The movement dynamics of autotomized lizards and their tails reveal functional costs of caudal autotomy

Abstract

Autotomy has evolved independently several times in different animal lineages. It frequently involves immediate functional costs, so regeneration evolved in many instances to restore the functionality of that body part. Caudal autotomy is a widespread antipredator strategy in lizards, although it may affect energy storage, locomotion dynamics, or survival in future encounters with predators. Here, we assessed the effect of tail loss on the locomotor performance of wall lizards (Podarcis muralis), as well as the recovery of locomotor functionality of lizards with regenerated tails, and the movement dynamics of shed tails that were either intact or having regenerated portions. Tail loss had no effect on locomotion over unhindered spaces, possibly due to compensation between a negative effect on the stride of front limbs, and a positive effect of losing mass and friction force. We found a clear negative impact of tail loss on locomotion in spaces with interspersed obstacles, in which tailed lizards jumped larger distances when leaving the obstacles. Besides, lizards that used the tail to push off the ground were able to approach the obstacles from further, so that the tail seemed to be useful when used during jumping. Regeneration fully restores lizard's locomotor capacities, but tail antipredator value, as indicated by the intensity of post-autotomic movements, is only partially retrieved. From these results, we propose that, together with the recovery of post-autotomy antipredator capacities, the restoration of the organismal locomotor performance may have been an important, yet frequently neglected factor in the evolution of lizard's regeneration ability.

Spinal ganglia and peripheral nerves innervating the regenerating tail and muscles of lizards

“…The innervation of myotomes is, therefore, relatively delayed in the regenerating tails of all different lizard species examined so far so (Fernandez-Rodriguez & Brana, 2020). Only in some geckos where a flexible cartilaginous tube made of elastic chondrocytes is formed, the segmented myomeres attached by connective bands to the cartilaginous axis can cause broad bending and even curling of the regenerated tail (Alibardi & Meyer-Rochow, 1989).…”

“…After the traumatic loss (accidental or predatory) or the voluntary release (autotomy) of the tail, a large organ counting 1/4th-1/6th of the entire body mass, lizards of most families undergo a process of regeneration of the tail (Alibardi, 2010(Alibardi, , 2017Boring et al, 1948-49;Bellairs & Bryant, 1985;Fernandez-Rodriguez & Brana, 2020;Fisher et al, 2012;Fraisse, 1885;Gilbert et al, 2013;Gordeev et al, 2020;Lozito & Tuan, 2016a, 2016b. The new tail is innervated by a simple ependymal tube as a continuation of the tail spinal cord and by numerous nerves that derive from the spinal cord and from the more proximal spinal ganglia to the regenerating tail.…”

“…Despite the rich innervation of muscles, the regenerated tail in most species is rigid and poorly functional and the formation of an un-segmented cartilaginous tube that calcifies after 2-3 months of regeneration, determines further tail stiffness(Alibardi & Meyer- Rochow, 1989;Lozito & Tuan, 2015, 2016a, 2016b. While a regenerated tail recovers most of the efficiency of the normal tail in terms of running speed and balance, instead obstacle avoidance, side flipping and uplifting movements are impaired and antipredatory autotomy quite reduced(Fernandez-Rodriguez & Brana, 2020). Only…”

Behavioral patterns in the early‐stage antipredator response change after tail autotomy in adult wall lizards

“…Autotomy is relatively common among vertebrates and can affect different peripheral expendable parts of the body, such as the limbs, the skin or the tail (Higham et al, 2013). In particular, caudal autotomy to avoid predation is very common and taxonomically widespread in lizards (Bateman & Fleming, 2009; Bellairs & Bryant, 1985; Greene, 1988), to such an extent that in many natural populations more than 50% of adult animals have mutilated or regenerated tails (Chapple et al, 2002; Downes & Shine, 2001; Fernández‐Rodríguez & Braña, 2020, for the herein studied population of Podarcis muralis ).…”

“…Despite the benefits of autotomy to avoid predation, the loss of a body part can entail several immediate consequences, such as decreased locomotor performance, degradation of social status, or restriction in communication between conspecifics, which may negatively affect daily activities, like habitat selection, foraging, moving, mating, or facing new predator encounters (see the reviews of Bateman & Fleming, 2009; Emberts et al, 2019; Lawrence, 2010; Maginnis, 2006). Because of these major drawbacks, autotomy is frequently followed by regeneration of the lost parts, which restores partially or completely their functionality (Fernández‐Rodríguez & Braña, 2020; Lin et al, 2017). However, regeneration takes time and, until it is complete, animals suffer from locomotor impairment and lack the possibility of using the lost parts as a distraction in new encounters with predators, so they might face an increased risk of predation (Fox & McCoy, 2000; Lin et al, 2017).…”