The Influence of Tail Autotomy on the Escape Response of the Cape Dwarf Gecko, Lygodactylus capensis

Tail autotomy as a defence against predators occurs in many species of lizard. Although tail autotomy may provide an immediate benefit in terms of survival it may nevertheless be costly due to other functions of the tail. For example, tail autotomy may affect the locomotory performance of lizards during escape. We investigated the influence of tail autotomy on the escape performance of the Cape Dwarf Gecko, Lygodactylus capensis, on a vertical and a horizontal surface. Autotomized geckos were significantly slower than intact geckos during vertical escape, whereas tail autotomy did not influence the horizontal escape speed. Backward falling of the autotomized geckos on the vertical platform may explain the reduced speed. In addition, tail autotomy did not significantly affect body curvature and stride length of the geckos. The observed decrease of escape speed on a vertical platform may influence the habitat use and behaviour of these geckos. Ecological consequences resulting from tail autotomy are discussed in light of these findings.     

The cannibalistic snail Agaronia propatula (Caenogastropoda,Mollusca) is reluctant to feed on autotomized ‘tails’ of conspecifics

Autotomy and cannibalism increase the complexity of the life history, population structure, and population dynamics of a species. Species in which autotomy is triggered by cannibalism have rarely been studied. It has been hypothesized that in the intertidal gastropod Agaronia propatula, autotomized tissues are highly attractive to cannibals and so increase the victim’s chance to escape. We tested the hypothesis by presenting autotomized ‘tails’ to foraging animals. The attack rates on autotomized ‘tails’ were lower than those on artificial objects reported previously. Autonomously moving autotomized ‘tails’ were more frequently ignored than non-moving and artificially moved ‘tail’ pieces. Thus, autotomized tissue repelled rather than attracted potential cannibals. Autotomy in A. propatula does not help to defend against cannibalism by offering the cannibal an attractive food item for consumption. It seems possible, though, that autotomized conspecifics are less attractive to cannibals than intact ones due to a repelling action of autotomized tissues.     

Flip,flop and fly: modulated motor control and highly variable movement patterns of autotomized gecko tails

Many animals lose and regenerate appendages, and tail autotomy in lizards is an extremely well-studied example of this. Whereas the energetic, ecological and functional ramifications of tail loss for many lizards have been extensively documented, little is known about the behaviour and neuromuscular control of the autotomized tail. We used electromyography and high-speed video to quantify the motor control and movement patterns of autotomized tails of leopard geckos (Eublepharis macularius). In addition to rhythmic swinging, we show that they exhibit extremely complex movement patterns for up to 30 min following autotomy, including acrobatic flips up to 3 cm in height. Unlike the output of most central pattern generators (CPGs), muscular control of the tail is variable and can be arrhythmic. We suggest that the gecko tail is well suited for studies involving CPGs, given that this spinal preparation is naturally occurring, requires no surgery and exhibits complex modulation.     

Effects of tail autotomy on survival,growth and territory occupation in free‐ranging juvenile geckos (Oedura lesueurii)

Abstract Many animals autotomize their tails to facilitate escape from predators. Although tail autotomy can increase the likelihood of surviving a predatory encounter, it may entail subsequent costs, including reduced growth, loss of energy stores, a reduction in reproductive output, loss of social status and a decreased probability of survival during subsequent encounters with predators. To date, few studies have investigated the potential fitness costs of tail autotomy in natural populations. I investigated whether tail loss influenced survival, growth and territory occupation of juvenile velvet geckos Oedura lesueurii in a population where predatory snakes were common. During the 3‐year mark–recapture study, 32% of juveniles voluntarily autotomized their tails when first captured. Analysis of survival using the program mark showed that voluntary tail autotomy did not influence the subsequent survival of juvenile geckos. Survival was age‐dependent and was higher in 1‐year‐old animals (0.98) than in hatchlings (0.76), whereas recapture probabilities were time‐dependent. Growth rates of tailed and tailless juveniles were very similar, but tailless geckos had slow rates of tail regeneration (0.14 mm day⁻¹). Tail autotomy did not influence rock usage by geckos, and both tailed and tailless juveniles used few rocks as diurnal retreat sites (means of 1.64 and 1.47 rocks, respectively) and spent long time periods (85 and 82 days) under the same rocks. Site fidelity may confer survival advantages to juveniles in populations sympatric with ambush foraging snakes. My results show that two potential fitness costs of tail autotomy – decreased growth rates and a lower probability of survival – did not occur in juveniles from this population. However, compared with juveniles, significantly fewer adult geckos (17%) voluntarily autotomized their tails during capture. Because adults possess large tails that are used for lipid storage, the energetic costs of tail autotomy are likely to be much higher in adult than in juvenile O. lesueurii.     

