Convergence of undulatory swimming kinematics across a diversity of fishes

Abstract

Fishes exhibit an astounding diversity of locomotor behaviors from classic swimming with their body and fins to jumping, flying, walking, and burrowing. Fishes that use their body and caudal fin (BCF) during undulatory swimming have been traditionally divided into modes based on the length of the propulsive body wave and the ratio of head:tail oscillation amplitude: anguilliform, subcarangiform, carangiform, and thunniform. This classification was first proposed based on key morphological traits, such as body stiffness and elongation, to group fishes based on their expected swimming mechanics. Here, we present a comparative study of 44 diverse species quantifying the kinematics and morphology of BCF-swimming fishes. Our results reveal that most species we studied share similar oscillation amplitude during steady locomotion that can be modeled using a second-degree order polynomial. The length of the propulsive body wave was shorter for species classified as anguilliform and longer for those classified as thunniform, although substantial variability existed both within and among species. Moreover, there was no decrease in head:tail amplitude from the anguilliform to thunniform mode of locomotion as we expected from the traditional classification. While the expected swimming modes correlated with morphological traits, they did not accurately represent the kinematics of BCF locomotion. These results indicate that even fish species differing as substantially in morphology as tuna and eel exhibit statistically similar two-dimensional midline kinematics and point toward unifying locomotor hydrodynamic mechanisms that can serve as the basis for understanding aquatic locomotion and controlling biomimetic aquatic robots.

In-line swimming dynamics revealed by fish interacting with a robotic mechanism

“…A key difference is the undulatory characteristic of thrust wakes that are produced by swimming fish. A trailing fish faces the oncoming flow at its head with an oscillating angle of attack, and (unlike the trailing cyclist) the trailing fish oscillates its head during swimming (30) further enhancing the time-dependent variation in flow in the head region. Our analysis showed that as a result of the oscillatory wake impinging on the fish head the pressure distribution in the head region is composed of both positive and negative pressures, and thus effectively reduces the overall pressure drag.…”

Swimming performance of sharks and rays under climate change

“…In fact, fishes display a remarkable diversity of morphology and behaviors to achieve a variety of movements, from longdistance migrations, to fast swimming and escape responses (Lauder 2015). Fish locomotion is a wellstudied topic (Bainbridge 1963;Sfakiotakis et al 1999;Lauder 2015;Saadat et al 2017;Di Santo et al 2021), however studies on the single and combined effect of temperature and acidification on many traits that affect locomotor performance are often lacking within the same group of fishes. The scarcity of "full picture" data sets makes the identification of sensitive and tolerant physiotypes complicated.…”

“…For instance, sharks exhibit an elongated body and swim using mostly their trunk and tail in an undulatory motion, while rays (i.e., skates and rays) have short, stiff head trunk regions forming a disc with slender tail and therefore swim using the pectoral fins (with a few exceptions) in undulatory (i.e., wave-like motion) or oscillatory (i.e., flapping up and down) motions (Rosenberger and Westneat 1999;Rosenberger 2001;Wilga and Lauder 2004). Morphological and kinematic characteristics of the body and fins explain how elasmobranch fishes move and provide cues on important adaptations that are involved with efficient locomotion (Lauder and Di Santo 2015;Di Santo et al 2021). In this review, we examine the effects of ocean warming and acidification on locomotion in sharks and rays.…”

EcoPhysioMechanics: Integrating Energetics and Biomechanics to Understand Fish Locomotion under Climate Change

“…Locomotor performance is a key contributor to the evolutionary success of fishes ( Breder 1926 ; Hunter 1998 ). As a consequence, fish locomotion has been a major topic of investigation for functional morphologists, physiologists, and engineers ( Breder 1926 ; Brett 1967 ; Lighthill 1971 ; Daniel 1984 ; Sfakiotakis et al 1999 ; Bale et al 2014 ; Lauder 2015 ; Di Santo et al 2021 ; Akanyeti et al 2022 ). Fishes display an extraordinary variety of body shapes and locomotor behaviors that they use to escape predators, attack prey, maneuver in complex habitats, perform large scale migrations, school, mate, communicate, and explore the substrate ( Johnson and Bennett 1995 ; Wilga and Lauder 2002 ; Shubin et al 2006 ; Clark 2016 ; Fox et al 2018 ; Jung et al 2018 ; Flowers et al 2020 ).…”

“…While linking climate data and ecophysiology has resulted in the establishment of the prolific field of “conservation physiology” ( Wikelski and Cooke 2006 ; Cooke et al 2013 ), biomechanics has yet to become integrated in many physiological studies, and it is rarely applied to work looking at locomotor performance under climate change scenarios ( Helmuth et al 2005 ; Denny and Helmuth 2009 ; Denny and Gaylord 2010 ; Carrington et al 2015 ; Currier et al 2021 ; Vilmar and Di Santo 2022 ). Successful integration has been slow mostly because physiologists and biomechanists generally focus on different aspects of locomotor performance ( Breder 1926 ; Fry 1947 ; Johnson and Bennett 1995 ; Di Santo et al 2021 ), and there is a lack of unifying frameworks to study mechanics and energetics of movement under a new interdisciplinary umbrella of “ EcoPhysioMechanics .” Ecological physiologists typically quantify the effect of abiotic factors on performance such as, for example, oxygen consumption during locomotion or digestion ( Fry 1947 ; Brett 1967 ; Roche et al 2013 ; Bale et al 2014 ; Deutsch et al 2015 ), while biomechanists focus on the relationship between form and function to understand how organisms move under different physical conditions ( Breder 1926 ; Lindsey 1978 ; Shadwick and Lauder 2006 ; Lauder 2015 ; Di Santo et al 2021 ). Yet, the integration of these two well-established fields, ecophysiology and biomechanics, presents the opportunity to link movement and energetics of locomotion to understand plasticity and selection under environmental change.…”