We present the first study that compares phenological variation in parasite load and inflammatory response in a lizard with asynchronous male and female gonadal cycles. Other studies have used many species with seasonal and synchronous reproductive cycles, in which it is difficult to decouple the effects of internal and external factors that can affect parasite abundance in each sex. Species with asynchronous reproductive cycles provide the opportunity to study the effects of seasonality and reproductive condition separately, but few studies have documented variation in parasite abundance in these species. We made an extensive comparison of parasite load and inflammatory response of the lizard Sceloporus torquatus, a species with asynchronous reproductive cycles, throughout its active period. We hypothesized that the parasite load would be higher in the period of maximum gonadal activity for each sex, negatively related to body condition and inflammatory response. Our results partially support the hypothesis; males had more parasites in summer than in spring and autumn, while females had more parasites in spring and summer than in autumn; however, we do not find a relationship between parasite load, body condition and inflammatory response. Our results indicated that host-parasite interactions are complex and depend upon both environmental and internal factors. Therefore, longer-term studies may provide a more comprehensive picture of host-parasite dynamics in populations of wild lizards.
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.
Ectotherms are vulnerable to environmental changes and their parasites are biological indicators of their health. Thus, parasite load in ectotherms is expected to show a marked phenology consistent with seasonal changes in the environment. The present study investigates temporal host-parasite dynamics in a lizard community in the Eastern Iberian Peninsula during an entire annual activity period. The host species investigated were Acanthodactylus erythrurus, Psammodromus algirus, and Psammodromus edwardsianus, three lizard species coexisting in a mixed habitat of forests and dunes, providing a range of body sizes, ecological requirements and life history traits. Habitat and climate were considered as potential environmental predictors of parasite abundance, while size, body condition, and sex were considered as intrinsic predictors. Linear models based on robust estimates were fitted to analyse parasite abundance and prevalence. Ectoparasitic haematophagous mites and blood parasites from two genera of haemococcidians were found: Lankesterella spp. and Schellackia spp. The former genus was almost exclusively infecting A. erythrurus, while Schellackia spp. infected the three host species. Habitat type was the only predictor that explained the abundance of all parasites, being mostly higher in the forest than in the dunes except for mites in P. algirus. Besides habitat, different predictors significantly explained different parasites, suggesting that particularities in each host-parasite relationship should be accounted even when parasites infect close-related hosts under the same environmental pressures. Our results support the concept that parasites of lizards can be biomarkers of environmental perturbation, but direction of relationships need to be carefully interpreted for each host-parasite assemblage.
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.
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 meters 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.
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.
Parasites are important in population dynamics. Since parasites compete with their host for resources, causing damage to many aspects of the host, parasitism interacts with many selective forces driving host's evolution. In a scenario of global change, there are many organisms shifting their distributions (i.e. parasites and their hosts); frequently towards higher latitudes and altitudes. Running studies in altitudinal gradient framework can help us to understand the adaptations of species to different environments (i.e. environmental conditions, species interactions). In this context, our aim was to determine patterns of variation in lizards' parasite (the ectoparasite Ophyonissus spp. and the intraerythrocitic parasite Hepatozoon spp) prevalence along altitude. For this aim we studied the Mediterranean lizard Psammodromus algirus (Linnaeus, 1758) in six localities along a 2200m altitudinal gradient. Under the hypothesis that warmer thermal conditions at lowlands predict better conditions for parasites development, we predict that lowlands populations will show higher parasites prevalence. According to our hypothesis, we found higher prevalence of ectoparasites in lowlands lizards, being inexistent over 2000 m asl. In contrast, intraerythrocitic parasites prevalence increased in altitude. The known transmitter of Hepatozoon found in lizards is mites of the genus Ophyonissus. Therefore, since we failed to find mites at highlands, our results suggest that might be another transmitter. More humid conditions at highlands suggest that mosquitos might be the transmitters. In addition, there were sexual differences in prevalence. Following the handicap principle, higher levels of testosterone may be the reason of higher prevalence in males, independently of the altitude.
Studying the causes of parasite geographic distribution is relevant to understand ecological and evolutionary processes that affect host populations as well as for species conservation. Temperature is one of the most important environmental variables affecting parasite distribution, as raising temperatures positively affect development, reproduction, and rate of transmission of both endo- and ectoparasites. In this context, it is generally accepted that, in mountains, parasite abundance decreases with elevation. However, empirical evidence on this topic is limited. In the present study, we analysed the elevational variation of haemoparasites and ectoparasites of a lizard, Psammodromus algirus, along a 2200-m elevational gradient in Sierra Nevada (SE Spain). As predicted, ectoparasite (mites, ticks, mosquitoes, and sandflies) abundance decreased with elevation. However, haemoparasite prevalence and intensity in the lizard augmented with altitude, showing a pattern contrary to their vectors (mites). We suggest that tolerance to haemoparasites may increase with elevation as a consequence of lizards at high altitudes taking advantage of increased body condition and food availability, and reduced oxidative stress. Moreover, lizards could have been selected for higher resistance against haemoparasites at lowlands (where higher rates of replication are expected), thus reducing haemoparasite prevalence and load. Our findings imply that, in a scenario of climate warming, populations of lizards at high elevation may face increased abundance of ectoparasites, with accompanied strong negative effects.