Adult Lizards Research Articles

Immune responses of a wall lizard to whole-body exposure to radiofrequency electromagnetic radiation

Purpose During the last three decades, the number of devices that emit non-ionizing electromagnetic radiation (EMR) at the wireless communication spectrum has rapidly increased and possible effects on living organisms have become a major concern. The purpose of this study was to investigate the effects of radiofrequency EMR emitted by a widely used wireless communication device, namely the Digital Enhanced Communication Telephony (DECT) base, on the immune responses of the Aegean wall lizard (Podarcis erhardii).Materials and methods Adult male lizards were exposed 24 h/day for 8 weeks to 1880–1900 MHz DECT base radiation at average electric field intensity of 3.2 V/m. Immune reactivity was assessed using the phytohemagglutinin (PHA) skin swelling and mixed lymphocyte reaction (MLR) tests.Results Our results revealed a noticeable suppression (approximately 45%) of inflammatory responses in EMR-exposed lizards compared to sham-exposed animals. T cell-mediated responses were marginally affected.Conclusion Daily radiofrequency EMR exposure seems to affect, at least partially, the immunocompetence of the Aegean wall lizard.

Ontogenetic Variation in the Thermal Biology of Yarrow's Spiny Lizard, Sceloporus jarrovii.

Climate change is rapidly altering the way current species interact with their environment to satisfy life-history demands. In areas anticipated to experience extreme warming, rising temperatures are expected to diminish population growth, due either to environmental degradation, or the inability to tolerate novel temperature regimes. Determining how at risk ectotherms, and lizards in particular, are to changes in climate traditionally emphasizes the thermal ecology and thermal sensitivity of physiology of adult members of a population. In this study, we reveal ontogenetic differences in thermal physiological and ecological traits that have been used to anticipate how ectotherms will respond to climate change. We show that the thermal biological traits of juvenile Yarrow’s Spiny Lizards (Sceloporus jarrovii) differ from the published estimates of the same traits for adult lizards. Juvenile S. jarrovii differ in their optimal performance temperature, field field-active body temperature, and critical thermal temperatures compared to adult S. jarrovii. Within juvenile S. jarrovii, males and females exhibit differences in field-active body temperature and desiccation tolerance. Given the observed age- and sex-related variation in thermal physiology, we argue that not including physiological differences in thermal biology throughout ontogeny may lead to misinterpretation of patterns of ecological or evolutionary change due to climate warming. Further characterizing the potential for ontogenetic changes in thermal biology would be useful for a more precise and accurate estimation of the role of thermal physiology in mediating population persistence in warmer environments.

Artificial Water Point for Livestock Influences Spatial Ecology of a Native Lizard Species.

Pastoralism is a major agricultural activity in drier environments, and can directly and indirectly impact native species in those areas. We investigated how the supply of an artificial watering point to support grazing livestock affected movement and activity patterns of the Australian sleepy lizard (Tiliqua rugosa) during a drought year. We observed 23 adult lizards; six had access to a dam, whereas 17 lizards did not. Lizards with access to the dam had larger home ranges, were substantially active on more days (days with >100 steps), and moved more steps per day compared to lizards that did not have access to the dam, both during the early and late period of our observation. Furthermore, while the two groups of lizards had similar body condition early in the season, they differed later in the season. Lizards with dam access retained, whereas lizards without access lost body condition. Local heterogeneity in access to an artificial water resource resulted in spatially dependent behavioural variation among sleepy lizard individuals. This suggests that sleepy lizards have flexible responses to changing climatic conditions, depending on the availability of water. Furthermore, while reducing activity appears a suitable short term strategy, if harsh conditions persist, then access to dams could be of substantial benefit and could support sustained lizard activity and movement and allow maintenance of body condition. Hence, artificial watering points, such as the dams constructed by pastoralists, may provide local higher quality refugia for sleepy lizards and other species during drought conditions.

