Differential recovery ability from infections by two blood parasite genera in males of a Mediterranean lacertid lizard after an experimental translocation.

Different blood parasites can co-infect natural populations of lizards. However, our knowledge of the host's ability to recover from them (i.e., significantly reduce parasitemia levels) is scarce. This has interest from an ecological immunology perspective. Herein, we investigate the host recovery ability in males of the lizard Psammodromus algirus infected by parasite genera Schellackia and Karyolysus. The role of lizard hosts is dissimilar in the life cycle of these two parasites, and thus different immune control of the infections is expected by the vertebrate host. As Schellackia performs both sexual and asexual reproduction cycles in lizards, we expect a better immune control by its vertebrate hosts. On the contrary, Karyolysus performs sexual reproductive cycles in vectors, hence we expect lower immune control by the lizards. We carried out a reciprocal translocation experiment during the lizards' mating season to evaluate both parasitemia and leukocyte profiles in male lizards, being one of the sampling plots close to a road with moderate traffic. These circumstances provide a combination of extrinsic (environmental stress) and intrinsic factors (reproductive vs. immune trade-offs) that may influence host's recovery ability. We recaptured 33% of the lizards, with a similar proportion in control and translocated groups. Karyolysus infected 92.3% and Schellackia 38.5% of these lizards. Hosts demonstrated ability to significantly reduce parasitemia of Schellackia but not of Karyolysus. This suggests, in line with our predictions, a differential immune relationship of lizards with these parasites, at time that supports that parasites with different phylogenetic origins should be analyzed separately in investigations of their effects on hosts. Furthermore, lizards close to the road underwent a stronger upregulation of lymphocytes and monocytes when translocated far from the road, suggesting a putative greater exposure to pathogens in the latter area.

First helminthological data on the Iberian adder, Vipera seoanei.

The helminth fauna present in the gut contents of Iberian adders, Vipera seoanei (Squamata: Viperidae), were characterised and analysed in respect to biological and eco-geographic factors that may affect the occurrence and diversity of helminths in this species. A total of 317 samples of preserved stomachs and intestines, covering the distributional range of V. seoanei, were examined. Similar to other Vipera species from the Iberian Peninsula, the helminth fauna was also impoverished in V. seoanei, but unlike other Vipera species from Central and East Europe, helminths were mostly found in adult vipers, and occurred in vipers located at the periphery of the species range, characterised by low elevation, high temperature and precipitation levels, and abundant pastures.

Fecal glucocorticoid metabolites and ectoparasites as biomarkers of heat stress close to roads in a Mediterranean lizard.

Differences between air and ground temperatures are expected to narrow with the advance of the season in temperate regions (aka seasonal restriction in the availability of thermal microhabitats), which may activate behavioral and physiological responses of ectotherm species adapted to temperate climates. However, according to cost-benefit models of ectotherm thermoregulation, we hypothesize that these responses may also carry some costs. We quantified seasonal shifts in thermoregulatory precision, concentration of fecal glucocorticoid metabolites, and load of ectoparasites in a Mediterranean lizard, Psammodromus algirus. We also tested whether the proximity to a road, a putative source of chronic stress, can facilitate the glucocorticoid-mediated response of lizards to heat stress. As expected, differences between body and environmental temperatures narrowed during the reproductive season and lizards responded by increasing their thermoregulatory precision and the secretion of glucocorticoids, as indicated by metabolites in feces. Interestingly, lizards tended to have higher glucocorticoid concentration when captured far from the road. This might reflect either a putative impairment of the glucocorticoid-mediated response of the lizards to heat stress close to the road or the plastic capability of P. algirus to acclimate to sources of moderate chronic stress. In the latter direction, the increase of both glucocorticoid metabolites and thermoregulatory precision supported that this Mediterranean species responds to environmental thermal restrictions with adaptive behavioral and physiological mechanisms. However, this was also associated with an increase in its susceptibility to ectoparasites, which represents an added cost to the current cost-benefit models of ectotherm thermoregulation.

Plasticity of haemoglobin concentration and thermoregulation in a mountain lizard.

The plastic capability of species to cope with the new conditions created by climate change is poorly understood. This is particularly relevant for organisms restricted to high elevations because they are adapted to cold temperatures and low oxygen availability. Therefore, evaluating trait plasticity of mountain specialists is fundamental to understand their vulnerability to environmental change. We transplanted mountain lizards, Iberolacerta cyreni, 800 m downhill to evaluate the plastic response in body condition, thermoregulation traits, haemoglobin level, and haemoparasite load. Initial measurements of body mass, total haemoglobin concentration ([Hb]), hematic parasite intensities, dorsal luminance, and thermoregulatory behaviour were resampled after two and four weeks of acclimation. We also tested whether an anti-parasitic drug reduced haemoparasite intensity. After only two weeks of acclimation to a lower elevation, lizards decreased 42% in [Hb], had 17% less parasite intensities, increased body condition by 25%, and raised by ~3% their mean preferred temperatures and their voluntary thermal maximum. The anti-parasitic treatment had no significant effect on the intensity of hematic parasites, but our results suggest that negative effects of haemoparasites on [Hb] are relaxed at lower elevation. The rapid plastic changes observed in thermal preferences, body condition, [Hb], and parasite intensity of I. cyreni demonstrate a potential plastic response of a mountain specialist. This may be adaptive under the climatic extremes typical of mountain habitats. However, there is uncertainty in whether the observed plasticity can also help overcome long term environmental changes.

