Prolonged use of a soft diet during early growth and development alters feeding behavior and chewing kinematics in a young animal model.

In infants and children with feeding and swallowing issues, modifying solid foods to form a liquid or puree is used to ensure adequate growth and nutrition. However, the behavioral and neurophysiological effects of prolonged use of this intervention during critical periods of postnatal oral skill development have not been systematically examined, although substantial anecdotal evidence suggests that it negatively impacts downstream feeding motor and coordination skills, possibly due to immature sensorimotor development. Using an established animal model for infant and juvenile feeding physiology, we leverage X-ray reconstruction of moving morphology to compare feeding behavior and kinematics between 12-week-old pigs reared on solid chow (control) and an age- and sex-matched cohort raised on the same chow softened to a liquid. When feeding on two novel foods, almond and apple, maintenance on a soft diet decreases gape cycle duration, resulting in a higher chewing frequency. When feeding on almonds, pigs in this group spent less time ingesting foods compared to controls, and chewing cycles were characterized by less jaw rotation about a dorsoventral axis (yaw) necessary for food reduction. There was also a reduced tendency to alternate chewing side with every chew during almond chewing, a behavioral pattern typical of pigs. These more pronounced impacts on behavior and kinematics during feeding on almonds, a tougher and stiffer food than apples, suggest that food properties mediate the behavioral and physiological impacts of early texture modification and that the ability to adapt to different food properties may be underdeveloped. In contrast, the limited effects of food texture modification on apple chewing indicate that such intervention/treatment does not alter feeding behavior of less challenging foods. Observed differences cannot be attributed to morphology because texture modification over the treatment period had limited impact on craniodental growth. Short-term impacts of soft-texture modification during postweaning development on feeding dynamics should be considered as potential negative outcomes of this treatment strategy.

Symphyseal morphology and jaw muscle recruitment levels during mastication in musteloid carnivorans.

In studies of mammalian mastication, a possible relationship has been proposed between bilateral recruitment of jaw adductor muscle force during unilateral chewing and the degree of fusion of the mandibular symphysis. Specifically, species that have unfused, mobile mandibular symphyses tend to utilize lower levels of jaw adductor force on the balancing (nonchewing) than the working (chewing) side of the head, when compared to related species with fused symphyses. Here, we compare jaw adductor recruitment levels in two species of musteloid carnivoran: the carnivorous ferret (unfused symphysis), and the frugivorous kinkajou (fused symphysis). During forceful chewing, we observe that ferrets recruit far more working-side muscle force than kinkajous, regardless of food toughness and that high working-to-balancing side ratios are the result of increased working-side force, often coupled with reduced balancing-side force. We propose that in carnivorans, high working-to-balancing side force ratios coupled with an unfused mandibular symphysis are necessary to rotate the hemimandible for precise unilateral occlusion of the carnassial teeth and to sustain laterally oriented force on the jaw to engage the carnassial teeth during shearing of tough foods. In contrast, the kinkajou's flattened cheekteeth permit less precise occlusion and require medially-oriented forces for grinding, thus, a fused symphysis is mechanically beneficial.

Characterizing tongue deformations during mastication using changes in planar components of three-dimensional angles.

Understanding of tongue deformations during mammalian mastication is limited, but has benefited from recent developments in multiplanar imaging technology. Here, we demonstrate how a standardized radiopaque marker implant configuration and biplanar fluoroscopy can quantify three-dimensional shape changes during chewing in pigs. Transverse and sagittal components of the three-dimensional angle between markers enable characterizing deformations in anatomically relevant directions. The transverse component illustrates bending to the left or to the right, which can occur symmetrically or asymmetrically, the latter sometimes indicating regional widening. The sagittal component reflects 'arching' or convex deformations in the dorsoventral dimension symmetrically or asymmetrically, the latter characteristic of twisting. Trends are detected in both the transverse and sagittal planes, and combinations thereof, to modify tongue shape in complex deformations. Both the transverse and sagittal components were also measured at key jaw and tongue positions, demonstrating variability particularly with respect to maximum and minimum gape. This highlights the fact that unlike tongue position, tongue deformations are more independent of jaw position, likely in response to the ever-changing bolus shape and position. From a methodological perspective, our study showcases advantages of a repeatable three-marker implant configuration suitable for animals of different sizes and highlights considerations for different implant patterns. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Regional Tongue Deformations During Chewing and Drinking in the Pig.

