Feeding in Atractaspis (Serpentes: Atractaspididae): a study in conflicting functional constraints

African fossorial colubroid snakes of the genus Atractaspis have relatively long fangs on short maxillae, a gap separating the pterygoid and palatine bones, a toothless pterygoid, and a snout tightly attached to the rest of the skull. They envenomate prey with a unilateral backward stab of one fang projected from a closed mouth. We combined structural reanalysis of the feeding apparatus, video records of prey envenomation and transport, and manipulations of live and dead Atractaspis to determine how structure relates to function in this unusual genus of snakes. Unilateral fang use in Atractaspis is similar to unilateral slashing envenomation by some rear-fanged snakes, but Atractaspis show no maxillary movement during prey transport. Loss of pterygoid teeth and maxillary movement during transport resulted in the inability to perform. 'pterygoid walk' prey transport. Atractaspis transport prey through the oral cavity using movement cycles in which mandibular adduction, anterior trunk compression, and ventral flexion of the head alternate with mandibular abduction and extension of head and anterior trunk over the prey. Inefficiencies in manipulation and early transport of prey are offset by adaptability of the envenomating system to various prey types in both enclosed and open spaces and by selection of prey that occupy burrows or tunnels in soil. Atractaspis appears to represent the evolutionary endpoint of a functional conflict between envenomation and transport in which a rear-fanged envenomating system has been optimized at the expense of most, if not all, palatomaxillary transport function.     

Post-cranial prey transport mechanisms in the black pinesnake, Pituophis melanoleucus lodingi: an x-ray videographic study

Most previous studies of snake feeding mechanisms have focused on the functional morphology of the highly specialized ophidian jaw apparatus. Although some of these studies have included observations of post-cranial movements during feeding, the functional roles of these movements have remained poorly understood. In this study, we used x-ray videography to examine post-cranial prey transport mechanisms in a colubrid snake, Pituophis melanoleucus lodingi. We found that prey transport in this species progresses through four distinct phases, three of which are characterized by either undulatory or concertina-like movements of the anterior portion of the trunk. In the first phase of transport (the oral phase), unilateral movements of the jaws are used to pull the head forward around the prey. In the second phase (the orocervical phase), unilateral jaw movements continue, but are augmented by concertina-like movements of the anterior portion of the trunk. In the third phase (the cervical phase), prey transport occurs exclusively through concertina-like movements of the neck. Finally, in the fourth phase (the thoracic phase), prey is transported to the stomach via undulatory movements of the trunk. Our observations of feeding behavior in a phylogenetically diverse sample of fourteen other snake species demonstrate that similar post-cranial transport mechanisms are used by a wide variety of alethinophidian snakes that feed on large, bulky prey.     

Prey Transport Mechanisms in Blindsnakes and the Evolution of Unilateral Feeding Systems in Snakes

Most snakes ingest and transport their prey via a jaw ratchetingmechanism in which the left and right upper jaw arches are advancedover the prey in an alternating, unilateral fashion. This unilateraljaw ratcheting mechanism differs greatly from the hyolingualand inertial transport mechanisms used by lizards, both of whichare characterized by bilaterally synchronous jaw movements.Given the well-corroborated phylogenetic hypothesis that snakesare derived from lizards, this suggests that major changes occurredin both the morphology and motor control of the feeding apparatusduring the early evolution of snakes. However, most previousstudies of the evolution of unilateral feeding mechanisms insnakes have focused almost exclusively on the morphology ofthe jaw apparatus because there have been very few direct observationsof feeding behavior in basal snakes. In this paper I describethe prey transport mechanisms used by representatives of twofamilies of basal snakes, Leptotyphlopidae and Typhlopidae.In Leptotyphlopidae, a mandibular raking mechanism is used,in which bilaterally synchronous flexions of the lower jaw serveto ratchet prey into and through the mouth. In Typhlopidae,a maxillary raking mechanism is used, in which asynchronousratcheting movements of the highly mobile upper jaws are usedto drag prey through the oral cavity. These findings suggestthat the unilateral feeding mechanisms that characterize themajority of living snakes were not present primitively in Serpentes,but arose subsequently to the basal divergence between Scolecophidiaand Alethinophidia.     

