult skeletal body size at year four or five. The sectioned bones, most notably the radius and ulna, are comparatively thick walled and compact. Our virtual osteohistological sections are one of the first for an early branching crocodyliform, and the broad sample of skeletal elements makes Orthosuchus a key anchor point for understanding the plesiomorphic life history traits of the clade.
... Calibration slide and ImageJ software were used to generate scale bars. To evaluate potential differences in bone compactness profiles among samples, we followed the procedure proposed by Girondot and Laurin (2003). Photomicrographs of the well-preserved samples (e.g., those with very few fractures and deformations) were converted into binary 8-bit images using Adobe Photoshop CC (Adobe Systems ® ) and then imported into Bone Profiler software (Girondot & Laurin, 2003). ...
... To evaluate potential differences in bone compactness profiles among samples, we followed the procedure proposed by Girondot and Laurin (2003). Photomicrographs of the well-preserved samples (e.g., those with very few fractures and deformations) were converted into binary 8-bit images using Adobe Photoshop CC (Adobe Systems ® ) and then imported into Bone Profiler software (Girondot & Laurin, 2003). The latter software estimates the relative area of cross-sections occupied by mineralized bone tissues, creating a compactness profile of each section. ...
Osteohistological evidence is widely used to infer paleobiological traits of fossil vertebrates, such as ontogeny and growth rates. Mesosaurs, an enigmatic group of aquatic reptiles from the early Permian, are the most well‐known Paleozoic amniotes from Africa and South America. Their fossils are abundant in South America, ranging from the central‐west region of Brazil to the southernmost areas, as well as parts of Paraguay and Uruguay. In this contribution, we examined the bone microstructure of Mesosaurus tenuidens by analyzing thin sections of axial and appendicular elements of several specimens collected from various Brazilian sites. The microstructure of the bones showed minimal histological variability among elements, predominantly composed of parallel‐fibered tissues, indicating slow growth rhythm, along with increased bone density attributed to pachyosteosclerosis. The cortical area consists of poorly vascularized parallel‐fibered bone tissue, which was interrupted by multiple cyclical growth marks, some of them being supernumerary, suggesting a strong influence of seasonality. Moreover, the organization of growth marks suggests distinct life history trajectories among individuals collected from different outcrops, reflecting environmental heterogeneity throughout the basin. Internally, the endosteal domain exhibits greater vascularization compared to the cortices and frequently contained calcified cartilage. In the ontogenetic series, there was a progressive filling of the medullary region from small to large individuals. The presence of the External Fundamental System (a proxy indicating somatic maturity) was observed in femora and ribs, suggesting that determinate growth was already occurring in Permian mesosaurs and may not be an exclusive specialization of crown amniotes.
... In this article, we use elliptic Fourier transforms to study the angular variation of several microanatomical parameters measured on mid-diaphyseal transverse sections of reptile femora with the BoneProfileR software (Girondot & Laurin, 2003;Gônet et al., 2022), such as bone compactness and the distance from the centre of the cross-section of the medullocortical transition, in order to quantitatively test for the first time if there is a relationship between locomotion and angular microanatomy in reptiles. We hypothesise that angular bone compactness varies according to the different mechanical constraints experienced by the femur of reptiles using different modes of locomotion. ...
... Some scans were of modest quality, so we increased the resolution using bicubic interpolation in ImageJ. Finally, we binarised the cross-sections before taking our microanatomical measurements with BoneProfileR v. 2.0-7 (Girondot & Laurin, 2003;Gônet et al., 2022). ...
Reptiles represent one of the most diverse groups of tetrapod vertebrates. Extant representatives of reptiles include lepidosaurs (lizards), testudines (turtles) and archosaurs (crocodiles and birds). In particular, they show an important locomotor diversity with bipedal, quadrupedal and facultatively bipedal taxa. This diversity is accompanied by substantial microanatomical disparity in the limb bones. Although many studies have highlighted the link between locomotion and bone microstructure, the latter has never been quantitatively studied from an angular perspective. Indeed, some taxa show microanatomical heterogeneity in cross-section. Here we show, using elliptic Fourier transforms and statistical analyses integrating phylogeny, how angular microanatomical parameters measured on reptilian femoral cross-sections, such as angular bone compactness, can be related to locomotion in this clade. Although phylogeny appears to have a significant impact on our results, we show that a functional signal exists. In particular, we show that bipeds and quadrupeds present a craniolateral-caudomedial and dorsoventral deficit in bone compactness, respectively. This reflects cross-sectional eccentricity in these directions that we relate to the forces acting upon the femur in different postural contexts. This work contributes to deciphering the complex interplay between phylogeny, femoral cross-sectional microanatomy and locomotion in reptiles.
... In this article, we use elliptic Fourier transforms to study the angular variation of several microanatomical parameters measured on mid-diaphyseal transverse sections of reptile femora with the BoneProfileR software (Girondot & Laurin, 2003;Gônet et al., 2022), such as bone compactness and the distance from the centre of the cross-section of the medullocortical transition, in order to quantitatively test for the first time if there is a relationship between locomotion and angular microanatomy in reptiles. We hypothesise that angular bone compactness varies according to the different mechanical constraints experienced by the femur of reptiles using different modes of locomotion. ...
... Some scans were of modest quality, so we increased the resolution using bicubic interpolation in ImageJ. Finally, we binarised the cross-sections before taking our microanatomical measurements with BoneProfileR v. 2.0-7 (Girondot & Laurin, 2003;Gônet et al., 2022). ...
Reptiles represent one of the most diverse groups of tetrapod vertebrates. Extant representatives of reptiles include lepidosaurs (lizards), testudines (turtles) and archosaurs (crocodiles and birds). In particular, they show an important locomotor diversity with bipedal, quadrupedal and facultatively bipedal taxa. This diversity is accompanied by substantial microanatomical disparity in the limb bones. Although many studies have highlighted the link between locomotion and bone microstructure, the latter has never been quantitatively studied from an angular perspective. Indeed, some taxa show microanatomical heterogeneity in cross-section. Here we show, using elliptic Fourier transforms and statistical analyses integrating phylogeny, how angular microanatomical parameters measured on reptilian femoral cross-sections, such as angular bone compactness, can be related to locomotion in this clade. Although phylogeny appears to have a significant impact on our results, we show that a functional signal exists. In particular, we show that bipeds and quadrupeds present a craniolateral-caudomedial and dorsoventral deficit in bone compactness, respectively. This reflects cross-sectional eccentricity in these directions that we relate to the forces acting upon the femur in different postural contexts. This work contributes to deciphering the complex interplay between phylogeny, femoral cross-sectional microanatomy and locomotion in reptiles.
... This method marks the bone tissue in black and vascular spaces (medullary cavity, vascular canals, and resorption cavities) in white. The binary images ( Figure S2) were quantitatively analyzed in R using the Bone Profile R package, (Girondot & Laurin, 2003;Gônet et al., 2022) to calculate the compactness parameters. We quantified the bone compactness (ratio between the surface occupied by bone tissues and the total bone surface (Laurin et al., 2004), as well as the relative width of the transition zone between the medulla and the cortex (S), the distance of this transition zone from the center of the sections (P), and the minimum (Min) and maximum (Max) values of bone compactness (Girondot & Laurin, 2003) (Table S1). ...
... The binary images ( Figure S2) were quantitatively analyzed in R using the Bone Profile R package, (Girondot & Laurin, 2003;Gônet et al., 2022) to calculate the compactness parameters. We quantified the bone compactness (ratio between the surface occupied by bone tissues and the total bone surface (Laurin et al., 2004), as well as the relative width of the transition zone between the medulla and the cortex (S), the distance of this transition zone from the center of the sections (P), and the minimum (Min) and maximum (Max) values of bone compactness (Girondot & Laurin, 2003) (Table S1). ...
Osteoderms are mineralized structures embedded in the dermis, known for non‐avian archosaurs, squamates, xenarthrans and amphibians. Herein, we compared the osteoderm histology of Brazilian Notosuchia of Cretaceous age using three neosuchians for comparative purposes. Microanatomical analyses showed that most of them present a diploe structure similar to those of other pseudosuchians, lizards and turtles. This structure contains two cortices (the external cortex composed of an outer and an inner layers, and the basal cortex) and a core in‐between them. Notosuchian osteoderms show high bone compactness (>0.85) with varying degrees of cancellous bone in the core. The neosuchian Guarinisuchus shows the lowest bone compactness with a well‐developed cancellous layer. From an ontogenetic perspective, most tissues are formed through periosteal ossification, although the mineralized tissues observed in baurusuchid LPRP/USP 0634 suggest a late metaplastic development. Histology suggests that the ossification center of notosuchian osteoderm is located at the keel. Interestingly, we identified Sharpey's fibers running perpendicularly to the outer layer of the external cortex in Armadillosuchus arrudai, Itasuchus jesuinoi and Baurusuchidae (LPRP/USP 0642). This feature indicates a tight attachment within the dermis, and it is evidence for the presence of an overlying thick leathery layer of skin over these osteoderms. These data allow a better understanding of the osteohistological structure of crocodylomorph dermal bones, and highlight their structural diversity. We suggest that the vascular canals present in some sampled osteoderms connecting the inner layer of the external cortex and the core with the external surface may increase osteoderm surface and the capacity of heat transfer in terrestrial notosuchians. This article is protected by copyright. All rights reserved.
... Relative cortical thickness can be measured with image processing software (e.g., Castanet and Caetano 1995), whereas more complex sets of parameters depicting the overall organization of a bone, its global compactness or the characteristics of its trabecular network can be obtained with software specifically designed for the study of bone tissues. Among them, Bone Profiler (Girondot and Laurin 2003) can extract several parameters that describe the distribution of bone tissue in a section, i.e., its compactness profile (technical details in Girondot and Laurin 2003). In brief, Bone Profiler models bone microanatomy using four main parameters, P, S, Min, and Max, and a few more that will not be presented here. ...
