Acta Herpetologica 14(1): 57-63, 2019 ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah DOI: 10.13128/Acta_Herpetol-24274 Does color polymorphism affect the predation risk on Phalotris lemniscatus (Duméril, Bibron and Duméril, 1854) (Serpentes, Dipsadidae)? Fernanda R. de Avila1,2,*, Juliano M. Oliveira3, Mateus de Oliveira1, Marcio Borges-Martins4, Victor Hugo Valiati2, Alexandro M. Tozetti1 1 Laboratório de Ecologia de Vertebrados Terrestres, Programa de Pós-Graduação em Biologia, Universidade do Vale do Rio dos Sinos, Avenida Unisinos, 950, Cristo Rei, CEP 93022-970, São Leopoldo, RS, Brasil. *Corresponding author. Email: fernandar.avila@gmail.com 2 Laboratório de Genética e Biologia Molecular, Programa de Pós-Graduação em Biologia, Universidade do Vale do Rio dos Sinos, Ave- nida Unisinos, 950, Cristo Rei, CEP 93022-970, São Leopoldo, RS, Brasil 3 Laboratório de Ecologia Vegetal, Programa de Pós-Graduação em Biologia, Universidade do Vale do Rio dos Sinos, Avenida Unisinos, 950, Cristo Rei, CEP 93022-970, São Leopoldo, RS, Brasil 4 Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Ave- nida Bento Gonçalves, 9500, Agronomia, CEP 91501-970, Porto Alegre, RS, Brasil Submitted on: 2018, 3rd December; revised on: 2018, 12th April; accepted on: 2018, 2nd May Editor: Rocco Tiberti Abstract. The snake Phalotris lemniscatus is a polymorphic species regarding color, which varies between light shades with a yellow predominance (pale yellow-brown) to darker shades with a red predominance (red-dark). Pale yellow- brown individuals are more frequent in coastal populations while there is a tendency of increasing the frequency of red-dark morphs in inland areas. Considering the variation in substrate color along the species distribution (light/ sandy on the coast to reddish and dark/argillaceous in inland areas), we raise the hypothesis that the predation rate of each morph would be lower in sites were its crypsis potential is higher. If correct, this hypothesis would reinforce the idea that the predation risk is one of the factors influencing the spatial structuring in morph frequency distributions in populations of P. lemniscatus. To test this hypothesis, we performed a field experiment using plasticine P. lemnis- catus artificial models that represent two morphs: red-dark and pale yellow-brown. The models were distributed in three localities where the following substrate types predominate: light (Coastal Site), intermediary (Lowland Site) and reddish dark (Highland Site). Our predictions were corroborated only at the coastal site, where the less cryptic morph was the most preyed one. We verified that there is a regional variation in the predation risk on different morphs. Thus, the possibility that the selective pressure by predators is a relevant element in the structuring of the frequencies of dif- ferent morph populations of this species cannot be completely excluded. Keywords. Behavior, Brazil, coral-pattern, mimetism, phenotype, snake. INTRODUCTION Polymorphism is characterized by the presence of different phenotypes in a population (Mayr, 1963) and does not only include the morphological features, but also those related to the life history and behavior of the organisms (Huxley, 1955; Hedrick, 2006). There are many processes behind the maintenance of different morphs in a population, and these processes are not easily identified (Calsbeek and Cox, 2012; Deitloff et al., 2013; Karpestam et al., 2016, Barnett et al., 2018). Questions such as “how do morphs vary their 58 Fernanda R. de Avila et alii appearance and abundance in a spatial scale” and “what are the habitat components that favor the existence and sympatry of two or more morphs” would be bet- ter answered from experiments performed under natu- ral conditions (Hoffman and Blouin, 2000; Roulin, 2004; Gray and McKinnon, 2006). In squamates, particularly in snakes, some of the most well-documented types of polymorphism are the multiple color forms (color polymorphism). From an ecological view, morphs can be considered cryptic (when they maximize the animal’s camouflage; Clarke, 1962; King and Lawson, 1995; Eizirik et al., 2003; Hoffman et al., 2006), aposematic (when they highlight a warning signal; Brodie and Brodie, 2004; Noonan and Comeault, 2009) or a combination of both (Brodie and Brodie, 1980; Wang and Shaffer, 2008; Barnett et al., 2018). Variations in the color are recorded in other taxa and are associated with an improvement in the performance of intraspecific communication, thermoregulation or as anti-predation mechanisms (Endler, 1978; Pérez et al., 2017). Snakes have many different and complex patterns of intraspe- cific color polymorphism, from systems with bright and contrasting colors to those with cryptic color sets or dis- ruptive patterns (Cox and Rabosky, 2013; Holmes et al., 2017; Martínez-Freiría et al., 2017; Santos et al., 2017). Undoubtedly, crypsis is an important factor