Turning maneuvers in sharks: Predicting body curvature from axial morphology

Given the diversity of vertebral morphologies among fishes, it is tempting to propose causal links between axial morphology and body curvature. We propose that shape and size of the vertebrae, intervertebral joints, and the body will more accurately predict differences in body curvature during swimming rather than a single meristic such as total vertebral number alone. We examined the correlation between morphological features and maximum body curvature seen during routine turns in five species of shark: Triakis semifasciata, Heterodontus francisci, Chiloscyllium plagiosum, Chiloscyllium punctatum, and Hemiscyllium ocellatum. We quantified overall body curvature using three different metrics. From a separate group of size‐matched individuals, we measured 16 morphological features from precaudal vertebrae and the body. As predicted, a larger pool of morphological features yielded a more robust prediction of maximal body curvature than vertebral number alone. Stepwise linear regression showed that up to 11 features were significant predictors of the three measures of body curvature, yielding highly significant multiple regressions with r² values of 0.523, 0.537, and 0.584. The second moment of area of the centrum was always the best predictor, followed by either centrum length or transverse height. Ranking as the fifth most important variable in three different models, the body's total length, fineness ratio, and width were the most important non‐vertebral morphologies. Without considering the effects of muscle activity, these correlations suggest a dominant role for the vertebral column in providing the passive mechanical properties of the body that control, in part, body curvature during swimming. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Vertebral numbers in male and female snakes: the roles of natural,sexual and fecundity selection

The relative numbers of trunk (body) and caudal (tail) vertebrae in snakes might be influenced by at least four processes: (1) natural selection for crawling speed, (2) fecundity selection for larger trunk size in females, (3) sexual selection for longer bodies or tails in males and/or (4) developmental constraints (if an increase in the number of body vertebrae requires a decrease in the number of tail vertebrae, or vice versa). These four hypotheses generate different predictions about the relationship between sex differences in the numbers of body vertebrae vs. tail vertebrae. I collated published data to test these predictions, both with raw data and using phylogenetically independent contrasts. Some snake lineages show a negative correlation between the magnitude of sex disparities in trunk vs. caudal vertebrae whereas other lineages show the reverse pattern, or no correlation. Thus, different selective pressures seem to have been important in different lineages. Vertebral numbers in snakes may offer a useful model system in which to explore the conflicts between natural, fecundity and sexual selection.     

A method for estimation of lateral and vertical mobility of platycoelous vertebrae of tetrapods

A new method for the estimation of dorsoventral and lateral mobility of platycoelous vertebrae with V-shaped (radial) articular facets on the zygapophyses is developed. This vertebral pattern is observed in dinosaurs, some other fossil reptiles, and in the cervical and lumbar regions of mammals. Based on theoretical biomechanical analysis of the intervertebral discs and articulations between zygapophyses, the estimation formulas are developed and calibrated, using precise measurements of mobility between cervical vertebrae of domestic sheep. The method is applied to the presacral vertebrae of the horned dinosaur Protoceratops andrewsi. In its cervical, lumbar, and anterior thoracic regions, the differences between the calculated amplitudes of movements and the sought true values are expected to range within ±5°. As compared to the sheep, Protoceratops shows a greater lateral mobility in the presacral region and reduced vertical mobility in the cervical region.     

