Herpetology Notes, volume 13: 241-244 (2020) (published online on 13 March 2020)

Mating behaviour of Enyalius boulengeri Etheridge, 1969 (Squamata, Leiosauridae)

André F. Barreto-Lima1,2*, Iago S. Ornellas2,3, Yhuri C. Nóbrega2,4, and Thiago Silva-Soares3

Information on the ecology of species in the genus taken. The air temperature and humidity of the area were Enyalius Wied-Neuwied 1821 (Leiosauridae) is limited, accessed through the Instituto Capixaba de Pesquisa, especially concerning their behaviour. This genus is Assistência Técnica e Extensão Rural (https://incaper. composed of diurnal, insectivorous (Jackson, 1978; Van es.gov.br). The climate of Santa Teresa is classified Sluys et al., 2004) and semi-arboreal lizards (Barreto- as oceanic without a dry season and with a temperate Lima et al., 2013). Its distribution is typically in the summer (Cfb), according to the Köppen Classification Atlantic Forest of Brazil, but some species occur in the (Alvares et al., 2013). Mean annual precipitation is 1868 Amazon Forest, in gallery forests of the ‘Cerrado’, and mm, highest in November and lowest in June, when the in dry forests of the ‘Caatinga’ biome (see Breitman et al., 2019). Enyalius boulengeri Etheridge, 1969 occurs in the Atlantic Forest, in the states of Espírito Santo and Minas Gerais, in southeastern Brazil (Costa and Bérnils, 2018), and its conservation status has not yet been assessed, since basic information on its biology is still scarce or non-existent in the literature. We here describe for the first time a copulation of E. boulenger under natural conditions, in a protected area in the state of Espírito Santo. In addition, we discuss the courtship and copulation behaviours of some other Enyalius species.

Materials and Methods Lizards were photographed with a Canon Power Shot SX50 HS camera and notes on their behaviour were

1 Instituto Nacional da Mata Atlântica, Av. José Ruschi, 4, Centro, Santa Teresa - ES, CEP 29.650-000, Brazil. 2 Instituto Marcos Daniel, Projeto Caiman, Av. Eugênio Pacheco de Queirós, s/n, Jardim Camburi, Vitória - ES, CEP 29.075-910, Brazil. 3 Universidade Federal do Espírito Santo, Laboratório de Genética e Evolução Molecular, Departamento de Biologia - CCHN/UFES. Av. Fernando Ferrari, 514, Vitória - ES, CEP 29.075-910, Brazil. Figure 1. Pair of Enyalius boulengeri during copulation 4 Centro Universitário FAESA, Departamento de Medicina behaviour, in an area of Atlantic Forest in the protected area Veterinária, Av. Vitória, 2220, Vitória - ES, CEP 29.053-360, Estação Biológica Santa Lúcia, municipality of Santa Teresa, Brazil. state of Espírito Santo, southeastern Brazil. Photo: I.S. * Corresponding author. Email: [email protected] Ornellas (2013). 242 André F. Barreto-Lima et al. mean rainfall is < 60 mm (Mendes and Padovan, 2000). (Grantsau, 1966), as well as copulations of E. perditus Mean annual temperature is 20°C (range: 14.3–26.2°C; (Barreto-Lima and Sousa, 2006) were observed. In both Thomaz and Monteiro, 1997). cases males bit the females’ neck during courtship and copulation. Under natural conditions, on tree trunks, Results and Discussion similar behaviours of males biting females’ necks and holding onto them with their feet were documented. In During a field expedition on 14 December 2013 at one instance, Vitt et al. (1996) documented a possible around 19:00 h, a copulating pair of E. boulengeri (Fig. post-copulation of E. leechii, in which lizards were 1) was found on a tree trunk in the Estação Biológica found sleeping in a posture similar to that observed in Santa Lúcia (ca. 19.9711°S, 40.5303°W; Datum: WGS copulations of Polychrus acutirostris by Vitt and Lacher 84; elevation 658 m), a protected 440-ha area in the (1981). A second case involved courtship display without municipality of Santa Teresa, state of Espírito Santo, copulation success in E. perditus (Migliore et al., 2014). southeastern Brazil. The lizards were copulating on a Also, courtship display followed by copulation in E. humid tree trunk about 1.7 m above the substrate and bilineatus on bare soil was reported, with the male remained immobile for ca. 30 min, with the observers biting and holding onto the female with its feet and toes a distance of 1 m away. Air temperature was ca. 23°C (Novelli et al., 2015). and humidity was 88%. The copulation was interrupted Curiously, during courtship and copulation the dorsal when a stick insect (Phasmatodea) climbed on the colour of those lizards can change quickly to a darker pair, causing the male lizard to jump to the ground, tone, as observed in males of E. perditus (Barreto- subsequently followed by the female, which ran away. Lima and Sousa, 2006) and E. bilineatus (Novelli et al., The male lizard advanced toward the researchers, 2015). These authors suggested that this phenomenon stopped ca. 30 cm in front of them, and bobbed his head might be a defensive strategy (i.e., cryptic coloration) a few times. After ca. 7 s the male ran towards another that evolved in order to avoid predators during the researcher and repeated the behaviour twice more until daylight, but this requires further studies. However, this it also ran away and disappeared into the forest litter. phenomenon was not observed in E. boulengeri in the Courtship and copulation behaviours of different present study, probably because our observation was species in the genus Enyalius may be similar, both in made at the beginning of the evening and did not require captivity (Grantsau, 1966; Barreto-Lima and Sousa, crypsis. On the other hand, about reproductive aspects 2006) and under natural conditions (Vitt et al., 1996; of this species, egg data from two dissected females of Migliore et al., 2014; Novelli et al., 2015) (Table 1). In E. boulengeri, collected in the Parque Municipal de São captivity (terraria), copulation in an E. catenatus pair Lourenço, municipality of Santa Teresa, Espírito Santo,