... Relative cortical thickness can be measured with image processing software (e.g., Castanet and Caetano 1995), whereas more complex sets of parameters depicting the overall organization of a bone, its global compactness or the characteristics of its trabecular network can be obtained with software specifically designed for the study of bone tissues. Among them, Bone Profiler (Girondot and Laurin 2003) can extract several parameters that describe the distribution of bone tissue in a section, i.e., its compactness profile (technical details in Girondot and Laurin 2003). In brief, Bone Profiler models bone microanatomy using four main parameters, P, S, Min, and Max, and a few more that will not be presented here. ...
... The compactness of both osteoderms and long bones was analyzed using Bone Profiler 4.5.5 Windows version (Girondot and Laurin, 2003). With this software it is possible to obtain the 'observed compactness' (OC), which is the proportion (values between 0-1) of cross-sectional area of an element that includes compact bone. ...
... Compactness profile parameters of femur of proterochampsid Chanaresuchus bonapartei (PVL 4575), obtained by Bone Profiler(Girondot and Laurin, 2003). Estimated snout-vent length: 336 mm. ...
Proterochampsids were a group of stem archosaurs from the Middle-Late Triassic of South America. Using for the first time in proterochampsids quantitative microanatomical and morphological data and an inference model, we analyze the microstructure of postcranial bones of proterochampsids to infer life-history traits dealing with growth dynamics, ontogenetic changes, dermal armor histogenesis and lifestyle. We studied proterochampsid individuals from the Middle-Late Triassic Chañares Formation: three specimens of Chanaresuchus bonapartei: PVL 4575 (osteoderms and femur), CRILAR-Pv 80 (osteoderm) and CRILAR-Pv 81 (humerus), and a femur of a non-identified Rhadinosuchinae specimen (CRILAR-Pv 488). The osteoderms show a compact-uniform composition of parallel-fibered bone and lines of arrested growth (LAGs). The long bones are composed mainly of highly vascularized, parallel-fibered bone and isolated areas of woven-fibered bone in the innermost portion of cortex (only in C. bonapartei PVL 4575). The absence of an external fundamental system (EFS) indicates that all of the sampled individuals were somatically immature at time of death. The absence of mineralized bundles of collagenous fibers supports intramembranous ossification as the developmental origin for the osteoderms. With an inference model used for the first time in proterochampsids, the lifestyle inferred for C. bonapartei is terrestrial. Histological evidence indicates that sexual maturity is reached before both somatic and skeletal maturity. The growth patterns among proterochampsids exhibit some degree of variation even within a single species. Such variation can be due to different causes, including possibly phenotypic plasticity.
... Relative cortical thickness can be measured with image processing software (e.g., Castanet and Caetano 1995), whereas more complex sets of parameters depicting the overall organization of a bone, its global compactness or the characteristics of its trabecular network can be obtained with software specifically designed for the study of bone tissues. Among them, Bone Profiler (Girondot and Laurin 2003) can extract several parameters that describe the distribution of bone tissue in a section, i.e., its compactness profile (technical details in Girondot and Laurin 2003). In brief, Bone Profiler models bone microanatomy using four main parameters, P, S, Min, and Max, and a few more that will not be presented here. ...
... Relative cortical thickness can be measured with image processing software (e.g., Castanet and Caetano 1995), whereas more complex sets of parameters depicting the overall organization of a bone, its global compactness or the characteristics of its trabecular network can be obtained with software specifically designed for the study of bone tissues. Among them, Bone Profiler (Girondot and Laurin 2003) can extract several parameters that describe the distribution of bone tissue in a section, i.e., its compactness profile (technical details in Girondot and Laurin 2003). In brief, Bone Profiler models bone microanatomy using four main parameters, P, S, Min, and Max, and a few more that will not be presented here. ...
... In order to evaluate femoral compactness profiles for potential terrestrial adaptation, the digital scans of the cross-sections were converted to binary 8-bit images in Adobe Photoshop CC (Adobe Systems) and imported into the software Bone Profiler [47]. Bone Profiler estimates bone compactness (the relative area of a cross-section occupied by mineralized bone tissue) by calculating the proportion of bone area observed in 51 zones averaged across 60 radial sectors, and constructs a 'compactness profile' from the centroid to the periphery of the outer bone wall. ...
... Varanopid specimens sampled histologically and associated measurements. CDI, cortico-diaphyseal index [47]; Circ, midshaft circumference in mm; K, relative medullary diameter; P, relative position of inflection point; PF-LAM, parallel-fibred to lamellar bone transition (sensu [49]) with simple canals and/or osteons; S, slope of medulla-cortex transition zone; Vasc dens , density of vascular canals per mm 2 . therefore low in all specimens (CDI, 0.468-0.542; ...
Varanopids were a group of small to medium-sized synapsids whose fossil record spans the Carboniferous through middle Permian. Although their phylogenetic relationships have received some interest in recent years, little is known about other aspects of their palaeobiology, including their skeletal growth, allometry and habitat preference. Here, we describe varanopid long bone histology based on a sample of well-preserved femora from the lower Permian Richards Spur fissure fill locality, Comanche County, Oklahoma, USA. The sample includes five femora from at least two varanopid taxa— Mycterosaurus and the large varanodontine Varanops brevirostris —and four additional mycterosaurine femora not diagnosed to genus. Prior work on femoral bone compactness provided a baseline to make lifestyle inferences and evaluate whether varanopids were ancestrally terrestrial. Moreover, the large availability of specimens spanning different sizes made possible an assessment of size-related ontogenetic histovariability. All specimens revealed moderately dense cortical bone tissues composed of sparsely vascularized parallel-fibred and lamellar bone with radially arranged rows of longitudinal canals (mostly simple), and many preserved regularly spaced growth marks (annuli and lines of arrested growth) as in modern varanids. We show that bone histology has the potential to explain how ballast was shed and the skeleton lightened for terrestrial mobility in ancestral synapsids and their basal amniote kin, as well as how adjustments in postnatal growth influenced the evolution of larger body sizes in the terrestrial frontier.
This article is part of the theme issue ‘Vertebrate palaeophysiology'.
... Regarding shell bone microanatomy, Scheyer (2007) studied histological sections in both extinct and extant taxa, recognizing a series of histological characteristics used to distinguish four different types of environmental adaptations (terrestrial, semi-aquatic, mainly aquatic and marine). These inferences, drawn initially from qualitative descriptions, were subsequently contrasted with quantitative data obtained using the Bone Profiler software, which estimates the percentage of bone compactness (C%, Girondot and Laurin, 2003). This method has been extensively employed during the past decade in several groups of turtles (e.g. ...
... For the quantitative microanatomical analysis, the compactness and the Cancellous Bone/Total plate (CB/TP) thickness ratio were obtained for 63 slices. Compactness was calculated using the Windows version 4.5.5 of Bone Profiler Software (Girondot and Laurin, 2003). For use within the program, images of the sectioned bones had to be binarized (black for bone and white for vascular spaces, Fig. 2A-O, 3A-U). ...
Extant turtles exhibit a range of ecological adaptations to terrestrial and pelagic marine habitats. Bone shell microanatomy, and specifically, qualitative and quantitative approaches to shell bone porosity, have been used to infer palaeoecology and habitat. However, such inferences are hindered by the lack of a comprehensive sampling of testudine taxa and, in some instances, of long bones of vertebrates other than turtles. In this paper, we carry out an osteohistological analysis of Testudinata shell bones, including 31 different taxa, both extant and extinct, of known habitats. Costal and peripheral elements of published species and new data presented here are statistically analysed. Although, in some cases, values are congruent with those expected for a particular habitat (e.g. Hydromedusa casamayorensis), this is not true for all taxa examined. Moreover, microanatomical features of several taxa (e.g. Chelonia mydas) are inconsistent with habitat data. Results indicate that, although the microanatomical structure of the shell is related to habitat, this is not the only influence and indeed, in several cases, not the most important factor.
... 68 This index also provides information on osteogenic dynamics when analyzed along with estimations of bone area (see Ref. 44). This parameter quantifies the ratio between the cortical thickness and the radius of the crosssection (see Ref. 64), so that higher values indicate thicker cortical walls and hence a higher rigidity to resist bending and torsional strains. 134 Both humeral (CDIh) and femoral (CDIf) parameters were calculated using binary images of bone area and empty space; the medullary cavity and resorption cavities are considered as empty spaces (thus increasing bone porosity), whereas nutrient arteries and void space are not included, thus minimizing the intrinsic bone porosity levels of the bone, but still keeping the general microanatomical design of the whole cross-section (see Ref. 44). ...
... CDI values were obtained from the software Bone Profiler Version 4.5.7. 64 We also assessed the intermembral index (IMI) 65 and the vertebral index (VI) (developed in this study). Apart from indicating leaping ability, the IMI has not shown clear functional correlates in mammals, especially those associated with either higher speed or lack of it. ...
Background
Subterranean mammals show a suite of musculoskeletal adaptations that enables efficient digging. However, little is known about their development. We assessed ontogenetic changes in functionally relevant skeletal traits, and ossification patterns (periosteal and endochondral bone modules) in a truly subterranean scratch‐digging rodent, Bathyergus. We studied 52 individuals (202 long bones) from a wild population by using a multiscale approach involving internal and external morphology.
Results
Multivariate analysis showed significant morphological changes during ontogeny. A specialized phenotype is expressed perinatally (eg, greater external robustness and developed olecranon, teres major, and deltoid processes), whereas adults presented slender bones with significantly thicker cross‐sections. Ossification modules scaled mostly isometrically with body size parameters. Periosteal modules showed high variability and tended to grow faster than endochondral modules.
Conclusions
Scratch‐digging adaptations appear at perinatal age and then specialize in subadults. Early development of agonistic and digging behaviors and onset of sexual maturation seems to contribute to its development, although genetic factors also seem to play an important role. Ontogenetic differences are probably a trade‐off to counteract weaker cortical bone properties and poor muscle development in juveniles, whereas slender but thicker cortical bones maximize bone resistance during burrow construction without compromising locomotor performance in adults.