Built for speed: strain in the cartilaginous vertebral columns of sharks

In most bony fishes vertebral column strain during locomotion is almost exclusively in the intervertebral joints, and when these joints move there is the potential to store and release strain energy. Since cartilaginous fishes have poorly mineralized vertebral centra, we tested whether the vertebral bodies undergo substantial strain and thus may be sites of energy storage during locomotion. We measured axial strains of the intervertebral joints and vertebrae in vivo and ex vivo to characterize the dynamic behavior of the vertebral column. We used sonomicrometry to directly measure in vivo and in situ strains of intervertebral joints and vertebrae of Squalus acanthias swimming in a flume. For ex vivo measurements, we used a materials testing system to dynamically bend segments of vertebral column at frequencies ranging from 0.25 to 1.00 Hz and a range of physiologically relevant curvatures, which were determined using a kinematic analysis. The vertebral centra of S. acanthias undergo strain during in vivo volitional movements as well as in situ passive movements. Moreover, when isolated segments of vertebral column were tested during mechanical bending, we measured the same magnitudes of strain. These data support our hypothesis that vertebral column strain in lateral bending is not limited to the intervertebral joints. In histological sections, we found that the vertebral column of S. acanthias has an intracentral canal that is open and covered with a velum layer. An open intracentral canal may indicate that the centra are acting as tunics around some sections of a hydrostat, effectively stiffening the vertebral column. These data suggest that the entire vertebral column of sharks, both joints and centra, is mechanically engaged as a dynamic spring during locomotion.     

Measured and modelled static and dynamic axial trunk torsion during twisting in males and females

Study of the mechanics of trunk twisting is special interest given epidemiological evidence linking occupational twisting to increased incidence of low back pain. An anatomically detailed, three-dimensional model of the trunk (rib cage, pelvis, five lumbar vertebrae and 50 muscles), was used to predict maximum axial trunk torque. Predicted axial torques were compared with measured torques. Thirty-one (10 male and 21 female) subjects performed maximum effort isometric twisting exertions, at 0° of twist and ±30° of twist together with dynamic exertions, at 30° s⁻¹ and 60° s⁻¹. Females were able to generate approximately two-thirds of the torque of males (males, 97 Nm; females 60 Nm, isometric at 0°). When the trunk was prerotated to 30°, subjects were able to generate greater torque when the effort was toward the 0° position (approximately 105 Nm by males and 68 Nm by females). Experimental data indicated that velocity of rotation and amount of twist are important modulators of axial torque. Changes in muscle length were demonstrated to be minimal from model output as most muscle length changes during a twist from 0° to 30°, measured between the pelvis and the shoulder harness, were less than 1%, although some portions of the abdominal obliques underwent a length excursion of 5%. The small changes in the individual muscle force components that contribute to twist, i.e. the muscle unit vector about the axial twist axis and its moment arm that change as a function of twisted position, do not entirely account for the measured differences in torque, suggesting that additional mechanisms influence axial torque generation.     

GEOGRAPHIC VARIATION AND PHENOTYPIC PLASTICITY OF NUMBER OF TRUNK VERTEBRAE IN SLENDER SALAMANDERS,BATRACHOSEPS (CAUDATA: PLETHODONTIDAE)

To understand the evolutionary significance of geographic variation, one must identify the factors that generate phenotypic differences among populations. I examined the causes of geographic variation in and evolutionary history of number of trunk vertebrae in slender salamanders, Batrachoseps (Caudata: Plethodontidae). Number of trunk vertebrae varies at many taxonomic levels within Batrachoseps. Parallel clines in number occur along an environmental gradient in three lineages in the Coast Ranges of California. These parallel clines may signal either adaptation or a shared phenotypically plastic response to the environmental gradient. By raising eggs from 10 populations representing four species of Batrachoseps, I demonstrated that number of trunk vertebrae can be altered by the developmental temperature; however, the degree of plasticity is insufficient to account for geographic variation. Thus, the geographic variation results largely from genetic variation. Number of trunk vertebrae covaries with body size and shape in diverse vertebrate taxa, including Batrachoseps. I hypothesize that selection for different degrees of elongation, possibly related to fossoriality, has led to the extensive evolution of number of trunk vertebrae in Batrachoseps. Analysis of intrapopulational variation revealed sexual dimorphism in both body shape and number of trunk vertebrae, but no correlation between these variables in either sex. Females are more elongate than males, a pattern that has been attributed to fecundity selection in other taxa. Patterns of covariation among different classes of vertebrae suggest that some intrapopulational variation in number results from changes in vertebral identity rather than changes in segmentation.     

