Stephen M. Reilly

THE EVOLUTION OF TETRAPOD FEEDING BEHAVIOR: KINEMATIC HOMOLOGIES IN PREY TRANSPORT

One of the major features of the aquatic‐to‐terrestrial transition in vertebrate evolution was the change in the mechanism used to transport prey from the jaws to the throat. Primarily, vertebrates use hydraulic transport, but the transition to terrestrial life was accompanied by modifications of the hyobranchial apparatus that permit tongue‐based transport. Despite an extensive data base on amniote feeding systems and mechanisms of intraoral prey transport, few data are available on the mechanism of prey transport in anamniote tetrapods. Transport cycles of four Ambystoma tigrinum (Amphibia) feeding on worms and crickets were filmed at 150 flames per second to produce quantitative profiles of the intraoral transport cycles for the two prey types. During the transport cycle the head and body remain stationary relative to the background: transport in Ambystoma tigrinum thus does not involve inertial movements of the head or body. Prey type had little effect on the kinematics of prey transport. The process of prey transport may be divided into four phases: preparatory, fast opening, closing, and recovery. The preparatory phase itself is divided into two parts: an extended segment that may include slight slow opening and a static phase prior to mouth opening where no change in gape occurs. The kinematic profile of transport in terrestrial salamanders is extremely similar to that used by fishes during hydraulic (aquatic) prey transport. We hypothesize that the distinct recovery and preparatory phases in the transport cycle of anamniote tetrapods are together homologous to the slow opening phases of the amniote cycle, and that during the evolution of terrestrial prey processing systems the primitive extended preparatory phase has become greatly compressed and incorporated into the amniote gape cycle.

The tale of the tail: limb function and locomotor mechanics in Alligator mississippiensis

SUMMARY Crocodilians tow their large muscular tail behind them during terrestrial bouts when they high walk (a walking trot). Analysis of ground reaction forces in the American alligator (Alligator mississippiensis) revealed the consequences of tail-dragging. Individual limb and tail ground reaction force records show that the hindlimbs of Alligator take on a substantial role in body mass support consistent with the more caudal location of its center of mass due to the presence of a particularly heavy tail (representing nearly 28% of total body mass). Furthermore, because the constant drag imposed by the tail is substantial, both fore- and hindlimbs in Alligator have a heightened propulsive role as a means of countering the net braking effect of the tail. Ground reaction forces of the whole body were used to assess how well Alligator was able to utilize mechanical energy-saving mechanisms (inverse pendulum or mass-spring). A high-walking Alligator recovers, on average, about 20% of its mechanical energy by inverse pendulum mechanics. These modest energy recovery levels are likely to be due to a combination of factors that may include low locomotor speed, imprecise coordination of contralateral limbs in the trot, frequent dragging of feet of protracting limbs during swing phase and, possibly, tail dragging.

Prey processing in amniotes: biomechanical and behavioral patterns of food reduction.

In this paper we examine the biomechanics of prey processing behavior in the amniotes. Whether amniotes swallow prey items whole or swallow highly processed slurries or boluses of food, they share a common biomechanical system where hard surfaces (teeth or beaks) are brought together on articulated jaws by the actions of adductor muscles to grasp and process food. How have amniotes modified this basic system to increase the chewing efficiency of the system? To address this question we first examine the primitive condition for prey processing representative of many of the past and present predatory amniotes. Because herbivory is expected to be related to improved prey processing in the jaws we review patterns of food processing mechanics in past and present herbivores. Herbivory has appeared numerous times in amniotes and several solutions to the task of chewing plant matter have appeared. Birds have abandoned jaw chewing in favor of a new way to chew--with the gut--so we will detour from the jaws to examine the appearance of gut chewing in the archosaurs. We will then fill in the gaps among amniote taxa with a look at some new data on patterns of prey processing behavior and jaw mechanics in lizards. Finally, we examine evolutionary patterns of amniote feeding mechanism and how correlates of chewing relate to the need to increase the efficiency of prey processing in order to facilitate increased metabolic rate and activity.

