Podarcis Sicula Research Articles

Eaten or beaten? Severe population decline of the invasive lizard Podarcis siculus (Rafinesque-Schmaltz, 1810) after an eradication project in Athens, Greece

Invasive species have been recognised as an important hazard to native communities. Amongst the mitigation measures that have been proposed to confront biological invasions, eradication projects are certainly the most drastic. In this short communication, a successful eradication project against a recently established population of the Italian wall lizard (Podarcissiculus) in Athens, Greece, is reported. To this aim, the Hellenic Herpetological Society received unforeseen aid from stray cats and, possibly, from the Οcellated skink (Chalcidesocellatus) and vegetation growth. Within three years, the initial thriving P.siculus population has shrunk to very few individuals.

Notes on egg and hatchling size in Podarcis siculus (Squamata: Lacertidae) from central Italy

Notes on egg and hatchling size in Podarcis siculus (Squamata: Lacertidae) from central Italy

How Glyphosate Impairs Liver Condition in the Field Lizard Podarcis siculus (Rafinesque-Schmaltz, 1810): Histological and Molecular Evidence.

The potential toxicity of glyphosate, a widely used broad-spectrum herbicide, is currently a great matter of debate. As vertebrate insectivores, lizards protect plants from herbivorous insects increasing plant biomass via the trophic cascade and represent an important link between invertebrates and higher predators. A negative effect of glyphosate on lizards' survival could have major impacts at the ecological levels. In this study, we investigated the effects of the exposure to low doses of glyphosate on the liver of the wall lizard Podarcis siculus, a suitable bioindicator of soil pollution. Two different doses of pure glyphosate (0.05 and 0.5 μg/kg body weight) were orally administered every other day for 3 weeks to sexually mature males and females. The results demonstrated that both doses, despite being very low, are toxic for the liver that showed clear signs of suffering, regardless of sex. The histological analysis provided a scenario of severe hepatic condition, which degenerated until the appearance of fibrotic formations. The morphological observations were consistent with a loss of liver physiological functions. Immunocytochemical investigations allowed us to detect an involvement of antioxidant/cytoprotective proteins, such as superoxide dismutase 1 (Cu/Zn SOD, known as SOD1), glutathione peroxidase 1 (GPx1), metallothionein (MT), and tumor suppressor protein 53, (p53) suggesting that the liver was trying to react against stress signals and damage induced by glyphosate. Finally, in situ hybridization and Real-Time PCR analysis showed the upregulation of estrogen receptor α and vitellogenin gene expression, thus demonstrating the xenoestrogenic action of glyphosate. The imbalance of the hormonal homeostasis could threaten the lizards' reproductive fitness and survival, altering the trophic cascade.

Can behaviour explain invasion success? A comparison between sympatric invasive and native lizards

To reduce the impact of biological invasions, we need to understand the behavioural mechanisms that enable some species to be successful invaders. Testing differences in behaviour between sympatric congeneric species with different invasive potential is an opportunity to study specific behavioural traits associated with invasion success. Using the invasive Italian wall lizard, Podarcis sicula, and a noninvasive congeneric, the green Iberian wall lizard, Podarcis virescens, which live in sympatry in a location that is novel for P. sicula, we tested their exploratory behaviour, neophobia and boldness: all traits that should promote invasion success. The invasive P. sicula was more exploratory, bold and neophilic than the sympatric native P. virescens. Native lizards had highly repeatable behaviour, whereas in P. sicula boldness was the only behavioural trait that was repeatable. The behavioural traits of the native species, but not the invasive species, were correlated. A lack of correlation between behavioural traits, as well as a lack of repeatability in two of the three behavioural traits, suggests higher levels of behavioural plasticity in P. sicula, which may also explain the success of this lizard during invasions. Our experiment highlights the potential importance of behavioural traits in invasions and provides insight into why P. sicula is such a successful invader.

Coexisting lacertid lizard species Podarcis siculus and Podarcis melisellensis differ in dopamine brain concentrations.

