Upper limits to body size imposed by respiratory–structural trade-offs in Antarctic pycnogonids

Abstract

Across metazoa, surfaces for respiratory gas exchange are diverse, and the size of those surfaces scales with body size. In vertebrates with lungs and gills, surface area and thickness of the respiratory barrier set upper limits to rates of metabolism. Conversely, some organisms and life stages rely on cutaneous respiration, where the respiratory surface (skin, cuticle, eggshell) serves two primary functions: gas exchange and structural support. The surface must be thin and porous enough to transport gases but strong enough to withstand external forces. Here, we measured the scaling of surface area and cuticle thickness in Antarctic pycnogonids, a group that relies on cutaneous respiration. Surface area and cuticle thickness scaled isometrically, which may reflect the dual roles of cuticle in gas exchange and structural support. Unlike in vertebrates, the combined scaling of these variables did not match the scaling of metabolism. To resolve this mismatch, larger pycnogonids maintain steeper oxygen gradients and higher effective diffusion coefficients of oxygen in the cuticle. Interactions among scaling components lead to hard upper limits in body size, which pycnogonids could evade only with some other evolutionary innovation in how they exchange gases.