The effect of body size on the thermoregulation of lizards on hot,dry Mediterranean islands

Body size shapes the overall biology of organisms. We assessed the impact of size on temperature regulation in populations of normal-sized and large-bodied insular Mediterranean lizards (Podarcis gaigeae, Lacertidae). We hypothesized that large lizards would achieve higher body temperatures and thermoregulate more effectively than their smaller kin. Large- and small-bodied lizards share the same thermoregulation pattern, achieving similar body temperatures in the field. Large lizards, however, prefer higher set-point temperatures. Lizards in both populations thermoregulate effectively, but large lizards thermoregulated less effectively than normal-sized lizards. The particular conditions at the islet that harbors the large-bodied population (harsh intraspecific competition) seem to account for this pattern.     

Hunt or hide: How insularity and urbanization affect foraging decisions in lizards

Foraging decisions should reflect a balance between costs and benefits of alternative strategies. Predation risk and resource availability in the environment may be crucial in deciding how cautious individuals should behave during foraging. These costs and benefits will vary in time and context, meaning that animals should be able to adjust their foraging behaviour to new or altered environments. Studying how animals do this is essential to understand their survival in these environments. In this study, we investigated the effect of both insularity and urbanization on risk‐taking and neophobia during foraging in the Dalmatian wall lizard (Podarcis melisellensis). Small islets tend to have both a lower number of predators and less resources. Therefore, islet populations were expected to show more risk‐taking behaviour and less neophobia in a foraging context. Previous studies on behaviour of urban lizards have yielded inconsistent results, but due to a lack of both predators and arthropod prey in urban habitats, we expected urban lizards to also take more risks and behave less neophobic. We sampled several inhabited and uninhabited locations on Vis (Croatia) and surrounding islets. Risk‐taking behaviour was tested by measuring the latency of lizards to feed in the presence of a predator model, and neophobia by measuring the latency to feed in the presence of a novel object. We found that islet lizards do indeed take more risks and were less vigilant, but not less neophobic. Urban and rural lizards did not differ in any of these behaviours, which is in sharp contrast with previous work on mammals and birds. The behavioural differences between islet and island lizards were novel, but not unexpected findings and are in line with the theory of “island tameness”. The effect of urbanization on the behaviour of animals seems to be more complex and might vary among taxa.     

Population divergence in chemical signals and the potential for premating isolation between islet- and mainland populations of the Skyros wall lizard (Podarcis gaigeae)

When sexually selected traits diverge because of different local selective environments, premating isolation might arise as a correlated response. However, sexually selected traits might also diverge by stochastic forces. Here, we show that odour-based mate preferences and scent composition have diverged between islet- and mainland populations of Skyros wall lizard, Podarcis gaigeae. We quantified the degree of scent-mediated premating isolation between populations. Islet lizards preferred scent from islet lizards, whereas the mainland populations were less discriminatory. The pheromone compositions differed more between islets than between islet- and mainland populations and did not differ significantly between mainland populations. There was a tendency for population divergence in pheromones to be positively correlated with neutral genetic divergence. This might indicate a role for genetic drift in evolutionary change in these signals and partial decoupling between signals and preferences. Our results suggest that chemical signals and associated mate preferences can diverge through stochastic and selective forces and influence premating isolation.     

Resting metabolic expenditure as a potential source of variation in growth rates of the sagebrush lizard

Along an elevational gradient on SW Utah, sagebrush lizards (Sceloporus graciosus) exhibit an unexpected pattern of growth. Lizards from a high elevation population grow faster than lizards from two populations at lower elevations despite shorter daily and seasonal activity. Results from a common environment study of growth suggest that the differences in growth are not due to adaptation to local environmental conditions. In this study, I test the hypothesis that higher growth rates in lizards from high elevation may be attributable to reduced resting metabolic expenditure compared to that of lizards from populations at two lower elevations. Resting metabolic rates were measured for individuals from each of the study populations across different times of day and over a broad range of temperatures. Under the same laboratory conditions, field-caught lizards from the high elevation population exhibited lower metabolic rates when compared to lizards from lower elevations. Daily resting metabolic expenditures were calculated using the observed metabolic rates coupled with estimates of daily activity. Daily resting metabolic expenditure was 50% greater for individuals from the two lower elevation populations, which could result in 12.5% more energy that could be potentially allocated to growth for lizards from high elevation. Such energetic savings may be able to explain differences in the patterns of growth observed in nature.     