The regenerated tail of juvenile leopard geckos (Gekkota: Eublepharidae: Eublepharis macularius) preferentially stores more fat than the original

The tail of many species of lizard is used as a site of fat storage, and caudal autotomy is a widespread phenomenon among lizards. This means that caudal fat stores are at risk of being lost if the tail is autotomized. For fat-tailed species, such as the leopard gecko, this may be particularly costly. Previous work has shown that tail regeneration in juveniles of this species is rapid and that it receives priority for energy allocation, even when dietary resources are markedly reduced. We found that the regenerated tails of juvenile leopard geckos are more massive than their original counterparts, regardless of dietary intake, and that they exhibit greater amounts of skeleton, inner fat, muscle and subcutaneous fat than original tails (as assessed through cross-sectional area measurements of positionally equivalent stations along the tail). Autotomy and regeneration result in changes in tail shape, mass and the pattern of tissue distribution within the tail. The regenerated tail exhibits enhanced fat storage capacity, even in the face of a diet that results in significant slowing of body growth. Body growth is thus sacrificed at the expense of rapid tail growth. Fat stores laid down rapidly in the regenerating tail may later be used to fuel body growth or reproductive investment. The regenerated tail thus seems to have adaptive roles of its own, and provides a potential vehicle for studying trade-offs that relate to life history strategy.     

On caudal prehensility and phylogenetic constraint in lizards: The influence of ancestral anatomy on function in Corucia and Furcifer

We examined caudal anatomy in two species of prehensile‐tailed lizards, Furcifer pardalis and Corucia zebrata. Although both species use their tails to grasp, each relies on a strikingly different anatomy to do so. The underlying anatomies appear to reflect phylogenetic constraints on the consequent functional mechanisms. Caudal autotomy is presumably the ancestral condition for lizards and is allowed by a complex system of interdigitating muscle segments. The immediate ancestor of chameleons was nonautotomous and did not possess this specialized anatomy; consequently, the derived arrangement in the chameleon tail is unique among lizards. The limb functions as an articulated linkage system with long tendinous bands originating from longitudinal muscles to directly manipulate vertebrae. Corucia is incapable of autotomy, but it is immediately derived from autotomous ancestors. As such, it has evolved a biomechanical system for prehension quite different from that of chameleons. The caudal anatomy in Corucia is very similar to that of lizards with autotomous tails, yet distinct differences in the ancestral pattern and its relationship to the subdermal tunic are derived. Instead of the functional unit being individual autotomy segments, the interdigitating prongs of muscle have become fused with an emphasis on longitudinal stacks of muscular cones. The muscles originate from the vertebral column and a subdermal collagenous tunic and insert within the adjacent cone. However, there is remarkably little direct connection with the bones. The muscles have origins more associated with the tunic and muscular septa. Like the axial musculature of some fish, the tail of Corucia utilizes a design in which these collagenous elements serve as an integral skeletal component. This arrangement provides Corucia with an elegantly designed system capable of a remarkable variety of bending movements not evident in chameleon tails. J. Morphol. 239:143–155, 1999. © 1999 Wiley‐Liss, Inc.     

Morphogenetic control during tail regeneration in Plethodon cinereus: the role of skeletal muscle

The caudal myofibers of Plethodon cinereus do not appear to participate directly in epimorphic tail regeneration following either autotomy or surgical amputation of the tail. The possibility that tail musculature might indirectly influence morphogenesis of the regenerate was tested by unilaterally removing 99% of the lateral muscle mass for five to six caudal segments. Ten days after muscle ablation, tails were amputated through the deficient area. Unlike previous experiences with ambystomid larvae, P. cinereus regulates completely producing a normal tail regenerate and at a rate comparable to that following simple amputation.     

