RELINQUISHING part of the body seems a drastic thing to do under any circumstances. But for many lizards, casting off the tail can mean the difference between life and death in the teeth of a predator. Other animals also shed parts of their bodies easily: many salamanders lose their tails, while brittlestars, spiders, crabs and some insects readily give up arms or legs. This process of self-mutilation is called autotomy, and is often followed by regrowth of the shed part.
Anyone who has tried to catch lizards and ended up clutching only part of the tail knows how effective autotomy is. The strategy also works well against natural predators: isolated tails turn up in the crops of birds of prey and in the stomachs of snakes and carnivorous mammals. Not all lizards get away but enough escape to make the strategy worthwhile. In a carefully controlled experiment in the mid-1970s, Jonathon Congdon and his colleagues at the Arizona State University exposed 30 western banded geckos (Coleonyx variegatus) with complete tails to spotted night snakes (Hypsiglena torquata ochrorhyncha), one of their natural predators. The snakes caught 19 of the geckos, but 11 escaped by shedding part of the tail. In contrast, in an experiment with 12 tailless geckos, the snakes caught all the animals. Similar results have been obtained with other kinds of lizards.
Shedding a tail has two advantages: it allows the lizard to break away from its pursuer, and it leaves a distraction that might divert the predator from further pursuit. After all, the tail often makes a good meal in itself and, unlike the fleeing lizard, is secured, while there is no guarantee that abandoning the tail and pursuing the rest of the lizard will result in capture.
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Most lizards have a standard, rather complex mechanism for shedding the tail, in which breakage takes place through the body of a vertebra (transvertebral autotomy). All vertebrae in the tail, except the first few, have fracture planes running across them. These are often visible in skeletons as partial splits. The planes of weakness continue through the fat, muscles and skin surrounding the vertebrae, so that the tail can break right across at these points. When a predator grasps the tail, muscles in the tail contract, causing the vertebra lying just in front of the point of contact to break. This ensures that the lizard loses the smallest piece of its tail necessary to allow escape. The shed part of the tail often thrashes vigorously, sometimes for five minutes or more, frequently holding the attention of the predator while the lizard flees. The tail muscles of some lizards respire anaerobically for longer than muscles in other parts of the body, which explains why the tail can keep moving for so long after it is detached from the body. The missing part usually regenerates within a few weeks. Although it often looks perfect from the outside, internally the regenerated tail is very different, with a simple tube of cartilage in place of the vertebrae. Once it has regrown, the tail can be broken again, but only in front of the regenerated section, where there are still vertebrae with planes of weakness.
Although this is what happens in most lizards, there are exceptions. For instance, some species have no tail-shedding mechanism at all; others have a simpler method in which breakage takes place between vertebrae (intervertebral autotomy) and these animals do not always grow a replacement part. Complete absence of autotomy and intervertebral breakage are not, as we might expect, successive stages in the development of the widespread transvertebral mechanism. Rather, they are derived from it. During the course of evolution, the complex transvertebral mechanism has been lost many times, and breakage between the vertebrae seems to be a rather inferior redevelopment of the strategy which has appeared as many as eight times.
At first sight, it is puzzling that a device which evidently works very well against predators should have disappeared so often. One factor which is significant in understanding why this is so is that tails are often very useful to their owners. A lizard that loses its tail has to pay the cost later.
In many cases, the tail is important in locomotion. Ground lizards from open habitats acquire most of their forward momentum from the back legs, and the tail acts as a counterpoise to the head and body, concentrating the body’s weight over the hind limbs. Also, because the back legs move in horizontal arcs, they tend to cause the hindquarters to oscillate from side to side, particularly on soft soil where the lizard lacks a firm footing. The tail acts as an inertial damper and controls this oscillation. Experiments show that lizards missing all or part of their tails are usually slower than intact animals of the same size and species and they cannot run so far before becoming exhausted. For lizards that climb in vegetation, the tail is often important in balancing and it may also act as a holdfast by twining around stems and twigs. Aquatic species use their tails for swimming; in some the tail is flattened from side to side, increasing its effectiveness as a paddle.