In the eastern Adriatic, Podarcis siculus, an invasive species, competitively excludes the native Podarcis melisellensis. Monoamine neurotransmitters-serotonin (5HT), dopamine (DA), and noradrenaline (NA)-are implicated in social behavior, and could lie at the basis of the direct behavioral interference of P. siculus with P. melisellensis. To understand the relationship between social behavior and monoamines, as well as the differences in behavior between P. siculus and P. melisellensis, we developed a high-performance liquid chromatography (UV/VIS detection) method with which we were able to reliably measure concentrations of 5HT, DA, and NA in 32 brains of the two lizard species. We observed no statistically significant influence of species, sex, or their interaction on brain NA and 5HT concentrations. Statistically significant influence of species on dopamine levels were recorded, with P. siculus having twice as much dopamine in their brains. Taking into account that asignificant aggressive relationship, with P. siculus dominating over P. melisellensis, has been previously observed, and that dopamine directly influences this behavior, the observed differences in dopamine levels could represent a trait in these species and may contribute to the competitive exclusion of P. melisellensis by P. siculus in the eastern Adriatic.

Seasonal and pharmaceutical-induced changes in selenoprotein glutathione peroxidase 4 activity in the reproductive dynamics of the soil biosentinel Podarcis sicula (Chordata: Reptilia).

There is rising concern for the interaction of environmental contaminants with brain transcriptome and the potential effect on reproductive processes. The present study sought to determine selenoprotein glutathione peroxidase 4 (gpx4) transcriptional activity in the brain and testis of the soil biosentinel, Podarcis sicula, through the main phases of the reproductive cycle and whether pharmaceuticals exert an endocrine disruption. Based on gpx4 cloned amminoacids sequence (GenBank AEX09236.1.), we used a bioinformatic approach to assess the structural role. Specifically, we detected seasonally the reactive oxygen species (ROS) level using electron spin resonance spectroscopy and gpx4 transcriptional activity using quantitative real-time polymerase chain reaction. In addition, the impact of pharmaceuticals was assessed after 21-days of treatment with ICI 182,780 and human chorionic gonadotropin administration in mating and winter stasis, respectively. Bioinformatic data shows the gpx4 proteic activity and a phylogenetic profile. ROS contents in lizard brain are significantly less than in testis and display higher levels after treatments. Brain gpx4 expression gives statistically significant seasonal differences, opposite trends in testis and altered expression in both tissues, with evidence of testis morphological and DNA disruption. Taken together, these results provide direct evidence that gpx4 in P. sicula plays a seasonal regulatory role and may be a reliable biomarker for reproductive health toxicity screening.

Health status of the lizard Podarcis siculus (Rafinesque-Schmaltz, 1810) subject to different anthropogenic pressures

The terrestrial lizard Podarcis siculus is the most abundant reptile in Italy, where is considered a ubiquitous species. This lizard is widely distributed from the islands to the Apennines, from cultivated fields to anthropized areas such as gardens and city parks. For this reason, these animals are exposed to extensive physical and chemical stresses, as well as to the possibility of coming into contact with industrial pollutants and substances used in agricultural practices. Here, we review the health status of lizard specimens inhabiting natural non-anthropized areas and fields devoted to organic farming, considering the condition of (1) liver, representing the main detoxifying organ, directly influenced by feeding, and (2) gonads, essential for reproduction and, therefore, for the survival of the species. The morphological and biomolecular condition of these organs was then compared with those obtained from lizard specimens experimentally treated with nonylphenol, a co-formulant of many insecticides and plant protection products widely used in conventional farming, known to have harmful estrogenic effects. Taken together, data demonstrate that lizards inhabiting manured soil are in good health status and show a regular morphology of liver, testis, and ovary. Animals are found to be less exposed to the toxic heavy metals cadmium and lead if compared with specimens collected in areas not devoted to agriculture, but probably more exposed to vehicular traffic. However, manure, as well as nonylphenol, exerts a xeno-estrogenic effect, particularly evident in male specimens, more sensitive to estrogenic contamination.

