Locomotion in the Biology of Large Aquatic Vertebrates

As aquatic vertebrates increase in size, hydrofoils, which use lift to generate thrust, are increasingly used as propulsors. One factor affecting the magnitude of the lift force is the area of the propulsor. Resistance to cruising and sprints is mainly due to drag, but inertia is important during maneuvers when animals accelerate or turn. The inertia of the body and entrained water, which is proportional to body volume, resists acceleration. Because a thrust that is proportional to surface area is used to maneuver a resistance that is proportional to volume, acceleration performance and maneuverability are expected to decline with increasing size, This trend is ameliorated to some extent by the high swimming speeds attainable by warm‐bodied vertebrates and the reduced resistance to acceleration characteristic of the skeletons of dolphins and ichthyosaurs. Maneuvers are essential for capture of elusive prey and avoidance of predators. As they increase in size, aquatic vertebrates use various means to ensure that their prey are less maneuverable than they. These include consumption of increasingly smaller prey relative to predator body size (culminating in filter feeding by the largest aquatic vertebrates); behaviors to concentrate, disturb, and disorient prey; and ambushing or suction feeding that avoid whole‐body acceleration. Advantages of warm muscles are seen in the ability of endotherms to take more maneuverable prey than can ectotherms of the same size. Young stages of large aquatic vertebrates could be especially vulnerable to predators; viviparity or spawning in productive patches provides for rapid growth through vulnerable stages.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/141968/1/tafs0629.pd

Microstructural features of the femur in early ophiacodontids: A reappraisal of ancestral habitat use and lifestyle of amniotes

AbstractOphiacodontids have long been considered the basalmost synapsids, and to have retained a fairly aquatic, piscivorous lifestyle typical of stem-amniotes. A restudy of their bone histology and microanatomy shows that Clepsydrops collettii, a Late Carboniferous ophiacodontid, has a thin, compact cortex and lacks a medullary spongiosa, two features that suggest a truly terrestrial lifestyle. The Early Permian Ophiacodon uniformis has a thicker cortex with a few resorption cavities and bone trabeculae surrounding the free medullary cavity. An inference model yields a terrestrial lifestyle for both taxa, though O. uniformis may have been slightly more aquatic (possibly amphibious) than C. collettii. However, an optimization of inferred lifestyle of other early stegocephalians (based on bone microanatomy) suggests that the first amniotes were terrestrial. The potentially amphibious lifestyle of O. uniformis, though not supported by our inference model, would thus be secondary. Histological features of femoral cortices in these two taxa closely resemble those previously described in extant species of large varanids and teids. This similarity, along with other comparative elements, is discussed in reference to the possible growth patterns and life history traits of Clepsydrops and O. uniformis

Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology

Bone microanalyses of extant vertebrates provide a necessary framework from which to form hypotheses regarding the growth and skeletochronology of extinct taxa. Here, we describe the bone microstructure and quantify the histovariability of appendicular elements and osteoderms from three juvenile American alligators (Alligator mississippiensis) to assess growth mark and tissue organization within and amongst individuals, with the intention of validating paleohistological interpretations. Results confirm previous observations that lamellar and parallel fibered tissue organization are typical of crocodylians, and also that crocodylians are capable of forming woven tissue for brief periods. Tissue organization and growth mark count varies across individual skeletal elements and reveal that the femur, tibia, and humerus had the highest annual apposition rates in each individual. Cyclical growth mark count also varies intraskeletally, but data suggest these inconsistencies are due to differing medullary cavity expansion rates. There was no appreciable difference in either diaphyseal circumference or cyclical growth mark circumferences between left and right element pairs from an individual if diaphyses were sampled from roughly the same location. The considerable intraskeletal data obtained here provide validation for long-held paleohistology assumptions, but because medullary expansion, cyclical growth mark formation, and variable intraskeletal growth rates are skeletal features found in tetrapod taxa living or extinct, the validations presented herein should be considered during any tetrapod bone microanalysis