The role of male coloration in the outcome of staged contests in the European common wall lizard (Podarcis muralis)

Colour signals play a key role in regulating the intensity and outcome of animal contests. Males of the common wall lizard (Podarcis muralis) show conspicuous ventrolateral ultraviolet (UV)-blue and black patches. In addition, some populations express a striking ventral colour polymorphism (i.e., discrete orange, white and yellow morphs). In this study, we set out to evaluate the potential signalling function of these colour patches by staging pairwise combats between 60 size-matched adult lizards (20 per morph). Combats were held in a neutral arena, with each lizard facing rivals from the three morphs in a tournament with a balanced design. We then calculated a fighting ability ranking using the Bradley–Terry model, and used it to explore whether ventral colour morph, the size of UV-blue and black patches or the spectral characteristics of UV-blue patches (i.e., brightness, hue, chroma) are good predictors of fighting ability. We did not find an effect of the UV-blue patches on contest outcome, but the size of black patches emerged as a good predictor of fighting ability. We also found that winners were more aggressive when facing rivals with black patches of similar size, suggesting that black patches play a role in rival assessment and fighting rules. Finally, we found that orange males lost fights against heteromorphic males more often than yellow or white males. In light of these results, we discuss the potential signalling function of ventrolateral and ventral colour patches in mediating agonistic encounters in this species.

Environment modulates population social structure: experimental evidence from replicated social networks of wild lizards

Social structure is a fundamental component of a population that drives ecological and evolutionary processes ranging from parasite transmission to sexual selection. Nevertheless, we have much to learn about factors that explain variation in social structure. We used advances in biologging and social network analysis to experimentally test how the local habitat, and specifically habitat complexity, modulates social structure at different levels in wild populations. Sleepy lizards, Tiliqua rugosa , establish nonrandom social networks that are characterized by avoidance of some neighbours and frequent interactions with one opposite-sex individual. Using synchronous GPS locations of all adult lizards, we constructed social networks based on spatial proximity of individuals. We increased habitat structural complexity in two study populations by adding 100 short fences across the landscape. We then compared the resulting movement behaviour and social structure between these populations and two unmanipulated populations. Social connectivity (network density) and social stability, measured at weekly intervals, were greater in populations with increased habitat structural complexity. The level of agonistic interaction (quantified as scale damage) was also higher, indicating a fitness cost of greater social connectivity. However, some network parameters were unaffected by increased complexity, including disassortative mixing by sex, and at the individual level, social differentiation among associates (coefficient of variation of edge weights) and maximal interaction frequencies (maximal edge weight). This suggests divergent effects of changed ecological conditions on individual association behaviour compared to the resulting social structure of the population. Our results contrast with those from studies of more gregarious species, in which higher structural complexity in the environment relaxed the social connectivity. This shows that the response to altered ecological conditions can differ fundamentally between species or between populations, and we suggest that it depends on their tendency for gregarious behaviour. • We investigated how environmental conditions modulate social structure. • We conducted a replicated experiment in wild lizard populations. • Network density was greater in populations with increased habitat complexity. • Social differentiation at the individual level was unaffected. • Our results suggest divergent effects on the individual and population level.

Estrogenic contamination by manure fertilizer in organic farming: a case study with the lizard Podarcis sicula.

In the last years, worldwide organic farming has grown exponentially; as a consequence, the use of animal manure as a soil fertility source has become the principal agricultural choice. However, the use of manure as fertilizer can increase the amount of steroid hormone metabolites in the soil. In southern Italy, lacertidae lizards are the most abundant vertebrate group in agroecosystems and have been identified as potential model species for ecotoxicological studies. The aim of this study was to understand if the manure applied in organic farming has estrogen-like effects in the lizard Podarcis sicula. Adult male lizards were captured in two organic agricultural fields (manure-treated sites) and in an uncultivated field (control site). Lizards from the two organic farms displayed hepatic biosynthetic alterations typical of an estrogenic contamination; hepatocytes contained both vitellogenin and estrogen receptor alpha transcripts and proteins, detected by in situ hybridization and immunocytochemistry. The same cells did not show cadmium, lead and metallothionein accumulation, indicative of the lack of inorganic contamination. These findings suggest that exogenous estrogens, arising from the use of manure, could affect the welfare of wild animals and animal breeding, leading to bioaccumulation of estrogens in food chain, with possible risk for human consumers. For this reason, organic farming should implement the use of sustainable practices such as crop rotation to preserve the soil biological activity, rather than organic manure as fertilizer.

Regeneration of Articular Cartilage in Lizard Knee from Resident Stem/Progenitor Cells.

