Using natricine snakes to test how prey type and size affect predatory behaviors and performance.

Introduction: Predation is a complex process for which behavior, morphology, and size of both predator and prey can affect the success and effectiveness of the predator. For predators such as snakes that swallow prey whole, gape ultimately limits prey size, but the behaviors used to select, capture, and consume prey and attributes of the prey can also affect maximal prey size. For example, swallowing live, struggling prey is difficult, but using coiling or envenomation to restrain or kill prey has evolved repeatedly in snakes. Methods: To test the potential benefits of these behaviors, we manipulated the type and size of prey, and determined how stereotyped predatory behavior was in a snake species (Liodytes rigida) that uses both coiling and envenomation to restrain and immobilize its formidable prey of crayfish. We also studied a close relative (Liodytes pygaea) that eats fish and salamanders to gain insights into the evolution of these traits. Results: For L. rigida, envenomation of hard-shell crayfish via their soft underside was very stereotyped (100% of feedings). Envenomation of soft-shell crayfish was less frequent (59% of feedings) but became more likely both with increased relative prey size and increased time after molt (hardness). L. rigida coiled more for hard-shell than soft-shell crayfish (77% vs. 30%). The probability of coiling was unaffected by prey size, but it increased with increased time after molt for the soft-shell crayfish. Liodytes rigida waited to swallow crayfish until they were completely immobile in 75% and 37% of the feedings with hard- and soft-shelled crayfish, respectively. Even with large prey L. pygaea never used coiling or envenomation, whereas previous studies of L. alleni, the sister species of L. rigida, observed non-lethal coiling without envenomation when eating hard-shell crayfish. Discussion: Our findings for the Liodytes clade of three species suggest that coiling evolved ancestral to the crayfish specialists (L. alleni; L. rigida), and envenomation by L. rigida subsequently evolved as an additional means of subduing formidable prey. The proximate benefits observed for coiling and envenomation in L. rigida support the evolutionary scenario that both traits evolved to enhance the feeding performance for more formidable prey.

When Food Fights Back: Skull Morphology and Feeding Behavior of Centipede-Eating Snakes.

Feeding is a complex process that involves an integrated response of multiple functional systems. Animals evolve phenotypic integration of complex morphological traits to covary and maximize performance of feeding behaviors. Specialization, such as feeding on dangerous prey, can further shape the integration of behavior and morphology as traits are expected to evolve and maintain function in parallel. Feeding on centipedes, with their powerful forcipules that pinch and inject venom, has evolved multiple times within snakes, including the genus Tantilla. However, the behavioral and morphological adaptations used to consume this dangerous prey are poorly understood. By studying snakes with varying degrees of dietary specialization, we can test the integration of diet, morphology, and behavior to better understand the evolution of consuming difficult prey. We studied the prey preference and feeding behavior of Tantilla using the flat-headed snake (T. gracilis) and the crowned snake (T. coronata), which differ in the percentage of centipedes in their diet. We then quantified cranial anatomy using geometric morphometric data from CT scans. To test prey preference, we offered multiple types of prey and recorded snake behavior. Both species of snakes showed interest in multiple prey types, but only struck or consumed centipedes. To subdue centipedes, crowned snakes used coiling and holding (envenomation) immediately after striking, while flat-headed snakes used the novel behavior of pausing and holding onto centipedes for a prolonged time prior to the completion of swallowing. Each skull element differed in shape after removing the effects of size, position, and orientation. The rear fang was larger in crowned snakes, but the mechanical advantage of the lower jaw was greater in flat-headed snakes. Our results suggest that the integration of behavioral and morphological adaptations is important for the success of subduing and consuming dangerous prey.

Visual Contrast and Intensity Affect Perch Choice of Brown Tree Snakes (Boiga irregularis) and Boa Constrictors (Boa constrictor).

Habitat structure can affect animal movement both by affecting the mechanical demands of locomotion and by influencing where animals choose to go. Arboreal habitats facilitate studying path choice by animals because variation in branch structure has known mechanical consequences, and different branches create discrete choices. Recent laboratory studies have found that arboreal snakes can use vision to select shapes and locations of destinations that mechanically facilitate bridging gaps. However, the extent to which the appearance of objects unrelated to biomechanical demands affects the choice of destinations remains poorly understood for most animal taxa including snakes. Hence, we manipulated the intensity (black, gray, or white), contrast, structure, and locations of destinations to test for their combined effects on perch choice during gap bridging of brown tree snakes and boa constrictors. For a white background and a given perch structure and location, both species had significant preferences for darker perches. The preference for darker destinations was strong enough to override or reduce some preferences for biomechanically advantageous destinations such as those having secondary branches or being located closer or along a straighter trajectory. These results provide a striking example of how visual cues unrelated to the physical structure of surfaces, such as contrast and intensity, can bias choice and, in some cases, supersede a preference for mechanically beneficial surfaces. Because these two species are so phylogenetically distant, some of their similar preferences suggest a sensory bias that may be widespread in snakes. The manipulation of surface color may facilitate management of invasive species, such as the brown tree snakes, by enhancing the efficiency of traps or making certain objects less attractive to them.