Abstracts

Introduction

Predation constitutes one of the major pressures negatively affecting natural populations. In context of lizards, the predation by a sympatric lizard and even by the same species represent two important sources of mortality (Vitt 2000VITT, L.J. 2000. Ecological consequences of body size in neonatal and small-bodied lizards in the Neotropics. Herpetol. Monogr. 14:388-400., Siqueira & Rocha 2008SIQUEIRA, C.C. & ROCHA, C.F.D. 2008. Predation by lizards as a mortality source for juvenile lizards in Brazil. South Am. J. Herpetol. 3:82-87, 10.2994/1808-9798(2008)3[82:PBLAAM]2.0.CO;2.
https://doi.org/10.2994/1808-9798(2008)3... ). At first glance, the incidence of these kind of predatory events appeared to be infrequent, but cases of saurophagy and cannibalism among lizards are increasingly documented (Pincheira-Donoso 2012PINCHEIRA-DONOSO, D. 2012. Intraspecific predation in theLiolaemus lizard radiation: a primer. Anim. Biol. 62:277-287, 10.1163/157075611X618219.
https://doi.org/10.1163/157075611X618219... , Robbins et al. 2013ROBBINS, T.R., SCHREY, A., MCGINLEY, S. & JACOBS, A. 2013. On the incidences of cannibalism in the lizard genus Sceloporus: updates, hypotheses, and the first case of siblicide. Herpetol. Notes 6:523-528.).

