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Herpetology Notes, volume 13: 981-987 (2020) (published online on 26 November 2020)

Anolis tandai, a new dietary record for the Amazon ringed , Rhinobothryum lentiginosum (Scopoli, 1785) (: )

Luis A. García–Ayachi1,2,3,*, Mallory Wittwer3, and Christopher Kirkby3

The Amazon banded snake is a rare, infrequently because they observed these on the ground observed of squamate with only a few (Martins and Oliveira, 1998; Doan and Arriaga, 2000; specimens stored in biological collections, despite its Duellman, 2005; Ribeiro Duarte, 2010; Avila–Pires et widespread distribution (Cunha and Nascimento, 1978). al., 2010). However, dietary information suggests that R. This snake lives in the lowland Amazonian forests of lentiginosum is a specialist that feeds on a variety , , , , , of terrestrial and arboreal species that range in size from , , , , and (Peters small species, such as Gonatodes spp. to the larger and Orejas–Miranda, 1970; Miranda et al., 2009; Iguana iguana (Table 1). Rhinobothryum lentiginosum Reynolds and MacCulloch, 2012; Uetz et al., 2020). likely forages in tree and bushes, and possibly preys Although it has been recorded in primary forest (Cunha on night–sleeping (Oliveira and Martins, 1998; and Nascimento, 1978; Cunha et al., 1985; Martins Martins and Oliveira, 1998; Vitt et al., 2000; Duellman, and Oliveira, 1998; Fraga et al., 2014), some records 2005; Ribeiro Duarte, 2010), and occasionally on , demonstrate that R. lentiginosum also inhabits secondary small and mammals (Zimmerman and Rodrigues, forest (Venegas and Couceiro, 2017), and more open, 1990; Avila–Pires et al., 2010). disturbed areas (Bernarde and Abe, 2006; França et al., Surprisingly, the most common tree–dwelling lizards 2006). Western Amazon records of this species include in the Amazon ( Anolis) have not previously been northern (Loreto department, Dixon and Soini, 1986; recorded in the diet of Rhinobothryum lentiginosum. Gagliardi–Urrutia, 2010), central (Ucayali department, With 436 species (Uetz et al., 2020), Anolis lizards Lehr and Aguilar, 2000), and southern Peru (Madre de are relatively common and are prey of many arboreal Dios department, Rodríguez and Cadle, 1990; Doan and and semi–arboreal snakes, as reported by many studies Arriaga, 2000; Duellman, 2005; von May et al., 2006; (Beebe, 1946; Duellman, 1958, 1978, 2005; Emsley, Catenazzi et al., 2013, Venegas and Couceiro, 2017). 1963; Henderson, 1974, 1982, 1984a,b, 1993, 2002; Rhinobothryum lentiginosum is a snake that is both Myers, 1974; Henderson and Nickerson, 1976; Cunha diurnal (Martins and Oliveira, 1998; Venegas and and Nascimento, 1978; Henderson et al., 1981, 2007; Couceiro, 2017) and nocturnal in its activities (Martins Cunha and Nascimento, 1982; Franz and Gicca, 1982; and Oliveira, 1998; Doan and Arriaga, 2000; Vitt et al., Nellis et al., 1983; Henderson and Horn, 1983; Seib, 2000; Duellman, 2005; Ribeiro Duarte, 2010). Previous 1984; Novo Rodríguez and de Arazoza Rodríguez, authors considered the species as being terrestrial, 1986; Rodríguez–Robles and Leal, 1993a,b; Dixon et al., 1993; Avila–Pires, 1995; Henderson and Sajdak, 1996; Gorzula and Señaris, 1998; Martins and Oliveira, 1998; Campbell, 1999; Stafford, 2003; Gutierrez and Arredondo, 2005; Pérez–Higareda et al., 2007; Halstead et al., 2008; Scartozzoni et al.,2009; Bernarde and Abe, 1 Instituto Peruano de Herpetología (IPH), Lima, Perú. 2010; García–Padilla and Luna–Alcántara, 2011; Ray et 2 División de Herpetología, Centro de Ornitología y al., 2011; Henderson and Pauers, 2012; Veríssimo et al., Biodiversidad (CORBIDI), Lima, Perú. 3 Asociación Fauna Forever, Puerto Maldonado, Madre de Dios, 2012; de Sousa et al., 2014; Natera et al., 2015; Clause Perú. and Clause, 2016; Solé and Dias, 2017; Henderson and * Corresponding author. E-mail: [email protected] Powell, 2018; Torres–Carvajal et al., 2018; Sosa et al., 982 Luis A. García–Ayachi et al.

