Consequences of lost endings: caudal autotomy as a lens for focusing attention on tail function during locomotion

Abstract

Autotomy has evolved in many animal lineages as a means of predator escape, and involves the voluntary shedding of body parts. In vertebrates, caudal autotomy (or tail shedding) is the most common form, and it is particularly widespread in lizards. Here, we develop a framework for thinking about how tail loss can have fitness consequences, particularly through its impacts on locomotion. Caudal autotomy is fundamentally an alteration of morphology that affects an animal's mass and mass distribution. These morphological changes affect balance and stability, along with the performance of a range of locomotor activities, from running and climbing to jumping and swimming. These locomotor effects can impact on activities critical for survival and reproduction, including escaping predators, capturing prey and acquiring mates. In this Commentary, we first review work illustrating the (mostly) negative effects of tail loss on locomotor performance, and highlight what these consequences reveal about tail function during locomotion. We also identify important areas of future study, including the exploration of new behaviors (e.g. prey capture), increased use of biomechanical measurements and the incorporation of more field-based studies to continue to build our understanding of the tail, an ancestral and nearly ubiquitous feature of the vertebrate body plan.

What is known and what is not yet known about deflection of the point of a predator’s attack

“…Considering first the deflective use of autotomic tails in lizards, despite the obvious defensive benefit, the resulting escape unavoidably comes at a cost. In many lizards, the tail acts as a fat store and so the loss of this fat store may make an individual more at risk from starvation (McConnachie & Whiting 2003;Gillis & Higham 2016). However, the distribution of energy reserves in species showing autotomy may mean that caudal fat storage does not always come into conflict with tail loss (Chapple & Swain 2002).…”

“…However, the distribution of energy reserves in species showing autotomy may mean that caudal fat storage does not always come into conflict with tail loss (Chapple & Swain 2002). A lizard's tail also has other functions, such as balance (Ballinger 1973;Gillis et al 2009;Libby et al 2012;Gillis & Higham 2016) and thermoregulation (Martin & Salvador 1993), and so tail loss comes with a number of costs alongside loss of fat store and a predator avoidance mechanism. Fundamentally, caudal autotomy may alter an animal's morphology such that its mass and mass distribution are affected, influencing locomotor activities often critical for survival and reproduction (see Bateman & Fleming (2009) and Gillis & Higham 2016 and references therein).…”

Conflicting evidence for the use of caudal autotomy in mesosaurs

“…While it has never been thoroughly investigated and little is known about their swimming habits, it has been suggested that mesosaurs could have used a sub-anguilliform (axial undulations that involve most of the body length, but especially the tail) mode of swimming 30,33 . If mesosaurs could autotomize their tails, this would have significantly affected their swimming capabilities and ability to catch prey 34 . The presence of autotomous caudal vertebrae in mesosaurs therefore leads us to question how important the tail was in propelling them through the water.…”

Patterns of growth in the presacral vertebral column of the leopard gecko (Eublepharis macularius)

“…The tail is held off the ground as the lizard walks at a normal pace, the standing wave produced by locomotory undulations of the trunk being transmitted as a travelling wave producing undulations in the tail (Jagnandan & Higham, 2017). The tail is autotomic (Cheek, 2005;Jagnandan et al 2014;Lynn et al, 2013;Russell et al, 2015), and loss of the entire tail results in the instantaneous loss of a considerable amount of weight (20-23% of total body mass in juveniles [Lynn et al, 2013]; 25% of total body mass in adults [Jagnandan et al, 2014]), and to the sudden absence of an appendage that plays a significant locomotory role (Gillis & Higham, 2016;Jagnandan & Higham, 2017). E. macularius adopts a more sprawling locomotory posture after tail loss, principally through adjustment of the angles adopted by the segments of the hindlimb, and pelvic rotation is reduced (Jagnandan & Higham, 2017;Jagnandan et al, 2014), but walking speed is unaffected (Jagnandan & Higham, 2017).…”