Unwrapping broken tails: Biological and environmental correlates of predation pressure in limbless reptiles.

Studying species interactions in nature often requires elaborated logistics and intense fieldwork. The difficulties in such task might hinder our ability to answer questions on how biotic interactions change with the environment. Fortunately, a workaround to this problem lies within scientific collections. For some animals, the inspection of preserved specimens can reveal the scars of past antagonistic encounters, such as predation attempts. A common defensive behaviour that leaves scars on animals is autotomy, the loss of a body appendage to escape predation. By knowing the collection site of preserved specimens, it is possible to assess the influence of organismal biology and the surrounding environment in the occurrence of autotomy. We gathered data on tail loss for 8189 preserved specimens of 33 snake and 11 amphisbaenian species to investigate biological and environmental correlates of autotomy in reptiles. We applied generalized linear mixed effect models to evaluate whether body size, sex, life-stage, habitat use, activity pattern, biome, tropicality, temperature and precipitation affect the probability of tail loss in limbless reptiles. We observed autotomy in 23.6% of examined specimens, with 18.7% of amphisbaenian and 33.4% of snake specimens showing tail loss. The probability of tail loss did not differ between snakes and amphisbaenians, but it was higher among large-sized specimens, particularly in adults and females. Chance of tail loss was higher for diurnal and arboreal species, and among specimens collected in warmer regions, but it was unaffected by biome, precipitation, and tropicality. Autotomy in limbless reptiles was affected by size-dependent factors that interplay with ontogeny and sexual dimorphism, although size-independent effects of life-stage and sex also shaped behavioural responses to predators. The increase in probability of tail loss with verticality and diurnality suggests a risk-balance mechanism between species habitat use and activity pattern. Although autotomy is more likely in warmer regions, it seems unrelated to seasonal differences in snakes and amphisbaenians activity. Our findings reveal several processes related to predator-prey interactions involving limbless reptiles, demonstrating the importance of scientific collections to unveil ecological mechanisms at different spatio-temporal scales.

Northward shifts of the distributions of Spanish reptiles in association with climate change.

It is predicted that climate change will drive extinctions of some reptiles and that the number of these extinctions will depend on whether reptiles are able to change their distribution. Whether the latitudinal distribution of reptiles may change in response to increases in temperature is unknown. We used data on reptile distributions collected during the 20th century to analyze whether changes in the distributions of reptiles in Spain are associated with increases in temperature. We controlled for biases in sampling effort and found a mean, statistically significant, northward shift of the northern extent of reptile distributions of about 15.2 km from 1940-1975 to 1991-2005. The southern extent of the distributions did not change significantly. Thus, our results suggest that the latitudinal distributions of reptiles may be changing in response to climate change.

Collapse of the endemic lizard Podarcis pityusensis on the island of Ibiza mediated by an invasive snake.

The invasive snake Hemorrhois hippocrepis colonized the island of Ibiza (Balearic Islands) in 2003 as stowaways inside trunks of olive trees imported for gardening. It has quickly spread since 2010, posing a threat to the island's only remaining endemic vertebrate, the Ibiza wall lizard Podarcis pityusensis. We map the yearly expansion rate of the snake and estimate via transect surveys how severely it affects the distribution and abundance of the endemic lizard. As well, we surveyed 9 of 30 small lizard populations on islets surrounding Ibiza that have been isolated since the Last Glacial Maximum. Snakes had invaded 49% of Ibiza's land area by 2018, and censuses show a critical contrast in lizard abundance between areas with and without snakes; almost all censuses in areas without snakes show lizard presence whereas nearly all censuses in areas with H. hippocrepis lack lizard sightings. Moreover, at least one subspecies previously thriving on one of the offshore islets has become extinct, and there have been several snakes recorded swimming between Ibiza and the surrounding islets. Therefore, lizard populations have been dramatically reduced or have vanished within the range of the snake, and our results quantitatively support upgrading this species' threat level for extinction. This study can inform to programs to manage invasive snake populations and to conservation actions to recover the endemic lizard.

Modelling functional response of reptiles to fire in two Mediterranean forest types.