Lizards of the genus Tropidurus are known to be ambush foragers with opportunistic feeding habits. Although their diet is primarily composed of arthropods, several species also feed on plant itens as well small vertebrates (Faria & Araújo 2004FARIA, R.R. & ARAÚJO, A.F.B. 2004. Syntopy of twoTropidurus lizard species (Squamata: Tropiduridae) in a rocky Cerrado habitat in Central Brazil. Braz. J. Biol. 64:775-786, 10.1590/S1519-69842004000500007.
https://doi.org/10.1590/S1519-6984200400... , Van Sluys et al. 2004VAN SLUYS, M., ROCHA, C.F.D., VRCIBRADIC, D., GALDINO, C.A.B. & FONTES A.F. 2004. Diet, activity and microhabitat use of two syntopicTropidurus species (Lacertilia: Tropiduridae) in Minas Gerais, Brazil. J. Herpetol. 38:606-611., Kolodiuk et al. 2010KOLODIUK, M.F., RIBEIRO, L.B. & FREIRE, E.M.X. 2010. Diet and foraging behavior of two species of Tropidurus (Squamata, Tropiduridae) in the Caatinga of northeastern Brazil. South Am. J. Herpetol. 5:35-44, 10.2994/057.005.0104.
https://doi.org/10.2994/057.005.0104... ). Among the vertebrate preys ofTropidurus, there are consumption records of mammals (Gasparini & Peloso 2007GASPARINI, J.L. & PELOSO, P.L. 2007. Tropidurus torquatus (Brazilian Collared Lizard). Diet. Herpetol. Rev. 38:464.), frogs (Vitt et al. 1996VITT, L.J., ZANI, P.A. & CALDWELL, J.P. 1996. Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia. J. T. Ecol. 12:81-101, 10.1017/S0266467400009329.
https://doi.org/10.1017/S026646740000932... , Kiefer et al. 2006KIEFER, M.C., SIQUEIRA, C.C., VAN SLUYS, M. & ROCHA, C.F.D. 2006. Tropidurus torquatus (Collared Lizard, Calango). Prey. Herpetol. Rev. 37:475-476., Ribeiro & Freire 2009RIBEIRO, L.B. & FREIRE, E.M.X. 2009. Tropidurus hispidus (NCN). Frog predation. Herpetol. Rev. 40:228-228., Costa et al., 2010COSTA, J.C.L., MANZANI, P.R., BRITO, M.P.L. & MACIEL, A.O. 2010.Tropidurus hispidus (Calango). Prey. Herpetol. Rev. 41:87.), but mainly of lizards. For instance, saurophagy was reported forT. hispidus (Spix, 1825) (Rojas-Runjaic et al. 2006ROJAS-RUNJAIC, F.J.M., FERRER, A., RIVAS, G.A. & MONTERO, Z.A. 2006. Tropidurus hispidus. Saurophagy. Herpetol. Rev. 37:474., Costa et al. 2010COSTA, J.C.L., MANZANI, P.R., BRITO, M.P.L. & MACIEL, A.O. 2010.Tropidurus hispidus (Calango). Prey. Herpetol. Rev. 41:87., Zanchi et al. 2012ZANCHI, D., PASSOS, D.C. & BORGES-NOJOSA, D.M. 2012.Tropidurus hispidus (Calango). Saurophagy. Herpetol. Rev. 43:141-142.),T. itambereRodrigues, 1987RODRIGUES, M.T. 1987. Sistemática, ecologia e zoogeografia dosTropidurus do grupo torquatus ao Sul do rio Amazonas (Sauria, Iguanidae). Arq. Zool. 31:105-230. (Faria & Araújo 2004FARIA, R.R. & ARAÚJO, A.F.B. 2004. Syntopy of twoTropidurus lizard species (Squamata: Tropiduridae) in a rocky Cerrado habitat in Central Brazil. Braz. J. Biol. 64:775-786, 10.1590/S1519-69842004000500007.
https://doi.org/10.1590/S1519-6984200400... ), T. montanusRodrigues, 1987RODRIGUES, M.T. 1987. Sistemática, ecologia e zoogeografia dosTropidurus do grupo torquatus ao Sul do rio Amazonas (Sauria, Iguanidae). Arq. Zool. 31:105-230. (Kiefer 1998KIEFER, M.C. 1998. Anotosaura brachylepis (NCN). Predation. Herpetol. Rev. 29:41.), and T. torquatus (Wied, 1820) (Teixeira & Giovanelli 1999TEIXEIRA, R.L. & GIOVANELLI, M. 1999. Ecologia deTropidurus torquatus (Sauria: Tropiduridae) da restinga de Guriri, São Mateus, ES. Rev. Bras. Biol. 59:11-18, 10.1590/S0034-71081999000100002.
https://doi.org/10.1590/S0034-7108199900... , Galdino & Van Sluys 2004GALDINO, C.A.B. & VANSLUYS,M. 2004. Tropidurus torquatus (Collared Lizard, Calango). Saurophagy. Herpetol. Rev. 35:173., Kokubum & Lemos 2004KOKUBUM, M.C. & LEMOS, F.G. 2004. Tropidurus torquatus (Calango). Saurophagy. Herpetol. Rev. 35:270-271., Kiefer et al. 2006KIEFER, M.C., SIQUEIRA, C.C., VAN SLUYS, M. & ROCHA, C.F.D. 2006. Tropidurus torquatus (Collared Lizard, Calango). Prey. Herpetol. Rev. 37:475-476., Peloso & Pavan 2007PELOSO, P.L. & PAVAN, S.E. 2007. Cnemidophorus nativo (NCN). Predation. Herpetol. Rev. 38:451-452.). Moreover, cannibalism was recorded in T. hispidus (Sales et al. 2011SALES, R.F.D., JORGE, J.S., RIBEIRO, L.B. & FREIRE, E.M.X. 2011. A case of cannibalism in the territorial lizard Tropidurus hispidus (Squamata: Tropiduridae) in Northeast Brazil. Herpetol. Notes 4:265-267.),T. hygomi Reinhardt & Lütken, 1861 (Dias & Rocha 2004DIAS, E.J.R. & ROCHA, C.F.D. 2004. Tropidurus hygomi (NCN). Juvenile predation. Herpetol. Rev. 35:398-399., Kohlsdorf et al. 2004KOHLSDORF, T., GODOY, C. & NAVAS, C.A. 2004. Tropidurus hygomi (NCN). Cannibalism. Herpetol. Rev. 35:398.), T. montanus (Kiefer & Sazima 2002KIEFER, M.C. & SAZIMA, I. 2002. Tropidurus montanus (NCN). Cannibalism. Herpetol. Rev. 33:136.), T. oreadicusRodrigues, 1987RODRIGUES, M.T. 1987. Sistemática, ecologia e zoogeografia dosTropidurus do grupo torquatus ao Sul do rio Amazonas (Sauria, Iguanidae). Arq. Zool. 31:105-230. (Araujo 1987ARAÚJO, A.F.B. 1987. Comportamento alimentar dos lagartos: o caso dos Tropidurus do grupo torquatus da Serra dos Carajás, Pará (Sauria: Iguanidae). An. Etol. 5:203-234.), and T. torquatus (Kiefer et al. 2006KIEFER, M.C., SIQUEIRA, C.C., VAN SLUYS, M. & ROCHA, C.F.D. 2006. Tropidurus torquatus (Collared Lizard, Calango). Prey. Herpetol. Rev. 37:475-476.).

