Natural History Notes and Geographic Distribution of the Poorly Known Echinanthera Amoena (Serpentes: Dipsadidae)

Herpetology Notes, volume 11: 925-928 (2018) (published online on 11 November 2018)

Natural history notes and geographic distribution of the poorly known Echinanthera amoena (Serpentes: Dipsadidae)

Weverton dos Santos Azevedo1,*, Ligia Grazziely dos Santos Amorim2, Frederico de Alcântara Menezes3, and Arthur Diesel Abegg1

The Echinanthera Cope, 1894 genus currently forests, between 500 and 1440 m a.s.l. (Marques et al., comprises six valid species, E. amoena (Jan, 1863), E. 2004, 2009; Bérnils, 2009; Silveira et al., 2010; Batista, cephalomaculata Di-Bernardo, 1994, E. cephalostriata 2017). In this study, we report the encounter of two E. Di-Bernardo, 1996, E. cyanopleura (Cope, 1885), E. amoena specimens, aiming at increasing the knowledge melanostigma (Wagler in Spix, 1824) and E. undulata on their defensive repertoire, microhabitat and daily (Wied, 1824) (Santos-Jr., 2009; Costa and Bérnils, activity. 2015), who are aglyphous (Gomes, 2012), with diets Due to the need to collect several snake species focused on ectothermic prey (Moura-Leite et al., 2003; for the international project “Scales of biodiversity” Marques et al., 2004; Pontes and Rocha, 2008; Salles (FAPESP: 2016/50127-5), on the association of venom and Silva-Soares, 2011; Gomes, 2012). The genus evolution and the rapid diversification of advanced occurs in South America, predominantly in the Brazilian snakes (Caenophidia), which the Butantan Institute is south and southeast regions (Santos-Jr., 2009; Salles a part of, a team composed by three collectors (WSA, and Silva-Soares, 2011; Gomes, 2012) and is found in LGA and ADA) carried out searches specifically aimed forested Atlantic Rainforest regions (Marques et al., at the collection of Echinanthera amoena specimens 2001; Santos-Jr, 2009; Marques et al., 2009; Gomes, (Collecting permit SISBio 9320-1). A five-day field 2012). Some species belonging to this genus are poorly expedition was carried out in the extreme south-central known, with few specimens in zoological collections region of the municipality of São Paulo, in the state of and few available natural history information, as is the São Paulo, Brazil (-23.964086°S, -46.738353°W, WGS case of E. cephalomaculata and E. amoena. 84; 805m a.s.l.), near the Curucutu Nucleus of Serra do Echinanthera amoena displays presumably terrestrial Mar State Park. This area was chosen due to the previous and diurnal habits, with oviparous reproduction and a diet record of an E. amoena specimen (Batista, 2017) on comprising anuran amphibians (Marques et al., 2004; the banks of the Camburi stream. Based on the report Marques et al., 2009). Records for this species coincide by Batista (2017) and anecdotal observation records with continuous forest areas in dense ombrophylous of E. amoena specimens close to lotic water bodies, a sampling effort of 4h a day was applied, during the morning and afternoon (totaling 80h of active search), traversing parts of the Camburi stream and checking several potential microhabitats in order to encounter

1 Instituto Butantan, Laboratório Especial de Coleções specimens (Fig. 1). Zoológicas, Avenida Vital Brasil, 1.500, Butantã, CEP On 31 January, 16:15h and 4 February 2018 at 13:40 05503-900 São Paulo, SP, Brazil. h, two Echinanthera amoena individuals were found: 2 Instituto Butantan, Laboratório de Ecologia e Evolução, one juvenile male, snout-vent length (SVL)= 227 mm, Avenida Vital Brasil, 1.500, Butantã, CEP 05503-900 São tail length (TL)=110 mm and one adult male, SVL= Paulo, SP, Brazil. 407 mm, TL= 200 mm, respectively (Fig. 2A,B). The 3 Universidade Federal de Viçosa, Departamento de Biologia recorded environmental conditions (temperature and Animal. Avenida P.H. Rolfs, s/no, Campus Universitário, CEP 36571-000, Viçosa, Minas Gerais, Brazil. humidity) on the encounter date were the following: * Corresponding author. Email: mean temperature (19.6 °C) and relative air humidity [email protected] (61.3%) on 31 January and mean temperature (19.8 °C) 926 dos Santos Azevedo et al.