As a muscular hydrostat, the tongue undergoes complex deformations during most oral behaviors, including chewing and drinking. During thesebehaviors, deformations occur in concert with tongue and jaw movements to position and transport the bolus. Moreover, the various parts of the tongue may move and deform at similar timepoints relative to the gape cycle or they may occur at different timepoints, indicating regional biomechanical and functional variation. The goal of this study is to quantify tongue deformations during chewing and drinking in pigs by characterizing intrinsic changes in tongue dimensions (i.e., length and width) across multiple regions simultaneously. Tongue deformations are generally larger during chewing cycles compared to drinking cycles. Chewing and drinking also differ in the timing, relative to the gape cycle, of regional length and width, but not total length, deformations. This demonstrates functional differences in the temporal dynamics of localized shape changes, whereas the global properties of jaw-tongue coordination are maintained. Finally, differences in the trade-off between length and width deformations demonstrate that the properties of a muscular hydrostat are observed at the whole tongue level, but biomechanical variation (e.g., changes in movements and deformations) at the regional level exists. This study provides new critical insights into the regional contributions to tongue deformations as a basis for future work on multidimensional shape changes in soft tissues.

En tant qu'hydrostat musculaire, la langue subit des déformations complexes pendant la plupart des comportements oraux, en particulier au cours de la mastication et de l'ingestion de liquide. Au cours de ces comportements, les déformations se produisent de concert avec les mouvements de la langue et des mâchoires pour positionner et transporter le bolus. De plus, les différentes parties de la langue peuvent se déplacer et se déformer à des moments similaires ou différents par rapport au cycle d'ouverture de la bouche, indiquant une variation biomécanique et fonctionnelle régionale de la langue. L'objectif de cette étude est de quantifier les déformations de la langue pendant la mastication et l'ingestion d'eau chez le porc en caractérisant les changements intrinsèques des dimensions de la langue (i.e., longueur et largeur) des différentes régions de la langue simultanément. Les déformations de la langue sont généralement plus importantes pendant les cycles de mastication que pendant les cycles d'ingestion d'eau. La mastication et l'ingestion d'eau diffèrent également dans le timing (par rapport au cycle d'ouverture de la bouche) des déformations régionales de la langue en longueur et en largeur, mais pas en longueur totale. Cela démontre des différences fonctionnelles dans la dynamique temporelle des changements localisés de la forme de la langue alors que les propriétés globales de la coordination mâchoire-langue sont maintenues. Enfin, les différences dans le compromis mettant en jeu les déformations en longueur et en largeur démontrent que les propriétés d'un hydrostat musculaire sont observées au niveau de la langue entière, mais qu'il existe une variation biomécanique (par exemple, des changements dans les mouvements et les déformations) au niveau régional. Cette étude fournit de nouvelles informations essentielles sur les contributions régionales des déformations de la langue, qui serviront de base aux travaux futurs sur les changements multidimensionnels de forme dans les tissus mous.

Jaw kinematics and tongue protraction-retraction during chewing and drinking in the pig.

Mastication and drinking are rhythmic and cyclic oral behaviors that require interactions between the tongue, jaw and a food or liquid bolus, respectively. During mastication, the tongue transports and positions the bolus for breakdown between the teeth. During drinking, the tongue aids in ingestion and then transports the bolus to the oropharynx. The objective of this study was to compare jaw and tongue kinematics during chewing and drinking in pigs. We hypothesized there would be differences in jaw gape cycle dynamics and tongue protraction-retraction between behaviors. Mastication cycles had an extended slow-close phase, reflecting tooth-food-tooth contact, whereas drinking cycles had an extended slow-open phase, corresponding to tongue protrusion into the liquid. Compared with chewing, drinking jaw movements were of lower magnitude for all degrees of freedom examined (jaw protraction, yaw and pitch), and were bilaterally symmetrical with virtually no yaw. The magnitude of tongue protraction-retraction (Txt), relative to a mandibular coordinate system, was greater during mastication than during drinking, but there were minimal differences in the timing of maximum and minimum Txt relative to the jaw gape cycle between behaviors. However, during drinking, the tongue tip is often located outside the oral cavity for the entire cycle, leading to differences between behaviors in the timing of anterior marker maximum Txt. This demonstrates that there is variation in tongue-jaw coordination between behaviors. These results show that jaw and tongue movements vary significantly between mastication and drinking, which hints at differences in the central control of these behaviors.

