Ecological significance of dorsal polymorphism in a Batesian mimic snake

Ecological significance of dorsal polymorphism in a Batesian mimic snake Batesian mimicry is the process in which harmless species adopt the appearance of a dangerous, aposematic species. In some prey species, both Batesian mimetic and non-Batesian morphs coex- ist, presupposing that both morphs have to be evolutionarily advantageous. The viperine snake, Natrix maura, exhibits a zigzag dorsal pattern and antipredatory behavior that mimics European vipers. This snake also has a striped dorsal pattern that coexists with the zigzag pattern. We have examined whether individuals belonging to different geographically structured clades were more likely to exhibit a certain dorsal pattern, and whether the zigzag pattern has a protective function by exposing artificial snakes to predation in natural environments, in addition to comparing antipreda- tory behavior between zigzag and striped snakes also in natural environments. Our results indicate that the striped pattern was not geographically structured, but habitat-dependent. Aerial predators less frequently attacked zigzag plasticine models than striped or unpatterned models. We detected a shift in antipredator behavior between the 2 morphs, as Batesian mimicking N. maura responded to an approaching potential predator by remaining immobile or fleeing at shorter distances than did striped ones. We conclude that Batesian mimics maintain the cryptic and aposematic value by resembling vipers, whereas in open habitats the non-Batesian mimic has altered its antipredator behavior to maintain its fitness. Key words: antipredatory strategies, aposematism, Batesian mimicry, crypsis, dorsal pattern, Natrix maura In the predator–prey context, prey have developed multiple strat- spider species mimic ants (Mclver and Stonedahl 1993). Among ver- egies to survive (Ruxton et al. 2004). Among others, aposematism tebrates, there are examples among fish (McCosker 1977), amphib- consists in the development of warning signals designed to dissuade ians (Kuchta 2005), and birds (Rowe et al. 1986), although Batesian potential predators (Poulton 1890; Rowe and Guilford 2000). mimicry is rare in mammals (but see Pough 1988). In this study, we Interestingly, some species have evolved to mimic aposematic species address an example of Batesian mimicry in snakes. to gain some functional advantage. In Batesian mimicry (Bates Snakes are highly polymorphic in dorsal patterning and an excel- 1862), harmless species adopt the appearance of a dangerous, apose- lent model group to address the evolutionary drivers of dorsal pat- matic species, to protect themselves from predation, although they tern design (Cox and Davis Rabosky 2013), with camouflage, are really inoffensive (Maynard Smith 1998). Batesian mimicry aposematism, and thermoregulation being the major evolutionary appears to be a widespread taxonomic phenomenon (Ruxton et al. drivers of dorsal pattern diversification (Allen et al. 2013). 2004). Edmunds (1974) provides many examples of mimetic associ- Moreover, many inoffensive snake species resort to Batesian mimi- ations in butterflies, some of them being Batesian mimics, and many cry by reproducing the aposematic dorsal pattern of dangerous V C The Author (2017). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 2 Current Zoology, 2017, Vol. 00, No. 00 species (Brodie and Brodie 2004). A classic example of aposematism common (see review in Allen et al. 2013), far fewer studies have occurs in European vipers of the genus Vipera, which present a dis- analyzed the same topic in mimetic species (but see Greene and tinctive set of morphological and behavioral characteristics, such as McDiarmid 1981; Cox and Davis Rabosky 2013). Similarly, few a short and stout body, head triangulation, coiling, snorting, and studies have addressed antipredator responses against predators zigzag dorsal pattern, which their potential predators relate to their other than humans (Gregory 2016). We specifically address the fol- high intensity of defences (Wu ¨ ster et al. 2004; Niskanen and lowing questions: Mappes 2005; Valkonen et al. 2011a). The zigzag dorsal pattern is (1) Is the occurrence of zigzag and bilineata dorsal patterns in N. maura geographically structured? Scha ¨ tti (1982) showed that the likely a multifunctional protective coloration; it provides protection bilineata pattern appeared fundamentally in coastal areas, against predation because of its aposematic role, although this pat- increasingly to the south and being completely absent in some popu- tern in certain settings would also favor crypsis (Cott 1940; Andre ´n lations. Later, Guicking et al. (2002) studied the phylogeography of and Nilson 1981; Shine and Madsen 1994; Santos et al. 2014). the species, providing a genetic framework for the analysis of the The elaborate and consistent set of morphological and behavio- spatial distribution of this trait. These authors detected 3 geographi- ral traits of most European viper species has been copied by the inof- fensive viperine snake Natrix maura (Linnaeus 1758) (Rollinat cally structured lineages from the Pliocene, 2 in Africa, and one in 1934) as defensive mimicry. This water snake is distributed by the Europe. If the occurrence of the bilineata pattern in N. maura was Western Palaearctic and mimics morphological and behavioral traits not geographically structured and occurred in all the lineages, we of European vipers with which it coincides geographically to some hypothesize that the dorsal dimorphism would have no relationship degree, for example, Vipera aspis (Linnaeus 1758), V. latastei Bosca ´ with the phylogeography of the species. 1878, and V. seoanei Lataste 1879 (Aubret and Mangin 2014; (2) Is the relative frequency of zigzag and bilineata patterns asso- Santos et al. 2014). For example, N. maura exhibits a zigzag dorsal ciated with any landscape appearance? In some snakes, strong selec- pattern (hereafter zigzag) formed by a wide and dark dorsal band, tion promotes variability across spatial scales (Cox and Davis zigzag shaped, from the neck to the tail, which contrasts with lighter Rabosky 2013). Despite the latitudinal cline of the bilineata fre- quency cited by Scha ¨ tti (1982), geographically close populations background body colors. Moreover, N. maura displays head trian- exhibit opposite frequencies of the zigzag and bilineata patterns gulation, a spring-like body posture (coiling), snorting, body infla- (Duguy and Saint-Girons 1993). Based on the field experience of the tion, and striking (Rollinat 1934). authors, the striped morphotype appears to be more common in Notably, N. maura also shows dorsal pattern variability, since wetlands and other open landscapes (see also Duguy and Saint- some specimens have a striped pattern of 2 dorso-lateral light bands Girons 1993; Santos 2009), but there are no studies on the associa- (longitudinally striped sensu von Helversen et al. 2013), or bilineata tion between habitat type and the frequency of the 2 dorsal pattern dorsal pattern (hereafter bilineata) (Scha ¨ tti 1982). Based on mito- across the range of N. maura. chondrial markers, these bilineata individuals are genetically indis- (3) Have bilineata snakes lost the Batesian-mimic role by no lon- tinguishable from the zigzag individuals of the same population ger resembling a viper? The zigzag pattern in N. maura is presumed (Carranza S, personal communication). Intraspecific variability in to have an aposematic, even cryptic function, due to its viper mime- snakes with one of the patterns being striped is quite common in sis, while the bilineata dorsal pattern in snakes does not (Brodie snakes, especially in Colubridae (Wolf and Werner 1994), and can 1992; Wolf and Werner 1994; Allen et al. 2013). Thus, in the be geographically structured or sympatric (Kark et al. 1997). The absence of behavioral modulation (i.e., by snake plasticine models) striped pattern tends to enhance a visual escape strategy, as snakes and maintaining similar background, we hypothesize that the non- can confuse predators by not providing body references in tracking Batesian (bilineata) individuals will be more frequently attacked by its movement (Pough 1976; Allen et al. 2013); this dazzle effect, the predators than will the Batesian (zigzag) ones. motion dazzle camouflage, has recently been supported experimen- (4) Do bilineata and zigzag N. maura display different antipreda- tally (Hogan et al. 2016). Accordingly, compared with non-striped tory behavior when confronted with predators? In snakes, dorsal snakes, striped ones usually show a high frequency of broken tails as pattern and antipredator behavior interact (Brodie 1992), and dorsal a consequence of failed predation events (Pleguezuelos et al. 2010). pattern diversification is related mainly to behavior, rather that hab- In the absence of temporal variation in selective forces, the main- itat choice (Allen et al. 2013). For this reason, the maintenance of tenance of polymorphism (variability within a geographical loca- striped individuals in a population is expected when this pattern can tion) and of polyphenism (variability between geographical confer some antipredatory and other evolutionarily advantages locations) presupposes that the morphs should thrive under different (Brodie 1992; Wolf and Werner 1994). Thus, we hypothesize that, environments (Wolf and Werner 1994; Shine and Harlow 1998). linked to the loss of the viper mimesis in striped N. maura, individu- For N. maura, the coexistence (syntopy) of bilineata and zigzag als would display different antipredatory strategies with regard to snakes also suggests the use of different antipredator strategies (i.e., their dorsal pattern: whereas Batesian mimic (zigzag) individuals are fast-moving vs. static snakes; Allen et al. 2013). Wolf and Werner expected to mirror viper strategy, that is, by staying immobile, non- (1994) suggested that striped snakes tend to thrive in open habitats, aposematic (bilineata) individuals are expected to try to escape, as while those with alternative dorsal patterns (i.e., blotched) prosper occurs in other striped snakes (Jackson et al. 1976; Brodie 1992; in structurally more complex habitats (see also Pough 1976). Wolf and Werner 1994; Pleguezuelos et al. 2010; Allen et al. 2013). Unfortunately, studies on the ecological drivers and the adaptive value of intraspecific dorsal variability in snakes under an experi- mental or comparative framework have been scarcely addressed Materials and Methods (but see Andre ´ n and Nilson 1981; Shine and Harlow 1998; Cox and Davis Rabosky 2013). Geography and spatial ecology of the variability The objective of this study is to uncover the evolutionary drivers The spatial distribution of the variability of N. maura was examined of the dorsal pattern dimorphism in N. maura. While the studies on by the analysis of bilineata and zigzag dorsal pattern frequencies in the function of dorsal patterns in model species (e.g., true vipers) are 917 individuals from 12 populations (Table 1), covering all the Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Santos et al.  