From tameness to wariness: chemical recognition of snake predators by lizards in a Mediterranean island.

Antipredatory defenses are maintained when benefit exceeds cost. A weak predation pressure may lead insular lizards to tameness. Podarcis lilfordi exhibits a high degree of insular tameness, which may explain its extinction from the main island of Menorca when humans introduced predators. There are three species of lizards in Menorca: the native P. lilfordi, only on the surrounding islets, and two introduced lizards in the main island, Scelarcis perspicillata and Podarcis siculus. In addition, there are three species of snakes, all introduced: one non-saurophagous (Natrix maura), one potentially non-saurophagous (Rhinechis scalaris) and one saurophagous (Macroprotodon mauritanicus). We studied the reaction to snake chemical cues in five populations: (1) P. lilfordi of Colom, (2) P. lilfordi of Aire, (3) P. lilfordi of Binicodrell, (4) S. perspicillata, and (5) P. siculus, ordered by increasing level of predation pressure. The three snakes are present in the main island, while only R. scalaris is present in Colom islet, Aire and Binicodrell being snake-free islets. We aimed to assess the relationship between predation pressure and the degree of insular tameness regarding scent recognition. We hypothesized that P. lilfordi should show the highest degree of tameness, S. perspicillata should show intermediate responses, and P. siculus should show the highest wariness. Results are clear: neither P. lilfordi nor S. perspicillata recognize any of the snakes, while P. siculus recognizes the scent of M. mauritanicus and reacts to it with typical well-defined antipredatory behaviours as tail waving and slow motion. These results rise questions about the loss of chemical recognition of predators during island tameness and its related costs and benefits for lizards of insular habitats. In addition, this highlights the necessity for strong conservation measures to avoid the introduction of alien predators.

Wind constraints on the thermoregulation of high mountain lizards.

Thermal biology of lizards affects their overall physiological performance. Thus, it is crucial to study how abiotic constraints influence thermoregulation. We studied the effect of wind speed on thermoregulation in an endangered mountain lizard (Iberolacerta aurelioi). We compared two populations of lizards: one living in a sheltered rocky area and the other living in a mountain ridge, exposed to strong winds. The preferred temperature range of I. aurelioi, which reflects thermal physiology, was similar in both areas, and it was typical of a cold specialist. Although the thermal physiology of lizards and the structure of the habitat were similar, the higher wind speed in the exposed population was correlated with a significant decrease in the effectiveness thermoregulation, dropping from 0.83 to 0.74. Our results suggest that wind reduces body temperatures in two ways: via direct convective cooling of the animal and via convective cooling of the substrate, which causes conductive cooling of the animal. The detrimental effect of wind on thermoregulatory effectiveness is surprising, since lizards are expected to thermoregulate more effectively in more challenging habitats. However, wind speed would affect the costs and benefits of thermoregulation in more complex ways than just the cooling of animals and their habitats. For example, it may reduce the daily activity, increase desiccation, or complicate the hunting of prey. Finally, our results imply that wind should also be considered when developing conservation strategies for threatened ectotherms.

Adaptive seasonal shifts in the thermal preferences of the lizard Iberolacerta galani (Squamata, Lacertidae).

The León rock lizard, Iberolacerta galani, lives in isolated mountains of Spain. We studied the seasonal changes in the thermal biology of I. galani between spring and summer. We calculated precision, accuracy and effectiveness of thermoregulation and the habitat thermal quality for spring, and compared with the values of summer. In addition, we studied how the shift in the thermal preferences of lizards would contribute to achieve a higher effectiveness of thermoregulation. Thermal preferences of León rock lizards are among the lowest in lacertids, and are also very narrow, maintaining the narrowness among seasons. As for summer (27.90-29.70°C, mean value =28.76°C), the thermal preferences of I. galani are also low in spring (29.60-31.10°C, mean value =30.38°C), supporting the idea that this species is adapted to cold environments. The habitat thermal quality is lower in spring (10.99°C) than in summer (9.36°C), while the effectiveness of thermoregulation is higher in spring (0.92) than in summer (0.80). We found that the seasonal shift in thermal preferences contributes significantly to enhance the effectiveness of thermoregulation in both seasons, more in spring (0.45°C) than in summer (0.16°C). Because I. galani inhabits isolated mountains, where the activity period is reduced from April to October, we hypothesize that the observed adaptation of the thermal preferences, which enhance thermoregulation to a larger extent in spring, may evolved to maximize performance during the reproductive season.

