Carbonelli Research Articles

Trophic niche changes associated with the eradication of invasive mammals in an insular lizard: an assessment using isotopes.

Invasive species are a major threat to island biodiversity, and their eradications have substantially contributed to the conservation of island endemics. However, the consequences of eradications on the trophic ecology of native taxa are largely unexplored. Here, we used the eradication of invasive black rats Rattus rattus and European rabbits Oryctolagus cuniculus from the Berlenga Island, in the western coast of Portugal, as a whole-ecosystem experiment to investigate the effects of the eradication of invasive mammals on the trophic niche and body dimensions of the island-restricted Berlenga wall lizard Podarcis carbonelli berlengensis over a 2-year period. Our results suggest an expansion of the isotopic niche and an intensification of the sexual dimorphism of the lizard following mammal eradication. Additionally, we found considerable variability in isotopic niche across the island and detected evidence of sex-specific and season-modulated nutritional requirements of this threatened reptile. Our findings support that the eradication of 2 of the planet’s most problematic invasive vertebrates led to changes in the lizard trophic niche and sexual dimorphism in just 2 years. This suggests that the ecological pressures—for example, prey availability and habitat structure—to which lizards are exposed have substantially changed post-eradication. Our study emphasizes the scientific value of island eradications as experiments to address a wide range of ecological questions and adds to the increasing body of evidence supporting substantial conservation gains associated with these restoration interventions.

Variable levels of introgression between the endangered Podarcis carbonelli and highly divergent congeneric species.

Recent empirical studies have demonstrated that speciation with gene flow is more common than previously thought. From a conservation perspective, the potential negative effects of hybridization raise concerns on the genetic integrity of endangered species. However, introgressive hybridization has also been growingly recognized as a source of diversity and new advantageous alleles. Carbonell's wall lizard (Podarcis carbonelli) is an endangered species whose distribution overlaps with four other congeneric species. Our goal here was to determine whether P. carbonelli is completely reproductively isolated from its congeners and to evaluate the relevance of hybridization and interspecific gene flow for developing a conservation plan. We used restriction site associated DNA (RAD) sequencing to discover SNPs in samples from four contact zones between P. carbonelli and four other species. Principal component analysis, multilocus genotype assignment and interspecific heterozygosity suggest incomplete reproductive isolation and ongoing gene flow between species. However, hybridization dynamics vary across all pairs, suggesting complex interactions between multiple intrinsic and extrinsic barriers. Despite seemingly ubiquitous interspecific gene flow, we found evidence of strong reproductive isolation across most contact zones. Instead, indirect effects of hybridization like waste of reproductive effort in small isolated populations may be more problematic. Our results highlight the need to further evaluate the consequences of introgression for P. carbonelli, both on a geographic and genomic level and included in a comprehensive and urgently needed conservation plan. Besides, those findings will add important insights on the potential effects of hybridization and introgression for endangered species.

Evaluating how species niche modelling is affected by partial distributions with an empirical case

Ecological niche models (ENMs) will successfully identify a species' ecological niche, provided that important assumptions are fulfilled, namely environment equilibrium and niche equality across the distribution. Violations may seriously affect ENM reliability, leading to erroneous biogeographic conclusions and inappropriate conservation prioritisation. We evaluate the robustness of ENMs against incomplete knowledge of distribution with a real example, the threatened Iberian lizard Podarcis carbonelli, whose distribution was gradually discovered over a long time period. We used several ENM methods for presence-only data (Maxent, ENFA, Bioclim, and Domain) to infer the realised ecological niche at two spatial resolutions (1 km and 200 m). The distribution data were split into four partial datasets corresponding to separate subranges: Central System (CS); Viseu-Aveiro (VA); Atlantic coast (AC); and Doñana (DO). We then accumulated the datasets following the species discovery sequence: CS + VA, CS + VA + AC, and CS + VA + AC + DO. Niche equivalence and similarity between partial models were compared using Ecospat. ENMs were strongly affected by the violation of niche equilibrium; only the VA subrange forecasts the complete species range. ENMs were also sensitive to the violation of niche equality: only VA models were similar to the Iberian model, altitude being the most important variable followed by annual precipitation, maximum temperature in July, and annual radiation. When the ENMs were applied only to the first subrange discovered (CS), only the VA area was predicted, while the other subranges might have remained unknown, thus compromising conservation strategies. As assumptions of niche equilibrium and equality were violated, likely owing to the species' ecological multimodality, the models generated were biased and of limited predictive value. ENMs are useful tools in biogeography and conservation, but only if their basal assumptions are achieved. Partial models may be useful if they are considered as representing different suitable habitats.