Dorsal polymorphism in a Batesian mimic snake 3 Figure 1. Geographic distribution of snakes belonging zigzag and bilineata patterns in the 12 sites studied along the Natrix maura range (A). On the top, examples of freshwater closed (B) and open (C) habitats where N. maura inhabits. On the bottom, living examples of snakes with the 2 dorsal patterns (D, E; photos by Rau´l Leo´ n). Pie charts depict the frequency of bilineata (red) and zigzag patterns (gray). Locality names in red refer to open (wetland) habitats, and in black to closed (river) habitats. phylogenetic clades (Guicking et al. 2002) and most of the range of study is V. latastei, both in North Africa and the Iberian Peninsula, the species (Figure 1A). We examined vouchers from scientific col- and both species shared the visually oriented and most specialized lections (nine localities) and field records of the authors and col- predator (snake-eater) in the study area, Circaetus gallicus; thus, V. latastei is the model species mimicked by N. maura. Vipera latas- leagues from specific sites (3 localities) corresponding to either of the 2 contrasting natural landscapes where the species thrives tei is a rather shy species with abundance hard to measure. (Santos 2009), that is, open and not-open habitats, with sample size However, to include the effect of the model species in the Batesian system, we have considered in our statistical analysis the distance of >15 (Table 1). Open habitats were marshlands and peat bogs where vegetation, depending on site, was composed of broadleaf cattail the closest viper population to each N. maura population, based on Typha latifolia, common reed Phragmites australis, bulrush Scirpus our field experience, and by the tool for measuring distances in Google Earth (Table 1). Although snake pigmentation fades some- holoschoenus, great fen-sedge Cladium mariscus, perennial saltwort what with preservation in liquid, all museum specimens were easily Sarcocornia fruticosa, and sedges (Carex sp.), reaching a height of 0.4–1.5 m, with grassland and reeds dominating in the banks. classified as zigzag or bilineata. Given that snake vouchers shrink due to fixative and the preservative process (Barry 2011), we esti- Closed habitats were rivers and streams with banks dominated by mated SVL for museum vouchers without fresh measurements by stones and thick vegetation, and, depending on sites, made up of willows (Salix sp.), silver poplar Populus alba, elm Ulmus minor, applying the regression of fresh against preserved SVL for this spe- cies (Santos et al. 2011). ash Fraxinus angustifolia, honeysuckle Lonicera arborea, and elm- leaf blackberry Rubus ulmifolius, with a height of 1.0–15.0 m (Figure 1B,C). Predation experiment with plasticine models For each individual examined, body size (snout–vent length, To test whether bilineata snakes lost their Batesian mimicry role SVL, to the nearest millimeter), sex (according to Feriche et al. compared with zigzag snakes, we performed a field-based predation 1993), and dorsal pattern (2 possibilities, zigzag and bilineata, experiment with plasticine models (see similar experiments in Figure 1D,E) were recorded. Although in Batesian mimicry systems Wu ¨ ster et al. 2004; Niskanen and Mappes 2005; Valkonen et al. mimic and model do not need to be strictly sympatric (Pfennig and 2011b). We made 12 bilineata and 12 zigzag plasticine models of Mullen 2010), it is also true that if the number of models decreases, snakes plus 12 patternless models as control (thereafter control). the benefits gained by mimics also decrease (Valkonen and Mappes Models were made by melting non-toxic plasticine (JOVER )in a 2014). The closest viper species to all populations considered in this silicone mould of a N. maura voucher from the study area (355 mm Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 4 Current Zoology, 2017, Vol. 00, No. 00 Table 1. Localities considered in this study for the analysis of the dorsal pattern in the viperine snake, Natrix maura, within the Western Mediterranean Locality Latitude Longitude Habitat Clade Distance to viper (km) N ZZ BL Sampling 0  0 Algeria 36 46N8 13 E Open Algerian 30 16 10 6 EBD 0  0 Rif Mountains 35 07N5 17 W Not-open Moroccan 20 41 40 1 Private collection S. Fahd 0  0 Baetic Mountains 37 12N3 42 W Not-open Iberian 15 77 76 1 DBAG 0  0 Burgos province 42 45N3 48 W Not-open Iberian 2 21 21 0 EBD 0  0 Ca ´ diz province 36 35N6 14 W Open Iberian 26 28 14 14 Field sampling, S. Busack 0  0 Cazorla Mountains 37 54N2 56 W Not-open Iberian 1 28 28 0 EBD 0  0 Delta Ebro 40 42N0 45 E Open Iberian 35 318 183 135 Field sampling 0  0 Donana ~ 36 59N6 26 W Open Iberian 5 113 69 44 EBD 0  0 Rı´o Frı´o River 37 09N4 12 W Not-open Iberian 3 147 147 0 DBAG 0  0 Matarranya River 41 07N0 12 E Not-open Iberian 10 50 50 0 Field sampling 0  0 Charca Sua ´ rez 36 43N3 12 W Open Iberian 18 37 21 16 Field sampling/DBAG 0  0 Puertollano pools 38 39N4 06 W Open Iberian 15 41 38 3 Field sampling Notes: We include the geographic coordinates for the barycentre of the localities, the habitat (2 possibilities, open when marshlands or peat bogs, and closed when others), the phylogenetic clade, the distance to the closest viper population (Vipera latastei), the sample size (N), the frequency of the bilineata (BL) and zig- zag (ZZ) dorsal pattern, and the provenance of the sample. Abbreviations are as follows: EBD, Estacio ´ n Biolo ´ gica de Donana, ~ Sevilla, Spain; DBAG, departa- mento de biologı´a animal, Granada University, Spain; CRBA, Centre de Recursos de Biodiversitat Animal, Barcelona University, Spain. tooth marks were observed, and recorded as made by birds when bill marks were detected (Niskanen and Mappes 2005). As preda- tors, birds are primarily visually oriented while mammals are pri- marily odour oriented. For this reason, marks caused by birds and mammals were recorded and analyzed separately. To avoid insect parasitism and damage, models were sprayed with insect repellent (Autan ; Valkonen et al. 2011b), and to avoid model displacement by predators, they were pegged to the soil by an iron wire that ran the full length of the model. Field experiments were performed in 2013 in Padul, and 2013, 2015, and 2016 in Charca Sua ´ rez, during May and June, a period with high diurnal activity of N. maura (Santos and Llorente 2001). Figure 2. Plasticine models used for the experimental study of predation upon the viperine snake, Natrix maura. From top to bottom, zigzag, striped We conducted 12 trials (4 in Padul and 8 in Charca Sua ´ rez) to check (bilineata) and uncolored (control) model. predation on plasticine models. At each trial, 27–36 models (9–12 sets of models with one model of each dorsal pattern per set) were placed on a grassland background on the banks of the wetlands. Sets SVL, the average body size for this population; N ¼ 290). The back- were placed 20–50 m apart, and models were spaced roughly 6 m ground body color of the models was made by melting brown, green, and white plasticine colors (ratio 10:5:1, respectively). The apart, in random order. Models were placed in the early morning pattern in zigzag models was painted with a permanent marker (08.00–09.00), and experimental trials lasted from 2 to 5 days, with no differences in the duration of trials between Padul and Charca (EDDING 500 ), 5 mm width, while the 2 mm wide dorso-lateral Sua ´ rez (Mann–Whitney U-test; Z ¼ 0.17, P ¼ 0.9). Models were stripes of the bilineata model were made by melting white, green, checked on a daily basis in late afternoon (19.00–20.00) during the and yellow plasticine colors (ratio 5:2:1, respectively). Control mod- trials. More than one attack on a single model during a trial was els exhibited only the ground color (Figure 2). Experiments with plasticine models were conducted in 2 local- considered a single-attack event to reduce pseudoreplication and ities from the south-eastern Iberian Peninsula, where both dorsal bias caused by potential multiple attacks from an individual preda- tor on a single plasticine model (Valkonen et al. 2011b). Thus, the patterns coexist, Charca Sua ´ rez, a 28 ha marshland, 200 m from the 0  0 sampling units were the models in each trial. A total of 104 models sea shore (3 32 W, 36 43 N, 1 m altitude), and Padul, a 85 ha peat 0  0 were examined in Padul (4 trials  27 models minus 4 models stolen bog, inland and 30 km from the other site (3 36 W, 37 00 N; 725 m altitude). The landscape of both study sites was formed by wetland by humans), and 276 in Charca Sua ´ rez (6 trials  36 models, and 2 trials with 30 models). vegetation, such as T. latifolia, P. australis, S. holoschoenus, the introduced giant cane Arundo donax, and C. mariscus in Charca Sua ´ rez. Based on the list of N. maura predators (Santos et al. 2011), Antipredatory behavior experiments during the study period, nine potential avian predators were As the previous predation experiments with plasticine models sug- reported in Charca Sua ´ rez (Ardea cinerea, A. purpurea, Ardeola ral- gested that bilineata snakes lost the advantages of the mimesis with loides, Bubulcus ibis, C. gallicus, Egretta garzetta, Larus michahel- vipers (see results below), we also examined differences in antipreda- lis, L. ridibundus, Porphyrio porphyrio; from the data of the tory behavior between bilineata and zigzag individuals. For this, we authors), and seven potential avian predators in Padul (A. cinerea, conducted a field experiment in Charca Sua ´ rez, a study area A. purpurea, B. ibis, C. gallicus, Circus aeruginosus, Egretta harboring both types of dorsal patterned N. maura. Surveys were garzetta, Nycticorax nycticorax;Pe ´ rez-Contreras J, personal conducted by a single researcher along a 1,500-m transect in the communication). Attacks were recorded as made by mammals when wetland banks, during May and June 2013, 2015, and 2016 (90 h of Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Santos et al.  Dorsal polymorphism in a Batesian mimic snake 5 surveys). Snakes were searched when basking very close to the water computes the likelihood ratio statistic of the model containing a par- (known as the K thermoregulatory strategy; Hailey and Davies ticular term or not (significant when P< 0.05). 