Cannibalism in the Andean lizard Liolaemus orientalis

ABSTRACT Cannibalism is a recurrent behavior across the animal kingdom, with important ecological and evolutionary consequences due to its potential trade-offs on the fitness of involved individuals and demography dynamics. Cannibalism has been reported in eight species of several phylogenetic lineages within Liolaemus, a highly diverse genus of Neotropical lizards. Within the Liolaemus montanus series, two species are reported to eat juveniles in captivity. We observed a female Liolaemus orientalis, another L. montanus series member, which had ingested a juvenile of its own species in the wild. As it generally happens with other lizards, cannibalism in Liolaemus has been suggested to be performed by the larger sex, with L. chiliensis being the only other case observed until now in which the cannibalistic individual was a female. The fact that females are slightly smaller than males in L. orientalis means that our observation is an exception to previously observed trends. We suggest that there is a relationship between this behavior and the presence of a masculine trait in the cannibalistic female: developed precloacal pores. We also discuss how refuge availability may influence demography and the probability of dispersing juveniles encountering adults, increasing the chances for cannibalism to play some role in population density regulation.


Introduction
Cannibalism or predation of conspecifics is a widespread behavior in the animal kingdom with important ecological and evolutionary implications (Polis 1981). Although in some cases cannibalism happens as a stochastic event, selective pressures and fitness tradeoffs may result in deterministic evolution of behaviors either favoring or avoiding cannibalism in different contexts (Rand & Andrews 1975;Polis 1981;Jenssen et al. 1989;Pfennig 1997;Lourdais et al. 2005). Cannibalism in reptiles is often regarded as an opportunistic result of encounters of different size classes, often with juveniles being the prey (Polis & Myers 1985). Hence, an important set of predators of juvenile lizards may be constituted by adults of the same species (Siqueira & Rocha 2008). The highly diverse genus Liolaemus, with more than 250 species (Schulte et al. 2000;Abdala & Quinteros 2014) is not an exception, as cannibalism has been observed in six Liolaemus species in the wild and in two additional species in captivity (reviewed by Pincheira-Donoso 2012; Villarreal et al. 2012). The general lack of knowledge on natural history and behavior within Liolaemus (Halloy et al. 2013), the difficulty of observing intraspecific predation events in nature, and the occurrence of this behavior across different phylogenetic groups within Liolaemus (Pincheira-Donoso 2012), suggests that the extent of cannibalism in this genus might be underestimated.
Although there is a general tendency of female cannibalism in the animal kingdom (Polis 1981), Siqueira and Rocha (2008) showed that cannibalism in lizards is usually performed by the larger sex. Within Liolaemus, either gender can be the biggest, depending on the species (Pincheira-Donoso & Tregenza 2011; Cox & Kahrl 2014). In seven out of the eight known cannibalistic Liolaemus species, intraspecific predation happened in males. The only exception reported so far was L. chiliensis, in which females preyed on juveniles and are larger than males (Pincheira-Donoso 2012). Such female-biased sexual size dimorphism is a plausible reason for this exceptional case of female cannibalism in Liolaemus (Pincheira-Donoso 2012).
Herein, we report the first evidence of cannibalism in Liolaemus orientalis Müller, 1924, a viviparous species of the Liolaemus montanus series (sensu Schulte et al. 2000;Lobo et al. 2010). This lizard is known from several localities in the Cordillera Oriental of the Andes in southeastern Bolivia and northwestern Argentina (Dirksen & De la Riva 1999;Díaz Gómez 2007). In the studied population, we could observe that L. orientalis has some slight sexual dimorphism in size, coloration and the expression of precloacal pores. Males reach slightly larger sizes than adult females, although that difference is not statistically significant (O. Jiménez-Robles, unpublished data). Juveniles are born with a disruptive dorsal pattern with transversal dark gray bars, which fade as they grow. Females of L. orientalis retain a faded juvenile pattern while males change coloration ontogenetically, turning to plain nickel-gray on dorsum (O. Jiménez-Robles, pers. obs.). All males possess developed precloacal pores, while most females lack them (O. Jiménez-Robles, pers. obs.).

Material and methods
During November 2012-January 2013 and November 2013-January 2014, we conducted research on habitat use, distribution and thermal ecophysiology of L. orientalis in the vicinities of Arenales (21.854°S, 65.012°W, WGS84, 3600-4300 m asl, Municipality of Yunchará, Province of Avilez, Reserva Biológica Cordillera de Sama, Department of Tarija, Bolivia).
When the weather conditions allowed their activity, one observer surveyed lizards by slowly walking along 200 m transects. As L. orientalis may have escape distances of more than 15 m (O. Jiménez-Robles, pers. obs.), the observer carefully scanned visually all available surfaces in a radius of 20 m at least. Once a lizard was detected, it was approached cautiously with the intention to noose it with a modified 3 m fishing rod and to measure body temperature (with a hand-held thermometer a few seconds after capture), substrate temperature, sex, body size (snout to vent length; SVL) and weight. We also recorded whether females had precloacal pores, and classified them as absent, vestigial or developed. After measurements were taken, individuals were released at the capture spot.

