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Antipredator Mechanisms of Leptodactylus Syphax Bokermann, 1969 (Anura: Leptodactylidae)

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Antipredator Mechanisms of Leptodactylus Syphax Bokermann, 1969 (Anura: Leptodactylidae) Herpetology Notes, volume 14: 257-261 (2021) (published online on 01 February 2021) Antipredator mechanisms of Leptodactylus syphax Bokermann, 1969 (Anura: Leptodactylidae) Felipe P. Sena1, Rayone A. Silva1, Antonia Joyce S. Santos1, Claylton A. Costa1,2, Sâmia Caroline M. Araújo1,3, and Etielle B. Andrade1,* Amphibians are important components of the Sá et al., 2014; Frost, 2021). food chain acting as prey for both vertebrates and Leptodactylus syphax Bokermann, 1969 is a medium- invertebrates (Toledo, 2005; Toledo et al., 2007). This sized species, widely distributed in the central and prey-predator relationship leads species make use of northeastern of Brazil, southern Paraguay, and eastern defensive strategies to deter, avoid or confuse predators, Bolivia (Frost, 2021). It was initially included in the L. using morphological, physiological, and behavioural pentadactylus group by Heyer (1969), and posteriorly responses selected by natural selection (Duellman and was placed in the L. fuscus group based on molecular and Trueb, 1994; Wells, 2007). Anurans developed several bioacoustic characters (de Sá et al., 2014). Individuals anti-predatory mechanisms, placed in three phases of this species have smooth skin with tubers on the back (avoid detection, prevent attacks, and counterattack), limited by the sacral and post-sacral regions, and males overall involving aposematic colouration, defensive develop spines on the hands and chest and hypertrophied posture, and toxin production (Toledo and Jared, 1995; arms to hold the females during the reproductive period Toledo and Haddad, 2009; Toledo et al., 2011; Ferreira (Heyer et al., 2010; de Sá et al., 2014). et al., 2019). Despite increasing in recent years, studies on the Leptodactylidae currently comprises 231 species anurans defensive behaviour are still scarce (Toledo et of large, medium, and small-sized frogs distributed al., 2011). Recently, Ferreira et al. (2019) published a throughout the Americas, from the southern United global database with a classification system for anuran States to the Patagonia region (Chile and Argentina) anti-predatory mechanisms, proposing three phases, (Frost, 2021). The 82 species belonging to the genus 12 mechanisms and 28 variations. Several defensive Leptodactylus Fitzinger, 1826, are distributed in behaviours have been reported for Leptodactylus four groups based on morphological and molecular (Ferreira et al., 2019), and among species of the L. characters: L. fuscus, L. latrans, L. melanonotus, and L. fuscus group the antipredator mechanisms have been pentadactylus groups, except three species that were not described only for eleven species (see Table 1). Herein, included in any group (L. hylodes, L. lauramiriamae and we present and describe some antipredator mechanism L. ochraceus) (de Sá et al., 2014; Frost, 2021). Among sensu Ferreira et al. (2019) of L. syphax registered them, L. fuscus group is the largest with 31 species (de in Caatinga-Cerrado transition areas in northeastern Brazil, and we also update the list presented in Ferreira et al. (2019) for the L. fuscus group. During fieldwork on 2 March 2019, we observed a 1 Grupo de Pesquisa em Biodiversidade e Biotecnologia do male of L. syphax vocalising under a rock formation Centro-Norte Piauiense, Instituto Federal de Educação, in a cerrado rupestre area, at the Sete Cidades National Ciência e Tecnologia do Piauí, Campus Pedro II, Pedro II, Park (4.0994°S, 41.7092°W; WGS 84), a conservation Piauí 64255-000, Brazil. unit located in transition area between the Cerrado 2 Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, Ilhéus, Bahia 45662- and Caatinga biomes in the state of Piauí, northeastern 900, Brazil. Brazil. As we approach, the individual interrupted the 3 Universidade Estadual do Maranhão - UEMA, Centro de call and hid in cracks under the rocks, and after a few Estudos Superiores de Caxias, Caxias, Maranhão 65604-380, attempts we collected him. The collected specimen Brazil. was deposited in the Biological Collection of Instituto * Corresponding author. E-mail: [email protected] Federal de Educação, Ciência e Tecnologia do Piauí, © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. Campus Pedro II (CBPII-060). 