A mineralogical study in contrasts: highly mineralized whale rostrum and human enamel

The outermost enamel of the human tooth and the rostrum of the whale Mesoplodon densirostris are two highly mineralized tissues that contain over 95wt.% mineral, i.e., bioapatite. However, the same mineral type (carbonated hydroxylapatite) does not yield the same material properties, as revealed by Raman spectroscopy, scanning electron microscopy, electron microprobe analysis, and synchrotron X-ray diffraction analysis. Overall, the outermost enamel of a tooth has more homogeneous physical and chemical features than the rostrum. Chemical comparison of rostrum and enamel shows bioapatite in the rostrum to be enriched in Na, Mg, CO3, and S, whereas the outermost enamel shows only a slightly enriched Cl concentration. Morphologically, mineral rods (at tens of μm scale), crystallites and prisms (at μm and sub-μm scale), and platelets (at tens of nm scale) all demonstrate less organized texture in the rostrum than in enamel. Such contrasts between two mineralized tissues suggest distinct pathways of biomineralization, e.g., the nature of the equilibrium between mineral and body fluid. This study illustrates the remarkable flexibility of the apatite mineral structure to match its chemical and physical properties to specific biological needs within the same animal or between species.The work was partially funded by NIH grant 1R21AR055184-01A2 and SRF for ROCS, SEM

Rethinking the nature of fibrolamellar bone : An integrative biological revision of sauropod plexiform bone formation

We present novel findings on sauropod bone histology that cast doubt on general palaeohistological concepts concerning the true nature of woven bone in primary cortical bone and its role in the rapid growth and giant body sizes of sauropod dinosaurs. By preparing and investigating longitudinal thin sections of sauropod long bones, of which transverse thin sections were published previously, we found that the amount of woven bone in the primary complex has been largely overestimated. Using comparative cellular and light-extinction characteristics in the two section planes, we revealed that the majority of the bony lamina consists of longitudinally organized primary bone, whereas woven bone is usually represented only by a layer a few cells thin in the laminae. Previous arguments on sauropod biology, which have been based on the overestimated amount, misinterpreted formation process and misjudged role of woven bone in the plexiform bone formation of sauropod dinosaurs, are thereby rejected. To explain the observed pattern in fossil bones, we review the most recent advances in bone biology concerning bone formation processes at the cellular and tissue levels. Differentiation between static and dynamic osteogenesis (SO and DO) and the revealed characteristics of SO- versus DO-derived bone tissues shed light on several questions raised by our palaeohistological results and permit identification of these bone tissues in fossils with high confidence. By presenting the methods generally used for investigating fossil bones, we show that the major cause of overestimation of the amount of woven bone in previous palaeohistological studies is the almost exclusive usage of transverse sections. In these sections, cells and crystallites of the longitudinally organized primary bone are cut transversely, thus cells appear rounded and crystallites remain dark under crossed plane polarizers, thereby giving the false impression of woven bone. In order to avoid further confusion in palaeohistological studies, we introduce new osteohistological terms as well as revise widely used but incorrect terminology. To infer the role of woven bone in the bone formation of fast-growing tetrapods, we review some aspects of the interrelationships between the vascularity of bone tissues, basal metabolic rate, body size and growth rate. By putting our findings into the context of osteogenesis, we provide a new model for the diametrical limb bone growth of sauropods and present new implications for the evolution of fast growth in vertebrates. Since biomechanical studies of bone tissues suggest that predominant collagen fibre orientation (CFO) is controlled by endogenous, functional and perhaps phylogenetic factors, the relationship between CFO and bone growth rate as defined by Amprino's rule, which has been the basis for the biological interpretation of several osteohistological features, must be revised. Our findings draw attention to the urgent need for revising widely accepted basic concepts of palaeohistological studies, and for a more integrative approach to bone formation, biomechanics and bone microstructural features of extant and extinct vertebrates to infer life history traits of long extinct, iconic animals like dinosaurs. © 2013 Cambridge Philosophical Society