Behav Ecol Sociobiol DOI 10.1007/s00265-016-2246-4 ORIGINAL ARTICLE Rapid acquisition of antipredatory responses to new predators by an insular lizard 1 1 1 Zaida Ortega & Abraham Mencía & Valentín Pérez-Mellado Received: 12 September 2016 /Revised: 20 October 2016 /Accepted: 24 October 2016 # Springer-Verlag Berlin Heidelberg 2016 Abstract Significance statement Alien predators may impose a great threat to naïve prey. Ibiza How naïve prey acquire antipredator behaviour is both impor- wall lizards (Podarcis pityusensis) live in Ibiza, a snake-free tant for basic scientific research and useful for the conserva- island until 2003. We studied the lizards’ discrimination of tion of native species subjected to biological invasions. The scents of two invader snakes: one that depredates lizards, the island of Ibiza (Spain) has been free from snakes until their horseshoe whip snake (Hemorrhois hippocrepis), and another introduction by humans in 2003. We compared the reaction of that does not, the ladder snake (Rhinechis scalaris). We com- lizards from Ibiza (where presently three species of snakes pared two populations of Ibiza wall lizards: one from the main cohabitate) and lizards from Sal Rossa (a nearby snake-free island of Ibiza, which coexists with both snakes, and another islet) to the scent of two snakes (one that feeds on lizards and from the nearby snake-free islet of Sal Rossa. Lizards from other that does not). The results were clear: lizards from Ibiza Ibiza recognized the scent of the horseshoe whip snake and react to the scent of the predatory snake with antipredatory responded with clear antipredatory behaviours. However, they behaviours, while ignoring the scent of the non-predatory reacted to the scent of the ladder snake similarly to that of the snake. Lizards from the snake-free island of Sal Rossa did controls (odourless control and pungent scent). Lizards from not react to any of the snakes. Our study shows that lizards Sal Rossa did not respond to any of the snakes or the controls. can rapidly acquire the ability to react to a completely new Our results show that lizards can rapidly acquire the ability to type of predator, most likely by learning. react to a novel predator. As only about ten generations of lizards have coexisted with snakes, the most plausible expla- Keywords Response to predators . Lizards . Snakes . nation to our results is that lizards have learned to associate the Chemical discrimination . Invasive species . Learning scent of the predatory snake with a threat. This is the first study reporting the rapid acquisition of lizards’ antipredatory responses to the chemical cues of novel predators. However, Introduction more research is needed in order to identify the mechanisms implicated in the response. Predation is one of the main evolutionary forces in animals (Endler 1986; Lima and Dill 1990). The hunting efficiency of predators usually coevolves with the antipredatory behaviours of the prey (Greene 1988; Vermeij 1994). Nonetheless, the Zaida Ortega and Abraham Mencía are cofirst authors. invasion of alien predators imposes new predator-prey inter- Communicated by T. Madsen actions among animals that do not share a common evolution- ary history (Strauss et al. 2006; Sih et al. 2010; Simberloff * Zaida Ortega et al. 2013). In this scenario, naïve native prey may be unable [email protected] to recognize predators or respond to them appropriately (Banks and Dickman 2007;Kovacsetal.2012;Cooper 1 Department of Animal Biology, University of Salamanca, Campus et al. 2014). In addition, sometimes, the alien predator has Miguel de Unamuno, s/n, 37007 Salamanca, Spain coevolved with similar prey in its original habitat, hence Page 2 of 9 Behav Ecol Sociobiol becoming a highly effective hunter of the naïve prey (Sih et al. expect that they show significant differences in their behav- 2010), which may result in the extinction of the naïve prey iours to harmless odours vs. odours from potential predators. (e.g. Blackburn et al. 2004). However, there are many cases in Thus, one would expect lizards to react with antipredatory which naïve prey may recognize and avoid novel predators behaviours if they recognize the odour as a threat, whereas despite not having a shared evolutionary history (e.g. Strauss no such behaviours would be displayed when encountering et al. 2006; Anson and Dickman 2013; Nunes et al. 2014). harmless odours. Such an ability may be innate and hence fixed by evolution If the ability to recognize the scents of predatory snakes is (e.g. Losos et al. 2006; Nunes et al. 2014), or it may be a trait not innate, we would expect that lizards from Sal Rossa, that is caused by predator exposure and subsequent learning to which have never encountered snake scents before, would avoid novel predators by the naïve prey (Kelley and Magurran not display antipredatory behaviours. These lizards would 2003; Griffin 2004; Ferrari et al. 