The epiphysis of femur and tibia in the lizard Podarcis muralis can extensively regenerate after injury. The process involves the articular cartilage and metaphyseal (growth) plate after damage. The secondary ossification center present between the articular cartilage and the growth plate is replaced by cartilaginous epiphyses after about one month of regeneration at high temperature. The present study analyzes the origin of the chondrogenic cells from putative stem cells located in the growing centers of the epiphyses. The study is carried out using immunocytochemistry for the detection of 5BrdU-labeled long retaining cells and for the localization of telomerase, an enzyme that indicates stemness. The observations show that putative stem cells retaining 5BrdU and positive for telomerase are present in the superficial articular cartilage and metaphyseal growth plate located in the epiphyses. This observation suggests that these areas represent stem cell niches lasting for most of the lifetime of lizards. In healthy long bones of adult lizards, the addition of new chondrocytes from the stem cells population in the articular cartilage and the metaphyseal growth plate likely allows for slow, continuous longitudinal growth. When the knee is injured in the adult lizard, new populations of chondrocytes actively producing chondroitin sulfate proteoglycan are derived from these stem cells to allow for the formation of completely new cartilaginous epiphyses, possibly anticipating the re-formation of secondary centers in later stages. The study suggests that in this lizard species, the regenerative ability of the epiphyses is a pre-adaptation to the regeneration of the articular cartilage.

Experience may allow increasing accuracy of the innate chemosensory recognition of snake predators by Iberian wall lizards

Many animals can recognize chemical cues of predators and show defensive responses, but antipredatory behavior can be costly and should be modulated depending on the level of risk posed by each predatory species. Recognition ability may be innate, but it is not clear whether there might also be local adaptation to predation pressure levels or some learning component. We examined the chemosensory ability of naive and adult Iberian wall lizards, Podarcis hispanicus, to detect chemical cues of two closely related Coronella snake species in two localities within the same continuous population. Lizards in each locality are sympatric with only one of the two snake species. Our results showed an innate chemosensory discrimination of predatory snake cues, as both adult lizards and captive reared naive hatchlings, which had not had any previous experience with the snake cues, had short latencies to the first tongue-flick, increased tongue-flick responses, and active escape behavior from the scent of either of the two snake species. Moreover, adult lizards, but not naive hatchlings, showed differential responses to the two different snake species, with higher responses to the snake species that is sympatric in each locality. This strongly suggests that there is a learning component acquired through previous lifetime experiences that may increase accuracy of the discrimination of the sympatric snake. Therefore, through learning of local conditions, lizards may modulate their innate antipredatory responses to the risk level posed by each snake species.

A place in the sun: interspecific interference affects thermoregulation in coexisting lizards

Solar radiation is in theory an unlimited resource on Earth, but can be locally limited. Heliothermic organisms use solar radiation to elevate their body temperatures, leading them to compete for sun-exposed areas, where interference for limited resource can occur. In coexisting lizard species, interference for basking sites could promote and direct interspecific interactions, which can be related to broader geographic species distribution patterns. We compared two competing lizard species (Podarcis muralis and Iberolacerta horvathi) that occupy sun-exposed gaps in a forested landscape in the Northern Dinaric Mountains (southern Europe). Both species exhibit an altitudinal segregation pattern with a high zone of overlap at middle altitudes. Using experimental thermal gradients, we tested for existence of interference competition. We used adult male lizards in three social contexts, alone as a measure of preferred body temperature (T p) and in conspecific or heterospecific pairs as a measure of realized body temperature (T r). I. horvathi achieved lower T r compared to its T p (alone), while T r of P. muralis did not vary between social contexts. The evidence for interference found in I. horvathi could not be explained by a change in their general movement pattern in a thermal gradient. Our results suggest that interference was a result of direct agonistic interactions, assessed by the frequency of approaches and touches. I. horvathi showed higher interference-susceptibility than P. muralis indicating an asymmetric interaction between the two species. Sunlight (as a resource) is an important factor influencing distribution patterns in assemblages of heliothermic ectotherms where sun-exposed basking sites are limited.