Does relaxed predation drive phenotypic divergence among insular populations?

The evolution of striking phenotypes on islands is a well‐known phenomenon, and there has been a long‐standing debate on the patterns of body size evolution on islands. The ecological causes driving divergence in insular populations are, however, poorly understood. Reduced predator fauna is expected to lower escape propensity, increase body size and relax selection for crypsis in small‐bodied, insular prey species. Here, we investigated whether escape behaviour, body size and dorsal coloration have diverged as predicted under predation release in spatially replicated islet and mainland populations of the lizard species Podarcis gaigeae. We show that islet lizards escape approaching observers at shorter distances and are larger than mainland lizards. Additionally, we found evidence for larger between‐population variation in body size among the islet populations than mainland populations. Moreover, islet populations are significantly more divergent in dorsal coloration and match their respective habitats poorer than mainland lizards. These results strongly suggest that predation release on islets has driven population divergence in phenotypic and behavioural traits and that selective release has affected both trait means and variances. Relaxed predation pressure is therefore likely to be one of the major ecological factors driving body size divergence on these islands.     

Impact of the experimental removal of lizards on Lyme disease risk

The distribution of vector meals in the host community is an important element of understanding and predicting vector-borne disease risk. Lizards (such as the western fence lizard; Sceloporus occidentalis) play a unique role in Lyme disease ecology in the far-western United States. Lizards rather than mammals serve as the blood meal hosts for a large fraction of larval and nymphal western black-legged ticks (Ixodes pacificus--the vector for Lyme disease in that region) but are not competent reservoirs for the pathogen, Borrelia burgdorferi. Prior studies have suggested that the net effect of lizards is to reduce risk of human exposure to Lyme disease, a hypothesis that we tested experimentally. Following experimental removal of lizards, we documented incomplete host switching by larval ticks (5.19%) from lizards to other hosts. Larval tick burdens increased on woodrats, a competent reservoir, but not on deer mice, a less competent pathogen reservoir. However, most larvae failed to find an alternate host. This resulted in significantly lower densities of nymphal ticks the following year. Unexpectedly, the removal of reservoir-incompetent lizards did not cause an increase in nymphal tick infection prevalence. The net result of lizard removal was a decrease in the density of infected nymphal ticks, and therefore a decreased risk to humans of Lyme disease. Our results indicate that an incompetent reservoir for a pathogen may, in fact, increase disease risk through the maintenance of higher vector density and therefore, higher density of infected vectors.     

Influence of predation pressure on the escape behaviour of Podarcis muralis lizards

Relationships between predator avoidance behaviour and predation pressure were investigated in the wall lizard, Podarcis muralis. The wariness of lizards belonging to high (1185m) and low elevation (308m) populations under two different predation pressure levels was compared. Wall lizards belonging to the lowland population experienced greater predation pressure than those belonging to the highland population. Lizards belonging to the population under higher predation pressure had higher frequency of refuge use, and had longer flight initiation distances (i.e. the distance lizards allowed the observer to approach before fleeing). In contrast, neither the distance fled (i.e. the total distance they fled in one continuous movement from the lizard's initial position until hiding or stopping at a safe distance) nor the distance to the nearest refuge were significantly different between populations. Escape responses were independent of ambient temperature in the lowland population, but animals belonging to the highland population had longer flight initiation distances when the ambient temperatures were higher. These findings suggest that predator avoidance behaviour may vary with predation pressure.     

