Herpetology Notes, volume 12: 447-451 (2019) (published online on 01 May 2019)

Reproductive mode and defensive behaviour of the South American aquatic snake Helicops pastazae (Serpentes: Dipsadidae)

Daniela García-Cobos1,2 ,* and Diego A. Gómez-Sánchez1

Helicops (Wagler, 1830) is a genus of aquatic snakes it is only known from its original description (Shreve, restricted to South America, it occurs between northern 1943), a re-description (Rossman, 1976), one recently Colombia to northern Argentina (Uetz et al., 2018). published dietary study (Almendáriz et al., 2017), and This group is characterized by presenting keeled several checklists (Pérez-Santos and Moreno, 1988; dorsal scales, one internasal scale, as well as dorsally Rivas et al., 2012; Pedroza-Banda et al., 2014; Wallach positioned eyes and nostrils due to their aquatic habitat et al., 2014). Although both Feldman et al. (2015) and (Segall et al., 2016). This genus presents both oviparous Uetz et al. (2018) report this species as viviparous, (egg-laying) and viviparous (live-bearing) species none of them provide any source that corroborates this (Greer, 1966). Of the 17 known species of the genus, statement. In addition, a detailed literature revision did nine are viviparous [H. carinicaudus (Wied-Neuwied, not allow us to find any published conclusive studies nor 1825), H. danieli Amaral, 1938, H. infrataeniatus Jan, observations supporting either reproductive mode for 1865, H. leopardinus (Schlegel, 1837), H. modestus this species. Furthermore, other aspects of the natural Günther, 1861, H. nentur, Costa et al., 2016, H. polylepis history of H. pastazae such as the defensive behaviour Günther, 1861, H. scalaris Jan, 1865, and H. trivittatus when threaten remains unknown, although a variety of (Gray, 1849)], two are oviparous (H. gomesi Amaral, defensive displays are common within different species 1921 and H. hagmanni Roux, 1910), and one presents of snakes (Greene, 1979). Here, we report for the first both reproductive modes [H. angulatus (Linnaeus, time the reproductive mode of H. pastazae as well as its 1758)] (Braz et al., 2016; see also Costa et al., 2016). defensive behaviour based on observations made both No information regarding the reproductive mode is in the field and in captivity. available for the remaining five species (H. pastazae Observations on the reproductive mode and defensive Shreve, 1943, H. apiaka Kawashita-Ribeiro et al., 2012, behaviour of H. pastazae were carried out in the Batá H. petersi Rossman, 1976, H. tapajonicus Frota, 2005, River in the municipality of Santa María, Boyacá, and H. yacu, Rossman and Dixon, 1975) (Braz et al., Colombia (4.857694°N, 73.265389°W, 800 m a.s.l.). 2016). While surveying exposed riverbed rocks at the margin Helicops pastazae is distributed from Peru to Venezuela of the Batá River on 20 December 2016 (early dry along the eastern Andean foothills (Rossman, 1976). season), we found a clutch of 11 eggs. These eggs This is one of the least studied species within the genus; were buried under a substratum composed of sand, small rocks and decomposing material located under a large rock separated about two meters from the edge of the river (Fig. 1A). Of the 11 eggs found, two were immediately fixed in formaldehyde (10%), one was attacked by ants and therefore did not contain a viable 1 Museo de Historia Natural ANDES, Departamento de Ciencias embryo. The remaining eight eggs were transported to Biológicas, Facultad de Ciencias, Universidad de los Andes. a residency in Bogotá in a plastic canister containing Apartado Aéreo 4976, Bogotá, Colombia. the same substratum in which they were found. Once 2 Instituto de Investigación de Recursos Biológicos, Alexander von Humboldt, Colecciones Biológicas, Villa de Leyva, in Bogotá, the eight eggs were relocated to a constantly Boyacá, Colombia. humid and ventilated terrarium under a heat lamp that * Corresponding author. E-mail: [email protected] maintained the mean temperature of about 20°C. 448 Daniela García-Cobos & Diego A. Gómez-Sánchez

Figure 1. (A) A clutch of 11 eggs of H. pastazae found in the field at the margin of the Batá River, Boyacá, Colombia under a large rock partly buried under sand and decomposing material. (B) New-born peaking its snout out through a small incision opened during the hatching.

We checked the eggs daily until the first hatching, found the individual around 10:00 a.m. in a resting which occurred during the night of 4 February 2017, 46 position under rocks at the edge of the Batá River. We days after the eggs were collected. Twenty-four hours manually relocated the individual from its shelter to later, the second and third individual began hatching approximately one meter apart from the river border, at night. However, the individuals did not completely and as we prevented the initial behaviour of the adult emerge from the eggs. Instead, the hatchlings continued female to escape to the river, it displayed an aggressive moving inside the egg constantly peeking out their behaviour by opening its mouth, expanding the head snout through a small incision for 19 hours, until they in a triangular shape, dorsally-ventrally flattening the emerged from the eggs. On 7 February 2017, three first third part of the body and by expelling a foul odour neonates slit the shells of their eggs and performed the from its cloacal glands (Fig. 2A, B). This display was same behaviour previously mentioned (Fig. 1B). This repeated three times during the encounter, each one behaviour was also exhibited by the seventh neonate lasting for about four seconds. During the entire time of that hatched on the night of 9 February, 2017. The the display, the snake raised and retracted back and forth remaining egg did not hatch and was probably infertile, as its interior was found desiccated, lacking any organic material. All of the seven neonatesTable were 1. Sex, euthanized snout-vent length (SVL), tail length (TL), and total length of seven hatchlings immediately after hatching, and the snout-vent length Table 1. Sex, snout-vent length (SVL), tail length (TL), and total length of seven hatchlings of Helicops pastazae born in (SVL) and tail length (TL) were measuredof Helicops with pastazae a ruler. born in captivity. Measurements are in mm. captivity. Measurements are in mm. Individuals were sexed by making a ventral longitudinal incision throughout the tail to detect the presence of hemipenis. The SVL of the hatchlings varied from 109 Sex SVL TL Total Length to 135 mm (x = 123.8 ± 10.7 mm, n = 7), and the TL Female 135 22 157 varied between 22 and 60 mm (x = 45.4 ± 11.9 mm, Female 132 50 182 n = 7) (Table 1). The sex ratio of the hatchlings was 2:5 (male:female). All specimens were deposited in the Female 109 40 149 reptile collection (ANDES-R) of the Museo de Historia Female 134 51 185 Natural, Universidad de los Andes, Bogotá, Colombia. Female 120 45 165 Additionally, we report the defensive behaviour Male 111 50 161 exhibited in situ by an adult female of H. pastazae, Male 126 60 186 observed in the field on 26 September, 2016. We