with dense high altitude forests, E. amoena appears to use very specific microhabitats, living on stream banks within forests. In fact, another survey of the snake fauna was conducted over a year (September 2016 to August 2017) at the Serra do Mar State Park (Curucutu Nucleus), very close to the area of our encounters, exploring forest areas (but not streams) and native fields, with no records for any E. amoena specimen (Valquiria O. Pereira pers. comm.). In general, Brazilian herpetofaunal surveys are conducted through active searches and the use of interception and pitfall traps (Bernarde, 2012). Pitfalls are generally installed relatively distant from water bodies, to avoid flooding on days with heavy rainfall; on Figure 1. Camburi stream, area of encounter of Echinanthera amoena specimens in the present work.

and relative air humidity (64.7%) on 4 February. Sunlight incidence on the forest was observed on both days, but accompanied by occasional rain. The specimens were collected and sent to the Special Laboratory of Zoological Collections, at the Butantan Institute, fixed in a 10% formaldehyde solution, preserved in 70% alcohol, and deposited in the “Alphonse Richard Hoge” herpetological collection under vouchers IBSP 89773 and IBSP 89774. Both specimens were found on the banks of the stream, resting on rocks covered by mosses. To our surprise, both specimens remained virtually immobile after being visualized, which is unusual behavior in snakes belonging to the Echinantherini tribe, who are notable by the slender body and rapid flight responses (ADA pers. obs.; Conrado Mario-da-Rosa, Leandro Malta-Borges, Noeli Zanella pers. comm.). Obviously, it is important to note that the specimens noticed collector approach, due to head movements, aiming at observing the collectors as they approached. After their capture, the specimens defended themselves through cloacal discharges, a very common defensive behavior in snakes and noted for all species belonging to the Echinantherini tribe (Marques et al. 2004, 2005, 2017; Abegg and Entiauspe-Neto, 2012). The literature records for Echinanthera amoena (Table Figure 2. Specimen of Echinanthera amoena A) adult 1), alongside anecdotal reports and the observations IBSP 89773 and (B) juvenile IBSP 89774. Collected near performed in the present study, allow us to question the Curucutu nucleus of Serra do Mar State Park, São Paulo Batista’s (2017) statement that E. amoena forages on the municipality, state of São Paulo, Brazil (-23.964086°S, - ground of continuous forest areas. Although associated 46.738353°W). Natural history notes and geographic distribution of Echinanthera amoena 927

Table 1. Records for Echinantera amoena.

