Rhythmic chew cycles with distinct fast and slow phases are ancestral to gnathostomes.

Intra-oral food processing, including chewing, is important for safe swallowing and efficient nutrient assimilation across tetrapods. Gape cycles in tetrapod chewing consist of four phases (fast open and -close, and slow open and -close), with processing mainly occurring during slow close. Basal aquatic-feeding vertebrates also process food intraorally, but whether their chew cycles are partitioned into distinct phases, and how rhythmic their chewing is, remains unknown. Here, we show that chew cycles from sharks to salamanders are as rhythmic as those of mammals, and consist of at least three, and often four phases, with phase distinction occasionally lacking during jaw opening. In fishes and aquatic-feeding salamanders, fast open has the most variable duration, more closely resembling mammals than basal amniotes (lepidosaurs). Across ontogenetically or behaviourally mediated terrestrialization, salamanders show a distinct pattern of the second closing phase (near-contact) being faster than the first, with no clear pattern in partitioning of variability across phases. Our results suggest that distinct fast and slow chew cycle phases are ancestral for jawed vertebrates, followed by a complicated evolutionary history of cycle phase durations and jaw velocities across fishes, basal tetrapods and mammals. These results raise new questions about the mechanical and sensorimotor underpinnings of vertebrate food processing. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Walking on chains: the morphology and mechanics behind the fin ray derived limbs of sea-robins.

Fish fin rays (lepidotrichia) are typically composed of paired and segmented flexible structures (hemitrichia) that help support and change the shape of the fins to affect water flow. Yet, marine ray-finned fish that are members of the family Priontinae (sea-robins) have specialized pectoral fin rays that are separated from the fin and used as limbs to walk along the seafloor. While previous kinematic studies have demonstrated the use of these specialized fin rays as walking appendages, there is little information on how the morphology of the 'walking rays' and associated musculature facilitate underwater walking. Here, we examine the musculoskeletal anatomy of the walking and pectoral fin rays in the striped sea-robin Prionotus evolans and compare the mechanical properties of the rays with those of the smaller northern sea-robin Prionotus carolinus We aimed to determine what structural modifications in the walking rays allow them to function as a supportive limb. We found enlarged processes for muscle attachment, bone extensions that brace the hemitrich articulations, and reduced flexibility and increased second moment of area along the rostro-caudal bending axis in the rays used for walking. This novel limb design may have promoted the benthic foraging behavior exhibited by these species by uncoupling locomotion and feeding.

Shearing overbite and asymmetrical jaw motions facilitate food breakdown in a freshwater stingray, Potamotrygon motoro.

Many species of fish process their prey with cyclic jaw motions that grossly resemble those seen in mammalian mastication, despite starkly different tooth and jaw morphologies. The degree of similarity between the processing behaviors of these disparate taxa has implications for our understanding of convergence in vertebrate feeding systems. Here, we used XROMM (X-ray reconstruction of moving morphology) to investigate prey processing behavior of Potamotrygon motoro, the ocellate river stingray, which has recently been found to employ asymmetrical, shearing jaw motions to break down its prey. We found that P. motoro modulates its feeding kinematics to produce two distinct types of chew cycles: compressive cycles and overbite cycles. The latter are characterized by over-rotation of the upper jaw relative to the lower jaw, past the expected occlusal limit, and higher levels of bilateral asymmetry as compared with compressive chews. We did not find evidence of the mediolateral shearing motions typical of mammalian mastication, but overbite cycles appear to shear the prey item between the upper and lower toothplates in a propalinal fashion. Additionally, comparison of hyomandibular and jaw motions demonstrates that the angular cartilages decouple jaw displacement from hyomandibular displacement in rostrocaudal and mediolateral directions. The multiple similarities between mammalian mastication and the dynamic processing behavior of P. motoro support the use of sub-family Potamotrygoninae as a model for studying evolutionary convergence of mastication-like processing.

Function of the hypobranchial muscles and hyoidiomandibular ligament during suction capture and bite processing in white-spotted bamboo sharks, Chiloscyllium plagiosum.

Suction feeding in teleost fish is a power-dependent behavior, requiring rapid and forceful expansion of the orobranchial cavity by the hypobranchial and trunk muscles. To increase power production for expansion, many species employ in-series tendons and catch mechanisms to store and release elastic strain energy. Suction feeding sharks such as Chiloscyllium plagiosum lack large in-series tendons on the hypobranchials, yet two of the hypobranchials, the coracohyoideus and coracoarcualis (CH and CA; hyoid depressors), are arranged in-series, and run deep and parallel to a third muscle, the coracomandibularis (CM, jaw depressor). The arrangement of the CH and CA suggests that C. plagiosum is using the CH muscle rather than a tendon to store and release elastic strain energy. Here we describe the anatomy of the feeding apparatus, and present data on hyoid and jaw kinematics and fascicle shortening in the CM, CH and CA quantified using sonomicrometry, with muscle activity and buccal pressure recorded simultaneously. Results from prey capture show that prior to jaw and hyoid depression the CH is actively lengthened by shortening of the in-series CA. The active lengthening of the CH and pre-activation of the CH and CA suggest that the CH is functioning to store and release elastic energy during prey capture. Catch mechanisms are proposed involving a dynamic moment arm and four-bar linkage between the hyoidiomandibular ligament (LHML), jaws and ceratohyals that is influenced by the CM. Furthermore, the LHML may be temporarily disengaged during behaviors such as bite processing to release linkage constraints.

