Ontogenetic influence on neural spine bifurcation in diplodocoidea (dinosauria: Sauropoda): A critical phylogenetic character

Within Diplodocoidea (Dinosauria: Sauropoda), phylogenetic position of the three subclades Rebbachisauridae, Dicraeosauridae, and Diplodocidae is strongly influenced by a relatively small number of characters. Neural spine bifurcation, especially within the cervical vertebrae, is considered to be a derived character, with taxa that lack this feature regarded as relatively basal. Our analysis of dorsal and cervical vertebrae from small‐sized diplodocoids (representing at least 18 individuals) reveals that neural spine bifurcation is less well developed or absent in smaller specimens. New preparation of the roughly 200‐cm long diplodocid juvenile Sauriermuseum Aathal 0009 reveals simple nonbifurcated cervical neural spines, strongly reminiscent of more basal sauropods such as Omeisaurus. An identical pattern of ontogenetically linked bifurcation has also been observed in several specimens of the basal macronarian Camarasaurus, suggesting that this is characteristic of several clades of Sauropoda. We suggest that neural spine bifurcation performs a biomechanical function related to horizontal positioning of the neck that may become significant only at the onset of a larger body size, hence, its apparent absence or weaker development in smaller specimens. These results have significant implications for the taxonomy and phylogenetic position of taxa described from specimens of small body size. On the basis of shallow bifurcation of its cervical and dorsal neural spines, the small diplodocid Suuwassea is more parsimoniously interpreted as an immature specimen of an already recognized diplodocid taxon. Our findings emphasize the view that nonmature dinosaurs often exhibit morphologies more similar to their ancestral state and may therefore occupy a more basal position in phylogenetic analyses than would mature specimens of the same species. In light of this, we stress the need for phylogenetic reanalysis of sauropod clades where vital characters may be ontogenetically variable, particularly when data is derived from small individuals. J. Morphol., 2012. © 2012 Wiley Periodicals, Inc.     

Biomechanical Reconstructions and Selective Advantages of Neck Poses and Feeding Strategies of Sauropods with the Example of Mamenchisaurus youngi

A very long neck is a characteristic feature of most sauropod dinosaurs. In the genus Mamenchisaurus, neck length is extreme, greater than 40 percent of total body length. However, the posture, utilization, and selective advantage of very long necks in sauropods are still controversial. An excellently preserved skeleton of Mamenchisaurus youngi, including a complete neck, provides an opportunity for a comprehensive biomechanical analysis of neck posture and mobility. The biomechanical evidence indicates that Mamenchisaurus youngi had a nearly straight, near horizontal neck posture and browsed at low or medium heights. The results differ from the findings for some other sauropod species, like Euhelopus, Diplodocus, and Giraffatitan (Brachiosaurus) that had been analyzed in previous studies with similar methods. The selective advantage of extreme neck length in sauropods is likely advantageous for different feeding strategies.     

Torsion and Bending in the Neck and Tail of Sauropod Dinosaurs and the Function of Cervical Ribs: Insights from Functional Morphology and Biomechanics

The long necks of sauropods have been subject to many studies regarding their posture and flexibility. Length of the neck varies among groups. Here, we investigate neck posture and morphology in several clades from a mechanical viewpoint. Emphasis is put on comparing sauropod necks and tails with structures in living archosaurs and mammals. Differences in the use made of necks and tails lead to clear-cut differences in the mechanical loads occurring in the same models. Ways of sustaining loads are identified by theoretical considerations. If the observed skeletal structures are suited to resist the estimated loading in a particular posture, this concordance is taken as an argument that this posture or movement was of importance during the life of the individual. Apart from the often-discussed bending in side view, we analyze the often overlooked torsion. Because torsional stresses in a homogenous element concentrate near the periphery, a cylindrical cross section gives greatest strength, and the direction of forces is oblique. In a vertebrate neck, during e.g. shaking the head and twisting the neck, oblique muscles, like the mm. scaleni, if activated unilaterally initiate movement, counterbalance the torsional moments and keep the joints between neck vertebrae in equilibrium. If activated bilaterally, these muscles keep the neck balanced in an energy-saving upright posture. The tendons of the mm. scaleni may have ossified as cervical ribs The long cervical ribs in brachiosaurids and mamenchisaurids seem to have limited flexibility, whereas the shorter cervical ribs in Diplodocidae allowed free movement. The tails of sauropods do not show pronounced adaptation to torsion, and seem to have been carried more or less in a horizontal, extended posture. In this respect, sauropod tails resemble the necks of herbivorous cursorial mammals. These analyses provide an improved understanding of neck use that will be extended to other sauropods in subsequent studies.     