Frequency of tail loss reflects variation in predation levels,predator efficiency,and the behaviour of three populations of brown anoles

We investigated two predictions regarding the incidence of tail regeneration in lizards for three populations of brown anoles exposed to varying predation levels from the same predator (cats). Firstly although inefficient predators are likely to increase the incidence of regenerated tails (i.e. lizards can escape through tail autotomy), highly efficient predators will kill and eat the lizard and thus leave no evidence of autotomy. At the site with no cats, only 4% of anoles demonstrated signs of tail regeneration. This value was not significantly different from the site where feral cats (i.e. ‘efficient’ predators that would capture prey to eat, as supported by behavioural observation) were present (7%). By contrast, 25% of anoles present at the site with pet cats (well‐fed domesticated cats that caught and played with anoles, i.e. were ‘inefficient’ predators) exhibited regenerated tails. Secondly, more obvious lizards are more susceptible to predation attempts. Supporting this hypothesis, our data indicate a higher incidence of regenerated tails (28%) was recorded amongst adult males (which are territorial, occupying exposed positions) compared to females and subadult males (17%) or juveniles (1%). In conclusion, the behaviour of both the predator and the lizard influences the frequency of regenerated tails in brown anoles. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 648–656.     

Effects of size,caudal autotomy,and predator kairomones on the foraging behavior of Allegheny Mountain dusky salamanders (<Emphasis Type="Italic">Desmognathus ochrophaeus</Emphasis>)

Prey must balance the conflicting demands of foraging and defensive behavior. Foraging under the threat of predation may be further complicated among species that engage in caudal autotomy, the loss of a portion of the tail at preformed breakage planes, because the tail may serve as an important energy storage organ and contribute to motility, culminating in a trade-off between foraging and predator avoidance. As a result of the advantages conferred by the presence of a tail, individuals that have recently undergone autotomy may be more motivated to forage despite elevated levels of threat indicated by predator kairomones. We used a full factorial design to evaluate the combined effects of body size, exposure to predator kairomones, and experience with autotomy on the latency to strike at Drosophila prey, number of strikes, and prey captured per strike by Allegheny Mountain dusky salamanders (Desmognathus ochrophaeus). In our study, caudal autotomy was the only significant main effect and influenced both the latency to attack prey and the number of strikes attempted. In terms of latency to attack prey, there was a significant interaction between body size and autotomy such that “small” salamanders (≤3.2 cm SVL) without tails delayed their foraging behavior. In terms of the number of strikes toward prey, there was a significant interaction between autotomy and exposure to predator kairomones such that individuals with intact tails exhibited a greater number of strikes, with the exception of the “large” (>3.2 cm SVL) salamanders, which performed fewer strikes when exposed to the snake kairomones. There was no significant effect on foraging efficiency, although the trend in the data suggests that autotomized individuals forage more efficiently. This study was designed to evaluate the confluence of factors related to size, caudal autotomy, and exposure to stimuli from predators and hints at the magnitude of caudal autotomy on antipredator decision-making. Our data suggest that despite the importance of tail tissue for energy storage, locomotion, and mating, salamanders without tails are cautious when foraging under elevated risk.     

Effect of temperature,photoperiod, and feeding on the rate of tail regeneration in a semiaquatic plethodontid salamander

