Cent. Eur. J. Biol. • 6(2) • 2011 • 293-299 DOI: 10.2478/s11535-010-0119-9

Central European Journal of Biology

Seeing through the lizard’s trick: do avian predators avoid autotomous tails?

Research Article

Bart Vervust*, Hans Van Loy, Raoul Van Damme

Laboratory for Functional Morphology, Department of Biology, University of Antwerp, B-2610 Wilrijk, Belgium

Received 24 June 2010; Accepted 16 November 2010

Abstract: Counter-adaptations of predators towards their prey are a far less investigated phenomenon in predator-prey interactions. Caudal autotomy is generally considered an effective last-resort mechanism for evading predators. However, in victim-exploiter relationships, the efficacy of a strategy will obviously depend on the antagonist’s ability to counter it. In the logic of the predator-prey arms race, one would expect predators to develop attack strategies that minimize the chance of autotomy of the prey and damage on the predator. We tested whether avian predators preferred grasping lizards by their head. We constructed plasticine models of the Italian wall lizard (Podarcis sicula) and placed them in natural habitat of the species. Judging from counts of beak marks on the models, birds preferentially attack the head and might also avoid the tail and limb regions. While a preference for the head might not necessarily demonstrate tail and limb avoidance, this topic needs further exploration because it suggests that even unspecialised avian predators may see through the lizard’s trick-of-the-tail. This result may have implications for our understanding of the evolution of this peculiar defensive system and the loss or decreased tendency to shed the tail on island systems with the absence of terrestrial predators.

Keywords: Autotomy • Predation • Predatory • Prey arms race • Podarcis sicula © Versita Sp. z o.o.

make a detour and approach spitting spiders (Scytodes 1. Introduction pallidus) from the rear, opposite the end from which There is increasing evidence that predators actually the scytodid’s spit is fired [4]. Broad headed snakes evolve counter-adaptations in response to the defensive (Hoplocephalus bungaroides) may have evolved an adaptations of their prey species. Several cases are extreme sit-and-wait foraging habit because their prey known in which predators have evolved morphological (velvet geckos, Oedura lesueurii) can detect chemicals or physiological mechanisms, which allow them to left behind by moving snakes [5]. circumvent defensive tactics of particular prey. For Caudal autotomy, the ability to shed the tail, is instance, Lake Tanganyika crabs Platytelphusa an intriguing defensive technique that has evolved armata have evolved robust chelae in response to numerous times in a variety of prey animals [6-8]. the unusually hard shells of their gastropod prey (e.g. Many aspects of lizard tail autotomy, including its Spekia, Neothauma) prey [1] and North American histological mechanisms, ecological significance, intra- garter snakes (Thamnophis sirtalis) have become and interspecific variability, phylogenetic distribution resistant to the TTX toxins of Taricha newts [2]. More and evolutionary history have received considerable commonly, animals adapt their predatory behaviour in attention (reviews in [8] and [9]).One facet that has not reaction to the defensive tactics employed by particular been considered is the question of whether predators prey species. Australian death adders (Acanthophis may develop (within a lifetime or on an evolutionary praelongus) have learned to delay the consumption of scale) behavioural mechanisms that lower the toxic toads (Bufo marinus) until the chemical defence effectiveness of tail autotomy as an escape tactic. The loses its potency [3]. Jumping spiders (Portia labiata) high number of autotomized tails – compared to entire

* E-mail: [email protected] 293 Seeing through the lizard’s trick: do avian predators avoid autotomous tails?