... To evaluate for ontogenetic variation in bone compactness, and to infer Macrospondylus ecology using a previously published lifestyle inference model (Quemeneur et al., 2013), microanatomical parameters of the complete (both SMNS specimens) or incomplete (GPIT-PV-84138) femoral cross sections were extracted using the software Bone Profiler version 4.5.8 that can deal with fragmentary bone sections (Girondot & Laurin, 2003;Gônet et al. 2021). Images of the cross-sections were first transformed into binary images (black for bone and white for void Abbreviations: Cg, global bone compactness for the entire area; FL, femoral length; Max, compactness of the outermost cortex (=maximum local compactness); Min, compactness in the center of the section (=minimal local compactness); P, relative distance from the centre of the section to the point of inflection (=size of the medullary cavity); S, reciprocal of the slope at the inflection point (=width of the transitional zone between cortex and medullary cavity); SVL, snoutvent length (measured from the anterior-most rostrum to posterior-most dorsal vertebra). ...
The Posidonienschiefer Formation of southern Germany has yielded an array of incredible fossil vertebrates. One of the best represented clades therein is Teleosauroidea, a successful thalattosuchian crocodylomorph group that dominated the coastlines. The most abundant teleosauroid, Macrospondylus bollensis, is known from a wide range of body sizes, making it an ideal taxon for histological and ontogenetic investigations. Previous studies examining thalattosuchian histology provide a basic understanding of bone microstructure in teleosauroids, but lack the taxonomic, stratigraphic, and ontogenetic control required to understand growth and palaeobiology within a species. Here, we examine the bone microstructure of three femora and one tibia from three different‐sized M. bollensis individuals. We also perform bone compactness analyses to evaluate for ontogenetic and ecological variation. Our results suggests that (1) the smallest specimen was a young, skeletally immature individual with well‐vascularized‐parallel‐fibered bone and limited remodeling in the midshaft periosteal cortex; (2) the intermediate specimen was skeletally immature at death, with vascularized parallel‐fibered bone tissue interrupted by at least 10 LAGs, but no clear external fundamental system (EFS), and rather extensive inner cortical bone remodeling; and (3) the largest specimen was skeletally mature, with parallel‐fibered bone tissue interrupted by numerous LAGs, a well‐developed EFS, and extensive remodeling in the deep cortex. Macrospondylus bollensis grew relatively regularly until reaching adult size, and global bone compactness values fall within the range reported for modern crocodylians. The lifestyle inference models used suggest that M. bollensis was well adapted for an aquatic environment but also retained some ability to move on land. Finally, both larger specimens display a peculiar, localized area of disorganized bone tissue interpreted as pathological.
... Second, these full pictures were binarized (using a threshold grayscale of 219) to produce a black and white duplicate, black corresponding to the bone matrix and white to the lumen let by the medullary and the vascular cavities. Finally, these binarized duplicates were processed by BoneProfileR web server v.2.4 build 766 (Girondot & Laurin, 2003). As one of our sections was incomplete (MNHN.F.RJN463 right femur), we followed the procedure described in Gônet et al. (2021) and removed a pie chart from the centroid. ...
Paleophysiology is an emergent discipline. Organismic (integrative) approaches seem more appropriate than studies focusing on the variation of specific features because traits are tightly related in actual organisms. Here, we used such an organismic approach (including lifestyle, thermometabolism, and hunting behavior) to understand the paleobiology of the lower Jurassic (Toarcian) thalattosuchian metriorhynchoid Pelagosaurus typus. First, we show that the lifestyle (aquatic, amphibious, terrestrial) has an effect on the femoral compactness profiles in amniotes. The profile of Pelagosaurus indicates that it was amphibious, with a foraging activity in shallow marine environments (as suggested by the presence of salt glands) and thermoregulatory basking behavior in land (as suggested by the presence of osteoderms with highly developed ornamentation). As for the thermometabolism, we show that the mass‐independent resting metabolic rate of Pelagosaurus is relatively high compared to the sample of extant ectothermic amniotes, but analysis of vascular canal diameter and inferences of red blood cell size refute the hypothesis suggesting incipient endothermy. Finally, the foraging behavior was inferred using two proxies. Pelagosaurus had a mass‐independent maximum metabolic rate and an aerobic scope higher than those measured in the almost motionless Iguana iguana, similar to those measured in the sit‐and‐wait predator Crocodylus porosus but lower than those quantified in the active hunter Varanus gouldii. These results suggest that Pelagosaurus may have had a hunting behavior involving a slow sustained swimming or a patient waiting in shallow waters, and may have caught preys like gharials, using fast sideways sweeping motions of the head.
... Além dos estudos descritivos qualitativos, é possível ainda trabalhar com dados histológicos quantitativos através de softwares como Bone Profiler (Girondot & Laurin, 2003) e BoneJ (Doube et al., 2010), que oferecem dados como taxa de compactação, parâmetros relacionados à trabécula, comprimento das fibras, entre outros. Diversos trabalhos já utilizaram esses softwares (Straeh et al., 2013;Amson et al., 2014;Asakura et al., 2017), principalmente para relacionar a taxa de compactação do osso com o estilo de vida da espécie (Laurin et al., 2004;Scheyer & Sander, 2009;Amson et al., 2014) As considerações de Woodward et al. (2018) são importantes também ao lembrar que embora os fósseis venham sendo seccionados por séculos, eles nunca foram amostrados sistematicamente, até pelo menos recentemente. ...
Mesmo após milhões de anos de soterramento, muitos vertebrados ainda apresentam a estrutura histológica do tecido ósseo preservada. Aspectos ontogenéticos, reconheci-mento de feições fossildiagenéticas, aprimoramento de estudos sistemáticos e anatômi-cos são os principais pontos abordados pelos estudos paleohistológicos. Dentre os ver-tebrados, os grupos mais estudados por esta ótica foram os dinossauros, pterossauros, ictiossauros, crocodilomorfos, testudines, cinodontes e peixes, sendo ainda discretos os estudos realizados com mamíferos, especialmente os mamíferos com carapaça óssea. Este trabalho pretende reunir o conhecimento disponível acerca da histologia de osteo-dermos de mamíferos cingulados, de forma a apresentar um panorama dos trabalhos atuais e um ponto de partida para futuros trabalhos.
... Interestingly, Black et al. (2012a) found that, in terms of limb proportions, N. lavarackorum was unique among marsupials in having significantly reduced hindlimbs relative to their forelimbs, which is a feature associated in extant prosimians with suspensory climbing behaviors and/or increased pedal friction on vertical surfaces. Exploring the idea that bone compactness and structural geometry is related to lifestyle, two lineages of modern tree sloths (Choloepus and Bradypus) that are known to have slow arboreal lifestyles were examined (Girondot and Laurin, 2003). They were found to have lower cortical compactness as compared to other similarsized taxa (Nyakatura, 2012;Montañez-Rivera et al., 2018) and other xenarthrans, and they also show high rates of bone remodeling that appear to be maintained at high levels throughout ontogeny (Montañez-Rivera et al., 2018). ...
Despite the recognition that bone histology provides much information about the life history and biology of extinct animals, osteohistology of extinct marsupials is sorely lacking. We studied the bone histology of the ca. 15-million-year-old Nimbadon lavarackorum from Australia to obtain insight into its biology. The histology of thin sections of five femora and five tibiae of juveniles, subadult, and adult Nimbadon lavarackorum was studied. Growth marks in the bones suggest that N . lavarackorum took at least 7–8 years (and likely longer) to reach skeletal maturity. The predominant bone tissue during early ontogeny is parallel-fibered bone, whereas an even slower rate of bone formation is indicated by the presence of lamellar bone tissue in the periosteal parts of the compacta in older individuals. Deposition of bone was interrupted periodically by lines of arrested growth or annuli. This cyclical growth strategy indicates that growth in N . lavarackorum was affected by the prevailing environmental conditions and available resources, as well as seasonal physiological factors such as decreasing body temperatures and metabolic rates.
... Nevertheless, the following the authors with Adobe Photoshop, to heighten the contrast between the dark and white parts. The bone compactness ('compacity') of several sections of this picture was calculated with the program 'boneprofiler' from the University of Montpellier, France (Girondot & Laurin 2003). ...
A cetacean vertebra from presumably Bartonian strata near Taradell, Northeastern Spain, described by Pilleri in 1989, is here re-examined. Also a description of the local stratigraphy is given. Notwithstanding the rather severe damage of the vertebral centrum, it shows the same characteristics, as vertebrae ascribed to Pachycetus (‘Platyosphys’; ‘Basilotritus’) sp. from, amongst others, Ukraine, Germany and Belgium. The characteristics are: the combined presence of a compact, circumferential multi-layered cortex, the pock-marked surface of the vertebral centrum, the pachyostotic pedicles of the neural arch and finally the probable elongation of the vertebral centrum, the transverse processes and the pedicles of the neural arch. The compactness of the midpart of the vertebral centrum has been measured and is compared with that of other taxa. The find extends the geographic distribution of this genus to Southwestern Europe. The vertebra appears to belong to a small species of Pachycetus, which was until now not known with certainty from Europe, although some similar-sized vertebrae from the Southern Bight of the North Sea, Belgium have recently been described.
... The four binary images (supplementary material) were analyzed quantitatively with the software Bone Profiler Version 4.5.8 (Girondot and Laurin, 2003) to infer on bone compactness and its profile. ...
