Anurans constitute essential components of the trophic system, since they are prey for a plethora of invertebrates and vertebrates (for a review see Toledo, 2005; Toledo et al., 2007). Among vertebrates, snakes stand out as the main predators of anurans (Toledo et al., 2007), but despite that, many aspects of this interaction remain to be explored. The considerable difficulty in observing this predator-prey interaction in situ represents a major obstacle to a better comprehension of this predator-prey dynamics (Fitch, 1987; Pombal Jr., 2007; Costa and Trevelin, 2020), being that most of the records of anuran ingestion by snakes come from stomach content analysis of museum specimens (Pombal Jr., 2007).

Anurans have developed several types of antipredator mechanisms (Toledo and Haddad, 2009a, b; Toledo et al., 2011, 2015). Among these, we highlight here the distress calls, which are defensive vocalisations widespread among anuran species, which can act against different groups of predators (Forti et al., 2018). These calls are emitted by juvenile and adult specimens (usually with open mouth) when subjugated by a potential predator, aiming to startle it and thus prevent an eventual predation (Toledo and Haddad, 2009a; Toledo et al., 2015; Köhler et al., 2017). Besides attempting to repel the predator, distress calls

may also alert nearby conspecifics about a potential predation risk (i.e. may function as a risk cue) (Forti et al., 2017a).

Leptodactylus macrosternum Miranda-Ribeiro, 1926 is a medium to large-sized frog (snout-vent length of males = 48.7–98.9 mm) widely distributed in the South American open diagonal, extending to many areas of the Atlantic Forest and throughout Amazonia, and also occurring in the Caribbean islands Trinidad and Tobago (Magalhães et al., 2020). There are predation records on this species by birds (Prado, 2003; Andrade et al., 2013; Aoki and Landgref-Filho, 2013), water bug nymph (Pereira et al., 2011), neotropical otter (Ferreira et al., 2017), snakes (Prado, 2003; Dorado-Rodrigues et al., 2012; Thaler et al., 2018), other frog species and also conspecifics (Sousa et al., 2016). Its distress call has been previously reported by Padial et al. (2006) (from central Bolivia), Dorado-Rodrigues et al. (2012) (from western Brazil) and Forti et al. (2017b) (from northern Brazil).

Lygophis lineatus (Linnaeus, 1758) is a slender, medium-sized (maximum total length of males = 635 mm; Michaud and Dixon, 1987) dipsadid snake broadly distributed in the northern portion of South America (Michaud and Dixon, 1987; Costa and Bérnils, 2018; Nogueira et al., 2019). Its diet is composed of anurans (Beebe, 1946; Michaud and Nixon, 1989; Escalona, 2012; Angarita-Sierra et al., 2013; Medina-Rangel and Cárdenas-Árevalo, 2015; Rojas-Murcia et al., 2015), geckos (Angarita-Sierra et al., 2013), insects (Freiberg, 1982), cricetid rodent (Michaud and Dixon, 1989), and there is also a report of cannibalism (Escalona, 2012).

Herein, to the best of our knowledge, we describe for the first time a predation event of a juvenile Leptodactylus macrosternum by a Lygophis lineatus. We also report the distress calls emitted by the frog during the subjugation by the snake, and highlight parameter variations in relation to the reported in literature for this species.

Herpetology Notes, volume 14: 949-953 (2021) (published online on 29 June 2021)

Leptodactylus macrosternum Miranda-Ribeiro, 1926 (Anura: Leptodactylidae) preyed upon by Lygophis lineatus (Linnaeus,

1758) (Serpentes: Dipsadidae), with notes on its distress call

André G. Lopes1,2,*, Jackson C. Sousa3, Rodrigo Tavares-Pinheiro3, and Carlos E. Costa-Campos3

1 Laboratório de Taxonomia e Sistemática de Anuros Neotropicais, Instituto de Ciências Exatas e Naturais do Pontal, Universidade Federal de Uberlândia, 38304-402 Ituiutaba, Minas Gerais, Brazil.