The anatomy of the bifurcated neural spine and its occurence within Tetrapoda

Vertebral neural spine bifurcation has been historically treated as largely restrictive to sauropodomorph dinosaurs; wherein it is inferred to be an adaptation in response to the increasing weight from the horizontally extended cervical column. Because no extant terrestrial vertebrates have massive, horizontally extended necks, extant forms with large cranial masses were examined for the presence of neural spine bifurcation. Here, I report for the first time on the soft tissue surrounding neural spine bifurcation in a terrestrial quadruped through the dissection of three Ankole‐Watusi cattle. With horns weighing up to a combined 90 kg, the Ankole‐Watusi is unlike any other breed of cattle in terms of cranial weight and presence of neural spine bifurcation. Using the Ankole‐Watusi as a model, it appears that neural spine bifurcation plays a critical role in supporting a large mobile weight adjacent to the girdles. In addition to neural spine bifurcation being recognized within nonavian dinosaurs, this vertebral feature is also documented within many members of temnospondyls, captorhinids, seymouriamorphs, diadectomorphs, Aves, marsupials, artiodactyls, perissodactyls, and Primates, amongst others. This phylogenetic distribution indicates that spine bifurcation is more common than previously thought, and that this vertebral adaptation has contributed throughout the evolutionary history of tetrapods. Neural spine bifurcation should now be recognized as an anatomical component adapted by some vertebrates to deal with massive, horizontal, mobile weights adjacent the girdles. J. Morphol. 275:1053–1065, 2014. © 2014 Wiley Periodicals, Inc.     

The Effect of Intervertebral Cartilage on Neutral Posture and Range of Motion in the Necks of Sauropod Dinosaurs

The necks of sauropod dinosaurs were a key factor in their evolution. The habitual posture and range of motion of these necks has been controversial, and computer-aided studies have argued for an obligatory sub-horizontal pose. However, such studies are compromised by their failure to take into account the important role of intervertebral cartilage. This cartilage takes very different forms in different animals. Mammals and crocodilians have intervertebral discs, while birds have synovial joints in their necks. The form and thickness of cartilage varies significantly even among closely related taxa. We cannot yet tell whether the neck joints of sauropods more closely resembled those of birds or mammals. Inspection of CT scans showed cartilage:bone ratios of 4.5% for Sauroposeidon and about 20% and 15% for two juvenile Apatosaurus individuals. In extant animals, this ratio varied from 2.59% for the rhea to 24% for a juvenile giraffe. It is not yet possible to disentangle ontogenetic and taxonomic signals, but mammal cartilage is generally three times as thick as that of birds. Our most detailed work, on a turkey, yielded a cartilage:bone ratio of 4.56%. Articular cartilage also added 11% to the length of the turkey''s zygapophyseal facets. Simple image manipulation suggests that incorporating 4.56% of neck cartilage into an intervertebral joint of a turkey raises neutral posture by 15°. If this were also true of sauropods, the true neutral pose of the neck would be much higher than has been depicted. An additional 11% of zygapophyseal facet length translates to 11% more range of motion at each joint. More precise quantitative results must await detailed modelling. In summary, including cartilage in our models of sauropod necks shows that they were longer, more elevated and more flexible than previously recognised.     

