Lacertid Research Articles

Complex patterns of morphological and mtDNA variation in Lacerta perspicillata (Reptilia; Lacertidae)

Lacerta perspicillata is a north-west African lacertid lizard that shows considerable intraspecific variation, with three subspecies described on the basis of colour pattern and body size. Recent observations of a population con- taining two morphological forms and more than one deep genetic lineage, as well as an apparent lack of concordance between forms and genetic lineages, suggest that the complexity is greater than previously thought. To analyse and quantify this variation, we studied the variability within this species at two levels: (1) external morphology (multivariate analysis of scalation, body dimensions, and colour pattern) and (2) mtDNA (sequencing and single- strand confirmation polymorphism analysis). Fifty-two individuals were studied at Taza, northern Morocco. Two morphological groupings (ostensibly representing two previously described subspecies) and two deep mtDNA lin- eages were detected at this site, with complete correspondence between the two. This, together with an apparent lack of hybrids, would normally support respective full species recognition. However, analysis of 98 individuals from other populations demonstrated that the situation is highly complex with the same genetic lineages having reversed mor- photypes in other areas, making such a designation difficult. Across the other studied populations, we found no sup- port for any of the currently recognized subspecies. The lack of congruence between mtDNA lineages and morphometric patterns (in some cases) and the morphological similarity among lizards from different lineages sug- gest ecophenotypic convergence or multiple introgressive hybridization. The study highlights the tremendous com- plexity that may exist within a taxon and the inadequacy of older alpha-taxonomy based designations in describing it. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 479-490. ADDITIONAL KEYWORDS: Balearic Islands - genetic variation - lizard - morphology - North Africa.

Relationships between chemosensory behaviour and foraging mode within lacertid lizards

We assess associations between chemosensory capacity and foraging mode within lacertid lizards. Species of Lacertidae differ considerably in indices of foraging mode, and therefore seem well suited to test the adaptive nature of a coupling between foraging and sensory ecology. We observed tongue-flick (TF) rates of members from eight species in the field and in experimental conditions with no prey stimuli, with chemical stimuli, with visual stimuli and with both chemical and visual stimuli. All species increased TF rates in response to both purely visual and purely chemical prey cues, and the increase was most pronounced when both types of stimuli were offered simultaneously. Absolute TF rates in experimental conditions differed considerably among species, and species means obtained in experimental situations correlated closely with those observed in the field. Species that spend a relatively large amount of their time budget actively searching for food tend to use their vomeronasal system more frequently. Although all species in our study retained the capacity of recognizing prey chemicals, our data corroborate the idea of a functional link between an active foraging style and the usage of chemical information.

Flight initiation distance in relation to substratum type, sex, reproductive status and tail condition in two lacertids with contrasting habits

Abstract Flight initiation distance in relation to substratum type, sex, reproductive status and tail condition was studied in two lacertid lizards with contrasting habits: the ground-dwelling common lizard Zootoca vivipara and the rupicolous Horvath's rock lizard Iberolacerta horvathi. These species were studied in sympatric populations in a mountain area in North-Eastern Italy, Tarvisio Forest. Mean escape distance was significantly higher in I. horvathi than in Z. vivipara. In both species there were significant differences between sexes, with males escaping at longer distances than females but there were no significant differences between adults and subadults. In both species there were no differences in escape distance of females in different reproductive states. In Z. vivipara specimens with broken tails escaped at a shorter distance than individuals with intact tails. Substratum type had a significant effect on escape distance in both species.

Assimilation of cadmium in a European lacertid lizard: Is trophic transfer important?

Apart from analyses for elemental contaminants in field-collected specimens, very little is known about the assimilation and accumulation of inorganic contaminants in reptiles. Recent dietary studies with reptiles (and some other vertebrates and invertebrates) have taken care to incorporate the principles of trophic transfer by pre-exposing prey items to the elemental contaminant of interest. However, there are conflicting data in the literature as to whether biologically incorporated metals are more bioavailable to consumers in a food chain than simple salts added to the diet, and this study examines this issue in a lacertid lizard. Adult individuals of Podarcis carbonelli were exposed to cadmium (Cd) in a 21-week dietary study to determine whether the form in which the Cd is provided influences assimilation efficiency for this metal. Lizards were provided with Cd that had either been biologically incorporated into crickets or as Cd(NO3)2 added superficially to crickets just prior to feeding. Radiospectrometric analysis for 109Cd in animal tissues and fecal material was used to follow Cd accumulation over the duration of exposure. The highest levels of accumulation were found within the gut. This, combined with the observation of higher rates of assimilation over the first five weeks, strongly suggests a rapid accumulation of Cd within the gut tissue followed by a slower redistribution to other tissues. No statistically different levels of Cd assimilation efficiency were detected between the two treatment groups, nor were there any statistically significant differences between the two treatment groups in relation to the proportional distribution to the gut, liver, or kidneys.

