Lacertid Research Articles

The use of a lacertid lizard as a model for reptile ecotoxicology studies: Part 2 – Biomarkers of exposure and toxicity among pesticide exposed lizards

As part of a wider study examining the impacts of corn pesticides on lacertid lizards in north-western Portugal, we examined various physiological, biochemical, and histological biomarkers of exposure and effect among field populations of Podarcis bocagei. Biomarkers included body condition index, standard metabolic rate, locomotor performance, parasitization, glutathione oxidative pathways and related enzyme activity, lipid peroxidation and liver and testis histology. Few of the various biomarkers investigated provided statistically significant evidence of toxic effect. However, using a weight of evidence approach, we conclude that pesticides are affecting lizards living in the vicinity of pesticide exposed corn agriculture sites. Lizards from these locations present a profile of animals under metabolic stress with reduced condition indices, increased standard metabolic rate, lower incidence of hepatocyte vacuolation, altered iron metabolism, increased activation of GSH oxidation pathways, and even increased prevalence of hemoparasites.

The use of a lacertid lizard as a model for reptile ecotoxicology studies - Part 1 Field demographics and morphology

At the European level, lacertid lizards have been proposed as potential model species for reptile ecotoxicology. We studied demographic and morphological aspects of natural field subpopulations of Podarcis bocagei inhabiting similar agricultural habitats which were either regularly exposed to pesticides, or not. Parameters examined in this study included population size and density, sex ratio, adult body size, fluctuating asymmetry in femoral pores and parasite prevalence. In general, we detected few statistically significant differences between the exposed and reference subpopulations. Although field situations are ecologically complex and factors other than pesticides may be acting, the absence of observable effects on field subpopulations is probably indicative that lizards are coping or compensating for this level of exposure.

Incidence patterns of ectodermic lesions in wild populations of Common Wall Lizard (Podarcis muralis)

Skin lesions frequently present in adult lizards may be due to a variety of causes, both physical and infectious, including excessively high humidity and environmental temperature, malnutrition, concurrent disease etc. On the other hand, skin lesions in lizards could be simple evidence of various behavioural patterns and biotic interactions. However, studies on frequencies of dermal lesions and their anatomical and environmental correlates in lacertid lizards are rare. Here, we use Podarcis muralis to analyse the relations between occurrence of ectodermal lesions and three possible indicators of environmental stress (body condition index – BCI, infestation by ticks and tail condition) by evaluating differences among local populations at uni- and multivariate level. Our results showed that BCI, together with body size and sexual size dimorphism, varied between populations but had no direct influence on the presence of lesions. Males had higher frequencies of lesions and ticks but lower frequencies of broken tails than females. All three parameters varied between sites likely due to differences in predation/parasite exposures and agonistic interactions with conspecifics between sexes and populations. Results of multivariate analyses suggested that the occurrence of lesions is decoupled from the other morphological stress indicators. Detected associations indicated that relations between presence of lesions and other analysed variables are rather complex. Directions for further research on ectodermal lesions in lacertid lizards are provided.

Synopsis of the helminth communities of the lacertid lizards from the Balearic and Canary Islands

Helminth communities of reptiles have usually been considered as depauperate and isolationist, with low abundance and species richness when compared to other vertebrates. Nevertheless there are some insular reptile populations in which this general rule is not fulfilled. In this study, we compare helminth faunas from two groups of lizards living in two different archipelagos and having different feeding habits. Lacertid lizards from Canary Islands, belonging to the endemic genus Gallotia, showed by contrast with other lacertids, a tendency to high consumption of plant matter and to rich and diverse helminth communities. Differences were found even between the lizards living in different islands, being the “giant lizard” G. stehlini the most herbivorous and G. atlantica the most carnivorous. Podarcis spp. from Balearic Islands showed lower tendency to herbivory which was not mirrored in their helminth communities. The composition and structure of helminth communities of lacertid lizards from both archipelagos are related to the conditions of insularity and the phylogeny of the hosts.

Extreme genetic diversity in the lizard Atlantolacerta andreanskyi (Werner, 1929): a montane cryptic species complex.

BackgroundAtlantolacerta andreanskyi is an enigmatic lacertid lizard that, according to the most recent molecular analyses, belongs to the tribe Eremiadini, family Lacertidae. It is a mountain specialist, restricted to areas above 2400 m of the High Atlas Mountains of Morocco with apparently no connection between the different populations. In order to investigate its phylogeography, 92 specimens of A. andreanskyi were analyzed from eight different populations across the distribution range of the species for up to 1108 base pairs of mitochondrial DNA (12S, ND4 and flanking tRNA-His) and 2585 base pairs of nuclear DNA including five loci (PDC, ACM4, C-MOS, RAG1, MC1R).ResultsThe results obtained with both concatenated and coalescent approaches and clustering methods, clearly show that all the populations analyzed present a very high level of genetic differentiation for the mitochondrial markers used and are also generally differentiated at the nuclear level.ConclusionsThese results indicate that A. andreanskyi is an additional example of a montane species complex.

