Are viviparous lizards from cool climates ever exclusively nocturnal? Evidence for extensive basking in a New Zealand gecko

Viviparity has evolved numerous times among squamate reptiles; however, the combination of viviparity and nocturnality is apparently rare among lizards. We used time‐lapse photography to examine evidence for diurnal activity in a viviparous lizard often described as nocturnal, the gecko Woodworthia ‘Otago/Southland’ from southern New Zealand (family Diplodactylidae). Evidence for diurnal emergence was extensive. Females have a higher incidence of basking compared to males, although no difference was detected between females in different reproductive conditions. Temperature loggers inserted into calibrated copper models were used to compare the body temperatures available to geckos in two basking positions and in two retreat types. Models in basking positions reached higher mean temperatures than models in retreats, although there was no significant effect of basking position or retreat type on model temperatures. Collectively, our results indicate that pregnant geckos that bask consistently could reduce gestation length by at least 14 days compared with females that remain in retreats. Extensive basking in this species adds to the growing evidence of diurno‐nocturnality in many New Zealand lepidosaurs, including other viviparous geckos. Our results lead us to question whether viviparity in lizards is ever compatible with ‘pure’ nocturnality in a cool climate. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, ●● , ●●–●●.     

Observations and comments on the body temperatures of some New Zealand reptiles

Abstract

Rectal body temperatures (BTs) of tuataras (Sphenodon punctatus) and of endemic, ovoviviparous gekkonid lizards—mainly Hoplodactylus maculatus (=H. pacificus) and Heteropholis manukanus—were taken together with ambient temperatures during early summer 1970 in areas of central New Zealand. The results, combined with earlier data, enable a number of conclusions to be drawn. (a) The preferred body temperature of heliotherm reptiles is best deduced from the mode of rectal BTS taken in the field, but that of non-heliotherms, when unimodal, from the median or mean. (b) Among Gekkonoidea, specific thermal relations are highly variable in several ways. (c) Sphenodon foraged on cool nights at BTs of 10.5–12.5°c, yet basked in the forest by day at BTs up to 24°c; in pasture it apparently basks within the burrow entrance. (d) Similarly, H. maculatus foraged at night at BTs of 10–13°c, but by day thermoregulated at BTs up to 33°c by ‘indirect basking’ (under thin cover) or ‘protected basking’ (in crevices penetrated by solar radiation). The average BT of females was 2°c higher than that of males, presumably because many females were gravid. (e) H. manukanus is (tertiarily) diurnal, and thermoregulated by basking up to a BT of 31 °c. Towards evening it apparently cooled down voluntarily. (f) Whereas a high daytime BT probably assists digestion in nocturnal foragers, a voluntary low night-time BT in diurnal reptiles may help to conserve energy.     

Predation by an exotic lizard,Anolis sagrei,alters the ant community structure in betelnut palm plantations in southern Taiwan

Abstract 1. Predators can affect prey directly by reducing prey abundance and indirectly by altering behavioural patterns of prey. From previous studies, there is little evidence that ant community structure is affected by vertebrate predation. 2. Researchers tend to consider the interactions between vertebrate predators and ants to be weak. The present study examined the impact of the exotic invasive lizard, Anolis sagrei, on the ant community structure by manipulating the density of lizards within enclosures. The natural density of A. sagrei in the field was surveyed and used as the stocking density rate in the lizard‐present sub‐enclosures. 3. Before the lizard density was manipulated, there was no difference in the ant diversity between sub‐enclosures. After the lizard density manipulation, the ant diversity in sub‐enclosures with A. sagrei present was significantly different from that of enclosures where the lizards were absent, although the overall ant abundance did not differ significantly. 4. The ant diversity difference was generated by a significant reduction of the ant species Pheidole fervens in sub‐enclosures with A. sagrei present. Such an abundance change might be the result of direct predation by the lizards, or it might be generated by a foraging site shift by this ant. 5. The results of this study thus demonstrated that the invasion of an exotic vertebrate can significantly alter the community structure of ants, perhaps through the combined direct and indirect effects of lizards on ants.     