Figure 2. Copulation in Enyalius boulengeri. (A) Detail of the male’s fifth toe holding the hind leg of the female. (B) Detail of the male inserting its hemipenis into the female’s cloaca. Photos: I.S. Ornellas (2013). Mating behaviour of Enyalius boulengeri 243

Table 1. Observations of effective copulations (or attempts) in pairs of Enyalius: species (number of couples), duration of copula (in minutes), localTable condition/biome, 1. Observations month, of effective hour copulations and source. (or attempts) in pairs of Enyalius: species (number of couples), duration of copula (in minutes), local condition/biome, month, hour and source.

Species Copula duration Local condition/ Month/ Source (No. of pairs) (min) biome hour of sighting E. bilineatus (01) < 21 natural (clean soil)/ November/ Novelli et al. (2015) ‘Cerrado’ 09:02 E. boulengeri (01) ca. 30 natural (tree trunk)/ December/ Present study Atlantic Forest ca. 19:00 E. catenatus (01) − captivity November/ Grantsau (1966) (terrarium) − E. leechii (01) − natural/ December/ Vitt et al. (1996), Amazon Forest 22:00 Ávila-Pires (pers. comm.) E. perditus (04) 24 (± 14.4) captivity November-December/ Barreto-Lima and Sousa (terrarium) between 14:25 and 17:07 (2006) (01) Unsuccessful natural (tree trunk)/ November/ Migliore et al. (2014) attempt Atlantic Forest 11:10