1987). When a snake was spotted, it was observed through binocu- A GLZ with a Poisson distribution was used to compare fleeing lars (8  30), its body size was estimated (SVL, to the nearest cm, distance of snakes of both dorsal patterns when confronted with a after training), and its dorsal pattern was classified as zigzag or bili- potential predator. Fleeing distance is a continuous variable; how- neata. The sex of the individuals was disregarded because of the ever, due to inaccuracies of some distance measurements we consid- lack of sexual differences in the frequency of both dorsal pattern ered fleeing distances in 0.5 m intervals, using a Poisson distribution (Duguy and Saint-Girons 1993) and in the burst speed in lab trials to perform the model. GLZs were performed with air temperature on defence behavior (Hailey and Davies 1986). Afterward, the (surrogate of body temperature) and body size as covariates, due to researcher approached slowly and directly at a constant speed of their potential effect on escape speed of this species. Body condition 0.8 m s , until the snake began to flee from the researcher. The flee- (BC) can be considered a surrogate of snake’s locomotor capacity ing distance was measured by a metric tape to the nearest 10 cm. (Jayne and Bennett 1990). Thus, we hypothesized that differences in Body temperature can affect reptile behavior, particularly when BC between zigzag and bilineata could be linked to variation in deciding whether to move or remain still when confronted by a escape distance to predators, that is, lower BC for snakes that flee at predator (Hertz et al. 1982). Unfortunately, some basking individu- longer distances, and higher BC for snakes that allow a closer als (all bilineata) fled to deep water when the researcher approach of predator. The residuals of the regression analysis approached, precluding capturing them to record body temperature. between log body mass and log SVL were used as a measure of BC. Thus, we recorded air temperature 1 m above ground (Hibok 14 We were unable to capture most of the individuals during our trials thermometer, to the nearest 0.1 C) as a surrogate of snake body to check differences in escape behavior between zigzag and bilineata temperature. Although body temperature of basking individuals of snakes in the face of an approaching predator. For this reason, BC this species is usually above air temperature, there is a good correla- was compared between zigzag and bilineata snakes from the same tion between the 2 temperatures (Hailey and Davies 1987), particu- locality, the Ebro Delta, where body mass and length were measured larly during spring (Santos 2009). Snakes escaping also precluded for a large sample size. BC was calculated separately for males and marking for individual identification; however, we assumed that the females (Santos and Llorente 2004). In the “Results” section, means large size of the study area minimized pseudoreplication of the data are followed by 61 SD. by recording the escape distance of the same individual several times. Results Of the 917 snakes examined, 687 were zigzag and 213 bilineata Statistical analyses (76% and 24%, respectively). However, there was interpopulation Two analyses were conducted to identify which factors could variation in the frequency of the 2 dorsal patterns across the N. explain the occurrence of each dorsal pattern of the viperine snake maura range (Figure 1A). The distribution of both dorsal patterns across its range: 1) with the entire data set (all localities, including museum specimens and live ones), we performed a generalized linear was puzzling; some sites were devoid of bilineata individuals, and model (GLZ) with a binomial distribution of the dependent variable bilineata frequencies differed markedly between pairs of nearby and a logit function, using dorsal pattern (zigzag and bilineata) as a sites. The bilineata dorsal pattern was present in regions with the 3 dependent variable, and sex and body size of individuals (SVL) as phylogenetic groups (Figure 1A and Table 1). factors. This analysis was aimed at examining the effects of factors The GLZ demonstrated that neither SVL (Wald Statistic ¼ 0.27, like sex and body size on the dorsal pattern occurrence regardless of P ¼ 0.6) nor sex (Wald Statistic ¼ 0.09, P ¼ 0.8) explained the occur- locality. 2) For each population, we used the percentage of snakes rence of the bilineata pattern on snakes. We repeated this analysis with a bilineata pattern as a dependent variable (percentages were with only animals examined at sites where at least one bilineata arc-sin transformed), and we performed a general linear model snake appeared, and the results were the same, that is, there were no (GLM) with the habitat type (open and closed habitats), the distance sexual or ontogenetic effects in dorsal pattern occurrence. The GLM (km) to the closest V. latastei population, and the latitude, as factors. indicated that the percentage of individuals with bilineata pattern at This second analysis assessed how landscape type, model organism each of the 12 populations was related to the habitat type proximity (viper), and geographic location affected the dorsal pat- (F ¼ 14.45, P ¼ 0.005); bilineata snakes were frequent only in open tern frequency of the bilineata pattern among the populations. To habitats, whereas this pattern was almost absent from closed habi- tats (Figure 1A). A nonparametric test using the percentage of occur- meet the assumption for a linear model, residuals of the dependent rence in each population confirmed significant differences between variable on the grouping factors were examined. the 2 major habitat types in the frequency of the 2 dorsal patterns Log-linear analyses were run to test differences in predation (Mann–Witney U-test, Z ¼ 2.86, P ¼ 0.004). By contrast, we found (depredated and non-depredated) among the 3 plasticine models no significant spatial effect, that is, geographic latitude of each pop- (zigzag, bilineata, and control) and the 2 study sites (Charca Sua ´ rez and Padul peat bog). We tested the association among these 3 cate- ulation (F ¼ 0.20, P ¼ 0.7), nor any relation with the distance to the gorical variables (predation, model type, and locality) in a multidi- closest V. latastei population, that is, the model species for the mimi- mensional contingency table. Log-linear analysis uses a likelihood cry (F ¼ 0.77, P ¼ 0.4). ratio chi-square statistic. The algorithm used generates several mod- From the 380 predation trials made with plasticine models (276 els to test interactions among all variables and selects the least com- in Charca Sua ´ rez and 104 in Padul), 100 attacks by avian predators plex model that best accounts for the variance in the observed were recorded (26.3% of the models). In total, bilineata was the frequencies. We were specifically interested in testing the association most frequently attacked model (n ¼ 45; 35% of the bilineata mod- of Predation Locality and PredationDorsal pattern. The results els examined), the control the second most attacked (n ¼ 32; 25% of were interpreted by checking the odds-ratio scores in expected val- the control models examined), and the zigzag pattern was the least ues of partial and marginal association tests. The odds ratio attacked (n ¼ 23; 19% of the zigzag models examined). The log Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 6 Current Zoology, 2017, Vol. 00, No. 00 Table 2. Partial and marginal association tests of the log linear Table 3. General linear models of differences in flight distance analysis for the attack condition (attacked and not attacked by between bilineata and zigzag Natrix maura phenotypes using birds), locality (Padul and Charca Suarez) and dorsal pattern (bili- snake body size (SVL, snout–vent length, in millimeter) and air neata, zigzag, and control) of plasticine models of Natrix maura in temperature ( C) as covariates in the population of Charca Sua´rez, 2 localities of south eastern Iberian peninsula where both natural south-eastern Iberian peninsula morphotypes for dorsal pattern (bilineata, zigzag) are represented Estimate Standard error Wald Stat P 2 2 df Partial X P Marginal X P SVL 0.000874 0.002 0.25682 0.61 Site (S) 1 79.40 <0.0001 79.40 <0.0001 Air temperature 0.006432 0.007 0.79421 0.37 Dorsal pattern (DP) 2 0.08 0.96 0.08 0.96 Dorsal pattern 0.601609 0.164 13.32934 <0.0001 Attacks (A) 1 87.28 <0.0001 87.28 <0.0001 S * DP 2 0.45 0.80 0.22 0.90 S * A 1 35.88 <0.0001 35.65 <0.0001 individuals were almost exclusively in open habitats, whereas zigzag DP * A 2 9.11 0.01 8.89 0.01 individuals were found in all types of habitats (see also Wolf and Werner 1994; Kark et al. 1997; Cox and Davis Rabosky 2013), Note: Sample size in the results section. although the most frequent in closed habitats. This result reveals why previous studies failed in fitting a geographic pattern for the linear analysis showed a significant interaction between Locality presence of both dorsal patterns in N. maura (Scha ¨ tti 1982; Duguy and Attacks, and between Model and Attacks (Table 2). The mar- and Saint-Girons 1993); mimicry is not restricted to one sex or to ginal frequency tables showed that the occurrence of attacks was ontogenetic stage, and variation occurred across habitat, rather than higher in Padul than Charca Sua ´ rez, and for bilineata than for the geography. In their review of the frequency of the striped dorsal pat- other 2 models. When mammal attacks were examined, we found tern in snakes, Wolf and Werner (1994) concluded that snakes bear- no differences in the frequency of attacks made on the 3 plasticine ing this phenotype inhabited habitats that were less structurally models (v ¼ 1.77, P ¼ 0.18). complex than those bearing blocked or cross-banded dorsal patterns Fleeing distances were recorded for eight bilineata (average flight (see also Pough 1976). distance 3.06 1.1 m), and 17 zigzag N. maura individuals (average Camouflage is frequently selected in snakes (Allen et al. 2013), flight distance 0.96 0.7 m). The GLZ showed that bilineata individ- with different habitats favoring different morphs (Kark et al. 1997; uals fled at the farther distances from the approaching potential Shine and Harlow 1998). We speculate that the zigzag dorsal pat- predator than did zigzag individuals, irrespective of body size or air tern would be beneficial in concealing individuals in more closed temperature (Table 3). It bears noting that 6 out 17 zigzag snakes habitats, where a chaos of images is created by lights and shadows recorded did not flee at all, and exhibited aposematic behavior such (Cuthill et al. 2017; Endler and Mappes 2017). While not proven, as head triangulation, coiling, snorting, and false attacks, only after this interpretation has been posed several times for this dorsal pat- they were gently captured by hand. The remaining 11 individuals tern in vipers (Shine and Madsen 1994; Niskanen and Mappes that fled to a very close distance from the researcher did not exhibit 2005). In contrast, striped snakes would be favored in more open aposematic behavior. habitats, where the combination of lights and shadows would create No differences were found in BC between zigzag and bilineata straighter forms on the background (Wolf