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Respond Behaviourally to Conspecific Male Scent Herpetozoa 34: 115–120 (2021) DOI 10.3897/herpetozoa.34.e62007 Females of the four-eyed frog, Pleurodema thaul (Anura, Leptodactylidae), respond behaviourally to conspecific male scent Valentina Rojas1, Antonieta Labra2,3, José Luis Valdés4,5, Nelson A. Velásquez1 1 Laboratorio de Comunicación Animal, Facultad de Ciencias Básicas, Universidad Católica del Maule. San Miguel 3605, 3480112, Talca, Chile 2 Centre for Ecological and Evolutionary Synthesis, University of Oslo, P.O. Box 1066, Blinder GNO-0316, Oslo, Norway 3 NGO Vida Nativa, Santiago, Chile 4 Departamento de Neurociencia, Facultad de Medicina, Universidad de Chile, Independencia 1027, 8380453, Santiago, Chile 5 Biomedical Neuroscience Institute (BNI), Facultad de Medicina, Universidad de Chile, Independencia 1027, 8380453, Santiago, Chile http://zoobank.org/DBF813DC-8CB9-4BC8-B98A-E5839353FA81 Corresponding author: Valentina Rojas ([email protected]) Academic editor: Eva Ringler ♦ Received 14 December 2020 ♦ Accepted 27 April 2021 ♦ Published 27 May 2021 Abstract Among amphibians, conspecific chemical communication has been widely studied in Caudata. Adult anurans, by contrast, have re- ceived less attention. Recently, it was shown that chemical scents are also relevant for adult anuran intraspecific communication. In this context, we evaluate whether females of the four-eyed frog (Pleurodema thaul) respond to conspecific male scents. We carried out a double choice experiment in a Y-maze. Females were repeatedly presented with the scents of several males versus distilled water. To extract the scent from males, we acoustically stimulated males and then used the water from their aquaria for the experi- ments. Our data suggest that females are capable of responding behaviourally to male scents, since they spent longer periods in the zones with male scent, rather than in zones with water. We propose that under natural breeding conditions, females of P. thaul may use either their chemical sense or chemical cues to facilitate their encounters with males. Key Words anuran communication, chemical communication, female choice, male scent Introduction been studied across ontogenetic stages and in different social situations across several taxa (Gorman and Mills Animal communication is a process by which information 1984; Roberts et al. 2003; Wyatt 2014). Particularly in is transferred from a sender to a receiver, provoking in amphibians, most knowledge regarding conspecific the receiver a behavioural or physiological reaction chemical communication has been developed for (Dusenbery 1992). This communication process is es- Caudata, where scents have a significant role in different sential for social interactions (e.g. agonistic interactions, aspects of their social life (Park and Sung 2006; Houck et courtship rituals), and can depend on different channels al. 2007, 2008). For instance, salamanders of the family (e.g. acoustic, visual, vibrational, chemical), which might Plethodontidae have been widely studied for the use of be utilised independently or in association (Partan 2004; chemical signals in their social interactions (Guillaume Bradbury and Vehrencamp 2011). 2000; Rollinson and Hackett 2015). It was observed that Chemical communication is one of the oldest systems males of Plethodon shermani produce a sexual pheromone of communication in the animal kingdom, and it has denominated Plethodon Receptivity Factor (PRF) that Copyright Valentina Rojas et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 116 Valentina Rojas et al.: Behavioral responses to chemical scents in anurans increases the female`s receptivity (Rollmann et al. 1999). in this species focuses on tadpoles using chemicals under In addition, courtship behaviour involving pheromone predation risk (Pueta et al. 2016; Pueta and Perotti 2016), delivery (Houck 2009), the genetic components for but the question of whether adults utilise scent recognition sex pheromone productions and their evolution across has not been studied yet. In this context, and considering amphibian groups, have been widely described (Watts the available information on sexual scents involved in et al. 2004). The genus Cynops, has received strong mate attraction in other anurans (Wabnitz et al. 1999), attention for their intersexual interactions mediated we aimed to determine whether female Pleurodema thaul by chemosignals (Toyoda et al. 2004). Kikuyama et al. responded behaviourally to male scents. (1995), discovered that males of the fire belly salamander (C. phyrrogaster) release a female-attracting pheromone (denominated Sodefrina) and males of C. ensicauda Methods release a peptide from their abdominal gland called Silefrin that attracted females (Yamamoto et al. 2000). Subjects The fire belly salamander and their Sodefrin pheromone have become a model for the study of sex pheromones in We collected a total of 13 individuals (3 males and 10 aquatic salamanders, resulting in the discovery of a multi- females) of Pleurodema thaul at Puente Negro (34°40'S, component pheromone system (Van Bocxlaer et al. 2016). 