Sexual Dimorphism, Reproductive Biology, and Dietary Habits of Psammophiine Snakes (Colubridae) from Southern Africa

Slender-bodied, diurnal “sand snakes” of the genus Psammophis are widespread and abundant through Africa, but the general biology of these animals remains poorly known. For example, sexual dimorphism is unstudied because it is difficult to determine the sex of live specimens (uniquely among snakes, the male hemipenis is vestigial). Our dissections of 700 preserved specimens provide detailed ecological information on ten psammophiine species from southern Africa. Males grow larger than females in most taxa, especially in species of large absolute body size. However, sex differences in body proportions (relative head size, relative tail length) are minor. Females produce small clutches (generally <10 eggs), with larger clutches in larger females in some but not all species. Psammophylax tritaeniatus differs from the nine Psammophis species studied in its higher fecundity and its primary reliance on mammalian rather than reptilian prey. Within Psammophis, five species (P. brevirostris, P. jallae, P. leopardinus, P. subtaeniatus, P. trigrammus) fed mostly on scincid lizards, two (P. namibensis, P. notostictus) fed mostly on lacertid lizards, and two (P. trinasalis, P. mossambicus) took approximately equal numbers of lizards and mammals. Although dietary composition thus varied with snake species and body size, conspecific males and females took similar prey types. Thus, despite reports of unusual mating systems in captive psammophiines, these snakes exhibit only minor sexual dimorphism in size, bodily proportions, and dietary habits.

Genetic differentiation of parthenogenetic lizards Darevskia rostombekowi (Family Lacertidae) as determined using nuclear and mitochondrial DNA markers

Genetic differentiation of parthenogenetic lizards Darevskia rostombekowi (Family Lacertidae) as determined using nuclear and mitochondrial DNA markers

Relationships between helminth communities and host traits in Podarcis bocagei and Podarcis carbonelli from NW Portugal

A parasitological survey was carried out to determine the relationships between helminth fauna and some biological traits of two host species of lacertid lizards. Size, sex, diet, and season of collection, as well as infracommunities and component communities of Podarcis bocagei and P. carbonelli from Douro litoral (northwest Portugal), have been analysed. In both host species, we found low values of parasite infection parameters and diversity. These findings were in accordance with their feeding habits, eating only animal prey and no plant matter. Evidences suggest a relationship between the presence of Brachylaima sp (Trematoda: Brachylaimidae) and the ingestion of snails by both lizard species. Spauligodon carbonelli (Nematoda, Pharyngodonidae), a specialist in Podarcis hosts, was the most important parasite, affecting mainly adult males with a prevalence of infection showing seasonal variation.

Digestive performance in five Mediterranean lizard species: effects of temperature and insularity

Temperature sensitivity of digestive processes has important ramifications for digestive performance in ectothermic vertebrates. We conducted a comparative analysis of temperature effects on digestive processes [gut passage times (GPTs) and apparent digestive efficiencies (ADEs)] in five lacertid lizards occurring in insular (Podarcis erhardii, P. gaigeae), and mainland (P. muralis, P. peloponnesiaca, Lacerta graeca) Mediterranean environments. GPTs were negatively correlated to temperature with mainland taxa having 10-20% longer GPTs than island taxa. In contrast to previous studies that estimate ADEs using bomb calorimetry, we compare ADEs by analyzing discrete efficiencies for lipids, sugars and proteins at three temperature regimes (20, 25, and 30 degrees C); each of these categories produces different results. ADEs for lipids and sugars showed a monotonic increase with temperature whereas ADEs for proteins decreased with temperature. Island taxa had consistently higher ADEs than their mainland counterparts for lipids and for proteins but not for sugars. They are characterized by superior energy acquisition abilities despite significantly shorter GPTs. Their increased digestive performance relative to the mainland species appears to allow them to maximize energy acquisition in unproductive island environments where food availability is spatially and seasonally clustered.