Fire is one of the main disturbances to terrestrial environments, transforming habitat structure and affecting community composition. Coupled with fire, forest type and vegetation structure modulate the taxonomic response to fire by ectotherm organisms such as reptiles. The response of each reptile species to fire is based on their functional attributes, which make some species resilient to fire and others vulnerable to that disturbance and only adapted to long-unburnt landscapes. We studied the functional response of a reptile community at 13 burnt sites within the African rim of the Western Mediterranean, and in two contrasting forest types, i.e. native cork oak forests (five sites) and pine plantations (eight sites). We compiled seven functional traits for the reptile species in the study areas, and quantified reptile functional diversity at each sampled plot. Variation in this index was examined from burnt to nearby unburnt plots, both in cork oak and pine forests, with generalized linear mixed models. Redundancy analysis was used to identify which functional traits were associated with particular plot types. We found 2149 individual reptiles from 15 species. The functional response of reptiles to fire was forest-type dependent: functional richness did not change with fire in cork oak forest plots, but increased with fire in the pine plantation ones. High reptile functional richness in cork oak plots was due to high species richness in this forest type. The functional-redundancy analysis showed that cork oak forest hosts a reptile community functionally composed of small Mediterranean ground- and rock-dwelling lizards. In pine plantation plots, however, saxicolous geckos and phytophagous tortoises indicate the availability of other microhabitat and food resources to be exploited by reptile species with different functional traits.

Reproduction ecology of the recently invasive snake Hemorrhois hippocrepis on the island of Ibiza.

Knowing the causes of biological invasion success can be relevant to combat future invasive processes. The recent invasion of the horseshoe whip snake Hemorrhois hippocrepis on the island of Ibiza provides the opportunity to compare natural history traits between invasive and source populations, and to unravel what makes this snake a successful invader that is threatening the only endemic vertebrate of the island, Podarcis pityusensis. This study compares the basic reproductive traits of mainland native and invasive populations of the snake. Our results revealed that invasive populations were characterized by female maturity at a smaller size, extended reproductive period, and much lower reproduction frequency compared to the native population. In contrast, some major reproductive traits-the abdominal fat body cycle, clutch size, hatchling body size, and hatchling body condition, did not differ between the two populations. Some of these results must reflect the environmental differences in the recently invaded island with respect to the source area, and overall plasticity of reproductive traits. Plasticity is evolutionarily interesting, and may aid the successful growth of this species in their invasiveness of Mediterranean islands like Ibiza. The most significant finding is that this expression of phenotypic plasticity occurred rapidly in this invasive population, within a period of 14 years maximum. Our results on the reproduction ecology of the invasive population were not conclusive regarding the factors determining the invasiveness of the snake and pointed to alternative causes.

Long-term trace element assessment after a mine spill: Pollution persistence and bioaccumulation in the trophic web.

Trace elements can be toxic when they cannot be easily removed after entering an ecosystem, so a long-term assessment is fundamental to guide ecosystem restoration after catastrophic pollution. In 1998, a pyrite mining accident in Aznalcóllar (south-western Spain) spilled toxic waste over a large area of the Guadiamar river basin, where, after restoration tasks, the Guadiamar Green Corridor was established. Eight years after the mine accident (2005-2006), the ground-dwelling insectivorous lizard Psammodromus algirus registered high trace-element levels within the study area compared to specimens from a nearby unpolluted control site. In 2017, 20 years after the accident, we repeated the sampling for this lizard species and also quantified trace elements in vegetation as well as in arthropod samples in order to identify remnant trace-element accumulation with the aim of assessing the transfer of these elements through the trophic web. We found remnant trace-element contamination in organisms of the polluted site compared to those from the unpolluted site. All trace-element concentrations were higher in arthropods than in plants, suggesting these compounds bioaccumulate through the trophic web. Lizards from the polluted areas had higher As, Cd, and Hg concentrations than did individuals from the unpolluted area. Lizard abundance between sampling periods (2005-06 and 2017) did not vary in unpolluted transects but strongly declined at polluted ones. By contrast, the Normalized Difference Vegetation Index indicated that in the study period, the vegetation was similar at the two sampling sites. These results suggest that, 20 years after the accident, the trace-element pollution could be the cause of a severe demographic decline of the lizard in the polluted area.

Bioaccumulation of heavy metals in the lizard Psammodromus algirus after a tailing-dam collapse in Aznalcóllar (Southwest Spain).