Functional morphology of the primate head and neck

The vertebral column plays a key role in maintaining posture, locomotion, and transmitting loads between body components. Cervical vertebrae act as a bridge between the torso and head and play a crucial role in the maintenance of head position and the visual field. Despite its importance in positional behaviors, the functional morphology of the cervical region remains poorly understood, particularly in comparison to the thoracic and lumbar sections of the spinal column. This study tests whether morphological variation in the primate cervical vertebrae correlates with differences in postural behavior. Phylogenetic generalized least-squares analyses were performed on a taxonomically broad sample of 26 extant primate taxa to test the link between vertebral morphology and posture. Kinematic data on primate head and neck postures were used instead of behavioral categories in an effort to provide a more direct analysis of our functional hypothesis. Results provide evidence for a function-form link between cervical vertebral shape and postural behaviors. Specifically, taxa with more pronograde heads and necks and less kyphotic orbits exhibit cervical vertebrae with longer spinous processes, indicating increased mechanical advantage for deep nuchal musculature, and craniocaudally longer vertebral bodies and more coronally oriented zygapophyseal articular facets, suggesting an emphasis on curve formation and maintenance within the cervical lordosis, coupled with a greater resistance to translation and ventral displacement. These results not only document support for functional relationships in cervical vertebrae features across a wide range of primate taxa, but highlight the utility of quantitative behavioral data in functional investigations. Am J Phys Anthropol 156:531–542, 2015. © 2015 Wiley Periodicals, Inc.     

The Articulation of Sauropod Necks: Methodology and Mythology

Sauropods are often imagined to have held their heads high atop necks that ascended in a sweeping curve that was formed either intrinsically because of the shape of their vertebrae, or behaviorally by lifting the head, or both. Their necks are also popularly depicted in life with poses suggesting avian flexibility. The grounds for such interpretations are examined in terms of vertebral osteology, inferences about missing soft tissues, intervertebral flexibility, and behavior. Osteologically, the pronounced opisthocoely and conformal central and zygapophyseal articular surfaces strongly constrain the reconstruction of the cervical vertebral column. The sauropod cervico-dorsal vertebral column is essentially straight, in contrast to the curvature exhibited in those extant vertebrates that naturally hold their heads above rising necks. Regarding flexibility, extant vertebrates with homologous articular geometries preserve a degree of zygapophyseal overlap at the limits of deflection, a constraint that is further restricted by soft tissues. Sauropod necks, if similarly constrained, were capable of sweeping out large feeding surfaces, yet much less capable of retracting the head to explore the enclosed volume in an avian manner. Behaviorally, modern vertebrates generally assume characteristic neck postures which are close to the intrinsic curvature of the undeflected neck. With the exception of some vertebrates that can retract their heads to balance above their shoulders at rest (e.g., felids, lagomorphs, and some ratites), the undeflected neck generally predicts the default head height at rest and during locomotion.     

Understanding selection for long necks in different taxa

There has been recent discussion about the evolutionary pressures underlying the long necks of extant giraffes and extinct sauropod dinosaurs. Here we summarise these debates and place them in a wider taxonomic context. We consider the evolution of long necks across a wide range of (both living and extinct) taxa and ask whether there has been a common selective factor or whether each case has a separate explanation. We conclude that in most cases long necks can be explained in terms of foraging requirements, and that alternative explanations in terms of sexual selection, thermoregulation and predation pressure are not as well supported. Specifically, in giraffe, tortoises, and perhaps sauropods there is likely to have been selection for high browsing. It the last case there may also have been selection for reaching otherwise inaccessible aquatic plants or for increasing the energetic efficiency of low browsing. For camels, wading birds and ratites, original selection was likely for increased leg length, with correlated selection for a longer neck to allow feeding and drinking at or near substrate level. For fish‐eating long‐necked birds and plesiosaurs a small head at the end of a long neck allows fast acceleration of the mouth to allow capture of elusive prey. A swan's long neck allows access to benthic vegetation, for vultures the long neck allows reaching deep into a carcass. Geese may be an unusual case where anti‐predator vigilance is important, but so may be energetically efficient low browsing. The one group for which we feel unable to draw firm conclusions are the pterosaurs, this is in keeping with the current uncertainty about the biology of this group. Despite foraging emerging as a dominant theme in selection for long necks, for almost every taxonomic group we have identified useful empirical work that would increase understanding of the selective costs and benefits of a long neck.     

