Keith A. Metzger

X-ray reconstruction of moving morphology (XROMM): precision, accuracy and applications in comparative biomechanics research

X-Ray Reconstruction of Moving Morphology (XROMM) comprises a set of 3D X-ray motion analysis techniques that merge motion data from in vivo X-ray videos with skeletal morphology data from bone scans into precise and accurate animations of 3D bones moving in 3D space. XROMM methods include: (1) manual alignment (registration) of bone models to video sequences, i.e., Scientific Rotoscoping; (2) computer vision-based autoregistration of bone models to biplanar X-ray videos; and (3) marker-based registration of bone models to biplanar X-ray videos. Here, we describe a novel set of X-ray hardware, software, and workflows for marker-based XROMM. Refurbished C-arm fluoroscopes retrofitted with high-speed video cameras offer a relatively inexpensive X-ray hardware solution for comparative biomechanics research. Precision for our biplanar C-arm hardware and analysis software, measured as the standard deviation of pairwise distances between 1 mm tantalum markers embedded in rigid objects, was found to be +/-0.046 mm under optimal conditions and +/-0.084 mm under actual in vivo recording conditions. Mean error in measurement of a known distance between two beads was within the 0.01 mm fabrication tolerance of the test object, and mean absolute error was 0.037 mm. Animating 3D bone models from sets of marker positions (XROMM animation) makes it possible to study skeletal kinematics in the context of detailed bone morphology. The biplanar fluoroscopy hardware and computational methods described here should make XROMM an accessible and useful addition to the available technologies for studying the form, function, and evolution of vertebrate animals.

Bone strain gradients and optimization in vertebrate skulls

It is often stated that the skull is optimally designed for resisting feeding forces, where optimality is defined as maximum strength with minimum material. Running counter to this hypothesis are bone strain gradients--variation in bone strain magnitudes across the skull--which in the primate skull have been hypothesized to suggest that different parts of the skull are optimized for different functions. In this paper strain gradients in the skulls of four genera of primates, Sus, and Alligator were documented and compared. Strain gradients were pervasive in all taxa sampled. Patterns of strain gradients showed inter-taxon differences, but strains in the mandible and zygomatic arch were always higher than those in the circumorbital and neurocranial regions. Strain magnitudes in Alligator were twice as high as those in mammals. Strain gradients were also positively allometric; i. e., larger primates show steeper gradients (larger differences) between the mandible and circumorbital region than smaller primates. Different strain magnitudes in different areas of the same animal are hypothesized to reflect optimization to different criteria. It is therefore hardly surprising that the skull, in which numerous functional systems are found, exhibits very steep gradients. Inter-specific differences in strain magnitudes at similar sites also suggest inter-specific differences in optimality criteria. The higher strain magnitudes in the Alligator skull suggest that the Alligator skull may be designed to experience extremely high strains less frequently whereas the primate skull may be designed to resist lower strains more frequently.

The evolution of cranial design and performance in squamates: Consequences of skull-bone reduction on feeding behavior

The evolution of cranial design in lepidosaurians is characterized by a general trend toward the loss of cranial elements. The evolution of relatively lighter skulls in squamates appears tightly coupled to a reduction in relative mass of the jaw adductor, implying functional consequences for bite force and feeding behavior. Interestingly, among squamates the postorbital bar was reduced or lost at least twice independently and taxa characterized by the loss of these cranial elements (e.g., geckos and varanids) are generally reported as having a mobile skull. In Gekkotans, the loss of the postorbital bar was accompanied by a reduction of the supratemporal bar, resulting in a pronounced cranial kinesis. Our data show that having a kinetic skull has functional consequences and results in a reduction in bite force. The lower bite force may in turn be responsible for the decreased feeding efficiency as reflected in the longer duration of intra-oral transport cycles. Gekkotans, however, appear to exploit their intracranial mobility in ways that increases the velocity of jaw movement during opening and closing, which may allow them to capture more elusive prey. The morphological changes observed in the evolution of the cranial system in squamates appear tightly linked to functional and constructional demands on the skull, making squamate skull evolution a model system to investigate the consequences of morphological changes in a complex integrated system of performance, behavior, and ecology.

