The many adaptations of bone

Studies concerned with the "adaptations" in bones usually deal with modelling taking place during the individual's lifetime. However, many adaptations are produced over evolutionary time. This survey samples some adaptations of bone that may occur over both length scales, and tries to show whether short- or long-term adaptation is important. (a) Woven and lamellar bone. Woven bone is less mechanically competent than lamellar bone but is frequently found in bones that grow quickly. (b) Stress concentrations in bone. Bone is full of cavities that potentially may act as stress concentrators. Usually these cavities are oriented to minimise their stress-concentrating effect. Furthermore, the "flow" of lamellae round the cavities will still further reduce their stress-concentrating effect, but the elastic anisotropy of bone will, contrarily, tend to enhance it in normal loading situations. (c) Stiffness versus toughness. The mineral content of bone is the main determinant of differences in mechanical properties. Different bones have different mineral contents that optimise the mix of stiffness and toughness needed. (d) Synergy of whole bone architecture and material properties. As bone material properties change during growth the architecture of the whole bone is modified concurrently, to produce an optimum mechanical behaviour of the whole bone. (e) Secondary remodelling. The formation of secondary osteones in general weakens bone. Various suggestions that have been put forward to account for secondary remodelling: enabling mineral homeostasis; removing dead bone; changing the grain of the bone; taking out microcracks. (f) The hollowness of bones. It is shown how the degree of hollowness is adapted to the life of the animal.     

四川自贡大山铺中侏罗世蜀龙和峨眉龙长骨骨组织结构的初步研究

通过对四川自贡大山铺恐龙动物群中两种主要蜥脚类恐龙—李氏蜀龙和天府峨眉龙肱骨和尺骨的骨组织结构观察,并与我国晚白垩世的几种恐龙长骨进行对比,结果发现:1)恐龙的长骨都具有快速的后生生长速率;2)恐龙的生长方式属于非限定生长,即在成年后并不停止生长;3)不同类型的恐龙到了成年以后,其骨沉积速率可能有较大差异;4)不同类型的恐龙在长骨的生长改建过程中,骨组织内部的重吸收作用有较大差异;5)生长轮结构在不同部位的骨骼中或在骨骼的生长发育过程中可能也有较大差异。     

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

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

Long bone microstructure gives new insights into the life of pachypleurosaurids from the Middle Triassic of Monte San Giorgio,Switzerland/Italy

The long bone microstructure of four pachypleurosaurid taxa from Monte San Giorgio (Switzerland/Italy) was studied. Pachypleurosaurids are secondarily aquatic reptiles that lived during the Middle Triassic in varying marine environments of the Tethys. All four pachypleurosaurids show high compactness values in their long bones based on a thick cortex and a calcified cartilaginous core, which remains in the medullary region throughout the ontogeny. Parts or even the entire embryonic bone layer composed of a mixture of woven-fibered bone tissue and parallel-fibered bone tissue is preserved in both pachypleurosaurid genera. The rest of the cortex consists of lamellar-zonal bone tissue type. Differences in the microstructure of the bones between the pachypleurosaurids are reflected in the occurrence of remodelling processes, which, if present, affect the innermost growth marks of the cortex or the calcified cartilaginous core. Further variation is present in the spacing pattern of the growth cycles, as well as in the degree of vascularisation of the lamellar-zonal bone tissue type. Our data on the microstructure of the long bones support previous studies on morphology and facies distribution, which indicated different habitats and adaptation to a secondary aquatic lifestyle for each pachypleurosaurid taxon. Life history data furthermore reflect different longevities and ages at sexual maturity. The bone histological data of the stratigraphically youngest and oldest pachypleurosaurid species might indicate possible climate-dependant reproductive seasons similar to Recent lacertilian squamates.     

Postnatal long bone growth in terrestrial placental mammals: Allometry,life history,and organismal traits

The ontogenetic allometry of long bone proportions is poorly understood in Mammalia. It has previously been suggested that during mammalian ontogeny long bone proportions grow more slender (positive allometry; length ∝ circumference^>1.0), although this conclusion was based upon data from a few small‐bodied taxa. It remains unknown how ontogenetic long bone allometry varies across Mammalia in terms of both taxonomy and body size. We collected long bone length and circumference data for ontogenetic samples of 22 species of mammals spanning six major clades and three orders of magnitude in body mass. Using reduced major axis bivariate regressions to compare bone length to circumference, we found that isometry and positive allometry are the most widespread patterns of growth across mammals. Negative allometry (i.e., bones growing more robust during ontogeny) occurs in mammals but is largely restricted to cetartiodactyls. Using regression slope as a proxy for long bone allometry, we compared long bone allometry to life history and organismal traits. Neonatal body mass, adult body mass, and growth rate have a negative relationship with long bone allometry. At an adult mass of roughly 15–20 kg, long bone growth shifts from positive allometry to mainly isometry and negative allometry. There were no significant relationships between ontogenetic long bone allometry and either cursoriality or basal metabolic rate. J. Morphol. © 2012 Wiley Periodicals, Inc.     

