Herpetology Notes, volume 11: 349-351 (2018) (published online on 02 May 2018)

Predation of Conepatus chinga (Molina, 1782) (Carnivora, Mephitidae) by Salvator merianae (Duméril and Bibron, 1839) (Squamata, Teiidae) in a field area of the state of Rio Grande do Sul, Brazil

Renata Cardoso Vieira¹,*, Arthur Schramm de Oliveira¹, Nelson Jurandi Rosa Fagundes² and Laura Verrastro¹

The Molina’s hog-nosed skunk, Conepatus chinga Gallardo, 1984; Winck et al., 2011). It is a terrestrial and (Molina, 1782), is one of the smallest carnivores of diurnal species; its activity varies seasonally (Van Sluys the State of Rio Grande do Sul (Trigo et al., 2013), and Rocha, 1999), with individuals more active on and belongs to the suborder Caniformia and family November and December. The species prefers refuges Mephitidae. Its average body length is 41 cm and near human constructions and males are territorial tail length is 15 cm, while the body mass varies from (Winck et al., 2011). The species is omnivorous, 1.5 kg to almost 3 kg, as males are larger and heavier including invertebrates, eggs, carcasses, plants and than females (Trigo et al., 2013). It differs from other fruits (Kiefer and Sazima, 2002; Péres Júnior, 2003; carnivores by the body structure, with short legs and Castro and Galetti, 2004). Small-sized vertebrates, such stocky body; it also presents a defence mechanism that as mammals with less than 1 kg, were also identified as consists of a pair of anal scent glands that secrete a fluid part of food items of the species (Vitt, 1995; Kiefer and with noxious odour (Nowak, 1999). It inhabits mainly Sazima, 2002; Péres Júnior, 2003; Castro and Galetti, open field habitats (Trigo et al., 2013) and seems to 2004). Here we report a predation event of C. chinga by tolerate disturbed environments (Kasper et al., 2009). S. merianae in an open area of the Brazilian Pampa in The species’ activity is mainly nocturnal and use more southern Brazil. frequently soil holes to rest (Kasper et al., 2012). During studies at Estação Experimental Agronômica da The black-and-white-tegu lizard, Salvator merianae Universidade Federal do Rio Grande do Sul (Agronomic (Duméril and Bibron, 1839), is a native species Experimental Station of the Federal University of Rio widely distributed in South America that belongs to Grande do Sul), in the municipality of Eldorado do the family Teiidae. It may reach 1.2 m of total length Sul (30º5’9.49 “S and 51º40’56.79” W), in Brazilian and weight over 4.5 kg (Fitzgerald, 1992). It presents Pampa, a predation event of C. chinga by S. merianae sexual dimorphism, as males are larger than females was recorded on October 23rd, 2014, between 1:48 and and have hypertrophied pterygomandibular muscles, 2:20 pm. which results in a more conspicuous jowl (Donadio and We were studying the population of S. merianae at the time of observation to obtain other ecological aspects. Because this we did not collect the specimen. The event occurred in a wooded area near the burrow used by an individual of S. merianae (30º 5’ 9.49” S; 51º 40’ 56.79” ¹ Departamento de Zoologia, Universidade Federal do Rio W), and was recorded using a digital camera Sony DSC- Grande do Sul. Avenida Bento Gonçalves 9500, Prédio H9 8.1 Megapixels, with 15x optical zoom. Image were 43435, sala 102, Agronomia, 91501-970 Porto Alegre, RS, deposited at the Coleção Herpetológica da Universidade Brazil. Federal do Rio Grande do Sul (Herpetological ² Departamento de Genética, Universidade Federal do Rio Grande do Sul. Avenida Bento Gonçalves 9500, Prédio Collection of the Federal University of Rio Grande 43312, sala 113, Agronomia, 91501-970 Porto Alegre, RS, do Sul - UFRGS) as a digital file (UFRGS 7472). The Brazil. lizard was an adult male identified through sexual * Corresponding author. E-mail: [email protected] dimorphism (see Winck et al., 2011). It maintained 350 Renata Cardoso Vieira et al.