Vertebrae of the sea snake <Emphasis Type="Italic">Palaeophis nessovi</Emphasis> Averianov (Acrochordoidea,Palaeophiidae) from the Eocene of western Kazakhstan and phylogenetic analysis of the superfamily Acrochordoidea

The vertebrae of sea snakes from five Eocene localities in western Kazakhstan are assigned to the species Palaeophis nessovi Averianov, 1997. The anterior trunk vertebrae have subcentral ridges, large posterior hypapophysis, and large synapophyses; the middle trunk vertebrae are slightly laterally compressed and their synapophyses are positioned highly; the posterior trunk vertebrae are strongly laterally compressed and have a well-developed haemal keel. Cladistic analysis has shown that the genus Palaeophis is not monophyletic; the genus Archaeophis is a more advanced palaeophiid than was previously thought.     

Husbandry of the little file snake,Acrochordus granulatus

Aquatic snakes of the family Acrochordidae are unusual in terms of appearance, biology, and natural history. In spite of many attractive and fascinating features, there are few zoological exhibits of acrochordid snakes, and as a result many aspects of their husbandry are poorly understood. The present paper summarizes aspects of acrochordid biology related to health and welfare of captive snakes, with emphasis on the little file snake, Acrochordus granulatus. Several key points emerge having crucial relevance to successful husbandry. (1) File snakes are sensitive to low temperatures and to rapid thermal change. Captive snakes do well when maintained at water temperatures of 27–30°C and will not thrive if water temperatures are below 25°C. (2) File snakes can be kept in either fresh water or seawater. Snakes in sea or brackish water dehydrate, however, and must be allowed to drink fresh water periodically. If snakes from marine populations are maintained in saline water, 60–70% seawater is recommended. In all cases, water should be filtered or changed periodically to maintain quality. (3) File snakes feed almost exclusively on fishes which are usually captured in body coils. Snakes are more inclined to feed well if live prey are offered in shallow water where they are more easily captured. (4) File snakes are nocturnal and prefer quiescent seclusion within darkened refugia during daylight hours. Providing snakes with refugia such as sections of PVC pipe (which simulate burrows) helps reduce stress and improves the chances of snakes feeding regularly. (5) Snakes tend to burrow, and they locomote by crawling as well as by swimming. Use of sharp or rough materials in aquaria should be avoided because of possible skin abrasion which increases permeability and provides sites for bacterial infection. © 1996 Wiley-Liss, Inc.     

Contribution of the vertebral artery to cerebral circulation in the rat snake Elaphe obsoleta

Blood supplying the brain in vertebrates is carried primarily by the carotid vasculature. In most mammals, cerebral blood flow is supplemented by the vertebral arteries, which anastomose with the carotids at the base of the brain. In other tetrapods, cerebral blood is generally believed to be supplied exclusively by the carotid vasculature, and the vertebral arteries are usually described as disappearing into the dorsal musculature between the heart and head. There have been several reports of a vertebral artery connection with the cephalic vasculature in snakes. We measured regional blood flows using fluorescently labeled microspheres and demonstrated that the vertebral artery contributes a small but significant fraction of cerebral blood flow (∼13% of total) in the rat snake Elaphe obsoleta. Vascular casts of the anterior vessels revealed that the vertebral artery connection is indirect, through multiple anastomoses with the inferior spinal artery, which connects with the carotid vasculature near the base of the skull. Using digital subtraction angiography, fluoroscopy, and direct observations of flow in isolated vessels, we confirmed that blood in the inferior spinal artery flows craniad from a point anterior to the vertebral artery connections. Such collateral blood supply could potentially contribute to the maintenance of cerebral circulation during circumstances when craniad blood flow is compromised, e.g., during the gravitational stress of climbing. J. Morphol. 238:39–51, 1998. © 1998 Wiley-Liss, Inc.     