Interspecific differences in chemical composition of femoral gland secretions between two closely related wall lizard species, Podarcis bocagei and Podarcis carbonelli

Chemical signals play an important role in intraspecific communication and social organization of many animals, but they also may be useful in interspecific recognition. In lizards, chemical signals are often contained in femoral gland secretions, of which composition may vary between species and populations. This may be especially important in recognition and reproductive isolation between closely related species. We analyzed by gas chromatography–mass spectrometry (GC–MS) the lipophilic fraction of femoral gland secretions of two closely related wall lizard species, Podarcis bocagei and Podarcis carbonelli to test for possible interspecific differences in chemical composition. We found 56 lipophilic compounds in femoral gland secretions of male P. bocagei and 60 in P. carbonelli. The main compounds were steroids and waxy esters, but we also found carboxylic acids and their esters, alcohols, amydes, aldehydes, squalene, ketones and furanones. There were significant differences between species with respect to the number and relative proportions of compounds. Differences in chemical composition might be a consequence of phylogenetic differences per se, but they could also be explained by ecological adaptation to different microclimatic conditions. These differences in chemical profiles may explain the known chemosensory interspecific recognition between these two lizards, contributing to their reproductive isolation.

Parasite specificity in Podarcis bocagei and P. carbonelli (Lacertidae) from NW Portugal: a host-parasite history

Host parasite specificity is related to several factors including the type of life cycle of the parasite, the habitat occupied by both parasites and hosts, and the food habits of the hosts. In this work, gastrointestinal helminths in two congeneric lacertid lizards, Podarcis bocagei and Podarcis carbonelli living in sintopy, have been analysed. Out of four helminth species found, three of them, the trematode Brachylaima sp., the cestode Oochoristica gallica and the nematode Skrjabinelazia hoffmanni, have indirect life cycles while the nematode Spauligodon carbonelli has a direct life cycle. Heteroxenous helminths showed low host specificity whereas S. carbonelli may be placed at an intermediate position in a continuum of the degree of specificity.

Thermoregulatory movement patterns of the lizard Podarcis carbonelli (Lacertilia: Lacertidae)

Using video cameras and motion detection software, we examined sequential positions of the lizard Podarcis carbonelli in a temperature gradient to look for patterns in spatial and temporal thermoregulatory movements. As lizards shuttled between warm and cool areas, their movements were typically slow; punctuated by bursts of speed. The animals were relatively inactive when heating, moved almost continually when cooling, and spent less time heating than cooling. Traditional modeling techniques proved unsuccessful, so we assessed the movement patterns with nonlinear dynamical techniques. The shuttling frequency, and the pattern of velocity changes, both met the qualitative attributes (self similarity, strange attractors, and noisy power spectra) and the quantitative criteria (positive Lyapunov exponent and capacity and/or correlation dimensions less than 5) that suggest deterministic chaos. These movement patterns appear regular, but at unpredictable times the patterns become disturbed before returning to regulation. There are both behavioral and physiological advantages to movements that follow a model of deterministic chaos control.

