Herpetological Journal FULL PAPER
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Volume 26 (April 2016), 149–155 FULL PAPER Herpetological Journal Published by the British Chemical discrimination of sympatric snakes by the Herpetological Society mountain lizard Iberolacerta galani (Squamata: Lacertidae) Abraham Mencía, Zaida Ortega & Valentín Pérez-Mellado Department of Animal Biology, University of Salamanca, Campus Miguel de Unamuno, 37007, Salamanca, Spain We conducted an experiment on chemical discrimination of two saurophagous snakes (the smooth snake,Coronella austriaca and the Seoane's viper, Vipera seoanei) as well as the aquatic Natrix maura, by the mountain lizard Iberolacerta galani. Using terraria, 24 lizards were exposed to scents by the three snakes as well as an odourless control. We quantified fourteen behavioural variables, twelve of which significantly differed among treatments. Lizards are able to recognise the scents of both predatory snakes, and react to them with intense antipredatory responses. The antipredatory behaviour found inI. galani was similar for the scents of the two different predatory snakes, despite differences in their foraging behaviour. The behaviour displayed by lizards confronted with chemical cues suggests an adaptation to minimise the likelihood of being attacked. Key words: antipredatory behaviour, chemoreception, Iberolacerta galani, Lacertidae, Reptiles, Squamata and benefits of reacting to different visually detectable INTRODUCTION attacks (Martín et al., 2009a). Moreover, I. cyreni is able to flexibly respond to attacks from terrestrial predators he hunting efficiency of predators goes hand in hand that differ in intensity, suggesting that it can adjust its Twith the efficiency of antipredatory behaviours of behaviour according to the costs associated with the prey (Vermeij, 1994). Recognising predators through perceived risk of predation (Martín et al., 2009b). chemoreception is common in vertebrates (fish: Helfman, In this study, we used the León rock lizard, I. galani 1989; Hirvonen et al., 2000; amphibians: Semlitsch from isolated high mountain habitats as a model & Gavasso, 1992; birds: Roth et al., 2008; mammals: organism. The population under study co-occurs with Apfelbach et al., 2005; reptiles: Cooper, 1990; Dial & two terrestrial predators: the smooth snake (Coronella Schwenk, 1996; Downs & Shine, 1998; Van Damme & austriaca) and the Seoane´s viper (Vipera seoanei), as well Quick, 2001; Labra & Niemeyer, 2004; see also Kats & as the aquatic snakeNatrix maura. Coronella austriaca is Dill, 1998 for a review), and the responsiveness of prey a saurophagous species which uses mixed strategies of is linked to the relationship with the predator (threat- ambush behaviour and active foraging (Goddard, 1984; sensitivity hypothesis: Helfman, 1989). Galán, 1998), while V. seoanei is mainly an ambush Reptiles have highly developed mechanisms of predator and a generalist forager that includes lizards chemical communication, and offer a unique opportunity in its diet (Saint-Girons, 1983; Braña, 1998a). Coronella to study antipredatory behaviour based on chemical austriaca is a non-venomous constrictor species, while V. stimuli (Schwenk, 1995). Lizards use chemoreception to seoanei is venomous. Natrix maura uses mixed foraging locate food (Cooper, 1994), in social interactions (Verbeek, strategies and mainly feeds on invertebrates, amphibian 1972), and to identify potential predators (Thoen et al., larvae and fish (Hailey & Davies, 1986; Braña, 1998b). We 1986; Dial et al., 1989; Cooper, 1990; Webb et al., 2009). establish whether I. galani is able to identify chemical Many reptiles show specific antipredatory behaviours in cues from snake predators, describe the response of response to chemical cues that prevent potential attacks lizards to chemical cues from predators, and describe (Kats & Dill, 1998; Mason & Parker, 2010). differences in antipredatory responses. Our hypothesis is It is well-established that lizards behave distinctly that I. galani is able to recognise the scent of its predators when presented with odours of potential predators and react to them with antipredatory responses (Thoen (Thoen et al., 1986; Van Damme et al., 1990, 1995; Van et al., 1986). The expected antipredatory response would Damme & Castilla, 1996; Van Damme & Quick, 2001). include a decrease of lizard movement, combined with a In the case of the genus Iberolacerta, I. cyreni is able high rate of tongue-flicks, tail waving and other jerking to assess the risk of predation and to balance the costs movements. Correspondence: Abraham Mencía ([email protected]) 149 A. Mencía et al. MATERIALS AND METHODS absorbent paper on the floor to retain the odour of each treatment. The control terrarium had the floor covered Study species with clean absorbent paper. In the three experimental The León rock lizard, I. galani, is a recently described terraria, a snake was introduced 24 hours before trials. lacertid lizard endemic to North-Western Spain (Arribas et The terraria were closed with transparent plastic covers. al., 2006). It inhabits rocky substrates above the tree line The snakes were removed from their terraria two minutes (>1400 m), and is an insectivorous species (unpublished before a trial and re-introduced after the trial. Each data). The ecology of I. galani is mainly unknown. lizard was subjected once to each treatment following a random order of permutations (4!