Borrelia burgdorferi (sensu lato) in ectoparasites and reptiles in southern Italy

BackgroundBorrelia burgdorferi (sensu lato) is a complex containing pathogenic bacteria of which some species, such as Borrelia lusitaniae, use birds, small mammals and reptiles as reservoirs. In Italy, the bacteria have been detected in reptilian and avian reservoirs in the northern and central regions.ResultsHere, 211 reptiles from three orders [Squamata (Sauria with seven species in five families and Ophidia with 11 species in three families), Crocodylia (one family and two species), and Testudines (two families and two species)] were examined for ectoparasites and molecular detection of B. burgdorferi (s.l.) in three different sites of southern Italy, an area for which no information was previously available on the occurrence of borreliosis in animals and humans. Borrelia lusitaniae was molecularly detected in larvae and nymphs (11.6%) of Ixodes ricinus infesting lizards (i.e. Podarcis muralis, Podarcis siculus and Lacerta bilineata) and in 12.3% blood samples of P. siculus. Finally, B. lusitaniae and Borrelia garinii were detected in 5.1% (32/630) of questing I. ricinus.ConclusionsThese results show the circulation of B. lusitaniae in southern Italy and suggest that P. siculus could play a role as a reservoir, representing a potential medical threat to humans living in or visiting these localities.

Aromatase immunolocalization and activity in the lizard's brain: Dynamic changes during the reproductive cycle

The purpose of the present study is to highlight the role of aromatase in the neuroendocrine control of the reproductive cycle of the male lizard Podarcis sicula during the three significant phases, i.e. the pre-reproductive, reproductive, and post-reproductive stages. Using immunohistochemical, biochemical, and hormonal tools, we have determined the localization and the activity of P450 aromatase (P450 aro) in the lizard's brain together with the determination of hormonal profile of sex steroids, i.e. testosterone and 17β-estradiol. The present data demonstrated that the localization of P450 is shown in brain regions involved in the regulation of the reproductive behavior (medial septum, preoptic area, and hypothalamus). Its activity, as well as the intensity of the signal, is modified according to the period of reproduction, resulting in functional dynamic changes. P450 aro activity and signal intensity decrease in the pre-reproductive period and progressively increase during the reproductive stage until it reaches the maximum peak level at the post-reproductive phase. P450 aro determines a local estrogen synthesis, balancing the testosterone and estradiol levels, and therefore its role is crucial, since it plays an important role in the neuroendocrine/behavioral regulation of the reproductive processes in the male lizard P. sicula.

The Potential Distribution and Morphological Data of <i>Podarcis siculus</i> (Rafinesque-Schmalstz, 1810) with New Locality Records from Turkey (Squamata: Sauria: Lacertidae)

In the present study, we contributed to knowledge of distribution of the Italian wall lizard, P. siculus in Turkey. Besides, we gave some morphological data about species from Akcakoca population. The morphological data of the specimens from Akcakoca were generally found to be similar with the known literature. Only some morphological characteristics were observed to be different from the features given in the literature. The mean of supraciliar granules (SCG) was found lower and the mean of median gularia (MG) was found to be higher than the mean values given in the literature. In addition, we found high percentage of five supralabial plates in anterior of oculars. The distribution of the species was found to be restricted between northeastern Marmara and western Black Sea regions, according to our distributional model. On the other hand, the distributional data of P. siculus in the present study exhibited that Canakkale and Samsun have not suitable habitats for the species. High AUC and lover standard deviation values (0.986 ± 0.006) showed that the potential distribution area of the species was congruent with its habitat preferences inhabited localities.