Using collaborative two-stage examinations to address test anxiety in a large enrollment gateway course.

Large enrollment foundational courses are perceived as "high stakes" because of their potential to act as barriers for progression to the next course or admittance to a program. The nature of gateway courses makes them ideal settings to explore the relationship between anxiety, pedagogical interventions, and student performance. Here, two-stage collaborative examinations were implemented to improve test-taking skills and address widespread test anxiety in an introductory human anatomy course. Test anxiety data were collected (using the Motivated Strategies for Learning Questionnaire) before the first examination and last examination. Most students experienced decreased test anxiety over the course of the semester; however, some students may have experienced performance limiting conditions due to test anxiety at the end of the semester based on academic ability in the course (in "C" students when compared to "A" students: P < 0.00006 and "B" students: P < 0.05), overall academic ability (in academically weaker students: P < 0.025), and demographic factors (in women: P < 0.025). The strongest performances on examinations were primarily observed in already academically strong students (mean individual performance: P < 0.000, mean group performance: P < 0.000). Furthermore, changes in test anxiety were not significantly associated with the group portion of the examinations. Patterns of changes in test anxiety over the course of the semester underscore a complex interaction between test anxiety, student background, and student performance. Results suggest that pathways for test anxiety in "high stakes" courses may be separate from the mechanisms responsible for the benefits of collaborative testing. Anat Sci Educ 10: 409-422. © 2017 American Association of Anatomists.

Eating with a saw for a jaw: functional morphology of the jaws and tooth-whorl in Helicoprion davisii.

The recent reexamination of a tooth-whorl fossil of Helicoprion containing intact jaws shows that the symphyseal tooth-whorl occupies the entire length of Meckel's cartilage. Here, we use the morphology of the jaws and tooth-whorl to reconstruct the jaw musculature and develop a biomechanical model of the feeding mechanism in these early Permian predators. The jaw muscles may have generated large bite-forces; however, the mechanics of the jaws and whorl suggest that Helicoprion was better equipped for feeding on soft-bodied prey. Hard shelled prey would tend to slip anteriorly from the closing jaws due to the curvature of the tooth-whorl, lack of cuspate teeth on the palatoquadrate (PQ), and resistance of the prey. When feeding on soft-bodied prey, deformation of the prey traps prey tissue between the two halves of the PQ and the whorl. The curvature of the tooth-whorl and position of the exposed teeth relative to the jaw joint results in multiple tooth functions from anterior to posterior tooth that aid in feeding on soft-bodied prey. Posterior teeth cut and push prey deeper into the oral cavity, while middle teeth pierce and cut, and anterior teeth hook and drag more of the prey into the mouth. Furthermore, the anterior-posterior edges of the teeth facilitate prey cutting with jaw closure and jaw depression. The paths traveled by each tooth during jaw depression are reminiscent of curved pathways used with slashing weaponry such as swords and knifes. Thus, the jaws and tooth-whorl may have formed a multifunctional tool for capturing, processing, and transporting prey by cyclic opening and closing of the lower jaw in a sawing fashion.

Jaws for a spiral-tooth whorl: CT images reveal novel adaptation and phylogeny in fossil Helicoprion.

New CT scans of the spiral-tooth fossil, Helicoprion, resolve a longstanding mystery concerning the form and phylogeny of this ancient cartilaginous fish. We present the first three-dimensional images that show the tooth whorl occupying the entire mandibular arch, and which is supported along the midline of the lower jaw. Several characters of the upper jaw show that it articulated with the neurocranium in two places and that the hyomandibula was not part of the jaw suspension. These features identify Helicoprion as a member of the stem holocephalan group Euchondrocephali. Our reconstruction illustrates novel adaptations, such as lateral cartilage to buttress the tooth whorl, which accommodated the unusual trait of continuous addition and retention of teeth in a predatory chondrichthyan. Helicoprion exemplifies the climax of stem holocephalan diversification and body size in Late Palaeozoic seas, a role dominated today by sharks and rays.

Tooth reorientation affects tooth function during prey processing and tooth ontogeny in the lesser electric ray, Narcine brasiliensis.