Jaw kinematics and tongue protraction-retraction during chewing and drinking in the pig.

Mastication and drinking are rhythmic and cyclic oral behaviors that require interactions between the tongue, jaw and a food or liquid bolus, respectively. During mastication, the tongue transports and positions the bolus for breakdown between the teeth. During drinking, the tongue aids in ingestion and then transports the bolus to the oropharynx. The objective of this study was to compare jaw and tongue kinematics during chewing and drinking in pigs. We hypothesized there would be differences in jaw gape cycle dynamics and tongue protraction-retraction between behaviors. Mastication cycles had an extended slow-close phase, reflecting tooth-food-tooth contact, whereas drinking cycles had an extended slow-open phase, corresponding to tongue protrusion into the liquid. Compared with chewing, drinking jaw movements were of lower magnitude for all degrees of freedom examined (jaw protraction, yaw and pitch), and were bilaterally symmetrical with virtually no yaw. The magnitude of tongue protraction-retraction (Txt), relative to a mandibular coordinate system, was greater during mastication than during drinking, but there were minimal differences in the timing of maximum and minimum Txt relative to the jaw gape cycle between behaviors. However, during drinking, the tongue tip is often located outside the oral cavity for the entire cycle, leading to differences between behaviors in the timing of anterior marker maximum Txt. This demonstrates that there is variation in tongue-jaw coordination between behaviors. These results show that jaw and tongue movements vary significantly between mastication and drinking, which hints at differences in the central control of these behaviors.

Unilateral lingual nerve transection alters jaw-tongue coordination during mastication in pigs.

During chewing, movements and deformations of the tongue are coordinated with jaw movements to manage and manipulate the bolus and avoid injury. Individuals with injuries to the lingual nerve report both tongue injuries due to biting and difficulties in chewing, primarily because of impaired bolus management, suggesting that jaw-tongue coordination relies on intact lingual afferents. Here, we investigate how unilateral lingual nerve (LN) transection affects jaw-tongue coordination in an animal model (pig, Sus scrofa). Temporal coordination between jaw pitch (opening-closing) and 1) anteroposterior tongue position (i.e., protraction-retraction), 2) anteroposterior tongue length, and 3) mediolateral tongue width was compared between pre- and post-LN transection using cross-correlation analyses. Overall, following LN transection, the lag between jaw pitch and the majority of tongue kinematics decreased significantly, demonstrating that sensory loss from the tongue alters jaw-tongue coordination. In addition, decrease in jaw-tongue lag suggests that, following LN transection, tongue movements and deformations occur earlier in the gape cycle than when the lingual sensory afferents are intact. If the velocity of tongue movements and deformations remains constant, earlier occurrence can reflect less pronounced movements, possibly to avoid injuries. The results of this study demonstrate that lingual afferents participate in chewing by assisting with coordinating the timing of jaw and tongue movements. The observed changes may affect bolus management performance and/or may represent protective strategies because of altered somatosensory awareness of the tongue.NEW & NOTEWORTHY Chewing requires coordination between tongue and jaw movements. We compared the coordination of tongue movements and deformation relative to jaw opening-closing movements pre- and post-lingual nerve transection during chewing in pigs. These experiments reveal that the timing of jaw-tongue coordination is altered following unilateral disruption of sensory information from the tongue. Therefore, maintenance of jaw-tongue coordination requires bilateral sensory information from the tongue.

Effects of food properties on chewing in pigs: Flexibility and stereotypy of jaw movements in a mammalian omnivore.