Pyrazole amino acids: hydrogen bonding directed conformations of 3‐amino‐1H‐pyrazole‐5‐carboxylic acid residue

A series of model compounds containing 3‐amino‐1H‐pyrazole‐5‐carboxylic acid residue with N‐terminal amide/urethane and C‐terminal amide/hydrazide/ester groups were investigated by using NMR, Fourier transform infrared, and single‐crystal X‐ray diffraction methods, additionally supported by theoretical calculations. The studies demonstrate that the most preferred is the extended conformation with torsion angles ? and ψ close to ±180°. The studied 1H‐pyrazole with N‐terminal amide/urethane and C‐terminal amide/hydrazide groups solely adopts this energetically favored conformation confirming rigidity of that structural motif. However, when the C‐terminal ester group is present, the second conformation with torsion angles ? and ψ close to ±180° and 0°, respectively, is accessible. The conformational equilibrium is observed in NMR and Fourier transform infrared studies in solution in polar environment as well as in the crystal structures of other related compounds. The observed conformational preferences are clearly related to the presence of intramolecular interactions formed within the studied residue. Copyright © 2017 European Peptide Society and John Wiley & Sons, Ltd.     

Vertebral number in adders, Vipera berus: direct and indirect effects on growth

Given the importance of body size, and thereby growth rate, for many reproductive parameters in snakes, morphological traits conferring an advantage in terms of growth may be important targets of selection. Studies have demonstrated effects of vertebral number of growth rate in garter snakes. In this study effects of total number of body vertebrae and of number of abnormal body vertebrae (obtained by counting number of ventral scutes and number of abnormal scutes) on growth rate in free-ranging male and female adders, Vipera berus (L.), are examined by calculating directional performance gradients (estimating linear effects) and stabilizing performance gradients (estimating curvilinear effects). After controlling for body size (SVL) female adders demonstrated a significant positive directional gradient for vertebral number, and a significant interaction between body size and vertebral number, showing that females with more vertebrae have higher size-specific growth rates, and that this effect is strongest among small, fast growing individuals. Females also showed a weak stabilizing effect of abnormal vertebrae. Males, on the other hand, showed a positive directional gradient for number of abnormal vertebrae, whereas no effect of vertebral number was observed. Indirect effects of the same variables were evaluated by use of path analysis. Generally, indirect effects were weak and did not substantially increase the amount of explained variance in growth rate. Field data showed that the correlation between vertebral number and growth rate in females was stronger in years with higher overall growth rate. To evaluate whether vertebral number and food availability show an interactive effect I used captive born juvenile adders in an experiment with two different food levels. The experiment confirmed the field data. No relationship between vertebral number and growth was observed in the low food level group, whereas in the high food level group a significant positive correlation was demonstrated. Finally, the heritability of vertebral number was examined using a mother-offspring regression and a full-sib analysis. The estimated heritabilities were 0.30 and 0.39, respectively. From these results it is concluded that both vertebral number and abnormal vertebral number may significantly affect growth in adders, but that this effect may differ between sexes and among years.     

A South American snake lineage from the Eocene Greenhouse of North America and a reappraisal of the fossil record of “anilioid” snakes

“Anilioidea” is a likely paraphyletic assemblage of pipe snakes that includes extant Aniliidae from equatorial South America, Uropeltoidea from South and Southeast Asia, and a fossil record that consists primarily of isolated precloacal vertebrae ranging from the earliest Late Cretaceous and includes geographic distributions in North America, South America, Europe, and Africa. Articulated precloacal vertebrae from the middle Eocene Bridger Formation of Wyoming, attributed to Borealilysia nov. gen., represent an unambiguous North American aniliid record and prompts a reconsideration of described pipe snakes and their resultant biogeographic histories. On the basis of vertebral apomorphies, the vast majority of reported fossils cannot be assigned to “Anilioidea”. Instead, most records represent stem taxa and macrostomatans erroneously assigned to anilioids on the basis of generalized features associated with fossoriality. A revised fossil record demonstrates that the only extralimital distributions of fossil “anilioids” consist of the North American aniliid record, and there is no unambiguous fossil record of Old World taxa. The occurrence of aniliids in the mid-high latitudes of the late early Eocene of North America is consistent with histories of northward shifts in equatorial ecosystems during the early Paleogene Greenhouse.     

