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Session Schedule & Abstracts

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Thursday 30th June, 2016

Symposium: New insights into skeletal microstructure of vertebrates, extant and extinct 2

Room: Salon A   11:30 am–1:00 pm

Moderator(s): E. Rega, M. Dean, & T. Owerkowicz
BON2-1  11:30 am  Functional cranial joint histology in reptiles and birds and its significance for avian cranial kinesis . Bailleul AM*, University of Missouri; Horner JR; Witmer LM; Holliday CM
Abstract: Joint microstructure has been intensively studied in mammals in many biological contexts, but comparatively little is known about joint tissues in the skulls of birds, archosaurs, and other reptiles, which is surprising given the extraordinary diversity of kinetic capacity among the fibrous and synovial joints that connect their cranial bones. The evolutionary origins of major clades hinge on modifications of their articulations. Thus, new data on cranial joint tissue structure and function are necessary to understand reptilian cranial evolution. Here, we investigated the microstructural details of numerous cranial joints (e.g., jaw, otic, palatobasal joints, craniofacial sutures, and flexion zones) of adult and young emus, ducks, alligators, lizards and several non-avian dinosaurs. Histology was paired with microCT data to better visualize 3D morphology. These findings were used to investigate 1) if clade-specific characteristics exist among reptiles at the microscopic scale; 2) if specific tissues coincide with particular loading environments; and 3) how joint structure reflects its function. For example, are akinetic synovial joints built similarly to mobile ones? How do flexion zones and other complex joints facilitate cranial kinesis? Whereas birds and non-avian dinosaurs form articular cartilage on the membrane bone components of their synovial joints, crocodilians and lizards do not. Moreover, whereas adult birds possess a periosteum in their craniofacial sutures, adult crocodilians and non-avian dinosaurs lack this layer, and sutural growth is mediated mostly via metaplasia. New data also show that suture fusion does not necessarily imply akinesis, since the flexible craniofacial hinge of ducks is a synostosis made of chondroid bone. These results have significant implications for the origins of avian cranial kinesis within non-avian dinosaurs, the developmental underpinnings of joint homology, and the inference of kinetic capacity in extinct reptiles.

BON2-2  12:00 pm  Atmospheric oxygen conditions do not constrain growth or biomechanical performance of limb bones in Alligatoridae: Alligator mississippiensis. Lujan S.L.*, California State University, San Bernardino; Owerkowicz T.O., California State University, San Bernardino; Elsey R.M., Louisiana Department of Wildlife and Fisheries, Grand Chenier LA; Hicks J.W., University of California, Irvine; Middleton K.M., University of Missouri, Columbia
Abstract: Growth rates in extinct taxa are frequently based on comparisons with those of extant relatives; this assumes that prevalent environmental conditions influencing growth were similar to those of modern day. An often overlooked factor is atmospheric oxygen; today's levels are 21% (normoxia) but during the Phanerozoic levels may have ranged from 15% O2 (hypoxia) to 35% O2 (hyperoxia). To test the effects of available oxygen on growth and biomechanics in a non-traditional vertebrate model, eggs were incubated and hatchlings of the American alligator reared in five distinct oxygen environments (16-36%). Alligators were sacrificed at intervals, femora removed and cross-sectional geometry of the mid-diaphyses studied. A preliminary analysis with femur length growth modeled as either a determinant or indeterminate process found no significant difference among treatments, so traits were standardized to this feature to compare differently sized animals. Results of analysis of covariance with femur length as covariate reveal no significant differences in cross-sectional geometry between treatment groups. Subsequent analyses with all groups pooled showed that anteroposterior and mediolateral diameters scale with significant negative allometry, while cross sectional area scales with significant positive allometry. Inertial moments also scale with negative allometry, but section moduli scale isometrically. The alligator femora exhibit a narrower mid-diaphyseal diameter but significantly more cortical bone than expected by isometry. The combination of these two scaling patterns results in a bone as resistant to bending as predicted. Lack of an observed treatment effect in either skeletal growth or limb biomechanics suggests that extant alligators are not limited by available oxygen. We hypothesize that the unique cardiac morphology in alligators may allow the animals to regulate their internal oxygen milieu independently of atmospheric conditions. Supported by NSF IOS- 0922756.