Among the wide diversity of notosuchian crocodyliforms, Baurusuchidae is remarkable by their morphology, indicating a terrestrial hypercarnivory habit during the Late Cretaceous of Gondwana. Commonly, amongst baurusuchids, the anatomy of the large-sized Stratiotosuchus maxhechti shows theropod mimic features in its skull and limb bones. Such similarities supported the hypothesis of competitive exclusion of medium to large-sized
theropods by baurusuchids. However, a recent taphonomical approach claims that other lines of evidence
should be considered (e.g., biomechanics); due to the biased fossil record found in Bauru Group. This approach supported niche partitioning between theropods and baurusuchids instead of competitive exclusion. Here we performed a paleohistological analysis on a baurusuchid (S. maxhechti) to evaluate if the terrestrial ecology implies fast growth and if the microstructure is similar to that found in theropods, with insights into a niche competition hypothesis. The samples were taken from one specimen with two femora and another one comprising the left ulna and tibia. All four samples show the presence of a fibrolamellar bone complex arranged in a cyclical growth. The growth zones are composed of woven matrix that gradually turns into a parallel-fibered bone, and is followed by lines of arrested growth (LAGs). There is also the presence of simple and
anastomosed vascular canals. Compared to living crocodylians the growth shows a higher depositional rate and a more complex organization pattern. In this respect, the growth dynamics are like medium-to-large theropods. Stratiotosuchus lacks an External Fundamental System (EFS), which indicates that the material studied here represents individuals that died before reaching maximum size, suggesting that it could take more than twelve years to reach full size. Comparing the body mass estimates by femoral circumference (∼178–180 kg) and the bone microstructure with theropods, they share a fast growth pattern of fibrolamellar bone complex. However, the body size diversity in both groups favors the niche partitioning hypothesis over the suggestion of competitive exclusion between baurusuchids and theropods.
... The four binary images (supplementary material) were analyzed quantitatively with the software Bone Profiler Version 4.5.8 (Girondot and Laurin, 2003) to infer on bone compactness and its profile. ...
... BoneProfileR (Girondot & Laurin, 2003;Gônet et al., 2022). ...
The water‐to‐land transition by the first tetrapod vertebrates represents a key stage in their evolution. Selection pressures exerted by this new environment on animals led to the emergence of new locomotor and postural strategies that favoured access to different ecological niches and contributed to their evolutionary success. Today, amniotes show great locomotor and postural diversity, particularly among Reptilia, whose extant representatives include parasagittally locomoting erect and crouched bipeds (birds), sub‐parasagittal ‘semi‐erect’ quadrupeds (crocodylians) and sprawling quadrupeds (squamates and turtles). But the different steps leading to such diversity remain enigmatic and the type of locomotion adopted by many extinct species raises questions. This is notably the case of certain Triassic taxa such as Euparkeria and Marasuchus. The exploration of the bone microanatomy in reptiles could help to overcome these uncertainties. Indeed, this locomotor and postural diversity is accompanied by great microanatomical disparity. On land, the bones of the appendicular skeleton support the weight of the body and are subject to multiple constraints that partly shape their external and internal morphology. Here we show how microanatomical parameters measured in cross‐section, such as bone compactness or the position of the medullocortical transition, can be related to locomotion. We hypothesised that this could be due to variations in cortical thickness. Using statistical methods that take phylogeny into account (phylogenetic flexible discriminant analyses), we develop different models of locomotion from a sample of femur cross‐sections from 51 reptile species. We use these models to infer locomotion and posture in 7 extinct reptile taxa for which they remain debated or not fully clear. Our models produced reliable inferences for taxa that preceded and followed the quadruped/biped and sprawling/erect transitions, notably within the Captorhinidae and Dinosauria. For taxa contemporary with these transitions, such as Terrestrisuchus and Marasuchus, the inferences are more questionable. We use linear models to investigate the effect of body mass and functional ecology on our inference models. We show that body mass seems to significantly impact our model predictions in most cases, unlike the functional ecology. Finally, we illustrate how taphonomic processes can impact certain microanatomical parameters, especially the eccentricity of the section, while addressing some other potential limitations of our methods. Our study provides insight into the evolution of enigmatic locomotion in various early reptiles. Our models and methods could be used by palaeontologists to infer the locomotion and posture in other extinct reptile taxa, especially when considered in combination with other lines of evidence. Reptiles show great diversity of locomotion and posture. We employed phylogenetically informed statistical methods to explore their bone microanatomy. We used our models to infer the locomotion of extinct reptiles that document the different episodes of postural diversification in this clade.
... Data for all left humeri were symmetrised so that the sample consisted of right side bones only. We binarised the cross-sections before taking our geometric and microanatomical measurements in ImageJ with the BoneJ plugin (Doube et al. 2010) and in R (R Core Team 2013) with the BoneProfileR package (Girondot and Laurin 2003;Gônet et al. 2022). A sample of the mammalian cross-sections used in this study are presented in Fig. 2. ...
Mammals have an evolutionary history spanning hundreds of millions of years. Today, mammals represent one of the most diverse groups of tetrapod vertebrates. In particular, they present a great postural diversity. The humerus adopts different positions: small mammals have a “crouched” posture with a quasi-horizontal humerus, while in the largest species, the humerus is more vertical. Some monotremes have more transversely oriented humeri similar to those of reptiles. The forelimb of moles is also modified in relation to their burrowing lifestyle. This postural diversity is accompanied by an important microanatomical disparity. Indeed, the bones of the appendicular skeleton support the weight of the body and are subjected to various forces that partly shape their external and internal morphology. We show here how geometric and microanatomical parameters measured in cross-section such as the polar section modulus or the position of the medullo-cortical transition can be related to posture. Using statistical methods that take phylogeny into account, we develop a postural model from a sample of humerus cross-sections belonging to 41 species of extant mammals. Our model can be used by palaeontologists to infer the posture of extinct synapsids. As an example, we infer the posture of two emblematic taxa: Dimetrodon natalis and Peratherium cuvieri. The results of the analysis indicate a sprawling posture for Dimetrodon and a crouched posture for Peratherium. This work contributes to unravel the complex interaction between phylogeny, humeral microanatomy and geometry, body mass, lifestyle and posture in mammals.
... Further histological descriptions were conducted by LOF. Microanatomical analyses of bone compactness were conducted by LOF utilizing the software Bone Profiler© following the protocol of Girondot and Laurin (2003). All the microphotographs under brightfield microscopy and polarized light were obtained using the Leica DM750P polarizing microscope in the Laboratorio de Geología de la Universidad del Desarrollo, Chile. ...
En este trabajo describimos la microanatomía e histología de varios huesos de un elasmosáurido juvenil de niveles del Maastrichtiano Superior de Isla Marambio (=Seymour), Antártica. Secciones finas fueron obtenidas a partir de la diáfisis de un propodio y de un fragmento de escápula. El análisis de la microanatomía fue realizado utilizando el software Bone Profiler© para medir la compactación del tejido óseo en dos propodios, una vértebra y fragmentos de escápula y pubis. Nuestros resultados muestran lo siguiente: (1) a nivel microanatómico, encontramos una alta densidad de matriz ósea en donde casi no habían espacios en la zona medular. Los valores del índice de compactación oscilaban entre 0,858-0,993 (valores de 0 a 1). Estos resultados sugieren un esqueleto denso parecido a un caso de osteosclerosis. (2) a nivel de la histología, no encontramos presencia de zonas de crecimiento ni anillos/LAGS en la zona cortical. En vez de eso, encontramos una corteza muy delgada compuesta por tejido primario entretejido altamente vascularizado con canales vasculares de disposición radial anastomosados, y una región medular compuesta por pocas trabéculas óseas, llena de de cartílago calcificado con cavidades de reabsorción y lagunas de Howship (=evidencia de actividad condroclástica). Estas características osteo-histológicas confirman la presencia de osteosclerosis (probablemente reflejando un modo de vida tipo-manatí/nadador pasivo) y sugiere fuertemente que este espécimen fue un juvenil de edad muy temprana al momento de morir.
... These centra are short and very broad (Fig. 8C), as in Ruthenosaurus (Reisz et al., 2011: fig. 3), but not in it is based on a single bone section only, and it must be tested on more material using quantitative and statistical comparisons (using for example the software Bone profiler, Girondot and Laurin, 2003). The anterior dorsal rib UM-LIE 03 may be the 5 th compared with those of Cotylorhynchus romeri (Stovall et spongiosa, the thin cortica, and the absence of a medulla is a typical pattern of aquatic tetrapods (e.g., Steyer et al. 2004). ...
Lalieudorhynchus gandi gen. nov. and sp. nov. is a new caseid synapsid from the Permian of the Lodève Basin, Occitanie, France. This new taxon is represented by a partial but well-preserved postcranial skeleton, and is characterized by the following apomorphies: a transverse section of the sacral and anterior caudal neural spines with a very thin keel-like process anteriorly, a slender dorsal tip of the dorsal and caudal spines, a narrow distal end of the first sacral rib, a fossa on triceps process of metacoracoid, and a very large distal tarsal 1 of same width than the astragalus, with nearly all sides being shallowly concave. The skeleton corresponds to a sub-adult individual that was excavated from the La Lieude Formation dated as Roadian-Capitanian (Guadalupian). A sedimentological and taphonomical analysis of the type locality, together with preliminary osteohistological observations, suggest that this new French caseid was rather aquatic, as already hypothesised for other large forms. A phylogenetic analysis of caseids is performed to test the position of this new taxon and to better understand the evolution of the clade: interestingly, Lalieudorhynchus gandi gen. nov. et sp. nov. is closer to the North American "Cotylorhynchus" hancocki than to the other French caseids Ruthenosaurus and Euromycter from the Artinskian of the geographically closer Rodez Basin. These two last caseids document the Artinskian radiation of the clade, which remained diverse until Olson's extinction. Caseids survived, as Lalieudorhynchus is one of the youngest representatives of the clade, and may have used novel ecological strategies to access their vegetarian food sources.
... The binary images (supplementary material) were analyzed quantitatively with the software Bone Profiler version 4.5.8 (Girondot & Laurin 2003) to infer on bone compactness profile from cross-sections. ...
