Jaw Prehension Research Articles

Using salamanders as model taxa to understand vertebrate feeding constraints during the late Devonian water-to-land transition.

The vertebrate water-to-land transition and the rise of tetrapods brought about fundamental changes for the groups undergoing these evolutionary changes (i.e. stem and early tetrapods). These groups were forced to adapt to new conditions, including the distinct physical properties of water and air, requiring fundamental changes in anatomy. Nutrition (or feeding) was one of the prime physiological processes these vertebrates had to successfully adjust to change from aquatic to terrestrial life. The basal gnathostome feeding mode involves either jaw prehension or using water flows to aid in ingestion, transportation and food orientation. Meanwhile, processing was limited primarily to simple chewing bites. However, given their comparatively massive and relatively inflexible hyobranchial system (compared to the more muscular tongue of many tetrapods), it remains fraught with speculation how stem and early tetrapods managed to feed in both media. Here, we explore ontogenetic water-to-land transitions of salamanders as functional analogues to model potential changes in the feeding behaviour of stem and early tetrapods. Our data suggest two scenarios for terrestrial feeding in stem and early tetrapods as well as the presence of complex chewing behaviours, including excursions of the jaw in more than one dimension during early developmental stages. Our results demonstrate that terrestrial feeding may have been possible before flexible tongues evolved. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

On the amphibious food uptake and prey manipulation behavior in the Balkan-Anatolian crested newt (Triturus ivanbureschi, Arntzen and Wielstra, 2013)

Feeding behavior in salamanders undergoing seasonal habitat shifts poses substantial challenges caused by differences in the physical properties of air and water. Adapting to these specific environments, urodelans use suction feeding predominantly under water as opposed to lingual food prehension on land. This study aims to determine the functionality of aquatic and terrestrial feeding behavior in the Balkan-Anatolian crested newt (Triturus ivanbureschi) in its terrestrial stage. During the terrestrial stage, these newts feed frequently in water where they use hydrodynamic mechanisms for prey capture. On land, prey apprehension is accomplished mainly by lingual prehension, while jaw prehension seems to be the exception (16.67%) in all terrestrial prey capture events. In jaw prehension events there was no detectable depression of the hyo-lingual complex. The success of terrestrial prey capture was significantly higher when T. ivanbureschi used lingual prehension. In addition to prey capture, we studied the mechanisms involved in the subduction of prey. In both media, the newts frequently used a shaking behavior to immobilize the captured earthworms. Apparently, prey shaking constitutes a significant element in the feeding behavior of T. ivanbureschi. Prey immobilization was applied more frequently during underwater feeding, which necessitates a discussion of the influence of the feeding media on food manipulation. We also investigated the osteology of the cranio-cervical complex in T. ivanbureschi to compare it to that of the predominantly terrestrial salamandrid Salamandra salamandra.

Underwater and Terrestrial Feeding in the Sri Lankan Wart-Frog, Lankanectes corrugatus

The vast majority of the world’s anurans feed terrestrially, with aquatic prey capture having been observed in only a handful of species. We tested the predation behaviour of the strictly aquatic ‘fanged’ frog Lankanectes corrugatus (Nyctibatrachidae) by providing specimens with both aquatic and terrestrial feeding opportunities. The frogs successfully captured prey both underwater and on land adjacent to water. During underwater feeding they located prey purely by tactile stimuli rather than by vision; prey were scooped into the open mouth using both hands. When feeding terrestrially, however, the frogs relied on visual cues alone when attacking prey, capturing prey items by lunging at them, grasping and scooping with the hands. Oral suction and tongue or jaw prehension were not observed in prey capture whether underwater or on land, and the 'fangs' do not appear to play a role in prey capture or ingestion.Ceylon Journal of Science (Bio. Sci.) 43 (2): 79-82, 2014

Hit or miss: Functional mechanisms underlying prey capture efficiency in three cordylid lizards

