Male spiny frogs enter the underwater battlefield with loose skin exhibiting enhanced penetration of capillaries into the epidermis

Abstract

The skin has multiple functions, and capillaries can penetrate the epidermis to shorten the diffusion path while allowing maintenance of overall epidermal thickness for nonrespiratory roles. However, a method for quantifying the capillary penetration extent is lacking. Such a method may facilitate making comparisons and detecting associations, potentially making the extent a useful variable in biological studies. We quantified the extent as the ratio of the average minimum thickness of epidermis overlying each capillary to the average epidermal thickness along a skin section and then explored its performance in the Emei mustache toad, Leptobrachium boringii, a species in which breeding males with loose skin call and fight each other with maxillary spines underwater. The ratio showed informative associations with other variables, such as perfused capillary density. It displayed small intragroup variation and could be more sensitive than other variables in revealing structural differences in the skin. The ratio estimates were lowest and were correlated with epidermal and stratum compactum thicknesses in breeding males, i.e., a covariation but not reinforcement against stabbing, constituting early evidence consistent with the increased extensibility of loose skin conferring a defensive advantage during combat in amphibians. In addition, our results lead to the hypothesis that high hemoglobin density along subepidermal capillaries favors the maintenance of low blood partial oxygen pressure and hence increases cutaneous oxygen uptake. We also provide evidence supporting the new idea that the cooccurrence of loose skin and underwater calling found in some frogs can be explained by the latter benefiting from a large functional respiratory surface area. Awareness of the usefulness of the ratio may promote its application and the quantification of the penetration. Regarding exchange surface design, these findings for L. boringii imply a case in which looseness increases surface area as well as prevents damage.