Snake lower jaw skin: Extension and recovery of a hyperextensible keratinized integument

Abstract

The skin of squamates consists of a keratinized epidermis divided into thick scale and thinner, folded interscale regions underlain by a dermis containing a complex array of fibrous connective tissues. We examined the skin of the lower jaw of watersnakes (Nerodia sipedon) to determine how skin morphology changes when highly stretched during ingestion of large prey. Video records of skin behavior in the lower jaws of watersnakes feeding on fish or anesthetized watersnakes being stretched on an Instron machine showed that most skin extension involves the interscale skin. The largest intermandibular separation recorded during feeding was 7.7× resting distance, but intermandibular separation reached 10× without tissue failure during mechanical testing. Histological and anatomical analyses of lower jaws fixed in resting, moderately or highly stretched conditions showed that stretching had little effect on scale regions of the epidermis. However, stretching flattened folds of interscale regions at both gross and cellular levels and imposed changes in epidermal cell shape. Stretching of the dermis is primarily limited to realignment of collagen and stretching of elastin in the deep dermis. The configuration of dermal elastin suggests a model for passive recovery of epidermal folding following release of tension.

A Model of the Anterior Esophagus in Snakes, with Functional and Developmental Implications

“…Modifications of the gut for increasing its circumference appear to be associated with many of the skeletal and muscular features documented for snakes (Cundall and Greene, ). The existence of additional specializations seems likely, particularly modifications for extreme extension at cellular levels (Close and Cundall, ).…”

Identification and comparative analysis of the epidermal differentiation complex in snakes

“…Snakes are reptiles that have lost their limbs during evolution and developed a unique predatory lifestyle that involves the ability to swallow prey of a diameter larger than that of their own body123. The skin of snakes, and more specifically the epidermis, consists of rigid scales and soft inter-scale regions, which together provide both mechanical resistance and flexibility45.…”

Highly extensible skeletal muscle in snakes

“…We then used univariate general linear regression of ingestion ratio (x) on change in intermandibular distance (y) to determine the relationship between increasing relative prey size and change in intermandibular distance. Our behavioral records established the normal timing and limits of strain of the intermandibular soft tissues, values we replicated during manual manipulations (Close and Cundall, 2014).…”

“…During swallowing, the distance between the right and left mandibular tips increases greatly, presumably imposing high levels of strain on the MIAA. The functions of this muscle and other closely associated intermandibular soft tissues (Close and Cundall, 2014) serve as major determinants of gape in snakes. The degree to which the MIAA extends during feeding events is currently undefined for any snake, and the problem of recovery from levels of extension that could be beyond the physiological limits of contraction have yet to be investigated.…”