Prey capture is one of the most important behaviours in organisms as it directly determines energy acquisition, which in turn is vital for fitness and survival. The contribution of specific prey capture mechanisms to prey capture efficiency, however, remains largely unresolved, especially in groups where a variety of mechanisms is present, such as lizards. Using three sympatric cordylid lizards as model organisms, we investigated (1) the effect of lingual prehension on prey capture efficiency when feeding on small prey (i.e. termites) and (2) whether in species that use jaw prehension to capture prey, prey capture efficiency decreases with increasing predator-prey size ratio. Prey capture efficiency, defined as the proportion of termites that was captured at first attempt, was higher in the species using lingual prehension than in the similarly-sized species using jaw prehension. In contrast, the two species using jaw prehension had a similar prey capture efficiency, despite differences in body size. The observed variation in prey capture efficiency between lingual and jaw prehension is discussed in the light of foraging mode in lizards.

Influence of diet on prehension mode in cordylid lizards: a morphological and kinematic analysis

AbstractLizards exhibit a variety of mechanisms to capture prey, including lingual prehension, jaw prehension and lingual pinning. Despite being the topic of numerous studies, the link between prehension mode and diet remains poorly understood, especially in clades where multiple prehension modes are present. We addressed this issue by comparing the feeding behaviour and tongue morphology of a termite‐eating specialist Ouroborus cataphractus with that of a closely related dietary generalist Karusasaurus polyzonus. We used high‐speed videography to test the effect of prey species (termite vs. small cricket) and prey size (small vs. large cricket) on prehension mode. In addition, we included several other cordylid lizards representing the major clades in the family into our analysis to examine whether the prehension modes present in O. cataphractus characterize all cordylid species or whether they represent isolated occurrences. Finally, we investigated the morphology of the tongue in Cordylidae, with emphasis on O. cataphractus and K. polyzonus, using light and scanning electron microscopy techniques. Our data showed that the consumption of termites in O. cataphractus has resulted in the evolution of a novel lingual prehension mode, during which the ventral surface of the tongue is used to apprehend prey. This is in contrast to other lizards, which use the dorsal surface of the tongue to contact prey. Moreover, we demonstrated that this novel lingual prehension mode is accompanied by distinct morphological elaborations of the tongue surface. None of the other cordylid lizards tested in our study used lingual prehension during prey capture, except K. polyzonus, which used the tongue in a very small percentage of feeding trials. Overall, this study suggests that dietary specialization might underlie the evolution of novel prehension mechanisms in lizards.

Prey capture in lizards: differences in jaw-neck-forelimb coordination

607..622 Although prey capture is thought to be based on the coordinated movements of the jaw and locomotor apparatus (i.e. the vertebral column and the limbs), jaw–neck–forelimb coordination has never been compared among related species. The kinematics of jaw, neck, and forelimb movements were recorded in lizards that use jaw prehension: Gerrhosaurus major, Tupinambis merianae, Varanus niloticus, and Varanus ornatus. These species provide a comparative framework to discuss the influence of morphological differences and ecological convergence on the jaw–neck–forelimb coordination patterns. Jaw–neck–forelimb coordination was quantified by determining whether maximum neck elevation and maximum forelimb flexion are synchronized with either the start of jaw opening or maximum gape. Significant differences in the jaw–neck–forelimb coordination pattern among species were observed, with maximum neck elevation being synchronized with the start of jaw opening in varanids, whereas in T. merianae and G. major, it is achieved closer to maximum gape. Differences in locomotor–feeding integration are suggested to be related to dietary specializations, and as such may play a role in feeding adaptation. The jaw–neck–forelimb coordination pattern used by varanids may indeed be advantageous to prepare a quick strike triggered from further away, providing a critical advantage when feeding on evasive prey. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 607–622.