Kinematics of the quadrate bone during feeding in mallard ducks

SUMMARY Avian cranial kinesis, in which mobility of the quadrate, pterygoid and palatine bones contribute to upper bill elevation, is believed to occur in all extant birds. The most widely accepted model for upper bill elevation is that the quadrate rotates rostrally and medially towards the pterygoid, transferring force to the mobile pterygoid–palatine complex, which pushes on the upper bill. Until now, however, it has not been possible to test this hypothesis in vivo because quadrate motions are rapid, three-dimensionally complex and not visible externally. Here we use a new in vivo X-ray motion analysis technique, X-ray reconstruction of moving morphology (XROMM), to create precise (±0.06 mm) 3-D animations of the quadrate, braincase, upper bill and mandible of three mallard ducks, Anas platyrhynchos. We defined a joint coordinate system (JCS) for the quadrato-squamosal joint with the axes aligned to the anatomical planes of the skull. In this coordinate system, the quadrates 3-D rotations produce an elliptical path of pterygoid process motion, with medial and rostrodorsal then lateral and rostrodorsal motion as the upper bill elevates. As the upper bill depresses, the pterygoid process continues along the ellipsoidal path, with lateral and caudoventral then medial and caudoventral motion. We also found that the mandibular rami bow outwards (streptognathy) during mandibular depression, which may cause the lateral component of quadrate rotation that we observed. Relative to the JCS aligned with the anatomical planes of the skull, a second JCS aligned with quadrato-squamosal joint anatomy did not produce a simpler description of quadrate kinematics.

Chewing variation in lepidosaurs and primates.

SUMMARY Mammals chew more rhythmically than lepidosaurs. The research presented here evaluated possible reasons for this difference in relation to differences between lepidosaurs and mammals in sensorimotor systems. Variance in the absolute and relative durations of the phases of the gape cycle was calculated from kinematic data from four species of primates and eight species of lepidosaurs. The primates exhibit less variance in the duration of the gape cycle than in the durations of the four phases making up the gape cycle. This suggests that increases in the durations of some gape cycle phases are accompanied by decreases in others. Similar effects are much less pronounced in the lepidosaurs. In addition, the primates show isometric changes in gape cycle phase durations, i.e. the relative durations of the phases of the gape cycle change little with increasing cycle time. In contrast, in the lepidosaurs variance in total gape cycle duration is associated with increases in the proportion of the cycle made up by the slow open phase. We hypothesize that in mammals the central nervous system includes a representation of the optimal chew cycle duration maintained using afferent feedback about the ongoing state of the chew cycle. The differences between lepidosaurs and primates do not lie in the nature of the sensory information collected and its feedback to the feeding system, but rather the processing of that information by the CNS and its use feed-forward for modulating jaw movements and gape cycle phase durations during chewing.

Material properties of mandibular cortical bone in the American alligator, Alligator mississippiensis

This study reports the elastic material properties of cortical bone in the mandible of juvenile Alligator mississippiensis obtained by using an ultrasonic wave technique. The elastic modulus, the shear modulus, and Poissons ratio were measured on 42 cylindrical Alligator bone specimens obtained from the lingual and facial surfaces of 4 fresh Alligator mandibles. The data suggest that the elastic properties of alligator mandibular cortical bone are similar to those found in mammals and are orthotropic. The properties most resemble those found in the cortex of mammalian postcranial long bones where the bone is most stiff in one direction and much less stiff in the two remaining orthogonal directions. This is different from cortical bone found in the mandibles of humans and some monkeys, where the bone has greatest stiffness in one direction, much less stiffness in another direction, and an intermediate amount in the third orthogonal direction. This difference suggests a relationship between levels of orthotropy and bending stress. The comparability of these elastic moduli to those of other vertebrates suggest that the high bone strain magnitudes recorded from the alligator mandible in vivo are not attributable to a lower stiffness of alligator mandibular bone.

In vivo bone strain and finite element modeling of the mandible of Alligator mississippiensis.

