Go Reconfigure: How Fish Change Shape as They Swim and Evolve

Abstract

The bodies of fish change shape over propulsive, behavioral, developmental, and evolutionary time scales, a general phenomenon that we call "reconfiguration". Undulatory, postural, and form-reconfiguration can be distinguished, studied independently, and examined in terms of mechanical interactions and evolutionary importance. Using a combination of live, swimming fishes and digital robotic fish that are autonomous and self-propelled, we examined the functional relation between undulatory and postural reconfiguration in forward swimming, backward swimming, and yaw turning. To probe how postural and form reconfiguration interact, the yaw turning of leopard sharks was examined using morphometric and kinematic analyses. To test how undulatory reconfiguration might evolve, the digital robotic fish were subjected to selection for enhanced performance in a simulated ecology in which each individual had to detect and move towards a food source. In addition to the general issue of reconfiguration, these investigations are united by the fact that the dynamics of undulatory and postural reconfigurations are predicted to be determined, in part, by the structural stiffness of the fish's body. Our method defines undulatory reconfiguration as the combined, point-by-point periodic motion of the body, leaving postural reconfiguration as the combined deviations from undulatory reconfiguration. While undulatory reconfiguration appears to be the sole or primary propulsive driver, postural reconfiguration may contribute to propulsion in hagfish and it is correlated with differences in forward, and backward, swimming in lamprey. Form reconfigures over developmental time in leopard sharks in a manner that is consistent with an allometric scaling theory in which structural stiffness of the body is held constant. However, correlation of a form proxy for structural stiffness of the body suggests that body stiffness may scale in order to limit maximum postural reconfiguration during routine yaw turns. When structural stiffness and undulatory frequency are modeled as determining the tail's undulatory wave speed, both factors evolve under selection for enhanced foraging behavior in the digital fish-like robots. The methods used in making these distinctions between kinds of reconfiguration have broad applicability in fish biology, especially for quantifying complex motor behaviors in the wild and for simulating selection on behavior that leads to directional evolution of functional phenotypes.

Robotic Models for Studying Undulatory Locomotion in Fishes

“…The promise of robotic models for studying the biomechanics of locomotion in fishes has just begun to be realized (Curet et al, 2011;Long et al, 2006Long et al, , 2010Tangorra et al, 2010Tangorra et al, , 2011, and fundamental questions relating to the mechanics of undulatory propulsion remain to be addressed. In particular, key unresolved issues are the extent to which changes in body stiffness during propulsion affect locomotor performance (see Long & Nipper, 1996) and how active modulation of stiffness during an undulatory cycle and across changes in swimming speed are achieved and affect propulsive speed and efficiency.…”

A robotic fish caudal fin: effects of stiffness and motor program on locomotor performance

“…Studies like these have used the caudal fin to create forward propulsion and to control simple turning maneuvers by biasing the flapping of the fin to one side of the robot. This approach has proven useful for a number of fish-inspired robotic designs (Barrett et al, 1999;Alvarado and Youcef-Toumi, 2006;Long et al, 2006;Zhang et al, 2008;Anton et al, 2009;Long et al, 2010;Low and Chong, 2010). However, a two-dimensional flatplate-like representation of the three-dimensional (3-D) fin motion without the ability to actively control tail conformation means that it is difficult for current robotic designs to control the direction and magnitude of the force vector.…”

Sustained periodic terrestrial locomotion in air‐breathing fishes

“…Many species of air-breathing fishes that voluntarily emerge onto land possess an elongate body form (Gillis, 1998;Clardy, 2012), including the American eel Anguilla rostrata (LeSueur 1817), the ropefish Erpetoichthys calabaricus Smith 1865 and the rock prickleback Xiphister mucosus (Girard 1858). Because of the shape of the body and the position, orientation and size of the fins (Ward & Mehta, 2010), these elongate fishes are compelled to use the axial body to produce locomotor movements on land and are unable to partition locomotor tasks to different musculoskeletal elements across environments.…”

“…Many fishes known to make terrestrial excursions have elongated body forms, relative to fully aquatic bony fishes. Based on the available anatomical data (Ward & Mehta, 2010;Gibb et al, 2013), no amphibious fish has a fineness ratio (body length divided by body depth; Webb, 1975) of 4·5 or less, although a streamlined body shape with a fineness ratio approaching 4·5 is common among fishes that dominate the aquatic realm (Webb, 1975;Ward & Mehta, 2010). Shorter body forms may limit the ability of the axial musculature to produce undulation-based terrestrial locomotion, perhaps because the axial body becomes too stiff due to the combination of a limited number of vertebral joints and dorsoventral extension of vertebral elements (Ashley-Ross et al, in press).…”

“…Shorter body forms may limit the ability of the axial musculature to produce undulation-based terrestrial locomotion, perhaps because the axial body becomes too stiff due to the combination of a limited number of vertebral joints and dorsoventral extension of vertebral elements (Ashley-Ross et al, in press). While amphibious fishes studied to date often have elongated body forms (fineness ratios >6; Ward & Mehta, 2010), all highly elongated fishes (fineness ratios >8.5; Ward & Mehta, 2010) appear to employ axial-based lateral undulations during terrestrial locomotion. In fact, as highly elongate fishes increase their number of vertebrae, they simultaneously reduce the size of the pectoral fin (Ward & Brainerd, 2007;Ward & Mehta, 2010).…”