Filling the Ark: Animal Welfare in Disasters

ABSTRACT

Populations of feral domestic cats and free-roaming, owned cats have increased throughout the United States, affecting wildlife and public health and warranting attention from a variety of management agencies. The contentious issue of feral cat management requires a greater understanding of public attitudes towards cats and preferences. We used an anonymous internet survey of randomly selected Athens-Clarke County, Georgia households to identify general public perceptions of domestic cats and preferences for cat management. We examined factors that may influence attitudes towards cats, and management including: knowledge about cats, experiences with cats and demographic variables. Results indicate that more residents have positive experiences with feral cats than negative, cat owners have greater knowledge of cats than non-cat owners, and animal welfare or conservation organization membership has a significant effect on attitudes towards cats. A majority of survey respondents agreed that more effective feral cat management is needed yet did not approve of trap-neuter-release (TNR) legislation recently passed in Athens-Clarke County. Logistic regression revealed that residents' attitudes were found to be more important than experiences or knowledge in supporting cat management legislation. Cat sanctuaries were found to be the most acceptable option to reduce feral cat populations (56%), followed by TNR (49%) and capturing and euthanizing cats (44%).     

Family and population effects on disease resistance in a reptile

Despite its importance in evolutionary biology, studies of the pattern of disease resistance in natural populations are rare. In this paper, we report patterns of infection of a viral eye disease in juvenile Swedish common lizards (Lacerta vivipara). Females were sampled at random from natural populations immediately prior to parturition with equal exposure of pathogens for all lizards once in captivity. No causative agents could be found that linked risk of disease to maternal/interfollicular transfer of pathogens. The results show that a major factor influencing offspring susceptibility is family identity, suggesting heritable variation in pathogen resistance. Our interpopulation comparison provides additional support for a link between genetics and disease resistance. Lizards in northern Sweden were not only more susceptible to the disease but were also more health compromised once infected, with relatively more reduced growth rate and increased mortality than lizards from the south. This scenario suggests that southern lizards have been under selection for resistance to this pathogen, whereas northern lizards have not, or at least not to the same degree. Thus, this study confirms the importance of genetic (family) effects on pathogen resistance with variation in this trait among natural populations.     

Food chemical cues elicit general and population-specific effects on lingual and biting behaviors in the lacertid lizard Podarcis lilfordi

Actively foraging lizards are capable of identifying prey using only chemical cues sampled by tongue-flicking, and the relatively few omnivorous and herbivorous lizards tested similarly can identify both animal and plant foods from chemical cues. Whether lizards that eat plants respond to cues specific to preferred plant types and whether there is geographic variability in responses to cues from various plants correlated with the importance of those plants in local diets is unknown. In three populations of an omnivorous lacertid, the Balearic lizard Podarcis lilfordi, we studied chemosensory sampling and feeding responses to chemical cues from plant and animal foods presented on cotton swabs. Each lizard population is endemic to one islet off the coast of Menorca, Balearic Islands, Spain. Lizards in all three populations discriminated chemical cues from plant and animal foods from control substances. Our results extend findings of prey chemical discrimination and plant chemical discrimination in omnivores, increasing confidence that correlated evolution has occurred between plant diet and chemosensory response to palatable plants. There were no consistent differences among populations in tongue-flicking and biting responses to stimuli from flowers of syntopic and allopatric plant species. The lizards may respond to cues indicative of palatability in a wide range of plant species rather than exhibiting strong responses only to locally available plant species. Nevertheless, tongue-flicking and biting frequencies varied among plant species, perhaps indicating food preferences. In addition, there were differences among populations in tongue-flick rates, latency to bite, and licking behavior. Licking was observed in only one lizard population as a response to floral chemicals from only one of the plants species tested, raising the possibility of a population-specific linkage between identification of a particular plant species and performance of an appropriate feeding response.     

Prevalence and abundance of Ixodes pacificus immatures (Acari: Ixodidae) infesting western fence lizards (Sceloporus occidentalis) in northern California: temporal trends and environmental correlates.