Morphology, Behavior, and Evolution: Comparative Kinematics of Aquatic Feeding in Salamanders

The kinematics of aquatic prey capture were studied in species representing six salamander families (Ambystomatidae, Amphiumidae, Cryptobranchidae, Dicamptodontidae, Proteidae, and Sirenidae) to test the hypothesis that the process of aquatic prey capture is similar in these families. Seven variables were digitized from high-speed video records of prey capture, and a nested analysis of variance was performed to test for both significant individual within taxon and among taxa effects. The time-to-peak head angle and gape variables showed no taxon effect, while the other five variables exhibited highly significant differences among taxa. Cryptobranchus and Siren showed the most divergent kinematic pattern from the other taxa in a multivariate analysis of all variables, while Ambystoma, Dicamptodon, and Amphiuma tended to have similar overall patterns of head movement. These results show that kinematic patterns during aquatic feeding are not conserved across salamander taxa, and that phylogenetic differentiation in head morphology has been accompanied by novelties in feeding function. The feeding mechanisms of Cryptobranchus and Amphiuma have a bidirectional hydrodynamic design with kinematic correlates that are similar to kinematic characteristics of aquatic feeding in turtles and transformed ambystomatid salamanders. A general framework is presented as an aid to understanding the interrelationships among muscle activity patterns, morphology, and behavior (kinematic patterns). By considering the distribution of taxa in three multivariate spaces, corresponding to three of the levels at which one might analyze a behavior (kinematics, morphology, and motor pattern), it is possible to identify patterns of correspondence among the levels, which aid in understanding the evolution of behavior.

Evolution of Motor Patterns: Aquatic Feeding in Salamanders and Ray-Finned Fishes

Patterns of muscle activity (motor patterns) have generally been found to be strongly conserved during the evolution of aquatic feeding behavior within closely related groups of fishes and salamanders. We conducted a test of the generality of motor pattern conservation with a much broader phylogenetic scope than has been done previously. Activity patterns of three cranial muscles were quantified from electromyographic (EMG) recordings made during suction feeding in a salamander (Ambystoma mexicanum) and 4 widely divergent species of ray-finned fishes (Amia calva, Notopterus chitala, Micropterus salmoides and Lepomis macrochirus). General features of the motor pattern were the same in all species, but multivariate and univariate analyses of variance revealed highly significant differences among the 5 species in the average muscle activity pattern, indicating that the motor pattern has not been precisely conserved among these 5 taxa. Five of eight EMG variables that describe the intensity and timing of muscle activity differed among species. Only the intensity of activity of the adductor mandibulae appears to be a strongly conserved feature of the suction feeding motor pattern in anamniotes. A discriminant function analysis of the 8 EMG variables successfully classified about two thirds of the feeding incidents as belonging to the correct species. In contrast to the results of previous studies of closely related taxa, we found that numerous quantitative differences exist among species, indicating that functionally significant details of suction feeding motor patterns have changed during evolution, whereas several general features of the pattern have been conserved.

Locomotion in the quail (Coturnix japonica): the kinematics of walking and increasing speed

ABSTRACT

Lizard Ecology: The Evolutionary Consequences of Foraging Mode

The foraging mode of lizards has been a central theme in guiding research in lizard biology for three decades. Foraging mode has been shown to be a persuasive evolutionary force molding the diet, ecology, behavior, anatomy, biomechanics, life history, and physiology of lizards. This volume reviews the state of our knowledge on the effects of foraging mode on these and other organismal systems to show how they have evolved with foraging mode over a wide taxonomic survey of lizard groups. The reviews presented here reveal the continuous nature of foraging strategies in lizards and snakes, providing the general reader with an up-to-date review of the field, and will equip researchers with new insights and future directions for the sit-and-wait vs. wide foraging paradigm. This volume will serve as a reference book for herpetologists, evolutionary biologists, ecologists, and animal behaviorists.