Sexual differences in behavioral thermoregulation of the lizard Scelarcis perspicillata.

Temperature determines all aspects of the biology of ectotherms. Although sexual differences in thermal ecology are not the rule in lizards, some species exhibit such differences. We studied the effect of sex and reproductive condition on the thermoregulation of an introduced population of Scelarcis perspicillata during the summer in Menorca (Balearic Islands, Spain). These lizards live in the wall surfaces of a limestone quarry, where the sun is scarce because of the narrowness of the quarry walls. The population is sexually dimorphic, with larger males than females. We measured body temperature (Tb) of adult males and females in the field, and air (Ta) and substrate temperature (Ts) at the capture sites, and recorded exposure to sunlight, height of the perch, and type of substrate. We also recorded operative temperatures (Te) as a null hypothesis of thermoregulation. Finally, we studied the thermal preferences of adult males and females in a laboratory thermal gradient. Thermal preferences were similar for pregnant and non-pregnant females, and sex did not affect the thermal preferences of lizards, even after controlling for the effect of body size. However, in the field, females achieved higher Tb than males, and occupied microhabitats with higher Ta and Ts and lower perch heights than males. Furthermore, females selected perches in full sun at a higher frequency than males. As a consequence, females achieved a higher accuracy and effectiveness of thermoregulation (0.89) than males (0.84). Thus, all else being equal, females would achieve a higher performance than males. The observed results are attributable to sexual differences in behaviour, probably in relation with the reproductive season.

Introducing Meta-Partition, a Useful Methodology to Explore Factors That Influence Ecological Effect Sizes.

The study of the heterogeneity of effect sizes is a key aspect of ecological meta-analyses. Here we propose a meta-analytic methodology to study the influence of moderators in effect sizes by splitting heterogeneity: meta-partition. To introduce this methodology, we performed a meta-partition of published data about the traits that influence species sensitivity to habitat loss, that have been previously analyzed through meta-regression. Thus, here we aim to introduce meta-partition and to make an initial comparison with meta-regression. Meta-partition algorithm consists of three steps. Step 1 is to study the heterogeneity of effect sizes under the assumption of fixed effect model. If heterogeneity is found, we perform step 2, that is, to partition the heterogeneity by the moderator that minimizes heterogeneity within a subset while maximizing heterogeneity between subsets. Then, if effect sizes of the subset are still heterogeneous, we repeat step 1 and 2 until we reach final subsets. Finally, step 3 is to integrate effect sizes of final subsets, with fixed effect model if there is homogeneity, and with random effects model if there is heterogeneity. Results show that meta-partition is valuable to assess the importance of moderators in explaining heterogeneity of effect sizes, as well as to assess the directions of these relations and to detect possible interactions between moderators. With meta-partition we have been able to evaluate the importance of moderators in a more objective way than with meta-regression, and to visualize the complex relations that may exist between them. As ecological issues are often influenced by several factors interacting in complex ways, ranking the importance of possible moderators and detecting possible interactions would make meta-partition a useful exploration tool for ecological meta-analyses.

Behavioral buffering of global warming in a cold-adapted lizard.