2 Departamento de Biologia/FFCLRP, Universidade de São Paulo, 14040-901 Ribeirão Preto, São Paulo, Brazil.

3 Laboratório de Herpetologia, Departamento de Ciências Biológicas e da Saúde, Universidade Federal do Amapá, 68903-419 Macapá, Amapá, Brazil.

* Corresponding author. E-mail: gomesandrebio@gmail.com

© 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0.

André G. Lopes et al.950

The predation event occurred on 5 February 2018, at ca. 13:00 h, in a flooded area amid human settlements in the municipality of Santana, Amapá State, Brazil (0.0365ºS, 51.1626ºW; datum WGS84). Specimens were not collected to avoid interfering and likely interrupting the interaction. Calls were recorded with a shotgun directional NTG1 RODE microphone coupled to a TASCAM DR-40 digital recorder, and analysed in Raven Pro v. 1.5 software (Center for Conservation Bioacoustics, 2014) with the following settings: window size = 1024 samples; 3dB filter bandwidth = 61.9 Hz; window type = Hann; overlap = 90% (locked); hop size = 2.31 ms; DFT size = 1024 samples; grid spacing = 43.1 Hz. Acoustic terminology and definitions followed Köhler et al. (2017). Dominant, maximum and minimum frequency values were respectively obtained through “Peak Frequency”, “Frequency 95%” and “Frequency 5%” functions. Sound figures were generated in R platform v.3.6.2 (R Core Team, 2019), using seewave v.2.1.6 (Sueur et al., 2008) and tuneR v.1.3.3 (Ligges et al., 2018) packages with the following settings: window = Hanning; overlap = 90%; FFT = 1024. The analysed sound file is deposited in the Herpetological Collection of the Universidade Federal do Amapá (CECC) (label: Leptodactylus_macrosternum_distress_call_5_02_2018) and in the Fonoteca Neotropical Jacques Vielliard (FNJV) (catalogue number: FNJV 50365).

After hearing the frog’s distress calls, we found a Lygophis lineatus (estimated total length of 500 mm) preying upon a juvenile Leptodactylus macrosternum

(estimated snout-vent length of 50 mm) amid the grassy vegetation of a wet ground. At first, the snake seized the frog with a bite on its right hind limb. The frog struggled to escape and emitted distress calls with its mouth wide open, but these attempts were unsuccessful. After subjugating the prey from the posterior portion of its body for ca. 15 minutes (Fig. 1A), the snake released it and then immediately made a rapid movement and struck the anterior portion of its body (Fig. 1B). After 25 minutes, the snake completely ingested (headfirst) the frog.

The distress calls emitted by the frog corresponded to two types of notes. The note type I (n = 13; Fig. 2A) sounds like a squeaky noise, and is composed of 15.69 ± 2.75 (10–19) well-defined frequency bands almost evenly spaced from each other, which presented different modulation patterns: ascending with some variation (n = 7; Fig. 2A); a slight descent at the onset followed by a gradual ascent, and a slight descent at the end (n = 3); gradual ascending, with a slight descent at the end (n = 2); gradual ascending with a slight descent at the end, followed by a slight ascent (n = 1). These notes have duration of 0.25 ± 0.02 s (0.20–0.28), minimum frequency at 1.85 ± 0.27 kHz (1.59–2.54), maximum frequency at 7.40 ± 0.60 kHz (6.59–8.61) and dominant frequency at 5.78 ± 1.18 kHz (2.50–7.11). The note type II (n = 7; Fig. 2B–D) sounds like a short cry, has lower amplitude than note type I, and presents a complex and variable spectral structure: 9.25 ± 2.5 (6–12) well-defined bands almost evenly spaced from each other, present only in the final portion of the note

Figure 1. Predation of a juvenile Leptodactylus macrosternum by a Lygophis lineatus. (A) Onset of the interaction, with the snake striking the posterior portion of the frog’s body. (B) Outcome of the interaction, with the snake starting to ingest (headfirst) the frog. Photographs by Jackson C. Sousa.