Brazil, revealed that the nests can vary from seven eggs Barreto-Lima, A.F., Sousa, B.M. (2006): Court and copulation (length: 1.78 +/-0.03, 1.75-1.85 cm; width: 0.91 +/-0.01, behaviors of Enyalius perditus Jackson, 1978 (Squamata, 0.9-0.95 cm) to 12 eggs (length: 1.68 +/-0.05; 1.61-1.8 Leiosauridae) in captivity conditions. Revista Brasileira de Zoociências 8: 193–197. cm; width: 1.01 +/-0.05, 0.91-1.1 cm) per pregnant Breitman, M.F., Domingos, F.M.C.B., Bagley, J.C., Wiederhecker, female (SVL = 9.1 and 10.6 cm, respectively) (Zocca H.C., Ferrari, T.B., Cavalcante, V.H.G.L., et al. (2018): A new C., pers. comm.). Finally, this study documents for species of Enyalius (Squamata, Leiosauridae) endemic to the first time the reproductive behaviour of E. boulengeri Brazilian Cerrado. Herpetologica 74: 355–369. under natural conditions. In addition, it is well known Costa, H.C., Bérnils, S.R. (2018): Répteis do Brasil e suas Unidades that some Enyalius species copulate during the months Federativas: Lista de espécies. Herpetologia Brasileira 8: 11-57. of tropical summer, supporting that the reproductive Etheridge, R. (1969): A review of the iguanid lizard genus Enyalius. period of these lizards must be seasonal. Bulletin of the British Museum (Natural History), Zoology 18: 233–260. Grantsau, R. (1966): Enyalius catenatus, das brasilianische Acknowledgments. We are grateful to D.De’N. Dalvi and E.L. “Chamäleon”. Aquarium-Terrarium Zeitschrift 19: 217–219. Muhl for support of our fieldwork, to D. Vrcibradic for confirming Mendes, S.L., Padovan, M.P. (2000): A Estação Biológica de our species identification and for a review, to T.C. Ávila-Pires and Santa Lúcia, Santa Teresa, Espírito Santo. Boletim do Museu de L.J. Vitt for the data on E. leechii, to B.M. Sousa for providing Biologia Mello Leitão 11/12: 7–34. a reference, and to A.M.S. Mota for the review of the text. Migliore, S.N., Braz, H.B., Almeida-Santos, S.M. (2014): Finally, our thanks to H. Kaiser and D. Santana for suggestions to improvement this text. This study is part of the project ‘Herpeto Reproductive aspects of two Enyalius lizards from the Atlantic Capixaba: for the knowledge and conservation of amphibians and forest in Southeastern Brazil. Herpetology Notes 7: 273–276. reptiles of Espírito Santo’. We thank support from FAPES/VALE/ Novelli, I.A., Sousa, B.M., Cozendey, P., Frieiro-Costa, F.A. FAPERJ Nº 01/2015 – Pelotização, Meio Ambiente e Logística. (2015): Natural history notes. Enyalius bilineatus (Two-lined Fathead Anole). Courtship behavior. Herpetological Review 46: 91–92. References Thomaz, L.D., Monteiro, R. (1997): Composição1 florística da Alvares, C.A., Stape, J.S., Sentelhas, P.C., Gonçalves, J.L.M., Mata Atlântica de encosta da Estação Biológica de Santa Lúcia, Sparovek, G. (2013): Koppen’s climate classification map for município de Santa Teresa, Espírito Santo. Boletim do Museu de Brazil. Meteorologische Zeitschrift 22: 711–728. Biologia Mello Leitão 7: 3–48. Barreto-Lima, A.F., Pires, E.O., Sousa, B.M. (2013): Activity, Van Sluys, M., Ferreira, M.V., Rocha, C.F.D. (2004): Natural history foraging mode and microhabitat use of Enyalius perditus of the lizard Enyalius brasiliensis (Lesson, 1828) (Leiosauridae) (Squamata) in a disturbed Atlantic rainforest in southeastern from an Atlantic Forest of Southeastern Brazil. Brazilian Journal Brazil. Salamandra 49: 177–185. of Biology 64: 353–356. 244 André F. Barreto-Lima et al.

Vitt, L.J., Ávila-Pires, T.C.S., Zani, P.A. (1996): Observations on the ecology of the rare Amazonian lizard, Enyalius leechii (Polychrotidae). Herpetological Natural History 4: 77–82. Vitt, L.J., Lacher, T.E. (1981): Behavior, habitat, diet, and reproduction of the iguanid lizard Polychrus acutirostris in the caatinga of northeastern Brazil. Herpetologica 37: 53–63.

Accepted by Diego Santana