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尽管工具使用可为使用者带来显著益处，但成本因素在工具使用行为的传播过程中所扮演的角色却鲜少受到关注。海绵工具使用是一种觅食策略，仅局限于澳大利亚鲨鱼湾的宽吻海豚（Tursiops aduncus）亚种群：这类海豚会将篮状海绵置于喙部，以此探查海底并驱赶隐匿的鱼类，在扩大搜索范围的同时，还能保护喙部免受磨损。尽管多数动物工具使用行为可延伸其表型，但我们假设海绵会干扰回声定位——这是海豚最精湛的感官技能，尤其是沿下颌接收回声的能力。为评估回声定位信号穿过海绵组织时的变化情况，我们基于两种海绵工具——肠形网海绵（Echinodictyum mesenterinum）与皂角海绵属（Ircinia spp.）的数字化模型，利用有限元分析模拟了回声定位过程。研究发现，当存在海绵时，回声定位信号的声学特性会发生改变：皂角海绵属物种存在时，信号的频率、时长、振幅以及波束模式均会发生显著变化，而肠形网海绵的影响则相对较弱。鉴于每种海绵都会对回声定位信号造成不同程度的失真，海豚必须在神经信号处理过程中进行适应性且灵活的补偿。这也解释了为何海绵工具使用需要花费极长的时间学习，且仅通过垂直传递，即便与工具使用者存在密切接触，也无法传播至其他个体。综上，这些研究结果为探究野生种群中塑造工具使用行为的内在与外在深层驱动力提供了极具说服力的洞察。