Person:

Blevins, Erin

Fishes are the most speciose group of living vertebrates, making up more than half of extant vertebrate diversity. They have evolved a wide array of swimming modes and body forms, including the batoid elasmobranchs, the dorsoventrally flattened skates and rays, which swim via oscillations or undulations of a broad pectoral fin disc. In this work I offer insights into locomotion by an undulatory batoid, freshwater stingray Potamotrygon orbignyi (Castelnau, 1855), combining studies of live animals, physical models, and preserved specimens. In Chapter 1, I quantify the three-dimensional kinematics of the P. orbignyi pectoral fin during undulatory locomotion, analyzing high-speed video to reconstruct three-dimensional pectoral fin motions. A relatively small portion (~25%) of the pectoral fin undulates with significant amplitude during swimming. To swim faster, stingrays increase the frequency, not the amplitude of propulsive motions, similar to the majority of studied fish species. Intermittently during swimming, a sharp, concave-down lateral curvature occurred at the fin margin; as the fin was cupped against the pressure of fluid flow this curvature is likely to be actively controlled. Chapter 2 employs a simple physical model of an undulating fin to examine the ground effects that stingrays may experience when swimming near a substrate. Previous research considering static air- and hydrofoils indicated that near-substrate locomotion offers a benefit to propulsion. Depending on small variations in swimming kinematics, undulating fins can swim faster near a solid boundary, but can also experience significant increases (~25%) in cost-of-transport. In Chapter 3, I determine how pectoral and pelvic fin locomotion are combined in P. orbignyi during augmented punting, a hybrid of pectoral and pelvic fin locomotion sometimes employed as stingrays move across a substrate. The timing of pectoral and pelvic fin motions is linked, indicating coordination of thrust production. Chapter 4 discusses pectoral fin structure and morphological variations within the fin, correlating morphology with the swimming kinematics observed in Chapter 1. Passive and active mechanisms may stiffen the anterior fin to create the stable leading edge seen during swimming; stingrays have converged on several structural features (fin ray segmentation and branching) shared by actinopterygian fishes.

Rajiform locomotion in fishes is dominated by distinctive undulations of expanded pectoral fins. Unlike other fishes, which typically interact with the fluid environment via multiple fins, undulating rays modulate a single control surface, the pectoral disc, to perform pelagic locomotion, maneuvering and other behaviors. Complex deformations of the broad, flexible pectoral fins occur as the undulating wave varies in three dimensions; pectoral fin kinematics and changes in waveform with swimming speed cannot be fully quantified by two-dimensional analyses of the fin margin. We present the first three-dimensional analysis of undulatory rajiform locomotion in a batoid, the freshwater stingray Potamotrygon orbignyi. Using three cameras (250framess–1), we gathered three-dimensional excursion data from 31 points on the pectoral fin during swimming at 1.5 and 2.5disclengthss–1, describing the propulsive wave and contrasting waveforms between swimming speeds. Only a relatively small region of the pectoral fin (~25%) undulates with significant amplitude (>0.5cm). Stingrays can maintain extreme lateral curvature of the distal fin margin in opposition to induced hydrodynamic loads, ʻcuppingʼ the edge of the pectoral fin into the flow, with potential implications for drag reduction. Wave amplitude increases across both anteroposterior and mediolateral fin axes. Along the anteroposterior axis, amplitude increases until the wave reaches mid-disc and then remains constant, in contrast to angulliform patterns of continuous amplitude increase. Increases in swimming speed are driven by both wave frequency and wavespeed, though multivariate analyses reveal a secondary role for amplitude.

Inspired by the relatively simple morphological blueprint provided by batoid fish such as stingrays and skates, we create a biohybrid system that enables an artificial animal, a tissue-engineered ray, to swim and phototactically follow a light cue. By patterning dissociated rat cardiac myocytes on an elastomeric body enclosing a microfabricated gold skeleton, we replicated fish morphology at one-tenth scale and captured basic fin deflection patterns of batoid fish. Optogenetics allows for phototactic guidance, steering and turning maneuvers. Optical stimulation induced sequential muscle activation via serpentine patterned muscle circuits leading to coordinated undulatory swimming. The speed and direction of the ray was controlled by modulating light frequency and by independently eliciting right and left fins, allowing the biohybrid machine to maneuver through an obstacle course.