Despite saurophagic and cannibalistic behaviors had been relatively well documented for Tropidurus lizards, the extent of these events remains misunderstood. Furthermore, of all saurophagic records involvingTropidurus lizards as predators, none included syntopic congeners as prey. Herein, we expand the knowledge on saurophagy by providing the first record of predation of T. jaguaribanusPassos, Lima & Borges-Nojosa, 2011PASSOS, D.C., LIMA, D.C. & BORGES-NOJOSA, D.M. 2011. A new species of Tropidurus (Squamata, Tropiduridae) of thesemitaeniatus group from a semiarid area in Northeastern Brazil. Zootaxa 2930:60-68. byT. hispidus.

Material and Methods

The observations were made during a field study on the geographical distribution of the species of the Tropidurus semitaeniatus group, at the vicinity of the Instituto Federal de Ciência, Educação e Tecnologia do Estado do Ceará - IFCE (5°52′59" S, 38°36′13" W, 137 m a.s.l., Datum: WGS 1984), Jaguaribe municipality, Ceará state, northeastern Brazil. The study area is located in a depression region between residual massifs along the middle course of the Jaguaribe River, where there are many rocky outcrops. This location is covered by secondary vegetation composed mainly of xerophytic shrubs and an ephemeral herbaceous stratum during the rainy season. The climate is semiarid and the environment is highly susceptible to desertification (Guerra et al. 2010GUERRA, M.D.F., SOUZA, M.J.N. & LUSTOSA, J.P.G. 2010. Desertificação em áreas semiáridas do Nordeste Brasileiro: O caso do município de Jaguaribe, Ceará. Rev. Geo. 2:67-80.).

Predatory event was video and photographically recorded in detail by two of us (DCP and FACM) about 5 meters from the lizards. After the end of the observations, both prey and predator were collected, fixed in 10% formalin, preserved in 70% ethanol, and deposited in the Coleção Herpetológica da Universidade Federal do Ceará (CHUFC L 5996 - T. jaguaribanus and CHUFC L 5997 - T. hispidus) . In the lab, the snout-vent length (SVL) of lizards was measured with calipers (to nearest 0.01 mm). An X-ray was made of the T. jaguaribanus specimen (VMI-Philips Compacto Plus 500 - 32 kV / 0.03 mAs / mA 100) to evaluate its bone injuries. It was then dissected to diagnose its cause of death by one of us (CHON), at the radiology sector at the Veterinary Hospital of the Universidade Estadual do Norte Fluminense Darcy Ribeiro.

Results

On the morning of 23 April 2015 at 09:14 a.m. an adult male Tropidurus hispidus (112.5 mm SVL) chased and caught an adult female of T. jaguaribanus (76.4 mm SVL) by its left hind limb (Figure 1A). After a few seconds, the predator vigorously shook the prey still firmly held between its jaws, while the prey writhed and bit its head in unsuccessful attempts to escape. Thereafter, the predator briefly released the prey triggering its escape, but soon pursued and recaptured it again. This process involving release, pursuit and recapture happened several times, differing only in the part of the prey's body (e.g., right hindlimb, thorax, and head, respectively) bitten by the predator (Figure 1B-D). Only 26 minutes after the beginning of the observations we assumed the death of the prey, due to the absence of any reaction to the last release event. On that occasion, the predator kept right off and gently touched the prey. Prey manipulation and observation lasted some minutes, afterwards the predator began to swallow it. There were two attemps to swallow the prey, both head-first. Initially, the predator tried to swallow the prey dorsally (Figure 1E), but failed. Then, it turned the prey with belly up and tried to swallow it again (Figure 1F). However, the predator was not able to swallow entirely the prey. At 10:16 a.m., after almost an hour, the predator started to lose interest for the prey, and we shot it down with an airgun. Then, both lizards were collected, taken to the lab and deposited at the scientific collection of the Universidade Federal do Ceará.