The prevalence and abundance of immature Ixodes pacificus ticks on western fence lizards (Sceloporus occidentalis) were examined in relation to time of year, host attributes (i.e., age, gender, and presence or absence of blood parasites), and 5 environmental characteristics, including topographic exposure and ground cover substrate, over a 2-year period in northern California. Lizards were infested with subadult ticks from early March until late July or early August, with peak median numbers of larvae and nymphs recorded in late April and early May of both years. Peak larval and nymphal abundances differed between years. The overall ratio of larvae to nymphs on adult male lizards was low, ranging from 0.80 in 1999 to 2.41 in 2000. Such intensive feeding of nymphs versus larvae on these lizards, which are reservoir-incompetent for Borrelia burgdorferi spirochetes, may explain previous observations of decreasing spirochetal infection prevalence from the nymphal to adult stage in northwestern California. Adult male lizards were more likely to be infested with nymphs and harbored greater abundances of larvae and nymphs than adult females. Lizards uninfected with blood parasites had more nymphs than infected lizards. The measured environmental characteristics could explain only a small percentage of the total variation observed in larval prevalence (22%) and in larval and nymphal abundance (12 and 3%, respectively).     

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

Island 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.     

Optimal escape theory predicts escape behaviors beyond flight initiation distance： risk assessment and escape by striped plateau lizards Sceloporus virgatus

Escape theory predicts that flight initiation distance (FID=distance between predator and prey when escape begins) is longer when risk is greater and shorter when escape is more costly. A few tests suggest that escape theory applies to distance fled. Escape models have not addressed stochastic variables, such as probability of fleeing and of entering refuge, but their economic logic might be applicable. Experiments on several risk factors in the lizard Sceloporus virgatus confirmed all predictions for the above escape variables. FID was greater when approach was faster and more direct, for lizards on ground than on trees, for lizards rarely exposed to humans, for the second of two approaches, and when the predator turned toward lizards rather than away. Lizards fled further during rapid and second consecutive approaches. They were more likely to flee when approached directly, when a predator turned toward them, and during second approaches. They were more likely to enter refuge when approached rapidly. A novel finding is that perch height in trees was unrelated to FID because lizards escaped by moving out of sight, then moving up or down unpredictably. These findings add to a growing body of evidence supporting predictions of escape theory for FID and distance fled. They show that two probabilistic aspects of escape are predictable based on relative predation risk levels. Because individuals differ in boldness, the assessed optimal FID and threshold risks for fleeing and entering refuge are exceeded for an increasing proportion of individuals as risk increases[Current Zoology 55(2):123-131,2009].     

Lizards reduce food consumption by spiders: mechanisms and consequences

Summary To determine the effect of lizards on webspider populations, we conducted a long-term field experiment in the Bahamas. Numbers of spider individuals were about 3 times higher in lizard-removal enclosures than in control enclosures with natural densities of lizards. Dietary analyses showed that lizards ate spiders and that lizard and spider diets overlapped substantially. Lizards reduced biomass of prey consumed by spiders; details indicated that they reduced biomass of large (> 4 mm) prey consumed by spiders more than biomass of small (4 mm) prey. Similarly, lizards reduced biomass of large aerial arthropods caught in sticky traps but not biomass of small aerial arthropods. We found no evidence that the lizard effect on prey consumption by spiders was caused by a spatial shift from areas with high aerial arthropod abundance to areas with low aerial arthropod abundance. Lizards reduced adult female cephalothorax width and fecundity of spiders. In a separate experiment, food-supplemented spiders were more fecund than control spiders. This study indicates that the interaction between lizards and spiders includes both predation and competition for food.     

