The lizard genus Enyalius (Leiosauridae) currently comprises nine species distributed mainly in the Atlantic Forest domain of South America, and in the Brazilian Amazon rainforest, Cerrado, and Caatinga (Frost et al., 2001; Rodrigues et al., 2006; Uetz, 2013). Species of Enyalius are insectivorous, diurnal, with arboreal or semi-arboreal habits (Jackson, 1978; Vitt et al., 1996; Zamprogno et al., 2001; Van Sluys et al., 2004; Rautenberg and Laps, 2010; Barreto-Lima and Sousa, 2011). Enyalius iheringii Boulenger, 1885 and E. perditus Jackson, 1978 are two species endemic to the Brazilian Atlantic forest in southeastern Brazil (Jackson, 1978), whose natural history, especially their reproductive aspects, is poorly known (Marques and Sazima, 2004; Barreto-Lima and Sousa, 2006; Rautenberg and Laps, 2010; Sturaro and Silva, 2010). Herein, we provide novel information on reproductive aspects of E. iheringii and E. perditus from São Paulo, southeastern Brazil.

On 3 November 2012 at 11:10 h (mid-spring), a couple of E. perditus (both with snout-vent length between 120-130 mm, approximately) were found in a copulation attempt, during a herpetofaunal survey in a fragment of Atlantic Forest with approximately 52 km2 at Juquiazinho district, in Juquitiba, São Paulo (-23.97203, -47.02294; datum=WGS84; 730 m a.s.l.), south-eastern Brazil. The couple was on a tree trunk about 1 m above ground. The male was biting the female’s neck when suddenly both fell from the trunk on the leaf litter. After the fall, the male remained on

the back of the female, biting her neck in an attempt to immobilize her (Fig. 1). Both remained in this position for about 30 seconds. After this, the female disengaged from the male and escaped, followed by the male a few seconds later. Effective copulation was not observed.

Courtship was previously reported for at least three species of Enyalius. Vitt et al. (1996) reported a possible courtship in field conditions for E. leechii (Boulenger, 1885), whereas Grantsau (1966) and Barreto-Lima and Sousa (2006) reported courtship and mating in captive conditions for E. catenatus and E. perditus. To our knowledge, our observation was the first courtship confirmed taken in field conditions for a species of Enyalius. In both captive reports, male bit females during attempted copulation. The pattern of courtship behaviour observed in nature was similar to those taken in captive conditions (Grantsau, 1966; Barreto-Lima and Sousa, 2006).

The period of courtship (spring) was coincident with the period of vitellogenesis and courtship/mating in captivity previously reported for the species (Barreto-Lima and Souza, 2006; Sturaro and Silva, 2010; Table 1). Coincidently, the same female involved in this courtship/mating episode was observed in the previous night. The individual was recognized for being in process of shedding skin (Fig. 2), in addition to the presence of a callosity in the tail. The shedding process is associated with the mating season of lizards and snakes (Mason and Gutzke, 1990; Marques et al., 2009), and several authors have suggested that shedding is part of the oestrus signal (Aldridge and Duvall, 2002). The proposed mechanism is that reproductive pheromones released at the time of shedding stimulate male courtship behaviour (Mason and Gutzke, 1990; Mason, 1992). Additionally, this female showed some light orange spots on the neck and throat during the copulation attempt, similarly to the observed by Sturaro and Silva (2010) in reproductive females, suggesting that this feature is an important courtship stimulator for

Herpetology Notes, volume 7: 273-276 (2014) (published online on 25 April 2014)

Reproductive aspects of two Enyalius lizards from the Atlantic forest in Southeastern Brazil

Serena Najara Migliore1,2, Henrique Bartolomeu Braz1 and Selma Maria Almeida-Santos1

1Laboratório de Ecologia e Evolução, Instituto Butantan - Av. Dr. Vital Brazil, 1500 – Butantã, São Paulo-SP, CEP 05503-900.

2Corresponding author: serena_891@hotmail.com; serena.migliore@butantan.gov.br

Serena Najara Migliore et al.274

males (Baird, 2004). Taken together, shedding process and colour signal suggest that the female of E. perditus was probably signalling her condition to the male.

Reproductive observations on Enyalius iheringii were taken from a female (voucher specimen: IBSPCR 0425; Instituto Butantan, São Paulo, Coleção de Referência) collected on 3 March 2012, in the Serra do Mar State Park, Ubatuba, São Paulo, southeastern Brazil. The female measured 103 mm of snout-vent length (SVL) and 203 mm of tail length (TL). It was kept in a cage containing branches and leaf litter. On 2 April 2012, it laid 18 eggs within the cage. Five eggs were infertile.