Revisiting the links between bone remodelling and osteocytes: insights from across phyla

We question two major tenets of bone biology: that the primary role of remodelling is to remove damage in the bone (so‐called damage‐driven remodelling) and that osteocytes are the only strain‐sensing orchestrators of this process. These concepts are distilled largely from research on model mammal species, but in fact, there are a number of features of various bones, from mammalian and non‐mammalian species, that do not accord with these ‘rules’. Here, we assemble a variety of examples, ranging from species that lack osteocytes but that still seem capable of remodelling their bones, to species with osteocytic bones that do not remodel, and to instances of inter‐species, inter‐bone and/or intra‐bone variation in bone remodelling that show that this purported repair process is not always where the ‘rules’ tell us it should be. This collection of points argues that our understanding of the advantages, roles and primary drivers of remodelling are inadequate and biased to quite a small phylogenetic cross section of the species that possess bone. We suggest a variety of new directions for bone research that would provide us with a better understanding of bone remodelling, tying together the interests of comparative biologists, palaeontologists and medical researchers.     

Note on the venous drainage of the gorilla (Gorilla gorilla) diploe

One-quarter or more of gorilla skulls manifest a canonically unrecognized foramen in the dorsal parieto-occipital region. This orifice (foramen obelionicum) affords exit to a notably large 'emergent' vein (vena obehonicd) draining the cranial vault diploe. These correlated structures affirm the presence of a mechanism of vault diploe drainage supplementary to that basic to all gorilla crania. Their anatomy is described herein. It is possible that the vena obelionica represents a Breschet formation, known so far for the human diploe only.     

Bone histology of Silesaurus opolensisDzik, 2003 from the Late Triassic of Poland

Fostowicz‐Frelik, ?. & Sulej, T. 2009: Bone histology of Silesaurus opolensisDzik, 2003 from the Late Triassic of Poland. Lethaia, Vol. 43, pp. 137–148. The phylogenetic relationships of Silesaurus opolensis have been the subject of intense debate since its discovery. Silesaurus possesses some features characteristic of ornithischian dinosaurs, such as the presence of a beak at the front of the lower jaw, yet it lacks a number of important femoral and dental synapomorphies of Dinosauria. The microstructure of the long bones (femur, tibia and metatarsal) and ribs of this species reveals a relatively intensive rate of growth, comparable with that seen in small dinosaurs and the gracile crocodylomorph Terrestrisuchus. Cortical bone formed mainly by periosteal tissue with fibro‐lamellar matrix (in older specimens parallel fibred) shows very little secondary remodelling and only in one specimen (large tibia ZPAL Ab III/1885) few lines of arrested growth are present in the outermost cortex. The vascularization is relatively dense, mainly longitudinal and ceases towards the periphery, forming almost avascular parallel fibred bone at the bone surface. This indicates maturation and significant decrease in the growth ratio in mature specimens of S. opolensis. The delicate trabeculae exhibit cores formed by the primary cancellous tissue lined with lamellar endosteal bone. The rather intense growth of S. opolensis implies a relatively high metabolic rate. Moreover, evidence from the fibro‐lamellar tissue, predominant in the cortex, suggests that this kind of rapid bone deposition could be more typical of Archosauria than previously assumed, a prerequisite for the evolution of the very fast growth rates observed in large ornithischians, sauropods and large theropods. □Archosauria, Bone histology, Dinosauriformes, Late Triassic, Silesaurus opolensis.     

Comparative analysis of bone remodelling models with respect to computerised tomography-based finite element models of bone

Subject-specific finite element models are an extensively used tool for the numerical analysis of the biomechanical behaviour of human bones. However, bone modelling is not an easy task due to the complex behaviour of bone tissue, involving non-homogeneous and anisotropic mechanical properties. Moreover, bone is a living tissue and therefore its microstructure and mechanical properties evolve with time in a known process called bone remodelling. This phenomenon has been widely studied, many being the numerical models that have been formulated to predict density distribution and its evolution in several bones. The aim of the present study is to assess the capability of a bone remodelling model to predict the bone density distribution of different types of human bone (femur, tibia and mandible) comparing the obtained results with the bone density estimated by means of computerised tomography. Good accuracy was observed for the bone remodelling predictions including the thickness of the cortical layer.     