2019; Fuentes–Montejo and Sánchez, 2019; Roberto R. lentiginosum (snout–vent length 492 mm, total body and Souza, 2020; Alamy, 2020a,b). length 632 mm) feeding on a female adult Anolis tandai During fieldwork in the southern Peruvian Amazon, we (Tandai’s anole, total body length 16 cm). We found the observed for the first time a species of Anolis predated by snake on a bush, 39 cm above the ground. The snake Rhinobothryum lentiginosum. On 9 September 2016 at had bitten into the dorsum of the lizard, which appeared 20:21 h, in the tropical humid lowland rainforest around to still be alive due to the continued movements of its Las Piedras Amazon Centre (LPAC), Las Piedras river limbs. The snake kept biting the lizard for ~2 minutes and basin (12°4’10.99”S, 69°29’36.86”W, altitude 226 m), until its death. At that point, with slow jaw movements, Madre de Dios department of Peru, we observed a female the snake manoeuvred the lizard to swallow it head first

Figure 1. An adult female Rhinobothryum lentiginosum feeding on a female Anolis tandai. (A) Initial sighting of R. lentiginosum hanging from a branch, biting dorsally the upper body of the lizard. (B-D) Sequence showing the swallowing of the lizard, head first. Photo by M. Wittwer. Anolis tandai, a new dietary record for the Amazon ringed snake 983

Table 1. List of prey items for Rhinobothryum lentiginosum as recorded in literature and in this study. Table 1. List of prey items for Rhinobothryum lentiginosum as recorded in literature and in this study.

Prey Item Reference Anolis tandai This study Kentropyx calcarata Kentropyx calcarata juvenile Remains of Ameiva ameiva de Arruda et al., 2015 Remains of Gonatodes sp. Remains of lizard, unidentifiable Remains of Mabuyidae Iguana iguana Ribeiro Duarte, 2010 Mabuya nigropunctata Bernarde and Abe, 2010 Birds, mammals Avila-Pires et al., 2010 Gonatodes humeralis Vitt et al., 2000 Gonatodes humeralis Martins and Oliveira, 1998 Gonatodes humeralis Mabuya sp. plica Oliveira and Martins, 1998 Plica umbra and remains of another lizards marmoratus and remains of another lizards frogs Zimmerman and Rodrigues, 1990

Table 2. List of snake species that prey on Anolis spp. as recorded in the literature and in this study. D = Diurnal; N = Nocturnal. Table 2. List of snake species that prey on Anolis spp. as recorded in the literature and in this study. D = Diurnal; N = Nocturnal.

Family Species Habit Prey References Chilabothrus monensis N Anolis sp. Nellis et al., 1983. cookii N Anolis griseus, A. trinitatis. Henderson et al., 2007; Henderson and Pauers, 2012; Henderson and Powell, 2018.