Reconstruction of the neck of Azhdarcho lancicollis and lifestyle of azhdarchids (Pterosauria, Azhdarchidae)

A computer reconstruction of isolated cervical vertebrae of Azhdarcho lancicollis from the Turonian of Uzbekistan allows three-dimensional model of the cervical region of the vertebral column of this animal. The relative length of cervical vertebrae (I + II < III < IV < V > VI > VII > VIII > IX) is the same as in pterodactyloids with short cervical vertebrae. An increase in neck length is provided mostly by the middle cervical vertebrae (IV–VI). In a neutral posture, the neck of azhdarchids was not straight, as often reconstructed, but S-shaped, with the maximum angles between the V–VI (20°), VI–VII (20°), and VIII–IX (17°) vertebrae. The feeding strategy of azhdarchids was probably similar to that of pelicans. In a search for prey, azhdarchids were soaring above the water surface of large inland or nearshore marine water bodies. Their prey (predominantly fish) was captured by the widely open mouth and fell into the throat sac, the presence of which is suggested by the spiral jaw joint. Prey was swallowed during the abrupt neck flexion in the posterior segment, which brought the head in an almost horizontal position. A storklike wading ecology for azhdarchids is less probable, because these clumsy on land animals were vulnerable to terrestrial predators.     

Regional variation in morphology of vertebral centra and intervertebral joints in striped bass,Morone saxatilis

The vertebral column of fishes has traditionally been divided into just two distinct regions, abdominal and caudal. Recently, however, developmental, morphological, and mechanical investigations have brought this traditional regionalization scheme into question. Alternative regionalization schema advocate the division of the abdominal vertebrae into cervical, abdominal, and in some cases, transitional regions. Here, we investigate regional variation at the level of the vertebrae and intervertebral joint (IVJ) tissues in the striped bass, Morone saxatilis. We use gross dissection, histology, and polarized light imaging to quantify vertebral height, width, length, IVJ length, IVJ tissue volume and cross‐sectional area, and vertical septum fiber populations, and angles of insertion. Our results reveal regional differences between the first four (most rostral) abdominal vertebrae and IVJs and the next six abdominal vertebrae and IVJs, supporting the recognition of a distinct cervical region. We found significant variation in vertebral length, width, and height from cranial to caudal. In addition, we see a significant decline in the volume of notochordal cells and the cross‐sectional area of the fibrous sheath from cranial to caudal. Further, polarized light imaging revealed four distinct fiber populations within the vertical septum in the cervical and abdominal regions in contrast with just one fiber population found in the caudal region. Measurement of the insertion angles of these fiber populations revealed significant differences between the cervical and abdominal regions. Differences in vertebral, IVJ, and vertical septum morphology all predict greater range of motion and decreased stiffness in the caudal region of the fish compared with the cervical and abdominal regions. J. Morphol., 2012. © 2011 Wiley Periodicals, Inc.     

Unique occipital articulation with the first vertebra found in pristigasterids, chirocentrids, and clupeids (Teleostei: Clupeiformes: Clupeoidei)