Highly‐enhanced larval growth during the cold season mediated by the basking behavior of the butterfly Parnassius citrinarius (Lepidoptera: Papilionidae)

Some insect species are thought to grow quickly, even in low temperatures under natural conditions, presumably by conducting basking behaviors to use sunlight. However, whether basking behavior in fact enhances developmental speed and shortens the larval period in the field has not been determined. Moreover, few studies have examined whether basking is behavioral thermoregulation or simply the result of highly‐heterogeneous heat environments in the field. To examine these issues, we conducted field observations and laboratory experiments using larvae of Parnassius citrinarius Motschulsky, which mature within a short period after the thaw in early spring. First, body temperatures of larvae were measured under sunny and cloudy conditions. Second, larval preference for warmer locations was examined. Finally, we compared the developmental speed of larvae when they basked under field conditions and when did not bask in laboratory conditions under different air temperature regimes. Under sunny conditions, larval body temperature was substantially higher than either the temperature of the host plant or the air temperature, and was equivalent to the temperature of dead leaves, which the larvae used as basking sites. In contrast, no such tendency was observed under cloudy conditions. Larvae exhibited an exclusive preference for warmer locations. Moreover, in the field, despite the low ambient temperature, larvae grew much faster than those reared in the laboratory. These results imply that the basking behavior of P. citrinarius larvae is active thermoregulation to maintain high body temperatures in the cold season.     

Post-feeding thermophily in lizards (Lialis burtonis Gray,Pygopodidae): Laboratory studies can provide misleading results

Many ectothermic vertebrates raise their preferred body temperature after feeding, likely expediting digestion. However, most studies documenting this phenomenon have relied upon laboratory thermal gradients, which grossly oversimplify an animal's environment. We explored the validity of thermal gradient methodology by investigating post-prandial thermophily in an Australian pygopodid lizard (Lialis burtonis Gray). Mean body temperatures did not differ between fed and unfed lizards in field enclosures. Feeding influenced body temperature in a thermal gradient, but in opposite directions depending on details of the methodology. When we introduced L. burtonis into the gradient at the warmer end, fed lizards had higher body temperatures than unfed conspecifics. However, the opposite was true when lizards were introduced at the cooler end. These contrasting results indicate that lizards with food in their stomachs did not seek out higher temperatures, but instead were more sedentary than unfed lizards. Our study highlights the need for caution in interpreting thermal gradient results unaccompanied by field data, and it demonstrates how minor changes in equipment design or procedures can significantly alter conclusions from laboratory studies.     

Thermal biology,microhabitat selection,and conservation of the insular lizard Podarcis hispanica atrata

Summary We studied aspects of the thermal biology and microhabitat selection of the endangered lizard Podarcis hispanica atrata during autumn in the field and laboratory. Body temperatures (T _b ) of active lizards were within a narrow range, were largely independent of ambient temperatures, and exhibited little diel variation. Activity T _b s largely coincided with the selected temperatures maintained in a laboratory thermogradient and with T _b s that maximize running performance. Alternation of basking with other activities and shuttling between sun and shade were obvious aspects of thermoregulatory behaviour. Lizards shifted microhabitat use throughout the day. During early morning and late afternoon, basking lizards were restricted to rocky sites surrounded by shrubs. Near midday lizards used a wider array of microhabitats, and many moved in open grassy sites. Juveniles maintained lower activity T _b s, had lower selected temperatures, and basked less frequently than the adults. Juveniles occupied open grassy patches more often than the adults. We discuss the relevance of our results for the conservation of this extremely rare lizard and the management of its habitats.     

Thermal sensitivity of sprint-running in the lizard Sceloporus undulatus: support for a conservative view of thermal physiology

Summary The thermal sensitivity of sprint-running ability was investigated in two populations of Sceloporus undulatus that occupy thermally distinct habitats. Integration of field and laboratory data indicates that lizards inhabiting a cool, high-elevation habitat are frequently active at body temperatures that retard sprint-running velocity, which could affect adversely their ability to evade predators and to capture prey. These negative effects might be expected to select for local adaptation of thermal physiology. No differences in thermal physiology (optimal temperature for sprinting, critical thermal limits) were found, however, between lizards from the two habitats.Preferred body temperature of Sceloporus undulatus is lower than the body temperature that maximizes sprint velocity but is still well within an optimal performance range where lizards can run at better than 95% of maximum velocity. Analysis of data from other studies shows a similar concordance of preferred body temperature and temperatures that maximize sprint velocity for some, but not all lizard species studied.Low diversity of predators and high levels of food may compensate in part for the reduced sprinting ability of highelevation lizards active at low body temperatures. The lack of population differentiation supports the view that lizard thermal physiology is evolutionarily conservative.     

