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      In Vivo Measurement of Mesokinesis in Gekko gecko: The Role of Cranial Kinesis during Gape Display, Feeding and Biting

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          Abstract

          Cranial kinesis refers to movements of skeletal sub-units relative to one another at mobile sutures within the skull. The presence and functional significance of cranial kinesis has been investigated in various vertebrates, with much of our understanding coming from comparative studies and manipulation of ligamentous specimens. Drawing on these studies, cranial kinesis in lizards has been modeled as a four-bar linkage system involving streptostyly (rotation of the quadrate), hypokinesis (dorsoventral flexion and extension of the palato-maxillary sub-unit), mesokinesis (dorsoventral flexion and extension of the snout at the fronto-parietal suture) and metakinesis (sliding movements between parietal and supraocciptal bones). In vivo studies, although limited, suggest that cranial kinesis serves an important role during routine behaviors such as feeding. Here, we use X-ray Reconstruction Of Moving Morphology to further quantify mesokinesis in vivo in Gekko gecko during three routine behaviors: gape display, biting and post-ingestion feeding. During gape display, the snout rotates dorsally above rest position, with mesokinesis accounting for a 10% increase in maximum gape over that achieved solely by the depression of the lower jaw. During defensive biting, the snout rotates ventrally below rest position to participate in gape closure. Finally, ventroflexion of the snout also occurs during post-ingestion feeding, accounting for 42% of gape closure during intra-oral transport, 86% during puncture-crushing, and 61% during pharyngeal packing. Mesokinesis thus appears to facilitate prey puncturing by allowing the snout to rotate ventrally so that the upper teeth pierce the prey item, thus limiting the need for large movements of the lower jaw. This is suggested to maintain a firm grip on the prey and reduce the possibility of prey escape. More generally, this study demonstrates that mesokinesis is a key component of defensive biting and gape display behaviors, as well as post-ingestion feeding, all of which are linked to organismal fitness.

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          Most cited references29

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          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.
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            Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches

            Background Damselfishes (Perciformes, Pomacentridae) are a major component of coral reef communities, and the functional diversity of their trophic anatomy is an important constituent of the ecological morphology of these systems. Using shape analyses, biomechanical modelling, and phylogenetically based comparative methods, we examined the anatomy of damselfish feeding among all genera and trophic groups. Coordinate based shape analyses of anatomical landmarks were used to describe patterns of morphological diversity and determine positions of functional groups in a skull morphospace. These landmarks define the lever and linkage structures of the damselfish feeding system, and biomechanical analyses of this data were performed using the software program JawsModel4 in order to calculate the simple mechanical advantage (MA) employed by different skull elements during feeding, and to compute kinematic transmission coefficients (KT) that describe the efficiency with which angular motion is transferred through the complex linkages of damselfish skulls. Results Our results indicate that pomacentrid planktivores are significantly different from other damselfishes, that biting MA values and protrusion KT ratios are correlated with pomacentrid trophic groups more tightly than KT scores associated with maxillary rotation and gape angle, and that the MAs employed by their three biting muscles have evolved independently. Most of the biomechanical parameters examined have experienced low levels of phylogenetic constraint, which suggests that they have evolved quickly. Conclusion Joint morphological and biomechanical analyses of the same anatomical data provided two reciprocally illuminating arrays of information. Both analyses showed that the evolution of planktivory has involved important changes in pomacentrid functional morphology, and that the mechanics of upper jaw kinesis have been of great importance to the evolution of damselfish feeding. Our data support a tight and biomechanically defined link between structure and the functional ecology of fish skulls, and indicate that certain mechanisms for transmitting motion through their jaw linkages may require particular anatomical configurations, a conclusion that contravenes the concept of "many-to-one mapping" for fish jaw mechanics. Damselfish trophic evolution is characterized by rapid and repeated shifts between a small number of eco-morphological states, an evolutionary pattern that we describe as reticulate adaptive radiation.
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              A functional consideration of cranial kinesis in lizards.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                31 July 2015
                2015
                : 10
                : 7
                : e0134710
                Affiliations
                [001]Ohio University Heritage College of Osteopathic Medicine, Department of Biomedical Sciences, Irvine Hall 228, Athens, OH, 45701, United States of America
                College of the Holy Cross, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SJM. Performed the experiments: SJM. Analyzed the data: SJM. Contributed reagents/materials/analysis tools: SJM SHW. Wrote the paper: SJM SHW.

                Article
                PONE-D-15-14423
                10.1371/journal.pone.0134710
                4521707
                26230087
                7ebd4c0a-5435-41b3-bf38-c8a8ed98037a
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 2 April 2015
                : 13 July 2015
                Page count
                Figures: 8, Tables: 5, Pages: 23
                Funding
                Funding for this project was provided by the National Science Foundation (MRI DBI-0922988), the Ohio Board of Regents, the Ohio University Office of the Vice President for Research and the Ohio University Heritage College of Osteopathic Medicine Research and Scholarly Affairs Committee (to SHW). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All kinematic data for each sequence analyzed are available within the paper as Supporting Information File S2.

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