Salamander tail autotomy improves survival, but loss of the tail can subsequently be costly. For example, burst swimming speed is significantly slower after autotomy in desmognathan salamanders, which may increase predation risk in aquatic habitats. However, any long-term cost of tail loss is contingent on the rate of tail regeneration. To examine variation among seasons and environments in the cost of tail autotomy, we tested the effect of temperature, photoperiod, and feeding on tail-length re-growth in the semiaquatic plethodontid salamander Desmognathus conanti. Eight experimental groups (n=15 each, equivalent in body size) were tested. After acclimation for four weeks at one of two temperatures (either 10 °C or 20 °C) and one of two photoperiods (either L:D 9.5:14.5 h or 14.5:9.5 h), 60% of the tail length was autotomized for each individual. After autotomy, each experimental group was maintained under unique conditions of temperature (either 10 °C or 20 °C), photoperiod (either L:D 9.5:14.5 h or 14.5:9.5 h), and feeding (either fasting or weekly feeding). The length of the regenerated tail portion for each individual was measured each week until the group with the fastest re-growth had regenerated 50% of the lost tail length. Low temperature had a large, negative effect, fasting had a small, negative effect, but photoperiod had no significant effect on tail re-growth. The large thermal effect resulted from a combination of delayed initiation of tail-length re-growth and reduced regeneration rate thereafter at low temperature. We conclude that the cost of salamander tail autotomy differs among seasons and environments based on variation in temperature and food availability.     

Tail regeneration following autotomy in the adult salamander Desmognathus fuscus

Tail regeneration occurs following autotomy of the tail in the salamander Desmognathus fuscus. Studies based on histology and autoradiography suggest that the cells of the regeneration blastema arise from the connective tissue of the tail stump. Following autotomy of the tail in Desmognathus the muscle of the regenerate is not derived from de differentiated or modulated striated muscle fibers of the autotomy stump. Possible sources of myogenic cells are discussed.     

Ultrastructural changes in skeletal muscle of the tail of the lizard Hemidactylus mabouia immediately following autotomy

Araújo, T.H., Faria, F.P., Katchburian, E. and Freymüller, E. (2009). Ultrastructural changes in skeletal muscle of the tail of the lizard Hemidactylus mabouia immediately following autotomy. —Acta Zoologica (Stockholm) 91 : 440–446. Although autotomy and subsequent regeneration of lizard tails has been extensively studied, there is little information available on ultrastructural changes that occur to the muscle fibers at the site of severance. Thus, in the present study, we examine the ultrastructure of the musculature of the remaining tail stump of the lizard Hemidactylus mabouia immediately after autotomy. Our results show that exposed portions of the skeletal muscle fibers of the stump that are unprotected by connective tissue bulge to produce large mushroom‐like protrusions. These exposed portions show abnormal structure but suffer no leakage of cytoplasmic contents. Many small and large vesicular structures appeared between myofibrils in the interface at this disarranged region (distal) and the other portion of the fibers that remain unchanged (proximal). These vesicles coalesce, creating a gap that leads to the release of the mushroom‐like protrusion. So, our results showed that after the macroscopic act of autotomy the muscular fibers release part of the sarcoplasm as if a second and microscopic set of autotomic events takes place immediately following the macroscopic act of autotomy. Presumably these changes pave the way for the formation of a blastema and the beginning of regeneration.     

Partial tail loss has no severe effects on energy stores and locomotor performance in a lacertid lizard, <Emphasis Type="Italic">Takydromus septentrionalis</Emphasis>

Many species of lizards use caudal autotomy as a defense strategy to avoid predation, but tail loss entails costs. These topics were studied experimentally in the northern grass lizard, Takydromus septentrionalis. We measured lipids in the three-tail segments removed from each of the 20 experimental lizards (adult females) initially having intact tails to evaluate the effect of tail loss on energy stores; we obtained data on locomotor performance (sprint speed, the maximal length traveled without stopping and the number of stops in the racetrack) for these lizards before and after the tail-removing treatments to evaluate the effect of tail loss on locomotor performance. An independent sample of 20 adult females that retained intact tails was measured for locomotor performance to serve as controls for successive measurements taken for the experimental lizards. The lipids stored in the removed tail was positively correlated with tailbase width when holding the tail length constant, indicating that thicker tails contained more lipids than did thinner tails of the same overall length. Most of the lipids stored in the tail were concentrated in the proximal portion of the tail. Locomotor performance was almost unaffected by tail loss until at least more than 71% of the tail (in length) was lost. Our data show that partial tail loss due to predatory encounters or other factors may not severely affect energy stores and locomotor performance in T. septentrionalis.     