Modelling the past and future distribution of contracting species. The Iberian lizard Podarcis carbonelli (Squamata: Lacertidae) as a case study

While glaciations constituted the major recent paleoclimatic event, inducing multiple oscillations on species’ ranges, future and rapid shifts are expected if global warming predictions are confirmed. Investigating the whole temporal spectrum of range shifts is of conservation importance since species suffering contractions during the interglacial periods may continue contracting in a warming scenario; lizards provide excellent models for such analysis. We investigated the historical biogeography of Podarcis carbonelli, a lacertid lizard endemic to the Western Iberian Peninsula with a fragmented distribution, likely resulting from an important reduction during the Pleistocene and Holocene. We modelled with Maxent its current distribution and projected it to past (Last Interglacial—LIG and Last Glacial Maximum—LGM) and future (2020, 2050 and 2080) scenarios. The consensus models predicted a larger suitable area than the currently occupied, in areas with a high humidity and low maximum temperatures. The LIG model indicated a reduced range restricted to the northern Portuguese coast, and the LGM model, a suitable area larger than the current. After the LGM, areas with suitable climate started regression till present, which is predicted to continue in future, with a northward range shift and a loss of suitable climate from inland zones towards the coast. The range of P. carbonelli may have been oscillating from the northern Portuguese coast to the south and to inland during the Pleistocene. The Portuguese West Atlantic coast, harbouring a substantial part of the species’ genetic diversity, with suitable climate during the LIG and LGM and forecasted to remain in the future, is not currently protected but deserves conservation priority.

Recent evolutionary history of the Iberian endemic lizards Podarcis bocagei (Seoane, 1884) and Podarcis carbonelli Pérez-Mellado, 1981 (Squamata: Lacertidae) revealed by allozyme and microsatellite markers

Podarcis bocagei and Podarcis carbonelli are two species of wall lizards endemic to the western Iberian Peninsula. A detailed phylogeographical study based on mitochondrial DNA (mtDNA) variation has shown that they responded differently to the Quaternary climatic oscillations. These differences have been attributed to their distribution patterns: P. bocagei is distributed in the north of the Peninsula and in a continuous fashion, whereas P. carbonelli has a more southern and fragmented distribution. In this study, we assessed whether nuclear markers reveal similar evolutionary patterns to those inferred from mtDNA variation. We studied a battery of allozyme and microsatellite loci in a geographically representative set of individuals from both species. For each species we evaluated overall levels of differentiation, patterns of geographical variation in genetic diversity, genetic relationships amongst localities, and applied model-based individual multilocus genotype clustering approaches to detect hidden population structure. Our results for P. bocagei are highly concordant with the phylogeographical scenario inferred from mtDNA variation: we found very low levels of population differentiation, consistent with survival in a single glacial refugium, and detected signatures of a rapid demographic and geographical expansion. The analyses of nuclear markers furthermore helped to identify a probable refugial area, as well as expansion routes. Additionally, in concordance with observations based on mtDNA variation, a low level of population differentiation was observed in P. carbonelli, but this was significantly higher than in P. bocagei. However, the geographical basis for differentiation in P. carbonelli is highly inconsistent between mtDNA and nuclear markers, suggesting a complex, albeit recent, history of fragmentation. A recent reduction of this species’ distribution has probably erased the signatures of glacial isolation and post-glacial expansion that are normally found in other Iberian species, suggesting that the currently observed pattern of genetic differentiation in this species was shaped more by recent genetic drift than by the Pleistocene climatic oscillations.

Sexual dimorphism in traits related to locomotion: ontogenetic patterns of variation in Podarcis wall lizards

Sexual dimorphism in body size and shape in animals is normally linked to sexual selection mechanisms that modify the morphological properties of each sex. However, sexual dimorphism of ecologically relevant traits may be amplified by natural selection and result in the ecological segregation of both sexes. In the present study, we investigated patterns of sexual dimorphism of morphological traits relevant for locomotion in two lacertid lizards, Podarcis bocagei and Podarcis carbonelli, aiming to identify ontogenetic sources of variation. We analysed trunk and limb variation in relation to total body size, as well as the covariation of different traits, aiming to shed light on the proximate causation of adult sexual dimorphism. We find that, although immatures are generally monomorphic, adult females have a longer trunk, and adult males have longer fore and hind limbs. Both sexes differ substantially with respect to their growth trajectories and relationships between traits, whereas, in some cases, there are signs of morphological constraints delimiting the observed patterns. Because of the direct connection between limb size/shape and locomotor performance, which is relevant both for habitat use and escape from predators, the observed patterns of sexual dimorphism are expected to translate into ecological differences between both sexes.