Bacteria and parasites in Podarcis sicula and P. sicula klemmerii

BackgroundNew epidemiological data on bacterial and parasitic infections in 24 Italian wall lizards, namely Podarcis sicula (mainland population) and P. sicula klemmerii (insular population) in southern Italy were provided. To achieve this goal, samples were collected from individuals belonging to the two populations and analysed by microbiological and parasitological methods.ResultsA wide range of bacteria (e.g. Pantoea spp., Citrobacter spp., Morganella spp., Pseudomonas, Enterobacter spp., Staphylococcus spp. and Escherichia coli) and parasites (e.g. Ophionyssus natricis, coccidia, Dicrocoelidae) were detected in both P. sicula and P. sicula klemmerii individuals. Insular population presented similar bacterial and parasitic diversity to its mainland counterpart. Ampicillin was the antimicrobial with the highest resistance rate.ConclusionThis study highlighted various bacteria and parasites, some of them potentially zoonotic. Further studies are needed to better understand the epidemiology and transmission routes of these pathogens along with their impact on the welfare and behaviour of Italian wall lizards.

Thermal tolerance varies with age and sex for the nonnative Italian Wall Lizard (Podarcis siculus) in Southern California

Temperature has a substantial effect on both the physiology and behavior of ectothermic animals such as lizards. Physiology and behavior can also be influenced by ontogenetic and sex differences, but these effects are largely understudied in lizards. We examined ontogenetic and sex-based differences in thermal tolerances, preferred temperature, and temperature-dependent evaporative water loss rates in Italian Wall Lizards, Podarcis siculus, collected from an introduced population near Los Angeles, California, USA that were acclimated to laboratory conditions. Podarcis siculus has been introduced to multiple localities in the USA and the Mediterranean region and has demonstrated remarkable ability to adapt to novel climatic conditions. In the California population, adults of both sexes had a higher critical thermal maximum (CTmax) than juveniles, and adult females had a lower critical thermal minimum (CTmin) than juveniles and adult males. Thus, adult females had a significantly wider thermal breadth (CTmax - CTmin) compared to adult males and juveniles. Mass-specific evaporative water loss was higher in juveniles compared to adult males at intermediate temperatures. There was no significant difference among groups for preferred temperature. This implies that thermal tolerance, a physiological characteristic, varies with age and sex for this population, whereas thermal preference, a behavioral characteristic, does not. Interestingly, CTmin for all age and sex classes was above temperatures likely experienced by some nonnative populations in winter, suggesting individuals need to find urban thermal retreats. These results add to the growing literature demonstrating that thermal tolerances and breadths can vary between sexes and across age classes in squamate species.

Spotlight on islands: on the origin and diversification of an ancient lineage of the Italian wall lizard Podarcis siculus in the western Pontine Islands

Groups of proximate continental islands may conceal more tangled phylogeographic patterns than oceanic archipelagos as a consequence of repeated sea level changes, which allow populations to experience gene flow during periods of low sea level stands and isolation by vicariant mechanisms during periods of high sea level stands. Here, we describe for the first time an ancient and diverging lineage of the Italian wall lizard Podarcis siculus from the western Pontine Islands. We used nuclear and mitochondrial DNA sequences of 156 individuals with the aim of unraveling their phylogenetic position, while microsatellite loci were used to test several a priori insular biogeographic models of migration with empirical data. Our results suggest that the western Pontine populations colonized the islands early during their Pliocene volcanic formation, while populations from the eastern Pontine Islands seem to have been introduced recently. The inter-island genetic makeup indicates an important role of historical migration, probably due to glacial land bridges connecting islands followed by a recent vicariant mechanism of isolation. Moreover, the most supported migration model predicted higher gene flow among islands which are geographically arranged in parallel. Considering the threatened status of small insular endemic populations, we suggest this new evolutionarily independent unit be given priority in conservation efforts.

Learning from others: an invasive lizard uses social information from both conspecifics and heterospecifics.

