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Consequences of Lost Endings: Caudal Autotomy As a Lens for Focusing Attention on Tail Function During Locomotion Gary Gillis1,* and Timothy E

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Consequences of Lost Endings: Caudal Autotomy As a Lens for Focusing Attention on Tail Function During Locomotion Gary Gillis1,* and Timothy E © 2016. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2016) 219, 2416-2422 doi:10.1242/jeb.124024 COMMENTARY Consequences of lost endings: caudal autotomy as a lens for focusing attention on tail function during locomotion Gary Gillis1,* and Timothy E. Higham2 ABSTRACT and maneuverability during flight (e.g. Sachs, 2007; Schmieder Autotomy has evolved in many animal lineages as a means of et al., 2014). predator escape, and involves the voluntary shedding of body Given this functionality, caudal autotomy, or the voluntary loss of parts. In vertebrates, caudal autotomy (or tail shedding) is the parts of the tail, might strike some as a particularly extreme measure most common form, and it is particularly widespread in lizards. to employ when escaping a predator. However, extreme measures Here, we develop a framework for thinking about how tail loss can are often called for when life is on the line, and the prospect of have fitness consequences, particularly through its impacts on losing an appendage becomes a little less problematic when that locomotion. Caudal autotomy is fundamentally an alteration of appendage can be regenerated. Among invertebrates, autotomized morphology that affects an animal’s mass and mass distribution. appendages vary widely and include limbs, antennae and feeding These morphological changes affect balance and stability, along structures (Fleming et al., 2007). But in vertebrates, the tail is the with the performance of a range of locomotor activities, from appendage most commonly subject to this self-induced shedding. running and climbing to jumping and swimming. These locomotor Although it is observed in a few mammals (e.g. Sumner and Collins, effects can impact on activities critical for survival and 1918) and amphibians (e.g. Wake and Dresner, 1967), caudal reproduction, including escaping predators, capturing prey and autotomy is most thoroughly studied in reptiles, and especially acquiring mates. In this Commentary, we first review work lizards (see Bateman and Fleming, 2009, for a recent review). illustrating the (mostly) negative effects of tail loss on locomotor Within lizards, interest has largely focused on understanding the performance, and highlight what these consequences reveal potential costs of tail loss for the animal, which can include about tail function during locomotion. We also identify important consequences for reproductive output, social status and energetics, ’ areas of future study, including the exploration of new behaviors in turn affecting an animal s fitness (Arnold, 1984; Maginnis, (e.g. prey capture), increased use of biomechanical 2006). Loss of the tail can also impact on fitness by affecting the measurements and the incorporation of more field-based studies way an animal moves, and a rapidly growing body of work is to continue to build our understanding of the tail, an ancestral and exploring the impact(s) of caudal autotomy on locomotion and nearly ubiquitous feature of the vertebrate body plan. locomotor performance (see McElroy and Bergmann, 2013, for a recent review). KEY WORDS: Lizard, Running, Jumping, Performance Although, from the animal’s perspective, the loss of major portions of the tail may pose serious locomotor consequences, Introduction from the perspective of the functional morphologist, it opens Many of us learned in introductory biology about the fundamental opportunities to better understand the important roles that tails play anatomical features that characterize vertebrates and other during routine modes of locomotion. Indeed, one can think of chordates, including the tail, a post-anal extension of the body’s caudal autotomy as presenting a natural experiment of sorts for axis and associated tissues (Kardong, 2009). As a fundamental studying how tails influence locomotor behavior. Like a physical or feature of vertebrates, tails are also strikingly diverse. Consider the mathematical modeler who can remove or eliminate specific parts of grossly asymmetrical caudal fin of the thresher shark as compared a system to gain insight into what happens when they are gone, a with its symmetrical counterpart in a great white, or the remarkable functional morphologist studying autotomy can assess an animal’s fan of the peacock relative to the long forked tail of the booted locomotion before and after tail loss, and make some inferences racket-tail hummingbird. Such anatomical diversity is matched by about the functional role of the tail when it is intact. functional breadth. Tails are known to be used for mate attraction In this Commentary, we outline a framework for thinking about (Bischoff et al., 1985), mating (Shine et al., 1999), grasping (Garber how tail loss affects locomotion (Fig. 1), and we review results from and Rehg, 1999) and defense (Arbour, 2009), among many other past studies to inform and support this framework. Finally, we also specialized roles. However, tails are likely