Spine neck geometry determines spino-dendritic cross-talk in the presence of mobile endogenous calcium binding proteins

Dendritic spines are thought to compartmentalize second messengers like Ca²⁺. The notion of isolated spine signaling, however, was challenged by the recent finding that under certain conditions mobile endogenous Ca²⁺-binding proteins may break the spine limit and lead to activation of Ca²⁺-dependent dendritic signaling cascades. Since the size of spines is variable, the spine neck may be an important regulator of this spino-dendritic crosstalk. We tested this hypothesis by using an experimentally defined, kinetic computer model in which spines of Purkinje neurons were coupled to their parent dendrite by necks of variable geometry. We show that Ca²⁺ signaling and calmodulin activation in spines with long necks is essentially isolated from the dendrite, while stubby spines show a strong coupling with their dendrite, mediated particularly by calbindin D28k. We conclude that the spine neck geometry, in close interplay with mobile Ca²⁺-binding proteins, regulates the spino-dendritic crosstalk.     

Investigation of whiplash injuries in the upper cervical spine using a detailed neck model

Whiplash injuries continue to have significant societal cost; however, the mechanism and location of whiplash injury is still under investigation. Recently, the upper cervical spine ligaments, particularly the alar ligament, have been identified as a potential whiplash injury location. In this study, a detailed and validated explicit finite element model of a 50th percentile male cervical spine in a seated posture was used to investigate upper cervical spine response and the potential for whiplash injury resulting from vehicle crash scenarios. This model was previously validated at the segment and whole spine levels for both kinematics and soft tissue strains in frontal and rear impact scenarios. The model predicted increasing upper cervical spine ligament strain with increasing impact severity. Considering all upper cervical spine ligaments, the distractions in the apical and alar ligaments were the largest relative to their failure strains, in agreement with the clinical findings. The model predicted the potential for injury to the apical ligament for 15.2 g frontal or 11.7 g rear impacts, and to the alar ligament for a 20.7 g frontal or 14.4 g rear impact based on the ligament distractions. Future studies should consider the effect of initial occupant position on ligament distraction.     

A potential link between lateral semicircular canal orientation,head posture,and dietary habits in extant rhinos (Perissodactyla,Rhinocerotidae)

Extant rhinoceroses share the characteristic nasal horn, although the number and size of horns varies among the five species. Although all species are herbivores, their dietary preferences, occipital shapes, and common head postures vary. Traditionally, to predict the “usual” head posture (the most used head posture of animals during normal unstressed activities, i.e., standing) of rhinos, the occipital shape was used. While a backward inclined occiput implies a downward hanging head (often found in grazers), a forward inclined occiput is related to the horizontal head posture in browsing rhinos. In this study, the lateral semicircular canal (LSC) of the bony labyrinth was virtually reconstructed from µCT‐images in order to investigate a possible link between LSC orientation and head posture in extant rhinoceroses. The usual head posture was formerly reconstructed for several non‐rhinoceros taxa with the assumption that the LSC of the inner ear is held horizontal (parallel to the ground) during normal activity of the living animal. The current analysis of the LSC orientation resulted in a downward inclined usual head posture for the grazing white rhinoceros and a nearly horizontal head posture in the browsing Javan rhinoceros. The other three browsing or mixed feeding species show subhorizontal (closer to horizontal than a downgrade inclination) head postures. The results show that anatomical and behavioral aspects, like occipital shape, presence and size of horns/tusk‐like lower incisors, as well as feeding and feeding height preferences influence the usual head posture. Because quantitative behavioral data are lacking for the usual head postures of the extant rhinos, the here described relationship between the LSC orientation and the resulting head posture linked to feeding preferences gives new insights. The results show, that the inner ear provides additional information to interpret usual head postures linked to feeding preferences that can easily be adapted to fossil rhinoceroses.     

Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites

Increases in cytosolic Ca2+ concentration ([Ca2+]i) mediated by NMDA-sensitive glutamate receptors (NMDARs) are important for synaptic plasticity. We studied a wide variety of dendritic spines on rat CA1 pyramidal neurons in acute hippocampal slices. Two-photon uncaging and Ca2+ imaging revealed that NMDAR-mediated currents increased with spine-head volume and that even the smallest spines contained a significant number of NMDARs. The fate of Ca2+ that entered spine heads through NMDARs was governed by the shape (length and radius) of the spine neck. Larger spines had necks that permitted greater efflux of Ca2+ into the dendritic shaft, whereas smaller spines manifested a larger increase in [Ca2+]i within the spine compartment as a result of a smaller Ca2+ flux through the neck. Spine-neck geometry is thus an important determinant of spine Ca2+ signaling, allowing small spines to be the preferential sites for isolated induction of long-term potentiation.     

