Ian K. Bartol - US grants

PROJECT ABSTRACTCollaborative Research. Ontogenetic Changes in Swimming Squid: An Integrative Examination of Jet Structure and Muscular Mechanics

Ian K. Bartol (Old Dominion University), Joseph T. Thompson (Saint Joseph's University), and Paul S. Krueger (Southern Methodist University)

Squids are versatile swimmers, having the ability to hover in one spot, change direction or orientation rapidly with apparent ease, and ascend/descend almost vertically. Although squids have fins and arms that are used to varying degrees for propulsion, stability, and maneuverability, it is the pulsed jet that is the foundation of the locomotive system. Pulsed jets in squids, which differ from the more familiar undulatory locomotion of fishes, aquatic reptiles, and aquatic mammals, are generated by alternately filling an internal mantle cavity with water and ejecting that water by powerful mantle contractions through a maneuverable funnel. Pulsed jetting is used by squids of remarkably different sizes, from hatchlings that are only a few millimeters in length to adults that may grow as large as 18 m. Over this wide size range, the physics of fluids plays an important role in the evolution of various jet features (e.g., characteristic vortices known as vortex rings) that are central to propulsive swimming performance. This collaborative project investigates how fluid mechanical constraints shape swimming strategies and muscular mechanics in squid of different life history stages, with the ultimate goal of assessing how propulsive efficiency changes with size. To accomplish this, jet flows, body movements, and muscle properties will be examined in two species of squids, the brief squid Lolliguncula brevis and the oval squid Sepioteuthis lessoniana. These squids, which vary in total length from < 1 cm as hatchlings to >15 cm as adults, will be trained to swim in a flow tank (i.e., an aquatic "treadmill") containing water seeded with light-reflective particles. As particle-laden water is expelled from the funnel, it will be illuminated with lasers and videotaped so that the jet velocity can be determined using a technique known as digital particle image velocimetry (DPIV). These DPIV data will provide direct measurements of jet features and propulsive efficiency. Multiple video cameras positioned on a motorized rail system will be used to collect high-resolution images of the mantle and funnel as the squids swim, providing valuable data on swimming behavior. Because the contractile properties of the mantle change with size and have direct effects on jet flows, detailed measurements of isolated bundles of mantle muscle also will be made using standard muscle mechanical techniques. The integration of DPIV, swimming footage, and muscle mechanical data promises to broaden our understanding of propulsive efficiency in jet-propelled organisms, especially at low size ranges where little is known about the jet mechanism, and provide insight into the evolution of ontogenetic changes in musculoskeletal support systems. These data are relevant not only for biological investigators but also for engineers and designers of emerging technologies, such as synthetic jets and pulsed-jet micro-vehicles. This project will engage undergraduate and graduate students in interdisciplinary research. It will also facilitate minority student involvement, either through direct participation in experiments or through educational development in local public schools and aquariums.

Quantitative assessment of animal swimming performance is essential to gaining an understanding the ability of aquatic species to compete in and withstand changes in their environment. A thorough understanding of swimming performance requires quantifying both the motion of the propulsors and the resulting fluid flow. For the myriad aquatic animals that use them, the ability to quantify simultaneously fluid flows produced by their various propulsors is constrained by the current methodological approaches that measure flow in only two dimensions. In this project, the investigators propose a novel 3D approach for studying swimming animals. They will focus on the two separate, but coordinated, propulsive systems of squid (jets and fins) as follows: (1) collect 3D data of the complete fluid flow (wake) generated by swimming squid (both fin and jet wakes simultaneously) and 3D kinematic data of the swimming motion; (2) apply new mathematical tools to quantitatively distinguish between hydrodynamic and kinematic patterns (i.e., gaits) based on their physical features; and (3) evaluate the propulsive performance (i.e., thrust and efficiency) associated with gaits identified in step 2. This quantitative approach will illuminate the selective pressures driving the structure, mechanics, and dynamics of the musculoskeletal system that powers and supports the propulsors. This research holds great promise for developing a universal framework for gait identification in any swimmer or flyer, especially those employing multiple propulsors, and thus may potentially transform current methods for studying locomotion. Beyond the field of biology, this quantitative, 3D approach could provide a valuable framework for engineers of bioinspired propulsion systems, who may be seeking improved propulsive performance in compact designs similar to what nature offers. Finally, the collaborative interdisciplinary nature of this project will allow undergraduate and graduate students with diverse backgrounds in physiology, biomechanics, and engineering to interact and acquire training in cutting edge technologies.

Squids and cuttlefishes are impressive swimmers, having the ability to hover, change direction rapidly, and even swim forward and backward with ease. The key to their locomotive prowess is coordination among their pulsed jet, flapping fins, and flexible arms, but little is presently known about how these units work together throughout these animals' lives as they encounter different physical environments, change developmentally, and experience dissimilar ecosystems. This project focuses on understanding how the jet, fins, and arms operate in concert to produce the necessary forces for exceptional turning, both in terms of muscle capabilities and hydrodynamics, in squid and cuttlefish of different developmental stages (hatchlings to adults). This work will involve cutting edge 3D flow visualization approaches, high-speed video analysis, and advanced mathematical tools that highlight the essential components of high-performance turns. This project promises to (1) advance our understanding of how highly maneuverable marine animals navigate through their complex habitats and (2) reveal key performance characteristics, structures, and behaviors that can be integrated potentially into the design of mechanical bio-inspired systems, such as autonomous underwater vehicles, to improve their turning/docking capabilities. This project incorporates a number of outreach projects, including demonstrations in local schools, participation in robotics competitions, development of web-based tutorials and summer camps, and presentations at aquariums and museums.

Maneuvering in the aquatic environment is a significant component of routine swimming, with proficient maneuvering being essential for predator avoidance, prey capture, and navigation. Despite its importance, understanding of the biomechanics of maneuvering behaviors is limited. An investigation of maneuvering performance in three morphologically distinct species of cephalopods is proposed here. The investigation explores three broad questions: (1) how are the fins, arms, and funnel-jet complex used in concert to maximize turning performance in adult cephalopods; (2) do the relative importance of turning rate and turning radius change over ontogeny and are fewer turning modes observed in young cephalopods; and (3) do fin, arm, and funnel musculoskeletal mechanics change over ontogeny and are such changes associated with differences in maneuvering? These questions will be addressed by collecting measurements of 3D high-speed kinematics and 2D/3D hydrodynamics of wake flows; performing mathematical analyses to quantitatively identify and categorize turning patterns; and measuring both the dynamic passive and active length-force relationship and maximum shortening velocity of muscle fibers that drive the movements used during turning and jet vectoring. The proposed work will: (1) provide data on how an ecologically important marine animal coordinates its novel dual-mode system (jet and fins) and arms to achieve high turning performance, (2) highlight the essential kinematic and hydrodynamic elements of turns, (3) offer insights into how maneuvering capabilities change over a broad ontogenetic range, and (4) provide novel data on the muscle properties of muscular hydrostatic organs and their role in turning.