Ecomorphology and ontogeny modulate the mechanical properties of shark skin.

Abstract

Shark skin is a biological composite of dermal denticles embedded in a multilayered network of collagen fibers. Variation of skin morphology (dermal denticles and collagen fibers) is observable among species, body regions, and developmental stages, and has been shown to relate to skin mechanics. The orientation of collagen fibers results in mechanical anisotropy; shark skin is more extensible when stressed longitudinally (anteroposterior) and stiffer when stressed perpendicularly (dorsoventral). To evaluate the impact of ecological and ontogenetic factors on mechanical behavior, we tested shark skin in uniaxial tension to failure and calculated the tensile strain and mechanical properties (strength, stiffness, and toughness) from 20 species, and quantified the effects of ecomorphotype and ontogeny, as well as stress axis and body region. The bonnethead shark Sphyrna tiburo was used as a case study to quantify mechanics in a single species across an ontogenetic series. We analyzed skin morphology and correlated this with mechanical behavior to understand the mechanisms that regulate skin function. Across ecomorphotypes, shark skin from deeper-water, non-migratory species (Ecomorphotype E) was stronger and tougher than skin from small-bodied, non-migratory species (Ecomorphotype B), and medium-bodied, migratory species (Ecomorphotype C) had stiffer skin than large-bodied, migratory species (Ecomorphotype D). We found skin from mature sharks was stronger, stiffer, tougher, and more extensible than skin from pups. These results indicate that ontogeny and ecomorphotype impact skin mechanics among sharks. Despite morphological diversity, aspects of skin morphology appear to play less of a role in regulating mechanical function. STATEMENT OF SIGNIFICANCE: The current study establishes a comparative framework for evaluating the mechanical properties of shark skin across ecologically and morphologically diverse species, for which the mechanical behavior of the skin has not been investigated. The results advance our understanding of effective modulation of skin mechanics across functional groups and life stages, allow for improved comparisons of mechanical behavior among marine organisms, and provide insight into the adaptive design of biological materials in marine environments.