lizards – found in predator stomachs [10], indicate on lizards. In 6% of the examined pellets (N=485) we that this is a highly effective antipredator strategy. On were able to find mandibles of lizards (B. Vervust, the other hand, caudal autotomy carries a series of unpublished). This high rate of occurrence suggests important and potentially lifelong costs (for an overview a potentially important predatory role of this gull in see [11]). (insular) lizard populations. More detailed information Here, we investigate the hypothesis that avian on the study system can be found in [21]. predators will prefer grasping lizards by the head to prevent both tail autotomy (inducing the likely escape 2.2 Model construction and experiment of the prey) and reducing the chance of damage to the Because direct observation of predation on lizards is predator. That such behaviour would arise does not difficult, we used the marks left behind by predators seem improbable, as many predators typically attack on plasticine models to make inferences about the particular parts of their prey’s body. For instance, sharks, predators’ target. Plasticine and clay models have lizards, birds, and mammals preferentially grasp and bite demonstrated their utility in many previous studies of their prey in the head or neck region [12-17]. While, this predation on reptiles (e.g. [17,21-23]). inclination is generally thought to aid speeding up the We produced 569 models of adult lizards by killing or swallowing process, or to serve in protection pouring non-toxic plasticine (Aquasoft, Eberhard against defensive biting, we examined which part of the Faber) into a flexible mould (pâte à modeller epoxy body of the lizard that an unspecialised avian predator superfine, Pascal Rosier) that was constructed using strikes at. a preserved museum specimen of Podarcis sicula, the same species native to the islets. Because males and females look the same from even a short 2. Experimental Procedures distance, we made use of a single morph only. The models were painted to resemble the colours of live 2.1 Study system and species animals according to the human visual system (non- This study was conducted on two small islets of the toxic paint LIVOS) and checked the reflectance of the Lastovo Nature reserve (Adriatic Sea, Croatia): Pod models using a photospectrometer. A methodological Mrčaru (42°46,7N; 16°46,7E) and Pod Kopište (42°45,7N; problem associated with the use of these models 16°43,7E). Both islands are uninhabited and consist of is a possible different perception of the models by an elevated and more vegetated centre encircled by a avian predators [24]. Therefore we test reflectance lower girdle of almost barren rocks. They contain dense of models with a spectrophotometer; reflectance populations of the Italian wall lizard (Podarcis sicula), spectra were obtained with a portable high-resolution a robust, diurnal, heliothermic lacertid lizard. There are photospectrometer (model HR 2000, Ocean Optics, no predatory mammals on the islands. Most predation Duiven, The Netherlands) to compare the colours of on Podarcis sicula is likely due to yellow-legged gulls the models (N=10) with those of real lizards (N=10). (Larus michahellis) which visit and nest on the islands This device detects reflection spectra of visible light in higher abundances than other species. Occasionally, and UV-reflectance (200-1100 nm) with a resolution other possible bird predators visit the islands, including of 1.5 nm. Visible and UV light is provided by a Ravens (Corvus corax), Falcons (Falco eleonorae, deuterium-tungsten light source (DH 2000-Bal, Ocean F. tinnunculus, F. peregrinus), common buzzards (Buteo Optics, Duiven, The Netherlands), which generates buteo), short-toed eagle (Circaetus gallicus), and illumination for wavelengths from 200 to 1100 nm. herons (Ardea cinerea, A. purpurea, Ardeola ralloides). We made use of a coincident reflectance probe It should be noted that all of these occasional species (QR400-7-UV/VIS-BX, Ø 2.6 mm, Ocean Optics, were only observed once of twice during the four-year Duiven, The Netherlands) to take spectra of the study on these islands. Additionally, gulls tend to chase surface of each individual. In order to characterize away more dangerous bird predators (e.g. crows and overall colouration, four reflectance spectra were taken falcons) and predation intensity increased near a gull across the body of the animal or model (interparietal, colony on Podarcis atrata [18]. The importance of gulls central mid dorsal spot and two lateral dorsal spots). as predators of lizards is debated (e.g. [19,20]). The spectra from these points were averaged by We conducted a dietary investigation and therefore calculating the mean reflectance intensity at the collected random faecal pellets from around the gull’s 876 increments from wavelengths 400–700 nm. The nests on the islands. The majority of regurgitates difference between real and replica lizards was contained food from only one foraging habitat. Our clearly reflected in their reflectance spectra and the dietary analyses showed that this species of gull feeds spectral parameters. Real lizards had low reflectance

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percentages for all wavelengths relative to the replica of the standard errors for the percentage values was lizards (B. Vervust, unpublished data). The replica performed using the equation: SE = sqrt (P(100-P)/n), lizards showed typical spectra with high reflectance of where P = the percentage and n = the sample size [26]. 550–680 nm. For determining whether our results might have been We placed the plasticine models in rows (average confounded by constant sum constraints, we repeated length: 65 m, range: 45-115 m), at approximately 2 m our analysis, leaving out the most attacked body region intervals, putting each model in approximately the (i.e., we tried to differentiate between preference and same position as the last real lizard observed prior avoidance). Statistical analyses were conducted with to positioning the model (for details see [21]). Lizard SPSS (version 15.0). densities on these islands are exceptionally high [25]. Because of the structural complexity of the islands, each model was not visible (from human eye view) from 3. Results the next, reducing the possible confounding effects of pseudoreplication. Between 48 and 52 hours later, We recorded a total of 851 beak marks on 208 of the we returned to the islands and noted the number and 569 lizard models (Table 1). 361 lizard models were location (head, trunk, tail, limbs) of beak marks on each intact and undisturbed. The distribution of scars along 2 model. We considered a model as “attacked” when it the model’s body length was not random (Χ 3 =204.22, exhibited a clear beak mark. We discarded scars on the P<0.001); a disproportionately higher number of models originating from territorial interactions with real attacks were located on the models’ head and there lizards and not from predatory attempts. were relatively few on the extremities such as limbs and tail (Figure 1). Rerunning the analysis but disregarding 2.3 Statistical analysis the marks on the heads also indicated a significant 2 We assume that if attack location is solely a function non-random distribution (Χ 2=251.67; P<0.001). Again of body area, larger body parts will receive more beak the extremities and especially the tail region were less marks. Therefore, we determined the relative surface often attacked than would be expected by chance. areas of the head, trunk, tail and limbs by scanning 10 plasticine models using a HP Scanjet model 5590. We then digitised the outlines and obtained the areas (above as seen from a birds perspective) with the TspDIG program (version 1.40, 01/17/2004; Rohlf J.F., Ecology and Evolution, SUNY, Stony Brook, 2007). We considered four areas: head including neck (bordered by the line between the anterior insertion of the upper arm), trunk, tail (bordered by the line between the posterior insertion of the thighs), and sum of the area of the fore- and hind legs. We took the average of these values and multiplied the percentage of the area with the observed numbers of attack as the null hypothesis. When a model exhibited several beak marks, the attack score was divided between the body parts. For instance, for a model with one beak mark on the head and one on the trunk, Figure 1. Expected (corrected for area of body part) and observed percentages of beak marks, for each body part. Circles = we recorded 0.5 head and 0.5 trunk (i.e. each attacked observed percentage, squares = expected percentages model was treated as a single observation). Calculation with standard errors.

