Canadian Journal of Zoology Tail breakage and predatory pressure upon two invasive snakes (Serpentes: Colubridae) at two islands in the Western Mediterranean Journal: Canadian Journal of Zoology Manuscript ID cjz-2020-0261.R2 Manuscript Type: Article Date Submitted by the 17-Jan-2021 Author: Complete List of Authors: Febrer-Serra, Maria; University of the Balearic Islands Lassnig, Nil; University of the Balearic Islands Colomar, Victor; Consorci per a la Recuperació de la Fauna de les Illes Balears Draft Sureda Gomila, Antoni; University of the Balearic Islands; Carlos III Health Institute, CIBEROBC Pinya Fernández, Samuel; University of the Balearic Islands, Biology Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: Zamenis scalaris, Hemorrhois hippocrepis, invasive snakes, predatory Keyword: pressure, Balearic Islands, frequency of tail breakage © The Author(s) or their Institution(s) Page 1 of 34 Canadian Journal of Zoology 1 Tail breakage and predatory pressure upon two invasive snakes (Serpentes: 2 Colubridae) at two islands in the Western Mediterranean 3 4 M. Febrer-Serra, N. Lassnig, V. Colomar, A. Sureda, S. Pinya* 5 6 M. Febrer-Serra. Interdisciplinary Ecology Group. University of the Balearic Islands, 7 Ctra. Valldemossa km 7.5, 07122 Palma, Balearic Islands, Spain. E-mail address: 8 [email protected]. 9 N. Lassnig. Interdisciplinary Ecology Group. University of the Balearic Islands, Ctra. 10 Valldemossa km 7.5, 07122 Palma, Balearic Islands, Spain. E-mail address: 11 [email protected]. 12 V. Colomar. Consortium for the RecoveryDraft of Fauna of the Balearic Islands (COFIB). 13 Government of the Balearic Islands, Spain. E-mail address: [email protected]. 14 A. Sureda. Interdisciplinary Ecology Group / Research Group on Community Nutrition 15 and Oxidative Stress (NUCOX) and IdisBa / CIBEROBN (Physiopathology of Obesity 16 and Nutrition). University of the Balearic Islands, Ctra. Valldemossa km 7.5, 07122 17 Palma, Balearic Islands, Spain. E-mail address: [email protected] 18 S. Pinya. Interdisciplinary Ecology Group. University of the Balearic Islands, Ctra. 19 Valldemossa km 7.5, 07122 Palma, Balearic Islands, Spain. E-mail address: 20 [email protected] 21 * Corresponding author: S. Pinya. Interdisciplinary Ecology Group, Biology 22 Department, Guillem Colom Casasnovas Building. University of the Balearic Islands. 23 Phone. +34 971173177. Rd Palma-Valldemossa, Km 7,5. CP: 07122 (Palma de 24 Mallorca, Balearic Islands, Spain). E-mail address: [email protected] 1 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 2 of 34 25 26 ABSTRACT 27 Tail breakage is an important anti-predator mechanism in snake populations, which can 28 be used as a proxy for predation intensity as natural observations of predator- 29 prey interactions are scarce. Frequency of tail breakage was calculated for two 30 Iberian colubrids recently introduced in the Balearic Islands (Western 31 Mediterranean, Spain): Hemorrhois hippocrepis (Linnaeus, 1758) in Eivissa and 32 Zamenis scalaris (Schinz, 1812) in Formentera. The effect of sex, life-stage, 33 dorsal coloration pattern, body length and body condition on frequency of tail 34 breakage and on remaining subcaudal scale pairs (SBC) were analyzed and 35 compared between the native range and the invaded islands. An increase of the 36 frequency of tail breakage withDraft body size was found, supporting a size-related 37 effect, which also occurs in the native range. Frequency of tail breakage of H. 38 hippocrepis was lower in Eivissa when compared with the original area, while in 39 Formentera Z. scalaris showed a higher frequency, which could be related to the 40 different predator community on each island compared with the mainland. The 41 study of the main ecological aspects of these recent introduced species may 42 allow to assess their potential impact on insular ecosystems and their native 43 biodiversity as well as to promote future control actions in these areas previously 44 free of snakes. 45 46 Key words: ladder snake, Zamenis scalaris, horseshoe whip snake, Hemorrhois 47 hippocrepis, invasive snakes, frequency of tail breakage, predatory pressure, Balearic 48 Island 2 © The Author(s) or their Institution(s) Page 3 of 34 Canadian Journal of Zoology 49 INTRODUCTION 50 In many species, tail breakage is believed to provide an effective antipredator 51 mechanism (Savage and Slowinski 1996; Prudente et al. 2007) and it can be used as 52 evidence of predation rate (Turner et al. 1982; Arnold 1988). However, despite of tail 53 breakage being widely used as a proxy of predation it could be also caused by 54 intraspecific competition or other confounding factors, as it has been observed in lizards 55 (Jaksić and Busack 1984; Jaksić and Green 1984; Itescu et al. 2016). Tail breakage in 56 snakes, also known as pseudoautotomy (Savage and Slowinski 1996), is thought to 57 occur when snakes are grasped by the tail during a predation event and then, a non- 58 spontaneous intervertebral breakage is produced by the rotational movement of the 59 snake in its attempts to escape (Cooper and Alfieri 1993; Savage and Slowinski 1996). 