=24 permutations), Maintenance and experimental procedures resulting in 96 trials (24 lizards x 4 treatments). Each On 31 May 2012, 24 adult lizards were collected by lizard was tested once a day within the normal activity noosing (X±SE, SVL=65.0±1.69 mm) at the Natural period (0900 to 1700 hours). Monument "Lago de La Baña" (León province, Spain). For The test room was dark and only the terrarium was transport to the laboratory, lizards were kept in individual illuminated by a 75 W bulb 50 cm above it. A temperature cloth bags placed inside individual terraria. To obtain of 30°C was maintained in the terrarium, which is within the scents of snakes, adult individuals of C. austriaca, V. the set-point range of preferred body temperatures of I. seoanei and N. maura were captured in the same area and galani (unpublished data). To avoid a potential decrease on the same day. Snakes were transported in a different in the scent concentration, we closed the terrarium vehicle than lizards in order to avoid any odour mixture. with a transparent cover when the lizard was placed The experiments were performed during the first week inside it, and recorded its behaviour over 15 minutes. of June 2012. Lizards were kept in individual terraria (40 All terraria were marked in six sectors of equal surface x 25 x 30 cm) with a substrate of artificial grass, and fed in order to count the number of times the lizard moved daily with crickets and Tenebrio molitor larvae; water was from one sector to another. Two observers were placed provided ad libitum. Snakes were housed in separate two metres from the terrarium opposite eachother. One terraria (50 x 30 x 30 cm) with a substrate of artificial observer recorded with binoculars the number of tongue grass and water ad libitum. To avoid odour mixture, flicks and antipredatory variables. The second observer snake terraria were placed in different rooms. recorded the number of movements and changes among Our experimental protocol was similar to those sectors. At the conclusion of the study (6 days), animals previously employed with geckos (Dial & Schwenk, 1996; were released at their capture sites. Downes & Shine, 1998; Webb et al., 2009) and lacertid lizards (Thoen et al., 1986; Van Damme et al., 1995; Van Behavioural observations Damme & Quick, 2001). We used an empty odourless We started to record a lizard’s behaviour five seconds terrarium as a control, and three terraria for treatments: after placing it in the centre of the experimental one with the odour from N. maura, and two terraria terrarium. The duration of each trial was 15 minutes. with odour cues from C. austriaca and V. seoanei. In all Fourteen behavioural variables were recorded: (i) Walk: four experimental terraria (60 x 40 x 40 cm) we placed the lizard walks normally, (ii) Change among sectors: the Table 1. Mean±SE of each behaviour and results from Friedman’s Test (Chi-squared values and p-values; n=24, df=3) for the 4 experimental treatments (Control, Natrix, Coronella and Vipera). 1 Significant differences are marked with *. Mean±SE (n=24) Friedman’s Friedman’s Behaviours Control Natrix Coronella Vipera Chi-squared p-value1 (i) Walk 74.5±9.72 75.29±7.76 1.91±0.63 0.12±0.12 62.16 <0.0001* (ii) Ch. among s. 20.88±2.73 21.92±2.57 5.79 ±1.59 3.46±0.61 48.71 <0.0001* (ii) Slow 0 0 12.42±2.18 14.79±2.23 64.82 <0.0001* (iv) Tongue-Flick 194.6±18.93 212.10±13.34 155.4±21.61 189.20±24.7 5.18 0.159 (v) Snout 29.83±4.69 27.88±3.28 4.12±1.22 3.25±0.84 53.08 <0.0001* (vi) Rubbing 70.08±10.43 68.04±8.92 4.58±1.51 2.87±1.17 61.06 <0.0001* (vii) Stand and s. 5.12±1.5 6.71±1.28 0.67±0.32 0.25±0.18 39.71 <0.0001* (viii) Head bob 0.17±0.13 0.12±0.69 6.54±1.42 8.87±1.82 46.94 <0.0001* (ix) Foot shake 2.46±1.42 2.15±0.77 9.67±2.45 14.96±4.76 17.98 0.0004* (x) Head raise 5.79±1.03 5.83±1.09 1.46±0.51 0.96±0.39 32.67 <0.0001* (xi) Tail waving 0 0.04±0.04 7.41±3.15 14.71±4.07 41.89 <0.0001* (xii) Walk time 231.50±32.43 227.7±22.65 5.12±1.76 0.12±0.12 62.71 <0.0001* (xiii) Slow time 0 0 161.4±31.45 221.7±31.95 65.39 <0.0001* (xiv) No move 662.2±32.64 668.2±23.32 738.9±31.54 678.6±31.94 7 0.072 150 Response of mountain lizards to snakes moves its head up and down, (xii) Walk time: total time the lizard moves normally, (xiii) Slow time: total time the lizard moves in slow motion, and (xiv) No move: total time the lizard stays immobile.