The remaining 13 eggs were measured, using a digital calliper (to the nearest 0.1 mm) and weighed, using a digital balance (to the nearest 0.01 g). Eggs averaged 15.0 ± 0.5 mm in length (range = 14.1–15.7 mm), 9.7 ± 0.7 mm in width (range = 8.8–11.2 mm), and 0.81 ± 0.10 g in mass (range = 0.70–1.05 g). After oviposition, the female weighed 24.0 g. The relative clutch mass (RCM; total clutch mass/maternal body mass after oviposition + total clutch mass; following Vitt and Price, 1982) was 0.378. Thirteen eggs were incubated. Eggs were housed in a plastic container, half-buried with moistened vermiculite, and maintained at room temperature

Figure 1. Copulation attempt in Enyalius perditus (Juquiazinho, Juquitiba, São Paulo, Brazil). Notice the male (green individual) biting female’s neck (brownish individual) in attempt to immobilize her.

Table 1.

Species Courtship Mating Vitellogenesis Gravidity or

egg-laying

Corpus luteum Hatching Clutch size

E. perditus Spring

(Nov-Dec)1,5

Spring

(Nov-Dec)1

Spring

(Nov)2

Spring

(Dec) and

summer (Jan)2

Summer

(Feb and Mar)2

- 7-142

E. iheringii - - Spring

(Dec) and

Summer (Jan)4

Summer

(Jan and Feb) and

Autumn (Apr)3,4,5

- Winter

(Aug)5

10-183,4,5

(1) Barreto-Lima and Sousa (2006); (2) Sturaro and Silva (2010); (3) Marques and Sazima (2004); (4) Rautenberg and Laps (2010); (5) Present study.

Table 1. Timing of reproductive events recorded for Enyalius perditus and E. iheringii in the literature and present study.

averaging 24° C. Eight eggs spoiled over incubation period due to fungal contamination. Hatchings (n = 4) occurred between 23 and 28 August 2012, after an incubation period ranging from 143 to 148 days. One egg failed to hatch. This egg was dissected, and it contained one full-term dead embryo with a malformation in the tail. Hatchlings averaged 27.5 ± 3.5 mm SVL (range = 25–30 mm), 49.0 ± 8.5 mm TL (range = 43–55 mm), and 0.77 ± 0.01 g (range = 0.76–0.78 g).

There are no data on RCM for other Enyalius but the value observed here in E. iheringii is high and close to the upper limit observed in other lizards (Vitt and Price, 1982). In lizards, RCM and foraging modes are associated. RCM tends to be relatively low within species that forage actively, and relatively high within species using the “sit-and-wait” foraging mode (Vitt and Price, 1982). Since females of Enyalius species appears to be “sit-and-wait” foragers (Sousa and Cruz, 2008; Borges et al., 2013) and move shorter distances than males (Barreto-Lima et al., 2013), the high RCM value observed here in E. iheringii appears to be congruent with such association.

Estimates on gravidity period and clutch size available in the literature for Enyalius were largely obtained from dissection of preserved females (Rand, 1982; Vitt et al., 1996; Marques and Sazima, 2004; Rautenberg and Laps, 2010; Sturaro and Silva, 2010). This is the first report of egg size, incubation period, and hatchling size of an Enyalius species. Gravid females of E. iheringii were previously found in January and February (Table 1) suggesting that the species presents some reproductive seasonality (Marques and Sazima, 2004; Rautenberg and Laps, 2010; R. Rautenberg, pers. com.). Our observation of egg laying in April corroborates this assumption but suggests that oviposition may be further extended (at least to early autumn) than previously thought. Considering the period of encounter of gravid females of E. iheringii and our hatching report, recruitment appears to occur from autumn to mid-winter (Table 1).

The few information available for E. perditus and E. iheringii impair broad comparisons between species and definitive generalization on the timing of reproductive events. However, taken together our data and literature

Figure 2. (A) The female Enyalius perditus observed one night before the copulation attempt. (B) Detail of the female’s head highlighting the piece of skin in the head above the eye, indicating the process of shedding.

Reproductive aspects of two Enyalius lizards from the Atlantic forest 275

information indicate certain similarity between species, at least on the timing of vitellogenesis and gravidity (Table 1). However, gravidity period appears to extend further (to early autumn) in E. iheringii. Detailed studies are clearly needed to fully understand the reproductive cycles of these species and test this assumption.

Acknowledgements. We thank M. T. Rodrigues, F. F. Curcio, and V. J. Germano for taxonomic identification of the specimens, and R. Recoder for the critical reading and comments on the manuscript. We also thank R. Rautenberg, A. F. Barreto-Lima, and B. Rocha for information on Enyalius specimens, and A. Silveira for assistance with hatchlings. PAP (Programa de Aprimoramento Profissional) provided a fellowship to S. N. Migliore, and FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) to H. B. Braz (grant no. 2009/54478-3).

References

Aldridge, R.D., Duvall, D. (2002): Evolution of the mating season in the pitvipers of North America. Herpetological Monographs 16: 1-25.

Baird, T.A. (2004): Reproductive coloration in female collared lizards, Crotaphytus collaris, stimulates courtship by males. Herpetologica 60: 337-348.