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Reproductive mode and defensive behaviour of Helicops pastazae 449

Figure 2. Defensive behaviour of Helicops pastazae. (A) Expansion of the head in a triangular shape while dorsally-ventrally flattening the first third part of the body. (B) Aggressive behaviour consisting in mouth opening and trying to strike the threat source.

the first part of the body and never took off its vision 25, x =10.2; De Aguiar and Di-Bernardo, 2005), H. from the source of threat. modestus (24; Da Silva and Travaglia-Cardoso, 2015), Reproductive mode is a major life-history component and H. angulatus (4-20; Martins and Oliveira, 1998; that can shape reproductive ecology. It is necessary to Ford and Ford, 2002). On the other hand, hatchling evaluate morphological characteristics of the eggs/ SVL is similar to that of many other congeneric such embryos and behavioural observations of parturition of as H. leopardinus (106-139 mm; Ávila et al., 2006), H. neonates or oviposition of the eggs, either in the field or in infrataeniatus (106-151 mm, x =129.4 mm; De Aguiar captivity, in order to reliably determine the reproductive and Di-Bernardo, 2005), H. modestus (120-160 mm, x mode of a given species (Blackburn, 1993). Our finding = 146 mm; Da Silva and Travaglia-Cardoso, 2015), and of a clutch of eggs composed of thick and opaque H. angulatus (x =139 mm; Ford and Ford, 2002). eggshells and the hatching of young approximately two The defensive behaviour observed for the adult months after the encounter provide conclusive evidence female of H. pastazae has been previously reported for to classify this population of H. pastazae as oviparous several other snake species. Among the aquatic snakes, (Blackburn, 1993; Braz et al., 2016). Even so, we cannot H. angulatus, H. carinicaudus, H. danieli and some determine this species as completely oviparous by only species of the genus Nerodia (Linnaeus, 1758) present using this single observation as it has been reported that a similar defensive repertoire (Scudder and Burghardt, at least one species of Helicops (H. angulatus) presents 1983; Martins and Oliveira, 1998, Marques & Sazima, reproductive bimodality, meaning that it present both 2004). Additionally, more distantly related species of viviparous and oviparous populations (Ford and Ford, neotropical Dipsadidae snakes such as Ninia atrata 2002; Braz et al., 2018). However, neither oviparity or (Hallowell, 1845), Dipsas sanctijoannis (Boulenger, bimodality are commonly found in Helicops and our 1911), Xenodon dorbignyi (Bibron, 1854), and Xenodon observation is an important contribution to categorizing severus (Linnaeus, 1758), among other species, exhibit a the reproductive mode of H. pastazae, as well as for similar behaviour when threatened (Tozetti et al., 2009; understanding the evolution of viviparism within the Kahn, 2010; Morales and Lasso, 2010; Angarita-Sierra, genus and can be helpful in future studies concerning 2015). The display of dorsally-ventrally flattening the viviparism in Squamates. body and positioning the head in a triangular shape has This single observation of the clutch size of H. an effect in increasing the apparent size of the individual pastazae is similar to that of H. leopardinus (4–11; Ávila and it is also used in order to imitate venomous pit et al., 2006) but fewer than that of H. infrataeniatus (1- vipers (Greene, 1979). Since this type of defensive 450 Daniela García-Cobos & Diego A. Gómez-Sánchez display is present in many distantly related species Brazil. Amphibia-Reptilia 26: 527–533. inhabiting different environments, it may have evolved Feldman, A., Bauer, A.M., Castro-Herrera, F., Chirio, L., Das, I., by convergence in various lineages (Greene, 1979). Doan, T.M., Erez, M., Meirte, D., Campos-Nogueira, C., Nagy, Z.T., Torres-Carvajal, O.M., Uetz, P., Meiri, S. (2015). The Unfortunately, field observations and studies of natural geography of snake reproductive mode: a global analysis of the history have strongly declined over the last decade evolution of snake viviparity. Global ecology and biogeography (Tewksbury et al., 2014), highlighting the importance of 24: 1433–1442. our contribution regarding the reproductive mode and Ford, N.B., Ford, D.F. (2002): Notes on the ecology of the defensive behaviour of Helicops pastazae. South American water snake Helicops angulatus (Squamata: Colubridae) in Nariva Swamp, Trinidad. Caribbean Journal of Acknowledgments. We would like to thank Henrique B. Braz Science 38: 129–132. and Juan Pablo Ramírez for their useful comments and corrections Greene, H.W. (1979): Behavioural convergence in the defensive to this work and to the herpetological group of Museo ANDES for displays of snakes. Experientia 35: 747–748. their encouragement and passion toward studying the snakes of Greer, A.E. 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Accepted by Anamarija Zagar