Mariliasuchus amarali Carvalho & Bertini, 1999 was a terrestrial quadruped crocodyliform from the Late Cretaceous of the Bauru Group, Brazil. In this paper we present the first study of the bone histology of this species. Moderate growth rate, interspersed by growth marks, was observed in thin sections of a rib and appendicular bones; growth patterns observed in M. amaralis appear similar to those observed in Triassic archosauriforms. The M. amarali cross-sections indicate growth variability between both the axial and appendicular bones. Distinctive remodeling processes were found in the radius, which had extensive inner cortex remodeling composed of compacted coarse cancellous bone. Furthermore, the medullary region was infilled with spongy bone.
... In parallel, several other studies have assessed the presence (and sometimes the strength) of the phylogenetic signal in bone microanatomy. These studies typically relied on a sigmoidal compactness profile model and the software Bone Profiler (see Girondot and Laurin 2003, and Chapter 4 of this book on Bone microanatomy) to analyze mid-diaphyseal cross sections of long limb bones. Three methods were used to test the presence of a phylogenetic signal: regressions on distance matrices with permutations to test their significance (Legendre et al. 1994), PVR with variance partition (Desdevises et al. 2003), and comparison of the squared length of the reference tree to that of a population of random trees obtained by reshuffling the terminal taxa ). ...
... In parallel, several other studies have assessed the presence (and sometimes the strength) of the phylogenetic signal in bone microanatomy. These studies typically relied on a sigmoidal compactness profile model and the software Bone Profiler (see Girondot and Laurin 2003, and Chapter 4 of this book on Bone microanatomy) to analyze mid-diaphyseal cross sections of long limb bones. Three methods were used to test the presence of a phylogenetic signal: regressions on distance matrices with permutations to test their significance (Legendre et al. 1994), PVR with variance partition (Desdevises et al. 2003), and comparison of the squared length of the reference tree to that of a population of random trees obtained by reshuffling the terminal taxa ). ...
... Body size affects preponderantly the investigated vertebral structure parameters among mammals. Mean vertebral global compactness (the ratio of cross-sectional area occupied by bone to total cross-sectional area, Cg [26]) and trabecular architecture within the vertebral body (centrum)-the Connectivity (approximates the number of trabeculae) and BV/TV (fraction of bone contained in the volume of interest [VOI] over total VOI volume) show a strong positive correlation with size, even when lifestyle is accounted for, as indicated by phylogenetically informed ANCOVAs (pANCOVAs, p values < 0.0001; pseudo R 2 = 0.44-0.68) and phylogenetically informed regression of the parameter against body mass (pANO-VAs, p values < 0.0001, pseudo R 2 = 0.44-0.63; ...
Background
Mammals are a highly diverse group, with body mass ranging from 2 g to 170 t, and encompassing species with terrestrial, aquatic, aerial, and subterranean lifestyles. The skeleton is involved in most aspects of vertebrate life history, but while previous macroevolutionary analyses have shown that structural, phylogenetic, and functional factors influence the gross morphology of skeletal elements, their inner structure has received comparatively little attention. Here we analysed bone structure of the humerus and mid-lumbar vertebrae across mammals and their correlations with different lifestyles and body size.
Results
We acquired bone structure parameters in appendicular and axial elements (humerus and mid-lumbar vertebra) from 190 species across therian mammals (placentals + marsupials). Our sample captures all transitions to aerial, fully aquatic, and subterranean lifestyles in extant therian clades. We found that mammalian bone structure is highly disparate and we show that the investigated vertebral structure parameters mostly correlate with body size, but not lifestyle, while the opposite is true for humeral parameters. The latter also show a high degree of convergence among the clades that have acquired specialised (non-terrestrial) lifestyles.
Conclusions
In light of phylogenetic, size, and functional factors, the distribution of each investigated structural parameter reveals patterns explaining the construction of appendicular and axial skeletal elements in mammalian species spanning most of the extant diversity of the clade in terms of body size and lifestyle. These patterns should be further investigated with analyses focused on specific lifestyle transitions that would ideally include key fossils.
... Quantitative parameters were used to describe the transverse sections, except those of extinct taxa showing an insufficient contrast between bone and the infilling sediment (see Table 1). The choice of parameters follows , using the BoneJ plugin (Doube et al. 2010) of ImageJ (Wayne Rasband National Institutes of Health, USA) and the software Bone Profiler (Girondot and Laurin 2003): A) CSAb (Cross-Sectional Area of bone), representing the surface occupied by bony tissues; B) CSAt (total Cross-Sectional Area), as the surface of the whole transverse section; C) C (Compactness), as the ratio of CSAb over CSAt; D) R, as the radius of the section approximated as a circle calculated based on the perimeter/2π, and used as a proxy of size; E) CSS (Cross-Sectional Shape), as the ratio between the maximal and minimal second moments of area (Imax/ Imin); F) Zpol (Polar Section Modulus) representing the resistance of a section to torsion and bending (see Ruff 2002;Ksepka et al. 2015); G) RMeanT, as the relative mean thickness of cortical bone (after separation by segmentation of the cortical and medullary areas), calculated as the absolute mean thickness of cortical bone divided by R; H) RSDT, as the relative standard deviation of cortical bone thickness; I) P: the extent of the medullary cavity as measured by the relative distance from the center of the section to the point where the most abrupt change in compactness occurs; and J) S: the width of the transitional zone between the compact cortex and the medullary cavity as measured by the reciprocal of the slope of the compactness profile at the inflection point. ...
Hippopotamoids are herbivorous mammals that originated in the late middle Eocene. This taxon includes animals with a great variety of sizes and body proportions, from small and gracile forms with slender limbs to heavy massive ones. Many hippopotamoids have previously been considered semi-aquatic but recent studies have highlighted a diversity of ecologies. This study focuses on bone microanatomy, one of the various proxies that enable inferring the ecology of extinct taxa. The comparative analysis of the inner structure of the stylopod bones in various hippopotamoids, based on both transverse and longitudinal virtual sections, highlights a diversity of patterns and clarifies previously proposed hypotheses about the ecology of the sampled hippopotamoids. The filling of the medullary area by spongious deposits in the pygmy hippopotamus, Choeropsis liberiensis, appears associated with frequent incursions into the water by an animal that essentially forages in forests. The common hippopotamus, Hippopotamus amphibius, which spends most of the day submerged in water, shows a greater filling of the medullary area by spongious bone and a thicker cortex. These observations coupled with comparisons with diverse terrestrial and semi-aquatic mammals of various sizes confirm that semi-aquatic lifestyle and heavy weight-bearing are associated with similar microanatomical specializations causing an increase in bone mass. However, for a given mass, comparisons enable determining if an additional increase in bone compactness occurs, as in Hippopotamus amphibius, in which case a semi-aquatic lifestyle could be inferred. Accordingly, this study suggests an essentially terrestrial lifestyle for Microbunodon minimum, Bothriodon velaunus, Elomeryx borbonicus, Merycopotamus medioximus, Paenanthracotherium bergeri, and probably also Saotherium cf. S. mingoz, a slight degree of water dependence in Brachyodus onoideus, and a stronger one in Libycosaurus bahri and Hexaprotodon garyam, though less intense than in Hippopotamus amphibius. Comparisons with other large terrestrial and semi-aquatic taxa, and based on a large part of the diaphysis, are required to better decipher the microanatomical changes associated with a semi-aquatic lifestyle from those linked to loading in heavy quadrupedal mammals.
... The compactness profile was analysed quantitatively on the Bone Profiler program version 4.5.8 (Girondot and Laurin 2003) using a binary image transformed from the actual thin sections using the Adobe Photoshop CC 2017. From this function, the following parameters were obtained by the program: global compactness (Cg); the relative distance from the section center to the point of most abrupt change in compactness, i.e., transition from medulla to cortex (P); and the reciprocal of the slope at the inflexion point (S). ...
Osteoderms of Hoplophorus euphractus are historically mistaken by other glyptodonts osteoderms, such as Glyptodon, Glyptotherium and Neosclerocalyptus, which has created confusion regarding the proper identification of the remains. Recent revisions have granted a better taxonomic understanding of these taxa. In this work, we present a morphological description of a carapace fragment with four articulated osteoderms and other post-cranium bones. Morphological and histological information of an isolated osteoderm and a limb bone from Hoplophorus euphractus was combined, allowing some perception into their paleobiology. The combined paleohistological analysis of two bone elements, osteoderm and humerus, corroborates with the idea of how the pattern of bone microstructure is useful for making inferences about the functional morphology of extinct species. In the humerus, it is identifiable a bone tissue derived from dynamic osteogenesis, with elongated osteocytes lacunae and collagen fibre with a preferably transverse orientation (perpendicular to the long axis). In the superficial and deep layers of the osteoderm, a bone tissue derived from a combination of dynamic and static osteogenesis is seen. In the trabeculae of the osteoderm, a lamellar bone tissue is present, more organized than the ones present in the other regions of the bone. Both histological and morphological features of the osteoderm and humerus can be interpreted as a representation of a mature ontogenetic stage. The preferentially transversely fibre alignment found in H. euphractus bone could be indicative of good resistance of compressive forces, but a more extensive research with a broader sample is necessary for more definitive conclusions.
... Bone compactness, measured on a section as the area occupied by mineralized tissue against total cross-sectional area, stems from the standard histomorphometric assessment of bone volume (Parfitt et al. 1987;Hua & Buffrénil 1996). Subsequently referred to as global compactness (Cg; Girondot and Laurin 2003), this parameter revealed clear lifestyle adaptations, in particular to the aquatic environment (Canoville & Laurin 2010). While bone microanatomy in amniotes is assumed to usually be rather uniform along the diaph-ysis of long bones (Houssaye et al. 2015;Amson & Kolb 2016), Cg is generally acquired at mid-diaphysis or at the growth centre of long bones. ...