Genetic admixture between the Iberian endemic lizardsPodarcis bocageiandPodarcis carbonelli: evidence for limited natural hybridization and a bimodal hybrid zone

When recently diverged taxa come into contact, the extent of introgression between them is related to the degree of differentiation that they have achieved. Studying contact zones is therefore essential to understand if differentiated taxa are reproductively isolated and, ultimately, if they are likely to remain distinct. Recent work on Iberian and North African wall lizards (Podarcis) has documented the existence of multiple evolutionary units, diagnosable both by genetic markers and morphology, but suggests that gene flow between distinct forms has occurred. Therefore, we were interested in evaluating how species boundaries are maintained in the areas where they meet. In this work, we study the contact zone between Podarcis bocagei and Podarcis carbonelli. We sampled a transect including the only locality where these two lizards are known to occur in syntopy and analysed a battery of 15 unlinked nuclear genetic markers and mitochondrial DNA. We also conducted a preliminary analysis of morphology and fertility. Using model-based clustering approaches, we show that the two species hybridize in the population where they have direct contact, but evidences of introgression are low for nearby populations. Although a significant number of individuals show evidence of admixture, this hybrid zone is clearly bimodal, suggesting strong barriers to gene flow, of which the putative nature are discussed. Interestingly, morphological analyses do not support the existence of intermediate forms among individuals that are admixed genetically. Taken together, these results constitute further evidence validating P. bocagei and P. carbonelli as distinct species. Resumen Cuando taxones que han divergido recientemente entran de nuevo en contacto, la extension de la introgresion entre los mismos esta relacionada con el grado de diferenciacion alcanzado. Estudiar las zonas de contacto resulta, pues, esencial para interpretar si estos taxones se hallan aislados reproductivamente y, en ultima instancia, si van permanecer diferenciados en el futuro. Estudios recientes sobre las lagartijas ibericas y norteafricanas del genero Podarcis han demostrado la existencia de multiples unidades evolutivas diagnosticables mediante marcadores geneticos y a traves de la morfologia si bien sugieren que ha tenido lugar flujo entre las distintas formas. Por consiguiente, estamos interesados en evaluar como se mantienen los limites entre las especies en las areas donde contactan. En este trabajo, estudiamos la zona de contacto entre P. bocagei y P. carbonelli. Muestreamos en un transecto que incluia la unica localidad conocida donde ambas se hallan en sintopia y analizamos una bateria de 15 marcadores nucleares no ligados y de ADN mitocondrial. Tambien llevamos a cabo analisis preliminares de morfologia y fertilidad. Mediante el empleo de enfoques de agregacion basados en modelos, mostramos que ambas especies hibridan en las poblaciones que contactan pero la evidencia de introgresion es reducida para las poblaciones adyacentes. Aunque un numero significativo de individuos muestra evidencia de mezcla, esta zona hibrida es claramente bimodal, lo cual sugiere fuertes barreras al flujo genetico cuya posible naturaleza se discute. Curiosamente, los analisis morfologicos no apoyan la existencia de formas intermedias entre los individuos geneticamente mixtos. En su conjunto, estos resultados constituyen una prueba mas de la validez de P. bocagei y P. carbonelli como especies distintas.