The function of the intramaxillary joint in the Round Island boa, Casarea dussumieri

The bolyeriid snakes Casarea dussumieri and Bolyeria multocarinata are unique among vertebrates in possessing an intramaxillary joint that separates the maxilla into anterior and posterior segments. In contrast to previous studies, which suggest that this joint permits enhanced elevation of the anterior maxillary teeth, our films of live Casarea show that the snout and anterior maxillary teeth are actively depressed 15° 20° below rest position through bilateral retraction of the palatomaxillary arches. Patterns of bone movement in living Casarea support the hypothesis that a caudally directed force is transmitted to the snout via the medial bones of the palatomaxillary arch, suggesting functional affinities between Casarea and higher henophidians.
The intramaxillary joint, in conjunction with the curvature of the mandibles, allows the jaws of Casarea to encircle hard, cylindrical prey held transversely in the mouth. Because the Mauritian terrestrial vertebrate fauna lacks mammals and is dominated by skinks and geckos, which Casarea is known to consume, we suggest that the intramaxillary joint functions in a manner analogous to that achieved by quite different maxillary modifications in colubrid scincivores. Although the origin of the bolyeriid intramaxillary joint remains unclear, its structural refinement and evolutionary stability may be due to selection pressures arising from limited prey diversity.     

Effects of dissociating agents on the fine structure of embryonic chick thyroid cells

Heads of the boid snakes Python sebae and Python molurus were dissected and the arthrology, myology and dentition studied. Living specimens of these species were observed and their feeding behavior analyzed by means of high- and regular-speed motion pictures. Camera speeds of up to 400 frames per second permitted examination of the jaw movements during the striking and seizing of prey. Motion picture studies conducted at regular speeds provided information on cranial movements during the swallowing of prey. The morphology of the head was correlated with observed movements in an attempt to analyze the functional and adaptive implications of the jaw apparatus. The cranial apparatus was discussed in terms of a linkage or kinematic chain whose constrainment and degrees of freedom were examined and compared with the jaw linkage of lizards. It was concluded that the very rigidly constrained mechanism in lizards is in remarkably sharp contrast to the very loose apparatus in snakes. Motions of various cranial bones were analyzed with particular attention given the mechanical factors involved. In full protraction the maxillae and palatines are lifted and rotated outward about a longitudinal axis. These movements are important in orienting the teeth with respect to the prey and are related to seizing and swallowing.     

The functional meaning of “prey size” in water snakes (Nerodia fasciata, Colubridae)

The evolutionary success of macrostomatan (enlarged-gape) snakes has been attributed to their ability to consume large prey, in turn made possible by their highly kinetic skulls. However, prey can be “large” in several ways, and we have little insight into which aspects of prey size and shape affect skull function during feeding. We used X-ray videos of broad-banded water snakes (Nerodia fasciata) feeding on both frogs and fish to quantify movements of the jaw elements during prey transport, and of the anterior vertebral column during post-cranial swallowing. In a sample of additional individuals feeding on both frogs and fish, we measured the time and the number of jaw protractions needed to transport prey through the buccal cavity. Prey type (fish vs. frog) did not influence transport kinematics, but did influence transport performance. Furthermore, wider and taller prey induced greater movements of most cranial elements, but wider prey were transported with significantly less anterior vertebral bending. In the performance trials, heavier, shorter, and wider prey took significantly more time and a greater number of jaw protractions to ingest. Thus, the functional challenges involved in prey transport depend not only upon prey mass, but also prey type (fish vs. frog) and prey shape (relative height, width and length), suggesting that from the perspective of a gape-limited predator, the difficulty of prey ingestion depends upon multiple aspects of prey size.     