Diet of the Tepalcatepec Valley whiptail,Aspidoscelis calidipes(Squamata: Teiidae), in Michoacán, México

Abstract We investigated the diet of the endemic teiid lizard Aspidoscelis calidipes in the Balsas-Tepalcatepec Basin in the state of Michoacan, Mexico, during 2010 and 2011. We removed, analyzed, and identified stomach contents to order or family. The diet of A. calidipes consisted of 27 prey taxa and the dietary diversity was low (H′ = 0.45). Termites and ants were the most important prey items. Adult and juvenile lizards consumed greater proportions of termites than any other prey item by number, volume, and frequency. Diet diversity of juveniles was higher (H′ = 1.15) than that of adults (H′= 0.28). Dietary overlap between adults and juveniles was 49%.

Age affects escape behavior by the zebra-tailed lizard (Callisaurus draconoides) more strongly than in other lizards

Prey of different ages may exhibit differences in escape behavior, including flight initiation distance (FID – predator-prey distance when escape begins) and distance fled before stopping (DF). Escape theory predicts FID and, in some circumstance, DF, based on trade-offs between conflicting cost of not fleeing (predation risk) and cost of fleeing (primarily opportunities to enhance fitness lost by fleeing). The prey’s expected lifetime fitness when an encounter begins also affects escape decisions. Because hatchling and adult lizards may differ in ways that affect all three of these factors, a priori prediction of age differences is not possible without measurements of all three. In a field study I found that hatchling zebra-tailed lizards (Callisaurs draconoides) had much shorter FID and DF than adults. These relationships were not affected by distance to refuge, which did not differ between ages, and refuge use was infrequent. The findings agree with those of all but one previous study of age differences, suggesting that hatchling lizards typically have shorter FID and DF than adults because they 1) assess risk as being lower due to lower attractiveness to or detectability by predators, lack of experience or greater maneuverability, 2) have greater opportunity cost due to the need for rapid growth and good body condition before winter, and possibly 3) have lower residual reproductive value due to higher mortality rate than adults. Effects of age and size are confounded, and smaller size may be the major reason for the shorter FID and distance fled of hatchlings.

European green lizard (Lacerta viridis) personalities: Linking behavioural types to ecologically relevant traits at different ontogenetic stages

Consistent individual differences within (animal personality) and across (behavioural syndrome) behaviours became well recognized during the past decade. Nevertheless, our knowledge about the evolutionary and developmental mechanisms behind the phenomena is still incomplete. Here, we explored if risk-taking and exploration were consistent and linked to different ecologically relevant traits in wild-caught adult male European green lizards (Lacerta viridis) and in their 2–3 weeks old laboratory-reared offspring. Both adults and juveniles displayed animal personality, consistency being higher in juveniles. We found correlation between risk-taking and exploration (suggestive of a behavioural syndrome) only in adults. Juveniles were more explorative than adults. Large or ectoparasite-free adult males were more explorative than small or parasitized males. Juvenile females tended to be more risk-taking than males. Behaviour of fathers and their offspring did not correlate. We conclude that European green lizards show high behavioural consistency and age is an important determinant of its strength and links to traits likely affecting fitness.

Sex, Age, and Population Density Affect Aggressive Behaviors in Island Lizards Promoting Cannibalism

AbstractIsland populations may evolve distinct behavioral repertoires as a response to the conditions of insular life. Strong intraspecific competition is typical in insular lizards and may include cannibalism. In this study, we investigated sexual and age patterns of aggression in two populations of the Skyros wall lizard (Podarcis gaigeae), one from the main island of Skyros (Aegean Sea, Greece) and another from the satellite islet Diavates. The latter is terrestrial predator‐free biotope, hosting a dense population of large‐bodied lizards that have been reported to exert cannibalism. In staged encounters, we examined the aggressive propensities of adult male and female lizards against their age‐peers and juveniles. Males from both populations were much more aggressive than females toward juveniles and other adults. Males from Diavates were more frequently aggressive to juveniles and other male lizards than males from Skyros. Diavates cannibals also captured their targets at shorter latency. We ascribe this distinct behavioral pattern to the high population density. Infanticide and intramale aggressiveness confer two great advantages to cannibals: food and elimination of future rivals.

Geographical variation in body size and sexual size dimorphism in an Australian lizard, Boulenger's Skink (Morethia boulengeri).