2012). Learning is well doc- act normally and similarly to controls and to the scent of umented in fish and has been reported to occur rapidly, only snakes. If lizards from Ibiza, which coexist with both types some days after the first visual encounter with the novel pred- of snake during the last decade, are able to recognize the ator, and even faster antipredator responses have been record- snake’s scent as a threat, we would expect that they react to ed with using predator chemical cues (usually by means of the scent with antipredatory behaviour but react normally to chemical alarm signals of conspecifics or heterospecifics; the controls. Finally, it is also possible that lizards from Ibiza Chivers et al. 1995; Brown et al. 1997). discriminate and react only to the scent of the predatory snake, Many animals are able to recognize predators by chemore- the horseshoe whip snake, and react normally to controls and ception, which allows potential prey to avoid risky encounters to the scent of the ladder snake. and, often, the costs of fleeing (Kats and Dill 1998; Apfelbach et al. 2005; Cooper et al. 2009). Reptiles have highly devel- oped mechanisms of chemoreception (Schwenk 1995), and several species of lizards have been reported to use them to Materials and methods identify and react to native predators (Thoen et al. 1986; Dial et al. 1989; Webb et al. 2009; Mencía et al. 2016). However, Study system long-term isolations from predators may result in that prey may have lost the ability to recognize predators (Blumstein The Ibiza wall lizard is a medium-sized lacertid lizard that 2002; Blumstein and Daniel 2005; Cox and Lima 2006). inhabits the main islands of Ibiza and Formentera and 42 The Mediterranean island of Ibiza has never been inhabited surrounding islets (Salvador 1984, 2014;Salvadorand by snakes (Kotsackis 1981; Alcover 2010) until their recent Pérez-Mellado 1984). On Ibiza, the wall lizards are exposed introduction via olive trees that were used for ornamental gar- to several predators: mammals, such as genets (Genetta dening in 2003 (Álvarez et al. 2010; Silva-Rocha et al. 2015). genetta) and feral cats (Felis silvestris), as well as birds such Hence, the Ibiza wall lizard, Podarcis pityusensis, first en- as kestrels (Falco tinnunculus) and barn owls (Tyto alba; countered snakes around one decade ago. Three invasive Alcover 1984; Salvador 2014). As mentioned previously, a snake species (the horseshoe whip snake, Hemorrhois decade ago, three species of snakes have invaded Ibiza and hippocrepis, the ladder snake, Rhinechis scalaris, and the hence constitute three additional potential predators. Sal Montpellier snake, Malpolon mosnpessulanus) are now pres- Rossa is an islet (<0.5 Ha) that is close to the Southeastern ent on the main island of Ibiza, while coastal islets are still free coast of Ibiza, where the only potential predators are birds. from snakes (Silva-Rocha et al. 2015). Thus, Ibiza wall lizards The horseshoe whip snake inhabits the South of the Iberian from coastal islets have never encountered snakes. We took Peninsula and the North of Tunisia, Algeria and Morocco advantage of this unique situation in order to test if recognition (Carranza et al. 2005; Silva-Rocha et al. 2015). Adult horse- and response to alien predators can be acquired in a naïve prey shoe whip snakes are active foraging snakes and feed mainly that lacks a common evolutionary history with their potential on mammals and reptiles such as lizards, but their diet also predators. To do this, we conducted experiments on chemical includes birds and invertebrates (Pleguezuelos and Moreno recognition of alien snakes by Ibiza wall lizards. We exposed 1990;PleguezuelosandFahd2004;Pleguezuelosand lizards from Ibiza (which have been in contact with snake Feriche 2014). The ladder snake inhabits the Iberian predators for about one decade) and lizards from the snake- Peninsula, the Southeast of France and the Northeast of Italy free islet of Sal Rossa to the scents of two of the alien snakes: (Pleguezuelos 1998). Adult ladder snakes are active foragers the horseshoe whip snake and the ladder snake. which feed on mammals and birds and do not depredate liz- In order to study the reaction of insular lizards to the chem- ards (Pleguezuelos 1998; Pleguezuelos et al. 2007). Both spe- ical cues of the recent invader species of snakes, we conducted cies have been recently introduced to Ibiza through ornamen- laboratory experiments with different odour treatments. If liz- tal gardening, and they have stable reproductive populations ards recognize the chemical cues of the snakes, we would in Ibiza (Pinya and Carretero 2011; Silva-Rocha et al. 2015). Behav Ecol Sociobiol Page 3 of 9 Experimental design the odourless control. We then allowed three different odours; i.e. horseshoe whip snake, ladder snake and cologne impreg- During June of 2014, we conducted three experiments: (1) nate the absorbent paper.