that might bring higher survival chances to the morphotype, since the animal’s color matches the color of the sub- strate, making it difficult to be detected by vision-orient- ed predators (Johannesson and Ekendahl, 2002; Venesky and Anthony, 2007). These predators are expected to find and attack more easily the more conspicuous morphs in the population, according to their crypsis (Stimson and Berman, 1990). In southern Brazil, there are consistent records of polymorphic variations spatially structured for the Dumeril’s Diadem Snake (Phalotris lemniscatus) (Dumé- ril, Bibron and Duméril, 1854) (Fig. 1A and 1C). This species has different morphs with shades going from red-dark to pale yellow-brown (Ferrarezzi, 1993; Este- ves, 2011; Noronha, 2012). The variations seem to be restricted to these shades, with only one record of albi- nism (Abegg, 2015) and no records of a melanistic form. The distribution of P. lemniscatus morphs is spatially structured in the following way: individuals of predomi- nantly pale yellow-brown color occur more frequently in populations from regions of sandy substrate of the south- ern Brazil and Uruguay coasts, while the predominantly red-dark individuals occur more frequently in more con- tinental regions of Brazil and Argentina (Noronha, 2012). In these more continental localities, the substrates are darker due to the predominance of organic matter and clay in the soil (Lema, 2002; Esteves, 2011), allowing dif- ferential crypsis between the morphs. Many snake predators in the extreme South of Brazil are visually oriented (e.g., birds: Dell’ Aglio et al., 2012; Santos et al., 2013), and probably respond to variations in the level of contrast between their prey and the substrate. With this premise, we expect that predation is an impor- tant selective factor for the definition of the rare (more predated) and more frequent (less predated) morphs in each population. Thus, the predation rate of the morphs of P. lemniscatus should vary between regions with different substrate colors, being higher on artificial models of the red-dark type than on those of the yellow-brown type in the coastal region, and the opposite in continental regions. Because predation events are generally difficult to observe in the wild, they have been largely studied using experimental approaches as a manner to observe the interactions between predator and prey (Brodie, 1993; Guimarães and Sawaya, 2011; Purger et al., 2017). The use of artificial plasticine models has been employed successfully in predation experiments with invertebrates (Koh and Menge, 2006), amphibians (Kuchta, 2006) and reptiles (Stuart-Fox et al., 2002; Valkonen et al., 2011; Dell´Aglio et al., 2012), with highlight on snakes (Brodie, 1993; Dell’Aglio et al., 2012; Farallo and Forstner, 2012; Santos et al., 2013; Akcali et al., 2019). In the present study, we used models of P. lemnisca- tus to test the hypothesis that the predation rate of each morph would be lower in sites were its crypsis potential is higher. If correct, this hypothesis would reinforce the idea that predation risk is one of the factors for the spa- tial structuring in the distribution of morph frequencies in populations of P. lemniscatus. MATERIAL AND METHODS We distributed, in the wild, two types of artificial models of the snake: red-dark and yellow-brown (Fig. 1B and 1D). Their color was based on live specimens captured in the study area in order to accurately represent the color of the morphs that have the extremes of variation between the lighter and darker shades (Noronha, 2012; Fig. 1A and 1C). These models were manufac- tured with non-toxic plasticine that allowed the record and quan- tification of marks left by predator attacks (Brodie, 1993). The models measured 30 cm in length and 1 cm in diameter, which represents the mean size of adult animals (Carreira et al., 2012). The samplings were performed in localities with different natural proportions in the abundance of the morphs of P. lemnis- catus, these being: 1 – Coastal Site (32°43’2.49”S; 52°28’29.87”W) in the municipality of Rio Grande (annual mean temperature of 17.5 °C, Rossato, 2014), where the pale yellow-brown morph is more abundant; 2 – Highland Site (29°39’23.04”S; 51°23’7.40”W) in the municipality of São Francisco de Paula, where the red- 59Polymorphism and predation risk in Phalotris lemniscatus dark morph is more abundant (annual mean temperature of 14.5 °C; Rossato, 2014; minimum temperatures frequently close to 0 °C in winter; Maluf, 2000); 3 – Lowland Site (29°27’0.20”S; 50°34’59.83”W) in the municipality of Capela de Santana (annual mean temperature of 17.0 °C; Rossato, 2014), where both morphs are observed in similar proportions (Noronha, 2012). The sam- pled localities extend in extreme points of an area of approxi- mately 12660 km² located at least at 404 km from each other (Fig. 2). The prevailing substrates in each locality are light and sandy (Coastal Site) and dark and argillaceous (Highland and Lowland Sites), allowing the evaluation of different contrast levels between model and background. We distributed 200 models in each locality (100 red-dark and 100 pale yellow-brown), along five transects, each 400 m long. The transects were at least 1000 m from each other and each received 40 snakes (one every 10 meters). In each transect, the two morphs were interspersed so that they had 20 red-dark and 20 pale yellow-brown models, a protocol similar to that of Dell’Aglio et al. (2012) and Farallo and Forstner (2012). We used this 1:1 ratio to avoid a possible frequency-dependent pre- dation effect. Each model received an identification code and its position was marked with a GPS device to facilitate their monitoring. We also took the care to arrange all the transects in an area of similar vegetation cover (low and scarce vegetation with the prevalence of exposed soil) that would not provide any visual barrier to the predators. Thus, the contrast between the models and the background happened due to the color of the artificial snake and the soil. The artificial models remained exposed in the field for 48 hours. During this time, they were inspected twice, after 24 and 48 hours since the installation. During the inspections, we recorded the presence of attack marks on the models. Each arti- ficial model that clearly showed marks of bird attack (e.g., peck- ings) was considered a predation event (Brodie, 1993; Dell’Aglio et al., 2012). The models showing attack marks during the first inspection were replaced by new models. It is worth highlight- ing that the three localities have a similar fauna of predatory birds (Fontana et al., 2008; Petry and Scherer, 2008; Accordi and Hartz, 2006), mainly of birds of prey (e.g., Caracara plan- cus, Milvago chimango), egrets (e.g., Ardea alba, Syrigma sibila- trix) and even some other generalist foragers (e.g., Guira guira). Data analysis Just clearly identifiable pecking marks were considered as an attack (or predation event). We quantified only the presence and not the number of marks. Thus, a model with one or more marks corresponded to one predation event. To evaluate the predation intensity of each morph, we calculated the predation rate. To do so, we divided the number of models of each morph with predation evidence (number of events) by the number of exposure hours of these models. The number of exposure hours corresponds to the total number of hours between the installa- tion of the model and its final inspection. This calculation was done for each transect. To test the differences in predation rates of the morphs between the localities we performed an Analysis of Variance with randomization test (Pillar and Orlóci, 1996). In these analyses, we used Euclidian distance matrices between the morphs, restricting the permutations within the transects (blocks) to control possible discrepancies in factors related to the predation that were not directly verified (e.g. number and species of predators). The Analyses of Variance were performed by means of the software MULTIV v.3.34b (Pillar, 1997). RESULTS We recorded altogether 162 predation events, which corresponds to an overall predation rate of 1.06 events per hour. At the Lowland Site, 90 models were attacked (23%). This locality had a larger number of attacks directed to the Fig. 1. General aspect of the specimens of Phalotris lemniscatus used as a reference to the pale yellow-brown (A) and red-dark (C) patterns and their models manufactured in plasticine (B and D, respectively). The image E show some marks considered as attacks from predators. Fig. 2. Geographic location of the sampling sites. 60 Fernanda R. de Avila et alii red-dark morph (57 models; 0.22 events per hour) than to the pale yellow-brown morph (33 models; 0.13 events per hour), this difference being marginally significant (SQE = 0.02; R2 = 41%; P = 0.057; n = 10). At the Coastal Site, we recorded 22 predation events (11%). As for the Low- land Site, the Coastal Site also showed more attacks on the red-dark models (16 models; 0.07 events per hour) than on the pale yellow-brown models (6 models; 0.03 events per hour) (SQE = 0.005; R2 = 25%; P = 0.049; n = 10). At the Highland Site, there was no significant variation in the number of attacks between the different morphs (SQE = 0.0004; R2 < 1%; P = 0.735; n = 10) (Fig. 3). DISCUSSION Our results suggest that the morphs of Phalotris lem- niscatus have different levels of predation and the preda- tion rate varies between areas. Our predictions regarding the importance of crypsis were corroborated only at the Coastal Site, where the predation rate was higher on the red-dark models that have higher contrast (less cryptic) in relation to the substrate of the region. Similar results were also observed for the morphs of the Mottled Rock Rattlesnake (Crotalus lepidus lepidus; Farallo and Forst- ner, 2012) and