Total lactate dehydrogenase activity of tail muscle is not cold-adapted in nocturnal lizards from cool-temperate habitats

The dependence of metabolic processes on temperature constrains the behavior, physiology and ecology of many ectothermic animals. The evolution of nocturnality in lizards, especially in temperate regions, requires adaptations for activity at low temperatures when optimal body temperatures are unlikely to be obtained. We examined whether nocturnal lizards have cold-adapted lactate dehydrogenase (LDH). LDH was chosen as a representative metabolic enzyme. We measured LDH activity of tail muscle in six lizard species (n = 123: three nocturnal, two diurnal and one crepuscular) between 5 and 35 °C and found no differences in LDH-specific activity or thermal sensitivity among the species. Similarly, the specific activity and thermal sensitivity of LDH were similar between skinks and geckos. Similar enzyme activities among nocturnal and diurnal lizards indicate that there is no selection of temperature specific LDH enzyme activity at any temperature. As many nocturnal lizards actively thermoregulate during the day, LDH may be adapted for a broad range of temperatures rather than adapted specifically for the low temperatures encountered when the animals are active. The total activity of LDH in tropical and temperate lizards is not cold-adapted. More data are required on biochemical adaptations and whole animal thermal preferences before trends can be established.     

Too cold is better than too hot: Preferred temperatures and basking behaviour in a tropical freshwater turtle

Thermoregulation is critical to the survival of animals. Tropical environments can be particularly thermally challenging as they reach very high, even lethal, temperatures. The thermoregulatory responses of tropical freshwater turtles to these challenges are poorly known. One common thermoregulatory behaviour is diurnal basking, which, for many species, facilitates heat gain. Recently, however, a north-eastern Australian population of Krefft's river turtles (Emydura macquarii krefftii) has been observed basking nocturnally, possibly to allow cooling. To test this, we determined the thermal preference (central 50% of temperatures selected) of E. m. krefftii in an aquatic thermal gradient in the laboratory. We then conducted a manipulative experiment to test the effects of water temperatures, both lower and higher than preferred temperature, on diurnal and nocturnal basking. The preferred temperature range fell between 25.3°C (±SD: 1.5) and 27.6°C (±1.4) during the day, and 25.3°C (±2.4) and 26.8°C (±2.5) at night. Based on this, we exposed turtles to three 24 h water temperature treatments (‘cool’ [23°C], ‘preferred’ [26°C] and ‘warm’ [29°C]) while air temperature remained constant at 26°C. Turtles basked more frequently and for longer periods during both the day and night when water temperatures were above their preferred range (the ‘warm’ treatment). This population frequently encounters aquatic temperatures above the preferred thermal range, and our results support the hypothesis that nocturnal basking is a mechanism for escaping unfavourably warm water. Targeted field studies would be a valuable next step in understanding the seasonal scope of this behaviour in a natural environment.     

Experimental manipulation reveals the importance of refuge habitat temperature selected by lizards

Refuges provide shelter from predators, and protection from exposure to the elements, as well as other fitness benefits to animals that use them. In ectotherms, thermal benefits may be a critical aspect of refuges. We investigated microhabitat characteristics of refuges selected by a heliothermic scincid lizard, Carlia rubrigularis, which uses rainforest edges as habitat. We approached lizards in the field, simulating a predator attack, and quantified the refuge type used, and effect of environmental temperatures (air temperature, substrate temperature and refuge substrate temperature) on the amount of time skinks remained in refuges after hiding (emergence time). In respone to our approach, lizards were most likely to flee into leaf litter, rather than into rocks or woody debris, and emergence time was dependent on refuge substrate temperature, and on refuge substrate temperature relative to substrate temperature outside the refuge. Lizards remained for longer periods in warmer refuges, and in refuges that were similar in temperature to outside. We examined lizard refuge choice in response to temperature and substrate type in large, semi‐natural outdoor enclosures. We experimentally manipulated refuge habitat temperature available to lizards, and offered them equal areas of leaf litter, woody debris and rocks. When refuge habitat temperature was unmanipulated, lizards (85%) preferred leaf litter, as they did in the field. However, when we experimentally manipulated the temperature of the leaf litter by shading, most skinks (75%) changed their preferred refuge habitat from leaf litter to woody debris or rocks. These results suggest that temperature is a critical determinant of refuge habitat choice for these diurnal ectotherms, both when fleeing from predators and when selecting daytime retreats.     