Osteoderm microstructure of “rauisuchian” archosaurs from South America

In this contribution we analyze and discuss the microanatomy and histology of postcranial osteoderms of a number of “rauisuchians” from different localities of South America (Argentina and Brazil). The studied sample includes osteoderms of Fasolasuchus tenax, Prestosuchus chiniquensis, Saurosuchus galilei and an undetermined rauisuchian from Brazil. The bone microanatomy of the osteoderms is variable: whereas some specimens have a rather compact structure, others show a diploe architecture with a central cancellous core bordered by two compact cortices. Both external and basal cortices are mainly composed of poorly vascularized, fine and coarse parallel-fibred bone and networks of interwoven and mineralized fiber bundles. The internal region of the non-remodeled specimens consists of a well-vascularized core in which the intrinsic fibers exhibit important variations (even in the same specimen), ranging from coarse, parallel-fibred to woven-fibred bone tissues. Lines of arrested growth (LAGs) are well recorded in both basal and external cortices. Differences in the bone microstructure (compact vs. diploe) could be related to the age, sex and reproductive status of the sampled individuals. Hence, age estimation based on the count of LAGs in rauisuchian osteoderms appears to be reliable only in the early stages of ontogeny. The bone microstructure suggests that rauisuchian osteoderms were originated through a mechanism that involves both intramembranous and metaplastic ossifications.     

Palaeohistology of the bones of pterosaurs (Reptilia: Archosauria): anatomy, ontogeny, and biomechanical implications

Thin sections from long bones of specimens representing pterosaurs ranging from the Early Jurassic to the latest Cretaceous provide a profile of bone histology across a range of sizes, skeletal elements, growth stages, and phylogenetic positions. Most pterosaur bone is fibro-lamellar, organized in an unusual way that suggests high growth rates through ontogeny. Fibro-lamellar deposits are finished by a relatively abrupt deceleration or cessation of growth represented by lamellar, poorly vascularized subperiosteal bone in what appear to be adults. Pterosaurs had the thinnest bone walls of any tetrapods; they complemented high rates of periosteal deposition with almost equally high rates of endosteal erosion. Pterosaurs show a great variety of histologic features that include articular calcified cartilage, sub-chondral bone plates, trabecular bone struts and related internal supports, and secondary deposition and remodeling of bone. They remodeled their bones internally by (1) depositing endosteal bone coatings on the inner cortex and over struts of pre-existing internal bone, (2) secondarily filling bone spaces, and (3) Haversian reworking. The construction of these struts reflects both developmental patterns of bone construction and biomechanical function. Alternating plywood-like layers of bone, heretofore undescribed in tetrapods, provided strength, as did the obliquely oriented system of reticular blood vessels in the bones. The distribution and ontogenetic features of pterosaur bone tissues, when combined with other evidence, suggest generally high growth rates, high metabolic levels, altricial birth, and extended parental care.     

Unexpected microanatomical variation among Eocene Antarctic stem penguins (Aves: Sphenisciformes)

The microanatomical and histological structure of Eocene Antarctic stem penguin tarsometatarsi is examined in order to characterise the bone microstructure. Eight adult tarsometatarsi belonging to eight fossil species (Palaeeudyptes gunnari, Palaeeudyptes klekowskii, Anthropornis grandis, Anthropornis nordenskjoeldi, Archaeospheniscus wimani, Marambiornis exilis, Delphinornis arctowskii and Delphinornis larseni) collected from the Antarctic A. nordenskjoeldi Biozone (La Meseta Formation, ～34.2 Ma) were examined. The thin sections revealed a distinctive microanatomical variation among taxa. Whereas Anthropornis spp., A. wimani and P. gunnari possess massive, clearly osteosclerotic bones (medullary cavities absent or strongly reduced), the bones of Delphinornis spp., P. klekowski and M. exilis exhibit well-developed medullary cavities. The cortical bone in all the specimens consists of primary, well-vascularised fibro-lamellar bone and variable amounts of secondary bone. Medullary cavities are coated by a thick layer of lamellar bone tissue and coarse compacted cancellous bone. Although several causes can explain the striking microanatomical variation (e.g. ontogeny), we interpret that such variation is related to differential adaptations to the aquatic life, for which taxa with more massive bones were possibly adapted to deeper and more prolonged diving excursions.     