Highly polymorphic tetranucleotide microsatellite loci for the eastern Canary Island lizard, Gallotia atlantica

AbstractWe describe 10 polymorphic tetranucleotide microsatellite loci from the eastern Canary Island lacertid lizard, Gallotia atlantica. Loci were isolated from a partial genomic library that had been enriched for AAAG repeat sequence. All loci were highly polymorphic (eight alleles or more) with observed heterozygosities from 0.75 to 1.00. At least four loci were successfully amplified and polymorphic in the Gran Canarian lacertid, Gallotia stehlini. These loci will be used to examine correlations between patterns of gene flow and recent volcanism on the island of Lanzarote.

Description of a new endemic species of mountain lizard from Northwestern Spain: Iberolacerta galani sp. nov. (Squamata : Lacertidae)

A new species of Iberolacerta is described from the Montes de León (northwest Iberia). This new species, Iberolacerta galani sp. nov., is characterized by its relatively large size, high number of blue ocelli on the shoulders and the relatively frequent contact or near-contact between the supranasal and the first loreal scale, the fairly straight squamosal bone (only curved on its posterior part), a unique karyotype in Iberolacerta combining 2n=36 chromosomes, an L-type NOR and differentiated W and Z sex chromosomes, and unique mitochondrial DNA sequences for the cytochrome b and 12S rRNA genes. The correlation analyses show that morphology in general, but especially scalation, is strongly correlated with the amount of precipitation during the months of lizard activity, which suggests that these are not good taxonomic characters, and that other characters apparently independent of the climate like for instance osteological, karyological and DNA features are much more reliable in delimiting species boundaries in Iberolacerta. According to our phylogenetic analyses, I. galani nov. is part of a very well supported clade that originated around 2.5 mya and also includes I. monticola and I. martinezricai. Phylogeny suggests I.martinezricai might be the sister taxon to I. galani nov. from which it split approximately 2 mya, at the beginning of the Pleistocene. The clade containing I. galani nov., I. martinezricai and I. monticola was probably widely distributed across western Iberia during moderately cool and moist phases of the Pleistocene, but it was probably restricted to its present range as a result of the general temperature increase during the Holocene and competition with other lacertid lizards. Iberolacerta galani nov. is endemic to the Montes de León, where it is isolated from the other species of the “monticola-group” by the Duero and Miño-Sil Rivers, but particularly by the Bibei river valley.

Phylogeography of the lacertid lizard, Psammodromus algirus, in Iberia and across the Strait of Gibraltar

AbstractAim To determine genetic substructuring within the lacertid lizard Psammodromus algirus. To compare levels of variation across a geological barrier, the Strait of Gibraltar, and to compare this against the known age of the barrier using a molecular clock hypothesis. To compare the effect of the barrier within this species with previously published data from other organisms.Location The Iberian Peninsula and North Africa.Methods Partial sequences from the mitochondrial cytochrome b, 12S rRNA and 16S rRNA genes were obtained from 101 specimens belonging to the subfamily Gallotiinae and used in this study. The data set was aligned using ClustalX and phylogenetic trees produced using both maximum‐parsimony and maximum‐likelihood methods. Maximum likelihood estimates of divergence times for the combined data set (12S + 16S + cytochrome b) were obtained after discovery of lineage rate constancy across the tree using a likelihood ratio test.Results Psammodromus algirus contains divergent eastern and western mtDNA clades within the Iberian Peninsula. The western clade has northern and southern lineages in Iberia and one in North Africa. This phylogeographical pattern indicates that the lizard invaded North Africa after the opening of the Strait, presumably by natural rafting.Main conclusions As in several other species, current patterns of genetic diversity within P. algirus are not directly related to the opening of the Strait of Gibraltar. Widespread sampling on both sides of the barrier is necessary to determine its effect on species in this area accurately.

Natural oak forest vs. ancient pine plantations: lizard microhabitat use may explain the effects of ancient reforestations on distribution and conservation of Iberian lizards

Natural vegetation in Europe appears nowadays deeply modified by human activities. In the Guadarrama Mountains (Central Spain), ancient reforestations with Scots pines, Pinus sylvestris, replaced original deciduous pyrenean oak, Quercus pyrenaica, forests (since the Roman period). However, the effect of reforestations on fauna remains little known, especially in reptiles. We described patterns of microhabitat selection in several species of Lacertid lizards, and analyzed whether the modification of the original vegetation affected distribution and population densities of lizards. The species of lacertid lizards found in oak forests (Psammodromus algirus, Lacerta lepida and Podarcis hispanica) were different to those of in pine plantations (Podarcis muralis and Podarcis hispanica). Lizards did not use habitat at random and this could explain differences in species found in both forests, which differed in some microhabitat structure characteristics. Most lizards selected microhabitats with rocky outcrops, with low cover of trees, and close to refuges. These microhabitat preferences also explained abundance of lizards in transects. From the perspective of conservation and management of lizards, pine plantations seem not to contribute too much to the diversity of lizard species because species typical from oak forests were lost. This study has implications for pine reforestation management, because allowing the recolonization by understory oaks, and leaving some open areas, without trees but with dense shrubs and rocks inside reforestations would contributed to maintain lizard populations.