() Corallus grenadensis N Anolis aeneus, A. griseus, A. richardi, Henderson, 1993; Henderson and Pauers, 2012; A. trinitatis, Anolis spp. Henderson and Powell, 2018. Corallus hortulanus N Anolis sp. Henderson, 2002. antiguae D Anolis sp. Henderson and Sajdak, 1996. D , A. marmoratus, A. oculatus, Henderson and Sajdak, 1996. Anolis sp. Alsophis rijersmai D Anolis gingivinus Henderson and Sajdak, 1996. Alsophis rufiventris D , A. wattsi, Anolis sp. Henderson and Sajdak, 1996. Alsophis spp. D Anolis spp. Henderson and Sajdak, 1996. portoricensis D Anolis cristatellus, A. evermanni, Rodríguez–Robles and Leal, 1993a,b; Henderson and A. monensis, A. pulchellus, A. stratulus, Sajdak, 1996. Anolis spp. Colubridae Cubophis cantherigerus D Anolis angusticeps, A. conspersus, Henderson, 1984a; Novo Rodriguez and de Arazoza () A. ophiolepis, A. porcatus, A. quadriocellifer, Rodriguez, 1986; Henderson and Sajdak, 1996. A. sagrei, Anolis sp. Cubophis vudii D Anolis brunneus, A. sagrei, A. scriptus, Henderson and Sajdak, 1996. Anolis sp. Erythrolamprus perfuscus D Anolis extremus Emsley, 1963; Michaud and Dixon, 1989. Haitiophis anomalus D Anolis sp. Henderson and Sajdak, 1996. Hypsirhynchus ferox D Anolis cybotes, Anolis spp. Henderson, 1984a,b. Hypsirhynchus parvifrons D Anolis brevirostris, A. chlorocyanus, Franz and Gicca, 1982; Henderson, 1984a. A. cybotes, Anolis sp. Laltris dorsalis D Anolis sp. Henderson, 1984a.

984 Luis A. García–Ayachi et al.

Table 2. Continued Table 2. List of snake species that prey on Anolis spp. as recorded in the literature and in this study. D = Diurnal; N = Nocturnal.

Family Species Habit Prey References ImantodesChilabothrus cenchoa monensis N Anolis cfsp. auratus, A. capito, A. barkeri, HendersonNellis et al., and 1983. Nickerson, 1976; Duellman, 1978; Corallus cookii N A.Anolis chrysolepis, griseus, A. frenatus,trinitatis. A. fuscoauratus, Campbell,Henderson 1999; et al., Martins2007; Henderson and Oliveira, and 1998;Pauers, 2012; A. lemurinus, A. mariarum, A. ortonii, Duellman,Henderson 2005;and Powell, Gutierrez 2018. and Arredondo, 2005; Boidae A. petersii, A. planiceps, A. punctatus, Pérez–Higareda et al., 2007; García–Padilla and Luna– (Boinae) Corallus grenadensis N A.Anolis rodriguezii, aeneus, A.A. trachyderma,griseus, A. richardi, A. uniformis, Alcántara,Henderson, 2011; 1993; Ray Henderson et al., 2011; and Pauers,de Sousa 2012; et al., AnolisA. trinitatis, sp. Anolis spp. 2014;Henderson Natera and et Powell,al., 2015; 2018. Clause and Clause, 2016; Corallus hortulanus N Anolis sp. Torres–CarvajalHenderson, 2002. et al., 2018; Alamy, 2020a. ImantodesAlsophis antiguae gemmistratus ND Anolis sp.sp. Henderson and Nickerson,Sajdak, 1996. 1976. ImantodesAlsophis antillensis inornatus ND Anolis sp.lividus, A. marmoratus, A. oculatus, Torres–CarvajalHenderson and Sajdak, et al., 2018. 1996. Leptodeira maculata N Anolis spp.sp. Duellman, 1958. LeptodeiraAlsophis rijersmai ashmeadii ND Anolis cfgingivinus auratus NateraHenderson et al., and 2015. Sajdak, 1996. LeptodeiraAlsophis rufiventris bakeri ND Anolis lineatussabanus, A. wattsi, Anolis sp. Duellman,Henderson 1958.and Sajdak, 1996. LeptodeiraAlsophis spp. frenata ND Anolis spp.spp. Duellman,Henderson 1958.and Sajdak, 1996. LeptodeiraBorikenophis polysticta portoricensis ND Anolis spp.cristatellus, A. evermanni, Duellman,Rodríguez–Robles 1958. and Leal, 1993a,b; Henderson and A. monensis, A. pulchellus, A. stratulus, Sajdak, 1996. Philodryas argentea D Anolis chrysolepis,spp. A. fuscoauratus, A. tandai, Duellman, 1978; Cunha and Nascimento, 1978; A. trachyderma. Avila–Pires, 1995. Colubridae Cubophis cantherigerus D Anolis angusticeps, A. conspersus, Henderson, 1984a; Novo Rodriguez and de Arazoza (Dipsadinae) Philodryas olfersii D AnolisA. ophiolepis, auratus A. porcatus, A. quadriocellifer, GorzulaRodriguez, and 1986; Señaris, Henderson 1998. and Sajdak, 1996. taeniata D AnolisA. sagrei, spp. Anolis sp. Myers, 1974. SiphlophisCubophis vudii compressus ND Anolis chrysolepis,brunneus, A. A. sagrei, fuscoauratus, A. scriptus, Anolis sp. MartinsHenderson and and Oliveira, Sajdak, 1998; 1996. Solé and Dias, 2017; Anolis sp. Torres–Carvajal et al., 2018; Alamy, 2020b. ThamnodynastesErythrolamprus perfuscuschimanta D Anolis sp.extremus GorzulaEmsley, and1963; Señaris, Michaud 1998. and Dixon, 1989. UromacerHaitiophis catesbyianomalus D Anolis sp.sp. Henderson etand al., Sajdak, 1981; Henderson,1996. 1982; Hypsirhynchus ferox D Anolis cybotes, Anolis spp. Henderson, 1984a.1984a,b. UromacerHypsirhynchus frenatus parvifrons D Anolis chlorocyanus,brevirostris, A. A. chlorocyanus, cybotes, A. olssoni, HendersonFranz and Gicca, and Horn, 1982; 1983; Henderson, Henderson, 1984a. 1984a. Table 2 continued AnolisA. cybotes, sp. Anolis sp.