An integrated Assessment of a group with complex systematics: the Iberomaghrebian lizard genus Podarcis (Squamata, Lacertidae)

A critical review of the evolutionary biology of Iberian and North African lizard members of the genus Podarcis (Lacertidae) based on phylogeny, phylogeography, morphometrics, behavior, ecology and physiology is presented. The Iberomaghrebian region is inhabited by at least 12 different evolutionary lineages that group into a monophyletic clade (except Podarcis muralis). In contrast to the current taxonomy, the saxicolous 'Podarcis hispanica' is paraphyletic with respect to Podarcis bocagei and Podarcis carbonelli, two currently recognized species. Nodes in the phylogenetic tree are deep, resulting from old divergences, clearly preceding the Pleistocene. Nevertheless, more recent range changes as a result of glaciations are also evident. The most plausible evolutionary scenario for this group indicates both vicariant and dispersal events. Although parapatry between lineages is the rule, sympatry and even syntopy are frequent, but usually between ground-dwelling and saxicolous forms. Contacts between forms with similar habitat use are rare and local. Morphological distinctiveness between lineages has been demonstrated, indicating historical constraints. However, other characters have repeatedly evolved under similar environmental pressures independently of the evolutionary lineage. Strong sexual dimorphism derives from sexual selection and is attained before sexual maturity, although developmental restrictions exist. Variation between populations is also important and derives from local variation in both natural (habitat, climate) and sexual (density) selective pressures. Evidence for short-term changes has already been found, particularly in insular populations. Reproductive isolation between syntopic forms and partner recognition are based on male-male competition and on visual and chemical recognition of females by conspecific males. Despite this ancient diversification, most forms maintain a degree of reproductive compatibility. Hybridisation may occur, but is limited, and there is evidence of selection against hybrids. The ecological analysis presented here does not support exploitative competition, but rather behavioral interference between forms. Ecomorph classification of lineages suggests character displacement between those with extensive range overlap. Finally, a critical assessment of the specific status of all lineages is provided and directions for further research are suggested.

Head shape allometry and proximate causes of head sexual dimorphism in Podarcis lizards: joining linear and geometric morphometrics

Podarcis bocagei and Podarcis carbonelli are two lacertid species endemic to the western Iberian Peninsula, and both show head size and shape sexual dimorphism. We studied immature and adult head sexual dimorphism and analysed ontogenetic trajectories of head traits with body and head size, aiming to shed light on the proximate mechanisms involved. Immatures were much less dimorphic than adults, but geometric morphometric techniques revealed that head shape sexual differences are already present at this stage. Males and females differed in allometry of all head characters with body size, with males showing a disproportionate increase of head size and dimensions. On the other hand, head dimensions and head shape changed with increasing head size following similar trends in both sexes, possibly indicating developmental restrictions. Consequently, adult sexual dimorphism for head characters in these species is the result of both shape differences in the immature stage and hypermetric growth of the head in relation to body size in males. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93, 111–124.

Bioaccumulation of Cd by a European lacertid lizard after chronic exposure to Cd-contaminated food

Apart from analyses for elemental contaminants in field collected specimens, very little is known about the assimilation, accumulation and toxic effects of inorganic contaminants in reptiles. This study examined the chronic accumulation of Cd in a European lacertid lizard (Podarcis carbonelli) following dietary provision of an environmentally realistic concentration of Cd for 21 weeks. 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. Among both treatment groups Cd accumulated in tissues in the following order of concentration: gut>liver>kidney>carcass. The majority of the Cd was retained within the gut, and transfer to internal organs was low. Morphological indices, brain and plasma cholinesterase activities, gut and liver metallothionein content, and standard metabolic rate were measured as biomarkers of exposure and effect; however, no differences between control lizards and Cd-treated lizards were observed.

Comparing patterns of nuclear and mitochondrial divergence in a cryptic species complex: the case of Iberian and North African wall lizards (Podarcis, Lacertidae)

