Free-living Lizards Research Articles

Tolerance and osmotic response to food deprivation and salt loading in the herbivorous non-drinking Moroccan Spiny-tailed lizard Uromastyx nigriventris (Sauria: Agamidae)

Abstract Animals inhabiting arid environments use a variety of behavioural and physiological strategies to balance their water and salt budgets. We studied the effects of dehydration and salt loading on osmoregulatory capacities in a large herbivorous desert lizard, the Moroccan Spiny-tailed lizard Uromastyx nigriventris, the family Agamidae. These lizards select plants with a high K+ to Na+ ratio of 15 to 20, and like other herbivorous lizards, effectively eliminate the extra electrolyte load, mainly via a pair of active nasal salt glands, which exude the extra ions from blood. Here we present results of a series of laboratory experiments, which tested a five-week food and water deprivation and the excretory response of nasal salt glands, during a short period of five days, following salt loading by two separated injections of KCl or NaCl at a 5-day interval (4th and 9th days). During food-water deprivation, hypohydrated lizards lost 32% of their initial body mass with a substantial decrease of their Body Condition Index and the tail volume as an index of energy (fat and then potential metabolic water) storage. Plasma osmolality significantly increased by 20%. There were also significantly increased plasma sodium, chloride, and total protein concentrations. On the other hand, there was no significant decrease in the plasma glucose level. Most of the salt loaded lizards secreted far more K+ than Na+ via the nasal glands, even after NaCl loading. The K+/Na+ ratio decreased only after two to three repetitive NaCl injections but insufficient Na+ was eliminated. Two successive KCl injections were successfully eliminated, but daily natural average K+ administration induced progressive hyperkaliemia. These experimental data agreed with previous observations showing variations of plasma Na+ and K+ concentrations in free-living lizards. The nasal gland constitutes the main route of Cl− excretion but the Cl−/(Na+ + K+) ratio may vary according to observations in other herbivorous species.

Thinking outside the box: problem-solving in free-living lizards

Despite evidence that organisms are more likely to exhibit their full range of cognitive abilities under conditions found in nature, studies evaluating cognition under such conditions remain rare, particularly in vertebrate species. Here, we conducted an experiment to evaluate problem-solving and motor self-regulation in free-living arboreal lizards, Anolis sagrei, under natural conditions. We presented lizards with a novel detour problem which challenged individuals to circumvent a transparent barrier in order to obtain a food reward. Individuals varied in their ability to solve the detour problem. Furthermore, those that solved the problem were able to improve their performance across trials by modifying the natural response of attempting to strike the reward through the transparent barrier, providing evidence of motor self-regulation. Solving the problem required individuals to modify their typical foraging behavior, as approaching the prey in a single burst of movement that culminated with an attack was an unsuccessful strategy. Contrary to expectations, our findings provide evidence of motor self-regulation in a visually oriented, sit-and-wait predator under natural conditions, suggesting motor self-regulation is not limited by foraging strategy. Our results also underscore the need to evaluate the cognitive abilities of free-living organisms in the wild, particularly for taxa that perform poorly under laboratory conditions. Studies of animal cognition have a long history in animal behavior, which, in vertebrate species, has been dominated by experiments conducted under controlled laboratory conditions. Here, we showed that experiments can be taken “outside the box,” from the laboratory into natural conditions, and by doing so overcome some of the obstacles that have hindered our ability to study cognition in species unlikely to remain motivated when removed from the wild. We implemented a modified version of the cylinder task, which provided the stimuli needed for a visually oriented, sit-and-wait foraging lizard to participate in the experiments. Individuals of Anolis sagrei learned to solve the task by modifying what was previously described as a stereotyped prey capture behavior. In addition, individuals decreased the number of times they attempted to strike the prey through the transparent barrier. These findings provide further evidence of behavioral flexibility in anoles and new evidence of motor self-regulation. The latter demonstrates the need to extend our current understanding of potential forces favoring the evolution of cognition beyond those that have been proposed in birds and mammals. More generally, our findings demonstrate the importance of using experimental paradigms that are rooted in an understanding of the natural history of the species of interest.