60 The tail of snakes does not regenerateDraft after breaking (Slowinski and Savage 1995) thus 61 leaving a permanent scar from the predation episode. Although some studies suggest 62 that tail losses might indicate inefficiency of predation due to prey survival (Mushinsky 63 and Miller 1993), frequency of tail breakage is widely used as an indirect evidence of 64 the predation pressure on snake populations (Mendelson 1992; Slowinski and Savage 65 1995; Fitch 2003; Pleguezuelos et al. 2010; 2018; Santos et al. 2011). Furthermore, 66 length of the tail stump relative to snout-vent length (SVL) or remaining subcaudal 67 scale pairs (SBC) are commonly used as a measure of tail-loss severity in injured snakes 68 (Aubret et al. 2005). 69 Frequency of tail breakage regarding life-stage, sex and geographic distribution (Fitch 70 2003; Bowen 2004; Placyk and Burghardt 2005; Pleguezuelos et al. 2010, 2018; Costa 71 et al. 2014), as well as intraspecific differences in frequency of tail breakage between 72 populations subjected to different predatory risk have been studied (Santos et al. 2011). 73 Some authors suggest that differences in frequency of tail breakage between populations 3 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 4 of 34 74 could be related to different diversity of predators and predation pressure of each area, 75 variables which change geographically (Placyk and Burghardt 2005; Costa et al. 2014). 76 Pleguezuelos et al. (2010, 2018) suggested that the differences in frequency of tail 77 breakage among the Iberian colubrids Hemorrhois hippocrepis (Linnaeus, 1758) and 78 Zamenis scalaris (Schinz, 1822) in mainland Spain could be related to their foraging 79 habits, which determined their exposure to predators and hence, the predation risk 80 (Pleguezuelos et al. 2007). Moreover, intraspecific competition, including male-male 81 combats, should be considered, especially in large males (Madsen et al. 1993). 82 However, very few cases have been observed in H. hippocrepis in their natural habitat 83 (Jiménez-Cazalla and Lora 2016) and none has been reported in Z. scalaris. 84 Hemorrhois hippocrepis is a medium-large sized colubrid (Pleguezuelos and Feriche 85 2014) that is sexual dimorphic, withDraft males being longer than females with higher values 86 in both body length (SVL) and tail length (Feriche et al. 1993; Pleguezuelos and Feriche 87 2014). It is considered a long-tailed colubrid as its tail length represents 22.9 % of the 88 total length of the snake (range: 20.47 % - 25.21 %, Feriche 1989). In contrast, Z. 89 scalaris is a short-tailed colubrid (15.5 % of total length; Feriche et al. 1993) that lacks 90 sexual dimorphism in body length, but on average, males have longer tail than females 91 (Feriche et al. 1993). This species also has an ontogenetic and anti-predatory behavior 92 change in the dorsal coloration pattern, which shifts from a ladder pattern in juveniles to 93 a striped pattern in adults. Juveniles depend on their crypsis to avoid predation, while 94 adults rely on rapid escape and the confusion of predators because of their stripped 95 pattern (Pleguezuelos et al. 1990, 2007, 2010). 96 H. hippocrepis and Z. scalaris have been recently introduced in the Balearic Islands 97 (Western Mediterranean, Spain) from their native range, the Iberian Peninsula 98 (mainland Spain) (Pinya and Carretero 2011). In recent years, many invasive species 4 © The Author(s) or their Institution(s) Page 5 of 34 Canadian Journal of Zoology 99 have been introduced to the Balearic Islands because of increasing international trade 100 (Perrings et al. 2005). Among the large number of introduced species, reptile exotic 101 species (19) outnumber native ones (2) currently inhabiting the Balearic Islands (Pinya 102 and Carretero 2011). The first report of H. hippocrepis in the Balearic Islands was in 103 2003 in Eivissa, followed by Mallorca in 2004 and Formentera in 2011 (Pinya and 104 Carretero 2011). On the other hand, Z. scalaris was reported for the first time in 2003 in 105 Eivissa, followed by Mallorca in 2004 and Formentera in 2006 (Pinya and Carretero 106 2011). It should be noted that both Eivissa and Formentera islands had remained free of 107 snakes until the introduction of these colubrid species (Silva-Rocha et al. 2015). 108 Currently, any species of the Colubridae family inhabiting Eivissa and Formentera is 109 considered legally invasive, given its inclusion in the Spanish Catalogue of Invasive 110 Alien Species (RD 630/2013). Draft 111 Considering frequency of tail breakage as an indicator of frequency of predation (Fitch 112 2003; Pleguezuelos et al. 2010, 2018; Santos et al. 2011), the main objective of the 113 study was to assess the relationship between frequency of tail breakage and life-history 114 and morphological traits of these two introduced colubrids in the Balearic Islands.