Quantification of heavy metal concentrations in biota is a common technique that helps environmental managers measure the level of pollutants circulating in ecosystems. Despite interest in heavy metals as indicators of localized pollution, few studies have assessed these pollutants in reptiles. In 1998, the tailing pond of a pyrite mine near Aznalcóllar (southwestern Spain), containing mud with high heavy metal concentrations, collapsed, releasing 6 million m(3) of toxic sludge into the Guadiamar Basin. Here we analyze heavy metal concentrations in the most common reptile in the area, the large psammodromus, Psammodromus algirus, a rather small lizard. We quantified levels of several elements (Hg, Sb, Cd, Cr, Tl, Sn, Ba, Cu, Pb, Sr, Mn, Rb, As, and Zn) in lizard tail clips collected in and around the affected area during the springs of 2005 and 2006. Samples were collected from two contaminated localities, one directly affected by the spill, and another adjacent to the tailing pond, but not covered by toxic mud. We also collected samples from a nonpolluted control site in the same basin. We found higher concentrations of As, Tl, Sn, Pb, Cd, and Cu in lizards from the affected area than in lizards from the control site, indicating the continued presence of heavy metal pollutants in the terrestrial food chain 8 years after the mine accident. We did not uncover sexual or annual differences in heavy metal concentrations, although concentrations increased with lizard size. We discuss how heavy metals moved across the food chain to lizards, despite intensive restoration efforts after the accident, and suggest that reptiles to be included in biomonitoring programs of heavy metals pollution in terrestrial habitats.

Ecological significance of dorsal polymorphism in a Batesian mimic snake.

Batesian mimicry is the process in which harmless species adopt the appearance of a dangerous, aposematic species. In some prey species, both Batesian mimetic and non-Batesian morphs coexist, presupposing that both morphs have to be evolutionarily advantageous. The viperine snake, Natrix maura, exhibits a zigzag dorsal pattern and antipredatory behavior that mimics European vipers. This snake also has a striped dorsal pattern that coexists with the zigzag pattern. We have examined whether individuals belonging to different geographically structured clades were more likely to exhibit a certain dorsal pattern, and whether the zigzag pattern has a protective function by exposing artificial snakes to predation in natural environments, in addition to comparing antipredatory behavior between zigzag and striped snakes also in natural environments. Our results indicate that the striped pattern was not geographically structured, but habitat-dependent. Aerial predators less frequently attacked zigzag plasticine models than striped or unpatterned models. We detected a shift in antipredator behavior between the 2 morphs, as Batesian mimicking N. maura responded to an approaching potential predator by remaining immobile or fleeing at shorter distances than did striped ones. We conclude that Batesian mimics maintain the cryptic and aposematic value by resembling vipers, whereas in open habitats the non-Batesian mimic has altered its antipredator behavior to maintain its fitness.

Loss of largest and oldest individuals of the Montpellier snake correlates with recent warming in the southeastern Iberian Peninsula.

The effects of climate change on organisms are now being extensively studied in many different taxa. However, the variation in body size, usually shrinkage in response to increasing temperature, has received little attention regarding to reptiles. During past periods of global warming, many organisms shrank in size, and current evidence and experiments manipulating temperature have shown a biomass decrease in some organisms with increasing temperatures. Here we test whether the body size of the Montpellier snake Malpolon monspessulanus from the southeastern Iberian Peninsula is changing and correlated with the increasing temperature in this region during a 39-year period (1976-2014). We measured the snout-vent length (SVL) of vouchers in scientific collections to check for trends in adult body size at the population level in relation with temperature, while controlling for the age of the individuals (estimated by skeletochronology, n =141). Given the great ontogenetic variation in body size of the study species, we categorized age in 3 classes: "young adults" (under 5 years old), "intermediate adults" (from 5 to 7 years old), and "old adults" (from 8 to 14 years old). By means of linear mixed models, we found a negative relationship between SVL of "old adults" and average annual temperature in the region during the lifetime of each individual. Our results indicate that largest and oldest individuals of the Montpellier Snake, that is, males because of strong sexual size dimorphism in this species, disappeared from the study population, and suggest that it occurred in response to rising environmental temperature.

Unravelling biodiversity, evolution and threats to conservation in the Sahara-Sahel.

