Tadpole Locomotion: Axial Movement and Tail Functions in a Largely Vertebraeless Vertebrate1

Abstract Synopsis.Tadpoles are exceptional among vertebrates in lacking vertebrae along most of their body axis. Their caudal myotomes are also unusually simple for free-living vertebrates. This overall morphological simplicity, in theory, makes tadpoles good models for exploring how vertebrates control undulatory movements. We used electromyography (EMG), high speed ciné, computational fluid dynamics (CFD), and mechanical tissue testing to understand how Rana tadpoles regulate their locomotion. Bullfrog (Rana catesbeiana) tadpoles have several patterns of muscle activity, each specific to a particular swimming behavior. Ipsilateral muscles in the tail were active either in series or simultaneously, depending on the tadpole's velocity, and linear and angular acceleration. When R. catesbeiana larvae swam at their natural preferred tail beat frequency, muscles at the caudal end of their tail were inactive. Mechanical tests of tissue further suggest that the preferred tail beat frequency closely matches the resonance frequency of the tail thus minimizing the energetic cost of locomotion. CFD modeling has demonstrated that the characteristically high amplitude oscillations at a tadpole's snout during normal rectilinear locomotion do not add to drag, as might be supposed, but rather help generate thrust. Mechanical testing of the tadpole tail fin has revealed that the fin is viscoelastic and stiffer in small rather than large deformations. This property (among others) allows the tail to be light and flexible, yet stiff enough to generate thrust in the absence of a bony or cartilaginous skeleton. Many recent studies have documented predator-induced polyphenism in tadpole tail shape. We suggest that this developmental plasticity in locomotor structures is more common in tadpoles than in other vertebrates because tadpoles do not need to reform skeletal tissue to change overall caudal shape. Tadpole tail fins and tip, in the absence of any skeleton, are fragile and often scarred by predators. Based on the high incidence of tail fin injury seen in tadpoles in the wild, we suggest that the tadpole tail fin and tip may play an ecological role that goes beyond serving as a propeller to help tadpoles stay beyond predators' reach. Those soft tissue axial structures, by failing under very small tensile loads, may also allow tadpoles to tear free of a predator's grasp.