How Successful Are Snakes?
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Herpetology Notes, volume 13: 649-660 (2020) (published online on 05 August 2020) Unsuccessful predation attempts by snakes on anuran amphibians: How successful are snakes? William P. Costa1,* and César C. Trevelin2 Abstract. Snakes and anurans are commonly involved in predator-prey interactions. The large number of records of predation events involving snakes and anurans suggests that snakes are frequently successful in their attempts to prey on these amphibians. However, two aspects of the data may lead to overestimates of the efficiency of the predator in these cases. One factor is that the principal source of the data on snake diets is the analysis of the stomach contents of snake specimens deposited in museums. The second is the paucity of data on the actual interaction between the predator and its prey, and the frequency with which the anurans are either able to escape the predator or are abandoned by snakes. Given this general lack of data on unsuccessful predator-prey interactions between snakes and anurans, the present study describes four unsuccessful predation attempts and discusses the potential consequences for both the predator and prey. These events involved three snakes of the family Dipsadidae and one of the family Viperidae, which are all venomous, and three anuran species of the family Leptadactylidae. The events were recorded at four localities in the Brazilian states of São Paulo, Minas Gerais, and Goiás between 2016 and 2018. In one of the four cases (Event 1), the anuran was able to escape, while in the other three events, the prey were abandoned by the snake. In one case (Event 3), the anuran was dead, while in the other two cases (Events 2 and 4), the animals were left with reduced mobility, and were thus more vulnerable to other predators. In two of these events (1 and 3), the predator attacked the anuran by grasping its posterior members, while in event 2, the strike was to the throat of the anuran, and in event 4, the anuran was grasped by its right flank. In the only case in which the prey was able to escape unharmed, the combination of the size of the animal and its resistance to the attack of the predator appear to have been decisive. In the three cases in which the anuran was abandoned by the predator, the initial point of contact may have determined the effectiveness of the attack, given the anatomical resistance exerted by the prey, even when it remains immobile. The fact that all the snakes included in the present study are venomous did not ensure the success of the predation attempts, which would have resulted in the waste of this resource (venom). Despite the difficulty of analysing unsuccessful predation attempts (and their consequences for both predator and prey) systematically, studies of this kind are necessary to advance the understanding of this type of interaction and, ultimately, to evaluate more conclusively the ecological dynamics of the relationship between snakes and anurans. Keywords. snakes, anurans, ecology interaction, predation attempts, predator-prey Introduction 1993; Martins and Oliveira, 1998; Wells, 2007; Toledo et al., 2007; Bernarde and Abe, 2010; Vargas-Salinas Snakes and anurans are important components of and Aponte-Gutierrez, 2013). The large number of terrestrial ecological communities, and are often records of this type of interaction indicate that anurans involved in predator-prey interactions, normally as are an important component of the diets of a number of predator and prey, respectively (Strüssmann and Sazima, different snake species (e.g. Martins et al., 1993; Toledo et al., 2007; Moya and Maffei, 2012; Bovo and Sueiro, 2012; Forti and Bertoluci, 2012; Falkenberg et al., 2013; Santos-Silva et al., 2014; Passos et al., 2017; Muscat and Moroti, 2018; Thaler et al., 2018). In rare cases, 1 Departamento de Bioestatística, Biologia Vegetal, however, large anurans are also known to have subdued Parasitologia e Zoologia, Instituto de Biociências, and ingested snakes, although these events appear to Universidade Estadual “Júlio de Mesquita Filho” (UNESP), be highly opportunistic (Branch, 1976; Silva, Costa campus Botucatu, SP, Brasil. and Feio, 2007; Camargo Filho et al., 2008; Fonseca 2 Departamento de Economia, Sociologia e Tecnologia, et al., 2012). It is worth mentioning that, one of the Faculdade de Ciências Agronômicas, Universidade Estadual “Júlio de Mesquita Filho” (UNESP), campus Botucatu, SP, advantages of exploiting anurans as a food is their lack Brasil. of anatomical structures that are difficult to digest, such * Corresponding author. E-mail: pinho_willi@hotmail.com as fur, claws or scales, which is further reinforced by 650 William P. Costa & César C. Trevelin the fact that many species form large aggregations of Paulo, and União de Minas (-19.2825°S, -50.4224°O), individuals in the vicinity of bodies of water during the in the state of Minas Gerais. The sites are located within breeding season (Duellman and Trueb, 1986; Wells, an area of transition between the Cerrado savannah of 2007). central Brazil and the Atlantic Forest of eastern Brazil, The typically discreet nature of predation events in and were originally covered by a mosaic of Cerrado the wild contributes to the scant and sporadic records of sensu stricto savanna vegetation and semi-deciduous this type of behaviour, which hamper a more systematic seasonal forest (Ab’Saber, 2003). All four localities are analysis of the phenomenon. In fact, the vast majority also within an area dominated by a tropical savannah of reported cases are derived from the analysis of the climate (Aw in the Köppen classification), with a dry stomach contents of specimens deposited in scientific season that coincides with the austral winter and rains collections, which represent the end result of successful concentrated during the austral summer (Rolim et al., predation events (Pombal, 2007). The efficiency of 2007; Cardoso et al., 2015; Reboita et al., 2015). this type of predatory behaviour in snakes nevertheless The events at Acreúna and Ouroeste were recorded at remain unclear, given the scant records of unsuccessful the margins of permanent lakes, while the record from attacks (Rocha-Lima et al., 2018). União de Minas was obtained at a temporary pond, and Unsuccessful predation events may result from errors the event at Palmeiras de Goiás took place in a fragment in the evaluation of the relative size of the prey, which of forest (Figures 1a, 2a, 3a, 4a). The encounters with is more typical of young snakes (Sazima and Martins, the animals occurred during nocturnal surveys of the 1990), in addition to the intrinsic predator-defence respective study sites. Once an attempted predation mechanisms available to the anurans (see Ferreira et al., was observed, the subsequent sequence of events was 2019). Unsuccessful attempts may result in energetic recorded from a distance of approximately two meters, attrition in both the predator and the prey which, in with a minimum of artificial illumination (red lights), in extreme cases, may even result in the deaths of both an attempt to minimise possible interference from the animals (Bernal and Palma, 2011; Cavalcanti et al., 2012; presence of the observers (Vargas-Salinas and Aponte- Caramaschi and Niemeyer, 2012; Fong et al., 2013). In Gutierrez, 2013; Mario-da-Rosa et al., 2020). some cases, the prey is too large to be swallowed by the predator, which may even be suffocated in the attempt Results and Discussion (e.g. Caramaschi and Niemeyer, 2012; Nogueira et al., The observed predation attempts involved four 2013; Filho et al., 2017), or it may escape, but eventually species of snake, including three representatives of the die from exhaustion or the toxic effects of the venom family Dipsadidae, Helicops modestus Günther, 1861, (Sazima and Martins, 1990; Rocha-Lima et al., 2018). Thamnodynastes strigatus (Günther, 1858), Xenopholis The systematic evaluation of these unsuccessful undulatus (Jensen, 1900), and one member of the family predation attempts, and their relevance to both the Viperidae, Bothrops moojeni Hoge, 1966. The potential predator and the prey, is a complex task, although it prey was all frogs of the family Leptodactilydae, that may provide fundamental insights into the dynamics of is, Leptodactylus chaquensis Cei, 1950, Leptodactylus the ecological interactions between snakes and anurans. labyrinthicus (Spix, 1824), and Physalaemus centralis In order to broaden the existing perspective on this Bokermann, 1962. All the snake species are known to important type of ecological interaction, the present include anurans in their diets (see Nogueira et al., 2003; study describes four unsuccessful predation attempts França et al., 2008; Scartozzoni, 2009), although none by snakes on anurans, with the aim of evaluating the of the anurans recorded as prey in the present study have eventual consequences for both predator and prey, from been recorded previously in the diets of any of the four the moment that the predator loses interest in the prey or snake species. it manages to escape. Helicops modestus vs. Leptodactylus chaquensis in Material and Methods Acreúna, Goiás (Event 01): this event occurred at 18:39 The events described in the present study were recorded h on 05-29-2016 near the internal margins of a lake (Fig. at four localities in central and southeastern Brazil– 1a) and it was perceived due to the distress vocalisations Acreúna (-17.3786°S, -17.3786°O) and Palmeiras de emitted by the anuran. Initially, an individual of the Goiás (-16.8758°S, -49.9702°O) in the state of Goiás, species Leptodactylus chaquensis was observed with Ouroeste (-20.0077°S, -50.4282°O), in the state of São its body slightly stretched out, partially submerged in Unsuccessful predation attempts by snakes on anuran amphibians 651 the water, with its right leg in this substrate and the left aquatic environments (Scartozzoni, 2005). The snakes leg hidden by the mud and vegetation (Fig.