In vitro virulence characteristics of rare serovars of Salmonella enterica isolated from sand lizards (Lacerta agilis L.)

The aim of this study was to estimate virulence potential of Salmonella enterica strains colonizing the gut of free-living sand lizards (Lacerta agilis L.). The strains belonged to three Salmonella serovars: Abony, Schleissheim, and Telhashomer. Adhesion and invasion abilities of the strains were determined in quantitative assays using the gentamicin protection method. Induction of apoptosis was assessed using HeLa cell monolayers. PCR assays were used for detection of 26 virulence genes localised within mobile elements: pathogenicity islands, virulence plasmids, and prophage sequences. In vitro studies revealed that all strains had adhesion and invasion abilities to human epithelial cells. The isolates were cytotoxic and induced apoptosis of the cells. The serovars differed in the number of virulence-associated genes: up to 18 genes were present in Salmonella Schleissheim, 17 in Salmonella Abony, whereas as few as six genes were found in Salmonella Telhashomer. Generally, Salmonella Abony and Salmonella Schleissheim did not differ much in gene content connected with the presence SPI-1 to -5. All of the strains lacked genes localised within bacteriophages and plasmids. The presence of virulence-associated genes and in vitro pathogenicity assays suggest that Salmonella sp. strains originating from autochthonous, free-living lizards can potentially infect and cause disease in humans.

Detection of zoonotic and livestock-specific assemblages of Giardia duodenalis in free-living wild lizards

Giardia duodenalis is a zoonotic parasite that infects the gut of a wide range of vertebrates, including numerous wildlife species. However, little is known about this protozoan parasite in reptiles. Fecal samples from 31 wild lizards were collected in Galicia (northwest Spain) and screened for the presence of Giardia by PCR amplification and sequencing of the ITS1-5.8S-ITS2 region in the ribosomal unit. This allowed detection of the parasite in 5 samples (16.1%), and enabled identification of G. duodenalis assemblage A2 in two samples of Iberian rock lizard (Iberolacerta monticola), G. duodenalis assemblage B in other two samples of I. monticola, and G. duodenalis assemblage E in one sample of Bocage's wall lizard (Podarcis bocagei). The results obtained after PCR amplification and sequencing of the SSU-rDNA gene confirmed the presence of G. duodenalis assemblage A in two samples of I. monticola. This is the first report of G. duodenalis in free-living lizards, although further studies are needed to distinguish between actual infection and mechanical dissemination of cysts. The detection of zoonotic and livestock-specific assemblages of G. duodenalis demonstrates the wide environmental contamination by this parasite, possibly due to human activities.

Spontaneous magnetic alignment behaviour in free-living lizards.

Several species of vertebrates exhibit spontaneous longitudinal body axis alignment relative to the Earth's magnetic field (i.e., magnetic alignment) while they are performing different behavioural tasks. Since magnetoreception is still not fully understood, studying magnetic alignment provides evidence for magnetoreception and broadens current knowledge of magnetic sense in animals. Furthermore, magnetic alignment widens the roles of magnetic sensitivity in animals and may contribute to shed new light on magnetoreception. In this context, spontaneous alignment in two species of lacertid lizards (Podarcis muralis and Podarcis lilfordi) during basking periods was monitored. Alignments in 255 P. muralis and 456 P. lilfordi were measured over a 5-year period. The possible influence of the sun's position (i.e., altitude and azimuth) and geomagnetic field values corresponding to the moment in which a particular lizard was observed on lizards' body axis orientation was evaluated. Both species exhibited a highly significant bimodal orientation along the north-northeast and south-southwest magnetic axis. The evidence from this study suggests that free-living lacertid lizards exhibit magnetic alignment behaviour, since their body alignments cannot be explained by an effect of the sun's position. On the contrary, lizard orientations were significantly correlated with geomagnetic field values at the time of each observation. We suggest that this behaviour might provide lizards with a constant directional reference while they are sun basking. This directional reference might improve their mental map of space to accomplish efficient escape behaviour. This study is the first to provide spontaneous magnetic alignment behaviour in free-living reptiles.