and Werner 1994). As N. individuals either in males (Student’s t ¼ 0.18, df ¼ 67, P ¼ 0.9) or in maura inhabits 2 highly contrasting aquatic habitats, wetlands and females (Student’s t ¼ 0.10, df ¼ 53, P ¼ 0.9). This suggests that rivers (Santos 2009), we propose here that heterogeneity in the vege- body shape of zigzag and bilineata individuals did not vary. tation structure surrounding water bodies would be the driving fac- tor for the emergence of dorsal pattern dimorphism in this species. Discussion Dorsal pattern and predator attacks Dorsal pattern and geography Our experiment with plasticine models within the same locality and In the interpretation of animal coloration, tests of geographical varia- habitat confirmed that predators responded differentially to the tion are critical (Cox and Davis Rabosky 2013; Santos et al. 2014). snake dorsal pattern. On a grassland background, control and bili- Our results on the geographic distribution of the 2 dorsal patterns of neata models were more frequently attacked by aerial, visually ori- the viperine snake were puzzling, although in contrast to Scha ¨tti ented predators (birds), than were zigzag models. This was the same (1982), we found that bilineata individuals were present in many result found with viper plasticine models (Valkonen et al. 2011b), inland regions. Notably, bilineata individuals also appeared in popula- confirming that snakes with the zigzag dorsal pattern better avoided tions representing the 3 phylogenetic lineages of the species, north- attacks than did snakes with other dorsal patterns (Wu ¨ ster et al. western Africa east of the Muluya River, north-western Africa west of 2004; Niskanen and Mappes 2005), at least when prey are static the Muluya River, and the European clade (Guicking et al. 2002, (Lindell and Forsman 1996). Our result supports the idea that the 2008). This suggests the character to be African and ancient, as the camouflage provided by the zigzag pattern or that predator wariness species evolved in that continent and clades separated 3.5–4.0 Myr to the model organisms (i.e., vipers) can drive a mimetic system in (Guicking et al. 2002)—although it may also have evolved repeatedly snakes (Greene and McDiarmid 1981; Cox and Davis Rabosky (by convergence) in response to similar ecological demands in the dif- 2013). ferent clades, as is common in snakes (Allen et al. 2013). In the Padul peat bog, plasticine replicas were more frequently attacked than those in Charca Sua ´ rez. Although the potential preda- Dorsal pattern and habitat tor communities were similar, we were unable to adequately meas- The polymorphism for the dorsal pattern in N. maura seems to be ure predator density at either site, and therefore we have no suitable linked to the habitat. Regardless of sex and body size, bilineata explanation for this difference. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Santos et al.  Dorsal polymorphism in a Batesian mimic snake 7 Dorsal pattern and snake behavior dorsal pattern in the viperine snake (as well as in vipers, the model One of the benefits of the high and constant body temperature that organism) would have a double function, concealing individuals N. maura maintains during its K thermoregulation is to retain a against the background and deterring predators. We also experimen- potential for instant high muscular performance (Hailey and Davies tally confirm the Batesian mimesis of the viperine snake to the 1986). Our study demonstrated that, when a potential predator European vipers as model organisms. We acknowledge that our results on attacks are based on plasti- approached, bilineata individuals fled from longer distances than cine models, and those on fleeing distance of live individuals are did zigzag individuals. Some of the latter even remained static until derived from a rather small sample size, which makes it advisable to they were captured by the researcher. Thus, viperine snakes with dif- discuss these issues under alternative hypotheses. The Batesian mime- ferent dorsal patterns varied their antipredatory strategies, suggest- sis of the viperine snakes on vipers do not limit to the zigzag dorsal ing adaptations to increase their fitness. Bilineata individuals, pattern, and includes other behavioral aposematic traits such as coil- lacking the camouflage or the aposematic effect of the zigzag pat- ing, striking, snorting, and head triangulation (Rollinat 1934; Aubret tern, begin to flee when a potential predator approaches. The dorsal and Mangin 2014). However, as we used the same cast (that was not stripe design is common in snakes, especially in the fastest species coiled neither showed head triangulation) for the 3 types of models (Brattstrom 1955). Snakes bearing this dorsal pattern rely on the (Figure 2), we deduce that the higher frequency of bird attacks to bili- confounding effect on predators of the dorsal stripes when the snake neata and control models was exclusively the consequence of the dif- moves (Pough 1976; Allen et al. 2013), making the formation of a ferences in dorsal design among models. The use of static behavior, search image more difficult (Hogan et al. 2016). That is, the percep- typically balling up, as defence in N. maura is more frequent in small tion of speed (von Helversen et al. 2013) and direction (Jackson individuals (Hailey and Davies 1986). However, we rule out the con- et al. 1976) is disrupted, and the location of the focal part of the founding effect of body size in zigzag and bilineata dorsal patterned body, the head (Langkilde et al. 2004), is more difficult (Brodie individuals when a potential predator approaches, as we failed to find 1992; Hu et al. 2009). This interpretation fits the link between the body-size differences between the individuals of different dorsal pat- bilineata dorsal pattern and open habitats found in this study. In terns recorded for this analysis. The same null hypothesis was con- open habitats such as wetlands, the vegetation has less structural firmed for the effect of sex, as sexual dichromatism is often absent in complexity and less irregularly shaped patterns of shadowing. In snakes (Shine and Madsen 1994). Lastly, in their laboratory experi- these micro-scenarios, we argue that the zigzag dorsal patterned ment, Hailey and Davies (1986) also found that starved snakes (for 4– viperine snakes would begin to leave evolutionary room for striped 5 weeks) were more likely to use static defence than post-absorptive snakes, which adopt longer escape distances from approaching pred- ones. We were unable to consider this factor in our trials, as most bili- ators (Allen et al. 2013). neata individuals fled to the water, so that the weight or feeding status of these specimens could not be checked. However, we minimized this Crypsis or aposematism? possibility, as the study site harbored a good population of birds and Experiments with plasticine models did not resolve the question that N. maura, likely for its abundant trophic resources (unpublished data differences in predation rates between morphotypes were the conse- of the authors). Moreover, during field surveys over 3 years, we never quence of the cryptic or aposematic role of the zigzag pattern, or found an emaciated individual of this species in the study area even whether both roles are acting. Several studies have demon- (n ¼ 60). strated the aposematic value of the zigzag pattern (Wu ¨ ster et al. 2004; Niskanen and Mappes 2005; Valkonen et al. 2011b). Ecological significance of dorsal polymorphism However, simultaneous adaptive benefits of this pattern cannot be ruled out, for example, a distance-dependent function for crypsis Assuming the ecological advantages of the zigzag pattern in N. (Valkonen et al. 2011b). We suggest 3 complementary reasons to maura, what are the evolutionary drivers of the maintenance of dor- explain the cryptic role of the zigzag pattern in the viperine snake sal polymorphism in this species? In this study, we have ruled out system: 1) the frequency of zigzag snakes is independent of the dis- the possibility that a historical (phylogeographic) factor could give tance to the aposematic viper model, taking into account that the rise to dorsal variability. Moreover, the result for the distance to the aposematic value of a design depends on the presence of the model closest viper population also suggests no effect of model-species (Pfennig et al. 2001). 2) The maintenance of the dorsal polymor- proximity on the frequency of the viperine snake dorsal pattern. By contrast, we have demonstrated that the coexistence of both designs phism in N. maura is habitat-dependent, suggesting some type of is habitat dependent, suggesting that snake populations generate concealment value for the zigzag pattern in more structured habi- individuals of both patterns, and these would increase their fitness tats. This habitat dependence is supported by the study of Santos (survival) depending on the habitat structure (Pyron and Burbrink et al. (2014), who verified that the zigzag design in V. latastei varied 2009). According to Levins (1968), phenotypic polymorphism geographically in relation to the lithology and land uses. 3) The increases fitness when a species occurs in heterogeneous environ- observed differences in escape behavior and approach distance ments. The landscape heterogeneity of the Mediterranean region, in between zigzag and bilineata viperine snakes. Selection from visually some places composed of a patchy distribution of freshwater envi- guided predators acts on the interaction between dorsal pattern and ronments surrounded by open or forested habitats, would have been behavior (Pough 1976; Lindell and Forsman 1996). The fact that the scenario to allow coexistence of alternative N. maura dorsal pat- most zigzag viperine snakes remain still before the predator (the terns adapted to different antipredatory strategies. researcher) begins any prey-catching behavior, and that only after handling displayed indisputable aposematic behaviors, such as head triangulation, snorting, and (false) attacks (authors, personal obser- Author contributions vation), suggests that the snakes firstly rely on the cryptic role of the zigzag dorsal pattern. If this camouflage strategy fails, the aforemen- X.S. and J.M.P. conceived the idea. X.S. analyzed the data, and all tioned signaling mechanisms trigger, and the aposematic role of the authors contributed to collecting the data and writing the zigzag dorsal pattern appears. Indeed, we conclude that the zigzag manuscript. 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Oecologia 116: polymorphism in snakes (Reptilia: Ophidia). Biol Rev 69:599–610. 113–119. Wu ¨ ster W, Allum CSE, Bjargardo ´ ttir IB, Bailey KL, Dawson KJ et al., 2004. Shine R, Madsen T, 1994. Sexual dichromatism in snakes of the genus Vipera: Do aposematism and Batesian mimicry require bright colours? A test, using a review and a new evolutionary hypothesis. J Herpetol 28:114–117. European viper markings. Proc Roy Soc B 271:2495–2499. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Current Zoology Oxford University Press