Ecogeographical rules help explain spatial and temporal patterns in intraspecific body size. However, many of these rules, when applied to ectothermic organisms such as reptiles, are controversial and require further investigation. To explore factors that influence body size in reptiles, we performed a heuristic study to examine body size variation in an Australian lizard, Boulenger's Skink Morethia boulengeri from agricultural landscapes in southern New South Wales, south-eastern Australia. We collected tissue and morphological data on 337 adult lizards across a broad elevation and climate gradient. We used a model-selection procedure to determine if environmental or ecological variables best explained body size variation. We explored the relationship between morphology and phylogenetic structure before modeling candidate variables from four broad domains: (1) geography (latitude, longitude and elevation), (2) climate (temperature and rainfall), (3) habitat (vegetation type, number of logs and ground cover attributes), and (4) management (land use and grazing history). Broad phylogenetic structure was evident, but on a scale larger than our study area. Lizards were sexually dimorphic, whereby females had longer snout-vent length than males, providing support for the fecundity selection hypothesis. Body size variation in M. boulengeri was correlated with temperature and rainfall, a pattern consistent with larger individuals occupying cooler and more productive parts of the landscape. Climate change forecasts, which predict warmer temperature and increased aridity, may result in reduced lizard biomass and decoupling of trophic interactions with potential implications for community organization and ecosystem function.

Differences in the thermal physiology of adult Yarrow's spiny lizards (Sceloporus jarrovii) in relation to sex and body size.

Sexual size dimorphism (SSD) is often assumed to reflect the phenotypic consequences of differential selection operating on each sex. Species that exhibit SSD may also show intersexual differences in other traits, including field-active body temperatures, preferred temperatures, and locomotor performance. For these traits, differences may be correlated with differences in body size or reflect sex-specific trait optima. Male and female Yarrow's spiny lizards, Sceloporus jarrovii, in a population in southeastern Arizona exhibit a difference in body temperature that is unrelated to variation in body size. The observed sexual variation in body temperature may reflect divergence in thermal physiology between the sexes. To test this hypothesis, we measured the preferred body temperatures of male and female lizards when recently fed and fasted. We also estimated the thermal sensitivity of stamina at seven body temperatures. Variation in these traits provided an opportunity to determine whether body size or sex-specific variation unrelated to size shaped their thermal physiology. Female lizards, but not males, preferred a lower body temperature when fasted, and this pattern was unrelated to body size. Larger individuals exhibited greater stamina, but we detected no significant effect of sex on the shape or height of the thermal performance curves. The thermal preference of males and females in a thermal gradient exceeded the optimal temperature for performance in both sexes. Our findings suggest that differences in thermal physiology are both sex- and size-based and that peak performance at low body temperatures may be adaptive given the reproductive cycles of this viviparous species. We consider the implications of our findings for the persistence of S. jarrovii and other montane ectotherms in the face of climate warming.

The vertebrate muscle-specific RING finger protein family includes MuRF4 – A novel, conserved E3-ubiquitin ligase

Muscle-specific RING finger (MuRF) proteins are E3-ubiquitin ligases and key regulators of muscle growth and turnover. Here, using a range of phylogenomic approaches, we established the complete-definitive MuRF family of vertebrates. Adding to recognized MuRF1, 2 and 3, we describe a novel family member, hereafter MuRF4, which was independently lost during placental mammal and bird evolution, but is otherwise conserved. MuRF4 transcripts were expressed in heart and skeletal muscles of zebrafish, but were barely detectable in striated muscles of adult anole lizards. We also demonstrate that MuRF1 underwent retrotransposition in the teleost fish ancestor, before the retrogene fully replaced the original gene and muscle-specific function.

Imidacloprid induces morphological and molecular damages on testis of lizard (Podarcis sicula)

The insecticide imidacloprid was evaluated under laboratory conditions in the adult male Italian wall lizards (Podarcis sicula) to assess its potential toxicity. By an acute oral test, LD50 was 503.76mg/kg. Changes in spermatogenesis, plasma sex hormone levels and androgen and oestrogen receptor mRNAs were analysed by subchronic test and simulated environmental exposure. 15-days subchronic test, in which lizards were orally dosed on alternate days at 0, 10, 50, 100mg/kg bw, showed a dose-dependent changes of testicular architecture and an increase of apoptotic processes. In a 30-days simulated environmental exposure spermatogenesis was arrested at secondary spermatocyte level and only few primary spermatocytes were TUNEL-positive. In all experimental groups imidacloprid was able to decrease both the level of sex hormones and the steroid receptor mRNAs. The results demonstrate that imidacloprid affects reproduction function of male lizards therefore precautions must be taken to minimize the harmful effects of this compound.