Alpine lizards living in restricted areas might be particularly sensitive to climate change. We studied thermal biology of Iberolacerta cyreni in high mountains of central Spain. Our results suggest that I. cyreni is a cold-adapted thermal specialist and an effective thermoregulator. Among ectotherms, thermal specialists are more threatened by global warming than generalists. Alpine lizards have no chance to disperse to new suitable habitats. In addition, physiological plasticity is unlikely to keep pace with the expected rates of environmental warming. Thus, lizards might rely on their behavior in order to deal with ongoing climate warming. Plasticity of thermoregulatory behavior has been proposed to buffer the rise of environmental temperatures. Therefore, we studied the change in body and environmental temperatures, as well as their relationships, for I. cyreni between the 1980s and 2012. Air temperatures have increased more than 3.5°C and substrate temperatures have increased by 6°C in the habitat of I. cyreni over the last 25 years. However, body temperatures of lizards have increased less than 2°C in the same period, and the linear relationship between body and environmental temperatures remains similar. These results show that alpine lizards are buffering the potential impact of the increase in their environmental temperatures, most probably by means of their behavior. Body temperatures of I. cyreni are still cold enough to avoid any drop in fitness. Nonetheless, if warming continues, behavioral buffering might eventually become useless, as it would imply spending too much time in shelter, losing feeding, and mating opportunities. Eventually, if body temperature exceeds the thermal optimum in the near future, fitness would decrease abruptly.

Are mountain habitats becoming more suitable for generalist than cold-adapted lizards thermoregulation?

Mountain lizards are highly vulnerable to climate change, and the continuous warming of their habitats could be seriously threatening their survival. We aim to compare the thermal ecology and microhabitat selection of a mountain lizard, Iberolacerta galani, and a widely distributed lizard, Podarcis bocagei, in a montane area. Both species are currently in close syntopy in the study area, at 1,400 m above the sea level. We determined the precision, accuracy and effectiveness of thermoregulation, and the thermal quality of habitat for both species. We also compared the selection of thermal microhabitats between both species. Results show that I. galani is a cold-adapted thermal specialist with a preferred temperature range of 27.9-29.7 °C, while P. bocagei would be a thermal generalist, with a broader and higher preferred temperature range (30.1-34.5 °C). In addition, I. galani selects rocky substrates while P. bocagei selects warmer soil and leaf litter substrates. The thermal quality of the habitat is higher for P. bocagei than for I. galani. Finally, P. bocagei achieves a significantly higher effectiveness of thermoregulation (0.87) than I. galani (0.80). Therefore, these mountain habitat conditions seem currently more suitable for performance of thermophilic generalist lizards than for cold-specialist lizards.

The peak of thermoregulation effectiveness: Thermal biology of the Pyrenean rock lizard, Iberolacerta bonnali (Squamata, Lacertidae).

We studied, at 2200m altitude, the thermal biology of the Pyrenean rock lizard, Iberolacerta bonnali, in the glacial cirque of Cotatuero (National Park of Ordesa, Huesca, Spain). The preferred thermal range (PTR) of I. bonnali indicates that it is a cold-adapted ectotherm with a narrow PTR (29.20-32.77°C). However, its PTR (3.57°C) is twice as wide as other Iberolacerta lizards, which may be explained by its broader historical distribution. The studied area is formed by a mosaic of microhabitats which offer different operative temperatures, so that lizards have, throughout their entire daily period of activity, the opportunity to choose the most thermally suitable substrates. I. bonnali achieves an effectiveness of thermoregulation of 0.95, which makes it the highest value found to date among the Lacertidae, and one of the highest among lizards. Their relatively wide distribution, their wider PTR, and their excellent ability of thermoregulation, would make I. bonnali lizards less vulnerable to climate change than other species of Iberolacerta. Thanks to its difficult access, the studied area is not visited by a large number of tourists, as are other areas of the National Park. Thus, it is a key area for the conservation of the Pyrenean rock lizard. By shuttling between suitable microhabitats, lizards achieve suitable body temperatures during all day. However, such thermally suitable microhabitats should vary in other traits than thermal quality, such as prey availability or predation risk. Hence, it seems that these not-thermal traits are not constraining habitat selection and thermoregulation in this population. Therefore, future research in this population may study the causes that would lead lizards to prioritize thermoregulation to such extent in this population.