Lizards may carry more than half of their total reserves of fat in the tail. Loss of these reserves makes the animal more susceptible to starvation, and in temperate areas they are more likely to die in hibernation. Less importantly, the loss can slow the animal’s growth and, in the case of females, reduce the weight or number of eggs in a clutch. In the side-blotched lizard, Uta stansburiana, loss of the tail can lead to a fall in social status. Some forms, such as the Arabian semaphore geckos (Pristurus), which signal with their tails, cannot communicate fully without it. Absence of the tail can have drawbacks, for lizards use their tails in a variety of ways to deter their attackers. Some tails make good whips or clubs; while some are broad and spiny and serve to block the owner’s burrow and keep out enemies. Some Australian geckos of the genus Diplodactylus squirt a sticky noxious liquid from the tail.
The importance of the tail, and so the cost of losing it, varies from species to species. We might expect that species that need their tails most are the ones most likely to have lost the means to shed them, while those that need them least dispense with them most easily. It is possible to test this idea by comparing the usefulness of tails to species that do not shed them with those that retain the mechanism. However, care is needed in making such comparisons. Some whole families of lizards, such as the chameleons and monitors, lack autotomy, and it seems likely that its absence is ancestral. Their tail shedding mechanism was almost certainly lost in the very distant past, so how useful the tail is to present forms may be irrelevant. Because of this, it is important to make comparisons within sets of close relatives where loss of autotomy is likely, in evolutionary terms, to be a recent event.
So there is no simple relationship between the usefulness of a tail and its owner’s ability to keep hold of it after all. On reflection, this is understandable, for the alternatives available to a fleeing lizard are usually stark. When closely pursued it must often either lose its tail or face death at the beak or teeth of its enemy. Given that death, like a diamond, is forever, it would pay to sacrifice even a very valuable tail, unless the loss was inevitably fatal.
Examination of particular cases suggests that not only do the costs of shedding the tail vary between species but so do the benefits. Moreover, while there are probably always tangible costs, benefits are sometimes negligible. Clearly, small and delicate species with many enemies are likely to benefit most from autotomy, although this is not always so. Those species that have lost the ability to shed their tails are generally those that would gain little by doing so, for instance, large species that can defend themselves directly with teeth and claws, and those that live where predators are few, on oceanic islands, for example. Other species that lack autotomy have unpalatable tails that might not distract a predator from continuing its pursuit. The tail in such cases may be very short or slender, so that it contains little nutriment, or is very spiny. Finally, some of the forms that lack autotomy are also slow moving and are unlikely to escape even if they did shed their tails.
More a hazard than a help
Where there is little or no benefit from losing the tail, then autotomy may be more of a hazard than a help. For instance, it could expose lizards to infection where the tail has broken off, and predators might take advantage of fragile tails to harvest them deliberately. Some small Australian monitor lizards – in this instance the predators – seem to do this with species of geckos that are difficult to catch and eat whole.
With species that have full sets of autotomy planes in their tail vertebrae, there is considerable variation in the ease with which they shed their tails. Often, this seems to be determined by the equilibrium between the costs and benefits of shedding tails. As we have seen, in ground lizards the tail is important in balancing the body over the back legs, and in preventing the hindquarters from wobbling. Many lizards that climb on steep rock faces do not have such problems; they use all four limbs to provide traction, so weight does not have to be concentrated over the hind feet and, as these are firmly attached to the rigid rock surface by claws or adhesive pads, they are not so likely to wobble from side to side. The penalties of losing a tail are smaller in these forms, and they seem to shed it more readily.
There is evidence that in some species the fragility of the tail varies in individual lizards, depending on their situation. Certainly, the animals seem to have some neural control over the process, for it is usually more difficult to cause breakage in unconscious lizards than conscious ones. Tame lizards are far less prone to shed their tails than wild animals. Again, observations of European lizards belonging to the lacertid family (wall and sand lizards) show that tails are easily knocked off fleeing animals but are harder to detach once the lizards are caught and held by the body, when autotomy has little advantage, or arguably, none at all. Some observations also suggest that starved geckos are less likely to shed their tails – and lose their shrinking fat reserves – than well-fed ones. Certain skinks appear to delay shedding their tail until it is certain that the predator has a firm grip on it. Several other phenomena are also best understood in terms of costs and benefits in particular circumstances. The ground skink, Scincella laterale, of the eastern US, returns to eat the detached organ if its pursuer has not done so, so limiting the cost, in terms of energy, of losing its tail. Other species become more secretive during the vulnerable period before the tail grows again, and some eat more while the tail is growing.