Color pattern facilitates species recognition but not signal detection: a field test using robots

There are many factors that affect signal design, including the need for rapid signal detection and the ability to identify the signal as conspecific. Understanding these different sources of selection on signal design is essential to explain the evolution of both signal complexity and signal diversity. We assessed the relative importance of detection and recognition for signal design in the blackbearded gliding lizard, Draco melanopogon, which uses the extension and retraction of a large, black-and-white dewlap (or throat fan) in territorial communication. We presented free-living lizards with robots displaying dewlaps of different designs that varied in the proportion of the black and white components. We found no effect of dewlap brightness or design on the time it took for a lizard to detect the robot, consistent with the view that initial detection is likely to be primarily elicited by movement rather than specific color or pattern. However, males (but not females) responded with a greater intensity to the dewlap treatment that most resembled the natural dewlap color and design of the species. Furthermore, males were more likely to display to any dewlap color in the presence of a neighbor. These results suggest that dewlap pattern may play an important role in species recognition but has minimal influence on the initial detection of the signal. Importantly, our results also highlight that factors unrelated to discrimination, such as social cues and individual motivational state, may affect responses to species identity cues.

Molecular Detection of Murine Herpesvirus 68 in Ticks Feeding on Free-living Reptiles

The MHV-68 (designed as Murid herpesvirus 4 (MuHV 4) strain 68) isolated from two rodents, Myodes glareolus and Apodemus flavicollis, is considered as a natural pathogen of free-living murid rodents. Recently, the detection of MHV antibodies in the blood of animals living in the same biotope as MHV-infected mice has suggested that ticks may have a role in the transmission of this pathogen. Ixodes ricinus is one the most abundant tick species in Europe known to transmit multiple pathogens causing human and animal diseases. In this study, nymphs and larvae feeding on 116 individuals of a temperate lizard species-the green lizard Lacerta viridis captured in the Slovak Karst National Park, were examined for MHV-68. The specific sequence of virion glycoprotein 150 was amplified in DNA individually isolated from I. ricinus ticks using single-copy sensitive nested polymerase chain reaction. MHV-68 was detected in ten of 649 nymphs and in five of 150 larvae, respectively. We found that 9.6% of green lizards fed at least one MHV-68-infected immature tick. Occurrence of MHV-68 within all ticks tested was 1.8%. This study is first to show that immature I. ricinus ticks feeding on free-living lizards in a Central European region could be infected with gammaherpesvirus (MHV-68), naturally infecting free-living murid rodents. Our results provide evidence supporting the hypothesis that ticks may play a mediating role in circulation of MHV-68 in nature.

ADAPTATION AND PLASTICITY OF ANIMAL COMMUNICATION IN FLUCTUATING ENVIRONMENTS

Adaptations that facilitate the reception of long-range signals under challenging conditions are expected to generate signal diversity when species communicate in different habitats. Although we have a general understanding of how individual communicating animals cope with conditions influencing signal detection, the extent to which plasticity and evolutionary changes in signal characteristics contribute to interspecific differences in signaling behavior is unclear. We quantified the visual displays of free-living lizards and environmental variables known to influence display detection for multiple species from two separate island radiations. We found evidence of both adaptive evolution and adaptive plasticity in display characteristics as a function of environmental conditions, but plasticity accounted for most of the observed differences in display behavior across species. At the same time, prominent differences between the two island radiations existed in aspects of signaling behavior, unrelated to the environment. Past evolutionary events have therefore played an important role in shaping the way lizards adjust their signals to challenges in present-day environments. In addition to showing how plasticity contributes to interspecific differences in communication signals, our findings suggest the vagaries of evolution can in itself lead to signal variation between species.