Locomotor performance of sand lizards (Lacerta agilis): effects of predatory pressure and parasite load

Locomotor performance affects foraging efficiency, predator avoidance and consequently fitness. Agility and speed determine the animal's social status and reflect its condition. In this study, we test how predatory pressure and parasite load influences locomotor performance of wild specimens of the sand lizard Lacerta agilis. Animals were chased on a 2-metre racetrack. Lizards with autotomy ran significantly faster than lizards with an intact tail, but there was no significant difference in running speed between individuals with fresh caudal autotomy and regenerated tails. Parasite presence and load, age and sex had no significant effect on speed. Our results indicate that autotomy either alters locomotory behaviour or that individuals with autotomised tails were those that previously survived contact with predators, and therefore represented a subgroup of the fastest individuals. Therefore, in general, predatory pressure but not parasites affected locomotor performance in lizards.     

Tail autotomy works as a pre‐capture defense by deflecting attacks

Caudal autotomy is a dramatic antipredator adaptation where prey shed their tail in order to escape capture by a predator. The mechanism underlying the effectiveness of caudal autotomy as a pre‐capture defense has not been thoroughly investigated. We tested two nonexclusive hypotheses, that caudal autotomy works by providing the predator with a “consolation prize” that makes it break off the hunt to consume the shed tail, and the deflection hypothesis, where the autotomy event directs predator attacks to the autotomized tail enabling prey escape. Our experiment utilized domestic dogs Canis familiaris as model predator engaged to chase a snake‐like stimulus with a detachable tail. The tail was manipulated to vary in length (long versus short) and conspicuousness (green versus blue), with the prediction that dog attacks on the tail should increase with length under the consolation‐prize hypothesis and conspicuous color under the deflection hypothesis. The tail was attacked on 35% of trials, supporting the potential for pre‐capture autotomy to offer antipredator benefits. Dogs were attracted to the tail when it was conspicuously colored, but not when it was longer. This supports the idea that deflection of predator attacks through visual effects is the prime antipredator mechanism underlying the effectiveness of caudal autotomy as opposed to provision of a consolation prize meal.     

The effects of tail autotomy on survivorship and body growth of Uta stansburiana under conditions of high mortality

We examined the effects of tail autotomy on survivorship and body growth of both adult and juvenile Uta stansburiana by directly manipulating tail condition. Tail loss decreased neither survivorship nor rate of body growth for individuals in two natural populations. Lack of an influence of tail loss on survivorship in these two populations may be the result of high mortality. Under high mortality any differential effects of tail loss will be lower than in populations facing lower mortality. Growth experiments in the laboratory demonstrated that, under conditions of minimal environmental variation and social interactions, there is no tradeoff between body growth and tail regeneration as has been suggested for other species of lizards. One possible reason for this difference is that U. stansburiana does not use the tail as a storage organ for lipids. The original and regenerated tails are composed mainly of protein. In general, any differential body growth between tailed and tailless individuals may be due to social interactions and not a diversion of limited energy into tail regeneration.     

Ceratal autotomy and regeneration in the aeolid nudibranch Phidiana crassicornis and the role of predators

Abstract. Ceratal autotomy by the aeolid nudibranch Phidinna crassicornis is common in the field and was induced in the laboratory by mechanical and predatory stimuli. The ceras detaches from the body wall along an autotomy plane located at its basal constriction. Cerata released copious amounts of mucus during autotomy and exhibited a prolonged writhing response that continued for several hours after detachment. Regeneration of cerata autotomized in the field and in the laboratory was documented. Four days after autotomy, regenerating cerata appeared as small protuberances. By day 24 the regenerates acquired their mature structural organisation and vivid colour. The cerata subsequently increased in length and diameter and were indistin‐guishable from surrounding cerata by 41 to 43 days after autotomy. Regeneration rates of cerata induced to autotomize in the laboratory and regeneration of cerata autotomized in the field were similar, averaging 0.08 and 0.067 mdday, respectively. The sequence of morphological events involved with regeneration following experimental and natural induction of autotomy was identical. The kelp crab Pugettia productn induced autotomy by holding cerata with its chelae. This crab also fed on autotomized cerata and consumed locomotory and ceratal mucus. Ceratal autotomy may be an important mechanism of escape from this predatory crustacean. Other potential predators including hermit crabs and tidepool sculpins did not elicit defensive behaviour in P. crussicornis. Nematocysts were present in the enidosacs and their role in defense was investigated. Fired nematocysts were observed in podia of the asteroid Crossaster papposus following ceratal contact but were not seen in the podia of Pycnopodia helianthoides in a similar trial. For P. crassicornis, the cnidosacs may function primarily as a storage device for safe sequestering of nematoeysts that could pose a threat to the digestive system. They did not play a major defensive role against the predators tested, but may be important in the field against other predators.     