This study recognized a W-shaped occipital articulation associated with the first vertebra in pristigasterids, chirocentrids, and clupeids as a unique character among teleosts, based on an evaluation of 43 species within 40 genera of these three families of the Clupeoidei. This occipital articulation is accompanied by an anterior extension of the neural arch bases, which are autogenous with the first vertebral centrum. In chirocentrids and many of the clupeid species examined, the anterior extension occurs on the second vertebra, and similar occipital articulation is found between the first and second vertebrae. The W-shaped occipital articulation is not found in any other teleosts, including Denticeps (suborder Denticipitoidei), which is thought to be a sister group to the suborder Clupeoidei. The W-shaped occipital articulation is absent in the other family of the Clupeoidei, Engraulidae, based on an evaluation of 11 species in 10 genera. Instead, the convex anterior surface of the first vertebral centrum forms a condyle that articulates with the basioccipital, and the neural arches fuse with the centrum behind this condyle. Therefore, it is unclear whether the anterior extension of the first vertebral neural arch bases, which causes the W-shaped occipital articulation, occurs in engraulids. Based on an evaluation of the osteological development of Konosirus punctatus and Engraulis japonicus, the cartilaginous neural arch bases of the first and second vertebrae extend anteriorly at an early developmental stage in the former, whereas no anterior extension of the first vertebral neural arch bases occurs at any developmental stage in the latter. Therefore, the anterior extension of the neural arch bases, which causes the W-shaped occipital articulation, seems to be a unique character of pristigasterids, chirocentrids, and clupeids among teleosts. Within the recent phylogenetic context, this character may be a synapomorphy of these three families.     

Dynamic changes in body form during swimming in the water snake Nerodia sipedon

Video records of swimming water snakes show that during moderate to rapid swimming, the rear half to two-thirds of the trunk is compressed laterally, approaching the body form of some sea snakes. Body form of swimming snakes differed significantly from their shape when resting on a flat surface or when anesthetized and suspended in water. The extent of lateral flattening is positively correlated with swimming speed, a relationship generally supported by tests of trunk models in a flow tank. In Nerodia, the ability to temporarily flatten the trunk depends on kinetic costovertebral joints, a large compressible body cavity, and the absence of ventral skeletal support - features found in most snakes. Histological studies and manipulations of partially dissected preserved specimens showed that the resting angle of the ribs is maintained by localized elastic hypertrophy of the costovertebral capsular ligament. Trunk form during swimming in Nerodia is proposed to arise from anteromedial movement of the distal rib powered by deep muscles acting in concert with those proposed to generate undulation of the vertebral column.     

Suboccipital muscle of sharpnose sevengill shark Heptranchias perlo and its possible role in prey dissection

Skull and head muscles of Heptranchias perlo were studied. Its distinctive features include the suboccipital muscles, described for the first time, the absence of the palatoquadrate symphysis, a longitudinally extended mouth, and teeth unsuited for dissecting prey in typical method of modern sharks, which is cutting motions powered by head shaking from side to side. The palatoquadrate cartilages of H. perlo and closely related Hexanchidae articulate with the neurocranium via orbital and postorbital articulations, which together allow for lateral expansion of the jaws, but restrict retraction and protraction. We interpret these features as an adaptation to a different method of prey dissection, that is, ripping in a backward pull. It employs the specific postorbital articulation together with the suboccipital muscles as force-transmitting devices, and is powered by swimming muscles which produce a rearward thrust of the tail. During this type of dissection, the anterior part of the vertebral column should experience a tensile stress which explains the replacement of rigid vertebral bodies by a collagenous sheath around the notochord in H. perlo. The backward-ripping dissection could have been common among ancient Elasmobranchii based on the similarly developed postorbital articulation, a longitudinally extended mouth, and the absence of the palatoquadrate symphysis. A biomechanical comparison with the extinct Pucapampella indicates that ancient elasmobranchs could be also specialized in the backward-ripping prey dissection, but their mechanism was different from that inferred for H. perlo. We suggest that in the early evolution of sharks this mechanism was replaced by head-shaking dissection and then later was restored in H. perlo on a new morphological basis. A new position of the postorbital articulation below the vertebral axis is fraught with the braincase elevation when backward ripping the prey, and as a counter-mean, requires formation of suboccipital portions of the axial musculature unknown in other sharks. Homology and origin of these portions is considered.