Colubridae UromacerLaltris dorsalis oxyrhynchus D Anolis spp.sp. HendersonHenderson, et 1984a. al., 1981; Henderson, 1982; (Dipsadinae) Henderson, 1984a. Dendrophidion nuchale D Anolis sp. Stafford, 2003.

Dendrophidion percarinatum D Anolis sp. Stafford, 2003. exoletus D Anolis sp. Roberto and Souza, 2020.

Chironius fuscus D Anolis sp. Beebe, 1946.

Chironius monticola D Anolis sp. Dixon et al., 1993.

Chironius multiventris D Anolis fuscoauratus Cunha and Nascimento, 1982.

Coluber constrictor D Halstead et al., 2008.

Drymobius chloroticus D Anolis sp. Seib, 1984. margaritiferus D Anolis sp. Seib, 1984. Drymoluber dichrous D Anolis fuscoauratus, Anolis sp. Duellman, 1978; Veríssimo et al., 2012. D Anolis sp. Martins and Oliveira, 1998. Leptophis depressirostris D Anolis sp. Torres–Carvajal et al., 2018. Leptophis mexicanus D Anolis capito, Anolis spp. Henderson, 1982; Fuentes–Montejo and Sánchez, 2019. flagellum D Anolis carolinensis Halstead et al., 2008. Mastigodryas amarali D Anolis planiceps Natera et al., 2015. Mastigodryas bruesi D Anolis aeneus, A.trinitatis Henderson and Powell, 2018. Mastigodryas melanolomus D Anolis rodriguezii, A. sagrei, Anolis sp. Seib, 1984; Sosa et al., 2019. aeneus D Anolis chrysolepis, A. tandai, Anolis sp. Beebe, 1946; Henderson, 1974; Cunha and Nascimento, 1978; Henderson, 1982; Avila–Pires, 1995. Oxybelis fulgidus D Anolis chrysolepis, A. ortonii, A. tandai, Beebe, 1946; Henderson, 1982; Avila–Pires, 1995; Anolis spp. Scartozzoni et al., 2009; Bernarde and Abe, 2010; Torres–Carvajal et al., 2018. Rhinobothryum lentiginosum D–N Anolis tandai This study. Bothriechis schlegelii D–N Anolis sp. Torres–Carvajal et al., 2018. Viperidae Crotalus durissus D–N Anolis sp. Natera et al., 2015. Porthidium nasutum D–N Anolis sp. Torres–Carvajal et al., 2018.