Prey capture in frogs: alternative strategies, biomechanical trade‐offs, and hierarchical decision making

Frogs exhibit flexible repertoires of prey-capture behavior, which depend primarily on visual analysis of prey attributes. We review three examples of how visual cues are used to modulate prey-capture strategies. (1) Dyscophus guineti modulates tongue aiming in response to prey location. These frogs turn only their heads to apprehend prey located at azimuths <40°. At azimuths >40°, the frogs switch from this strategy to one in which both head and tongue are aimed toward prey. (2) Rana pipiens modulates its feeding behavior in response to prey size, using tongue prehension for capturing small prey but switching to jaw prehension to capture large prey. (3) In Cyclorana novaehollandiae, visual processing of prey attributes involves hierarchical decision making. These frogs first assess prey size. For large prey, they ignore velocity but not shape. For small prey, they ignore shape but not velocity. Alternative prey-capture strategies are associated with biomechanical trade-offs that result from the interaction between the feeding apparatus and varying attributes of prey. Alternative strategies likely exist because biomechanical constraints prevent any one strategy from being effective over a range of prey attributes. Taken together, these studies emphasize the requirement that predators must somehow tune prey-capture kinematics simultaneously to multiple attributes of prey. In frogs, the choice among alternative prey-capture strategies involves a hierarchical decision-making process. Hierarchical decision making is expected to be widespread among animals. However, no previous studies were found except for humans, who frequently use this type of approach to make complex decisions.

Locomotor–feeding coupling during prey capture in a lizard(Gerrhosaurus major): effects of prehension mode

In tetrapods, feeding behaviour in general, and prey capture in particular, involves two anatomical systems: the feeding system and the locomotor system. Although the kinematics associated with the movements of each system have been investigated in detail independently, the actual integration between the two systems has received less attention. Recently, the independence of the movements of the jaw and locomotor systems was reported during tongue-based prey capture in an iguanian lizard (Anolis carolinensis), suggesting a decoupling between the two systems. Jaw prehension, on the other hand, can be expected to be dependent on the movements of the locomotor system to a greater degree. To test for the presence of functional coupling and integration between the jaw and locomotor systems, we used the cordyliform lizard Gerrhosaurus major as a model species because it uses both tongue and jaw prehension. Based on a 3-D kinematic analysis of the movements of the jaws, the head, the neck and the forelimbs during the approach and capture of prey, we demonstrate significant correlations between the movements of the trophic and the locomotor systems. However, this integration differs between prehension modes in the degree and the nature of the coupling. In contrast to our expectations and previous data for A. carolinensis, our data indicate a coupling between feeding and locomotor systems during tongue prehension. We suggest that the functional integration between the two systems while using the tongue may be a consequence of the relatively slow nature of tongue prehension in this species.

Cranial morphology and ontogeny of the Permo-Carboniferous temnospondyl Archegosaurus decheni Goldfuss, 1847 from the Saar–Nahe Basin, Germany

ABSTRACTMorphology and ontogenetic changes in the skull and hyobranchium of the Permo-Carboniferous temnospondyl Archegosaurus decheni from the Saar–Nahe Basin (SW Germany) are described in detail, based on 181 skulls ranging from 18 to 279 mm in length. Three-dimensional skull reconstructions including the palate of different growth stages are provided. The extremely elongate choanae and up to four median symphyseal teeth are unique to A. decheni. Among neurocranial elements, the exoccipital is well ossified and forms the paroccipital process as in stereospondyls. The shaft of the stapes which projects into the squamosal embayment grows with positive allometry and possesses a distinct lateral process. The basibranchial is well ossified in adults and exhibits a complex, spoon-like morphology. Small larvae were euryphagous and used non-directed suction and jaw prehension during prey capture. Larger larvae and adults were mainly ichthyophagous, as is indicated by the increasingly elongated snout, differentiation of marginal teeth, and nutrition remains. After a prolonged larval period, juvenile and adult A. decheni remained in the aquatic habitat, as suggested by the presence of lateral line sulci, the ‘aquatic type’ of septomaxilla and choana, and the absence of a nasolacrimal duct.

