Cultural transmission of animal tool-use driven by trade-offs: Insights from sponge-using dolphins

Although tool-use offers obvious benefits to the user, the role of costs in the spread of tool use has received scant attention. Sponge tool-use is a foraging technique restricted to a subpopulation of bottlenose dolphins (Tursiops aduncus) in Shark Bay, Australia that carry basket sponges on their beaks to probe the seafloor and flush out camouflaged fish, simultaneously widening the search area and protecting the beak from abrasion. While most instances of animal tool-use extend the phenotype, we hypothesized that sponges interfere with echolocation, the most exquisite skill a dolphin has, particularly reception of echoes along the lower jaw. To evaluate how echolocation signals change while traveling through sponge tissue, we simulated echolocation using finite-element analysis based on digital models of two species of sponge tools (Echinodictyum mesenterinum and Ircinia spp.). We find that acoustic properties of the echolocation signal are changed when the sponge is present: frequency, duration, amplitude, and beam pattern are all substantially altered in the presence of Ircinia spp. and, to a lesser extent, E. mesenterinum. Given these distortions to the echolocation signal that vary with each sponge, the dolphins have to adaptively and flexibly compensate during neural signal processing. This explains why sponging takes so long to learn, is strictly vertically transmitted, and does not spread to others despite close association with tool users. Taken together, these findings provide a compelling look at the underlying intrinsic and extrinsic forces shaping tool-use in wild populations