9RXFKHU /RFDOLWLHV /DWLWXGH /RQJLWXGH 6RXUFH 6mR3DXOR6WDWH ,%63 6mR3DXOR 7KLVVWXG\ ,%63 6mR3DXOR 7KLVVWXG\ ,%63 %DQDQDO 'L%HUQDUGR %pUQLOV ,%63 %DQDQDO 'L%HUQDUGR %pUQLOV ,%63 -XTXLWLED 3HGUD/LVD 'L%HUQDUGR %pUQLOV ,%63 3LQGDPRQKDQJDED 'L%HUQDUGR %pUQLOV ,%63 6mR9LFHQWH 5LR%UDQFR 'L%HUQDUGR %pUQLOV ,%63 6mR3DXOR 7UHPHPEp+RUWR)ORUHVWDO 'L%HUQDUGR %pUQLOV =8(& &DUDJXDWDWXED 3DUTXH(VWDGXDOGD6HUUD 'L%HUQDUGR 0DUTXHVHWDO GR0DU %pUQLOV ,%63 6mR3DXOR 3LQKHLULQKR+RUWR)ORUHVWDO 'L%HUQDUGR %pUQLOV 0DUTXHVHWDO ,%63 &XEDWmR 3LDoDJXHUD %pUQLOV ,%63 6mR3DXOR 9LOD0DWLOGH 0DUTXHVHWDO ,%63 ,WDQKDpP 3DUTXH(VWDGXDOGD6HUUDGR 7KLVVWXG\ 0DU ,%63 ,WDQKDpP 3DUTXH(VWDGXDOGD6HUUDGR 7KLVVWXG\ 0DU 0LQDV*HUDLV6WDWH ,%63 %DHSHQGL 'L%HUQDUGR %pUQLOV 0=8)9 *RYHUQDGRU9DODGDUHV 3LFRGR,ELWXUXQD %pUQLOV 015- 6DQWD5LWDGH,ELWLSRFD 3DUTXH(VWDGXDO 6LOYHLUDHWDO GR,ELWLSRFD 015- 6DQWD5LWDGH,ELWLSRFD 3DUTXH(VWDGXDO 6LOYHLUDHWDO GR,ELWLSRFD 0=863 $OWR&DSDUDy 3DUTXH1DFLRQDOGR &DVVLPLURHWDO &DSDUDy9DOH9HUGH 3DUDQi6WDWH ,%63 $UDSRQJDV 'L%HUQDUGR ,%63 $UDSRQJDV 'L%HUQDUGR ,%63 0DOOHW 'RUL]RQ 'L%HUQDUGR %pUQLOV 0+1&, 6mR-RVpGRV3LQKDLV 5HSUHVDGH %pUQLOV *XDULFDQD 5LRGH-DQHLUR6WDWH 015- 3DUDWL 3HGUD%UDQFD 'L%HUQDUGR %pUQLOV 015- 3DUDWL 3HGUD%UDQFD 'L%HUQDUGR %pUQLOV =8)5- 5LRGH-DQHLUR 6mR&RQUDGR %pUQLOV 015- &DFKRHLUDVGH0DFDFX 5HVHUYD 6LOYHLUDHWDO (FROyJLFDGH*XDSLDoX (VStULWR6DQWR6WDWH =8)5- 6DQWD7HUH]D %pUQLOV 6DQWD&DWDULQD6WDWH &&1* %OXPHQDX %pUQLOV 0+1&, %OXPHQDX %pUQLOV 928 dos Santos Azevedo et al. the other hand, active demand is hardly conducted along de São Paulo. Dissertação de Mestrado. Universidade Estadual streams during the daytime period (ADA, pers. obs.). Paulista “Júlio de Mesquita Filho”, p. 113. In general, water bodies are explored at night, as this Bérnils, R.S. (2009): Composição e Padrões de Distribuição de Caenophidia (Squamata, Serpentes) das Serras Atlânticas e facilitates finding anuran amphibians in reproduction, Planaltos do Sudeste da América do Sul. Tese de Doutorado. as well as their nocturnal predators. This sampling Universidade Federal do Rio de Janeiro, p. 808. failure may be responsible for the low amounts of E. Bernarde, P.S. (2012): Anfíbios e répteis: introdução ao estudo da amoena specimens available in zoological collections herpetofauna brasileira. Anolis Books, p. 320. and, consequently, for the general lack of knowledge on Costa, H.C., Bérnils, R.S. (2015): Répteis brasileiros: Lista de the species. espécies 2015. Herpetologia Brasileira 4: 75–93. The general Echinanthera amoena coloration pattern Freitas, M.A. (2003): Serpentes brasileiras. Malha-de-Sapo Publicações e Consultoria Ambiental, Lauro de Freitas, p. 160. is intriguing (Fig. 2), consisting of scintillating green Gomes, C.A. (2012): História natural das serpentes dos gêneros on the dorsal anterior region and darkening towards Echinanthera e Taeniophallus (Echinantherini). Dissertação de the tail, which is dark brown, very different from what Mestrado. Universidade Estadual Paulista “Júlio de Mesquita is observed for other species belonging to the genus, Filho”, p. 68. whose coloration is relatively homogeneous throughout Marques, O.A.V., Sazima, I. (2004): História natural dos répteis the body. At the same time, the environment that E. da Estação Ecológica