Repertoire of Antipredator Displays in Siphlophis Longicaudatus (Serpentes: Dipsadidae)
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Herpetology Notes, volume 11: 157-160 (2018) (published online on 10 February 2018) Repertoire of antipredator displays in Siphlophis longicaudatus (Serpentes: Dipsadidae) Valquiria de Oliveira Pereira1,*, Frederico de Alcântara Menezes2, Weverton dos Santos Azevedo1 and Arthur Diesel Abegg1 The mechanisms of interaction between prey and Alencar et al., 2009). S. longicaudatus occurs in forested predator are complex and very diverse in snakes, areas (Gaiarsa et al., 2013), in the Atlantic Forest constituting important elements for a deeper domain, in both the southern and southeastern regions understanding of their natural history (Greene, 1988; of Brazil (Alencar et al., 2009; Bérnils, 2009; Costa et Maia-Carneiro et al., 2012; Martins, 1996; Martins et al., 2010), in the following ecoregions (sensu Olson al., 2008). In general, snakes use primary defences, et al., 2001): Serra do Mar Coastal Forests, Araucaria such as camouflage, to avoid direct confrontation Moist Forests, Coastal Bahia Forests and Interior Bahia with predators (Greene, 1988). However, when direct Forests (Thomassen et al., 2015). confrontation does occur, snakes will then depend Few data in the literature are available on the general on secondary defences to survive (Silva, 2016). The biology of S. longicaudatus (Alencar et al., 2009), Dipsadidae Bonaparte, 1840 family (sensu Grazziotin including on defensive behaviours. Marques et al. et al., 2012) is widely distributed in the Neotropical (2004) cite four defensive behaviours for this species: region, encompassing a large number of species with erratic movements, striking, tail vibration and cloacal different evolutionary lineages and, consequently, the discharge. In this study, we report five other defence presence of very distinct defensive repertoires among behaviours for S. longicaudatus that were, until now, species (Marques et al., 2004; Sawaya, 2010). unknown, and compare the repertoire of this species with Knowledge on the natural history of Neotropical that of other Neotropical snakes. For this comparison, snakes has progressed markedly in the last decades the dataset from Tozetti et al. (2010) was used, which (Marques et al., 2004, Marques et al., 2005, Carreira comprises, in addition to S. longicaudatus, two other et al., 2005, Cacciali et al., 2016). However, little is species belonging to the same genus, Siphlophis pulcher known about the defensive repertoires of many species, (Raddi, 1820) and Siphlophis compressus (Daudin, especially those considered rare or difficult to encounter 1803) whose defensive repertoires are described in (Menezes et al., 2015, Menezes et al., 2017). Marques et al. (2004) and Fraga et al. (2013). Thus, we Siphlophis longicaudatus (Andersson, 1901) is a elaborated the similarity analysis with a binary matrix medium-sized snake that presents nocturnal activity of the presence/absence of 12 defence behaviours in 25 and semi-arboreal habits (Barbo, 2008; Marques et al., species. We conducted comparisons between taxa using 2004). It displays opistoglyph dentition and its diet is Jaccard’s similarity index and clustered the species composed, mainly, of lizards (Prudente et al., 1998; using the Pair Group Average Method (UPGMA). A cophenetic correlation coefficient was calculated to evaluate the representativity of the similarity matrix in the dendrogram where values ≥ 0.8 are considered adequate (Rohlf, 2000). This multivariate analysis was 1 Instituto Butantan, Laboratório Especial de Coleções elaborated using the vegan package of the R software (R Zoológicas. Avenida Vital Brasil, 1500, Butantã, 05503-900, Core Team 2016) (Oksanen et al., 2015). São Paulo, Estado de São Paulo, Brazil. 2 Universidade Federal de Viçosa, Departamento de Biologia On December 18, 2014 at 09:40 PM, in the municipality Animal. Avenida P.H. Rolfs, s/nº, Campus Universitário, CEP of Cotia (-23.5993S, -46.9190W), in the state of São 36571-000, Viçosa, Minas Gerais, Brazil. Paulo, Southeastern Brazil, a S. longicaudatus specimen * Corresponding author: [email protected] was found moving on the ground in a forested area. The 158 Valquiria de Oliveira Pereira et al. Figure 1. Siphlophis longicaudatus, found in the municipality of Cotia (São Paulo, Brazil), and its observed defensive behaviours: head elevation (A); triangulation of the head (B); S-shaped neck (C); hiding the head (D and E); body in a spherical conformation (F). snake was captured for identification and released the of the body (Fig. 1C); hiding the head under body turns next morning. When captured, the individual defended (Fig. 1D-E) and curling up, assuming a spherical body itself through erratic movements and cloacal discharge, conformation (Fig. 1F). according to Marques et al. (2004). During the release, Head triangulation was one of the most frequent on the morning of the following day, the snake presented behaviours observed in the study performed by Tozetti a series of defensive behaviours not reported in the et al. (2009) on Xenodon dorbignyi (Duméril, Bibron literature, as follows: elevation of the head and anterior and Duméril, 1854) associated with elevation of portion of the body (Fig. 1A); triangulation of the head the head and anterior portion of the body. A similar (Fig. 1B); formation of an “S” with the anterior region behaviour was observed for Erythrolamprus miliaris Repertoire of antipredator displays in Siphlophis longicaudatus 159 Figure 2. Dendrogram for the cluster analysis of defensive displays observed for some Brazilian dipsadid snakes. The cluster analysis was performed using “UPGMA” method after adding the new data on Siphlophis to the character matrix of Tozetti et al. (2009). (Linnaeus, 1758), in a study conducted by Menezes et contrast to species of Xenodon and Erythrolamprus al. (2015). The behaviours of raising and triangulating where defensive behaviours are not phylogenetically the head and forming an “S” with the neck possibly informative, the clustering of Siphlophis species in our make the animal appear larger and more intimidating to dendrogram suggests that defensive behaviours might visually oriented predators, such as birds and mammals be highly conserved in this genus, even independent of (Tozetti et al., 2009). The presence of these behaviours the colour pattern of the species, since S. compressus in S. longicaudatus is surprising, since this species is quite conspicuous, while S. longicaudatus displays displays mainly nocturnal activity (thus, being less a more cryptic colouring. However, this issue is still likely to encounter visually oriented animals), unlike under-explored for snakes in the Neotropical region, X. dorbignyi and E. miliaris, which are predominantly and further studies with a greater range of species diurnal (Marques et al., 2004; Tozetti et al., 2009). and their respective defensive repertoires could better However, the fact that the S. longicaudatus specimen address this issue. presented the behaviours during the day may have influenced the different defensive behaviours exhibited, Acknowledgements. The authors would like to thank Alexandro like in the case of Simophis rhinostoma (Schlegel, 1837) Marques Tozetti, for information on the defensive repertoire of that alters its defensive behaviour under different light the species used in the similarity analysis and to anonymous reviewers, who have substantially improved this work with their conditions (Marques, 2000). comments and suggestions. The UPGMA dendrogram (Fig. 2) shows a cophenetic coefficient of 0.893 indicative of a good References representation of the similarity matrix. Inspection of Alencar, L.R.V., Righi, A.F., Nascimento, L.B., Morato, S.A.A. the dendrogram show similar results as in Tozetti et (2009): Siphlophis longicaudatus (Brazilian Spotted Night al. (2009), with the formation of two major groupings Snake): Habitat. Herpetological Bulletin (108). (Fig. 2): Group 1 - contains most Lygophis Fitzinger, Barbo, F.E. (2008): Composição, História natural, Diversidade 1843 and Erythrolamprus Wagler, 1830 species, e Distribuição das serpentes no município de São Paulo, SP. including Siphlophis Fitzinger, 1843 species; and Dissertação de Mestrado. Universidade de São Paulo. 90 pp. group 2 - composed mostly of species belonging to the Bérnils, R.S. (2009): Composição e Padrões de Distribuição de Caenophidia (Squamata, Serpentes) das Serras Atlânticas e Xenodon Boie, 1826 genus. Species belonging to the Planaltos do Sudeste da América do Sul. Tese de Doutorado. Siphlophis genus, added in this study, form a smaller Universidade Federal do Rio de Janeiro. 808 pp. group, within group 1, with S. longicaudatus and S. Cacciali, P., Scott, N.J., Ortiz, A.L.A., Fitzgerald, L.A., Smith, P. compressus sharing very similar defence tactics. In (2016): The Reptiles of Paraguay: Literature, Distribution, and 160 Valquiria de Oliveira Pereira et al. an Annotated Taxonomic Checklist. Special Publication of the Menezes, F.A., Fiorillo, B.F., Gonzalez, R.C. (2015): Hooding Museum of Southwestern Biology 11: 1-373. behavior in Erythrolamprus miliaris Linnaeus, 1758 (Serpentes: Carreira, S., Meneghel, M., Achaval, F. (2005): Reptiles de Uruguay. Dipsadidae). Herpetology Notes 8: 291-293. Facultad de Ciencias, Univ. de La República, Montevideo. Menezes, F. A., Fiorillo, B.F., Franco, F.L., Feio, R.N. (2017): Costa, H.C., São-Pedro, V.A., Feio, R.N. (2010): A new record of Repertoire of antipredator displays in the poorly known the poorly known Amazonian snake Siphlophis worontzowi. Atlantic forest snake, Gomesophis