Functional morphology of the pharyngeal jaw apparatus in moray eels

Moray eels (Muraenidae) are a relatively large group of anguilliform fishes that are notable for their crevice-dwelling lifestyle and renowned for their ability to consume large prey. Morays apprehend their prey by biting and then transport prey by extreme protraction and retraction of their pharyngeal jaw apparatus. Here, we present a detailed interpretation of the mechanisms of pharyngeal jaw transport based on work with Muraena retifera. We also review what is known of the moray pharyngeal jaw apparatus from the literature and provide comparative data on the pharyngeal jaw elements and kinematics for other moray species to determine whether interspecific differences in morphology and behavior are present. Rather than comprising broad upper and lower processing tooth plates, the pharyngeal jaws of muraenine and uropterygiine morays, are long and thin and possess large, recurved teeth. Compared with the muraenines, the pharyngobranchials of the uropterygiines do not possess a horn-shaped process and their connection to the fourth epibranchial is dorsal rather than medial. In addition, the lower tooth plates do not exhibit a lateral groove that serves as a site of muscle attachment for the pharyngocleitheralis and the ventral rather than the lateral side of the lower tooth plate attaches to the fourth ceratobranchial. In all morays, the muscles positioned for protraction and retraction of the pharyngeal apparatus have undergone elongation, while maintaining the generalized attachment sites on the bones of the skull and axial skeleton. Uropterygiines lack a dorsal retractor muscle and we presume that retraction of the pharyngeal jaws is achieved by the pharyngocleitheralis and the esophagus. The fifth branchial adductor is greatly hypertrophied in all species examined, suggesting that morays can strongly adduct the pharyngeal jaws during prey transport. The kinematics of biting behavior during prey capture and transport resulted in similar magnitudes of cranial movements although the timing of kinematic events was significantly different and the duration of transport was twice as long as prey capture. We speculate that morays have evolved this alternative prey transport strategy as a means of overcoming gape constraints, while hunting in the confines of coral reefs.     

Functional morphology of the palato‐maxillary apparatus in “Palatine dragging” snakes (Serpentes: Elapidae: Acanthophis,Oxyuranus)

Elapid snakes have previously been divided into two groups (palatine erectors and palatine draggers) based on the morphology and inferred movements of their palatine bone during prey transport (swallowing). We investigated the morphology and the functioning of the feeding apparatus of several palatine draggers (Acanthophis antarcticus, Oxyuranus scutellatus, Pseudechis australis) and compared them to published records of palatine erectors. We found that the palatine in draggers does not move as a straight extension of the pterygoid as originally proposed. The dragger palato‐pterygoid joint flexes laterally with maxillary rotation when the mouth opens and the jaw apparatus is protracted and slightly ventrally during mouth closing. In contrast, in palatine erectors, the palato‐pterygoid joint flexes ventrally during upper jaw protraction. In draggers, the anterior end of the palatine also projects rostrally during protraction, unlike the stability of the anterior end seen in erectors. Palatine draggers differ from palatine erectors in four structural features of the palatine and its relationships to surrounding elements. The function of the palato‐pterygoid bar in both draggers and erectors can be explained by a typical colubroid muscle contraction pattern, which acts on a set of core characters shared among all derived snakes. Although palatine dragging elapids share a fundamental design of the palato‐maxillary apparatus with all higher snakes, they provide yet another demonstration of minor structural modifications producing functional variants. J. Morphol. 2010. © 2009 Wiley‐Liss, Inc.     

Cephalic anatomy of the rare Indonesian snake Anomochilus weberi

The head of Anomochilus weberi combines features seen in living uropeltines and scolecophidians, two clades of fossorial snakes that appear to have the most specialized and, at the same time, the most divergent modifications of the head. However, the weakly supported premaxilla of Anomochilus departs from both scolecophidian and uropeltine modes of reinforcing the anterior tip of the snout, suggesting that Anomochilus is a less specialized burrower. Its skull also has a number of features unusual among snakes, including a unique buttress on the anterior ends of the septomaxillae, an ectopterygoid reduced to a splint that touches neither maxilla nor pterygoid, a short maxillary tooth row oriented at 45° to the long axis of the skull, and a braincase and snout complex that are uniformly wide. The features of the upper jaw are predicted to confer behavioural and mechanical attributes intermediate between those of typhlopid scolecophidians and uropeltines.     