Long bones comprise articular ends (epiphyses) joined by transitional metaphyses and a diaphysis (shaft). The structure of the latter is often viewed as regularly tubular across tetrapods (limbed vertebrates). However, assessments of the bone structure along the whole diaphysis are rare. Here I assess whole‐diaphysis profiles of global compactness (bone fraction) of 164 species of extant and extinct therian mammals (marsupials + placentals) in a phylogenetically informed context. Generally terrestrial, mammals have acquired multiple times the highly specialised aerial, fully aquatic, and subterranean lifestyles, allowing to potentially associate specific traits with these lifestyles. I show that there is a consistent increase in global compactness along the diaphysis in most mammals. This pattern is modified in a limited number of specialised species: all aerial clades (gliders and bats) have rather uniform and low values, while cetaceans’ humeral diaphysis is marked by a slightly more compact mid‐diaphyseal region. Among subterranean clades, structure alterations are most obvious in fossorial talpids (true moles) and their highly modified humerus. These results call for the investigation of bone structure in whole skeletal elements of key fossils in order to reconstruct the patterns of evolutionary modifications associated with lifestyle transitions.
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... The binary images were quantitatively analyzed with the software Bone Profiler Version 4.5.8 (Girondot & Laurin, 2003) to infer on bone compactness and its profile. The basal and external cortices exhibit similar microanatomy (Figures 2a, 3a, and 4a). ...
Pelomedusoides had a recognised diverse Early Cretaceous fauna of turtles in Northeast Brazil. Within them, the bothremydid Cearachelys placidoi has a relatively abundant record. This diversity contrasts with the scarcity of osteohistological studies in this group. The relatively well‐preserved shell of C. placidoi (UFRPE 5600), from the Aptian age of Araripe Basin, is studied here for the purpose of filling this gap. We performed the osteohistological description of the plastron of a new specimen of C. placidoi. Also, to conduct a comparative study, we carried out histological sections in bones of the recent chelid Phrynops sp. Our histological findings indicate similarities between the histological pattern of freshwater turtles and the coastal marine C. placidoi. Moreover, osteohistological features imply metaplastic incorporation of dermal interwoven structural fiber bundles. Lastly, the xiphiplastron of C. placidoi shows an increase of bone compactness over its craniocaudal axis. This microanatomical feature is exclusive to Cearachelys so far.
... Além dos estudos descritivos qualitativos, é possível ainda trabalhar com dados histológicos quantitativos através de softwares como Bone Profiler (Girondot & Laurin, 2003) e BoneJ (Doube et al., 2010), que oferecem dados como taxa de compactação, parâmetros relacionados à trabécula, comprimento das fibras, entre outros. Diversos trabalhos já utilizaram esses softwares (Straeh et al., 2013;Amson et al., 2014;Asakura et al., 2017), principalmente para relacionar a taxa de compactação do osso com o estilo de vida da espécie (Laurin et al., 2004;Scheyer & Sander, 2009;Amson et al., 2014) As considerações de Woodward et al. (2018) são importantes também ao lembrar que embora os fósseis venham sendo seccionados por séculos, eles nunca foram amostrados sistematicamente, até pelo menos recentemente. ...
Mesmo após milhões de anos de soterramento, muitos vertebrados ainda apresentam a estrutura histológica do tecido ósseo preservada. Aspectos ontogenéticos, reconheci-mento de feições fossildiagenéticas, aprimoramento de estudos sistemáticos e anatômi-cos são os principais pontos abordados pelos estudos paleohistológicos. Dentre os ver-tebrados, os grupos mais estudados por esta ótica foram os dinossauros, pterossauros, ictiossauros, crocodilomorfos, testudines, cinodontes e peixes, sendo ainda discretos os estudos realizados com mamíferos, especialmente os mamíferos com carapaça óssea. Este trabalho pretende reunir o conhecimento disponível acerca da histologia de osteo-dermos de mamíferos cingulados, de forma a apresentar um panorama dos trabalhos atuais e um ponto de partida para futuros trabalhos.
... The thin section was studied and analyzed using a compound microscope (DM 2500M, Leica) with a digital camera (DFC 420C, Leica). Comparative material of S. geographicus included already published shell bone sections (59 ), and overall bone compactness was calculated using Bone Profiler software (66). ...
Despite being among the largest turtles that ever lived, the biology and systematics of Stupendemys geographicus remain largely unknown because of scant, fragmentary finds. We describe exceptional specimens and new localities of S. geographicus from the Miocene of Venezuela and Colombia. We document the largest shell reported for any extant or extinct turtle, with a carapace length of 2.40 m and estimated mass of 1.145 kg, almost 100 times the size of its closest living relative, the Amazon river turtle Peltocephalus dumerilianus , and twice that of the largest extant turtle, the marine leatherback Dermochelys coriacea . The new specimens greatly increase knowledge of the biology and evolution of this iconic species. Our findings suggest the existence of a single giant turtle species across the northern Neotropics, but with two shell morphotypes, suggestive of sexual dimorphism. Bite marks and punctured bones indicate interactions with large caimans that also inhabited the northern Neotropics.
... To do so, we connected the top of the crests of the ornamentation with a virtual black line of one pixel in the most parsimonious way to embed the surface of the pits into the vascular measurements (electronic supplementary material, S3). We exported the pictures in TIFF format (electronic supplementary material, S2) and analysed them with Bone profiler [49] in order to measure the area occupied by the empty spaces proportionally to the entire area covered by bone and vascular spaces (as detailed in electronic supplementary material, S3). ...
Studies on living turtles have demonstrated that shells are involved in the
resistance to hypoxia during apnea via bone acidosis buffering; a process
which is complemented with cutaneous respiration, transpharyngeal and
cloacal gas exchanges in the soft-shell turtles. Bone acidosis buffering
during apnea has also been identified in crocodylian osteoderms, which
are also known to employ heat transfer when basking. Although diverse,
many of these functions rely on one common trait: the vascularization of
the dermal shield. Here, we test whether the above ecophysiological functions
played an adaptive role in the evolutionary transitions between land
and aquatic environments in both Pseudosuchia and Testudinata. To do
so, we measured the bone porosity as a proxy for vascular density in a set
of dermal plates before performing phylogenetic comparative analyses.
For both lineages, the dermal plate porosity obviously varies depending
on the animal lifestyle, but these variations prove to be highly driven by
phylogenetic relationships. We argue that the complexity of multi-functional
roles of the post-cranial dermal skeleton in both Pseudosuchia and Testudinata
probably is the reason for a lack of obvious physiological signal, and
we discuss the role of the dermal shield vascularization in the evolution of
these groups.
... Sections were converted into binary black and white images using Corel Photo Paint X4. The extent of compactness was then determined using Bone Profiler for Windows V4.5.8 (Girondot & Laurin, 2003) and further information regarding Min (value for the minimum compactness), Max (value for the maximum compactness), S (the value proportional to the width of the transition zone between the medullary cavity and cortex) and P (the value of the transition area between the medullary cavity and compact cortex) were also obtained. These values were used to predict lifestyle for the humerus (Canoville & Laurin, 2010), radius (Laurin, Canoville & Germain, 2011) and tibia ( Kriloff et al., 2008). ...
Testudines are a group of reptiles characterized by the presence of a shell covered by keratinous shields. Stigmochelys pardalis is the most widely distributed terrestrial testudine in southern Africa. Although relatively common with some life history traits being well known, the growth of this species has yet to be studied in any detail. The bone microanatomy of this clade differs from that found in other amniotes, where terrestrial species tend to display characteristics normally seen in aquatic species and vice versa. A detailed histological analysis of the limb bones of S. pardalis reveals extensive variation through ontogeny. Cortical bone becomes increasingly thicker through ontogeny and is finally resorbed in the late sub-adult stage, resulting in a thin cortex and a large infilled medullary cavity. The predominant bone tissues are parallel-fibred and lamellar-zonal for the forelimbs and hind limbs respectively. The oldest individual displayed an External Fundamental System indicating that the growth rate had decreased substantially by this stage. Variability is prevalent between the forelimb and hind limb as well as between early and late sub-adults Forelimb elements exhibit characteristics such as faster growing parallel-fibered bone tissue, slightly higher vascularization and a predominance of annuli over Lines of Arrested Growth (LAG) compared to the hind limb which exhibits poorly vascularized, slower growing lamellar-zonal bone interrupted by LAGs. These differences indicate that the forelimb grew more rapidly than the hind limb, possibly due to the method of locomotion seen in terrestrial species. The extensive bone resorption that occurs from the early sub-adult stage destroys much of the primary cortex and results in a significantly different ratio of inner and outer bone diameter ( p = 3.59 × 10 ⁻⁵ ; df = 28.04) as well as compactness ( p = 2.91 × 10 ⁻⁵ ; df = 31.27) between early and late sub-adults. The extensive bone resorption seen also destroys the ecological signal and infers an aquatic lifestyle for this species despite it being clearly terrestrial. This supports the results of other studies that have found that using bone microanatomy to determine lifestyle in testudines does not produce accurate results.
... For this purpose, previous studies have resorted to manually or automatically segmenting the skeletal element with other (commercial, closed-source) softwares (Behrooz et al. 2017;Gross et al. 2014;. It is noteworthy that the free but closed-source software Bone Profiler (Girondot and Laurin 2003), implements an automatic global compactness acquisition. But the latter is restricted to acquiring parameters for single sections, and large porosity linking the outside of the bone to its internal vacuities, if present, will bias the output. ...