Anolis tandai, a new dietary record for the Amazon ringed snake 985

(Fig. 1). Having completely swallowed the lizard, we em Espigão do Oeste, Rondônia, Brasil. Biota Neotropica 10: proceeded to capture, measure, sex (by massaging the 167–173. cloaca for presence of hemipenes) the snake, and finally Campbell, J.A. (1999): Amphibians and of northern , the Yucatán, and . USA, University of released it near the point of capture. Oklahoma Press. This is the first record of an anole lizard, Family Catenazzi, A., Lehr, E., von May, R. (2013): The amphibians and , in the diet of Rhinobothryum lentiginosum. reptiles of Manu National Park and its buffer zone, Amazon Therefore, we add R. lentiginosum to the list of more basin and eastern slopes of the Andes, Peru. Biota Neotropica than 50 snakes known to prey on anoles; some of these 13: 269–283. snake species have nocturnal habits (16 species, 30%), Clause, J.K., Clause, A.G. (2016): cenchoa (Blunt– which would mean that they are feeding on sleeping headed Tree Snake). Diet. Herpetological Review 47: 312–313. Anolis. In addition to R. lentiginosum, Oxybelis aeneus, Cunha, O.R., Nascimento, F.P. (1978): Ofıdios da Amazonia, X–As cobras da Regiao Leste do Pará. Belém, Publicações Avulsas do Oxybelis fulgidus and Philodryas argentea are known Museu Paraense Emılio Goeldi. predators of Anolis tandai (Table 2). During our search Cunha, O.R., Nascimento, F.P. (1982): Ofídios da amazônia XV– of information about snakes that feed on anole lizards, As espécies de Chironius da Amazônia Oriental (Pará, Amapá we tried to collect as much data as possible, however e Maranhão) (Ophidia: Colubridae). Memórias do Instituto we have some limitations, such as national books and Butantan 46: 139–172. reports from some countries that remain unavailable. Cunha, O.R., Nascimento, F.P., Avila–Pires, T.C. (1985): Os repteis da área de Carajás, Pará, Brasil (Testudines e Squamata) I. Publicações Avulsas do Museu Paraense Emılio Goeldi 40: Acknowledgements. We would like to thank Fauna Forever 9–92. (www.faunaforever.org) for supporting this research as part of de Arruda, L.A.G., de Carvalho, M.A., Kawashita–Ribeiro, their forest conservation and biodiversity monitoring programme, R.A. (2015): New records of the Amazon Banded Snake and the Alliance for Research and Conservation in the Amazon (ARCAmazon) for granting access to the Las Piedras Amazon Rhinobothryum lentiginosum (Serpentes: Colubridae) from Mato Centre (LPAC). Thanks to all the staff at LPAC for providing a Grosso State, Brazil, with natural history notes. Salamandra 51: comfortable and beautiful place to stay and conduct our research. 199–205. Thanks to the Fauna Forever research volunteers Max Homer de Sousa, K.R.M., Prudente, A.L.C., Maschio, G.F. (2014): and Lina Madsen for all their assistance in the field. Thanks to Reproduction and diet of (Dipsadidae: Fernando Ayala, Robert Henderson for providing us with relevant Dipsadinae) from the Brazilian Amazon. 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Accepted by Michael Jowers