Combining different sources of information is essential for a complete understanding of the process of genetic differentiation between species. The Iberian and North African wall lizard (Podarcis) species complex has been the object of several studies regarding morphological and mitochondrial DNA variation but, so far, no large-scale survey of nuclear variation within this group has been accomplished. In this study, ten polymorphic allozyme loci were studied in 569 individuals collected across the Iberian Peninsula and North Africa. The obtained data were analysed using both conventional population genetic tools and recent Bayesian model-based clustering methods. Our results show that there are several well-differentiated entities corroborating the major splits observed in mtDNA analyses. These groups correspond not only to the fully recognized species Podarcis bocagei, Podarcis carbonelli, and Podarcis vaucheri but also to multiple forms within the polytypic Podarcis hispanica, all of which have a similar level of differentiation to that observed between the acknowledged species. However, relationships between forms are weakly supported both by population and individual clustering methods, suggesting a scenario of a rapid diversification that contrasts to the clear bifurcating model assumed from previous mtDNA analyses. Individual multilocus analyses report few individuals misassigned or apparently admixed, some of which are most likely explained by the persistence of high levels of ancestral polymorphism. Other admixed individuals, however, are probably the result of limited levels of gene flow between forms. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 121–133.

Contrasting patterns of population subdivision and historical demography in three western Mediterranean lizard species inferred from mitochondrial DNA variation

Pleistocene climatic oscillations were a major force shaping genetic variability in many taxa. We analyse the relative effects of the ice ages across a latitudinal gradient in the Western Mediterranean region, testing two main predictions: (i) species with historical distributions in northern latitudes should have experienced greater loss of suitable habitat, resulting in higher extinction of historical lineages than species distributed in southern latitudes, where the effects of the ice ages were not as drastic. This would be reflected in the observation of lower diversity and number of differentiated lineages in northern areas. (ii) a signature of demographic expansion following the climate amelioration should be obvious in northern species, whereas in the south evidence of long-term effective population size stability should be observed. We used as models three species of wall lizards (Podarcis bocagei, Podarcis carbonelli and Podarcis vaucheri) that replace each other along the study area. We investigated the patterns of mitochondrial DNA diversity and subdivision and obtained demographic parameter estimates for each species. Our results suggest that P. bocagei, the northernmost species, bears low genetic diversity, a shallow coalescent history and marks of a demographic expansion. In contrast, P. vaucheri, the species with a southernmost distribution, shows deeper coalescence events, complex geographical substructure and no evidence for population growth. The species with an intermediate distribution, P. carbonelli, shows average levels of diversity, substructure and population growth. Taken together, these results conform to our main predictions and are explained by a differential influence of the ice ages on distinct latitudes.

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.

Factores ambientales condicionantes de la presenciade la lagartija de Carbonell Podarcis carbonelli (Pérez-Mellado, 1981) en la comarca de Doñana

Environmental factors determining the presence of the Carbonell lizard Podarcis carbonelli (Pérez-Mellado, 1981) in the Doñana area The Carbonell lizard (Podarcis carbonelli) is an Iberian endemism. The region of Doñana is its southernmost and more isolated stronghold. We used logistic regressions to investigate the factors conditioning the presence of this lizard in Doñana. All selected models retained the distance to the coast as the main variable. This variable is related with less humidity and more continental climatic conditions, including more extreme temperatures, when further from the coast. This climatic factor was observed both spatially and temporarily, with adult lizards drastically reducing their activity both in winter and in summer. We observed juveniles from June to January, with a maximum in September. Scrubland management was another important environmental factor affecting the presence of lizards. The probability of finding this species was higher where the scrubland was partially cleared, and lower in areas with a high plant cover (hygrophytic scrubland) or in areas with sparse vegetation (dune scrubland), probably due to a lower amount of incident light and less protection when moving between refuges, respectively.

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.

Podarcis carbonelli Pérez-Mellado, 1981 is a distinct species

AbstractPodarcis carbonelli is considered a full species on the basis of its morphological and genetic divergence from P. bocagei and P. hispanica. Podarcis carbonelli differs from P. bocagei in all twelve biometric variables compared and also in chromatic patterns. Podarcis carbonelli diverges from P.bocagei by more than 13% between cytochrome b sequences (mitochondrial DNA), a value typically reported between congeneric reptile species. Biogeographical criteria also support this hypothesis, as both lizard forms have different distribution ranges with a limited parapatric zone of contact without morphological intermediates.