the sand hills mice (Linnen et al., 2013), both in the United States. Experiments with artificial models showed that differential crypsis and predation are the main forces of the spatial structuring of the western rattlesnake’s morphs (Farallo and Forstner, 2012). Simi- larly, Linnen et al. (2013) pointed out that the color of the soil offers differential camouflage opportunity to san- dhill mice against owls and other raptors and is determi- nant to the spatial structuring of their colored morphs. However, our data show that predation does not seem to be the main factor acting on the spatial struc- turing of the morphs of P. lemniscatus since the naturally more uncommon morph in the Lowland Site was the one that suffered less predation (pale-yellow). In other words, the low frequency of the pale-yellow morph in the Low- land Site population does not seem to be the result of predation. It is worth highlighting that all the sampled locali- ties have a similar predator composition. However, there is a possibility of existing regional variations in the abil- ity of these predators in detecting prey, which would have influenced the local number of attacks on each model type. Experiments showed that the capacity of preda- tors to detect the different morphs based on motionless prey is variable and depends on their ability to generate a specific searching image according to the form, size and color of the prey (e.g., Brodie, 1993; Olsson, 1993; Got- mark, 1994). It is reasonable to imagine that the search image established by a predator is compatible with a certain type of prey that has a higher probability of being found. Thus, the naturally rare morphs in each locality may not be part of the searching image of local predators (Dukas, 1998). In this case, they might not be easily detectable, even if their color shows more contrast with the background. Therefore, their predation rate would remain relatively low, even if their population was experimentally increased with the introduction of artificial models (Wennersten and Forsman, 2009; Karpestam et al., 2014). In addition, animals that attack potentially dangerous organisms (e.g., snakes) commonly reduce their exploratory behavior toward new and different prey morphs (Greenberg and Mettke-Hofmann, 2001), thus exhibiting a neophobic behavior (avoiding a new environmental aspect) (Greggor et al., 2016). Although possible, this hypothesis would be Fig. 3. Mean predation rate (events per hour) on the different morphs (red-dark and pale yellow-brown) in the three areas (High- land, Lowland and Coastal). 61Polymorphism and predation risk in Phalotris lemniscatus applicable to the lowland and highland sites, but not to the coastal site, where the less common and less cryptical models were the most preyed ones. Our results point toward the possibility that other factors besides crypsis interfere on the predation rate. Among those, we can mention the mimetic aposemat- ic potential of the red morph since their bright colors are associated with poisonous or nonpalatable animals (Cuthill et al., 2005; Tarvin et al., 2017). The establish- ment of a parallel between our data and such studies seems convenient due to the slightly reddish pattern of one of the morphs of P. lemniscatus. Yet, the effective- ness of the aposematism based on coral-like coloration is questionable regarding canids (Tozetti et al., 2004) and birds (Smith, 1969). Besides the passive strategies such as crypsis and immobility (Venesky and Anthony, 2007), snakes show active defense strategies or behavioral dis- plays such as escape (Forsman and Appelqvist, 1998; Creer, 2005; Allen et al, 2013). Additionally, P. lemnisca- tus has the antipredatory behavior called “erratic move- ments” (Tozetti et al., 2009), which would reduce the predation effectiveness after being detected by a predator (Forsman and Appelqvist, 1998). These behaviors may act in combination with the crypsis for the maintenance of each morph in each population. Our study failed to obtain answers to the proposed questions. One of the reasons might be that the frequen- cy of different morphs in each population may be related to other environmental factors such as thermoregulation (Trullas et al., 2007). 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Soc. Lond. B Bio. 276: 2187-2194. Acta Herpetologica Vol. 14, n. 1 - June 2019 Firenze University Press Uzungwa Scarp Nature Forest Reserve: a unique hotspot for reptiles in Tanzania John Valentine Lyakurwa1,2,*, Kim Monroe Howell2, Linus Kasian Munishi1, Anna Christina Treydte1,3 Experience of predacious cues and accessibility to refuge minimize mortality of Hylarana temporalis tadpoles Santosh Mogali*, Bhagyashri Shanbhag, Srinivas Saidapur Tonal calls as a bioacoustic novelty in two Atlantic Forest species of Physalaemus (Anura: Leptodactylidae) Thiago R. de Carvalho1,*, Célio F.B. 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