Chewing is a rhythmic oral behavior that requires constant modifications of jaw movements in response to changes in food properties. The food-specific kinematic response is dependent on the potential for kinematic flexibility allowed by morphology and modulation of motor control. This study investigates the effects of food toughness and stiffness on the amplitude and variability of jaw movements during chewing in a typical omnivorous mammalian model (pigs). Jaw movements were reconstructed using X-ray Reconstruction Of Moving Morphology (XROMM) and kinematic data associated with the amplitude of jaw pitch (opening-closing) and jaw yaw (mediolateral rotation) were extracted for each cycle. Between-food differences were tested for the amplitude of jaw movements during each phase of the gape cycle, as well as in their respective within-food variability, or stereotypy, as indicated by coefficients of variation. With increasing toughness, jaw pitch amplitude is decreased during fast close, larger and more stereotyped during slow close, smaller but more variable during slow open, and more variable during fast open. In addition, when chewing on tougher foods, the amplitude of jaw yaw during slow close only increases in a subset of individuals, but all become less variable (i.e., more stereotyped). In contrast, increasing food stiffness has no effect on the amplitude or the variability of jaw pitch, whereas jaw yaw increases significantly in the majority of individuals studied. Our data demonstrate that food stiffness and toughness both play a role in modulating gape cycle dynamics by altering the trajectory of jaw movements, especially during the slow-close phase and tooth-food-tooth contact, albeit differently. This highlights how a generalist oral morphology such as that of pigs (e.g., bunodont teeth lacking precise occlusion, permissive temporomandibular joint allowing extensive condylar displacements in 3 dimensions) enables organisms to not only adjust chewing movements in their amplitude, but also in their variability.

The effect of unilateral lingual nerve injury on the kinematics of mastication in pigs.

OBJECTIVE: This study evaluates the effect of unilateral lingual sensory loss on the spatial and temporal dynamics of jaw movements during pig chewing. DESIGN: X-ray Reconstruction of Moving Morphology (XROMM) was used to reconstruct the 3-dimensional jaw movements of 6 pigs during chewing before and after complete unilateral lingual nerve transection. The effect of the transection were evaluated at the temporal and spatial level using Multiple Analysis of Variance. Temporal variables include gape cycle and phase durations, and the corresponding relative phase durations. Spatial variables include the amplitude of jaw opening, jaw yaw, and mandibular retraction-protraction. RESULTS: The temporal and spatial dynamics of jaw movements did not differ when chewing ipsilateral versus contralateral to the transection. When compared to pre-transection data, 4 of the 6 animals showed significant changes in temporal characteristics of the gape cycle following the transection, irrespective of chewing side, but the specific response to the lesion was highly dependent on the animal. On the other hand, in affected individuals the amplitude of jaw movements was altered similarly in all 3 dimensions: jaw opening and protraction-retraction increased whereas jaw yaw decreased. CONCLUSION: The variable impact of this injury in this animal model suggests that individuals use different compensatory strategies to adjust or maintain the temporal dynamics of the gape cycle. Because the amplitude of jaw movements are more adversely affected than their timing, results suggest that maintaining the tongue-jaw coordination is critical and this can come at the expense of bolus handling and masticatory performance.

Flexibility of feeding movements in pigs: effects of changes in food toughness and stiffness on the timing of jaw movements.

In mammals, chewing movements can be modified, or flexible, in response to changes in food properties. Variability between and within food in the temporal characteristics of chewing movements can impact chewing frequency and rhythmicity, which in turn may affect food breakdown, energy expenditure and tooth wear. Here, we compared total chewing cycle duration and intra-cycle phase durations in pigs chewing on three foods varying in toughness and stiffness: apples (low toughness, low stiffness), carrots (high toughness, low stiffness), and almonds (high toughness, high stiffness). We also determined whether within-food variability in timing parameters is modified in response to changes in food properties. X-ray Reconstruction Of Moving Morphology (XROMM) demonstrates that the timing of jaw movements are flexible in response to changes in food properties. Within each food, pigs also exhibited flexibility in their ability to vary cycle parameters. The timing of jaw movements during processing of high-toughness foods is more variable, potentially decreasing chewing rhythmicity. In contrast, low-toughness foods result in jaw movements that are more stereotyped in their timing parameters. In addition, the duration of tooth-food-tooth contact is more variable during the processing of low-stiffness foods compared with tough or stiff foods. Increased toughness is suggested to alter the timing of the movements impacting food fracture whereas increased stiffness may require a more cautious control of jaw movements. This study emphasizes that flexibility in biological movements in response to changes in conditions may not only be observed in timing but also in the variability of their timing within each condition.