A molecular phylogeny of the eastern group of ocellated lizard genus Timon (Sauria: Lacertidae) based on mitochondrial and nuclear DNA sequences

Timon, a small genus of lacertid lizards, includes four species distributed in two separate ranges in the western and eastern part of the Mediterranean Basin. Phylogenetic relationships between the two groups have not been resolved, and the taxonomic situation of the two subspecies of the eastern representative of the genus, Timon princeps, is not clear. To address these questions, partial DNA sequences of two nuclear (β-fibrinogen intron 7 and C-mos) and three mitochondrial (cytochrome b, 12S rRNA and 16S rRNA) genes were analyzed. Based on the high genetic distance between the two subspecies of T. princeps we promote their taxonomic status to full species, Timon princeps and Timon kurdistanicus. Divergence time estimates based on other lacertid species suggest that the separation of the green (Lacerta) and ocellated (Timon) lizards took place around 12 My ago, and that the Eastern group underwent speciation around 4-5 my ago, perhaps associated with the uplifting of the Zagros mountains. As expected given this ancient divergence and complex paleogeography, considerable levels of genetic diversity are recovered within both taxa, with geographically close individuals showing very divergent haplotypes.

Tail tip removal for tissue sampling has no short-term effects on microhabitat selection by Podarcis bocagei , but induced autotomy does

Tail tip removal is a common method for obtaining tissue samples for genetics and other studies on lizards. This study evaluates the effect of tail tip autot- omy on microhabitat selection in the lacertid Podarcis bocagei. Different-length tail fragments were experimentally removed from lizards of a small population. Forc- ing lizards to autotomise small tail tips ( 5 cm). After autotomy these lizards were observed to favour more closed habitats, where predator avoidance is expected to be more efficient, although of potentially lower thermal quality.

Thermal constraints on embryonic development as a proximate cause for elevational range limits in two Mediterranean lacertid lizards

Local adaptation and range restrictions in alpine environments are central topics in biogeographic research with important implications for predicting impacts of global climate change on organisms. Temperature is strongly coupled to elevation and greatly affects life history traits of oviparous reptiles in mountain environments. Thus, species may encounter barriers for expanding their ranges if they are unable to adapt to the changing thermal conditions encountered along elevational gradients. We sought to determine whether thermal requirements for embryonic development provide a plausible explanation for elevational range limits of two species of lacertid lizards that have complementary elevational ranges in a Mediterranean mountain range (Psammodromus algirus is found at elevations below 1600 m and Iberolacerta cyreni is found at elevations above 1600 m). We combined experimental incubation of eggs in the laboratory with modelled estimates of nest temperature in the field. In both species, increasing temperature accelerated development and produced earlier hatching dates. The species associated with warmer environments (P. algirus) experienced an excessive hatching delay under the lowest incubation temperature. Moreover, newborns from eggs incubated at low temperatures showed poor body condition and very slow rates of postnatal growth. In contrast, eggs of the strictly alpine species I. cyreni exhibited shorter incubation periods than P. algirus that allowed hatching before the end of the active season even under low incubation temperatures. This was countered by lower reproductive success at higher temperatures, due to lower hatching rates and higher incidence of abnormal phenotypes. Elevational range limits of both species coincided well with threshold temperatures for deleterious effects on embryonic development. We suggest that incubation temperature is a major ecophysiological factor determining the elevational range limits of these oviparous lizards with predictable consequences for mountain distributions under future warmer climates.

Population density of syntopic, differently sized lizards in three fragmented woodlands from Mediterranean Central Italy

The population density of three lacertid lizards (Podarcis sicula, Podarcis muralis, Lacerta viridis) was studied along several transects crossing agro-forest habitats in Mediterranean central Italy. Overall, seven transects, in three different wooded patches, were walked for lizards. Distance sampling (with uniform model design) was applied to the dataset in order to calculate population size, dispersion, and coefficient of variation at each site. In order to detect which factors may influence lizard density, a Generalized Linear Model (GLZ; multinomial distribution and cumulative log link function) was built, with environmental variables and density of predators’ variables being included in the model as covariates (scale predictor). Density of the three lizard species differed significantly among study sites, evidencing species-specific responses to local patch conditions. None of the environmental variables taken separately in the GLZ model influenced significantly the lizard densities, whereas lizards densities showed species-specific response to the considered environmental variables. The largest species (L. viridis) showed the highest density in the fragment with the most irregular shape and largest wood size, whereas the two smaller Podarcis species presented their highest population density in the site with the smallest wood patch and with a very low snake density. Density of P. sicula was negatively correlated with both the woodland area and Colubridae density, and was positively correlated with woodland shape (i.e. with circularity).

