Constriction Behavior, a Key Innovation In Snake Evolution: The Integration of Ethology and Physiology

Among living tetrapod vertebrates, snakes exhibit the most radical shifts in feeding biology and among limbless squamate reptiles, only snakes have undergone a substantial adaptive radiation. The behavioral innovation, constriction, has been associated with the success of this clade. Constriction is a prey restraint behavior that enabled snakes to immobilize and subdue extremely large prey items relative to their own body mass. This behavior pattern is associated with the incredible shifts observed in snake feeding biology from consuming small meals frequently to less frequent feeding on large prey. Although constriction is an ethological homology for the majority of snakes, variations of constriction postures have been documented in many derived snake lineages. Nevertheless, the mechanisms driving behavioral variation are not well understood. In this dissertation, I attempt to use a comparative hierarchical approach to examine constriction behavior at both the ethological and physiological levels in order to better understand the behavioral variation of this key innovation. As reviewed in Part 1, derived snake lineages seem to have several methods with which to restrain prey. Prey restraint methods appear to vary with respect to prey characteristics (size, shape, activity level). On the other hand, intermediate taxa (boas and pythons) are thought to be less variable in the prey restraint phase of feeding. The kinematics of loop application pattern also appears to differ between intermediate and derived snake groups. Derived snakes use the lateral part of their body to wind prey whereas boas tend to bend ventrally around prey. The polarity for variable prey restraint behavior and loop application patterns have not been determined as observations on feeding behavior for basal snake taxa are lacking. I report on stimulus control studies evaluating prey restraint behavior and loop application pattern for basal and intermediate snake taxa in Part 2. Testing for the effects of prey size and status on the prey restraint behavior enabled me to polarize variable prey restraint behavior and loop application pattern. Prey size and status had varying effects on the capture position, prey restraint method, prey restraint time and swallowing time for basal and semi-fossorial boas while individuals of B. constrictor only constricted prey. Looping one or more times around prey was observed during the intraoral transport (swallowing) phase of feeding in the majority of trials for L. bicolor and Erycine snakes (Eryx muelleri, Charina bottae, Lichanura triviragata). Loop application patterns varied across snake taxa with basal and semi-fossorial boas applying loops laterally around prey. Individuals of B. constrictor bent ventrally around prey. The ability to vary prey restraint behavior, in response to prey characteristics and applying loops laterally around prey is probably the ancestral condition in snakes. Intermediate taxa, such a boas exhibit a derived simplified behavioral repertoire. Examining the underlying physiology of a complex motor pattern, such as constriction behavior, can provide a better understanding of the hierarchical structure of organisms in nature. As an ethological homology, constriction behavior provides us with the opportunity to trace evolutionary change at other levels of biological organization and to examine how various levels within a hierarchy relate to one another. Although constriction is an important key innovation associated with the adaptive radiation of snakes, few studies have examined the underlying physiological patterns of this complex motor pattern that may account for the kinematic variability of constriction postures among snakes. In Parts 3 & 4, I comparatively examine the muscle activity patterns during constriction for basal and intermediate snake lineages. I specifically investigated how the underlying physiological mechanisms of constriction correspond to the postural changes observed at the behavioral level using electromyography. Lateral bending and unilateral muscle activity patterns were predominant in the basal taxon, Loxocemus bicolor. Lateral bending and unilateral muscle activity patterns were also observed in derived snake taxa previously documented. Ventral bending and bilateral epaxial muscle activity patterns were predominant in intermediate lineages and present in derived snake lineages. Therefore, similar to prey restraint behaviors, three epaxial muscle activity patterns were observed: 1) mostly lateral bending with unilateral epaxial muscle activity, 2) mostly ventral bending with bilateral muscle activity and 3) mostly lateral and some bilateral bends associated with both unilateral and bilateral epaxial muscle activity, “mixed”. The kinematic and muscle activity patterns correspond with the ethological data in Part 2. Lateral bending and unilateral epaxial muscle activity support the more variable prey restraint behaviors observed in basal and derived snake taxa. Ventral bending and bilateral activity supports the highly stereotyped behavior patterns observed in intermediate snake taxa. A ‘mixed’ kinematic and epaxial activity pattern supports highly variable prey restraint methods as observed from previous research on gopher snakes and kingsnakes. Thus the patterns of epaxial muscle activity underlying constriction behavior can be correlated with the variability in prey restraint postures. In Part 5, I integrate the behavioral, physiological, and ecological differences reported for L. bicolor and Boid snakes, from the stimulus control data and the physiological data collected in this study, to further discuss the origin and evolution of feeding behavior among basal, intermediate and derived snake taxa