Pelvic function in anuran jumping: Interspecific differences in the kinematics and motor control of the iliosacral articulation during take-off and landing.

Although the anuran pelvis is thought to be adapted for jumping, the function of the iliosacral joint has seen little direct study. Previous work has contrasted the basal "lateral-bender" pelvis from the "rod-like" pelvis of crown taxa hypothesized to function as a sagittal hinge to align the trunk with take-off forces. We compared iliosacral movements and pelvic motor patterns during jumping in the two pelvic types. Pelvic muscle activity patterns, iliosacral anteroposterior (AP) movements and sagittal bending of the pelvis during the take-off and landing phases were quantified in lateral bender taxa Ascaphus (Leiopelmatidae) and Rhinella (Bufonidae) and the rod-like Lithobates (Ranidae). All three species exhibit sagittal extension during take-off, therefore, both pelvic types employ a sagittal hinge. However, trunk elevation occurs significantly earlier in the anuran rod-like pelvis. Motor patterns confirm that the piriformis muscles depress the urostyle while the longissimus dorsi muscles elevate the trunk during take-off. However, the coccygeoiliacus muscles also produce anterior translation of the sacrum on the ilia. A new model illustrates how AP translation facilitates trunk extension in the lateral-bender anurans that have long been thought to have limited sagittal bending. During landing, AP translation patterns are similar because impact forces slide the sacrum from its posterior to anterior limits. Sagittal flexion during landing differs among the three taxa depending on the way the species land. AP translation during landing may dampen impact forces especially in Rhinella in which pelvic function is tuned to forelimb-landing dynamics. The flexibility of the lateral-bender pelvis to function in sagittal bending and AP translation helps to explain the retention of this basal configuration in many anurans. The novel function of the rod-like pelvis may be to increase the rate of trunk elevation relative to faster rates of energy release from the hindlimbs enabling them to jump farther. J. Morphol. 277:1539-1558, 2016. © 2016 Wiley Periodicals, Inc.

Functional evolution of jumping in frogs: Interspecific differences in take-off and landing.

Ancestral frogs underwent anatomical shifts including elongation of the hindlimbs and pelvis and reduction of the tail and vertebral column that heralded the transition to jumping as a primary mode of locomotion. Jumping has been hypothesized to have evolved in a step-wise fashion with basal frogs taking-off with synchronous hindlimb extension and crash-landing on their bodies, and then their limbs move forward. Subsequently, frogs began to recycle the forelimbs forward earlier in the jump to control landing. Frogs with forelimb landing radiated into many forms, locomotor modes, habitats, and niches with controlled landing thought to improve escape behavior. While the biology of take-off behavior has seen considerable study, interspecific comparisons of take-off and landing behavior are limited. In order to understand the evolution of jumping and controlled landing in frogs, data are needed on the movements of the limbs and body across an array of taxa. Here, we present the first description and comparison of kinematics of the hindlimbs, forelimbs and body during take-off and landing in relation to ground reaction forces in four frog species spanning the frog phylogeny. The goal of this study is to understand what interspecific differences reveal about the evolution of take-off and controlled landing in frogs. We provide the first comparative description of the entire process of jumping in frogs. Statistical comparisons identify both homologous behaviors and significant differences among species that are used to map patterns of trait evolution and generate hypotheses regarding the functional evolution of take-off and landing in frogs.

Effect of Postnatal Myostatin Inhibition on Bite Mechanics in Mice.