species interact agonistically disputing space resources. Diet is an essential and dynamic component of biological communities that may generate interactions between coexisting species (Duffield and Bull, 1998; Huang, 2010; Juri et al., 2015), being considered one of the main components of interactions between species (Pianka, 1982). Salvator merianae can be considered an omnivore and opportunistic predator that feeds on any resources available in the environment, even if these are not common components of its diet, such as invertebrates, eggs, carcasses, plants and fruits (Kiefer and Sazima, 2002; Péres Júnior, 2003; Castro and Galetti, 2004). The event described here indicates that the diet of S. merianae can comprise not only small, Figure 1. Adult male of Salvator merianae feeding on but also medium-sized mammals, even though this Conepatus chinga at the municipality of Eldorado do Sul, consumption may be occasional and opportunistic. State of Rio Grande do Sul, Brazil. Photo: Arthur Schramm. However, significant associations between body size and prey dimensions have been reported for lizards (Van Sluys et al., 2004). Females of S. merianae, for example, complement their diets with larger preys, such the skunk in the mouth, trapped by the dorsal region as mammals (Juri et al., 2015). Colli and collaborators of the head, and hit the prey on the ground by turning report that S. merianae and S. rufescens tend to consume the head (Figure 1). The lizard bit and let the prey go more organic matter (fruits) and vertebrates compared to several times, while the skunk tried to escape at every closely related species (Tupinambis cerradensis and T. new advance of the lizard. After the skunk stopped longilineus) with smaller body size (Colli et al., 1998). moving for several seconds (more than 30 seconds), it The reproductive behaviour is another key factor that was verified that the skunk was dead assumed through may influence the feeding habit (Juri et al., 2015). The visual observation. When the lizard noted the presence predation reported here occurred in the reproductive of the observer, it interrupted the predation behaviour period (October), suggesting that the increase of and began to move towards its burrow, carrying the energetic need after hibernation (March – August; prey (Figure 2). During the movement, the lizard stopped several times within bushes, releasing the prey, waiting for some time (about 30 to 40 seconds), snatching the prey again and resuming the movement to the burrow. The lizard managed to enter the burrow, which consisted of an abandoned water pipe, taking the prey that was still intact, and started feeding inside it. The entire predation event recorded (from the death of the skunk until the movement of the lizard inside the burrow) lasted approximately 32 minutes. At 5:04 pm of the same day we returned to the burrow and it was possible to observe that the lizard was still ingesting the prey. Two days after this predation event (October 25th, 2014), at the same study area, we observed an individual of S. merianae and a skunk fighting for a burrow. In this situation there was no predation, but the lizard remained in the burrow after driving the skunk away. It should also be noted that skunks can also include Figure 2. Adult male of Salvator merianae carrying an small reptiles in their diet (Kasper et al 2016), including individual of Conepatus chinga to its burrow at the municipality young S. merianae (personal communication, Kasper, of Eldorado do Sul, State of Rio Grande do Sul, Brazil. Photo: C.B.). Both mentioned behaviours emphasize that these Arthur Schramm. Predation of Conepatus chinga by Salvator merianae in Brazil 351