Metamorphosis and evolution of feeding behaviour in salamanders of the family Plethodontidae

Plethodontid salamanders capture prey with enhanced tongue protraction relative to other salamander taxa, yet metamorphosing plethodontids are hypothesized to be constrained relative to direct-developing plethodontids in their degree of tongue evolution (protraction length and velocity) by the presence of a larval stage in development. In this biphasic life history the hyobranchial apparatus serves the conflicting functions of larval suction feeding and adult tongue protraction. The deletion of the larval stage removes one of the conflicting functions and has thus permitted direct-developing plethodontids to circumvent this constraint and evolve extremely long tongues, which in some species can be projected to 80% of body length. To evaluate this constraint hypothesis and explore taxonomic diversity of feeding behaviours, we studied feeding in larvae, adults and metamorphosing individuals of seven species of metamorphosing plethodontids from the basal taxa Desmognathinae and Hemidactyliini using direct observations, high-speed videography and kinematic analysis. We found that larval plethodontids suction feed, but feeding is suspended entirely during metamorphosis, and aquatic adults do not suction feed. Adults have exapted the terrestrial modes of tongue and jaw prehension for aquatic prey capture. These findings substantiate the premise that suction feeding and tongue protraction are conflicting functions, and thus our results support the constraint hypothesis. Plethodontid adults have evolved their extreme tongue protraction ability at the expense of adult suction feeding. The rapid metamorphosis that characterizes plethodontids may be an adaptation that minimizes the non-feeding period imposed by the evolution of derived tongue protraction in adults.

Prey Capture Behavior in the Blue-Tongued Skink, Tiliqua scincoides

Squamate prey capture evolved in two general directions; one toward an emphasis upon lingual prehension and the other toward an emphasis upon jaw prehension. In basal squamates (Iguania) lingual prehension characterizes prey capture. All other squamates (Scleroglossa) tend to use their jaws for prey prehension and the role of the tongue as a prehensile organ is reduced. However, within some scleroglossan lizards, lingual and jaw modes of prehension are present Selection of a distinct prehension mode during a feeding bout in these lizards has been hypothesized to be related to prey size. To test for the presence of lingual prehension and correlation with prey size, we examined feeding behavior in the blue-tongued skink, Tiliqua scincoides using two prey types (mealworm and cricket). We confirmed that this skink uses both lingual and jaw modes of prehension with accompanying characteristic jaw kinematic profiles. With crickets, only jaw prehension was exhibited, but both modes were used when feeding on equivalently sized prey, mealworms. Consequently, prehension mode is not exclusively elicited by prey size. We, therefore, hypoth- esize that selection of prehension modes, lingual or jaws, in these basal scleroglossans also includes prox- imate factors related to prey behavior.

Sensory modulation and behavioral choice during feeding in the Australian frog, Cyclorana novaehollandiae.

This study investigates how visual and tactile sensory information, as well as biomechanical effects due to differences in physical characteristics of the prey, influence feeding behavior in the frog Cyclorana novaehollandiae. Video motion analysis was used to quantify movement patterns produced when feeding on five prey types (termites, waxworms, crickets, mice and earthworms). Twelve kinematic variables differed significantly among prey types, and twelve variables were correlated with prey characteristics (including mass, length, height and velocity of movement). Results indicate that C. novaehollandiae uses a different strategy to capture each prey type. Visual assessment of prey characteristics appeared to be more important in modulating feeding behavior that tactile cues or biomechanical effects. We propose a hierarchical hypothesis of behavioral choice, in which decisions are based primarily on visual analysis of prey characteristics. In this model, the frogs first choose between jaw prehension and tongue prehension based on prey size. If they have chosen jaw prehension, they next choose between upward or downward head rotation based on length and height of the prey. If they have chosen tongue prehension, they next choose between behavior for fast and slow prey. Final decisions may be the result of behavioral fine tuning based on tactile feedback.

The roles of visual and proprioceptive information during motor program choice in frogs.