Performance consequences of a trophic polymorphism: feeding behavior in typical and cannibal phenotypes of Ambystoma tigrinum

Aquatic feeding behavior, prey capture performance, and morphological aspects of the feeding mechanism were compared in typical and cannibal phenotypes of Ambystoma tigrinum melanostictum to test the hypothesis that the trophic polymorphism affords a performance advantage in feeding. Similar-sized salamanders of the two phenotypes differed morphologically in size of the vomerine tooth patches and head width but not in size of the gape or mass of the hyoid retractor muscles used in suction feeding. Suction feeding and prey handling performance did not differ between the two morphs feeding on live guppies or small conspecific salamanders. However, differences were found in willingness to feed on conspecifics and prey handling performance when feeding on larger salamander larvae. Thus, cannibal morphs possess a significant performance advantage only during predation on large conspecifics. The performance advantage on large prey appears to be a consequence of greater prey handling ability facilitated by the increased size of the vomerine tooth patches.

Whole-body mechanics and gaits in the gray short-tailed opossum Monodelphis domestica: integrating patterns of locomotion in a semi-erect mammal.

SUMMARY Gaits (footfall patterns) and external mechanical energy patterns of the center of mass were quantified in a generalized, semi-erect mammal in order to address three general questions. First, do semi-erect mammals exhibit the walk/run gait transitions that have been proposed as the primitive condition for tetrapods? Second, do small, semi-erect mammals employ the energy-saving pendular and spring-based mechanics used by erect mammals? Third, how well do mechanical locomotor patterns of the center of mass correlate with gaits? Monodelphis domestica utilizes only fast walking and running trot gaits over a fivefold increase in speed, over which we could illicit constant velocity steps, although running trots were their preferred gait. In sustained level locomotion the opossums did not use other walking gaits presumed to be primitive for tetrapods. Across the full range of speeds their trotting gaits exhibited force patterns and in-phase mechanical energy fluctuations that are characteristic of spring-mass mechanics. Thus, opossums appear to prefer trotting gaits with bouncing mechanics for sustained locomotion. Integration of center-of-mass versus footfall perspectives reveals that spring-mass mechanics is associated with both walking trot and running trot gaits. Furthermore, the onset of an aerial phase was not clearly associated with either the walk/run gait transition (50% duty factor) or a change in center-of-mass mechanics. The assumption that energy-saving mechanisms are ubiquitous among mammals is tenuous because small non-cursorial mammals do not appear to use pendular-based mechanics for sustained locomotion and, although they prefer spring-based mechanics, they probably lack clear musculoskeletal spring elements that could store energy during running. Thus, it appears that simply paying for locomotion with muscular work may be the primitive condition for mammals.

Amphibian Feeding Behavior: Comparative Biomechanics and Evolution

The clade Amphibia is critical for our understanding of vertebrate evolution. Because of their position as a basal lineage of tetrapods, nearly all aspects of amphibian biology are of special interest to those interested in the origin of terrestrial life and in the morphological, physiological, ecological, and behavioral changes involved in aquatic to terrestrial transitions. In addition, amphibian taxa illustrate with particular clarity the phenomenon of metamorphosis, allowing the experimental study of aquatic-to-terrestrial transitions on a single individual during ontogeny. Although phylogenetic relationships among the three extant amphibian clades (and among fossil amphibian taxa) are still a matter of debate (Bolt 1977; Carroll and Holmes 1980; Duellman and Trueb 1986; Trueb and Cloutier 1991), the relevance of amphibian clades to problems in vertebrate biology is not at issue. Extant amphibian lineages, because of their phylogenetic position near the base of the tetrapod radiation and because of the mosaic nature of character distribution in these taxa (many amphibian taxa retain large numbers of primitive features in the musculoskeletal system, while at the same time displaying numerous derived characteristics), are prime candidates for comparisons to both fish and amniote clades.