Ecological significance of dorsal polymorphism in a Batesian mimic snake

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Abstract

Batesian mimicry is the process in which harmless species adopt the appearance of a dangerous, aposematic species. In some prey species, both Batesian mimetic and non-Batesian morphs coex- ist, presupposing that both morphs have to be evolutionarily advantageous. The viperine snake, Natrix maura, exhibits a zigzag dorsal pattern and antipredatory behavior that mimics European vipers. This snake also has a striped dorsal pattern that coexists with the zigzag pattern. We have examined whether individuals belonging to different geographically structured clades were more likely to exhibit a certain dorsal pattern, and whether the zigzag pattern has a protective function by exposing artificial snakes to predation in natural environments, in addition to comparing antipreda- tory behavior between zigzag and striped snakes also in natural environments. Our results indicate that the striped pattern was not geographically structured, but habitat-dependent. Aerial predators less frequently attacked zigzag plasticine models than striped or unpatterned models. We detected a shift in antipredator behavior between the 2 morphs, as Batesian mimicking N. maura responded to an approaching potential predator by remaining immobile or fleeing at shorter distances than did striped ones. We conclude that Batesian mimics maintain the cryptic and aposematic value by resembling vipers, whereas in open habitats the non-Batesian mimic has altered its antipredator behavior to maintain its fitness. Key words: antipredatory strategies, aposematism, Batesian mimicry, crypsis, dorsal pattern, Natrix maura In the predator–prey context, prey have developed multiple strat- spider species mimic ants (Mclver and Stonedahl 1993). Among ver- egies to survive (Ruxton et al. 2004). Among others, aposematism tebrates, there are examples among fish (McCosker 1977), amphib- consists in the development of warning signals designed to dissuade ians (Kuchta 2005), and birds (Rowe et al. 1986), although Batesian potential predators (Poulton 1890; Rowe and Guilford 2000). mimicry is rare in mammals (but see Pough 1988). In this study, we Interestingly, some species have evolved to mimic aposematic species address an example of Batesian mimicry in snakes. to gain some functional advantage. In Batesian mimicry (Bates Snakes are highly polymorphic in dorsal patterning and an excel- 1862), harmless species adopt the appearance of a dangerous, apose- lent model group to address the evolutionary drivers of dorsal pat- matic species, to protect themselves from predation, although they tern design (Cox and Davis Rabosky 2013), with camouflage, are really inoffensive (Maynard Smith 1998). Batesian mimicry aposematism, and thermoregulation being the major evolutionary appears to be a widespread taxonomic phenomenon (Ruxton et al. drivers of dorsal pattern diversification (Allen et al. 2013). 2004). Edmunds (1974) provides many examples of mimetic associ- Moreover, many inoffensive snake species resort to Batesian mimi- ations in butterflies, some of them being Batesian mimics, and many cry by reproducing the aposematic dorsal pattern of dangerous V C The Author (2017). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 2 Current Zoology, 2017, Vol. 00, No. 00 species (Brodie and Brodie 2004). A classic example of aposematism common (see review in Allen et al. 2013), far fewer studies have occurs in European vipers of the genus Vipera, which present a dis- analyzed the same topic in mimetic species (but see Greene and tinctive set of morphological and behavioral characteristics, such as McDiarmid 1981; Cox and Davis Rabosky 2013). Similarly, few a short and stout body, head triangulation, coiling, snorting, and studies have addressed antipredator responses against predators zigzag dorsal pattern, which their potential predators relate to their other than humans (Gregory 2016). We specifically address the fol- high intensity of defences (Wu ¨ ster et al. 2004; Niskanen and lowing questions: Mappes 2005; Valkonen et al. 2011a). The zigzag dorsal pattern is (1) Is the occurrence of zigzag and bilineata dorsal patterns in N. maura geographically structured? Scha ¨ tti (1982) showed that the likely a multifunctional protective coloration; it provides protection bilineata pattern appeared fundamentally in coastal areas, against predation because of its aposematic role, although this pat- increasingly to the south and being completely absent in some popu- tern in certain settings would also favor crypsis (Cott 1940; Andre ´n lations. Later, Guicking et al. (2002) studied the phylogeography of and Nilson 1981; Shine and Madsen 1994; Santos et al. 2014). the species, providing a genetic framework for the analysis of the The elaborate and consistent set of morphological and behavio- spatial distribution of this trait. These authors detected 3 geographi- ral traits of most European viper species has been copied by the inof- fensive viperine snake Natrix maura (Linnaeus 1758) (Rollinat cally structured lineages from the Pliocene, 2 in Africa, and one in 1934) as defensive mimicry. This water snake is distributed by the Europe. If the occurrence of the bilineata pattern in N. maura was Western Palaearctic and mimics morphological and behavioral traits not geographically structured and occurred in all the lineages, we of European vipers with which it coincides geographically to some hypothesize that the dorsal dimorphism would have no relationship degree, for example, Vipera aspis (Linnaeus 1758), V. latastei Bosca ´ with the phylogeography of the species. 1878, and V. seoanei Lataste 1879 (Aubret and Mangin 2014; (2) Is the relative frequency of zigzag and bilineata patterns asso- Santos et al. 2014). For example, N. maura exhibits a zigzag dorsal ciated with any landscape appearance? In some snakes, strong selec- pattern (hereafter zigzag) formed by a wide and dark dorsal band, tion promotes variability across spatial scales (Cox and Davis zigzag shaped, from the neck to the tail, which contrasts with lighter Rabosky 2013). Despite the latitudinal cline of the bilineata fre- quency cited by Scha ¨ tti (1982), geographically close populations background body colors. Moreover, N. maura displays head trian- exhibit opposite frequencies of the zigzag and bilineata patterns gulation, a spring-like body posture (coiling), snorting, body infla- (Duguy and Saint-Girons 1993). Based on the field experience of the tion, and striking (Rollinat 1934). authors, the striped morphotype appears to be more common in Notably, N. maura also shows dorsal pattern variability, since wetlands and other open landscapes (see also Duguy and Saint- some specimens have a striped pattern of 2 dorso-lateral light bands Girons 1993; Santos 2009), but there are no studies on the associa- (longitudinally striped sensu von Helversen et al. 2013), or bilineata tion between habitat type and the frequency of the 2 dorsal pattern dorsal pattern (hereafter bilineata) (Scha ¨ tti 1982). Based on mito- across the range of N. maura. chondrial markers, these bilineata individuals are genetically indis- (3) Have bilineata snakes lost the Batesian-mimic role by no lon- tinguishable from the zigzag individuals of the same population ger resembling a viper? The zigzag pattern in N. maura is presumed (Carranza S, personal communication). Intraspecific variability in to have an aposematic, even cryptic function, due to its viper mime- snakes with one of the patterns being striped is quite common in sis, while the bilineata dorsal pattern in snakes does not (Brodie snakes, especially in Colubridae (Wolf and Werner 1994), and can 1992; Wolf and Werner 1994; Allen et al. 2013). Thus, in the be geographically structured or sympatric (Kark et al. 1997). The absence of behavioral modulation (i.e., by snake plasticine models) striped pattern tends to enhance a visual escape strategy, as snakes and maintaining similar background, we hypothesize that the non- can confuse predators by not providing body references in tracking Batesian (bilineata) individuals will be more frequently attacked by its movement (Pough 1976; Allen et al. 2013); this dazzle effect, the predators than will the Batesian (zigzag) ones. motion dazzle camouflage, has recently been supported experimen- (4) Do bilineata and zigzag N. maura display different antipreda- tally (Hogan et al. 2016). Accordingly, compared with non-striped tory behavior when confronted with predators? In snakes, dorsal snakes, striped ones usually show a high frequency of broken tails as pattern and antipredator behavior interact (Brodie 1992), and dorsal a consequence of failed predation events (Pleguezuelos et al. 2010). pattern diversification is related mainly to behavior, rather that hab- In the absence of temporal variation in selective forces, the main- itat choice (Allen et al. 2013). For this reason, the maintenance of tenance of polymorphism (variability within a geographical loca- striped individuals in a population is expected when this pattern can tion) and of polyphenism (variability between geographical confer some antipredatory and other evolutionarily advantages locations) presupposes that the morphs should thrive under different (Brodie 1992; Wolf and Werner 1994). Thus, we hypothesize that, environments (Wolf and Werner 1994; Shine and Harlow 1998). linked to the loss of the viper mimesis in striped N. maura, individu- For N. maura, the coexistence (syntopy) of bilineata and zigzag als would display different antipredatory strategies with regard to snakes also suggests the use of different antipredator strategies (i.e., their dorsal pattern: whereas Batesian mimic (zigzag) individuals are fast-moving vs. static snakes; Allen et al. 2013). Wolf and Werner expected to mirror viper strategy, that is, by staying immobile, non- (1994) suggested that striped snakes tend to thrive in open habitats, aposematic (bilineata) individuals are expected to try to escape, as while those with alternative dorsal patterns (i.e., blotched) prosper occurs in other striped snakes (Jackson et al. 1976; Brodie 1992; in structurally more complex habitats (see also Pough 1976). Wolf and Werner 1994; Pleguezuelos et al. 2010; Allen et al. 2013). Unfortunately, studies on the ecological drivers and the adaptive value of intraspecific dorsal variability in snakes under an experi- mental or comparative framework have been scarcely addressed Materials and Methods (but see Andre ´ n and Nilson 1981; Shine and Harlow 1998; Cox and Davis Rabosky 2013). Geography and spatial ecology of the variability The objective of this study is to uncover the evolutionary drivers The spatial distribution of the variability of N. maura was examined of the dorsal pattern dimorphism in N. maura. While the studies on by the analysis of bilineata and zigzag dorsal pattern frequencies in the function of dorsal patterns in model species (e.g., true vipers) are 917 individuals from 12 populations (Table 1), covering all the Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Santos et al.  