Behavioural thermoregulation by the endangered crocodile lizard (Shinisaurus crocodilurus) in captivity

Understanding the factors that may affect behavioural thermoregulation of endangered reptiles is important for their conservation because thermoregulation determines body temperatures and in turn physiological functions of these ectotherms. Here we measured seasonal variation in operative environmental temperature (T_e), body temperature (T_b), and microhabitat use of endangered crocodile lizards (Shinisaurus crocodilurus) from a captive population, within open and shaded enclosures, to understand how they respond to thermally challenging environments. T_e was higher in open enclosures than in shaded enclosures. The T_b of lizards differed between the open and shaded enclosures in summer and autumn, but not in spring. In summer, crocodile lizards stayed in the water to avoid overheating, whereas in autumn, crocodile lizards perched on branches seeking optimal thermal environments. Crocodile lizards showed higher thermoregulatory effectiveness in open enclosures (with low thermal quality) than in shaded enclosures. Our study suggests that the crocodile lizard is capable of behavioural thermoregulation via microhabitat selection, although overall, it is not an effective thermoregulator. Therefore, maintaining diverse thermal environments in natural habitats for behavioural thermoregulation is an essential measure to conserve this endangered species both in the field and captivity.     

Low cost of locomotion in lizards that are active at low temperatures

The nocturnality hypothesis of K. Autumn and coworkers states that nocturnal geckos have evolved a low energetic cost of locomotion (C(min)). A low C(min) increases maximum aerobic speed and partially offsets the decrease in maximum oxygen consumption caused by activity at low nocturnal temperatures. We tested whether a low C(min) is unique to nocturnal geckos or represents a more general pattern of convergent evolution among lizards that enables nocturnality and/or cold-temperature activity. We measured C(min) in four carefully selected lizard species from New Zealand (two nocturnal and two diurnal; n=5-9 individuals per species), including a nocturnal and diurnal gecko (a low C(min) is a gecko trait and is not related to nocturnality), a nocturnal skink (a low C(min) is related to being nocturnal), and a diurnal skink active at low temperatures (a low C(min) is related to being active at low body temperatures). The C(min) values of the four species measured in this study (range=0.21-2.00 mL O(2) g(-1) km(-1)) are lower than those of diurnal lizards from elsewhere, and the values are within or below the 95% confidence limits previously published for nocturnal geckos. A low C(min) increases the range of locomotor speeds possible at low temperatures and provides an advantage for lizards active at these temperatures. We accepted the hypothesis that nocturnal lizards in general have a low C(min) and provide evidence for a low C(min) in lizards from cool-temperate environments. The low C(min) in lizards living at high latitudes may enable extension of their latitudinal range into otherwise thermally suboptimal habitats.     

Nocturnal lizards from a cool-temperate environment have high metabolic rates at low temperatures