The radiography showed multiple bone fractures throughout the prey's body (Figure 2) as follows: jaw (complete fracture of the left mandibular bone), right forelimb (luxation of the radioulnar and radiocarpal joints), left hind limb (transversal fracture of the femur), right hind limb (spiral fracture of the fibula). The necropsy also revealed several tegumentary perforations at the bite sites, lacerations and edemas in vicinity of the fractured bones, as well hemorrhagic areas in the femoral region of the left hind limb and in the tibial region of the right hind limb. In addition, the lizard's skull was smashed, estimated about 12% by comparing the photographic records of the beginning and end of the predatory event (head height 7.0 and 6.1 mm, respectively). However, although the hypovolemic shock might be generally the cause of death in severely injured animals (Fighera et al. 2008FIGHERA, R.A., SILVA, M.C., SOUZA, T.M., BRUM, J.S., KOMMERS, G.D., GRAÇA, D.L., IRIGOYEN, L.F. & BARROS, C.S.M. 2008. Aspectos patológicos de 155 casos fatais de cães atropelados por veículos automotivos. Cienc. Rural 38:1375-1380.), we were not able to accurately evaluate the seriousness of the cranial trauma due to the small body size of the prey, and so the causa mortis of the specimen could not be precisely determined.

Discussion

The Neotropical lizard Tropidurus hispidus has a wide geographical distribution, occurring in Caatinga semiarid and coastal areas in northeastern Brazil as well as in Amazonian savanna enclaves in northern South America (Carvalho 2013CARVALHO, A.L.G. 2013. On the distribution and conservation of the South American lizard genus Tropidurus Wied-Neuwied, 1825 (Squamata: Tropiduridae). Zootaxa 3640:042-056, 10.11646/zootaxa.3640.1.3.
https://doi.org/10.11646/zootaxa.3640.1.... ). As is know for mostTropidurus, this species feeds mainly on arthropods, but leaves, flowers and fruits also may compose its diet (Vitt 1995VITT, L.J. 1995. The ecology of tropical lizards in the caatinga of northeast Brazil. Oklah. Mus. Nat. Hist. 1:1-29., Van Sluys 2004, Kolodiuk et al. 2010KOLODIUK, M.F., RIBEIRO, L.B. & FREIRE, E.M.X. 2010. Diet and foraging behavior of two species of Tropidurus (Squamata, Tropiduridae) in the Caatinga of northeastern Brazil. South Am. J. Herpetol. 5:35-44, 10.2994/057.005.0104.
https://doi.org/10.2994/057.005.0104... ). Moreover, small vertebrates have been also reported among its prey, such as the frogs Elachistocleis ovalis(Schneider, 1799) (Vitt et al. 1996VITT, L.J., ZANI, P.A. & CALDWELL, J.P. 1996. Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia. J. T. Ecol. 12:81-101, 10.1017/S0266467400009329.
https://doi.org/10.1017/S026646740000932... ) andScinax x-signatus (Spix, 1824) (Ribeiro & Freire 2009RIBEIRO, L.B. & FREIRE, E.M.X. 2009. Tropidurus hispidus (NCN). Frog predation. Herpetol. Rev. 40:228-228.), beyond the lizards Colobosaura modesta (Reinhardt and Lütken, 1862) (Costa et al. 2010COSTA, J.C.L., MANZANI, P.R., BRITO, M.P.L. & MACIEL, A.O. 2010.Tropidurus hispidus (Calango). Prey. Herpetol. Rev. 41:87.), Cnemidophorus ocellifer (Spix, 1825) (Zanchi et al. 2012ZANCHI, D., PASSOS, D.C. & BORGES-NOJOSA, D.M. 2012.Tropidurus hispidus (Calango). Saurophagy. Herpetol. Rev. 43:141-142.) and Norops auratus (Daudin, 1802) (Costa-Campos & Souza 2013COSTA-CAMPOS, C.E. & SOUZA, N.S. 2013. Tropidurus hispidus (Peters' Lava Lizard). Saurophagy. Herpetol. Rev. 44:215-216.). Although T. hispidus is commonly found in sympatry with other congeners, as T. erythrocephalusRodrigues 1987RODRIGUES, M.T. 1987. Sistemática, ecologia e zoogeografia dosTropidurus do grupo torquatus ao Sul do rio Amazonas (Sauria, Iguanidae). Arq. Zool. 31:105-230., T. hygomiand T. montanus (Rodrigues 1987RODRIGUES, M.T. 1987. Sistemática, ecologia e zoogeografia dosTropidurus do grupo torquatus ao Sul do rio Amazonas (Sauria, Iguanidae). Arq. Zool. 31:105-230.), to our knowledge there is no record of congeneric saurophagy between syntopic Tropidurus species. Tropidurus hispidus and T. jaguaribanus live in syntopy on rocky outcrops along the Jaguaribe Valley in the state of Ceará (Passos et al. 2011PASSOS, D.C., LIMA, D.C. & BORGES-NOJOSA, D.M. 2011. A new species of Tropidurus (Squamata, Tropiduridae) of thesemitaeniatus group from a semiarid area in Northeastern Brazil. Zootaxa 2930:60-68.) and although agonistic encounters between the species eventually occur, they usually tolerate the proximity to each other (Passos pers. obs.). Thus, this is the first record of T. jaguaribanus as prey of T. hispidus and the first report of congeneric saurophagy among different species of syntopicTropidurus.