Photobiosynthetic Opportunity and Ability for UV-B Generated Vitamin D Synthesis in Free-Living House Geckos (Hemidactylus turcicus) and Texas Spiny Lizards (Sceloporus olivaceous)

The opportunity and ability to photobiosynthesize vitamin D3 by exposing skin to ultraviolet-B (UVB) irradiation from the sun was compared using the nocturnal/crepuscular Mediterranean House Gecko Hemidactylus turcicus and the diurnal Texas Spiny Lizard Sceloporus olivaceous. Texas spiny lizards had a greater opportunity for photobiosynthetic production of vitamin D3 than geckos. This was revealed by vitamin D3 photoproduct production in models (ampoules containing an alcohol solution of vitamin D3 precursor) placed at locations inhabited by free-living lizards at similar times of occupancy. Alternatively, geckos seemed able to maximize their limited photobiosynthetic opportunity with a higher rate of conversion of provitamin D3 to photoproducts. This was revealed by photoproduct conversion in patches of lizard skin exposed to ultraviolet lamps in the laboratory. Stomach-content analysis showed the spiny lizards to have dietary sources of vitamin D3, the geckos may or may not. This is the first documentation that mostly nocturnal geckos may rely on photobiosynthesis of vitamin D3 and that they might have a more sensitive mechanism than diurnal lizards to compensate for their limited exposure to natural UVB radiation. Future studies should investigate sexual, seasonal, age, and species differences in photobiosynthetic opportunity and ability.

Effects of testosterone on locomotor performance and growth in field-active northern fence lizards, Sceloporus undulatus hyacinthinus.

The role of steroids in locomotor performance and growth was examined in free-living lizards. Male northern fence lizards (Sceloporus undulatus hyacinthinus) with experimentally elevated plasma testosterone concentrations had greater sprint speed (+24%) and burst stamina (+17%) than sham-implanted males after 14-23 d in the field. This enhanced performance was associated with significant energetic costs, as the testosterone-implanted lizards had reduced growth rates, and, in a companion experiment, field-active testosterone-implanted lizards had smaller fat-body masses than controls after just 3-4 wk. These results suggest that, in addition to influencing a variety of behavioral and morphological traits, testosterone may play an important role in the regulation of locomotor performance. Also, natural levels of locomotor performance may be constrained, in part, by associated costs of elevated plasma testosterone concentrations.

External and internal influences on indices of physiological stress: II. Seasonal and size‐related variations in blood composition in free‐living lizards, Sceloporus occidentalis

Seasonal changes in blood composition (plasma osmolality, total plasma protein, hematocrit) in two free-living populations of fence lizards, Sceloporus occidentalis, one living in a very arid environment (Pearblossom, CA) and another in a milder desert (Bend, OR), were analyzed. In this analysis, two features of reptilian physiology and ecology were incorporated: ontogenetic variation in blood composition and seasonal variation in body-size distribution. The population living in the arid environment, but not the mild environment, exhibited significant seasonal changes in blood composition: mean plasma osmolality increased (345 +/- 4 to 356 +/- 3 mOsmol/kg) and mean plasma protein (4.19 +/- 0.20 to 3.34 +/- 0.14 g/dl) and hematocrit decreased (43.8 +/- 0.3 to 31.6 +/- 0.4) from April to August. These changes suggested that the physiological condition of the California population was affected by seasonal changes in the external environment. However, among individuals, a significant portion of the variation in blood composition was associated with an internal factor, body size. Larger lizards had higher osmolality, total protein, and hematocrit than smaller lizards in all seasons. In addition, the mean body size of active lizards decreased from April to August in California, but not Oregon. Because the body-size distribution of active lizards in California shifted between seasons, changes in mean population values of these blood parameters probably do not accurately reflect changes that occur within individuals and therefore may be misleading in assessing the physiological consequences of drought.

Effects of Nymphal Ticks and Their Interaction with Malaria on the Physiology of Male Fence Lizards

Ectoparasites infest many lizard species, but the physiological consequences of infestation in free-living lizards have not been studied. We examined male western fence lizards, Sceloporus occidentalis, infested with ticks, Ixodes pacificus, in northern California. Many lizards in this population were also infected with malaria, Plasmodium mexicanum. We found that the effects of nymphal ticks on blood composition and body condition (relative body weight) depended on the age of the lizard host and whether the lizard was also infected with malaria. Adult male lizards, but not juveniles, infested with ticks had lower hematocrits than uninfested lizards. Although the reduction in hematocrit that accompanies the mean level of tick infestation probably does not substantially affect the lizards, heavy infestations (>5 ticks per lizard) may significantly limit the aerobic capacity and behavior of the lizard host. Lizards parasitized with both ticks and malaria had significantly lower body condition than lizards with one or neither parasite.

