Department of Biology, Tufts University, 200 Boston Ave Ste 4700, Medford, MA 02155, USA.
National Institute of Neurological Disorders and Stroke, National Institutes of Health, 35 Convent Drive, Bethesda, MD, USA.
Integr Comp Biol. 2021 Sep 8;61(2):427-441. doi: 10.1093/icb/icab071.
Swimming in schools has long been hypothesized to allow fish to save energy. Fish must exploit the energy from the wakes of their neighbors for maximum energy savings, a feat that requires them to both synchronize their tail movements and stay in certain positions relative to their neighbors. To maintain position in a school, we know that fish use multiple sensory systems, mainly their visual and flow sensing lateral line system. However, how fish synchronize their swimming movements in a school is still not well understood. Here, we test the hypothesis that this synchronization may depend on functional differences in the two branches of the lateral line sensory system that detects water movements close to the fish's body. The anterior branch, located on the head, encounters largely undisturbed free-stream flow, while the posterior branch, located on the trunk and tail, encounters flow that has been affected strongly by the tail movement. Thus, we hypothesize that the anterior branch may be more important for regulating position within the school, while the posterior branch may be more important for synchronizing tail movements. Our study examines functional differences in the anterior and posterior lateral line in the structure and tail synchronization of fish schools. We used a widely available aquarium fish that schools, the giant danio, Devario equipinnatus. Fish swam in a large circular tank where stereoscopic videos recordings were used to reconstruct the 3D position of each individual within the school and to track tail kinematics to quantify synchronization. For one fish in each school, we ablated using cobalt chloride either the anterior region only, the posterior region only, or the entire lateral line system. We observed that ablating any region of the lateral line system causes fish to swim in a "box" or parallel swimming formation, which was different from the diamond formation observed in normal fish. Ablating only the anterior region did not substantially reduce tail beat synchronization but ablating only the posterior region caused fish to stop synchronizing their tail beats, largely because the tail beat frequency increased dramatically. Thus, the anterior and posterior lateral line system appears to have different behavioral functions in fish. Most importantly, we showed that the posterior lateral line system played a major role in determining tail beat synchrony in schooling fish. Without synchronization, swimming efficiency decreases, which can have an impact on the fitness of the individual fish and group.
长期以来,人们一直假设在学校游泳可以让鱼类节省能量。鱼类必须利用邻居的尾流能量来实现最大的节能效果,这一壮举要求它们协调尾鳍的运动,并保持相对于邻居的特定位置。为了在群体中保持位置,我们知道鱼类会使用多种感觉系统,主要是视觉和侧线水流感觉系统。然而,鱼类如何在群体中协调它们的游泳动作仍然不太清楚。在这里,我们测试了一个假设,即这种同步可能取决于侧线感觉系统两个分支的功能差异,该系统检测靠近鱼体的水的运动。位于头部的前分支遇到的是基本未受干扰的主流流,而位于躯干和尾部的后分支遇到的是受尾鳍运动强烈影响的流。因此,我们假设前分支可能更重要的是调节群体内的位置,而后分支可能更重要的是协调尾鳍的运动。我们的研究检查了前侧线和后侧线在鱼类群体结构和尾鳍同步中的功能差异。我们使用了一种广泛存在的水族馆鱼类,即巨型大鳍脂鲤,Devario equipinnatus。鱼在一个大型圆形水箱中游泳,立体视频记录用于重建群体中每个个体的三维位置,并跟踪尾鳍运动以量化同步性。对于每个群体中的一条鱼,我们使用氯化钴分别消融前区、后区或整个侧线系统。我们观察到,消融侧线系统的任何区域都会导致鱼以“盒状”或平行游泳的形式游动,这与正常鱼观察到的菱形形成不同。仅消融前区不会显著降低尾鳍拍打同步性,但仅消融后区会导致鱼停止同步尾鳍拍打,主要是因为尾鳍拍打频率急剧增加。因此,前侧线和后侧线系统似乎在鱼类中具有不同的行为功能。最重要的是,我们表明后侧线系统在决定群体鱼类的尾鳍同步方面起着主要作用。没有同步性,游泳效率会降低,这会对个体鱼和群体的适应性产生影响。