Spinal cord regeneration in a tail autotomizing urodele

Adult urodele amphibians possess extensive regenerative abilities, including lens, jaws, limbs, and tails. In this study, we examined the cellular events and time course of spinal cord regeneration in a species, Plethodon cinereus, that has the ability to autotomize its tail as an antipredator strategy. We propose that this species may have enhanced regenerative abilities as further coadaptations with this antipredator strategy. We examined the expression of nestin, vimentin, and glial fibrillary acidic protein (GFAP) after autotomy as markers of neural precursor cells and astroglia; we also traced the appearance of new neurons using 5‐bromo‐2′‐deoxyuridine/neuronal nuclei (BrdU/NeuN) double labeling. As expected, the regenerating ependymal tube was a major source of new neurons; however, the spinal cord cranial to the plane of autotomy showed significant mitotic activity, more extensive than what is reported for other urodeles that cannot autotomize their tails. In addition, this species shows upregulation of nestin, vimentin, and GFAP within days after tail autotomy; further, this expression is upregulated within the spinal cord cranial to the plane of autotomy, not just within the extending ependymal tube, as reported in other urodeles. We suggest that enhanced survival of the spinal cord cranial to autotomy allows this portion to participate in the enhanced recovery and regeneration of the spinal cord. J. Morphol. 2011. © 2011 Wiley Periodicals, Inc.     

No behavioural compensation for fitness costs of autotomy in a lizard

Abstract Antipredator mechanisms employed by animals are obviously beneficial if they increase survival, but their use may be costly and decrease fitness. Fitness costs of antipredator mechanisms may, in turn, be defrayed by behavioural compensation. We used lizards as a model to measure behavioural fitness costs of the antipredator mechanism, autotomy, as they commonly lose their tails when attacked by predators. In addition, we examined whether male skinks, Carlia jarnoldae (Scincidae), behaviourally compensate for tail loss by comparing the behaviour of tailed and tailless males in experimental enclosures, either alone, with a conspecific male or female, or with a predator. Tailless males experience several costs of autotomy including reduced energy stores, and loss of autotomy as a defence. We identified an additional cost of tail loss: reduced mating success. However, this species did not behaviourally compensate these costs. Instead, characteristics of the ecology of C. jarnoldae may minimize the costs of autotomy. This species experiences an extended breeding season, which means that they experience reduced mating success for only 20% of this breeding season. Additionally, the presence of inguinal fat stores which supply energy in addition to stores in the tail reduce energetic costs.     

Influence of Social Factors on Seasonal Variations in Plasma Testosterone Levels of Microcebus murinus

Blue tail coloration in hatchling skinks (Eumeces fasciatus and E. laticeps) appears to be an antipredatory adaptation that distracts attention away from the body to the tail. The tail itself serves as a decoy that may be autotomized as a final defense against capture. The effectiveness of intact tails in deflecting attacks from the body was 50% against scarlet kingsnakes in the experimental conditions used. Brightness rather than hue presumably accounts for the higher attack frequency on blue than black tails in this study, but the blue color may have evolved in response to avian predation. Repeated predation without ill effects by several predators allows rejection of the hypothesis that the blue tail is aposematic for the predators tested. The hypothesis that blue tails provide stimuli inhibiting aggression or predation by adult male conspecifics is untenable for E. laticeps because adult males readily eat intact hatchlings. Although this study provides no statistical evidence that blue tail coloration inhibits attack by female E. laticeps on hatchlings, the trend of predation rates on blue- and black-tailed hatchlings is in the direction predicted for inhibition.