(n = 4; Fig. 2B); energy continuously distributed over the note bandwidth (n = 2; Fig. 2C); well-defined bands almost evenly spaced from each other, present only in the initial (11 bands) and final (6 bands) portions of the note (n = 1; Fig. 2D). These notes have duration of 0.18 ± 0.05 s (0.10–0.25), minimum frequency at 1.43 ± 0.12 kHz (1.25–1.55), maximum frequency at 7.10 ± 0.60 kHz (6.37–7.80) and dominant frequency at 2.94 ± 1.48 kHz (1.38–5.17).

The call parameters presented here are compatible with that previously reported for this species (Padial et al., 2006; Dorado-Rodrigues et al., 2012; Forti et al., 2017b). The spectral structure presented by the notes type I, consisting of well-defined modulated bands almost evenly spaced from each other, is a common feature among the distress calls of Leptodactylus species (e.g., Padial et al., 2006; Toledo and Haddad, 2009b). In contrast, notes type II presented a

different and variable spectral structure compared to the notes type I (see Fig. 2) and to the previous descriptions (Padial et al., 2006; Dorado-Rodrigues et al., 2012; Forti et al., 2017b). Nonetheless, high intraspecific variation in the distress call is common for Leptodactylus species (e.g., Hödl and Gollmann, 1986; Padial et al., 2006; Forti et al., 2017b). Some studies suggest that variations in anuran distress calls may be related to body size (Stănescu et al., 2018) and the degree of distress (Martins and Haddad, 1988; Padial et al., 2006). However, the actual influence of the distress level on the call properties still need to be better explored.

The natural history of Lygophis lineatus is still largely unknown, with only a few sporadic reports on its diet (Beebe, 1946; Freiberg, 1982; Michaud and Nixon, 1989; Escalona, 2012; Angarita-Sierra et al., 2013; Medina-Rangel and Cárdenas-Árevalo, 2015;

Leptodactylus macrosternum preyed upon by Lygophis lineatus 951

Figure 2. Audiospectrograms and respective oscillograms depicting the variation in the distress calls of Leptodactylus macrosternum. (A) Note type I; notice the several well-defined frequency bands almost evenly spaced from each other. (B–D) Note type II; notice the well-defined frequency bands, almost evenly spaced from each other, present only in certain portions of the notes in B and D, whereas the energy of the note in C is continuously distributed over the note bandwidth. All notes are from the same recording, and all figures were generated with FFT of 1024. Relative amplitude scale (40 dB) of spectrograms is represented by colors, being red the maximum amplitude.

Rojas-Murcia et al., 2015) and reproduction (Daza-R, 2005). Herein, we described in detail a predation event of a Leptodactylus macrosternum by this snake, thus adding this frog species as a new item to its diet. This record contributes to the knowledge on the diet of Ly. lineatus, and also provides important insights on its capacity and strategy to subjugate a prey such as a medium-sized frog. Future studies are still needed to fill the knowledge gaps in the natural history of Ly. lineatus.

The present study provides an important contribution to a better understanding of the predator-prey dynamics involving snakes and anurans, especially given the difficulty in obtaining complete records of such interactions in situ (Fitch, 1987; Pombal Jr., 2007; Costa and Trevelin, 2020). Predation records, although usually scarce, are essential to achieve a thorough comprehension of the ecological aspects related to this interaction. We also provided data on the distress call of Leptodactylus macrosternum, reporting new variations in call parameters in relation to the previously reported for this species. This type of data may be useful, for instance, for future evolutionary, behavioural, and other applied studies in bioacoustics.

Acknowledgements. We thank Dr. Lucas R. Forti for the pre-peer review and helpful suggestions on the original version of this study, Dr. Ariovaldo A. Giaretta for a helpful comment, and an anonymous reviewer for making valuable suggestions. Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) currently provides a master’s fellowship to AGL (process #130380/2020-2). PIBIC/CNPq/UNIFAP program for the Scientific Initiation scholarship to JCS. The Cornell Lab of Ornithology (Center for Conservation Bioacoustics) provided a free license of Raven Pro 1.5 software to AGL.

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Accepted by Anyelet Valencia-Aguilar