258 Felipe P. Sena et al. Table 1. Antipredator Table 1. Antipredator mechanisms mechanisms recorded inrecorded species in of species the Leptodactylus of the Leptodactylus fuscus fuscusgroup, group, adapted adapted from from Ferreira Ferreira et al. et (2019). al. (2019). Species Antipredator mechanisms Reference L. cunicularius Sazima and Background matching Toledo et al. (2010) Bokermann, 1978 L. didymus Heyer et al., 1996 Background matching, jump away, cloacal Ferreira et al. (2019) discharge L. fragilis (Brocchi, 1877) Background matching, body inflation, mouth Bernal (2012) gape, distress call L. fuscus (Schneider, 1799) Background matching, immobility, interrupt Hödl and Gollmann (1986); Toledo and calling, death feigning, hide, jump away, Haddad (2009); Toledo et al. (2010, 2011); cloacal discharge, distress call Haddad et al. (2013); Ferreira et al. (2019) L. laticeps Boulenger, 1918 Disruptive, body inflation, poisonous Abalos (1967); Ferreira et al. (2019) L. marambaiae Izecksohn, 1976 Background matching, immobility, Siqueira et al. (2006) contraction, death feigning, jump away L. mystaceus (Spix, 1824) Background matching, cloacal discharge, Toledo and Haddad (2009); Toledo et al. distress call (2011); Haddad et al. (2013) L. mystacinus (Burmeister, 1861) Background matching, body inflation, rear Carvalho-Jr (2005); Toledo and Haddad elevation, death feigning, cloacal discharge, (2009); Toledo et al. (2010, 2011); Haddad slippery, poisonous, distress call et al. (2013); Ferreira et al. (2019) L. notoaktites Heyer, 1978 Background matching, hidden, death feigning, Haddad et al. (2013); Ferreira et al. (2019) L. plaumanni Ahl, 1936 Background matching, body inflation, death Toledo et al. (2010); Haddad et al. (2013) feigning L. syphax Bokermann, 1969 Interrupt calling, hide, immobility, body Present study inflation, body elevation, gland exposure, secretion L. troglodytes Lutz, 1926 Background matching, mouth gape, kick, Toledo and Haddad (2009); Haddad et al. distress call (2013); Santos-Silva et al. (2014); Sales et al. (2015) The next day, when photographed, the specimen of elevation of body, in which only the rear limbs were L. syphax showed some antipredator mechanisms in raised, and full elevation of body, in which were raised response to our approach. First, the male remained all limbs (Toledo et al., 2011; Ferreira et al., 2019). motionless with his body close to the ground (Fig. 1A), Gland exposure behaviour is observed mainly among inflating the body as we approach (Fig. 1B), and raising members of Bufonidae (Ferreira et al., 2019), so this is the body to show the posterior thigh region (Fig. C) the first record for the genus Leptodactylus. while keeping the head facing downwards with open Body elevation behaviour is used by 21 anuran families eyes. When perceiving a closer approach, the male also and is associated with toxic species (Toledo et al., 2011; raised the forelimbs, remaining in this position for a few Ferreira et al., 2019). Within the Leptodactylidae, seconds (Fig. 1D, E). We also noticed the release of skin this behaviour is used by species of the Leiuperinae secretion (Fig. E), mainly in the inguinal and posterior and Leptodactylinae subfamilies (Toledo et al., 2011; thigh region, and gland exposure posture, in which the Ferreira et al., 2019), being observed in seven species male partially sloped the body or turned the posterior of Leptodactylus: L. insularum Barbour, 1906 (Franzen, part of the body towards the aggressor (team member) 2017), L. labyrinthicus (Spix, 1824) (Toledo et al., 2005, when being stimulated (Fig. 1F). The body elevation 2011), L. laticeps Boulenger, 1918 (Heyer and Scott Jr., posture (or “body raising” sensu Toledo et al., 2011) 2006), L. pentadactylus (Laurenti, 1768) (Villa, 1969), has been described as an attack prevention mechanism, L. stenodema Jiménez de la Espada, 1875 (Lima1 et al., in which it consists of elevating the body keeping the 2005), L. syphax (present study), and L. vastus Lutz, 1930 members vertically stretched, allowing the exposure of (Castro et al., 2017). However, only the species of the L. aposematic colours or not. This behaviour is more used pentadactylus group (L. labyrinthicus, L. pentadactylus, by toxic species that have macroglands in the posterior and L. vastus) use aposematism for warning (Toledo et region of the body (Toledo et al., 2011; Ferreira et al., al., 2011). Brodie et al. (1998) suggest that the presence 2019). The individual sequentially used the partial of the aposematic colouration is a characteristic derived Antipredator mechanisms of Leptodactylus syphax 259 Figure 1. Antipredator mechanisms of Leptodactylus syphax (CBPII–060, snout-vent length: 78.02 mm); (A) immobility, (B) body inflation, (C) partial and (D) total body elevation, (E) secretion (black arrows) and (F) gland exposure (white arrows). Photos by Etielle Andrade. from body elevation behaviour as a form of warning, Production of cutaneous secretions is a as observed in species of the genus Uperoleia Gray, symplesiomorphic characteristic among anurans and 1841. Individuals of L. syphax do not have aposematic is associated with the integument moist and defence colouration, however, we observed a male raising his against parasites (mucous
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