Tropidurus hispidus is one of the largest species of thetorquatus group (Rodrigues 1987RODRIGUES, M.T. 1987. Sistemática, ecologia e zoogeografia dosTropidurus do grupo torquatus ao Sul do rio Amazonas (Sauria, Iguanidae). Arq. Zool. 31:105-230., Freitas & Silva 2005FREITAS, M.A. & SILVA, T.F.S. 2005. Guia ilustrado: a herpetofauna da Mata Atlântica nordestina. Editora USEB, Pelotas.), whilst T. jaguaribanus is the largest one of thesemitaeniatus group (Passos et al. 2011, Passos et al. 2013PASSOS, D.C., LIMA, D.C. & BORGES-NOJOSA, D.M. 2013. Clutch size, incubation time and hatchling morphometry of the largest knownTropidurus of the semitaeniatus group (Squamata, Tropiduridae), in a semi-arid area from northeastern Brazil. Herpetol. Bul. 123:23-25.). In general, juvenile lizards are more susceptible to predation in both saurophagic and cannibalistic interactions (Siqueira & Rocha 2008SIQUEIRA, C.C. & ROCHA, C.F.D. 2008. Predation by lizards as a mortality source for juvenile lizards in Brazil. South Am. J. Herpetol. 3:82-87, 10.2994/1808-9798(2008)3[82:PBLAAM]2.0.CO;2.
https://doi.org/10.2994/1808-9798(2008)3... ). Their smaller relative size compared to adults, their higher relative abundance as well the lack of experience in avoid predators may explain this trend (Vitt 2000VITT, L.J. 2000. Ecological consequences of body size in neonatal and small-bodied lizards in the Neotropics. Herpetol. Monogr. 14:388-400.). In fact, the majority of records of saurophagy and cannibalism in T. hispidus were directed against juveniles (e.g.Sales et al. 2011SALES, R.F.D., JORGE, J.S., RIBEIRO, L.B. & FREIRE, E.M.X. 2011. A case of cannibalism in the territorial lizard Tropidurus hispidus (Squamata: Tropiduridae) in Northeast Brazil. Herpetol. Notes 4:265-267.) or species of smaller body size (e.g. Zanchi et al. 2012ZANCHI, D., PASSOS, D.C. & BORGES-NOJOSA, D.M. 2012.Tropidurus hispidus (Calango). Saurophagy. Herpetol. Rev. 43:141-142.). However, the case reported herein involved adult individuals of two of the largest species of the genus Tropidurus. This itself would already be noteworthy, even more if added to the complex hunting behavior performed repeatedly by T. hispidus.

Acknowledgements

We thank Izamaro Araújo, director of the Instituto Federal de Ciência, Educação e Tecnologia do Estado do Ceará - Campus Jaguaribe, for the opportunity to work on the IFCE's property, and Jean Nixon for fieldwork assistance. We also thank Helena Hokamura, head of radiology sector from Veterinary Hospital of Universidade Estadual do Norte Fluminense Darcy Ribeiro, for logistical support and the radiological analysis. We are grateful to Daniel Cassiano Lima and Laís Feitosa Machado for the critical review of a previous version of this manuscript. We are also grateful to Gunther Köhler and an anonymous referee for the valuable suggestions to this paper. DCP is funded by a Doctor's degree scholarship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES. The collecting permit 42552-4 was granted by the Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio.

References

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