Quantifying the inner structure of bones is central to various analyses dealing with the phenotypic evolution of animals with an ossified skeleton. Computed tomography allows to assess the repartition of bone tissue within an entire skeletal element. Two parameters of importance for such analyses are the global compactness (Cg) and total cross-sectional area (Tt.Ar). However, no open-source, time-efficient methods are available to acquire these parameters for whole bones. A methodology to assess the variation of these parameters along a profile following one of the studied bone’s anatomical axes is also wanting. Here I present an ImageJ macro and associated R script to automatically acquire Cg and Tt.Ar along an axis of the skeletal element of interest using a slice-by-slice approach. No manual segmentation is required and several bones can be present on the analysed scan, as long as the bone of interest is isolated and the largest element on each slice. While some bias might be involved by the automatic acquisition, semi-automatic slice exclusion and correction procedures can be used to efficiently account for it. As a test case, µCT-data was gathered for the mid-lumbar vertebra of over 70 mammals. The two evaluated correction procedures proved to perform equally well, with a slight advantage for the one relying on the exclusion of local outliers. The presented macro allows to efficiently build a dataset concerned with the quantification of bone inner structure. The code being readily available, further improvement of the methodology and adjustment to particular needs can be easily performed.
... Scanned pictures of thin sections were transformed into black (vascular spaces) and white (bone) pictures (S4) that were analyzed with the program Bone Profiler (Girondot and Laurin, 2003) (Table 2; Fig. 3; S3). We examined five parameters provided by this software to characterize the bone density distribution: C, P, S, Min and Max. ...
Placodontia, an enigmatic group of durophagous and in part heavily armoured animals, were members of Sauropterygia, the most diverse and successful group of Mesozoic marine reptiles. Microanatomy and histology of long bones of several armoured and non-armoured Placodontia were studied, covering most of their taxonomic breadth, to elucidate the paleoecology, physiology, and lifestyle of its members. Results reveal an unexpected and not phylogenetically or stratigraphically related disparity of microanatomical and histological features for the group. The non-armoured Paraplacodus and the heavily armoured Psephoderma grew with lamellar-zonal bone tissue type, which is typical for modern sauropsids. In the former, the tissue is nearly avascular surrounding a compacted medullary region, whereas in the latter, the lamellar-zonal bone tissue is vascularized framing a large open medullary cavity and a perimedullary region. Armoured Henodus and Placodontia indet. aff. Cyamodus as well as non-armoured Placodus exhibit a reduced medullary cavity and grew with highly vascularized plexiform to radiating fibro-lamellar bone. Several long bones of Placodontia indet. show circumferential fibro-lamellar bone and can be distinguished into two groups on the basis of microanatomical features. In addition, all bones that grew with fibro-lamellar bone show locally primary spongeous-like architecture and had secondarily widened primary osteons throughout the cortex, resulting in a secondarily spongeous tissue. The highly vascularized fibro-lamellar bone of these Placodontia indicates growth rates comparable to that of open marine ichthyosaurs. Differences in microanatomy and bone histology as expressed by a principal component analysis, thus clearly indicate different paleoecologies, including differences in lifestyle and swimming modes and capabilities in Placodontia. This would have reduced competition in the shallow marine environments of the Tethys and might be a key to their success and diversity. A certain developmental plasticity among the studied placodonts is interpreted as response to different environmental conditions as is obvious from inter- and intraspecific histological variation. Most striking is the difference in life history strategy in armoured Psephoderma and non-armoured Paraplacodus when compared to armoured Henodus , Placodontia indet. aff. Cyamodus , non-armoured Placodus , and Placodontia indet. Bone tissue of Psephoderma and Paraplacodus indicates low growth rates and a low basal metabolic rate, as many modern sauropsids have such as the marine iguana, whereas the others grew with extremely fast growth rates, more typical for birds and mammals, indicating an increased basal metabolic rate.
... Bone compactness of femur SMNS 91357 is 96.8%. The analysis of this femur with Bone Profiler 16 and including the resulting values of this analysis into the Supplementary Excel Sheet (SOM4) of 17 revealed parameters that suggests an amphibious mode of life. ...
Unlike any other tetrapod, turtles form their dorsal bony shell (carapace) not from osteoderms, but by contribution of the ribs and vertebrae that expand into the dermis to form plate-like shell components. Although this was known from embryological studies in extant turtles, important steps in this evolutionary sequence have recently been highlighted by the Triassic taxa Pappochelys, Eorhynchochelys and Odontochelys, and the Permian Eunotosaurus. The discovery of Pappochelys shed light on the origin of the ventral bony shell (plastron), which formed from enlarged gastralia. A major question is whether the turtle shell evolved in the context of a terrestrial or aquatic environment. Whereas Odontochelys was controversially interpreted as aquatic, a terrestrial origin of turtles was proposed based on evidence of fossorial adaptations in Eunotosaurus. We report palaeohistological data for Pappochelys, a taxon that exemplifies earlier evolutionary stages in the formation of the bony shell than Odontochelys. Bone histological evidence reveals (1) evolutionary changes in bone microstructure in ribs and gastralia approaching the turtle condition and (2) evidence for a predominantly amphibious or fossorial mode of life in Pappochelys, which support the hypothesis that crucial steps in the evolution of the shell occurred in a terrestrial rather than fully aquatic environment.
... Bone compactness estimates were made using the program Bone Profiler v.4.5.8 (Girondot & Laurin, 2003). The colour and sizes of the vascular spaces in the rib sections made it impossible for the software to automatically distinguish between surfaces, so the vascular spaces were highlighted and the section image converted to black-and-white in Photoshop before running in Bone Profiler (Supporting Information, Fig. S2). ...
Durophagous mosasaurs are rare members of Late Cretaceous marine faunal assemblages and new fossil discoveries can shed light on their anatomy, functional morphology and evolutionary history. Here we describe a new species in the durophagous genus Globidens from the Maastrichtian phosphate deposits of Morocco, based on a partial disarticulated skull and cervical vertebral series. This new species shares many anatomical similarities with the only other described Maastrichtian species, G. phosphaticus, but differs in several key features, including the absence of pronounced swellings and sulci on the crushing teeth and the absence of cervical zygosphenes and zygantra. Histological thin sections of a rib from the holotype show that this was not a juvenile individual and reveal osteosclerotic-like bone compactness for the first time in a paddle-bearing mosasaurine. We interpret the highly compact ribs, as well as several peculiarities of the temporal arcade and lower jaws, as adaptations to a diet of benthic, hard-bodied prey.
The external morphology and microanatomy of 32 partial and complete Hyperodapedon premaxillae was examined to assess their functional attributes. This revealed morphological correlates for innervation of Hyperodapedon premaxillae in the form of posteriorly opening enlarged neurovascular foramina associated with several grooves, and a prominent neurovascular sulcus. Scanning electron microscopy shows numerous small, circular foramina in clusters along the lateroventral surface towards the anterior tip and along the ventral edge, often in a preferred orientation. These are found associated with high rugosity along the elongated anterolateral depression, and were related to nutrient supply and/or part of the neurovascular system. Selected premaxillae show extremely high bone compactness indices (especially at the anterior end) suggesting specialized osteosclerotic conditions, and dense and compact bone microstructure with almost no clear transition between the outer compact cortex and inner core. With ontogeny, the premaxillae became lateromedially thickened by deposition of lamellar zonal bone, and highly vascularized and dense from intense Haversian remodelling, suggesting pachyosteosclerosis of the premaxillae. Other characteristic features include profuse open vascular channels or a frayed margin at the anteroventral tip, and dense bundles of long and wavy extrinsic fibres. These features, along with high bone compactness, decrease posteriorly towards the naris. It is proposed that the Hyperodapedon premaxillae were covered by keratinized epithelium or rhamphotheca at the anterior end, and had heightened sensory capabilities that aided foraging for mussels and other invertebrates in soft sediments under shallow water. Such enhanced sensory capability is reported for the first time in an early‐diverging archosauromorph.
A basal member of Balaenomorpha (Cetacea, Mysticeti), Persufflatius renefraaijeni, n. gen., n. sp., is described based on cranial material discovered in upper Miocene deposits of Liessel (the Netherlands). Thanks to the palynological analysis of an associated sediment sample, the specimen is dated from the late Tortonian (Dinozone SNS M14: c. 8.2-7.6 Ma). Our phylogenetic analysis recovers the new taxon at the base of the successful crown mysticete clade leading to modern rorquals. Though the holotype is
only partially preserved (it consists of the partial right side of the neurocranium), it provides new data on the cranial anatomy of these early relatives of extant rorquals, which are poorly represented in the global fossil record. Several skull parts (postglenoid process of the squamosal, base of the zygomatic process of the squamosal, the
anteromedioventral portion of the squamosal bone, and the exoccipital) show unusual swelling due to pachyostosis, giving the whole lateral basicranial region an inflated aspect.
We present a detailed histological study of long bones from an ontogenetic series of Mussaurus patagonicus, an early sauropodomorph from the Lower Jurassic of Argentina. Twenty long bones, including humeri, femora and fibulae, obtained from 13 individuals of different body sizes were sampled for histological analysis. In general terms, the cortical bone is formed by a well vascularized fibrolamellar and parallel fibred bone. Except for the smaller individuals, cyclical growth marks (CGMs) are well recorded in all the specimens but their number and relative position is highly variable. Mussaurus exhibits marked variation regarding relative growth rate, with some individuals growing much faster than others. Such variation affects the size of the adult individuals, which results in a poor correlation between the body size and the age/ontogenetic stage for this taxon. These discrepancies may be related to sexual dimorphism and/or developmental plasticity. Intraspecific variation is also recorded with regard to the growth strategies, which can vary from cyclical, as in other early sauropodomorphs, to continuous, as reported in sauropods. Sexual maturity appears to have been reached between 23 and 31 years, which is delayed in comparison to other early sauropodomorphs but more comparable with derived sauropods. The attainment of somatic maturity appears to have been reached at about 14 years after onset of sexual maturity. Mussaurus is a sauropodiform, phylogenetically closer to sauropods than most other Early Jurassic sauropodomorphs, and therefore provides critical information for understanding palaeobiological aspects of the origin of sauropods and the onset of gigantism in this lineage.