to have evolved in include a discussion of potential areas ripe for future research. vertebrates as locomotory structures (Gans, 1989) and, as such, Although a number of different vertebrate groups undergo caudal currently serve myriad functions in multiple environments, autotomy, including salamanders (Wake and Dresner, 1967), lizards including aquatic propulsion (e.g. Feilich and Lauder, 2015; (Bellairs and Bryant, 1985; Arnold, 1984), snakes (Cooper and Flammang et al., 2011), balance in terrestrial and arboreal habitats Alfieri, 1993) and some rodents (McKee and Adler, 2002), the bulk (e.g. Larson and Stern, 2006; Walker et al., 1998) and in-air stability of our discussion below will focus on lizards, which are by far the best-studied group in the context of how tail loss affects locomotion. 1Department of Biology, Mount Holyoke College, South Hadley, MA 01075, USA. 2Department of Biology, University of California, Riverside, CA 92521, USA. A framework for investigating caudal autotomy In Fig. 1 we outline a framework, based on Arnold’s morphology, *Author for correspondence ([email protected]) performance, fitness paradigm (Arnold, 1983), and the expanded G.G., 0000-0002-8553-7821 paradigm described by Garland and Losos (1994) that includes Journal of Experimental Biology 2416 COMMENTARY Journal of Experimental Biology (2016) 219, 2416-2422 doi:10.1242/jeb.124024 constrained by biomechanics (Fig. 1). Caudal autotomy can be Glossary thought of simply as a change, albeit rapid and potentially quite Moment of inertia radical, in morphology – an animal with an intact tail is transformed A body’s tendency or ability to resist rotation about an axis. into an animal missing part or all of that tail. That change in Ground reaction force morphology has physiological and biomechanical consequences, ’ The force exerted by the ground against the body in reaction to the body s such as altering the position of the center of mass (CoM), decreasing exertion of a force against the ground. Inertial appendage available energy stores or modifying the way axial and limb muscles An appendage, like the tail, whose movements give rise to inertial forces might be recruited (Fig. 1). Those physiological and biomechanical that can be used to move or reorient the body. consequences can then alter performance (e.g. sprint speed) and locomotor behavior (e.g. running kinematics) that, in turn, can affect tasks relevant to fitness such as escaping predators or capturing prey behavior, for thinking about how tail loss ultimately can affect (Fig. 1). Below, we review past literature to establish the validity of ecological functions with fitness consequences (such as predator this framework, before proceeding to highlight important areas of evasion and prey capture) through its effects on locomotor future research. biomechanics, behavior and performance. Here, we consider performance as a quantitative measure of how well an animal Morphological, physiological and biomechanical executes an ecologically relevant task that is vital for survival consequences of tail loss (Irschick and Higham, 2016). Thus, behavior and performance are The two immediate consequences of losing part of the tail are the inextricably linked (performance constrains behavior), and both are reduction in body mass and subsequent anteriorly directed shift in the animal’s CoM (Figs 1 and 2). Lizard tails and bodies span a range of sizes and proportions, so autotomy events can have Mate acquisition a variety of impacts on body mass. For example, an animal with a Prey capture long slender tail that autotomizes just the tip is likely to experience a (tasks) Escape predation Territoriality Fitness negligible change in body mass as compared with animals with more robust tails, which can account for close to 25% of body mass (Higham and Russell, 2010; Jagnandan et al., 2014). Similarly, subsequent shifts in the position of the CoM can be negligible or up to 15–20% of snout–vent length, depending on the amount of tail Jumping lost and the relative length and mass of the tail in relation to the body Swimming (Fig. 2). In some lizards, the tail is also an important site for storing Climbing Running lipids, so that in addition to losing mass and having their CoM Behavior position shift, animals may also be losing critical energy stores – – when parts of a tail are lost (e.g. Dial and Fitzpatrick, 1981; Fleming + – – et al., 2009). Constrains Further, in addition to causing a rapid change in body mass, caudal autotomy can lead to reduced frictional resistance in animals whose Speed Endurance Balance tails drag against the ground (Snyder, 1952). And in species for which Maneuverability Stability the tail serves as an inertial appendage (see Glossary) (Jusufi et al., Performance , Position Muscle Constrains function of CoM Body mass biomechanics physiology and Morphology Tail autotomy Intraspecific Predation competition attempt Fig. 1. A framework for thinking about the ways in which autotomy can affect organismal fitness. Autotomy affects morphology, physiology and biomechanics by altering several key traits, and these in turn will alter behavioral outcomes via changes in performance. Lower level traits (e.g. Fig. 2. Tail loss affects the position of the center of mass.
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