Results
On 26 December 2013, at 12:27 h and 4290 m asl, a female of L. orientalis was found basking on a stone of less than 50 cm in length. Her intra-cloacal temperature was 32.5°C and substrate temperature was 27.3°C. While being handled, she vomited an immature male of her own species (Figure 1). It had been swallowed head-first, with the head being partially digested, while the posterior part of the body was still intact (except for the missing tail tip). The preyed individual had a SVL of 45 mm, tail length >19 mm and weight of 2.5 g. The female size (81 mm of SVL, 96 mm of tail length, and 15.2 g of weight after vomiting) was slightly below the most frequent observed SVL for adult females in this population and conserved a faint juvenile dorsal color pattern, suggesting that she was still growing. She had developed precloacal pores (Figure 1b).

Discussion
Our observation is the second reported case of female cannibalism in Liolaemus. Contrarily to the predictions of Siqueira and Rocha (2008) for lizards, and Pincheira-Donoso (2012) for the genus Liolaemus, cannibalism is not always performed by the larger sex. At least the exceptional case of female cannibalism in L. orientalis follows the common pattern observed in other animals (Polis 1981) where females are usually the cannibalistic sex.
However, cannibalism in L. orientalis could be a behavior also carried out by males. In some lizards, several degrees of female masculinization have been observed both in aggressive behavior and physical traits (Viets et al. 1993;Hews & Quinn 2003;Swierk & Langkilde 2013). In the genus Liolaemus, males generally have precloacal pores, but there is variation in their occurrence in females; if present, they are always smaller and less numerous than those of males (Valdecantos et al. 2014). In the L. orientalis population of Arenales, the expression of fully developed precloacal pores in females was observed in this cannibalistic female and three other females (while we observed other 32 females with no pores and 16 with vestigial pores). Further evidence is needed to understand the biological meaning of the different expression of precloacal pores in females of Liolaemus, and to know if their presence has any relation with aggressive behavior and infanticide risk.
Previous observations of intraspecific predation within the montanus series took place in laboratory conditions with L. huacahuasicus (Halloy & Halloy 1997) and L. forsteri (Villarreal et al. 2012). Hence, our observation in L. orientalis confirms that cannibalism happens in nature in free-ranging members of the Liolaemus montanus series (sensu Schulte et al. 2000).
Cannibalism in the animal kingdom is usually conditioned by size differences. This explains its higher occurrence in large species (Polis 1981). Pincheira-Donoso (2012) detected that large species of Liolaemus were more likely to be cannibalistic, with all the reports belonging to species in the far right range of body size frequency distribution for the genus, with the exception of L. darwinii, which has a medium size. The other cannibalistic species not included in that analysis, L. huacahuasicus, L. forsteri, and L. orientalis, would be also in the right side of size frequency distribution and reinforce the same conclusions.
The risk of cannibalism in the wild may be also affected by demographic factors (Polis 1981). Liolaemus orientalis in the Cordillera de Sama occurs at relatively low densities when compared with other lizards, such as the smaller Liolaemus spp. that live below 3800 m asl in the study area (Jiménez-Robles, unpublished). Despite these low densities, the limited availabilities of refuges in its habitat may increase the chances of individual encounters. This means that dispersing juveniles could face some intraspecific predation risk by the relatively high probability of coming across an adult when seeking for a refuge. Under these habitat constraints, cannibalism may be a way of regulating population densities, especially when approaching carrying capacity.
Given the lower substrate temperature, the cannibalistic female was likely raising her body temperature mainly through heliothermy, although with the thigmothermic contribution of a substrate with high thermal inertia such as a stone. Probably she was trying to optimize digestion of her prey while basking. The juvenile, with approximately a sixth of the mass of the predator, did not even fit into her stomach, so the urgency of digesting it was even higher. Preying on such big items undoubtedly contributes great nutritive benefits but it also implies some costs, such as an urgent need to bask for more time to accelerate digestion and a higher risk of predation or losing the stomach content after a stressing event (as happened in the reported case).

Acknowledgments
José A. Alfaro, Edmundo Martínez and other rangers and managers of SERNAP (Servicio Nacional de Áreas Protegidas) provided logistic support in Reserva Biológica Cordillera de Sama. James Aparicio (CBF-MNHN) helped with bureaucracy for research permits, which were provided by the Ministerio de Medio Ambiente y Agua of Bolivia (VMA-DGBAP 1866/2012). Nellsy A. Ohara lent her camera for taking the pictures, and she together with Ramiro Estrada-Núñez provided assistance during data collection. Anne Zillikens and three anonymous reviewers provided comments that improved the manuscript.

Disclosure statement
No potential conflict of interest was reported by the authors.

Funding
Research costs were supported by the Spanish Ministerio de Economía y Competitividad [project CGL2011-30393] (Principal Investigator, I. De la Riva). O. Jiménez-Robles was supported by a JAE-pre grant from the Consejo Superior de Investigaciones Científicas (CSIC).