Age-Dependent Utilization of Shelters and Habitat in Two Reptile Species with Contrasting Intraspecific Interactions

animals Article Age-Dependent Utilization of Shelters and Habitat in Two Reptile Species with Contrasting Intraspecific Interactions Aleksandra Kolanek 1,2, * , Stanisław Bury 2,3 , Edyta Turniak 2 and Mariusz Szymanowski 1 1 2 3 * Department of Geoinformatics and Cartography, Institute of Geography and Regional Development, University of Wroclaw, pl. Uniwersytecki 1, 50-137 Wrocław, Poland; NATRIX Herpetological Association, ul. Legnicka 65, 54-206 Wrocław, Poland; (S.B.); (E.T.) Institute of Environmental Sciences, Jagiellonian University, ul. Gronostajowa 7, 30-387 Kraków, Poland Correspondence: Received: 23 September 2019; Accepted: 15 November 2019; Published: 18 November 2019



 Simple Summary: Intraspecific interactions are known to affect habitat use in birds and mammals but their role in spatial ecology of reptiles is far less recognized. Our comparative study shows that species known to exhibit intraspecific predation (smooth snake Coronella austriaca) express clearly different patterns of habitat and shelter occupancy than a species with no such cannibalistic behavior (slow worm Anguis fragilis). Specifically, juvenile smooth snakes prefer sites and shelters not occupied by the adults, even despite suboptimal habitat conditions. We propose that such division indicates an avoidance of predation pressure set by larger individuals on the younger and smaller ones. On the contrary, in slow worms no tendency for intraspecific avoidance are observed, since specimens of different ages commonly share the same area and shelters. This points to higher flexibility in habitat use in slow worms, while the smooth snake population is spatially structured, with juveniles dispersed to the margins of the population range. For endangered smooth snakes, habitat conservation should therefore include a wide buffer zone to maintain the youngest fraction of the population. Future studies on habitat utilization in squamates needs to pay more attention to the social cues, a commonly overlooked aspect in the spatial ecology of reptiles. Abstract: Reptiles undergo worldwide decline driven mostly by habitat change. Detailed recognition of factors underlying spatial structure and habitat utilization is therefore a prerequisite of effective conservation of this group. While the body of data on spatial ecology of reptiles is rapidly growing, studies on social factors remain still underrepresented. We studied age-specific patterns of shelter use, range size, and habitat preferences in the context of intraspecific interactions in the smooth snake Coronella austriaca—known to exhibit intraspecific predation—and the limbless lizard slow worm Anguis fragilis—with no such behavior observed. Despite smaller availability of preferred microhabitats, juveniles of smooth snakes occupied habitat and shelters located at the edge of the population range that did not overlap with adults. No such pattern was observed in the slow worm. Our study indicates that intraspecific interactions affect the spatial ecology of squamates. Passive and active protection of habitat must include wide buffers to preserve the poorly detectable young fraction of the population. Keywords: age-dependence; spatial ecology; intraspecific predation; reptiles; habitat use Animals 2019, 9, 995; doi:10.3390/ani9110995 www.mdpi.com/journal/animals Animals 2019, 9, 995 2 of 12 1. Introduction Loss of natural habitats and changes in their structure are among the major challenges in biodiversity conservation [1]. Understanding how species use their habitats is therefore helpful to orientate management and planning of protected areas [2]. Most studies on habitat utilization of terrestrial vertebrates have focused on mammals (e.g., [3]) and birds (e.g., [4]), with amphibians [5] and reptiles receiving less attention (e.g., [6]). In snakes, patterns of habitat use are most commonly interpreted through the lens of size-dependent trophic niche partitioning, i.e., ontogenetic differences in diet [7] or, sometimes, by variation in thermoregulatory strategies [8]. However, recent findings suggest that social interaction may be an important, although overlooked, factor in snake ecology [9,10]. Dietary preference is commonly different between adult and juvenile snakes (e.g., [11]), and it might also differ due to sex-specific body size variation [12,13]. Although dietary niche partitioning is important in snakes, not all shifts in space utilization can be explained by variation in dietary niches (e.g., [14]). Studies have shown that the scent of conspecific may attract snakes and affect the direction of their movement [15]. The opposite reaction, the avoidance of conspecifics, is likely to occur in species exhibiting intraspecific antagonistic behaviors such as cannibalism. Intraspecific predation is expected to promote shifts in habitat choice mainly in juveniles, expected to avoid competition with large-sized adults. So far only studies on other squamates, lizards, show such spatial division between juveniles and adults choosing different branches in trees and shrubs in the cannibalistic common chameleons (Chamaeleo chamaeleon; [16]). The avoidance behavior is proposed to be a factor of population regulation in snakes [17], but it still remains unknown whether it could be affected by intraspecific predation. We aimed to investigate patterns of habitat use in the context of age and intraspecific interactions. We compared two sympatric species of reptiles, the smooth snake Coronella austriaca and the legless lizard, slow worm Anguis fragilis. These two species show similar habitat preferences, comparable body size, and both have a viviparous mode of reproduction. However, the smooth snake is known to exhibit cannibalism [17,18], whereas the legless lizard is a non-territorial species that does not exhibit cannibalism [19]. Since cannibalistic behavior exerts the strongest pressure from adults towards juveniles, we assume the presence of age-dependent shifts in artificial shelter utilization and spatial distribution by those snakes as an indication of adult avoidance by juveniles. We expect adult and juvenile snakes to occupy different shelters (without overlapping) and to exhibit no tendency for spatial clustering, understood as reduced distance between individuals compared to random placements [20]. In contrast, adult and juvenile legless lizards are expected to either co-occur in the same shelter or to show clustered spatial distribution. Next to social cues, microhabitat conditions can also drive spatial distribution, therefore we have additionally controlled for the variation in microhabitat parameters in the studied area. Snake habitat use is generally related to climate, land cover structure, vegetation, and topography [21–24]. Given the small scale of the study area, we used the potential insolation and vegetation height to measure environmental conditions around each artificial shelter. These two factors (r (...truncated)