Terrestrial locomotion in elongate fishes: exploring the roles of morphology and substrate in facilitating locomotion

Abstract

Highly elongate body plans have evolved multiple times in the Actinopterygii, and members of many of these groups are known to use lateral undulation on land. Here, we quantified components of the axial skeleton for four phylogenetically disparate actinopterygian fishes and one sarcopterygian to determine whether axial morphology may affect their locomotor kinematics. We tested species in water and on two terrestrial substrates: loose wet pebbles and wet sand. Differences in axial morphology translated to differences in wavelengths, amplitudes, and frequencies at the center of the body and tail while swimming, but overall, we consistently observed a similar shift in kinematic patterns when fish were moving on the two terrestrial treatments. Generally, our kinematic data support our hypothesis that elongate fishes increased their wave frequency and shorten their wavelengths on terrestrial substrates but we also observed lower wave amplitudes contrary to our prediction. As anticipated, animals exhibited a higher distance ratio (DR), our metric of locomotor efficiency, at the head, center of the body, and tail in aquatic trials. DRs were between 25% and 50% higher in water compared to terrestrial treatments. Locomotion was less effective on wet sand substrate compared to loose wet pebble substrate as exhibited by the discrepancy in DRs and wave patterns along the fish. These data suggest that loose wet pebble substrates do indeed provide vertical points for lateral force transmission and that highly elongate fish have an advantage when moving along this substrate. Our species varied greatly in their total vertebral numbers, 93–129, and in their proportion of precaudal (42–102) and caudal vertebral numbers (10–64). Therefore, despite major differences in vertebral proportions, we find that fishes with anguilliform body plans share similar suites of kinematic patterns within aquatic versus terrestrial treatments and that a pebble substrate can better facilitate axial movements.

Locomotor kinematics on sand versus vinyl flooring in the sidewinder rattlesnake Crotalus cerastes

“…Previous studies have found kinematic differences on sand vs. solid substrates for many kinds of locomotion. For example, eels differ in their kinematics and performance when moving terrestrially on sand vs. pebble substrates (Mehta et al, 2020;Redmann et al, 2020), box turtles have shorter strides and lower speeds on sand than on Styrofoam (Claussen et al, 2002), human athletes use different ankle and hip joint kinematics during squat jumps on rigid vs. sand surfaces (Giatsis et al, 2004), and a cursorial gecko species was shown to change its body angle and duty factor during transitions from firm to sand surfaces (Naylor and Higham, 2022). On the other hand, one experiment showed that kangaroo rats could hop at 1.8 m s -2 on either sand or a solid surface without changing any of the kinematic variables that were measured (hop period, hop length, duty cycle) (Hall et al, 2022).…”

Snowflake morays, Echidna nebulosa, exhibit similar feeding kinematics in terrestrial and aquatic treatments

“…Many extant fish taxa are able to make terrestrial excursions ( Johnels, 1957 ; Chave and Randall, 1971 ; Pace and Gibb, 2011 , 2014 ; Kawano and Blob, 2013 ; Standen et al, 2016 ; Bressman et al, 2019 ) and either breathe air or withstand hypoxia for extended periods of time ( Sayer, 2005 ). Studies focused on amphibious species have mainly examined the kinematics of fishes moving on land ( Hsieh, 2010 ; Pace and Gibb, 2011 ; Kawano and Blob, 2013 ; Ward et al, 2015 ; Mehta et al, 2020 ), physiological adaptations to the terrestrial environment ( LeBlanc et al, 2010 ; Turko et al, 2019 ) and the genetics therein ( You et al, 2018 ). Fewer studies have explored other behaviors while on land such as socialization ( Taylor et al, 2008 ; Ord and Hsieh, 2011 ) and feeding ( Seghers, 1978 ; Van Wassenbergh et al, 2006 ; Van Wassenbergh, 2013 ; Michel et al, 2014 , 2015a , b ).…”

Mini‐series: The axial skeleton – diversity, patterning, and function

“…In this mini‐series, Mehta et al ., (2020) ask whether axial morphology affects locomotor kinematics in elongate fishes. The authors analyzed how five phylogenetically disparate, elongate fishes with high vertebral counts move in both water and on terrestrial substrates.…”