As a negative regulator of muscle size, myostatin (Mstn) impacts the force-production capabilities of skeletal muscles. In the masticatory system, measures of temporalis-stimulated bite forces in constitutive myostatin KOs suggest an absolute, but not relative, increase in jaw-muscle force. Here, we assess the phenotypic and physiologic impact of postnatal myostatin inhibition on bite mechanics using an inducible conditional KO mouse in which myostatin is inhibited with doxycycline (DOX). Given the increased control over the timing of gene inactivation in this model, it may be more clinically-relevant for developing interventions for age-associated changes in the musculoskeletal system. DOX was administered for 12 weeks starting at age 4 months, during which time food intake was monitored. Sex, age and strain-matched controls were given the same food without DOX. Bite forces were recorded just prior to euthanasia after which muscle and skeletal data were collected. Food intake did not differ between control or DOX animals within each sex. DOX males were significantly larger and had significantly larger masseters than controls, but DOX and control females did not differ. Although there was a tendency towards higher absolute bite forces in DOX animals, this was not significant, and bite forces normalized to masseter mass did not differ. Mechanical advantage for incisor biting increased in the DOX group due to longer masseter moment arms, likely due to a more anteriorly-placed masseter insertion. Despite only a moderate increase in bite force in DOX males and none in DOX females, the increase in masseter mass in males indicates a potentially positive impact on jaw muscles. Our data suggest a sexual dimorphism in the role of mstn, and as such investigations into the sex-specific outcomes is warranted.

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

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.

Morphology and fibre-type distribution in the tongue of the Pogona vitticeps lizard (Iguania, Agamidae).

Agamid lizards use tongue prehension for capturing all types of prey. The purpose of this study was to investigate the functional relationship between tongue structure, both surface and musculature, and function during prey capture in Pogona vitticeps. The lack of a detailed description of the distribution of fibre-types in the tongue muscles in some iguanian lizards has hindered the understanding of the functional morphology of the lizard tongue. Three methodological approaches were used to fill this gap. First, morphological analyses were performed (i) on the tongue surface through scanning electron microscopy, and (ii) on the lingual muscle by histological coloration and histochemistry to identify fibre-typing. Secondly, kinematics of prey capture was quantified by using high-speed video recordings to determine the movement capabilities of the tongue. Finally, electromyography (EMG) was used to identify the motor pattern tongue muscles during prey capture. Morphological and functional data were combined to discuss the functional morphology of the tongue in agamid lizards, in relation to their diet. During tongue protraction, M. genioglossus contracts 420 ± 96 ms before tongue-prey contact. Subsequently, Mm. verticalis and hyoglossus contract throughout tongue protraction and retraction. Significant differences are found between the timing of activity of the protractor muscles between omnivorous agamids (Pogona sp., this study) and insectivorous species (Agama sp.), despite similar tongue and jaw kinematics. The data confirm that specialisation toward a diet which includes more vegetal materials is associated with significant changes in tongue morphology and function. Histoenzymology demonstrates that protractor and retractor muscles differ in fibre composition. The proportion of fast glycolytic fibres is significantly higher in the M. hyoglossus (retractor muscle) than in the M. genioglossus (protractor muscle), and this difference is proposed to be associated with differences in the velocity of tongue protrusion and retraction (5 ± 5 and 40 ± 13 cm s(-1) , respectively), similar to Chamaeleonidae. This study provides a way to compare fibre-types and composition in all iguanian and scleroglossan lizards that use tongue prehension to catch prey.

Flexibility in locomotor-feeding integration during prey capture in varanid lizards: effects of prey size and velocity.

Feeding movements are adjusted in response to food properties, and this flexibility is essential for omnivorous predators as food properties vary routinely. In most lizards, prey capture is no longer considered to solely rely on the movements of the feeding structures (jaws, hyolingual apparatus) but instead is understood to require the integration of the feeding system with the locomotor system (i.e. coordination of movements). Here, we investigated flexibility in the coordination pattern between jaw, neck and forelimb movements in omnivorous varanid lizards feeding on four prey types varying in length and mobility: grasshoppers, live newborn mice, adult mice and dead adult mice. We tested for bivariate correlations between 3D locomotor and feeding kinematics, and compared the jaw-neck-forelimb coordination patterns across prey types. Our results reveal that locomotor-feeding integration is essential for the capture of evasive prey, and that different jaw-neck-forelimb coordination patterns are used to capture different prey types. Jaw-neck-forelimb coordination is indeed significantly altered by the length and speed of the prey, indicating that a similar coordination pattern can be finely tuned in response to prey stimuli. These results suggest feed-forward as well as feed-back modulation of the control of locomotor-feeding integration. As varanids are considered to be specialized in the capture of evasive prey (although they retain their ability to feed on a wide variety of prey items), flexibility in locomotor-feeding integration in response to prey mobility is proposed to be a key component in their dietary specialization.