Does follicle excision always result in enlargement of offspring size in lizards?

An experimental reduction of offspring number has been reported to result in enlargement of offspring size in lizards. We applied the "follicle excision" technique to a lacertid lizard (Takydromus septentrionalis) to examine whether this effect is generalisable to lizards. Of the 82 females that produced 3 successive clutches in the laboratory, 23 females underwent follicle excision after they oviposited the first clutch. Follicle excision reduced clutch size, but did not alter egg size. This result indicates that egg size is not altered during vitellogenesis in T. septentrionalis. Females undergoing follicle excision produced a third clutch (a second post-surgical clutch) as normally as did control females. Females switched from producing more but smaller eggs early in the breeding season to fewer but larger eggs later in the season. Our results indicate that female T. septentrionalis maximize reproductive success by diverting an optimal, rather than a higher, fraction of the available energy to individual offspring. This optimized allocation of the available energy to offspring production explains why follicle excision does not result in enlargement of egg size in this species. Our study provides evidence that an experimental reduction of offspring number does not always result in enlargement of offspring size in lizards.

TWO NEW SPECIES IN THE GENUS PSAMMODROMUS (REPTILIA: LACERTIDAE) FROM THE IBERIAN PENINSULA

The lacertid lizard Psammodromus algirus has been considered a uniform species across its distribution area in North Africa and southwestern Europe. Coloration data and discriminant function analysis of morphological data corroborate mitochondrial DNA and allozyme data to indicate northern and southern Iberian populations represent unknown species that are described here. Additional work is needed to fully understand biogeography and variation in this species complex.

Intestinal helminth communities of Podarcis bocagei and Podarcis carbonelli (Sauria: Lacertidae) in NW Portugal

Abstract A survey of gastrointestinal helminth communities of Podarcis bocagei and Podarcis carbonelli (Sauria: Lacertidae) from NW Portugal was conducted to determine the prevalence, intensity and diversity of intestinal parasites in these lizards. A few parasite species were found in both hosts, their prevalences, mean intensities and abundances of infection being low or very low. Low values of richness and abundance of parasite species were also found in the helminth infracommunities of individuals of both host species. These low values of parameters of infection and diversity are discussed and compared between both host species and among other Iberian lacertid lizards.

Phenotypic plasticity in reproductive traits induced by food availability in a lacertid lizard, Takydromus septentrionalis

Understanding the proximate determinants of phenotypic variations in life‐history traits can provide powerful insights into a species’ life‐history strategies. I experimentally manipulated availability of food (high vs low) to examine plasticity in the reproductive traits of northern grass lizards, Takydromus septentrionalis (Lacertidae), from eastern China. Food availability significantly affected reproductive frequency and thereby seasonal reproductive output, but had little effect on reproductive output per clutch. Low‐food females postponed reproduction and produced less clutches in the reproductive season than did high‐food females. After producing their second clutches, low‐food females were in lower body condition than the high‐food counterparts. By the end of the experiment, however, all females exhibited similar body condition. Clutch size and clutch mass differed between the first and second clutches but not between the treatments. Egg size and phenotypic traits of hatchlings (body size, morphology and locomotor performance) in T. septentrionalis did not vary significantly from first to second clutches nor between the two treatments. These results support optimal egg size (offspring) theory. Female T. septentrionalis “decide” whether or not to reproduce largely based on current energy intake; lowered feeding rates thus delay oviposition and reduce reproductive frequency. In contrast, clutch size, egg size and relative clutch mass remain unchanged.