The dental anatomy of elasmobranch fishes (sharks, rays and relatives) creates a functional system that is more dynamic than that of mammalian dentition. Continuous dental replacement (where new teeth are moved rostrally to replace older ones) and indirect fibrous attachment of the dentition to the jaw allow teeth to reorient relative to the jaw over both long- and short-term scales, respectively. In this study, we examine the processing behavior and dental anatomy of the lesser electric ray Narcine brasiliensis (Olfers, 1831) to illustrate that the freedom of movement of elasmobranch dentition allows a functional flexibility that can be important for complex prey processing behaviors. From static manipulations of dissected jaws and observations of feeding events in live animals, we show that the teeth rotate during jaw protrusion, resulting in a secondary grasping mechanism that likely serves to hold prey while the buccal cavity is flushed free of sediment. The function of teeth is not always readily apparent from morphology; in addition to short-term reorientation, the long-term dental reorientation during replacement allows a given tooth to serve multiple functions during tooth ontogeny. Unlike teeth inside the mouth, the cusps of external teeth (on the portion of the tooth pad that extends past the occlusal plane) lay flat, such that the labial faces act as a functional battering surface, protecting the jaws during prey excavation.

Evolution of asynchronous motor activity in paired muscles: effects of ecology, morphology, and phylogeny.

Many studies of feeding behavior have implanted electrodes unilaterally (in muscles on only one side of the head) to determine the basic motor patterns of muscles controlling the jaws. However, bilateral implantation has the potential to achieve a more comprehensive understanding of modification of the motor activity that may be occurring between the left and right sides of the head. In particular, complex processing of prey is often characterized by bilaterally asynchronous and even unilateral activation of the jaw musculature. In this study, we bilaterally implant feeding muscles in species from four orders of elasmobranchs (Squaliformes, Orectolobiformes, Carcharhiniformes, Rajoidea) in order to characterize the effects of type of prey, feeding behavior, and phylogeny on the degree of asynchronous muscle activation. Electrodes were implanted in three of the jaw adductors, two divisions of the quadratomandibularis and the preorbitalis, as well as in a cranial elevator in sharks, the epaxialis. The asynchrony of feeding events (measured as the degree to which activity of members of a muscle pair is out of phase) was compared across species for capture versus processing and simple versus complex prey, then interpreted in the contexts of phylogeny, morphology, and ecology to clarify determinants of asynchronous activity. Whereas capture and processing of prey were characterized by statistically similar degrees of asynchrony for data pooled across species, events involving complex prey were more asynchronous than were those involving simple prey. The two trophic generalists, Squalus acanthias and Leucoraja erinacea, modulated the degree of asynchrony according to type of prey, whereas the two behavioral specialists, Chiloscyllium plagiosum and Mustelus canis, activated the cranial muscles synchronously regardless of type of prey. These differences in jaw muscle activity would not have been detected with unilateral implantation. Therefore, we advocate bilateral implantation in studies of cranial muscle function in fishes, particularly when investigating behaviors associated with processing complex prey. Incorporating this methodology will provide a more detailed understanding of the coordination and evolution of paired-muscle function in the feeding apparatus relative to behavioral and ecological performance.

Morphology and mechanics of the teeth and jaws of white-spotted bamboo sharks (Chiloscyllium plagiosum).

The teeth of white-spotted bamboo sharks (Chiloscyllium plagiosum) are used to clutch soft-bodied prey and crush hard prey; however, the dual function is not evident from tooth morphology alone. Teeth exhibit characteristics that are in agreement with a clutching-type tooth morphology that is well suited for grasping and holding soft-bodied prey, but not for crushing hard prey. The dual role of this single tooth morphology is facilitated by features of the dental ligament and jaw joint. Tooth attachment is flexible and elastic, allowing movement in both sagittal and frontal planes. During prey capture spike-like tooth cusps pierce the flesh of soft prey, thereby preventing escape. When processing prey harder than the teeth can pierce the teeth passively depress, rotating inward towards the oral cavity such that the broader labial faces of the teeth are nearly parallel to the surface of the jaws and form a crushing surface. Movement into the depressed position increases the tooth surface area contacting prey and decreases the total stress applied to the tooth, thereby decreasing the risk of structural failure. This action is aided by a jaw joint that is ventrally offset from the occlusal planes of the jaws. The offset joint position allows many teeth to contact prey simultaneously and orients force vectors at contact points between the jaws and prey in a manner that shears or rolls prey between the jaws during a bite, thus, aiding in processing while reducing forward slip of hard prey from the mouth. Together the teeth, dental ligament, and jaws form an integrated system that may be beneficial to the feeding ecology of C. plagiosum, allowing for a diet that includes prey of varying hardness and elusiveness.