The impact of tick load on the fitness of their lizard hosts

A survey was conducted of natural populations of the sleepy lizard Tiliqua rugosa in South Australia to determine whether infestation by ectoparasitic ticks reduced their fitness. Between 1982 and 1990, 2183 captures of 824 individual lizards were made in an area where they were infested by the tick Aponomma hydrosauri, and 3668 captures of 586 individual lizards were made in an area where they were infested with the tick Amblyomma limbatum. Lizards with high tick loads in one year tended to have high loads the next year. Longevity of lizards in the study was either not correlated with tick load, or positively correlated. Size achieved was greater amongst lizards with greatest tick load, and lizards in mating pairs had higher tick loads than those never found in pairs. The data do not support the hypothesis that tick load diminishes host fitness.     

Regulation of gut function varies with life-history traits in chuckwallas (Sauromalus obesus: Iguanidae)

We examined the effects of hibernation and fasting on intestinal glucose and proline uptake rates of chuckwallas (Sauromalus obesus) and on the size of organs directly or indirectly related to digestion. These lizards show geographic variation in body size and growth rate that parallels an elevational gradient in our study area. At low elevation, food is available only for a short time during the spring; at high elevation, food may also be available during summer and autumn, depending on rainfall conditions in a given year. We hypothesized that low-elevation lizards with a short season of food availability would show more pronounced regulation of gut size and function than high-elevation lizards with prolonged or bimodal food availability. Hibernating lizards from both elevations had significantly lower uptake rates per milligram intestine for both nutrients, and lower small intestine mass, than active lizards. The combination of these two effects resulted in significantly lower total nutrient uptake in hibernating animals compared to active ones. The stomach, large intestine, and cecum showed lower masses in hibernators, but these results were not statistically significant. The heart, kidney, and liver showed no difference in mass between hibernating and nonhibernating animals. Lizards from low elevations with a short growing season also showed a greater increase in both uptake rates and small intestine mass from the hibernating to the active state, compared to those from high elevations with longer growing seasons. Thus, compared to those from long growing season areas, lizards from short growing season areas have equal uptake capacity during hibernation but much higher uptake capacity while active and feeding. This pattern of regulation of gut function may or may not be an adaptive response, but it is consistent with variation in life-history characteristics among populations. In areas with a short season, those lizards that can extract nutrients quickly and then reduce the gut will be favored; in areas where food may be available later in the year, those lizards that maintain an active gut would be favored. While other researchers have found much greater magnitudes of gut regulation when making comparisons among species, we find the different patterns of change in gut function between different populations of chuckwallas particularly intriguing because they occur within a single species.     

The effects of prey species on food conversion efficiency and growth of an insectivorous lizard

Little is known about the effects of different prey species on lizard growth. We conducted a 6‐week study to determine the relative effects of prey species on growth parameters of hatchling western fence lizards, Sceloporus occidentalis. Lizards were fed house cricket nymphs, Acheta domesticus, or mealworm larvae, Tenebrio molitor. The effects of prey species on growth were determined by measuring prey consumption, gross conversion efficiency of food [gain in mass (g)/food consumed (g)], gain in mass, and gain in snout–vent length. Lizards grew well on both the prey species. However, lizards that fed on crickets consumed a significantly higher percentage of their body mass per day than those fed mealworms. Nevertheless, lizards that consumed mealworms ingested significantly more metabolizable energy, had significantly higher food conversion efficiencies, significantly higher daily gains in mass, and significantly greater total growth in mass than lizards that fed on crickets. Zoo Biol 27:181–187, 2008. © 2008 Wiley‐Liss, Inc.     

Devil Declines and Catastrophic Cascades: Is Mesopredator Release of Feral Cats Inhibiting Recovery of the Eastern Quoll?