Among the geckos, which are mostly nocturnal, several forms have tails that break only at the base, so that they lose the whole organ instead of the smallest portion to make good their escape. At first sight, such a strategy is paradoxical, especially as many of the species involved have particularly plump tails well provided with fat, so that the loss is especially costly. But this modification is characteristic of slow species and ones that hunt far from their refuges. These forms are unlikely to escape by speed, so leaving the predator with a particularly worthwhile distraction makes good tactical sense.
Another way of encouraging a predator to devote its attention to the tail, rather than the indispensable head and body, is to make it more conspicuous. Cornered lizards often wave their tails or thrash them vigorously from side to side. Some have brightly coloured tails, and experiments show that these are more effective diversions. The American milk snake, Lampropeltis triangulum, often strikes at the blue tails of baby skinks belonging to the genus Eumeces. If the bright pigment is covered over with paint, the snake almost always attacks the more vulnerable and dull-coloured body. Not surprisingly, bright colouring is most common in lizards that can most afford to lose the tail, such as rock-climbing species, and among those most vulnerable to predators. These include young animals, which are small and easily caught, and active forms from very open habitats where effective camouflage is difficult to achieve.
The distribution and type of colouring often enhances its effect. In species that shed the whole tail the entire organ may be strikingly pigmented. But in forms that lose as little of the tail as possible, the bright colour is best developed towards the tip. Species that are active during the day often have brightly coloured tails that make them obvious to daytime predators with colour vision, such as hawks, while those of nocturnal species are usually banded black and white. In many groups of diurnal lizards, the commonest tail colour is blue or blue-green, a colour that is conspicuous close to but less so at a distance than red or yellow. Blue-green is not likely to attract predators that have not already seen the lizard.
The fact that a lizard has lost its tail tells us something of its history. We might also expect that counting the number of such animals in a population will provide useful information, but interpreting the figures is fraught with difficulty. Some biologists suggest that the proportion of docked animals reflects the degree of predation: the more broken tails, the more frequent the attacks. But as Thomas Schoener, an ecologist from the University of California at Davis, has pointed out, a high proportion of damaged tails could simply reflect the inefficiency of the predator. A truly efficient predator, which regularly caught whole lizards, would leave no broken-tailed survivors in the population.
To complicate matters further, some lizards lose their tails in fights between rivals; and individuals of long-lived species are more likely to lose their tails at some time in their life. Another factor that must be taken into account is how easily lizards of particular species shed their tails. There is certainly a strong correlation between the number of animals that lose tails and the circumstances in which they evolved: more animals have broken tails where the costs of losing a tail are low. Animals belonging to species that climb on open rock surfaces have more broken and regenerated tails than ground dwellers, for example. All these factors probably affect the incidence of damaged tails at times, but teasing them apart requires considerable knowledge of both the lizards concerned and their enemies.
While the incidence of loss varies among those lizards that can shed their tails, some groups of lizards seem to have lost the ability entirely early in their history. In most cases, they have not redeveloped the strategy even though the modern representatives of the families concerned may live in a way very similar to members of other families which retain autotomy and appear to benefit from it. This suggests that tail shedding evolves with difficulty or only in rather special circumstances. Some idea of what these may be are evident among the agamid lizards (the chisel-teeth lizards). While most agamids cannot shed their tails, some have redeveloped the strategy as intervertebral breakage. Indeed, autotomy by this inferior mechanism seems to have evolved as many as eight times within this group. In some cases, part of the tail can be shed but not replaced. If this is so, autotomy should develop only in circumstances where the lizard can afford to dispense with the lost section permanently. This has happened in agamids such as the stellio agamas that live on rocks, but otherwise it only occurs in ground lizards with extremely long tails and which shed just the tip, such as the dragon lizards (Amphibolorus) in Australia.
Tail shedding in lizards is a deceptive phenomenon. At first sight, it seems a simple adaptation that allows animals to escape their enemies. But, like many other strategies for survival, it turns out to be highly complex. In some cases it is finely tuned to the situations in which lizards live and to the proclivities and powers of perception of their predators. In others, previous evolutionary history has determined how it happens and whether it happens at all.
Nicholas Arnold researches in zoology at the Natural History Museum, London.
Further reading ‘Caudal autotomy as a defence’, Biology of the Reptilia, vol 16, 1988, p 235. ‘Autotomy and regeneration in reptiles’, Biology of the Reptilia, vol 15B, 1985, p 301. ‘Evolutionary aspects of tail shedding in lizards and their relatives’, Journal of Natural History, vol 18, 1984, p 127.