Dorsal polymorphism in a Batesian mimic snake 3 Figure 1. Geographic distribution of snakes belonging zigzag and bilineata patterns in the 12 sites studied along the Natrix maura range (A). On the top, examples of freshwater closed (B) and open (C) habitats where N. maura inhabits. On the bottom, living examples of snakes with the 2 dorsal patterns (D, E; photos by Rau´l Leo´ n). Pie charts depict the frequency of bilineata (red) and zigzag patterns (gray). Locality names in red refer to open (wetland) habitats, and in black to closed (river) habitats. phylogenetic clades (Guicking et al. 2002) and most of the range of study is V. latastei, both in North Africa and the Iberian Peninsula, the species (Figure 1A). We examined vouchers from scientific col- and both species shared the visually oriented and most specialized lections (nine localities) and field records of the authors and col- predator (snake-eater) in the study area, Circaetus gallicus; thus, V. latastei is the model species mimicked by N. maura. Vipera latas- leagues from specific sites (3 localities) corresponding to either of the 2 contrasting natural landscapes where the species thrives tei is a rather shy species with abundance hard to measure. (Santos 2009), that is, open and not-open habitats, with sample size However, to include the effect of the model species in the Batesian system, we have considered in our statistical analysis the distance of >15 (Table 1). Open habitats were marshlands and peat bogs where vegetation, depending on site, was composed of broadleaf cattail the closest viper population to each N. maura population, based on Typha latifolia, common reed Phragmites australis, bulrush Scirpus our field experience, and by the tool for measuring distances in Google Earth (Table 1). Although snake pigmentation fades some- holoschoenus, great fen-sedge Cladium mariscus, perennial saltwort what with preservation in liquid, all museum specimens were easily Sarcocornia fruticosa, and sedges (Carex sp.), reaching a height of 0.4–1.5 m, with grassland and reeds dominating in the banks. classified as zigzag or bilineata. Given that snake vouchers shrink due to fixative and the preservative process (Barry 2011), we esti- Closed habitats were rivers and streams with banks dominated by mated SVL for museum vouchers without fresh measurements by stones and thick vegetation, and, depending on sites, made up of willows (Salix sp.), silver poplar Populus alba, elm Ulmus minor, applying the regression of fresh against preserved SVL for this spe- cies (Santos et al. 2011). ash Fraxinus angustifolia, honeysuckle Lonicera arborea, and elm- leaf blackberry Rubus ulmifolius, with a height of 1.0–15.0 m (Figure 1B,C). Predation experiment with plasticine models For each individual examined, body size (snout–vent length, To test whether bilineata snakes lost their Batesian mimicry role SVL, to the nearest millimeter), sex (according to Feriche et al. compared with zigzag snakes, we performed a field-based predation 1993), and dorsal pattern (2 possibilities, zigzag and bilineata, experiment with plasticine models (see similar experiments in Figure 1D,E) were recorded. Although in Batesian mimicry systems Wu ¨ ster et al. 2004; Niskanen and Mappes 2005; Valkonen et al. mimic and model do not need to be strictly sympatric (Pfennig and 2011b). We made 12 bilineata and 12 zigzag plasticine models of Mullen 2010), it is also true that if the number of models decreases, snakes plus 12 patternless models as control (thereafter control). the benefits gained by mimics also decrease (Valkonen and Mappes Models were made by melting non-toxic plasticine (JOVER )in a 2014). The closest viper species to all populations considered in this silicone mould of a N. maura voucher from the study area (355 mm Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 4 Current Zoology, 2017, Vol. 00, No. 00 Table 1. Localities considered in this study for the analysis of the dorsal pattern in the viperine snake, Natrix maura, within the Western Mediterranean Locality Latitude Longitude Habitat Clade Distance to viper (km) N ZZ BL Sampling 0  0 Algeria 36 46N8 13 E Open Algerian 30 16 10 6 EBD 0  0 Rif Mountains 35 07N5 17 W Not-open Moroccan 20 41 40 1 Private collection S. Fahd 0  0 Baetic Mountains 37 12N3 42 W Not-open Iberian 15 77 76 1 DBAG 0  0 Burgos province 42 45N3 48 W Not-open Iberian 2 21 21 0 EBD 0  0 Ca ´ diz province 36 35N6 14 W Open Iberian 26 28 14 14 Field sampling, S. Busack 0  0 Cazorla Mountains 37 54N2 56 W Not-open Iberian 1 28 28 0 EBD 0  0 Delta Ebro 40 42N0 45 E Open Iberian 35 318 183 135 Field sampling 0  0 Donana ~ 36 59N6 26 W Open Iberian 5 113 69 44 EBD 0  0 Rı´o Frı´o River 37 09N4 12 W Not-open Iberian 3 147 147 0 DBAG 0  0 Matarranya River 41 07N0 12 E Not-open Iberian 10 50 50 0 Field sampling 0  0 Charca Sua ´ rez 36 43N3 12 W Open Iberian 18 37 21 16 Field sampling/DBAG 0  0 Puertollano pools 38 39N4 06 W Open Iberian 15 41 38 3 Field sampling Notes: We include the geographic coordinates for the barycentre of the localities, the habitat (2 possibilities, open when marshlands or peat bogs, and closed when others), the phylogenetic clade, the distance to the closest viper population (Vipera latastei), the sample size (N), the frequency of the bilineata (BL) and zig- zag (ZZ) dorsal pattern, and the provenance of the sample. Abbreviations are as follows: EBD, Estacio ´ n Biolo ´ gica de Donana, ~ Sevilla, Spain; DBAG, departa- mento de biologı´a animal, Granada University, Spain; CRBA, Centre de Recursos de Biodiversitat Animal, Barcelona University, Spain. tooth marks were observed, and recorded as made by birds when bill marks were detected (Niskanen and Mappes 2005). As preda- tors, birds are primarily visually oriented while mammals are pri- marily odour oriented. For this reason, marks caused by birds and mammals were recorded and analyzed separately. To avoid insect parasitism and damage, models were sprayed with insect repellent (Autan ; Valkonen et al. 2011b), and to avoid model displacement by predators, they were pegged to the soil by an iron wire that ran the full length of the model. Field experiments were performed in 2013 in Padul, and 2013, 2015, and 2016 in Charca Sua ´ rez, during May and June, a period with high diurnal activity of N. maura (Santos and Llorente 2001). Figure 2. Plasticine models used for the experimental study of predation upon the viperine snake, Natrix maura. From top to bottom, zigzag, striped We conducted 12 trials (4 in Padul and 8 in Charca Sua ´ rez) to check (bilineata) and uncolored (control) model. predation on plasticine models. At each trial, 27–36 models (9–12 sets of models with one model of each dorsal pattern per set) were placed on a grassland background on the banks of the wetlands. Sets SVL, the average body size for this population; N ¼ 290). The back- were placed 20–50 m apart, and models were spaced roughly 6 m ground body color of the models was made by melting brown, green, and white plasticine colors (ratio 10:5:1, respectively). The apart, in random order. Models were placed in the early morning pattern in zigzag models was painted with a permanent marker (08.00–09.00), and experimental trials lasted from 2 to 5 days, with no differences in the duration of trials between Padul and Charca (EDDING 500 ), 5 mm width, while the 2 mm wide dorso-lateral Sua ´ rez (Mann–Whitney U-test; Z ¼ 0.17, P ¼ 0.9). Models were stripes of the bilineata model were made by melting white, green, checked on a daily basis in late afternoon (19.00–20.00) during the and yellow plasticine colors (ratio 5:2:1, respectively). Control mod- trials. More than one attack on a single model during a trial was els exhibited only the ground color (Figure 2). Experiments with plasticine models were conducted in 2 local- considered a single-attack event to reduce pseudoreplication and ities from the south-eastern Iberian Peninsula, where both dorsal bias caused by potential multiple attacks from an individual preda- tor on a single plasticine model (Valkonen et al. 2011b). Thus, the patterns coexist, Charca Sua ´ rez, a 28 ha marshland, 200 m from the 0  0 sampling units were the models in each trial. A total of 104 models sea shore (3 32 W, 36 43 N, 1 m altitude), and Padul, a 85 ha peat 0  0 were examined in Padul (4 trials  27 models minus 4 models stolen bog, inland and 30 km from the other site (3 36 W, 37 00 N; 725 m altitude). The landscape of both study sites was formed by wetland by humans), and 276 in Charca Sua ´ rez (6 trials  36 models, and 2 trials with 30 models). vegetation, such as T. latifolia, P. australis, S. holoschoenus, the introduced giant cane Arundo donax, and C. mariscus in Charca Sua ´ rez. Based on the list of N. maura predators (Santos et al. 2011), Antipredatory behavior experiments during the study period, nine potential avian predators were As the previous predation experiments with plasticine models sug- reported in Charca Sua ´ rez (Ardea cinerea, A. purpurea, Ardeola ral- gested that bilineata snakes lost the advantages of the mimesis with loides, Bubulcus ibis, C. gallicus, Egretta garzetta, Larus michahel- vipers (see results below), we also examined differences in antipreda- lis, L. ridibundus, Porphyrio porphyrio; from the data of the tory behavior between bilineata and zigzag individuals. For this, we authors), and seven potential avian predators in Padul (A. cinerea, conducted a field experiment in Charca Sua ´ rez, a study area A. purpurea, B. ibis, C. gallicus, Circus aeruginosus, Egretta harboring both types of dorsal patterned N. maura. Surveys were garzetta, Nycticorax nycticorax;Pe ´ rez-Contreras J, personal conducted by a single researcher along a 1,500-m transect in the communication). Attacks were recorded as made by mammals when wetland banks, during May and June 2013, 2015, and 2016 (90 h of Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Santos et al.  Dorsal polymorphism in a Batesian mimic snake 5 surveys). Snakes were searched when basking very close to the water computes the likelihood ratio statistic of the model containing a par- (known as the K thermoregulatory strategy; Hailey and Davies ticular term or not (significant when P< 0.05). 