Myhrvold et al. suggest that our inference of subaqueous foraging among spinosaurids is undermined by selective bone sampling, inadequate statistical procedures, and use of inaccurate ecological categorizations. Myhrvold et al. ignore major details of our analyses and results, and instead choose to portray our inferences as if they were based on qualitative interpretations of our plots, without providing additional analyses to support their claims. In this manuscript, we thoroughly discuss all the concerns exposed by Myhrvold et al.. Additional analyses based on our original datasets and novel data presented by Myhrvold et al. do not change our original interpretations: while the spinosaurid dinosaurs Spinosaurus and Baryonyx are recovered as subaqueous foragers, Suchomimus is inferred as a non-diving animal.
Secondary aquatic adaptations evolved independently more than 30 times from terrestrial vertebrate ancestors1,2. For decades, non-avian dinosaurs were believed to be an exception to this pattern. Only a few species have been hypothesized to be partly or predominantly aquatic3–11. However, these hypotheses remain controversial12,13, largely owing to the difficulty of identifying unambiguous anatomical adaptations for aquatic habits in extinct animals. Here we demonstrate that the relationship between bone density and aquatic ecologies across extant amniotes provides a reliable inference of aquatic habits in extinct species. We use this approach to evaluate the distribution of aquatic adaptations among non-avian dinosaurs. We find strong support for aquatic habits in spinosaurids, associated with a marked increase in bone density, which precedes the evolution of more conspicuous anatomical modifications, a pattern also observed in other aquatic reptiles and mammals14–16. Spinosaurids are revealed to be aquatic specialists with surprising ecological disparity, including subaqueous foraging behaviour in Spinosaurus and Baryonyx, and non-diving habits in Suchomimus. Adaptation to aquatic environments appeared in spinosaurids during the Early Cretaceous, following their divergence from other tetanuran theropods during the Early Jurassic17. In extinct species including non-avian dinosaurs, bone density is shown to be a reliable indicator of aquatic behavioural adaptations, which emerged in spinosaurids during the Early Cretaceous.
Dicynodonts represent an emblematic Permian-Triassic (P-Tr) taxa to survive the big crisis at the end of Permian. The evolution of Triassic dicynodonts and their recovery conditions are still unclear. This work focused on the Laotian and Moroccan forms. The post-crisis recovery of dicynodonts would appear to be earlier as supported by the description of two new Laotian species (Counillonia superoculis and Repelinosaurus robustus) in Early Triassic. Despite their non-consensual phylogenetic relationships, they support the survivorship of multiple lineages across the P-Tr boundary. Paleophysiological models inferred high metabolism in Permian and Triassic studied dicynodonts, refuting the hypothesis of a high metabolism to mainly explain differential survival beyond the crisis. They also highlighted a unique acquisition of the endothermy in Synapsida occurring at least in middle Permian at the Neotherapsida node. Considering the age and the terrestrial lifestyle of dicynodonts, a terrestrial connection between the Indochina Block and Pangea could thus be interpreted at least in late Permian-Early Triassic. A new dicynodont postcranial material discovered in Morocco was studied and a taxonomic revision of the Moroccan forms was made. Moghreberia nmachouensis was considered as valid and clearly distinguished from Placerias. The restudy of the cranial material of Azarifeneria did not allow distinguishing it from other Triassic genera. In addition to Moghreberia, a second morphotype, more robust, could be noticed in the postcranial material. The large size of Moghreberia and of the second big morphotype confirmed an increase of the body size in dicynodonts during the Triassic.
Evidence for terrestriality in early tetrapods is fundamentally contradictory. Fossil trackways attributed to early terrestrial tetrapods long predate the first body fossils from the Late Devonian. However, the Devonian body fossils demonstrate an obligatorily aquatic lifestyle. Complicating our understanding of the transition from water to land is a pronounced gap in the fossil record between the aquatic Devonian taxa and presumably terrestrial tetrapods from the later Early Carboniferous. Recent work suggests that an obligatorily aquatic habit persists much higher in the tetrapod tree than previously recognized. Here, we present independent microanatomical data of locomotor capability from the earliest Carboniferous of Blue Beach, Nova Scotia. The site preserves limb bones from taxa representative of Late Devonian to mid-Carboniferous faunas as well as a rich trackway record. Given that bone remodels in response to functional stresses including gravity and ground reaction forces, we analysed both the midshaft compactness profiles and trabecular anisotropy, the latter using a new whole bone approach. Our findings suggest that early tetrapods retained an aquatic lifestyle despite varied limb morphologies, prior to their emergence onto land. These results suggest that trackways attributed to early tetrapods be closely scrutinized for additional information regarding their creation conditions, and demand an expansion of sampling to better identify the first terrestrial tetrapods.
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.
Multiple limb bones of different Middle Triassic capitosaurs from India including Cherninia denwai and Paracyclotosaurus crookshanki were examined to reveal differences in palaeobiology and lifestyle adaptations. Limb bone anatomy of Cherninia is characterized by distinct torsion and its absence in the fore and hindlimb bones, respectively. Substantial torsion is seen in all the limb bones of P. crookshanki. Woven fibred bone tissue, a very rapidly deposited tissue mostly seen in the embryos and very young individuals of higher vertebrates, is reported for the first time in a juvenile temnospondyl. Predominance of incipient fibrolamellar bone tissue is seen in a large bodied Middle Triassic temnospondyl suggesting that such tissues in non‐amniotes helped in achieving large body sizes rapidly. Highly vascularized woven fibred bone tissue in the early ontogeny, transforming to a more stable incipient fibrolamellar bone tissue associated with growth marks later in ontogeny characterizes C. denwai. This suggests rapid sustained growth slowed down and became punctuated later in ontogeny. A continuous slow growth throughout ontogeny is suggested for P. crookshanki as parallel fibred bone and azonal lamellar bone tissue are seen in all the examined limb bones. The growth of C. denwai and P. crookshanki had variable susceptibility to seasonal fluctuations. The onset of sexual maturity was at 55% adult size for Cherninia as implied from the change in tissue type. Cherninia inhabited the bottom of the water column and acted as a passive benthic predator whereas Paracyclotosaurus was a shallow water predator that retained a high level of terrestriality.
The first two volumes are complete revisions of Kendall's two volumes, written in 1943 and 1946. Harvard Book List (edited) 1971 #77 (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Some bones have slender marrow cavities and relatively thick walls. Others have wide cavities and thinner walls. Such differences are described by a quantity K, the ratio of the internal to the external diameter. A theoretical analysis shows that the optimum value of K, which allows the mass of a bone to be minimized, depends on whether the bone is selected principally for yield or fatigue strength, for ultimate strength, for impact strength or for stiffness. It also depends on whether the cavity is filled with marrow or with gas. The values of K found in the limb bones of mammals, birds and a few reptiles are surveyed, and compared to the theoretical optima.
Variation in long bone cross-sectional geometry can be given a more precise functional interpretation using engineering beam theory. However, difficulties in measurement technique have generally prevented studies of large samples of cross sections in this way. In the present study, an automated system utilizing an electronic digitizer and computer software was used to analyze cross-sectional geometric properties of 11 femoral and tibial locations in 119 individuals from the Pecos Pueblo, New Mexico site. The data generated allow identification of clear differences in geometric properties between different regions of the femur and tibia. These differences appear to be related to specific in-vivo mechanical loadings of the lower limb bones, serving to reduce stress and strain under these loadings. The data are also used to investigate possible differences in loading of the femur and tibia in the Pecos and modern samples, and between humans and a nonhuman primate sample.
Cortical area, maximum second moment of area and polar moment were calculated for the long bones of 39 species of birds. Regressions of all these parameters to body mass were established. At the same time, the orientations of the maximum second moment of area were statistically tested. The parameters calculated on humerus and ulna scaled according to the predictions derived from the geometric similarity hypothesis, while those calculated for the long bones of the leg showed higher exponents, very close to the predictions of the elastic similarity hypothesis. Confidence intervals calculated for radius parameters appeared to agree with both predictions. Only the for tarsometarsus was it impossible to establish a global orientation pattern for the maximum second moment of area. In the other cases, the orientation was: sagittal in the radius, posteromedial-anterolateral in the proximal long bones (humerus and femur) and posterolateral-anteromedial in the distal long bones (ulna and tibiotarsus). The implications of the present findings are discussed in terms of the possible correlations between the orientation patterns produced in the cross-sectional geometry of avian long bones and the load carried.
The first quantitative experimental data on growth dynamics of the primary cortical bone of young ratites demonstrate the following. 1) From hatching to 2 months of age, cortical thickness remains constant, thereby expressing equilibrium between periosteal bone deposition and an endosteal bone resorption. 2) Radial growth rates of the diaphyseal bone cortex are high (10-40 microns.day-1 on average--maximum 80 microns.day-1) in the hindlimb (femur, tibiotarsus and tarsometatarsus). Wing bones are smaller and later developed. They have lower rates of radial osteogenesis (2-14 microns.day-1). 3) High growth rates are linked to densely vascularized primary bone belonging to the reticular or laminar tissue types. Growth rates fall when bone vascular density decreases. These results emphasize the importance of examining a large number of skeletal elements in order to build a precise knowledge of the general relationship between bone growth rate and bone tissue type. They also stress the potential of bone growth rate quantification among extinct tetrapods, including non-avian dinosaurs.
Implications for assessing growth in dinosaurs. Comptes Rendus de l'Académie des Sciences de Paris, Sciences de la vie
- K C Rogers
- J Cubo
- J.-J Boisard
---, K. C. Rogers, J. Cubo, and J.-J. Boisard. 2000. Periosteal bone
growth rates in extant ratites (ostrich and emu). Implications for
assessing growth in dinosaurs. Comptes Rendus de l'Académie des
Sciences de Paris, Sciences de la vie/Life sciences 323:543-550.
- M Kendall
- A Stuart
Kendall, M., and A. Stuart. 1979. The Advanced Theory of Statistics,
Vol. 2. Charles Griffin, London, 748 pp.