70°53'W) in central Chile, and transported them to the Anurans have been described as acoustically laboratory in Talca, Chile. All specimens were sepa- dependent; several studies have, however, by now rated by sex and housed individually in glass aquaria demonstrated that scents can mediate conspecific (15 × 20 × 30 cm) with water and gravel. The individuals recognition (Kiseleva 1996; Carlson et al. 2015), provide were maintained in an animal room with an inverted information about kinship identity (Waldman 1985) and photoperiod (12Light: 12Dark), with a temperature of play a role in predator-prey interactions in the larval 21 ± 1 °C (mean ± SD), and were fed tenebrionid larvae stages of anurans (Pearl et al. 2003; Chivers and Ferrari once a week, according to the described care instruction 2013; Troyer and Turner 2015). Even learning of chemical for laboratory animals (National Research Council 2010). cues at embryonic stages has been described (Hepper and After finishing all experiments and re-adapting the frogs Waldman 1992). Additionally, chemical signals are also to their normal photoperiod, we returned all of them in a important in different social contexts in adult anurans healthy condition to their geo-referenced collecting point. (Kam 2002; Still et al. 2019). For instance, Leiopelma hamiltoni releases a chemical compound in the faeces that provides information to conspecific individuals about the Conspecific male scents solution size of the sender (Lee and Waldman 2002). In courtship situations, it has been observed that males of Litoria To obtain male scent during their reproductive state (see splendida release a sexual pheromone called Splendipherin Chu and Wilczynski 2001), we acoustically stimulated that elicits changes in postural and permanence times in males as follows: after one week of acclimation, each females (Wabnitz 1999). A recent study has contributed male P. thaul was isolated for 10 days in an aquarium knowledge about anuran chemical communication (20 × 8 × 15 cm), containing 50 ml of distilled water through the study of compound secretions (Brunetti et al. and previously washed gravel. To simulate the acoustic 2019) and also several investigations provided evidence conditions experienced by males at night during the for their role in social interactions (Pearl et al. 2000; breeding season, we placed all 3 males in their individual Asay et al. 2005; King et al. 2005). For example, Byrne aquaria, into a semi-anechoic chamber (with the walls and Keogh (2007) showed that the Australian terrestrial and ceiling covered with a 25 cm-high foam wedge) Pseudophryne bibronii toadlets use scents to identify and to avoid sound reverberation and external noises. The locate potential mates. In addition, the frog Lithobates male advertisement call was continuously broadcasted pipiens shows differences in their behavioural responses for one hour in complete darkness. We repeated this for to adult male and female chemical cues (Graham et al. 10 consecutive days, according to Chu and Wilczynski 2020). Compared with other amphibian groups, however, (2001). For the playbacks, we used a personal computer more investigation describing chemical communication (Macbook Unibody, Apple Inc. Cupertino, CA, USA), in adult anurans is still needed. controlling the amplitude with a programmable Adult males of the four-eyed frog, Pleurodema thaul, attenuator (PA5, Tucker-Davis Technologies). emit advertisement calls during the reproductive season, The calls were amplified (NAD C326BEE, NAD inflating their vocal sacs while floating on the surface Electronics, Pickering, Canada), and broadcasted via of slow-flowing streams or pools (Penna and Veloso two loudspeakers (Behringer 1C, Behringer, Willich, 1990; Velásquez et al. 2014). Research has shown that Germany) with an intensity of 70 dB SPL RMS (Penna females do not exhibit a preference for males based on and Solís 1998; Penna et al. 2008) measured inside each their calls (Velásquez et al. 2015). Alternatively, their aquarium with a sound level meter (Bruel and Kjaer preference may be guided by male scent. Currently, the 2238; Bruel & Kjaer Instruments, Inc., MA, USA). The only information available on chemosensory recognition aquaria were placed on an anti-vibration table and
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