Path tortuosity changes the transport cost paradigm in terrestrial animals

Rory P Wilson,Richard Gunner,Anne Loison,M Rowan Brown,Mathieu Garel,Melitta A Mcnarry,Luca Börger,Michael S Painter,Mark D Holton,Pascal Marchand,Richard S Metcalfe,Kelly A Mackintosh,Kayleigh A R Rose,James Redcliffe,Miloš Ježek ,Nikki J Marks ,Carole Toïgo ,Nigel C Bennett ,Václav Silovský ,David Scantlebury

doi:10.1111/ecog.05850

Abstract

The time that animals spend travelling at various speeds and the tortuosity of their movement paths are two of the many things that affect space‐use by animals. In this, high turn rates are predicted to be energetically costly, especially at high travel speeds, which implies that animals should modulate their speed according to path characteristics. When animals move so as to maximize distance and minimize metabolic energy expenditure, they travel most efficiently at the speed that gives them a minimum cost of transport (COTmin), a well‐defined point for animals that move entirely in fluid media. Theoretical considerations show though, that land animals should travel at their maximum speed to minimize COT, which they do not, instead travelling at walking pace. So, to what extent does COTmin depend on speed and turn rate and how might this relate to movement paths? We measured oxygen consumption in humans walking along paths with varied tortuosity at defined speeds to demonstrate that the energetic costs of negotiating these paths increase disproportionately with both speed and angular velocity. This resulted in the COTmin occurring at very low speeds, and these COTmin speeds reduced with increased path tortuosity and angular velocity. Logged movement data from six free‐ranging terrestrial species underpinned this because all individuals turned with greater angular velocity the slower their travel speeds across their full speed range. It seems, therefore, that land animals may strive to achieve minimum movement costs by reducing speed with increasing path variability, providing one of many possible explanations as to why speed is much lower than currently predicted based on lab measurements of mammalian locomotor performance.

Highlights

Movement is a fundamental tenet of the animal kingdom, with animals moving at varying speeds in chosen directions to use space over time in defined ways that is presumed to enhance their survival and lifetime reproductive success (Williams et al 2002)
3-D plots of the interrelationship between metabolic power or the cost of transport with speed and angular velocity demonstrate how power increased disproportionately with increasing angular velocity, which resulted in clear COTmin that did not occur at the higher walking speeds
Previous works have indicated that turns are energetically costly (Wilson et al 2013, McNarry et al 2017) but, due to their experimental protocol, these authors could not define how the costs of transport relate to angular velocity and speed, nor that angular velocity could have created clear minima in costs of transport at such low speeds

Summary

Introduction

Movement is a fundamental tenet of the animal kingdom, with animals moving at varying speeds in chosen directions to use space over time in defined ways that is presumed to enhance their survival and lifetime reproductive success (Williams et al 2002). 3) animals may move at a speed that minimizes the cost of transport (COTmin speed), maximizing the distance travelled per unit of energy (Tucker 1970, Watanabe et al 2011). The lowest theoretical costs of transport in terrestrial animals should occur at their maximum speeds (but see Hoyt and Taylor 1981, Daley et al 2016). These are not the speeds at which animals normally travel as they move through their environment in natural contexts (Schooley et al 1996). We equipped six species of free-living animal with tags that allowed us to study animal speed in tandem with angular velocity to see how our physiological findings translated into patterns of movement in the natural environment

Participants

Results

Discussion