Barreto-Lima, A.F., Sousa, B.M. (2006): Court and copulation behaviors of Enyalius perditus Jackson, 1978 (Squamata, Leiosauridae) in captivity conditions. Revista Brasileira de Zoociências 8: 193-197.

Barreto-Lima, A.F., Sousa, B.M. (2011): Feeding ecology and sexual dimorphism of Enyalius perditus in an Atlantic forest, Brazil. Herpetological Bulletin 118: 1-9.

Barreto-Lima, A.F., Pires, E.O., Sousa, B.M. (2013): Activity, foraging mode and microhabitat use of Enyalius perditus (Squamata) in a disturbed Atlantic rainforest in southeastern Brazil. Salamandra 49: 177-185.

Borges, V.S., Pires, R.C., Linares, A.M., Eterovick, P.C. (2013): Diet of Enyalius bilineatus (Leiosauridae: Squamata) at a site in southeastern Brazil: effects of phylogeny and prey availability. Journal of Natural History 47: 2785-2794.

Boulenger, G.A. (1885): Catalogue of the lizards in the British Museum (Natural History), 2nd Edition. London: British Museum (Natural History).

Frost, D.R., Etheridge, R., Janies, D., Titus, T.A. (2001): Total evidence, sequence alignment, evolution of Polychrotid lizards, and a reclassification of the Iguania (Squamata: Iguania). American Museum Novitates 3343: 1-38.

Grantsau, R. (1966): Enyalius catenatus, das Brasilianische “Cameleon”. Aquarien Terrarien Zeitschrift 19: 217-219.

Jackson, J.F. (1978): Differentiation in the genera Enyalius and Strobilurus (Iguanidae): implications for Pleistocene climatic changes in eastern Brazil. Arquivos de Zoologia 30: 1-79.

Marques, O.A.V., Almeida-Santos, S.M., Rodrigues, M.G., Camargo, R. (2009): Mating and reproductive cycle in the Neotropical colubrid snake Chironius bicarinatus. South American Journal of Herpetology 4: 76-80.

Marques, O.A.V., Sazima, I. (2004): História natural dos répteis da Estação Ecológica Juréia-Itatins. In: História Natural da Estação Ecológica Juréia-Itatins: Ambiente Físico, Flora e Fauna, p. 257-277. Marques, O.A.V., Duleba, W., Eds., Ribeirão Preto, Holos.

Mason, R.T., Gutzke, W.H.N. (1990): Sex recognition in the leopard gecko, Eublepharis macularius (Sauria: Gekkonidae). Possible mediation by skin-derived semiochemicals. Journal of Chemical Ecology. 16: 27-36.

Mason, R.T. (1992): Reptilian pheromones. In: Biology of the Reptilia, Volume 18, Physiology E, Hormones, Brain, and Behavior, p. 114–228. Gans, C., Crews, D., Eds., Chicago, The University of Chicago Press.

Rand, A.S. (1982): Clutch and egg size in Brazilian iguanid lizards. Herpetologica 38: 171-178.

Rautenberg, R., Laps, R.R. (2010): Natural history of the lizard Enyalius iheringii (Squamata, Leiosauridae) in southern Brazilian Atlantic forest. Iheringia Série Zoologia 100: 287-290.

Rodrigues, M.T., Freitas, M.A., Silva, T.F.S., Bertolotto, C.E.V. (2006): A new species of lizard genus Enyalius (Squamata, Leiosauridae) from the highlands of Chapada Diamantina, state of Bahia, Brazil, with a key to species. Phyllomedusa 5: 11-24.

Sousa, B.M., Cruz, C.A.G. (2008): Hábitos alimentares de Enyalius perditus (Squamata, Leiosauridae) no Parque Estadual do Ibitipoca, Minas Gerais, Brasil. Iheringia, Série Zoologia 98: 260-265.

Sturaro, M.J., Silva, V.X. (2010): Natural history of the lizard Enyalius perditus (Squamata: Leiosauridae) from an Atlantic forest remnant in southeastern Brazil. Journal of Natural History 44: 1225-1238.

Uetz, P. (2013): Enyalius, The Reptile Database. Available at: http://www.reptile-database.org. Last accessed on 19 September 2013.

Van Sluys, M., Ferreira, V.M., Rocha, C.F.D. (2004): Natural history of the lizard Enyalius brasiliensis (Lesson, 1828) (Leiosauridae) from an Atlantic forest of southeastern Brazil. Brazilian Journal of Biology 64:353-356.

Vitt, L.J., Price, H.J. (1982): Ecological and evolutionary determinants of relative clutch mass in lizards. Herpetologica 38: 237-255.

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.

Zamprogno, C., Zamprogno, M.G.F., Teixeira, R.L. (2001): Evidence of terrestrial feeding in the arboreal lizard Enyalius bilineatus (Sauria, Polychrotidae) of south-eastern Brazil. Revista Brasileira de Biologia 61: 91-94.

Serena Najara Migliore et al.276

Accepted by Diogo Provete; Managing Editor: Diogo Provete