1987). When a snake was spotted, it was observed through binocu- A GLZ with a Poisson distribution was used to compare fleeing lars (8  30), its body size was estimated (SVL, to the nearest cm, distance of snakes of both dorsal patterns when confronted with a after training), and its dorsal pattern was classified as zigzag or bili- potential predator. Fleeing distance is a continuous variable; how- neata. The sex of the individuals was disregarded because of the ever, due to inaccuracies of some distance measurements we consid- lack of sexual differences in the frequency of both dorsal pattern ered fleeing distances in 0.5 m intervals, using a Poisson distribution (Duguy and Saint-Girons 1993) and in the burst speed in lab trials to perform the model. GLZs were performed with air temperature on defence behavior (Hailey and Davies 1986). Afterward, the (surrogate of body temperature) and body size as covariates, due to researcher approached slowly and directly at a constant speed of their potential effect on escape speed of this species. Body condition 0.8 m s , until the snake began to flee from the researcher. The flee- (BC) can be considered a surrogate of snake’s locomotor capacity ing distance was measured by a metric tape to the nearest 10 cm. (Jayne and Bennett 1990). Thus, we hypothesized that differences in Body temperature can affect reptile behavior, particularly when BC between zigzag and bilineata could be linked to variation in deciding whether to move or remain still when confronted by a escape distance to predators, that is, lower BC for snakes that flee at predator (Hertz et al. 1982). Unfortunately, some basking individu- longer distances, and higher BC for snakes that allow a closer als (all bilineata) fled to deep water when the researcher approach of predator. The residuals of the regression analysis approached, precluding capturing them to record body temperature. between log body mass and log SVL were used as a measure of BC. Thus, we recorded air temperature 1 m above ground (Hibok 14 We were unable to capture most of the individuals during our trials thermometer, to the nearest 0.1 C) as a surrogate of snake body to check differences in escape behavior between zigzag and bilineata temperature. Although body temperature of basking individuals of snakes in the face of an approaching predator. For this reason, BC this species is usually above air temperature, there is a good correla- was compared between zigzag and bilineata snakes from the same tion between the 2 temperatures (Hailey and Davies 1987), particu- locality, the Ebro Delta, where body mass and length were measured larly during spring (Santos 2009). Snakes escaping also precluded for a large sample size. BC was calculated separately for males and marking for individual identification; however, we assumed that the females (Santos and Llorente 2004). In the “Results” section, means large size of the study area minimized pseudoreplication of the data are followed by 61 SD. by recording the escape distance of the same individual several times. Results Of the 917 snakes examined, 687 were zigzag and 213 bilineata Statistical analyses (76% and 24%, respectively). However, there was interpopulation Two analyses were conducted to identify which factors could variation in the frequency of the 2 dorsal patterns across the N. explain the occurrence of each dorsal pattern of the viperine snake maura range (Figure 1A). The distribution of both dorsal patterns across its range: 1) with the entire data set (all localities, including museum specimens and live ones), we performed a generalized linear was puzzling; some sites were devoid of bilineata individuals, and model (GLZ) with a binomial distribution of the dependent variable bilineata frequencies differed markedly between pairs of nearby and a logit function, using dorsal pattern (zigzag and bilineata) as a sites. The bilineata dorsal pattern was present in regions with the 3 dependent variable, and sex and body size of individuals (SVL) as phylogenetic groups (Figure 1A and Table 1). factors. This analysis was aimed at examining the effects of factors The GLZ demonstrated that neither SVL (Wald Statistic ¼ 0.27, like sex and body size on the dorsal pattern occurrence regardless of P ¼ 0.6) nor sex (Wald Statistic ¼ 0.09, P ¼ 0.8) explained the occur- locality. 2) For each population, we used the percentage of snakes rence of the bilineata pattern on snakes. We repeated this analysis with a bilineata pattern as a dependent variable (percentages were with only animals examined at sites where at least one bilineata arc-sin transformed), and we performed a general linear model snake appeared, and the results were the same, that is, there were no (GLM) with the habitat type (open and closed habitats), the distance sexual or ontogenetic effects in dorsal pattern occurrence. The GLM (km) to the closest V. latastei population, and the latitude, as factors. indicated that the percentage of individuals with bilineata pattern at This second analysis assessed how landscape type, model organism each of the 12 populations was related to the habitat type proximity (viper), and geographic location affected the dorsal pat- (F ¼ 14.45, P ¼ 0.005); bilineata snakes were frequent only in open tern frequency of the bilineata pattern among the populations. To habitats, whereas this pattern was almost absent from closed habi- tats (Figure 1A). A nonparametric test using the percentage of occur- meet the assumption for a linear model, residuals of the dependent rence in each population confirmed significant differences between variable on the grouping factors were examined. the 2 major habitat types in the frequency of the 2 dorsal patterns Log-linear analyses were run to test differences in predation (Mann–Witney U-test, Z ¼ 2.86, P ¼ 0.004). By contrast, we found (depredated and non-depredated) among the 3 plasticine models no significant spatial effect, that is, geographic latitude of each pop- (zigzag, bilineata, and control) and the 2 study sites (Charca Sua ´ rez and Padul peat bog). We tested the association among these 3 cate- ulation (F ¼ 0.20, P ¼ 0.7), nor any relation with the distance to the gorical variables (predation, model type, and locality) in a multidi- closest V. latastei population, that is, the model species for the mimi- mensional contingency table. Log-linear analysis uses a likelihood cry (F ¼ 0.77, P ¼ 0.4). ratio chi-square statistic. The algorithm used generates several mod- From the 380 predation trials made with plasticine models (276 els to test interactions among all variables and selects the least com- in Charca Sua ´ rez and 104 in Padul), 100 attacks by avian predators plex model that best accounts for the variance in the observed were recorded (26.3% of the models). In total, bilineata was the frequencies. We were specifically interested in testing the association most frequently attacked model (n ¼ 45; 35% of the bilineata mod- of Predation Locality and PredationDorsal pattern. The results els examined), the control the second most attacked (n ¼ 32; 25% of were interpreted by checking the odds-ratio scores in expected val- the control models examined), and the zigzag pattern was the least ues of partial and marginal association tests. The odds ratio attacked (n ¼ 23; 19% of the zigzag models examined). The log Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 6 Current Zoology, 2017, Vol. 00, No. 00 Table 2. Partial and marginal association tests of the log linear Table 3. General linear models of differences in flight distance analysis for the attack condition (attacked and not attacked by between bilineata and zigzag Natrix maura phenotypes using birds), locality (Padul and Charca Suarez) and dorsal pattern (bili- snake body size (SVL, snout–vent length, in millimeter) and air neata, zigzag, and control) of plasticine models of Natrix maura in temperature ( C) as covariates in the population of Charca Sua´rez, 2 localities of south eastern Iberian peninsula where both natural south-eastern Iberian peninsula morphotypes for dorsal pattern (bilineata, zigzag) are represented Estimate Standard error Wald Stat P 2 2 df Partial X P Marginal X P SVL 0.000874 0.002 0.25682 0.61 Site (S) 1 79.40 <0.0001 79.40 <0.0001 Air temperature 0.006432 0.007 0.79421 0.37 Dorsal pattern (DP) 2 0.08 0.96 0.08 0.96 Dorsal pattern 0.601609 0.164 13.32934 <0.0001 Attacks (A) 1 87.28 <0.0001 87.28 <0.0001 S * DP 2 0.45 0.80 0.22 0.90 S * A 1 35.88 <0.0001 35.65 <0.0001 individuals were almost exclusively in open habitats, whereas zigzag DP * A 2 9.11 0.01 8.89 0.01 individuals were found in all types of habitats (see also Wolf and Werner 1994; Kark et al. 1997; Cox and Davis Rabosky 2013), Note: Sample size in the results section. although the most frequent in closed habitats. This result reveals why previous studies failed in fitting a geographic pattern for the linear analysis showed a significant interaction between Locality presence of both dorsal patterns in N. maura (Scha ¨ tti 1982; Duguy and Attacks, and between Model and Attacks (Table 2). The mar- and Saint-Girons 1993); mimicry is not restricted to one sex or to ginal frequency tables showed that the occurrence of attacks was ontogenetic stage, and variation occurred across habitat, rather than higher in Padul than Charca Sua ´ rez, and for bilineata than for the geography. In their review of the frequency of the striped dorsal pat- other 2 models. When mammal attacks were examined, we found tern in snakes, Wolf and Werner (1994) concluded that snakes bear- no differences in the frequency of attacks made on the 3 plasticine ing this phenotype inhabited habitats that were less structurally models (v ¼ 1.77, P ¼ 0.18). complex than those bearing blocked or cross-banded dorsal patterns Fleeing distances were recorded for eight bilineata (average flight (see also Pough 1976). distance 3.06 1.1 m), and 17 zigzag N. maura individuals (average Camouflage is frequently selected in snakes (Allen et al. 2013), flight distance 0.96 0.7 m). The GLZ showed that bilineata individ- with different habitats favoring different morphs (Kark et al. 1997; uals fled at the farther distances from the approaching potential Shine and Harlow 1998). We speculate that the zigzag dorsal pat- predator than did zigzag individuals, irrespective of body size or air tern would be beneficial in concealing individuals in more closed temperature (Table 3). It bears noting that 6 out 17 zigzag snakes habitats, where a chaos of images is created by lights and shadows recorded did not flee at all, and exhibited aposematic behavior such (Cuthill et al. 2017; Endler and Mappes 2017). While not proven, as head triangulation, coiling, snorting, and false attacks, only after this interpretation has been posed several times for this dorsal pat- they were gently captured by hand. The remaining 11 individuals tern in vipers (Shine and Madsen 1994; Niskanen and Mappes that fled to a very close distance from the researcher did not exhibit 2005). In contrast, striped