Specializations of the Body Form and Food Habits of Snakes

Viperid snakes have stouter bodies, larger heads, and longerjaws than snakes in other families; there are no major differencesbetween the two subfamilies of vipers in these features. A suiteof morphological characters that facilitates swallowing largeprey finds its greatest expression among vipers, but certainelapid and colubrid snakes have converged upon the same bodyform. The number of jaw movements required to swallow prey islinearly related to the size of a prey item when shape is heldconstant. Very small and very large prey are not disproportionatelydifficult for a snake to ingest. Vipers swallow their prey withfewer jaw movements than do colubrids or boids and can swallowprey that is nearly three times larger in relation to theirown size. Proteolytic venom assists in digestion of prey, andmelanin deposits shield the venom glands from light that woulddegrade the venom stores. Ancillary effects of the morphologicalfeatures of vipers, plus the ability to ingest a very largequantity of food in one meal, should produce quantitative andqualitative differences in the ecology and behavior of vipersand other snakes.     

Burrowing with a kinetic snout in a snake (Elapidae: Aspidelaps scutatus)

Of the few elongate, fossorial vertebrates that have been examined for their burrowing mechanics, all were found to use an akinetic, reinforced skull to push into the soil, powered mostly by trunk muscles. Reinforced skulls were considered essential for head‐first burrowing. In contrast, I found that the skull of the fossorial shield‐nosed cobra (Aspidelaps scutatus ) is not reinforced and retains the kinetic potential typical of many non‐fossorial snakes. Aspidelaps scutatus burrows using a greatly enlarged rostral scale that is attached to a kinetic snout that is independently mobile with respect to the rest of the skull. Two mechanisms of burrowing are used: (1) anteriorly directed head thrusts from a loosely bent body that is anchored against the walls of the tunnel by friction, and (2) side‐to‐side shovelling using the head and rostral scale. The premaxilla, to which the rostral scale is attached, lacks any direct muscle attachments. Rostral scale movements are powered by, first, retractions of the palato‐pterygoid bar, mediated by a ligament that connects the anterior end of the palatine to the transverse process of the premaxilla and, second, by contraction of a previously undescribed muscle slip of the m. retractor pterygoidei that inserts on the skin at the edge of the rostral scale. In derived snakes, palatomaxillary movements are highly conserved and power prey capture and transport behaviors. Aspidelaps scutatus has co‐opted those mechanisms for the unrelated function of burrowing without compromising the original feeding functions, showing the potential for evolution of functional innovations in highly conserved systems.     

Prey transport in "palatine-erecting" elapid snakes

Cobras and mambas are members of a group of elapid snakes supposedly united by the morphology and inferred behavior of their palatine bone during prey transport (palatine erectors). The palatine erectors investigated (Dendroaspis polylepis, Naja pallida, Ophiophagus hannah, Aspidelaps scutatus, A. lubricus) show differences in the morphology of their feeding apparatus that do not affect the overall behavior of the system. We delineated the structures directly involved in producing palatine erection during prey transport. Palatine erection can be achieved by a colubroid muscle contraction pattern acting on a palato-pterygoid bar with a movable palato-pterygoid joint and a palatine that is stabilized against the snout. The palatine characters originally proposed to cause palatine erection are not required to produce the behavior and actually impede it in Naja pallida. Palatine-erecting elapids share a fundamental design of the palato-maxillary apparatus with all higher snakes. A set of plesiomorphic core characters is functionally integrated to function in prey transport using the pterygoid walk. Variant characters are either part of a structural periphery unrelated to the core structures that define function or patterns of variation are subordinate character sets operating within functional thresholds of a single system.     