The eastern quoll (Dasyurus viverrinus) is a medium-sized Australian marsupial carnivore that has recently undergone a rapid and severe population decline over the 10 years to 2009, with no sign of recovery. This decline has been linked to a period of unfavourable weather, but subsequent improved weather conditions have not been matched by quoll recovery. A recent study suggested another mechanism: that declines in Tasmanian devil (Sarcophilus harrisii) populations, due to the spread of the fatal Devil Facial Tumour Disease, have released feral cats (Felis catus) from competitive suppression, with eastern quoll declines linked to a subsequent increase in cat sightings. Yet current evidence of intraguild suppression among devils, cats and quolls is scant and equivocal. We therefore assessed the influences of top-down effects on abundance and activity patterns among devils, feral cats and eastern quolls. Between 2011 and 2013, we monitored four carnivore populations using longitudinal trapping and camera surveys, and performed camera surveys at 12 additional sites throughout the eastern quoll’s range. We did not find evidence of a negative relationship between devil and cat abundance, nor of higher cat abundance in areas where devil populations had declined the longest. Cats did not appear to avoid devils spatially; however, there was evidence of temporal separation of cat and devil activity, with reduced separation and increasing nocturnal activity observed in areas where devils had declined the longest. Cats and quolls used the same areas, and there was no evidence that cat and quoll abundances were negatively related. Temporal overlap in observed cat and quoll activity was higher in summer than in winter, but this seasonal difference was unrelated to devil declines. We suggest that cats did not cause the recent quoll decline, but that predation of juvenile quolls by cats could be inhibiting low density quoll populations from recovering their former abundance through a ‘predator pit’ effect following weather-induced decline. Predation intensity could increase further should cats become increasingly nocturnal in response to devil declines.     

Effects of hypoxia on the thermal physiology of a high-elevation lizard: implications for upslope-shifting species

Montane reptiles are predicted to move to higher elevations in response to climate warming. However, whether upwards-shifting reptiles will be physiologically constrained by hypoxia at higher elevations remains unknown. We investigated the effects of hypoxic conditions on preferred body temperatures (T_pref) and thermal tolerance capacity of a montane lizard (Phrynocephalus vlangalii) from two populations on the Qinghai–Tibet Plateau. Lizards from 2600 m a.s.l. were exposed to O₂ levels mimicking those at 2600 m (control) and 3600 m (hypoxia treatment). Lizards from 3600 m a.s.l. were exposed to O₂ levels mimicking those at 3600 m (control) and 4600 m (hypoxia treatment). The T_pref did not differ between the control and hypoxia treatments in lizards from 2600 m. However, lizards from 3600 m selected lower body temperatures when exposed to the hypoxia treatment mimicking the O₂ level at 4600 m. Additionally, the hypoxia treatment induced lower critical thermal minimum (CT_min) in lizards from both populations, but did not affect the critical thermal maximum (CT_max) in either population. Our results imply that upwards-shifting reptiles may be constrained by hypoxia if a decrease in T_pref reduces thermally dependent fitness traits, despite no observed effect on their heat tolerance.     

Geographic variation in the effects of heat exposure on maximum sprint speed and Hsp70 expression in the western fence lizard Sceloporus occidentalis

We examined whether western fence lizards Sceloporus occidentalis occurring in thermally divergent environments display differential responses to high temperature in locomotor performance and heat-shock protein (Hsp) expression. We measured maximum sprint speed in S. occidentalis from four populations at paired latitudes and elevations before and after exposure to an experimental heat treatment and then quantified hind-limb muscle Hsp70 expression. Lizards collected from northern or high-elevation collection sites suffered a greater reduction in sprint speed after heat exposure than lizards collected from southern or low-elevation sites. In addition, lizards from northern collection sites also exhibited an increase in Hsp70 expression after heat exposure, whereas there was no effect of heat exposure on Hsp70 expression in lizards from southern collection sites. Across all groups, there was a negative relationship between Hsp70 expression and sprint speed after thermal stress. This result is significant because (a) it suggests that an increase in Hsp70 alone cannot compensate for the immediate negative effects of high-temperature exposure on sprint speed and (b) it demonstrates a novel correlation between an emergent property at the intersection of several physiological systems (locomotion) and a cellular response (Hsp70 expression). Ultimately, geographic variation in the effects of heat on sprint speed may translate into differential fitness and population viability during future increases in global air temperatures.