Species that are able to solve novel problems through social learning from either a conspecific or a heterospecific may gain a significant advantage in new environments. We tested the ability of a highly successful invasive species, the Italian wall lizard Podarcis sicula, to solve a novel foraging task when social information was available from both a conspecific and an unfamiliar heterospecific (Podarcis bocagei). We found that Italian wall lizards that had access to social information made fewer errors, regardless of whether the demonstrator was a conspecific or a heterospecific, compared to Italian wall lizards that individually learnt the same task. We suggest that social learning could be a previously underappreciated, advantageous mechanism facilitating invasions.

Where to live in Lisbon: urban habitat used by the introduced Italian wall lizard (<em>Podarcis siculus</em>)

Exotic animal invasions constitute a major threat to biodiversity worldwide. Our assessment determined the core range occupied by the Italian wall lizard (Podarcis siculus) in the urban area of Parque das Nações (Lisbon, Portugal), where it was accidentally introduced two decades ago. Des-pite the apparent current scenario of non-expansion, the alien species interferes with the local distribution pattern of the native P. virescens, with both lizard species shown to use the available microhabitats differently. The native P. virescens population displays an overall heterogeneous distribution in the urban matrix. On the other hand, the occupancy of the exotic species clusters within the original area of introduction (garden in front of the Lisbon Oceanarium), as well as in adjacent gardens. There, P. siculus replaced the native P. virescens as the only lizard species present. Appa-rently, there is no known reason there that prevents the alien lizard from colonizing more available geographic area and expanding.

Quantity Discrimination in Trained Lizards (Podarcis sicula).

Quantitative abilities have been reported in many animal species. Two main methods have been extensively used: spontaneous choice tests and training procedures. A recent study showed that ruin lizards are capable of spontaneously discriminating between the surface area of two food items of different size, but failed when food was presented in sets of discrete items differing in number. In the present study, we used a training procedure to further investigate quantitative abilities in ruin lizards. Subjects were presented with two sets of yellow disks differing either in number (Experiment 1) or in area (Experiment 2) and were trained on different discriminations of increasing difficulty (1 vs. 4, 2 vs. 4, and 2 vs. 3). Results showed that lizards were more accurate in discriminating sets of discrete items differing in number than the area of two individual items, in contrast to what had earlier been observed in spontaneous choice tests. Although we cannot exclude other factors that affected the performance of ruin lizards, the poor accuracy here observed in both experiments might reflect a true limit in lizards’ quantitative abilities.

Reproductive expression dynamics and comparative toxicological perspective of beta estrogen receptor gene in the male wall lizard, Podarcis sicula Rafinesque, 1810 (Chordata: Reptilia)

Over the last few decades, due to its relevant function in male reproduction assessment, important molecular achievements have been made in the molecular characterization of estrogen receptor genes in various species. Our work focuses on a male seasonal breeder, the bioindicator Podarcis sicula, because of its peculiar gonadal anatomy, similar to that of humans. Based on the cloned lizard’s gene sequence fragment of estrogen receptor beta, esr2 (GenBank JN705543.1), we found DNA binding domain identity of 99% as well as a homologous sequence with humans. Furthermore, in order to better illustrate how this gene is regulated in the lizard’s reproductive system organs, we investigated the transcriptional activity of esr2 in brain and testis tissues during mating and winter stasis phases of the reproductive cycle. Quantitative real time-polymerase chain reaction (qRT-PCR) analyses performed on male gonadal tissues demonstrate a significant increase in esr2 expression during mating compared to the winter stasis period, while in the brain, esr2 shows the opposite trend. Next, we provide morphological evidence of the detrimental effect on spermatogenesis of a pure anti-estrogen treatment (ICI 182,780) and the corresponding effect on esr2 expression in lizard specimens during the mating period which, upon treatment, was found to be no different from the expression levels in winter stasis both in the brain and in the testis. In this study, we explore the potential use of Podarcis sicula as a model for human testis development and maturation, as well as esr2 expression for toxicological screening in one-testis gonadectomy.