Biomechanical implications of lumbar spinal ligament transection

Many lumbar spine surgeries either intentionally or inadvertently damage or transect spinal ligaments. The purpose of this work was to quantify the previously unknown biomechanical consequences of isolated spinal ligament transection on the remaining spinal ligaments (stress transfer), vertebrae (bone remodelling stimulus) and intervertebral discs (disc pressure) of the lumbar spine. A finite element model of the full lumbar spine was developed and validated against experimental data and tested in the primary modes of spinal motion in the intact condition. Once a ligament was removed, stress increased in the remaining spinal ligaments and changes occurred in vertebral strain energy, but disc pressure remained similar. All major biomechanical changes occurred at the same spinal level as the transected ligament, with minor changes at adjacent levels. This work demonstrates that iatrogenic damage to spinal ligaments disturbs the load sharing within the spinal ligament network and may induce significant clinically relevant changes in the spinal motion segment.     

Some sauropods raised their necks—evidence for high browsing in Euhelopus zdanskyi

A very long neck that is apparently suitable for feeding at great heights is a characteristic feature of most sauropod dinosaurs. Yet, it remains controversial whether any sauropods actually raised their necks high. Recently, strong physiological arguments have been put forward against the idea of high-browsing sauropods, because of the very high blood pressure that appears to be inevitable when the head is located several metres above the heart. For the sauropod Euhelopus zdanskyi, however, biomechanical evidence clearly indicates high browsing. Energy expenditure owing to high browsing is compared with energy costs for walking a distance. It is demonstrated for Euhelopus as well as for the much larger Brachiosaurus that despite an increase in the metabolic rate, high browsing was worthwhile for a sauropod if resources were far apart.     

Flexibility along the neck of the ostrich (Struthio camelus) and consequences for the reconstruction of dinosaurs with extreme neck length

The gross morphology and the flexibility along the neck of the ostrich (Struthio camelus) were examined using fresh tissue as well as neck skeletons. The results of the morphologic studies were compared with results from observations of living ostriches. The investigation was focused on differences in the morphology and the function between different sections of the neck. Additionally, the function of major dorsal neck ligaments was examined, including measurements of force-strain-relations. Comparative studies of giraffes (Giraffa camelopardalis) and camels (Camelus bactrianus) were conducted to find relations between the flexibility along the neck and the general feeding strategy. The examinations revealed that the neck of the ostrich can be divided into four sections with different functions. The first is the atlas-axis-complex which is responsible for torsion. The adjacent cranial section of the neck is flexible in dorsoventral and lateral directions but this part of the neck is usually kept straight at rest and during feeding. Dorsoventral flexibility is highest in the middle section of the neck, whereas the base of the neck is primarily used for lateral excursions of the neck. For giraffes and camels, the posture and utilization of the neck are also reflected in the flexibility of the neck. For all three species, it is possible to reconstruct the pattern of flexibility of the neck by using the neck skeletons alone. Therefore, it appears reasonable to reconstruct the neck utilization and the feeding strategies of dinosaurs with long necks by deriving the flexibility of the neck from preserved vertebrae. For Diplodocus carnegii the neck posture and the feeding strategy were reconstructed. Two neck regions, one around the 9th neck vertebra and the second at the base of the neck, indicate that Diplodocus, like the ostrich, adopted different neck postures. The neck was probably kept very low during feeding. During interruptions of the feeding, e.g., in an alert, the head could have been lifted in an economic way by raising the cranial section of the neck. During standing and locomotion the head was probably located well above the shoulders.     