Anatomical study of the skull of amphisbaenian Diplometopon zarudnyi (Squamata,Amphisbaenia)

This study investigates the amphisbaenian species skull which includes cranium, lower jaw and hyoid apparatus. The medial dorsal bones comprise the premaxilla, nasal, frontal and parietal. The premaxilla carries a large medial tooth and two lateral ones. The nasals are paired bones and separated by longitudinal suture. Bones of circumorbital series are frontal, orbitosphenoid and maxilla. The occipital ring consists of basioccipital, supraoccipital and exooccipital. Supraoccipital and basioccipital are single bones while the exo-occipitals are paired. The bones of the palate comprise premaxilla, maxilla, septomaxilla, palatine, pterygoid, ectopterygoid, basisphenoid, parasphenoid, orbitosphenoid and laterosphenoid. Prevomer and pterygoid teeth are absent. Palatine represent by two separate bones. The temporal bones are clearly visible. The lower jaw consists of the dentary, articular, coronoid, supra-angular, angular and splenial. The hyoid apparatus is represented by a Y-shaped structure. The mandible is long and is suspended from the braincase via relatively short quadrate. There is an extensive contact between the long angular and the large triangular coronoid. Thus inter-mandibular joint is bridged completely by the angular and consequently, the lower jaws are relatively rigid and kinetic. The maxillae are suspended from the braincase largely by ligaments and muscles rather than through bony articulation. In conclusion, the skull shape affects feeding strategy in Diplometopon zarudnyi. The prey is ingested and transported via a rapid maxillary raking mechanism.     

Terrestrial feeding in the Mudskipper Periophthalmus (Pisces: Teleostei): A cineradiographic analysis

Mudskipping gobies (Periophthalminae) are among the most terrestrial of amphibious fishes. Specializations associated with terrestrial prey capture and deglutition have been studied in Periophthalmus koelreuteri by light and X-ray cinematography which permits direct visualization of pharyngeal jaw movement during deglutition. Anatomical specializations of the pharyngeal jaws are described and include depressible teeth, a large ventral process on ceratobranchial five, and muscular modifications.
Multiple terrestrial feedings occur by Periophthalmus without a return to the water, and cineradiography reveals that the buccal cavity is often filled with air during terrestrial excursions in contrast to some previous hypotheses. Transport of the prey into the oesophagus occurs primarily by anteroposterior movement of the upper pharyngeal jaw. The lower pharyngeal jaw plays a limited role in food transport and may serve primarily to hold and position prey. The bite between upper and lower pharyngeal jaws occurs between the anterior teeth, and both jaws are protracted together during raking of food into the oesophagus. Functional specializations correlated with terrestrial feeding include obligatory use of pharyngeal jaws for swallowing even small prey items and positioning of the prey in the pharynx by pharyngeal jaw and hyoid movements alone.
This analysis of terrestrial feeding allows hypotheses of design constraints imposed by the aquatic medium on fishes to be raised and tested.     

The naso-frontal joint in snakes as revealed by high-resolution X-ray computed tomography of intact and complete skulls

The naso-frontal joint of snakes is described on the basis of high-resolution X-ray computed tomography scans of single individuals of spirit-preserved snake specimens. The suspension of the snout unit from the braincase at the naso-frontal joint shows some broad evolutionary trends among snakes with potential phylogenetic implications, such as sutured or fused medial frontal flanges formed by the medial frontal pillars and the frontal subolfactory processes (in alethinophidians), the restriction of the usually extended dorsoventral contact of the medial nasal flange with the medial frontal flanges to a dorsal or ventral contact (in macrostomatans), and the transfer of the main element of snout suspension from the nasal to the septomaxilla (in colubroids). Some phylogenetic implications of the morphological characters identified in this study are outlined and discussed.     

Functional plasticity of the venom delivery system in snakes with a focus on the poststrike prey release behavior