snakes would be favored in more open aposematic behavior. habitats, where the combination of lights and shadows would create No differences were found in BC between zigzag and bilineata straighter forms on the background (Wolf and Werner 1994). As N. individuals either in males (Student’s t ¼ 0.18, df ¼ 67, P ¼ 0.9) or in maura inhabits 2 highly contrasting aquatic habitats, wetlands and females (Student’s t ¼ 0.10, df ¼ 53, P ¼ 0.9). This suggests that rivers (Santos 2009), we propose here that heterogeneity in the vege- body shape of zigzag and bilineata individuals did not vary. tation structure surrounding water bodies would be the driving fac- tor for the emergence of dorsal pattern dimorphism in this species. Discussion Dorsal pattern and predator attacks Dorsal pattern and geography Our experiment with plasticine models within the same locality and In the interpretation of animal coloration, tests of geographical varia- habitat confirmed that predators responded differentially to the tion are critical (Cox and Davis Rabosky 2013; Santos et al. 2014). snake dorsal pattern. On a grassland background, control and bili- Our results on the geographic distribution of the 2 dorsal patterns of neata models were more frequently attacked by aerial, visually ori- the viperine snake were puzzling, although in contrast to Scha ¨tti ented predators (birds), than were zigzag models. This was the same (1982), we found that bilineata individuals were present in many result found with viper plasticine models (Valkonen et al. 2011b), inland regions. Notably, bilineata individuals also appeared in popula- confirming that snakes with the zigzag dorsal pattern better avoided tions representing the 3 phylogenetic lineages of the species, north- attacks than did snakes with other dorsal patterns (Wu ¨ ster et al. western Africa east of the Muluya River, north-western Africa west of 2004; Niskanen and Mappes 2005), at least when prey are static the Muluya River, and the European clade (Guicking et al. 2002, (Lindell and Forsman 1996). Our result supports the idea that the 2008). This suggests the character to be African and ancient, as the camouflage provided by the zigzag pattern or that predator wariness species evolved in that continent and clades separated 3.5–4.0 Myr to the model organisms (i.e., vipers) can drive a mimetic system in (Guicking et al. 2002)—although it may also have evolved repeatedly snakes (Greene and McDiarmid 1981; Cox and Davis Rabosky (by convergence) in response to similar ecological demands in the dif- 2013). ferent clades, as is common in snakes (Allen et al. 2013). In the Padul peat bog, plasticine replicas were more frequently attacked than those in Charca Sua ´ rez. Although the potential preda- Dorsal pattern and habitat tor communities were similar, we were unable to adequately meas- The polymorphism for the dorsal pattern in N. maura seems to be ure predator density at either site, and therefore we have no suitable linked to the habitat. Regardless of sex and body size, bilineata explanation for this difference. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox058/4430504 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Santos et al.  Dorsal polymorphism in a Batesian mimic snake 7 Dorsal pattern and snake behavior dorsal pattern in the viperine snake (as well as in vipers, the model One of the benefits of the high and constant body temperature that organism) would have a double function, concealing individuals N. maura maintains during its K thermoregulation is to retain a against the background and deterring predators. We also experimen- potential for instant high muscular performance (Hailey and Davies tally confirm the Batesian mimesis of the viperine snake to the 1986). Our study demonstrated that, when a potential predator European vipers as model organisms. We acknowledge that our results on attacks are based on plasti- approached, bilineata individuals fled from longer distances than cine models, and those on fleeing distance of live individuals are did zigzag individuals. Some of the latter even remained static until derived from a rather small sample size, which makes it advisable to they were captured by the researcher. Thus, viperine snakes with dif- discuss these issues under alternative hypotheses. The Batesian mime- ferent dorsal patterns varied their antipredatory strategies, suggest- sis of the viperine snakes on vipers do not limit to the zigzag dorsal ing adaptations to increase their fitness. Bilineata individuals, pattern, and includes other behavioral aposematic traits such as coil- lacking the camouflage or the aposematic effect of the zigzag pat- ing, striking, snorting, and head triangulation (Rollinat 1934; Aubret tern, begin to flee when a potential predator approaches. The dorsal and Mangin 2014). However, as we used the same cast (that was not stripe design is common in snakes, especially in the fastest species coiled neither showed head triangulation) for the 3 types of models (Brattstrom 1955). Snakes bearing this dorsal pattern rely on the (Figure 2), we deduce that the higher frequency of bird attacks to bili- confounding effect on predators of the dorsal stripes when the snake neata and control models was exclusively the consequence of the dif- moves (Pough 1976; Allen et al. 2013), making the formation of a ferences in dorsal design among models. The use of static behavior, search image more difficult (Hogan et al. 2016). That is, the percep- typically balling up, as defence in N. maura is more frequent in small tion of speed (von Helversen et al. 2013) and direction (Jackson individuals (Hailey and Davies 1986). However, we rule out the con- et al. 1976) is disrupted, and the location of the focal part of the founding effect of body size in zigzag and bilineata dorsal patterned body, the head (Langkilde et al. 2004), is more difficult (Brodie individuals when a potential predator approaches, as we failed to find 1992; Hu et al. 2009). This interpretation fits the link between the body-size differences between the individuals of different dorsal pat- bilineata dorsal pattern and open habitats found in this study. In terns recorded for this analysis. The same null hypothesis was con- open habitats such as wetlands, the vegetation has less structural firmed for the effect of sex, as sexual dichromatism is often absent in complexity and less irregularly shaped patterns of shadowing. In snakes (Shine and Madsen 1994). Lastly, in their laboratory experi- these micro-scenarios, we argue that the zigzag dorsal patterned ment, Hailey and Davies (1986) also found that starved snakes (for 4– viperine snakes would begin to leave evolutionary room for striped 5 weeks) were more likely to use static defence than post-absorptive snakes, which adopt longer escape distances from approaching pred- ones. We were unable to consider this factor in our trials, as most bili- ators (Allen et al. 2013). neata individuals fled to the water, so that the weight or feeding status of these specimens could not be checked. However, we minimized this Crypsis or aposematism? possibility, as the study site harbored a good population of birds and Experiments with plasticine models did not resolve the question that N. maura, likely for its abundant trophic resources (unpublished data differences in predation rates between morphotypes were the conse- of the authors). Moreover, during field surveys over 3 years, we never quence of the cryptic or aposematic role of the zigzag pattern, or found an emaciated individual of this species in the study area even whether both roles are acting. Several studies have demon- (n ¼ 60). strated the aposematic value of the zigzag pattern (Wu ¨ ster et al. 2004; Niskanen and Mappes 2005; Valkonen et al. 2011b). Ecological significance of dorsal polymorphism However, simultaneous adaptive benefits of this pattern cannot be ruled out, for example, a distance-dependent function for crypsis Assuming the ecological advantages of the zigzag pattern in N. (Valkonen et al. 2011b). We suggest 3 complementary reasons to maura, what are the evolutionary drivers of the maintenance of dor- explain the cryptic role of the zigzag pattern in the viperine snake sal polymorphism in this species? In this study, we have ruled out system: 1) the frequency of zigzag snakes is independent of the dis- the possibility that a historical (phylogeographic) factor could give tance to the aposematic viper model, taking into account that the rise to dorsal variability. Moreover, the result for the distance to the aposematic value of a design depends on the presence of the model closest viper population also suggests no effect of model-species (Pfennig et al. 2001). 2) The maintenance of the dorsal polymor- proximity on the frequency of the viperine snake dorsal pattern. By contrast, we have demonstrated that the coexistence of both designs phism in N. maura is habitat-dependent, suggesting some type of is habitat dependent, suggesting that snake populations generate concealment value for the zigzag pattern in more structured habi- individuals of both patterns, and these would increase their fitness tats. This habitat dependence is supported by the study of Santos (survival) depending on the habitat structure (Pyron and Burbrink et al. (2014), who verified that the zigzag design in V. latastei varied 2009). According to Levins (1968), phenotypic polymorphism geographically in relation to the lithology and land uses. 3) The increases fitness when a species occurs in heterogeneous environ- observed differences in escape behavior and approach distance ments. The landscape heterogeneity of the Mediterranean region, in between zigzag and bilineata viperine snakes. Selection from visually some places composed of a patchy distribution of freshwater envi- guided predators acts on the interaction between dorsal pattern and ronments surrounded by open or forested habitats, would have been behavior (Pough 1976; Lindell and Forsman 1996). The fact that the scenario to allow coexistence of alternative N. maura dorsal pat- most zigzag viperine snakes remain still before the predator (the terns adapted to different antipredatory strategies. researcher) begins any prey-catching behavior, and that only after handling displayed indisputable aposematic behaviors, such as head triangulation, snorting, and (false) attacks (authors, personal obser- Author contributions vation), suggests that the snakes firstly rely on the cryptic role of the zigzag dorsal pattern. If this camouflage strategy fails, the aforemen- X.S. and J.M.P. conceived the idea. X.S. analyzed the data, and all tioned signaling mechanisms trigger, and the aposematic role of the authors contributed to collecting the data and writing the zigzag dorsal pattern appears. Indeed, we conclude that the zigzag manuscript. 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