Immunocompetence and parasite infestation in a melanistic and normally-coloured population of the lacertid lizard, Podarcis siculus

Abstract Melanism is the occurrence of individuals that are darker in skin pigmentation than their conspecifics, which is a common colour polymorphism among vertebrates. Due to the pleotropic effects of the POMC gene that is responsible for melanin-based colouration, dark pigmentation often co-varies with a range of other phenotypic traits. Still, not much is known on the link between melanin-based colouration and immunity in lizards. In this study, we examined and compared the immunocompetence and degree of ectoparasite infestation of Podarcis siculus lizards from a fully melanistic population on an islet in the Tyrrhenian Sea, with conspecifics from a ‘normally’-coloured population on the mainland. Our findings show that both males and females from the melanistic population were less parasitized by ectoparasites and had a greater cellular immune response to a phytohemagglutinin injection than normally-coloured conspecifics. This outcome is in line with the “genetic link hypothesis”, which predicts that melanistic individuals will be more resistant to parasites than non-melanistic individuals due to the pleiotropic POMC gene. In addition, we found correlative evidence for a link between ectoparasite load and PHA immune response, but this was only true for males from the normally-coloured population. Immunological data on additional melanistic and non-melanistic populations of Podarcis siculus in the Mediterranean basin would provide us better insight into patterns of co-variation between immunity and melanism in lizards.

Better to be resident, larger or coloured? Experimental analysis on intraspecific aggression in the ruin lizard

AbstractTerritoriality evolves when the benefits gained from exclusive access to limited resources exceed the costs of defence. Sometimes animals evolve distinct morphs, that may reflect different capability, and in some territorial species of lizards the polymorphism is associated to alternative strategies, both for reproductive efficiency and territorial dominance. It is known that normally larger males are more aggressive and are able to defend a larger area and for longer than small males; in fact this dynamic is widespread in many animal species including the genus Podarcis. The aim of our study was to test which factors determine the outcome of fighting in the strongly territorial Italian ruin lizard, Podarcis siculus, using two types of contests: (1) resident versus intruder and (2) in a neutral arena. Furthermore, because these lizards are characterized by strong ventral colour variability, usually restricted to jaws and throat, we wanted to investigate if coloured lizards have higher chances at winning than white lizards. The results showed that the fight's result was significantly influenced by the state of residence, while the colour had no effect; instead, the snout to vent length difference between opponents had significant influence on the outcome in the neutral arena. Our results suggest that, in this lizard, both the size and the state of residency, no matter of colour, play an important role to determine the outcome of a fight, however, highly depending on the contest. We think that P. siculus should be object of future studies, focusing on behavioural and ecological aspects, even considering the occurrence of different colours within and among populations.

Testicular steroidogenic enzymes in the lizard Podarcis sicula during the spermatogenic cycle

Steroidogenic Acute Regulatory protein (StAR), 3β-hydroxysteroid dehydrogenase (3β-HSD), 17β-hydroxysteroid dehydrogenase (17β-HSD), 5α-Reductase (5α-Red), P450 aromatase are key enzymes involved in steroidogenesis. Recently, we showed the expression and the localization of P450 aromatase in Podarcis sicula testis during the different phases of the reproductive cycle, showing its involvement in the control of steroidogenesis, particularly in 17β-estradiol synthesis. Now, we have investigated the presence and distribution of the other enzymes involved in steroidogenesis, i.e. StAR, 3β-HSD, 17β-HSD and 5α-Red, during three significant periods of the reproductive cycle: summer stasis (July–August), autumnal resumption (November) and reproductive period (May–June). We demonstrated for the first time that all these enzymes are always present in somatic cells (Leydig and Sertoli) and germ cells (spermatogonia, spermatocytes I and II, spermatids and spermatozoa) of Podarcis testis, mainly in spermatids and spermatozoa. The present results strongly suggest that in Podarcis testis both somatic and germ cells could be involved in local sex hormone synthesis and that 5α-Red and P450 could carry out a pivot role.