Evolution and development of ventricular septation in the amniote heart.

During cardiogenesis the epicardium, covering the surface of the myocardial tube, has been ascribed several functions essential for normal heart development of vertebrates from lampreys to mammals. We investigated a novel function of the epicardium in ventricular development in species with partial and complete septation. These species include reptiles, birds and mammals. Adult turtles, lizards and snakes have a complex ventricle with three cava, partially separated by the horizontal and vertical septa. The crocodilians, birds and mammals with origins some 100 million years apart, however, have a left and right ventricle that are completely separated, being a clear example of convergent evolution. In specific embryonic stages these species show similarities in development, prompting us to investigate the mechanisms underlying epicardial involvement. The primitive ventricle of early embryos becomes septated by folding and fusion of the anterior ventricular wall, trapping epicardium in its core. This folding septum develops as the horizontal septum in reptiles and the anterior part of the interventricular septum in the other taxa. The mechanism of folding is confirmed using DiI tattoos of the ventricular surface. Trapping of epicardium-derived cells is studied by transplanting embryonic quail pro-epicardial organ into chicken hosts. The effect of decreased epicardium involvement is studied in knock-out mice, and pro-epicardium ablated chicken, resulting in diminished and even absent septum formation. Proper folding followed by diminished ventricular fusion may explain the deep interventricular cleft observed in elephants. The vertical septum, although indistinct in most reptiles except in crocodilians and pythonidsis apparently homologous to the inlet septum. Eventually the various septal components merge to form the completely septated heart. In our attempt to discover homologies between the various septum components we aim to elucidate the evolution and development of this part of the vertebrate heart as well as understand the etiology of septal defects in human congenital heart malformations.

Extreme variant of the triploid parthenogenetic lizardAspidoscelis exsanguis(Squamata: Teiidae) from New Mexico

Abstract Parthenogenetic reproduction in several all-female species of whiptail lizards (genus Aspidoscelis) does not preclude the occasional production of extreme variants. An adult lizard with a unique combination of dorsal color pattern, scutellation, and meristic characters captured 20 August 2013 approximately 200 m east of the Rio Grande in Bosque Farms, Valencia County, New Mexico, was inferred to be an extreme variant of triploid, hybrid-derived Aspidoscelis exsanguis which was also observed near the point of capture. There was no basis for identifying the specimen as a tetraploid hybrid because morphology did not reflect that origin and no gonochoristic species (e.g., Aspidoscelis marmorata or Aspidoscelis inornata) was known to occur at the site. Morphological analyses also ruled out the possibility that it could be an extreme variant of diploid parthenogenetic Aspidoscelis neomexicana, which is syntopic with A. exsanguis in Bosque Farms.

Temporal and ontogenetic variation in the escape response of Ameiva festiva (Squamata, Teiidae)

Several factors have been shown to affect lizard escape behavior (flight initiation distance or FID, the distance between predator and prey when the prey initiates escape). Patterns of daily activity, such as foraging or movement behavior, vary with respect to time of day, supporting that escape responses may vary temporally as well. However, there remains scant information regarding the effects of time of day on FID. During peak activity, FID may decrease due to increased cost of giving up resources (e.g., prey or potential mates). An alternative hypothesis is that FID may increase because lizard activity in general may serve to alert a predator in advance of its approach. A lizard in this scenario may be favored to flee sooner rather than later. Moreover, juvenile and adult lizards of multiple species may differ in behavioral, ecological, and morphological traits that could influence escape decisions. I tested the effects of time of day (in 30-min intervals) and age (juvenile or adult) on the FID of a tropical whiptail lizard, Ameiva festiva in Costa Rica. I found that A. festiva escape responses varied with time of day such that in general, their FID decreased throughout the day. In addition, I observed a peak in FID from mid to late-morning that matches published estimates of peak activity times for A. festiva. Overall, juvenile A. festiva initiated an escape response sooner than adults, which may be related to differences in perceived risk associated with differences in size and predator experience between the two age groups. I conclude that escape responses may be contingent on both the activity level of the animal at the time of approach and its age.