Morphology of the Podarcis wall lizards (Squamata: Lacertidae) from the Iberian Peninsula and North Africa: patterns of variation in a putative cryptic species complex

Cryptic species complexes represent groups that have been classified as a single species, because of the difficulty in distinguishing its members morphologically. Morphological investigation following the discovery of cryptic diversity is crucial for describing and conserving biodiversity. Here we present a detailed account of morphological variation in a group of Iberian and North African Podarcis wall lizards of the family Lacertidae, trying to elucidate the morphological patterns observed between known mitochondrial lineages. Our results reveal very high morphological variation within lineages, considering both biometric and pholidotic traits, but also indicate that lineages are significantly different from each other. The main sources of variation, both globally and between lineages, arise from body size, head dimensions, and limb length, possibly pointing to underlying ecological mechanisms. A combination of body size, body shape, and continuous pholidotic traits allows a relatively good discrimination between groups, especially when comparing one group with the rest or pairs of groups. However, ranges of variation greatly overlap between groups, thereby not allowing the establishment of diagnostic traits. The high morphological variation observed indicates that external morphology is not particularly useful for species delimitation in this group of lizards, as local adaptation seems to play a major role in within- and between-group differentiation. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 164, 173–193.

Intraspecific Variation of Reproductive Traits in a Mediterranean Lizard: Clutch, Population, and Lineage Effects

Widely distributed terrestrial ectotherms from the southern European peninsulas show patterns of subdivision (related to isolation in temperate refugia) that allow us to test the relative importance of phylogeographic lineage, population of origin and familial effects as sources of variation for life-history traits. We collected gravid females from 15 geographically separated populations of the lacertid lizard Psammodromus algirus, a widely distributed species with well differentiated eastern and western lineages. We incubated eggs under two treatments of constant (28°C) and fluctuating (28 ± 4°C) temperature, and we examined clutch, population, and lineage effects on several traits of females, eggs, and hatchlings. Incubation time was mainly explained by differences between lineages, but it was also influenced by population and female effects. Within each lineage, incubation was shorter at cooler and wetter sites, and for a given climate it was shorter for eastern than for western populations, suggesting that countergradient variation has evolved independently in the two lineages. Female size, clutch size, and relative fecundity were primarily influenced by inter-population differences, a pattern that seemed attributable to environmental differences in productivity, because mean female size was positively correlated with a gradient of increasing precipitation and decreasing temperature. Clutch size was mainly, but not entirely, dependent on female SVL, suggesting both a proximate effect of local conditions and intrinsic differences among populations. Females from drier and warmer sites produced larger hatchlings. Mean egg mass was mainly determined by familial effects. Eggs incubated at a constant temperature hatched earlier than did their siblings incubated at fluctuating temperatures, a fact that could be explained by considering that in Mediterranean environments developmental rate might increase at a lower speed above average incubation temperature than it does decrease below it.

A molecular phylogeny of Equatorial African Lacertidae, with the description of a new genus and species from eastern Democratic Republic of the Congo

Currently, four species of the lacertid lizard genus Adolfus are known from Central and East Africa. We sequenced up to 2,825 bp of two mitochondrial (16S and cyt b) and two nuclear (c-mos and RAG1) genes from 41 samples of Adolfus (representing every species), two species each of Gastropholis and Holaspis, and in separate analyses combined this data with GenBank sequences of all other Eremiadini genera and four Lacertini outgroups. Data from DNA sequences were analyzed with maximum parsimony (PAUP), maximum-likelihood (RAxML) and Bayesian inference (MrBayes) criteria. Results demonstrated that Adolfus is not monophyletic: A. africanus (type species), A. alleni and A. jacksoni are sister taxa, whereas A. vauereselli and a new species from the Itombwe Plateau of Democratic Republic of the Congo are in a separate lineage. Holaspis and Gastropholis were recovered in separate clades. Based on this molecular data, relatively substantial sequence divergence and multiple morphological differences, we describe a new genus of lacertid for the lineage including A. vauereselli and the new Itombwe species. The recognition of this new, endemic genus underscores the conservation importance of the Albertine Rift, especially the Itombwe Plateau, a unique region that is severely threatened by unchecked deforestation, mining and poaching.