Forces experienced during feeding are thought to strongly influence the morphology of the vertebrate mandible; in vivo strain data are the most direct evidence for deformation of the mandible induced by these loading regimes. Although many studies have documented bone strains in the mammalian mandible, no information is available on strain magnitudes, orientations or patterns in the sauropsid lower jaw during feeding. Furthermore, strain gage experiments record the mechanical response of bone at a few locations, not across the entire mandible. In this paper, we present bone strain data recorded at various sites on the lower jaw of Alligator mississippiensis during in vivo feeding experiments. These data are used to understand how changes in loading regime associated with changes in bite location are related to changes in strain regime on the working and balancing sides of the mandible. Our results suggest that the working side mandible is bent dorsoventrally and twisted about its long‐axis during biting, and the balancing side experiences primarily dorsoventral bending. Strain orientations are more variable on the working side than on the balancing side with changes in bite point and between experiments; the balancing side exhibits higher strain magnitudes. In the second part of this paper, we use principal strain orientations and magnitudes recorded in vivo to evaluate a finite element model of the alligator mandible. Our comparison demonstrates that strain orientations and mandibular deformation predicted by the model closely match in vivo results; however, absolute strain magnitudes are lower in the finite element model.

Inertial feeding in the teiid lizard Tupinambis merianae: the effect of prey size on the movements of hyolingual apparatus and the cranio-cervical system.

SUMMARY In most terrestrial tetrapods, the transport of prey through the oral cavity is accomplished by movements of the hyolingual apparatus. Morphological specializations of the tongue in some lizard taxa are thought to be associated with the evolution of vomerolfaction as the main prey detection mode. Moreover, specializations of the tongue are hypothesized to compromise the efficiency of the tongue during transport; thus, driving the evolution of inertial transport. Here we use a large teiid lizard, Tupinambis merianae, as a model system to test the mechanical link between prey size and the use of inertial feeding. We hypothesize that an increase in prey size will lead to the increased recruitment of the cranio-cervical system for prey transport and a reduced involvement of the tongue and the hyolingual apparatus. Discriminant analyses of the kinematics of the cranio-cervical, jaw and hyolingual systems show that the transport of large prey is indeed associated with a greater utilization of the cranio-cervical system (i.e. neck and head positioning). The tongue retains a kinematic pattern characteristic of lingual transport in other lizards but only when processing small prey. Our data provide evidence for an integration of the hyolingual and cranio-cervical systems; thus, providing partial support for an evolutionary scenario whereby the specialization of the tongue for chemoreception has resulted in the evolution of inertial transport strategies.

Quantitative analysis of the effect of prey properties on feeding kinematics in two species of lizards

SUMMARY Studies of the functional morphology of feeding have typically not included an analysis of the potential for the kinematics of the gape cycle to vary based on the material properties of the prey item being consumed. Variation in prey properties is expected not only to reveal variation in feeding function, but allows testing of the functional role of the phases of the gape cycle. The jaw kinematics of two species of lizards are analyzed when feeding trials are conducted using quantitative control of prey mass, hardness and mobility. For both species, there were statistically significant prey effects on feeding kinematics for all the prey properties evaluated (i.e. prey mass, hardness and mobility). Of these three prey properties, prey mass had a more significant effect on feeding kinematics than prey hardness or mobility. Revealing the impact of varying prey properties on feeding kinematics helps to establish the baseline level of functional variability in the feeding system. Additionally, these data confirm the previously hypothesized functional role of the slow open (SO) phase of the gape cycle as allowing for physical conformation of the tongue to the surface of the food bolus in preparation for further intraoral transport.

Utility of Skeletal Mass as a Measure of Body Size in Lizards

Abstract Appropriate and relevant measures of body size are essential to understand scaling relationships or to compare morphometric data from specimens or taxa of different sizes. Traditionally, body mass and snout–vent length have been used as measures of body size in lizards. Here, we report on the relevance of an alternative measure of size, skeletal mass, which is highly correlated with traditional body size measures and may have more practical value when using skeletal measurements based on museum collections.