Variation in the effect of profitability on prey size selection by the lacertid lizard Psammodromus algirus

Maximizing the average rate of energy intake (profitability) may not always be the optimal foraging strategy for ectotherms with relatively low energy requirements. To test this hypothesis, we studied the feeding behaviour of captive insectivorous lizards Psammodromus algirus, and we obtained experimental estimates of prey mass, handling time, profitability, and attack distance for several types of prey. Handling time increased linearly with prey mass and differed significantly among prey types when prey size differences were controlled for, and mean profitabilities differed among prey taxa, but profitability was independent of prey size. The attack distance increased with prey length and with the mobility of prey, but it was unrelated to profitability. Thus, lizards did not seem to take account of the rate of energy intake per second as a proximate cue eliciting predatory behavior. This information was combined with pitfall-trap censuses of prey (in late April, mid-June and late July) that allowed us to compare the mass of the prey captured in the environment with that of the arthropods found in the stomachs of sacrificed free-living lizards. In April, when food abundance was low and lizards were reproducing, profitability had a pronounced effect on size selection and lizards selected prey larger than average from all taxa except the least profitable ones. As the active season progressed, and with a higher availability of food, the number of prey per stomach decreased and their mean ize increased. The effect of profitability on size selection decreased (June) and eventually vanished (July-August). This variation is probably related to seasonal changes in the ecology of lizards, e.g. time minimization in the breeding season as a means of saving time for nonforaging activities versus movement minimization by selecting fewer (but larger) prey in the postbreeding season. Thus, the hypothesis that maximizing profitability could be just an optional strategy for a terrestrial ectothermic vertebrate was supported by our data.

Tail injuries increase the risk of mortality in free-living lizards (Uta stansburiana).

Caudal autotomy is an effective anti-predator mechanism used by many lizard species. Fitness benefits of surviving a predatory attack are obvious, although lizards that autotomize their tails may be at greater risk during subsequent encounters with predators than lizards with complete tails. In previous laboratory studies, tail-less lizards were more vulnerable to capture by predators, but little is known about the relative survival of tailed versus tail-less lizards in nature. This study reports on significant associations between naturally incurred tail injuries and the subsequent risk of mortality in 7 populations of the lizard Uta stansburiana. I used standard mark-recapture techniques to document survival and quantified tail injuries by estimating tail completeness. I then used sampled randomization tests to compare intitial tail completeness values of surviving versus non-surviving lizards. I evaluated overall patterns by comparising the means of tail completeness values of survivors versus non-survivors among mark-recapture sequences. Lizards with incomplete tails suffered higher mortality in the field, although this was not true for every comparison considered (i.e., for every mark-recapture sequence analyzed), and the overall trend was much stronger for adult males than for either adult females or juveniles. Higher mortality among lizards with incomplete tails is presumably a consequence of increased vulnerability to capture by predators. Vulnerability to predation of tail-injured lizards may be confounded by reduced social status in this species, because social subordination can result in the occupation of an inferior home range.

Effects of different loads on the nasal gland secretion of the lizard Uromastix acanthinurus (agamidae) and relations with its function

1. 1. Uromastix acanthinurus exhibits experimentally a large variability in the cation and anion ratio of the nasal salt secretion. But recently collected lizards clearly secreted far more K + than Na + via the nasal gland, even after NaCl loading. 2. 2. The K +/Na + ratio decreased only after two repetitive NaCl injections but insufficient Na + was eliminated. Two separate KCl injections were successfully eliminated but daily natural average K + administration induced progressive hyperkalemia. 3. 3. These experimental data agreed with previous observations showing variations of plasma Na + and K + concentrations in free-living lizards. 4. 4. The nasal gland constitues the main route of Cl − excretion but the Cl/(Na + K) ratio may vary according to observations in other herbivorous species. 5. 5. Finally, increased concentrations of alkali metals seemed effective stimulants for nasal salt secretion whereas pure osmotic loads did not.