Phylogeny and Relationships of the Mountain Lizards of Europe and Near East ( Archaeolacerta Mertens, 1921, sensu lato ) and Their Relationships Among the Eurasian Lacertid Radiation

Archaeolacerta s. l., in the currently utilized sense results to be a polyphyletic taxon, composed of three monophyletic and phylogenetically well differentiated taxa: a) Archaeolacerta (s. str.) Mertens, 1921, which includes three species: A. bedriagae , A. oxycephala , and A. mosorensis , distributed by the northern part of the Central Mediterranean (Corsica, Sardinia, and west Balcanic Peninsula). His most related genera seem to be Teira (his adelphotaxon in our study), Apathya , and Omanosaura . b) Iberolacerta gen. nov., with two subgenera: Iberolacerta s. str. and Pyrenesaura subgen. nov. includes six species: I. monticola , I. cyreni , I. bonnali , I. aranica , I. aurelioi , and I. horvathi . They are distributed by the mountains of Western Europe (Iberian Peninsula, Pyrenees, Central and Eastern Alps and the north of the Dinaric Chains). His adelphotaxon are the Caucasian and Near East species of Darevskia gen. nov. c) The third taxa is Darevskia gen. nov., which includes the species of the « L». saxicola complex besides « L». derjugini , « L». praticola , and « L». chlorogaster . They are distributed by Eastern Europe, Caucasus, and Near East. Other clear relationships among some taxa of the Eurasian Radiation [= «Eurasische linie» from (Mayer and Benyr, 1994)] have been found: Algyroides seems to be the sister group of the species considered of uncertain phylogenetic relationships belonging to the « L». danfordi-laevis group and of Podarcis . « L». brandtii seems to be a very primitive species within the Eurasian Radiation. Omanosaura and Apathya appear as sister taxa. « L». graeca occupies a very basal position in the sister group of Podarcis and relatives (see above). « L». andreanskyi is the sister species of the Darevskia nov. and Iberolacerta nov. clade. The assimilation of « L». andreanskyi to Teira is very problematic. Also the « L». parva group seems to be related to Timon . Some groups of species like « L». brandtii , « L». parva-fraasii and « L». danfordi-laevis probably merit generic rank, but it is necessary a more deep study before to take a decision.

A New Species of Eremias (Sauria: Lacertidae) from Fars Province, South-Central Iran

A new species of the lacertid genus and subgenus Eremias is described based on material collected by the senior author from 150 km northeast of Shiraz, Fars province, south-central Iran at about 1800 m elevation. It differs from all other Iranian species of the typical subgenus ( E. persica , E. strauchi , E. velox , and E. lalezharica ) in that it has a very distinctive and unique color pattern, unmistakable in this character: the wide dorsolateral stripe is uniformly black without light spots and there is no ocelli on the upper surface of limbs; the third pair of submaxillary shields are separated by 4 granular scales; and the tympanic shield is rudimentary and almost absent. The new species is sympatric with Eremias persica and apparently restricted in distribution to the steppes and open plains in the northern regions of Fars province, south-central Iran.

Comparative Study of DNA Repetitive Sequences by Means of Restriction Endonucleases Among Populations and Subspecies of Some Lacertid Lizard Species

As was shown earlier with reference to several animal taxa, characterization of highly repetitive DNA sequences by their susceptibility to restriction endonucleases (DNA taxoprinting) does not exhibit any differences between species populations. This method was used in our study on the populations and subspecies of some lacertid lizards: Lacerta raddei, L. saxicola, L. rudis , and L. agilis . These features were shown to be practically indistinguishable in two Armenian populations (Gosh and Khosrov) of L. raddei ; the third population (Egegnadzor) demonstrates some differences. Two subspecies of Caucasian L. rudis and five subspecies of L. agilis inhabiting distant parts of the extensive range have minimal dissimilarities in the taxoprints studied. Comparison of L. saxicola subspecies, three of which inhabit the Caucasus and one the Crimea ( L. s. lindholmi ) presented no significant differences in any of the taxoprints of Caucasian subspecies studied up to now, while Crimean subspecies is significantly dissimilar, not less than other species are dissimilar from each other. It was suggested that L. s. lindholmi may be considered as an individual species. The molecular characteristics of genomic DNA used seem to be useful in animal taxonomy.

