Herpetology Notes, volume 11: 429-431 (2018) (published online on 09 May 2018)

The Defensive Behaviour of Tzabcan , tzabcan Klauber, 1952 (: )

Rubén Alonso Carbajal-Márquez1,3,*, J. Rogelio Cedeño-Vázquez1, Christian M. García-Balderas1,3, Tania Ramírez-Valverde1 and Gustavo Ernesto Quintero-Díaz2,3

Interactions between prey and predator are key with : C. atrox (Cowles, 1977; Meinzer, elements of a natural history, and this knowledge 1993; Cornett, 2001; Sherbrooke and Westphal, 2006), C. contributes to the development of evolutionary biology viridis (Duvall et al., 1985; Alcock, 1998), and C. ruber and ecological studies. Therefore, antipredator (Rubio, 1998). Medica (2009) recorded head-hiding and behaviours are important factors in the evolutionary saltation as defensive behaviours of a male C. scutulatus processes of many , and they are intrinsically scutulatus from and head-hiding of a female associated with survivorship, increasing capacity to specimen from . This of saltation behaviour obtain resources, and exploitation of the environment was also documented for C. s. scutulatus from , (Lima and Dill, 1990; Downes, 2001; Tozetti et and C. s. salvini from Puebla and Veracruz (Armstrong al., 2009). Given their unique tail morphology and and Murphy, 1979; Bartholomew and Nohavec, 1995). that they are venomous, rattlesnakes have attracted considerable attention regarding defence mechanisms in Neck flattening is another type of defensive behaviour . Besides the rattle, several additional defensive that has been reported for both sexes of C. scutulatus mechanisms are displayed by rattlesnakes, such as salvini and a male of C. s. scutulatus, where the neck hissing, body posture, scent glands, and extended (immediately posterior to the head) spreads laterally and protraction of the tongue as a warning signal (Campbell the cervical spine is straight and aligned with the head and Lamar, 2004). A few species (e.g., Crotalus molossus (Glenn and Lawler, 1987; Brown et al., 2000). Neck and C. polystictus) also use an open-mouth threat or flattening is different from the body flattening observed move the head in a provocative way (Armstrong and in C. s. scutulatus in which an adult flattens its head and Murphy, 1979; Campbell and Lamar, 2004). trunk against the substrate and elevates its tail without rattling, and also differs from the bloating of the neck One additional defensive behaviour is head or body regions recognized as stereotyped behaviour in concealment, which also occurs in a number of unrelated several rattlesnakes including C. scutulatus (Armstrong non-venomous and venomous snakes (Bustard, 1969; and Murphy, 1979; Glenn and Lawler, 1987). Whereas, Greene, 1973), and has been documented in several in C. durissus a dorso-ventral flattening has been instances as a result of human or predator interactions documented (Benicio and Martins, 2018).

The Tzabcan rattlesnake, Crotalus tzabcan, is a large (up to 1600 mm), endemic to the Yucatán Peninsula (Lee, 1996). Despite the relatively wide distribution of 1 El Colegio de la Frontera Sur, Departamento de Sistemática C. tzabcan, little is known about its Natural History and y Ecología Acuática, Unidad Chetumal, Avenida Centenario behaviour. Campbell (1998) described the defensive Km 5.5, 77014, Chetumal, Quintana Roo, México posture in specimens from Belize and El Petén 2 Universidad Autónoma de Aguascalientes, Centro de (Guatemala) as dramatic, with almost half of the anterior Ciencias Básicas, Departamento de Biología, C.P. 20131, body raised off the ground and held vertically with the Aguascalientes, Aguascalientes, México 3 Conservación de la Biodiversidad del Centro de México, neck curved into a sharp crook with the head facing the A.C. Andador Torre de Marfil No. 100, C.P. 20229, adversary. While the posterior part of the body is in a Aguascalientes, Aguascalientes, México large, open coil, except for the tail and rattle, which are * Corresponding author. E-mail: [email protected] raised vertically, in about the centre of the coil. 430 Rubén Alonso Carbajal-Márquez et al.

Figure 1. Defensive behaviour of a juvenile Crotalus tzabcan at Chichén-Itzá, Yucatán, México: A) displaying a complete head hiding, body flattening, and coiling behaviour; B) displaying a neck flattening behaviour. Photos by Rubén A. Carbajal- Márquez.