Isolation and sequencing of seven Sox genes from the lacertid lizard Eremias breuchleyi

The Sox family of genes shares a high sequence similarity with the HMG box region of the human Y chromosomal gene, SRY. We used highly degenerate primers to clone and sequence seven Eremias breuchleyi Sox genes (EbSox2, EbSox3, EbSox4, EbSox11, EbSox12, EbSox14 and EbSox21). A database search for the cloned sequences revealed the following percentage identity with the homologous human SOX genes: EbSox2 = 96%, EbSox3 = 88%, EbSox4 = 94%, EbSox11 = 99%, EbSox12 = 96%, EbSox14 = 98%, EbSox21 = 97%. Cluster analysis indicates that they seem to belong to group B and group C of Sox gene family, respectively.

Ontogenetic shifts in thermal tolerance, selected body temperature and thermal dependence of food assimilation and locomotor performance in a lacertid lizard, Eremias brenchleyi

We used Eremias brenchleyi as a model animal to examine differences in thermal tolerance, selected body temperature, and the thermal dependence of food assimilation and locomotor performance between juvenile and adult lizards. Adults selected higher body temperatures (33.5 vs. 31.7 °C) and were able to tolerate a wider range of body temperatures (3.4–43.6 vs. 5.1–40.8 °C) than juveniles. Within the body temperature range of 26–38 °C, adults overall ate more than juveniles, and food passage rate was faster in adults than juveniles. Apparent digestive coefficient (ADC) and assimilation efficiency (AE) varied among temperature treatments but no clear temperature associated patterns could be discerned for these two variables. At each test temperature ADC and AE were both higher in adults than in juveniles. Sprint speed increased with increase in body temperature at lower body temperatures, but decreased at higher body temperatures. At each test temperature adults ran faster than did juveniles, and the range of body temperatures where lizards maintained 90% of maximum speed differed between adults (27–34 °C) and juveniles (29–37 °C). Optimal temperatures and thermal sensitivities differed between food assimilation and sprint speed. Our results not only show strong patterns of ontogenetic variation in thermal tolerance, selected body temperature and thermal dependence of food assimilation and locomotor performance in E. brenchleyi, but also add support for the multiple optima hypothesis for the thermal dependence of behavioral and physiological variables in reptiles.

Partial tail loss has no severe effects on energy stores and locomotor performance in a lacertid lizard, Takydromus septentrionalis

Many species of lizards use caudal autotomy as a defense strategy to avoid predation, but tail loss entails costs. These topics were studied experimentally in the northern grass lizard, Takydromus septentrionalis. We measured lipids in the three-tail segments removed from each of the 20 experimental lizards (adult females) initially having intact tails to evaluate the effect of tail loss on energy stores; we obtained data on locomotor performance (sprint speed, the maximal length traveled without stopping and the number of stops in the racetrack) for these lizards before and after the tail-removing treatments to evaluate the effect of tail loss on locomotor performance. An independent sample of 20 adult females that retained intact tails was measured for locomotor performance to serve as controls for successive measurements taken for the experimental lizards. The lipids stored in the removed tail was positively correlated with tailbase width when holding the tail length constant, indicating that thicker tails contained more lipids than did thinner tails of the same overall length. Most of the lipids stored in the tail were concentrated in the proximal portion of the tail. Locomotor performance was almost unaffected by tail loss until at least more than 71% of the tail (in length) was lost. Our data show that partial tail loss due to predatory encounters or other factors may not severely affect energy stores and locomotor performance in T. septentrionalis.

Reproductive Investment of a Lacertid Lizard in Fragmented Habitat

Abstract: We studied the effect of habitat fragmentation on female reproductive investment in a widespread lacertid lizard ( Psammodromus algirus) in a mixed‐forest archipelago of deciduous and evergreen oak woods in northern Spain. We captured gravid females in fragments (≤10 ha) and forests (≥ 200 ha) and brought them to the laboratory, where they laid their eggs. We incubated the eggs and released the first cohort of juveniles into the wild to monitor their survival. Females from fragments produced a smaller clutch mass and laid fewer eggs (relative to mean egg mass) than females of similar body size from forests. Lizards did not trade larger clutches for larger offspring, however, because females from fragments did not lay larger eggs (relative to their number) than females from forests. Among the first cohort of juveniles, larger egg mass and body size increased the probability of recapture the next year. Thus, fragmentation decreased the relative fecundity of lizards without increasing the quality of their offspring. Reduced energy availability, increased predation risk, and demographic stochasticity could decrease the fitness of lizards in fragmented habitats, which could contribute to the regional scarcity of this species in agricultural areas sprinkled with small patches of otherwise suitable forest. Our results show that predictable reduction of reproductive output with decreasing size of habitat patches can be added to the already known processes that cause inverse density dependence at low population numbers.