We explored variations in the morphology and function of the envenomation system in the four families of snakes comprising the Colubroidea (Viperidae, Elapidae, Atractaspididae, and Colubridae) using our own prey capture records and those from the literature. We first described the current knowledge of the morphology and function of venom delivery systems and then explored the functional plasticity found in those systems, focusing on how the propensity of snakes to release prey after the strike is influenced by various ecological parameters. Front-fanged families (Viperidae, Elapidae, and Atractaspididae) differ in the morphology and topographical relationships of the maxilla as well as in the lengths of their dorsal constrictor muscles (retractor vomeris; protractor, retractor, and levator pterygoidei; protractor quadrati), which move the bones comprising the upper jaw, giving some viperids relatively greater maxillary mobility compared to that of other colubroids. Rear-fanged colubrids vary in maxillary rotation capabilities, but most have a relatively unmodified palatal morphology compared to non-venomous colubrids. Viperids launch rapid strikes at prey, whereas elapids and colubrids use a variety of behaviors to grab prey. Viperids and elapids envenomate prey by opening their mouth and rotating both maxillae to erect their fangs. Both fangs are embedded in the prey by a bite that often results in some retraction of the maxilla. In contrast, Atractaspis (Atractaspididae) envenomates prey by extruding a fang unilaterally from its closed mouth and stabbing it into the prey by a downward-backwards jerk of its head. Rear-fanged colubrids envenomate prey by repeated unilateral or bilateral raking motions of one or both maxillae, some aspects of which are kinematically similar to the envenomation behavior in Atractaspis. The envenomation behavior, including the strike and prey release behaviors, varies within families as a function of prey size and habitat preference. Rear-fanged colubrids, arboreal viperids, and elapids tend to hold on to their prey after striking it, whereas atractaspidids and many terrestrial viperids release their prey after striking it. Larger prey are more frequently released than smaller prey by terrestrial front-fanged species. Venom delivery systems demonstrate a range of kinematic patterns that are correlated to sometimes only minor modifications of a common morphology of the jaw apparatus. The kinematics of the jaw apparatus are correlated with phylogeny, but also show functional plasticity relating to habitat and prey.     

Jaw muscles and the skull in mammals: the biomechanics of mastication.

Among non-mammalian vertebrates, rigid skulls with tight sutural junctions are associated with high levels of cranial loading. The rigid skulls of mammals presumably act to resist the stresses of mastication. The pig, Sus scrofa, is a generalized ungulate with a diet rich in resistant foods. This report synthesizes previous work using strain gages bonded to the bones and sutures of the braincase, zygomatic arch, jaw joint, and mandible with new studies on the maxilla. Strains were recorded during unrestrained mastication and/or in anesthetized pigs during muscle stimulation. Bone strains were 100-1000 micro epsilon, except in the braincase, but sutural strains were higher, regardless of region. Strain regimes were specific to different regions, indicating that theoretical treatment of the skull as a unitary structure is probably incorrect. Muscle contraction, especially the masseter, caused strain patterns by four mechanisms: (1) direct loading of muscle attachment areas; (2) a compressive reaction force at the jaw joint; (3) bite force loading on the snout and mandible; and (4) movement causing new points of contact between mandible and cranium. Some expected patterns of loading were not seen. Most notably, strains did not differ for right and left chewing, perhaps because pigs have bilateral occlusion and masseter activity.     

Ecomorphological relationships among Caribbean tetraodontiform fishes

The anatomy of the oral jaw apparatus, lever-arm mechanics and the diet of six species of Caribbean fishes in the order Tetraodontiformes were investigated to explore the relationships between trophic morphology and feeding habit in these fishes. Tetraodontiforms use their oral jaw apparatus to capture and reduce a broad range of prey types such as plankton, polychaete worms, holothuroids, sea urchins, crabs, molluscs, gorgonians and algae. The different feeding habits of tetraodontiforms are reflected by differences in the morphological and biomechanical features of their oral jaw apparatus that appear to enhance their abilities to feed on hard prey organisms. Species that bite and crush hard, benthic prey organisms had more massive bones and muscles, longer jaw-opening in-levers, and higher jaw-closing lever ratios than the planktivorous, suction-feeding species. Masses of the jaw and suspensorium bones and lower jaw adductor muscles as well as the jaw-opening in-levers and jaw-closing lever ratios of crushers were greater than those of biters. In contrast, the mass of the adductor muscle of the upper jaw did not vary among species with different diets, indicating that this muscle may not be central to the factors that determine patterns of prey use in these fishes. The diversity of feeding behaviours and the wide range of feeding habits among fishes in the order Tetraodontiformes illustrate the versatility of the oral jaw apparatus as a single functional feeding system in fishes.