Reproduction of Acanthodactylus erythrurus in Its Northern Boundary

Variation in the reproductive cycle of two populations of Acanthodactylus erythrurus living in coastal sandy areas of the NE extreme of its range was analyzed. This species exhibits strong influence of historical factors in its reproductive traits: vernal spermatogenic cycle, short incubation, K-selection, and high egg size variation. The populations studied are more similar to others from the Mediterranean coast than to those from Central Spain. In comparison with the latter, reproductive season is longer, adult sizes are smaller and sexual dimorphism is reduced. A second clutch can be laid when the reproductive season is long enough. Nevertheless, phenology in this species is less variable than in other Mediterranean Lacertidae. Since no evidence of suboptimal conditions was found in any population, it is concluded that factors other than reproductive ones may have restricted the range of this species in NE Spain.

Structure, Localization, and Stability of Chromosomes in Karyotype Evolution in Lizards of the Lacertidae Family

The chromosomes of eight lacertid species were studied by standard and banding techniques (C- and NOR-banding, telomeric sequences) and chromosomal interlocation during mitosis and meiosis was investigated. The data obtained are discussed in the light of modern ideas of the interrelation between DNA changes, karyotype evolution, and speciation. The assumption is voiced on the optimal number of arms and, consequently, the “optimal” number of functional telomeres in the Lacertidae, which in its turn may be associated with the structure of the nucleus and with canalization of the genome as a whole.

A New Species of Spauligodon (Nematoda: Oxyurida: Pharyngodonidae) in Geckos from São Nicolau Island (Cape Verde) and Its Phylogenetic Assessment

A new nematode species, Spauligodon nicolauensis n. sp., is described from geckos Tarentola bocagei and Tarentola nicolauensis on the island of São Nicolau, Cape Verde. The new nematode was found in the pellets obtained directly from the geckos in a non-invasive fashion, and its identity was assessed both at morphologic and genetic levels. The new species has morphological similarities with Spauligodon tarentolae Spaul, 1926, also parasitizing geckos from the Canary Islands. However, the male cloacal region in the new species is distinct, presenting a different shape of the caudal papillae. The overall resemblance probably resulted from colonization via descent from an ancestor of S. tarentolae carried by the ancestor of Cape Verde Tarentola. The analysis of nuclear DNA sequences confirms that the new species is phylogenetically distinct from all other Spauligodon species already analyzed, forming a group clearly separated from species parasitizing lacertid lizards. The COI genetic distance suggests that the S. nicolauensis n. sp. found in the 2 species of geckos in São Nicolau Island may have resulted from a host-switching event, when they came into contact after the unification of the island.

Comparative skull osteology of the lacertid lizards Eremias persica and Mesalina watsonana (Sauria: Lacertidae)

The skull of two lacertid lizards of Iran including Eremias persica from Isfahan Province, Central Iranian Plateau and Mesalina watsonana from Birjand in Southern Khorasan Province, Eastern Iran, was described and compared based on seven dry skull preparations. Prominent differences included: the shape of the premaxilla and its articulation with other skull elements, the shape of the frontal (particularly the form of its processes), the number of dentary teeth, the shape of the jugal, and the position of the parietal opening. Also in E. persica, the nasals were in contact with each other whereas in M. watsonana they were separated by the nasal process of the premaxilla and anteromedial process of the frontal. Absence of pterygoid teeth in M. watsonana and extended pyriform recess in E. persica also represented further differences. Our study contributes to the baseline understanding of squamate osteology and more specifically will facilitate further studies on lacertid morphological disparity.

COMPARATIVE STUDIES ON LIZARDS BASED ON THE CRANIAL OSTEOLOGY OF Lacerta media AND Laudakia caucasia (SQUAMATA: SAURIA)

In spite of numerous studies done on the morphometric characters of lizards, information about the detailed characters of their skeletons remains insufficient. In this study, the skulls of two different species of lizards, cleared and double-stained, have been examined and compared: Laudakia caucasia Eichwald, 1831 and Lacerta media Lantz and Cyren, 1920. The aim of this paper is to study the characteristics and peculiarities of the skulls of the two above-mentioned species of lizards in order to facilitate diagnosis and identification of the living species and subfossil remains and to evaluate changes in skull morphology in a phylogenetic context. For doing this, characters of the skull and mandibular elements were studied. The existence of differences between these two genera and families Laudakia caucasia (Agamidae) and Lacerta media (Lacertidae), according to the bone and skull characters, have been explained. The obvious differences that show off are: dimension of the supratemporal fossae, thickness of the individual bones, and head length/width ratio. Other obvious differences are the type of dentition, differences in form, size and special manner of joining bones like existence of differences in lower jaw and braincase architecture, and reviewing some differences in the skulls of two different phylogenetic lines.