BON2-3  12:15 pm  Effect of embryonic calcium constraint on post-hatching growth and bone microstructure in the American alligator (Alligator mississippiensis). Membreno N.A.*, California State University, San Bernardino; Elsey R.M., Rockefeller Wildlife Refuge, Louisiana Dept. of Wildlife and Fisheries; Owerkowicz T., California State University, San Bernardino
Abstract: Among oviparous reptiles, archosaurs lay eggs with the thickest and most rigid eggshells. During embryonic development, archosaurs mobilize eggshell calcium to the yolk sac, and upon hatching rely on this calcium reservoir to supplement their dietary calcium intake. This additional source of calcium may have allowed archosaurs to achieve high post-hatching growth rates. We tested this hypothesis by incubating eggs of the American alligator, and following post-hatching growth for over two months. The calcareous eggshells were either experimentally peeled or sham-handled with the fibrous shell membrane left intact in both treatment groups. At hatching, experimental animals were significantly smaller than the clutch-matched controls. There was considerable variation in growth rates within both groups, but overall control animals grew significantly faster than experimental ones. Standardized to bone length, femora and lower jaws of three month-old experimental animals had smaller cross-sectional area, second moment of area, and polar moment of inertia. Cortical thickness was decreased, as was lacunar density. Incomplete osteone formation resulted in prominent vascular spaces in the lower jaws of experimental alligators. Considering a lower bone mineral content in the experimental group, these results suggest that insufficient calcium supply exerts negative feedback on bone tissue growth, and archosaurs cannot compensate for decreased material stiffness by augmenting the geometric properties of skeletal elements, even those critical to locomotion or feeding. We propose that selective forces on post-hatching survival drove the evolution of ever-thicker and mineralized eggshell of archosaur eggs. Eggshell and bone microstructure of extinct archosaurs may contain clues to their calcium-handling strategies.

BON2-4  12:30 pm  How's your apatite? Structure and mechanics of elasmobranch skeletal tissues. Porter ME*, Florida Atlantic University, FL USA; Huber DR, Department Biology, The University of Tampa, Tampa, FL USA; Seidel R, Department Biomaterials, Max Planck Institute of Colloids & Interfaces, Potsdam, Germany; Ford J, Department Radiology, University of South Florida Morsani College of Medicine, Tampa, FL USA; Decker S, Department Radiology, University of South Florida Morsani College of Medicine, Tampa, FL USA; Dean MN, Department Biomaterials, Max Planck Institute of Colloids & Interfaces, Potsdam, Germany
Abstract: Elasmobranchs are singular among vertebrate clades in having cartilaginous skeletons. An understanding of the functional properties of elasmobranch skeletal tissues, and their phylogenetic relationships to other vertebrate tissues, is only possible through investigations of their growth, structure, and mechanical behavior. Despite meticulous early work on elasmobranch skeletal anatomy, the study of fine-scale skeletal structure and its relationship to skeletal mechanics is still in its infancy. Previous efforts have been limited by difficulties in visualizing and mechanically testing biological tissues with complex ultrastructures and comprised of materials with dissimilar mechanical properties. However, advances in imaging resolution and techniques, and the increased application of engineering tools to biological questions have brought rich insight into the form and function of elasmobranch tissues. We synthesize available data on the anatomy of the known types of elasmobranch cartilage (areolar cartilage, tessellated cartilage), discussing the mechanics and ultrastructure of these tissues, while also highlighting less studied natural variations on tessellated cartilage (e.g., structural reinforcements in the jaws of durophagous species, "woody" cartilage in lamnid rostra) and types of pathologic mineralization (e.g., vertebral calluses, mineralized endophytic masses), which have been linked to developmental, nutritional, and behavioral factors. Furthermore, we integrate our knowledge of skeletal structure and tissue mechanics, by presenting data from physical and FEA models that speak to the functional advantages and disadvantages of a purely cartilaginous skeleton and selective pressures associated with its evolution. In particular, we highlight recent modeling data showing that stress distribution and mechanical efficiency appear to be improved in more derived morphologies, where mineralized cartilage is more homogeneously distributed.

BON2-5  12:45 pm  Evolution read in tooth and jaw: synchrotron tomography reconstructs a comparative model for dental evolution in Osteichthyes. Welten M.C.M.*, University of Bristol, Bristol, UK; Cerny R., Charles University, Prague, Czech Republic; Donoghue P.C.J., University of Bristol, Bristol, UK
Abstract: Teeth are a key vertebrate innovation, underlying the diversification of jawed vertebrates and their dominance in vertebrate diversity. Moreover, teeth are an important model system in evolutionary and developmental biology, to understand development of organ systems in vertebrates. However, our understanding of the evolution of teeth could not be more confused, with competing hypotheses seeking to explain the evolutionary origins of teeth. Previous studies focused mainly on sharks, which were considered to reflect ancestral conditions. However, sharks are derived and have lost many skeletal elements present in primitive jawed vertebrates and, therefore, are not an effective ancestral model. To better constrain ancestral patterns of tooth evolution, we characterised tooth development in Polypterus senegalus. This non-teleost actinopterygian occupies a unique phylogenetic position at the base of the clade of extant actinopterygians and shows many primitive features. It can be considered as a useful model for phylogenetic comparisons of oral and pharyngeal tooth development, and thus yield insights into the evolution of teeth. We employed Synchrotron Radiation X-ray Tomographic Microscopy (SRXTM) at the Swiss Light Source; as well as molecular biology techniques to characterise tooth initiation and development in Polypterus senegalus, and to compare these to dental development in Danio rerio, a derived, teleost actinopterygian, and to a tetrapod sarcopterygian such as Mus. Our results show tooth initiation and development in Polypterus senegalus, which possesses both pharyngeal and oral dentition, and in Danio rerio, which has pharyngeal dentition only. Moreover, our high resolution, three-dimensional analysis gives insight into spatial relations of developing dentitions, thus contributing complementary information to previous studies; while application of molecular biological techniques elucidates the earliest onset of tooth formation in Polypterus senegalus.

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