Geographic patterns of stress in insular lizards reveal anthropogenic and climatic signatures.

Anthropization of insular ecosystems may have negative impacts on native populations of lizards, which provide core ecosystem services on islands. We aimed to identify environmental factors to explain the interlocal variation in faecal glucocorticoids, parasite intensity, and body condition in populations of insular lizards. A cross-sectional design during the summer of 2017 and 2018 was used to sample 611 adult lizards, Gallotia galloti. Interlocal variation of three stress indicators was analysed in response to environmental variables across a wide environmental gradient in Tenerife (Canary Islands): (i) concentration of faecal glucocorticoids, (ii) intensities of infection by hematic parasites, and (iii) body condition. The data, with low spatial autocorrelation, were analysed using multimodel inference and model cross-validation. Bioclimatic variables associated with the extreme hot and dry climate of summer were the most informative predictors. Interlocal variation in faecal corticosterone in males was best fitted to a model that included the maximum temperature of the warmest month, although the best predictor was habitat anthropization. The thermal annual range, associated with extreme thermal events, was positively related to faecal corticosterone in females. Extreme hot temperatures were positively related to the median parasite intensities in both sexes, while the highest mean intensities of infection were found in females from the most xeric coastal localities. None of the predictors tested, including faecal glucocorticoids, explained individual or interlocal variation in body condition. Effects of human pressure and climate change on insular populations of lizards can be additive. However, the uncoupled relationship found between body condition and the faecal glucocorticoid content suggests that current negative effects may be aggravated during drought periods in summer. Given the impact of climate change on islands, our results may be of application to other archipelagos, where lizards also play key ecological roles.

To cool or not to cool? Intestinal coccidians disrupt the behavioral hypothermia of lizards in response to tick infestation.

It is generally accepted that parasites exert negative effects on their hosts and that natural selection favors specific host responses that mitigate this impact. It is also known that some components of the host immune system often co-evolve with parasite antigens resulting in a host-parasite arms race. In addition to immunological components of the anti-parasitic response, host behavioral responses are also important in this arms race and natural selection may favor avoidance strategies that preclude contact with parasites, or shifts in the host's thermoregulatory strategy to combat active infections (e.g., behavioral fever). Ticks are widespread parasites with direct and indirect costs on their vertebrate hosts. Their saliva provokes hemolysis in the blood of their hosts and can transmit a plethora of tick-borne pathogens. We enquired whether tick infestation by Ixodes pacificus can provoke a thermoregulatory response in Sceloporus occidentalis. For this, we compared the thermoregulatory behavior of tick-infested lizards against tick-infested lizards co-infected with two different species of coccidians (Lankesterella occidentalis and Acroeimeria sceloporis). After this, lizards were kept in individual terraria with a basking spot and fed ad libitum. We found that tick-infested lizards sought cooler temperatures in proportion to their tick load, and this response was independent of the co-infection status by L. occidentalis. This was consistent in April and June (when tick loads were significantly lower) and suggests a conservative strategy to save energy which might have been selected to overcome tick infestations during phenological peaks of this parasite. However, this behavior was not observed in lizards co-infected with A. sceloporis, suggesting that co-infection with this intestinal parasite prompt lizards to be active. Cost of tick infestation was confirmed because housed lizards lost weight at a constant ratio to initial tick load, independently of other infections. The broader implications of these findings are discussed in the context of climate change.

Phylogenetic analysis based on 18S rRNA gene sequences of Schellackia parasites (Apicomplexa: Lankesterellidae) reveals their close relationship to the genus Eimeria.

In the present study we detected Schellackia haemoparasites infecting the blood cells of Lacerta schreiberi and Podarcis hispanica, two species of lacertid lizards from central Spain. The parasite morphometry, the presence of a refractile body, the type of infected blood cells, the kind of host species, and the lack of oocysts in the fecal samples clearly indicated these blood parasites belong to the genus Schellackia. Until now, the species of this genus have never been genetically characterized and its taxonomic position under the Lankesterellidae family is based on the lack of the exogenous oocyst stage. However, the phylogenetic analysis performed on the basis of the 18S rRNA gene sequence revealed that species of the genus Schellackia are clustered with Eimeria species isolated from a snake and an amphibian species but not with Lankesterella species. The phylogenetic analysis rejects that both genera share a recent common ancestor. Based on these results we suggest a revision of the taxonomic status of the family Lankesterellidae.