Previous studies have shown that leopard frogs, Rana pipiens, use tongue prehension to capture small prey and jaw prehension to capture large prey. After hypoglossal nerve transection, the frogs fail to open their mouths when attempting to feed on small prey, but open their mouths and capture large prey. Here, we investigate how visual information about the prey and proprioceptive information from the tongue interact to influence the motor program choice. Using pieces of earthworm of various sizes, we found that Rana exhibits two different behavior patterns based on prey size. The frogs captured the 1.5-cm prey using tongue prehension, whereas 2.0-cm and larger prey were captured using jaw prehension. After hypoglossal transection, the frogs never opened their mouths when they tried to feed on 1.5-cm prey. When feeding on 3.0-cm and larger prey after transection, they always opened their mouths and captured the prey using jaw prehension. When offered 2.0-cm prey, they alternated randomly between opening and not opening the mouth. Therefore, deafferentation changed the pattern of motor program choice at the behavioral border. This implies that afferents from the tongue interact with visual input to influence motor program choice.

Modulation of prey‐capture behavior in Plethodon cinereus (Green) (Amphibia: Caudata)

AbstractMany feeding kinematic studies do not identify sources of mechanical variation related to the type or size of prey. Studies of salamanders have concentrated on determining the morphological basis of feeding mechanics or on phylogenetic comparisons; few have examined variability within a species. A series of feeding trials was designed to test whether Plethodon cinereus of different age/size classes exhibits stereotypic patterns in capturing prey of differing type and size. Stopframe video analyses of feedings were made using 19 salamanders of varying body size and four prey types chosen to resemble items in the natural diet of the species. Five morphological features of each salamander, length and width of prey items, and 15 kinematic variables were used to describe each feeding trial.Statistical analyses of kinematic and morphological variables show that the feeding behavior of this species varies significantly with prey type. Effects of salamander size and prey size within prey types were a source of variation in some kinematic variables; among‐individual variation partitioned with salamander body size. Different feeding modes resulted from distinctive combinations of distances from prey, amount of tongue protrusion, body movements, and duration of mouth closure, which varied with the use of jaw prehension and lingual prey capture. Presence of a repertoire of behaviors, composed of versatile combinations of movements, suggests that Plethodon cinereus modulates feeding mechanics to capture different types of prey. Consideration of natural prey in experiments, and of prey type in comparisons made across taxa, are necessary to investigations of the evolution of feeding behaviors. © 1995 Wiley‐Liss, Inc.

Feeding behaviour in two scleroglossan lizards: Lacerta viridis (Lacertidae) and Zonosaurus laticaudatus (Cordylidae)

This paper deals with a description of feeding phases in the scleroglossan lizard Zonosaurus laticaudatus by using high‐speed cinematography. Capture modes are compared with Lacerta viridis. Z. laticaudatus uses the tongue for capturing small prey while both species use jaw prehension for large prey. L. viridis always uses jaw prehension for small prey.

The Modulation of Feeding Behavior in Response to Prey Type in the Frog Rana Pipiens

ABSTRACT Using high-speed video motion analysis, the kinematics of feeding behavior was studied in Rana pipiens. Rana pipiens exhibits differing behavior patterns depending upon prey type. When feeding on small prey such as waxworms, R. pipiens uses tongue protraction to catch prey, minimizing head and body movements. When feeding on the larger earthworm, it arches its body, flexes the head downwards and uses jaw prehension to capture the prey. Time to completion of tongue retraction, time to completion of mouth closing, duration of tongue retraction, duration of mouth closing, total time that the mouth is open and maximum tongue reach were significantly longer during waxworm feedings than during earthworm feedings. The tongue angle and degree of head flexion were significantly greater during earthworm feedings. These different kinematic patterns correspond to differences in feeding behavior among major taxa of anurans. Phylogenetically primitive archaeobatrachian frogs have short tongues which can be protracted only a few millimeters. In contrast, many neobatrachians have long tongues which they project to catch small prey. The similarity between the behavior that neobatrachians use to catch large prey and the movement patterns of archaeobatrachians suggests that Rana pipiens has retained the plesiomorphic archaeobatrachian motor pattern and uses it to catch large prey, while evolving a new motor pattern for catching small prey.