Load-sharing in the lumbosacral spine in neutral standing & flexed postures – A combined finite element and inverse static study

Understanding load-sharing in the spine during in-vivo conditions is critical for better spinal implant design and testing. Previous studies of load-sharing that considered actual spinal geometry applied compressive follower load, with or without moment, to simulate muscle forces. Other studies used musculoskeletal models, which include muscle forces, but model the discs by simple beams or spherical joints and ignore the articular facet joints.This study investigated load-sharing in neutral standing and flexed postures using a detailed Finite Element (FE) model of the ligamentous lumbosacral spine, where muscle forces, gravity loads and intra-abdominal pressure, as predicted by a musculoskeletal model of the upper body, are input into the FE model. Flexion was simulated by applying vertebral rotations following spine rhythm measured in a previous in-vivo study, to the musculoskeletal model. The FE model predicted intradiscal pressure (IDP), strains in the annular fibers, contact forces in the facet joints, and forces in the ligaments. The disc forces and moments were determined using equilibrium equations, which considered the applied loads, including muscle forces and IDP, as well as forces in the ligaments and facet joints predicted by the FE model. Load-sharing was calculated as the portion of the total spinal load carried along the spine by each individual spinal structure. The results revealed that spinal loads which increased substantially from the upright to the flexed posture were mainly supported by the discs in the upright posture, whereas the ligaments’ contribution in resisting shear, compression, and moment was more significant in the flexed posture.     

Molecular phylogenetics and the evolution of labral spines among eastern Pacific ocenebrine gastropods

Labral spines are sharp projections of the apertural lip found in some marine gastropods that are used to penetrate hard-shelled prey. The majority of gastropod genera that contain labral spine-bearing species are found in the subfamily Ocenebrinae (Gastropoda: Muricidae). To reconstruct the evolutionary history of labral spine-bearing and labral spine-lacking gastropods in the eastern Pacific (EP) Ocean, partial sequences of two mitochondrial genes (cytochrome oxidase I and 12S rRNA) were obtained from representative taxa. Despite high nucleotide bias, a variety of phylogenetic reconstruction methods produced the same tree topology. The traditional taxonomic view that all "Nucella-like" spine-bearing taxa in the EP belong to a monophyletic "Acanthina" is rejected due to nonmonophyly of this group. The more recently recognized "Acanthinucella" is also not monophyletic, and we therefore propose the new genus Mexacanthina for two Mexican species formerly assigned to Acanthinucella. The genus Ocinebrina, which first appears in the middle Eocene, is not a stem EP ocenebrine lineage and may also not be a monophyletic clade. Tracing the evolutionary history of labral spines among extant lineages indicates that the absence of a labral spine is ancestral for all EP ocenebrines. Ancestral conditions could not be resolved unambiguously for all nodes of the phylogeny based on extant taxa. However, by jointly considering both molecular phylogenetic relationships and the phylogenetic affinities of several extinct taxa, all remaining character state transformation can be inferred unambiguously. Based on this analysis, a labral spine likely evolved independently in at least four lineages of EP ocenebrines. Although homoplasy appears to characterize labral spine evolution among ocenebrine gastropods, the structural position of a labral spine was evolutionarily altered in one lineage, indicating that different types of labral spines do not necessarily reflect convergent evolution.     

Cervical spine morphology and ligament property variations: A finite element study of their influence on sagittal bending characteristics

Cervical spine finite element models reported in biomechanical literature usually represent a static morphology. Not considering morphology as a model parameter limits the predictive capabilities for applications in personalized medicine, a growing trend in modern clinical practice. The objective of the study was to investigate the influence of variations in spinal morphology on the flexion-extension responses, utilizing mesh-morphing-based parametrization and metamodel-based sensitivity analysis. A C5-C6 segment was used as the baseline model. Variations of intervertebral disc height, facet joint slope, facet joint articular processes height, vertebral body anterior-posterior depth, and segment size were parametrized. In addition, material property variations of ligaments were considered for sensitivity analysis. The influence of these variations on vertebral rotation and forces in the ligaments were analyzed. The disc height, segmental size, and body depth were found to be the most influential (in the cited order) morphology variations; while among the ligament material property variations, capsular ligament and ligamentum flavum influenced vertebral rotation the most. Changes in disc height influenced forces in the posterior ligaments, indicating that changes in the anterior load-bearing column of the spine could have consequences on the posterior column. A method to identify influential morphology variations is presented in this work, which will help automation efforts in modeling to focus on variations that matter. This study underscores the importance of incorporating influential morphology parameters, easily obtained through computed tomography/magnetic resonance images, to better predict subject-specific biomechanical responses for applications in personalized medicine.