Pufferfish inflation: drivers of axial and hoop skin strain and regional variation across the body

Pufferfish skin undergoes large multi-axial extensions during defensive inflation behaviour, as water is pumped into the stomach and the fish increases its body volume threefold. This remarkable capacity for deformation thus raises questions on how skin extension is spatially distributed across the body, and how skin extension relates to changes in body volume and stomach pressure. However, directly measuring skin extension remains experimentally challenging, particularly when attempting to preserve the body′s complex 3D geometry and natural multiaxial strain during ex vivo testing. We used biplanar x-ray videography to measure skin strain (fluoromicrometry) and body volume (dynamic digital endocast) simultaneously with stomach pressure recordings during natural and artificial inflations in porcupinefish (Diodon holocanthus). We found no significant difference in maximum body volumes, body dimensions, peak pressures, and skin extension at maximum inflation between natural and artificial inflation conditions. In all inflations, volume increased steadily while stomach pressure only increased during the last 25-50% of inflation. Skin extension varied biaxially, with mean strains reaching up to 74% in the axial direction and 112% in the hoop direction as the fish became nearly spherical. The greatest skin extensions occurred most dorsocranially (axial) and ventrolaterally (hoop). Strains in the hoop direction were only significantly different between body regions (dorsal, lateral and ventral), with the greatest hoop strains occurring in the ventral body region. Our findings may provide insight into existing hypotheses regarding the relationship between volume, pressure, and skin structure and behaviour, while also providing direct in vivo measurements to inform biomimetic design.