Number of scars 1 2 3 4 5 6 7 8 9 10 12 13 14 17

Head 96 26 18 16 5 6 3 2 0 0 0 0 0 0

Trunk 56 35 9 22 15 5 6 1 2 4 1 1 1 1

Limbs 17 9 6 1 1 1 1 0 0 0 0 0 0 0

Tail 17 8 5 2 4 1 1 0 0 0 0 0 0 0

Table 1. Frequency of scars on the lizard models. Data are shown in the form of counts of scars on body part.

295 Seeing through the lizard’s trick: do avian predators avoid autotomous tails?

4. Discussion example movement of the tail, will make this body part more conspicuous and possibly make birds more likely This study showed that even these unspecialised to attack it. In a set-up similar to ours, Shepard (2007) avian predators might have a preference for attacking [17] found that models of four different lizard body the head of model lizards, resulting from an innate or shapes were preferentially attacked in the head by both learning process. While a preference for the head might lizard (Ameiva ameiva) and bird predators. Predators not necessarily demonstrate tail avoidance, this topic may target the rostral end of prey because the head needs further exploration because it suggests that and neck regions contain vital and vulnerable parts that even unspecialised avian predators (seagulls) may see are relatively accessible [14,17,27,28]. In other cases, through the lizard’s trick-of-the-tail. This result may have seizing the head or neck of the prey may protect the implications for our understanding of the evolution of predator against dangerous defensive behaviour such this peculiar defensive system. There are many reasons as retaliatory biting [30,31] or spitting [4]. An additional why attacking the head would be preferred over the advantage for predators preying on lizards and other body or tail that has nothing to do with tail autotomy. animals with autotomous tails might be that the head is Our results are in accordance with earlier studies, firmly secured to the trunk and situated far away from involving a variety of predator and prey species. For the detachable end, so that the risk of ending up with but instance, loggerhead shrikes (Lanius ludovicianus) a minor bit of the prey is limited. attack their rodent prey mostly in the head and neck However, the relatively low proportion of predatory region [27-29]. Grasshopper mice (Onychomys marks that we observed on our lizard models cannot be torridus) kill horned lizards (Phrynosoma cornutum and explained solely in terms of a preference for the head P. modestum) by chewing their cranium [14]. Opossums region. Tails also had proportionately fewer bite signs than (Didelphis albiventris) subjugate pitvipers (Bothrops the trunk and limbs, suggesting that the bird predators jararaca) by biting them in the head or neck region [30]. were actively avoiding the tail region. From the point of Grisons (Galictis spp.) handle snakes in a similar way the predator, this obviously makes sense – by targeting [13]. Burton’s legless lizards (Lialis burtonis) strike prey the other regions of a lizard’s body, it can get around the skinks (Eulamprus heatwolei) preferentially in the head autotomy trick and benefit from the full energetic contents region [31]. Even venomous snake species that release of his catch. Although it is reasonable to assume that prey after the first bite, typically target the head or thorax selection should favour this kind of prudent predatory region [32-34]. A methodological problem associated behaviour, we have no idea whether the tail avoidance with the use of models is a possible different perception in birds is adaptive in the sense that it arose as a genetic of the models by avian predators. We found a slightly counter-adaptation in response to the prey’s autotomous different reflectance of our models than values from real abilities. Several studies have presented evidence that lizards, and future studies should try to circumvent this different aspects of foraging behaviour can be innate (e.g. problem. [35-39]), so the hypothesis that bird brains are genetically Additionally, we do not know the order of pecks, i.e. programmed to avoid grabbing lizard tails remains viable. which body-part is pecked at first. In nature, predators However it is also possible that birds (like herpetologists) likely have only one chance to capture and kill their prey learn to avoid grasping tails in the course of their lifetimes. and do not have the opportunity for multiple strikes at A large number of studies have revealed the importance of different parts of the same prey item’s body. If most learning and prior experience on foraging proficiency in a attacks on models are directed towards the head, then wide variety of predator species, ranging from arthropods these are probably also the first strikes the predator to humans (e.g. [40-43]). The ontogenetic flexibility of made. In our analysis, we removed these first strikes, foraging behaviour may vary considerably among even which likely left us with mostly secondary, tertiary, etc. closely related species (e.g. [42,44]), but theoretically strikes, which may be rare in natural situations. Also, it one would expect specialist foragers to have genetically stands to reason that if a predator strikes a plasticine fixed foraging techniques, and generalists to have model once, then the probability that it strikes the same flexible (learned) methods (cf. [42,45]). If so, because in model in a particular region for second and third strikes our study system none of the predator species can be may change depending on where the previous strike considered a lizard-hunting specialist, we suspect that occurred (i.e., learning). Thus, a given body region the tail avoidance behaviour is acquired through learning does not have the same probability of being targeted or prior experience. It would be interesting to compare over time, so it is difficult to draw conclusions without the frequency of attacks on the tail of models exposed taking this into account. Finally, any potential effect of to predators that differ in their prior experience with prey movement (living organisms are not static), for lizards, and between generalist and specialist predators.