Deserts and arid regions are generally perceived as bare and rather homogeneous areas of low diversity. The Sahara is the largest warm desert in the world and together with the arid Sahel displays high topographical and climatic heterogeneity, and has experienced recent and strong climatic oscillations that have greatly shifted biodiversity distribution and community composition. The large size, remoteness and long-term political instability of the Sahara-Sahel, have limited knowledge on its biodiversity. However, over the last decade, there have been an increasing number of published scientific studies based on modern geomatic and molecular tools, and broad sampling of taxa of these regions. This review tracks trends in knowledge about biodiversity patterns, processes and threats across the Sahara-Sahel, and anticipates needs for biodiversity research and conservation. Recent studies are changing completely the perception of regional biodiversity patterns. Instead of relatively low species diversity with distribution covering most of the region, studies now suggest a high rate of endemism and larger number of species, with much narrower and fragmented ranges, frequently limited to micro-hotspots of biodiversity. Molecular-based studies are also unravelling cryptic diversity associated with mountains, which together with recent distribution atlases, allows identifying integrative biogeographic patterns in biodiversity distribution. Mapping of multivariate environmental variation (at 1 km × 1 km resolution) of the region illustrates main biogeographical features of the Sahara-Sahel and supports recently hypothesised dispersal corridors and refugia. Micro-scale water-features present mostly in mountains have been associated with local biodiversity hotspots. However, the distribution of available data on vertebrates highlights current knowledge gaps that still apply to a large proportion of the Sahara-Sahel. Current research is providing insights into key evolutionary and ecological processes, including causes and timing of radiation and divergence for multiple taxa, and associating the onset of the Sahara with diversification processes for low-mobility vertebrates. Examples of phylogeographic patterns are showing the importance of allopatric speciation in the Sahara-Sahel, and this review presents a synthetic overview of the most commonly hypothesised diversification mechanisms. Studies are also stressing that biodiversity is threatened by increasing human activities in the region, including overhunting and natural resources prospection, and in the future by predicted global warming. A representation of areas of conflict, landmines, and natural resources extraction illustrates how human activities and regional insecurity are hampering biodiversity research and conservation. Although there are still numerous knowledge gaps for the optimised conservation of biodiversity in the region, a set of research priorities is provided to identify the framework data needed to support regional conservation planning.

Morphology matches mtDNA lineages in the southern smooth snake (Coronella girondica) from Iberia.

The rise of molecular techniques in the study of evolutionary histories has resulted in a gradual abandonment of morphological characters as the only sources of phylogenetic inference. However, morphological characters may be valuable for phylogenetic reconstruction, especially for tracking adaptive changes across phylogeographic groups defined by genetic markers. We examined the discriminative power of morphological characters between four mitochondrial clades covering almost the entire distribution area of the smooth snake Coronella girondica in the Western Mediterranean. We detected three characters showing sexual dimorphism (relative tail length, number of ventral and of subcaudal scale counts) and, more interestingly, two characters (number of subcaudal and of dorsal rows) displaying interclade differences. Almost all C. girondica examined had 21 dorsal rows except those from a narrow coastal belt in the south-eastern Iberian Peninsula, which had 19 dorsal rows. The distribution of these specimens matches a mitochondrial clade that originated approximately 1.4-2.0 million years ago. Both of these morphological characters support a Betic lineage with a rather well-defined contact zone with the other Iberian lineage, which has been maintained even without the existence of current geographic barriers. The long-term survival of the Betic lineage throughout the Pleistocene climatic oscillations suggests a systematic revision within C. girondica.

Patterns of tail breakage in the ladder snake (Rhinechis scalaris) reflect differential predation pressure according to body size.

Predator-prey interactions are key factors in the evolution of defensive tactics. In snakes, shy organisms from which direct evidence of predator-prey interactions is difficult to obtain, injuries are potential indicators of both the nature and frequency of interactions. We studied the incidence of tail breakage and body scarring in the ladder snake, Rhinechis scalaris, an actively foraging Mediterranean snake, and tested several hypotheses that link body injuries and snake life-history traits, mainly under sexual and ontogenetic aspects. Evidence is presented supporting an ontogenetic shift in the frequency of tail breakage, with the incidence of tail loss increasing as a logistic function of snake size. We relate this finding to the adaptive significance of ontogenetic shifts in dorsal pattern and the reaction of snakes to approaching predators; small individuals are more likely to remain immobile than are medium to large individuals, the former aided by a concealing dorsal pattern with transverse lines, and the latter by a striped pattern. This species exhibited sex differences in body scarring but not in tail breakage, nor did we encounter evidence to suggest that snakes experience multiple tail breaks over time, thus failing to support the sexual difference and multiple tail breakage hypotheses. Moreover, we failed to find a lower frequency of body scarring than tail breakage; hence, our results do not afford evidence that frequency of tail breakage represents an inefficiency of predators in catching or dispatching ophidian prey.