Ectotherms from low-temperature environments have higher metabolic rates at low temperatures than those from warm-temperature environments. We predicted that nocturnal lizards, which are active at much lower environmental temperatures than diurnal lizards, would also have higher metabolic rates at low temperatures, and by association a lower thermal sensitivity (Q ₁₀) than diurnal and crepuscular lizards. We measured the rate of oxygen consumption ( [(V)\dot]\textO ₂ \dot{V}{\text{O}}_{ 2} ) of eight cool-temperate species of lizard (four nocturnal, three diurnal, and one crepuscular) at 13 and 26°C and analyzed log transformations of these data using log mass as a covariate. As expected, [(V)\dot]\textO ₂ \dot{V}{\text{O}}_{ 2} was positively correlated with temperature in all eight species, with [(V)\dot]\textO ₂ \dot{V}{\text{O}}_{ 2} being two to four times higher at 26°C than at 13°C. As predicted, at 13°C (but not 26°C) the [(V)\dot]\textO ₂ \dot{V}{\text{O}}_{ 2} was significantly higher in nocturnal than diurnal lizards. Species-specific differences and mass scaling factors explain the patterns of thermal sensitivity seen among these eight lizard species. Thermal sensitivity is strongly influenced by mass, with smaller species generally having higher thermal sensitivity of their metabolic rate, and this result deserves further exploration among other ectotherms. We conclude that, along with the previously reported lower cost of locomotion found in nocturnal lizards, they also partially offset the thermal handicap of activity at low body temperatures by having an elevated [(V)\dot]\textO ₂ \dot{V}{\text{O}}_{ 2} at lower temperatures.     

Thermal biology and locomotor performance of the Andean lizard Liolaemus fitzgeraldi (Liolaemidae) in Argentina

Ectotherms thermoregulate to maintain their body temperature within the optimal range needed for performing vital functions. The effect of climate change on lizards has been studied as regards the sensitivity of locomotor performance to environmental temperatures. We studied thermoregulatory efficiency and locomotor performance for Liolaemus fitzgeraldi in the Central Andes of Argentina. We determined body temperature, micro-environmental temperatures and operative temperatures in the field. In the laboratory, we measured preferred temperatures and calculated the index of thermoregulatory efficiency. We estimated the thermal sensitivity of locomotion by measuring sprint speed (initial velocity and long sprint) and endurance at five different body temperatures. Body temperature was not associated with either micro-environmental temperature, nor did it show differences with preferred temperatures. Thermoregulatory efficiency was moderate (0.61). Initial velocity and long sprint trials showed differences at different temperatures; however, endurance did not. Moreover, the optimal temperatures for the performance trials showed no significant differences among themselves. We conclude that Liolaemus fitzgeraldi has thermal sensitivity in locomotor performance with respect to body temperature and that it is an eurythermic lizard that experiences a large variation in body temperature and that has thermal flexibility in the cold.     

Behavior as a Tool for Welfare Improvement and Conservation Management in the Endangered Lizard (Gallotia bravoana)

The study assessed the behavior of Gallotia bravoana (La Gomera, Canary Islands, one of the world's most threatened reptiles) to facilitate management decisions and improve welfare during initial stages of a species' recovery plan. The study analyzed—and remote-controlled video cameras filmed—the behavior of lizards housed in 3 outdoor enclosures, from May to September 2000. Daily activity showed a bimodal or unimodal pattern, all specimens basking more during June, with the largest male was the most active. Adults ate a higher percentage of vegetable items; subadults, a comparatively larger proportion of larvae and adult insects. The study analyzed individual compatibility; all interacted during 2 short periods. Aggression occurred mainly between males; because most directed high-intensity aggression toward a specific lizard, the study recommended isolating this lizard in a separate enclosure. The study recommended keeping 2 male-female pairs, who demonstrated social tolerance, as breeding pairs in separated terraria. Typical courtship behavior (head-bob sequences) occurred mainly during July, with highest frequency by the oldest male. Behavioral assessment provided data for improving the individuals' welfare in the enclosures and to select specific pairs for breeding.     

The impact of tick parasites on the behaviour of the lizard Tiliqua rugosa

Populations of the Australian sleepy lizard, Tiliqua rugosa, near Mt. Mary, South Australia carry natural infestations of two tick species Aponomma hydrosauri and Amblyomma limbatum. In field experiments at two sites, 18 km apart, lizards with experimentally increased tick loads had smaller home ranges, moved shorter distances in a day, and were found basking more but moving less often than lizards from which ticks were experimentally removed. The results were consistent for adult lizards in two years, and for sub-adults in a third year. Laboratory trials showed that juvenile lizards that had tick infestations had lower sprint speeds than uninfested siblings, and that adults with tick infestations had less endurance than those that were uninfested. The results contrast with those of a previous survey that showed that lizards with high tick loads had greater body size and remained longer at a site, but indicate that there may be a balance, for lizards, between the fitness advantages in occupying habitats with high-quality resources, and the costs from parasites that also prefer those habitats. Received: 02 March 1999 / Accepted: 07 October 1999     

