Batoid skin mechanical properties and morphology vary among functional swimming styles

Abstract

Batoids are cartilaginous fishes that are dorsoventrally compressed in body shape and so experience unique mechanical limitations on the effective modulation of stress forces across various swimming styles. Previous research showed that the skin of one batoid species was anisotropic, where the mechanical behavior varied between longitudinal (parallel to the vertebral column) and hoop axes (perpendicular to the vertebral column). Due to the diversity of swimming modalities employed across batoids, the patterns of mechanical behavior may vary. To explore the effect of locomotor strategy on skin mechanics, we used six species to represent styles: axial undulation (Atlantic guitarfish Rhinobatos lentiginosus), pectoral disc undulation (Atlantic stingray Hypanus sabinus, bluntnose stingray Hypanus say, yellow stingray Urobatis jamaicensis), semi-oscillation (smooth butterfly ray Gymnura micrura), and oscillation (cownose ray Rhinoptera bonasus). We tested dorsal, ventral, and composite skin samples in quasi-static uniaxial tension to failure and quantified the variability in mechanical behaviors among functional groups, regions of the body and disc, and between sexes and stress axes. We hypothesized that mechanical behaviors (tensile strain, strength, stiffness, toughness) and morphology of batoid skin would vary among swimming styles. While strain and stiffness measurements are approximate, the observed differences between groups support the conclusion that undulators had the most extensible skin whereas axial-undulators had the strongest and stiffest skin. We assessed sex differences in mechanical behaviors using Atlantic stingrays, and we found male stingrays had stronger and tougher skin than females. Lastly, we discuss the implications of dermal denticles, which may affect mechanical properties.

Statement of significance

This study provides a framework for understanding the mechanical properties of batoid skin across groups of species that utilize different swimming styles. A previous study examined just a single species, offering limited insight into the skin mechanics of a large, diverse clade of cartilaginous fishes. The results presented here include data from individual layers and composite skin samples from six species, which can be used to design mechanically specialized biomimetic and bio-inspired materials. These data provide biological ranges for batoid skin mechanics and offer insight as to the effective modulation of mechanical behavior among locomotor styles.