While conducting a study on C. tzabcan autecology, elevated the body or attempted to bite, and always we found a juvenile male (snout–vent length 680 mm, facing directly toward us. Two additional juveniles tail length 55 mm) moving in leaf litter of dry forest from the vicinity of Chetumal, Quintana Roo, , near Chichén-Itzá, Yucatán, Mexico (20.678925° N, - were observed performing the same neck flattened 88.567719° W, WGS84, 35 m a.s.l.) on 15 July 2015. behaviour. When we approached to take pictures, the snake coiled, flattened its body and hid its head in the centre of its When threatened, rattlesnakes typically rely on crypsis coil, but without rattling, and remained in this position before mounting behavioural defences (Putman and approximately three minutes before beginning to move Clark, 2015). To humans, crypsis in rattlesnakes (e.g., again (Fig. 1A). When we relocated the snake and miliarius) is less effective when the snake is positioned it to take additional photos, it spread the neck stretched out and moving, and the rattlesnake is more immediately posterior to the head several times (Fig. likely to respond defensively when is encountered 1B) and then flattened the rest of its body against the stretched out on open trail than when coiled. However, substrate while backing up without rattling, or without it must also be taken into account that intrinsic factors The Defensive Behaviour of Tzabcan Rattlesnake 431

(e.g., body temperature, size, experience) affect the Crotalus durissus Linnaeus, 1758. Herpetozoa 30: 217–218. defensive response (Glaudas, 2004; Glaudas et al., Brown, J.F.W., Marden, W.M., Hardy, D.L. (2000): Natural History 2005). When finding the juvenile C. tzabcan moving Notes: Crotalus scutulatus scutulatus (Mojave Rattle-snake). Defensive Behavior. Herpetological Review 31: 45. in the leaf litter in a stretched out position, it seems Bustard, H.R. 1969. Defensive behavior and locomotion of that it influenced to display non-aggressive defensive the Pacific boa, aspera, with a brief review of head behaviour, being less perceptible by not rattling; or it concealment in snakes. Herpetologica 25: 164–170. could have been influenced by previous experiences Campbell, J.A. (1998): Amphibians and of Northern with humans since Chichén-Itzá is a tourist site. It has Guatemala, Yucatán, and Belize. Norman, USA, University of been documented in other pitvipers like Agkistrodon Press, piscivorus, that they habituate to handling by humans Campbell, J.A., Lamar, W.W. (2004): The Venomous Reptiles of the Western Hemisphere., Ithaca and London. Comstock. and their behavioural responses become increasingly Cornett, J.W. (2001): The Roadrunner. Palm Springs, USA, Nature passive (Glaudas, 2004). Trails Press. Cowles, R.B. (1977): Journal: A Naturalist Reflects on Arid Head concealing behaviour and remaining in this California. Berkeley, USA, University of California Press. position for a prolonged period of time may be a Downes, S. (2001): Trading heat and food for safety: costs of mechanism to avoid direct head injuries by predators. predator avoidance in a . Ecology 82: 2870–2881. Duvall, D., King, M.B., Gutzwiller, K.J. (1985): Behavioral ecology Head flattening followed by body flattening, is not and ethology of the prairie rattlesnake. National Geographic unique to rattlesnakes, and may function to create the Research 1: 80–111. illusion that a snakes is larger than it actually is, causing Glaudas, X. (2004): Do Cottonmouths (Agkistrodon piscivorus) a predator to misjudge its ability to subdue its prey habituate to human confrontations? Southeastern Naturalist 3: (Tozetti et al., 2009). This neck and body flattening 129–138. display, along with head hiding described above for Glaudas, X., Farrell, T.M., May, P.G. (2005): Defensive behavior C. tzabcan, appear to be defensive behaviours and of free-ranging Pigmy rattlesnake (Sistrurus miliarius). Copeia 2005: 196–200. probably have important survival value, particularly in Glenn, J.L., Lawler H.E. (1987): Natural History Notes: Crotalus juvenile specimens, since many predators direct their scutulatus salvini (Huamantlan Rattlesnake). Behavior. attack specifically at the heads of snakes (Bustard, 1969; Herpetological Review 18: 15–16. Greene, 1973). The knowledge of Greene, H.W. (1973): Defensive Tail Display by Snakes and defensive behaviour is limited,��������������������� with the majority of Amphisbaenians. Journal of 7: 143–161. these behaviours only described as anecdotes (Glaudas, Lee, J.C. (1996): The Amphibians and Reptiles of the Yucatán 2004). Further research is necessary to understand Peninsula. Ithaca, USA, Comstock Publishing Associates, Cornell University Press. how pitvipers react to predators, including human Lima, S.L., Dill, L.M. (1990): Behavioral decisions made under the confrontations. Since field experiments are commonly risk of predation: a review and prospectus. Canadian Journal of logistically difficult, greater understanding maybe can Zoology 68: 619–640. be achieved by future research in field with species with Medica, P.A. (2009): Crotalus scutulatus scutulatus (Mojave large populations and in laboratory in the case of rare Rattlesnake). Defensive behavior/ saltation and head hiding. species. 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