New insights from bone microanatomy of the Late Triassic Hyperodapedon (Archosauromorpha,Rhynchosauria): implications for archosauromorph growth strategy

Bone microanatomy of multiple postcranial skeletal elements of several individuals of Hyperodapedon collected from India is reported. This reveals that fibrolamellar bone tissue is predominant in the mid‐ and inner cortices, whereas the peripheral region of the cortex is composed of either parallel‐fibred and/or lamellar bone. The pattern of primary osteons mostly ranges between laminar and subplexiform. Such predominance of fibrolamellar bone tissue in the cortex suggests an overall fast growth, which slowed down considerably later in ontogeny. Four distinct ontogenetic stages are identified based on the bone microstructure. During the juvenile stage, growth was fast and continuous, but it became punctuated during the early and late sub‐adult stages. In adult individuals, growth was slow and showed periodic interruption but did not stop completely, suggesting that Hyperodapedon had an indeterminate growth strategy. Interelemental histovariations affecting cortical thickness, organization of the vascular network, incidence of growth rings and extent of secondary reconstruction are noted. Throughout ontogeny, the femora show higher cortical thickness than humeri and tibiae, suggesting differential appositional growth rate between the skeletal elements. Differences in cortical thickness are noted in the ribs, which suggest differential functional constraints based on anatomical site‐specific occurrences. Although fibrolamellar bone tissue became progressively more dominant towards the archosaurs, there are considerable variations in the growth patterns of the archosauromorphs. This is exemplified by the bone microstructure of Hyperodapedon, which deviates from the generalized slow‐growth pattern proposed for all basal archosauromorphs, suggesting that rapid growth was already present in the archosauromorphs. The cortical thickness of various long bones of Hyperodapedon bears similarity with that of several extant terrestrial quadrupeds, suggesting that Hyperodapedon was essentially a terrestrial quadruped.     

Muscle‐induced loading as an important source of variation in craniofacial skeletal shape

The shape of the craniofacial skeleton is constantly changing through ontogeny and reflects a balance between developmental patterning and mechanical‐load‐induced remodeling. Muscles are a major contributor to producing the mechanical environment that is crucial for “normal” skull development. Here, we use an F₅ hybrid population of Lake Malawi cichlids to characterize the strength and types of associations between craniofacial bones and muscles. We focus on four bones/bone complexes, with different developmental origins, alongside four muscles with distinct functions. We used micro‐computed tomography to extract 3D information on bones and muscles. 3D geometric morphometrics and volumetric measurements were used to characterize bone and muscle shape, respectively. Linear regressions were performed to test for associations between bone shape and muscle volume. We identified three types of associations between muscles and bones: weak, strong direct (i.e., muscles insert directly onto bone), and strong indirect (i.e., bone is influenced by muscles without a direct connection). In addition, we show that although the shape of some bones is relatively robust to muscle‐induced mechanical stimulus, others appear to be highly sensitive to muscular input. Our results imply that the roles for muscular input on skeletal shape extend beyond specific points of origin or insertion and hold significant potential to influence broader patterns of craniofacial geometry. Thus, changes in the loading environment, either as a normal course of ontogeny or if an organism is exposed to a novel environment, may have pronounced effects on skeletal shape via near and far‐ranging effects of muscular loading.     

Postnatal ontogeny, population structure, and extinction of the giant moa Dinornis

Recent reinterpretation of the giant moa Dinornis as consisting of two sexually dimorphic allospecies permits thorough site-by-site investigation of the ontogeny and population biology of this genus. Analysis of subadult skeletal material from natural swamp sites in the North and South Islands of New Zealand forms the basis for recognition of growth series for each long bone element, characterized by sequential formation of fossulae in the femur and fusion of bones in the tibiotarsus and tarsometatarsus. Femora reached progressive developmental stages more rapidly than the other long bones, but all three elements reached maturity at about the same time. Patterns of bone fusion in Dinornis are more similar to those in Apteryx than in Struthio, and kiwi are recognized as a suitable developmental analog for interpreting moa ontogeny. Samples from Bell Hill Vineyard Swamp (South Island) and Makirikiri swamp (North Island) are interpreted as representing autochthonous moa populations; comparison with stages of kiwi long bone development suggests that Dinornis at these sites had high adult survivorship in strongly K-selected populations, with 72.5-87.3% of individuals having achieved adult body mass, and 55.9-78.2% being sexually mature. The pattern of low fecundity and probable high longevity in both Dinornis species suggests that populations were vulnerable to loss of adults, primarily through hunting, rather than as a result of habitat destruction.