Dangerous neighborhood : saurophagy between syntopic Tropidurus lizards

Saurophagy constitutes an important source of mortality among lizards and has been reported for the genus Tropidurus. However, the extension of this behavior remains unknown. Herein, we record the predation of T. jaguaribanus by its congener T. hispidus. This is the first report of saurophagy among different species of syntopic Tropidurus. Furthermore, whereas published records of saurophagy tend to be directed against juveniles, this case involved two adult individuals.


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 2000, Siqueira & Rocha 2008).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 2012, Robbins et al. 2013).
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 involving Tropidurus 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. jaguaribanus Passos, Lima & Borges-Nojosa, 2011 by T. 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 Cie ˆncia, Educac¸a ˜o e Tecnologia do Estado do Ceara ´-IFCE (5°52'59" S, 38°36'13" W, 137 m a.s.l., Datum: WGS 1984), Jaguaribe municipality, Ceara ´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. 2010).
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 Colec¸a ˜o Herpetolo ´gica da Universidade Federal do Ceara ´(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 Ceara ´.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. 2008), 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.
Tropidurus hispidus and T. jaguaribanus live in syntopy on rocky outcrops along the Jaguaribe Valley in the state of Ceara ´ (Passos et al. 2011) 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 syntopic Tropidurus.
Tropidurus hispidus is one of the largest species of the torquatus group (Rodrigues 1987, Freitas & Silva 2005), whilst T. jaguaribanus is the largest one of the semitaeniatus group (Passos et al. 2011, Passos et al. 2013).In general, juvenile lizards are more susceptible to predation in both saurophagic and cannibalistic interactions (Siqueira & Rocha 2008).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 2000).In fact, the majority of records of saurophagy and cannibalism in T. hispidus were directed against juveniles (e.g.Sales et al. 2011) or species of smaller body size (e.g.Zanchi et al. 2012).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.

Figure 1 .
Figure 1.Saurophagic behavior of Tropidurus hispidus on Tropidurus jaguaribanus.(A) prey capture by the left hindlimb; (B) prey recapture by the right hind limb; (C) prey recapture by the thorax; (D) prey recapture by the head; (E) dorsal attempt to swallow the prey; (F) ventral attempt to swallow the prey.