Juréia-Itatins. In: Marques O.A.V, Duleba W. (Eds.), Estação Ecológica Juréia-Itatins: Ambiente Físico, amoena inhabits (rocks covered with mosses, on stream Flora e Fauna. +olos, Ribeirão Preto. banks) is also a mosaic of green and brown (Fig. 1). Marques, O.A.V., Eterovic, A., Endo, W. (2001): Seasonal activity This fact, coupled with our observations about the of snakes in the Atlantic forest in southeastern Brazil. Amphibia primary defensive behavior of the captured specimens Reptilia 20: 103‒111. (remaining immobile), suggests that camouflage and Marques, O.A.V., Eterovic, A., Guedes, T.B., Sazima, I. (2017): immobility seem to be the main defense mechanisms of Serpentes da Caatinga: guia ilustrado. Ponto A. this species, which has been neglected by the scientific Marques, O.A.V., Eterovic, A., Nogueira, C.C., Sazima, I. (2016): Serpentes do Cerrado: guia ilustrado. Holos Editora. literature until now (Marques et al., 2001; Freitas, Marques, O.A.V., Eterovic, A., Sazima, I. (2004): Snakes of the 2003). Brazilian Atlantic Forest: an illustrated field guide for the Serra The encounter of two Echinanthera amoena specimens do Mar Range. +olos Editora. on rocks located on stream banks aids in elucidating Marques, O.A.V., Eterovic, A., Sazima, I. (2005): Serpentes do basic questions about the microhabitats occupied by Pantanal: guia ilustrado. Holos Editora. this species, and also corroborates unpublished records Moura-Leite, J.C., Bérnils, R.S., Morato, S.A.A., Langone, J.A. (2003): Diet. Echinanthera cephalostriata (NCN). that E. amoena are associated with lotic water bodies, Herpetological Review 34: 149. probably foraging by day. Furthermore, this suggests Pontes, J.A.L., Rocha, C.F.D. (2008): Serpentes da Serra do that, in subsequent herpetofaunal surveys congruent Mendanha, Rio de Janeiro, RJ, ecologia e conservação. with the geographic distribution of this species, Technical Books Editora Ltda, Rio de Janeiro, Brasil, p. 147. researchers should conduct careful observations along Rocha, C.F.D., Bergallo, H.G., Pombal Jr, J.P., Geise, L., Sluys, streams within the forest throughout the day, aiming M. V., Fernandes, R., Caramaschi, U. (2004): Fauna de anfíbios, at encountering more specimens and filling gaps about répteis e mamíferos do Estado do Rio de Janeiro, sudeste do Brasil. Publicações Avulsas do Museu Nacional 104: 3‒23. our understanding of the natural history, morphology, Salles, R.D.O.L., Soares, T.S. (2011): Predation on Leptodactylus taxonomy and other little known E. amoena aspects. spixi (Anura: Leptodactylidae) by Echinanthera undulata (Squamata: Dipsadidae). Herpetology Notes 4: 125‒126. Acknowledgements. The authors are grateful to Giuseppe Puorto Santos-Jr., A.P. (2009): Revisão taxonômica do grupo de (IBSP) for providing the fall data of the specimens under his care Taeniophallus occipitalis e o relacionamento filogenético da and to Felipe Gobbi Grazziotin (IBSP), for the financial support tribo Echinantherini (Serpentes, Dipsadidae, Xenodontinae). for the development of the expedition. The Francisco Luís Franco Tese de Doutorado. Pontificia Universidade Catolica do Rio and Renato Silveira Bérnils for reviewing the manuscript. Grande do Sul, p. 261.

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