Winck and Cechin, 2008) and during the reproductive 2435.2010.01776.x period (September – December; Winck et al., 2011) Huang, W.S. (2010): Foraging behaviors of two sympatric could also explain the occasional predation of a larger ant species in response to lizard eggs. Zoology 113: 85-90. doi:10.1016/j.zool.2009.06.003 prey. On the other hand, it is important to highlight Kasper, C.B., Peters, F.B., Christoff, A.U., Freitas, T.R. (2016): that the energetic advantage could be counterbalanced Trophic relationships of sympatric small carnivores in by the associated risk of injuries that such prey can fragmented landscapes of southern Brazil: niche overlap and cause. Besides, the predation could be an opportunistic potential for competition. Mammalian https://doi.org/10.1515/ consequence of a dispute for shelter, once we recorded mammalia-2014-0126. both species fighting for the same space. Therefore, the Kasper, C.B., Soares, J.B.G., Freitas, T.R.O. (2012): Differential trade-off between capturing a larger prey available in patterns of home-range, net displacement and resting sites use of Conepatus chinga in southern Brazil. Mammalian Biology, the environment and not several smaller preys can be 77(5), 358–362. http://doi.org/10.1016/j.mambio.2012.03.006 a fundamental factor for the occasional predation of C. Kasper, C.B., Fontoura-Rodrigues, M.L., Cavalcanti, G.N., Freitas, chinga by S. merianae to occur. T.R.O., Rodrigues, F.H.G., Oliveira, T.G., Eizirik, E. (2009): In addition, the use of soil holes by both species Recent advances in the knowledge of Molina’s Hognosed Skunk coinciding with the fact that S. merianae is active Conepatus chinga and Striped Hog-nosed Skunk C. semistriatus throughout the day (Van Sluys and Rocha, 1999), a in South America. Small Carnivore Conservation 41: 25–28. period that the skunk has little activity (Kasper et al., Kiefer, M.C., Sazima, I. (2002): Diet of juvenile tegu lizard Tupinambis merianae (Teiidae) in southeastern Brazil. 2012), makes the last more susceptible prey. This record Amphibia-Reptilia 23: 105-108. of predation highlights that S. merianae can predate a Nowak, R.M. (1999): Walker’s mammals of the world. Baltimore: medium-sized mammal during the reproductive period. The Johns Hopkins University Press, v. 1, 517p. Péres Junior, A.K. (2003): Sistemática e conservação do gênero References Tupinambis (Squamata, Teiidae). Tese Doutorado, Universidade de Brasília, 192p. Bergamaschi, H., Guadagnin, M.L. (1990): Agroclima da Estação Pianka, E.R. (1982): Ecologia evolutiva. Barcelona, Omega, 365p. Experimetal Agronômica. Porto Alegre, Departamento de Trigo, T.C., Rodrigues, M.L.F., Kasper, C.B. (2013): Carnívoros Plantas Forrageiras e Agrometereologia, Continentais. In: Mamíferos do Rio Grande do Sul, pp.343-377. Castro, E.R., Galetti, M. (2004): Frugivoria e dispersão de sementes Weber, M.M., Roman, C., Cáceres, N.C. Ed., UFSM, Santa pelo lagarto teiú Tupinambis merianae (Reptilia: Teiidae). Maria. Papéis Avulsos de Zoologia São Paulo 44 (6): 91 – 94. Winck, G.R. (2007): História natural de Tupinambis merianae Colli, G.R., Péres-Jr, A.K., Cunha, H.J. (1998): A new species (Squamata, Teiidae) na Estação Ecológica do Taim, Extremo of Tupinambis (Squamata: Teiidae) from Central Brazil, with Sul do Brasil. Universidade Federal de Santa Maria. analysis of morphological and genetic variation in the genus. Winck, G., Cechin, S. (2008): Hibernation and emergence pattern Herpetologica 54 (4): 477-492. of Tupinambis merianae (Squamata: Teiidae) in the Taim Donadio, O.E., Gallardo, J.M. (1984) Biología y conservación de Ecological Station, southern Brazil. Journal of Natural History las especies del género Tupinambis (Squamata, Sauria, Teiidae) 42 (3): 239-247. en la República Argentina. Revista del Museo Argentino de Van-sluys, M., Rocha, C.F.D. (1999): Tupinambis merianae Ciencias Naturales Bernardino Rivadavia 13:117–127. (Common Tegu) Activity. Herpetologica Review 30 (1): 42–43. Duffield, G.A., Bull, C.M. (1998): Seasonal and ontogenetic Van-sluys, M., Ferreira, V.M., Rocha, C.F.D. (2004): Natural changes in the diet of the Australian skink Egernia stokesii. history of lizard Enyalius brasiliensis (Lesson, 1828) Herpetologica 54: 414-419. (Leiosauridae) from an Atlantic Forest of southeastern Brazil. Fitzgerald, L.A. (1992): La Historia Natural de Tupinambis. Brazilian Journal of Biology 64: 353-356. doi: 10.1590/S1519- Revista UNA, Universidad Nacional de Asunción, Paraguay 3 69842004000200021 (3): 71–72. Vitt, L.J. (1995): The ecology of tropical lizards in the Caatinga of González-Suárez, M., Mugabo, M., Decenciere, B., Perret, S., northeast Brazil. Occasional Papers of the Oklahoma Museum Claessen, D., Galliard, J.F. (2011): Disentangling the effects of of Natural History 1: 1-29. predator body size and prey density on prey consumption in a lizard. Functional Ecology 25: 158-165. doi:10.1111/j.1365-

Accepted by Mirco Solé