The effect of carbon dioxide enrichment on apparent stem respiration from <Emphasis Type="Italic">Pinus taeda</Emphasis> L. is confounded by high levels of soil carbon dioxide

Huey and Slatkin’s (Q Rev Biol 51:363–384, 1976) cost–benefit model of lizard thermoregulation predicts variation in thermoregulatory strategies (from active thermoregulation to thermoconformity) with respect to the costs and benefits of the thermoregulatory behaviour and the thermal quality of the environment. Although this framework has been widely employed in correlative field studies, experimental tests aiming to evaluate the model are scarce. We conducted laboratory experiments to see whether the common lizard Zootoca vivipara, an active and effective thermoregulator in the field, can alter its thermoregulatory behaviour in response to differences in perceived predation risk and food supply in a constant thermal environment. Predation risk and food supply were represented by chemical cues of a sympatric snake predator and the lizards’ food in the laboratory, respectively. We also compared males and postpartum females, which have different preferred or “target” body temperatures. Both sexes thermoregulated actively in all treatments. We detected sex-specific differences in the way lizards adjusted their accuracy of thermoregulation to the treatments: males were less accurate in the predation treatment, while no such effects were detected in females. Neither sex reacted to the food treatment. With regard to the two main types of thermoregulatory behaviour (activity and microhabitat selection), the treatments had no significant effects. However, postpartum females were more active than males in all treatments. Our results further stress that increasing physiological performance by active thermoregulation has high priority in lizard behaviour, but also shows that lizards can indeed shift their accuracy of thermoregulation in response to costs with possible immediate negative fitness effects (i.e. predation-caused mortality).     

Cool running: locomotor performance at low body temperature in mammals

Mammalian torpor saves enormous amounts of energy, but a widely assumed cost of torpor is immobility and therefore vulnerability to predators. Contrary to this assumption, some small marsupial mammals in the wild move while torpid at low body temperatures to basking sites, thereby minimizing energy expenditure during arousal. Hence, we quantified how mammalian locomotor performance is affected by body temperature. The three small marsupial species tested, known to use torpor and basking in the wild, could move while torpid at body temperatures as low as 14.8-17.9°C. Speed was a sigmoid function of body temperature, but body temperature effects on running speed were greater than those in an ectothermic lizard used for comparison. We provide the first quantitative data of movement at low body temperature in mammals, which have survival implications for wild heterothermic mammals, as directional movement at low body temperature permits both basking and predator avoidance.     

升温对北草蜥雌体繁殖、卵孵化及幼体特征的影响

在围栏条件下,比较升温和对照处理北草蜥(Takydromus septentrionalis)繁殖、卵孵化及幼体特征的差异,以揭示升温对其繁殖生活史特征的作用。升温处理对北草蜥母体体温有显著影响,但并不影响其繁殖输出。升温显著影响卵孵化期和幼体的运动能力,但不影响幼体大小等形态特征。升温条件下孵出的幼体运动能力较弱。结果表明,北草蜥母体能耐受短期的环境增温,维持相对恒定的繁殖输出;升温能影响幼体的功能表现,进而可能改变后代适合度。     

Factors Influencing the Selection of Basking Perches on Cardon Cacti by Spiny-Tailed Iguanas (Ctenosaura hemilopha)1

The selection of optimal basking perches to achieve preferred body temperatures and avoid predation risks is one of the most important behavioral decisions that a lizard makes. We studied perch selection by the spiny-tailed Iguana (Ctenosaura hemilopha) in Baja California Sur where they bask on elevated cacti. The more important factor determining cardon selection by iguanas was the presence of old woodpecker holes which could be used as refuges within the top 50 cm of a branch. Other factors are the height of the cardon, the presence of some other holes and the number of branches of the plant. These data suggest that predation risk is the strongest factor affecting the selection of certain cardons as basking structures by spiny-tailed iguanas. Because the holes are mainly old woodpecker nests, the choice of a cardon as a refuge-perching site has to be related to a prior selection by woodpeckers.