Jaw and hyolingual movements during prey transport in varanid lizards: effects of prey type.

The ability to modulate feeding kinematics in response to prey items with different functional properties is likely a prerequisite for most organisms that feed on a variety of food items. Variation in prey properties is expected to reveal variation in feeding function and the functional role of the different phases in a transport cycle. Here we describe the kinematics of prey transport of two varanid species, Varanus niloticus and Varanus ornatus. These species were selected for analysis because of their highly specialised hyolingual system and food transport mechanism (inertial food transport). In these animals, tongue and hyoid movements are expected to make no, or only a minor, contribution to prey transport. We observed statistically significant prey type effects that could be associated with prey properties such as mass, size and mobility. These data show that both species are capable of modulating the kinematics of food transport in response to different prey types. Moreover, not only the kinematics of the jaws were modulated in response to prey characteristics but also the anterior/posterior movements of the tongue and hyoid. This suggests a more important role of the tongue and hyolingual movements in these animals than previously suspected. In contrast, head movements were rather stereotyped and were not modulated in response to changes in prey type.

Mandibular corpus bone strains during mastication in goats (Capra hircus): a comparison of ingestive and rumination chewing.

OBJECTIVE: To compare the mechanical loading environment of the jaw in goats during ingestive and rumination chewing. DESIGN: Rosette strain gauges were attached to the external surface of the mandibular corpus in five goats to record bone strains during the mastication of hay and rumination. RESULTS: Strain magnitudes and maximum physiological strain rates during the mastication of hay are significantly higher than during rumination chewing on the working and balancing sides. Principal strain ratios and orientations are similar between the two chewing behaviours. Loading and chewing cycle duration are all longer during rumination chewing, whereas chew duty factor and variances in load and chewing cycle durations are higher during ingestive chewing. For most of the variables, differences in strain magnitudes or durations are similar at all three gauge sites, suggesting that rumination and ingestive chewing do not differentially influence bone at the three gauge sites. CONCLUSIONS: Despite lower strain magnitudes, the repetitive nature of rumination chewing makes it an important component of the mechanical loading environment of the selenodont artiodactyl jaw. However, similarities in principal strain orientations and ratios indicate that rumination chewing need not be considered as a unique loading behaviour influencing the biomechanics of the selenodont artiodactyl jaw. Differences in loading and chewing cycle durations during rumination and ingestion demonstrate flexibility in adult chewing frequencies. Finally, although the low within-sequence variability in chewing cycle durations supports the hypothesis that mammalian mastication is energetically efficient, chewing during rumination may not be more efficient than during ingestion.

Separating the effects of prey size and speed on the kinematics of prey capture in the omnivorous lizard Gerrhosaurus major.

Feeding behavior is known to be modulated as prey properties change. During prey capture, external prey properties, including size and mobility, are likely some of the most important components in predator-prey interactions. Whereas prey size has been demonstrated to elicit modulation of jaw movements during capture, how prey speed affects the approach and capture of prey remains unknown. We quantified the kinematics associated with movements of both the feeding and locomotor systems during prey capture in a lizard, Gerrhosaurus major, while facing prey differing in size and mobility (newborn mice, grasshoppers, and mealworms). Our data show that the feeding and locomotor systems were recruited differently in response to changes in the size or speed of the prey. The timing of jaw movements and of the positioning of the head are affected by changes in prey size-and speed, to a lesser extent. Changes in prey speed resulted in concomitant changes in the speed of strike and an early and greater elevation of the neck. External prey properties, and prey mobility in particular, are relevant in predator-prey interactions and elicit specific responses in different functional systems.

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

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.