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Do Avian Predators Avoid Autotomous Tails?

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Do Avian Predators Avoid Autotomous Tails? 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 294 B. Vervust et al. 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.
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