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While natural selection could have been acting for tail We also do not know the frequency of gull’s attacks avoidance to be hardwired in predators, it should be either from the ground or from aerial attacks. But noted that not all lizards autotomize their tails. Further, unquantified observations suggest that gulls attacked our because learning to avoid attacking the tail is not a costly models from the air. The lizards of our study system live thing to learn, it seems unlikely that hard wiring such a on islands with limited predators. Several authors found thing would be strongly selected for. In order to test the that autotomy varies with predation risk [49]. If future idea of tail avoidance, future research could use models research on the interaction between visually oriented of lizard species that the predator is familiar with that do predators (birds) shows a clear avoidance of the tail and do not autotomize their tail to investigate if there is a region, the outcome of this result does not hold for other difference in predator attacks on body regions. (chemical oriented) predators such as snakes and rats. Our results suggest that even generalist predators The review of Bateman and Fleming (2009) [9] suggested may circumvent tail-autotomy. Why then, can lizards that knowledge of how different predator taxa attack still shed their tails? Shouldn’t natural selection push lizards will inform us about autotomy frequency pattern lizards to abandon an unsuccessful anti-predation differences between populations. Avian predators might strategy? Perhaps caudal autotomy is still valuable as not be a selective force resulting in the maintenance of a defence technique against un-experienced predators. autotomy, seeing as they will come directly from above Possibly, our methodology using immobile models also and are also often much larger than their prey. This is underestimates the number of times that lizards will supported by Cooper et al. (2004) [49] who found loss of be attacked on the tail, even by experienced hunters. autotomy in lacertids on islands where the only predators Behaviour of live lizards in the field (e.g. defensive and tail were gulls and kestrels. Most predators are well aware displays) may lead to different patterns of attack to those of where the head and eyes of very different taxa are observed in this study. However, we never observed situated, which influences attack and defence/vigilance such behaviour in our study species. In addition, the behaviour. Attacking the head induces an immediate kill costs of having an autotomous tail may not be great and it incapacitates the area most likely to inflict damage [46,47], so the selection gradient working against tail- on the predator. This hypothesis seems more probable shedding ability should also be rather shallow. From a and logical and seems considerably stronger than that of different perspective, the ability to shed the tail has been autotomy, especially given the prevalence of this type of lost (and has re-evolved) several times in squamate attack behaviour among predators of all trophic levels, as evolutionary history, a fact usually attributed to shifts mentioned above, attacking both autotomising and non- in the cost-benefit balance of the strategy [8,48]. We autotomising prey. We feel that this intriguing possibility here suggest that changes in the ability of the predator deserves further study. community to see through the lizards’ tail trick may be a factor that has been overlooked in this respect. For instance, for lizards hunted by a specialist predator Acknowledgements that has evolved the skill to avoid the treacherous tail, autotomy has little selective advantage. We appreciated the help and company of Jan Scholliers In our study system, the proportion of lizards showing in the field. This study is part of larger projects supported tail autotomy differed considerably. We found a significant by the FWO – Flanders (project nr. G.0111.06) and the different degree of autotomy frequency, ranging from Research Fund of the Republic of Croatia (project nr. 25.5% in the Pod Mrčaru population up to 41% in de Pod 183007). Research was carried out under research Kopište population [25]. This is in accordance with the permit UP/I 612-07/04-33/267 issued by the Croatian suspected difference in predation pressure [21]. Ministry of Culture.

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