Evolution of jumping capacity in Tropidurinae lizards: does habitat complexity influence obstacle‐crossing ability?

Jumping performance is relevant for lizards in many ecological contexts and might be favoured during the colonization of structurally complex habitats. Although ground-dwelling lizards use jumps to overcome small obstacles in their natural environments, jumping capacity has been mostly studied in arboreal species. Here, we analysed the evolution of jumping behaviour and performance in lizards from eight ground-dwelling species of Tropidurinae attempting to cross obstacles of different heights in a jumping track, both when undisturbed and under continuous stimulation. To establish ecological correlates with habitat complexity, individuals from two contrasting Brazilian habitats, the arid Caatingas (sand species) and the savannah-like Cerrados (rock species), were compared. Rock species jumped more often and crossed higher obstacles than sand ones in both tests, and performed more vertical than horizontal jumps. Although sand species performed less jumps, they were more successful at crossing the obstacles presented in comparison with rock species. Phylogenetic analyses confirmed these findings and demonstrated a large divergence in jumping capacity between sister-species from different habitats. Therefore, the differences in propensity and endurance for jumping activity appear to be independent of phylogenetic relationships in Tropidurinae and likely reflect an adaptation to the contrasting environments inhabited. The ecological implications of these findings are discussed.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 393–402.     

The impact of insularity on the thermoregulation of a Mediterranean lizard

The overall biology of ectotherms is strongly affected by the thermal quality of the environment. The particular conditions prevailing on islands have a strong effect on numerous features of animal life. In this study we compared mainland and island populations of the lizard Lacerta trilineata and hypothesized that insularity would affect the thermoregulatory strategy. Continental habitats were of lower thermal quality, experiencing more intense fluctuations and had higher values of operative temperatures. Nevertheless mainland lizards selected for higher body temperatures in the lab and showed more effective thermoregulation during summer than their island peers. Lizards achieved similar body temperatures in the field in both types of habitat, underlining the importance of predation as a potential factor to mainland lizards that failed to reach their higher thermal preferences. Both island and mainland populations of L. trilineata have been adapted to their thermal environment, supporting the labile view on the evolution of thermal physiology for this species.     

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.     

Thermal regimes during incubation do not affect mean selected temperatures of hatchling lizards (Bassiana duperreyi, Scincidae)

Incubation temperatures profoundly affect many phenotypic traits of squamate reptiles, and mean selected body temperatures of such animals also are plastic in response to environmental factors. Plausibly, then, incubation temperatures might affect hatchling thermoregulation, either via adaptation (i.e., populations that historically experience different nest conditions, also will diverge in hatchling thermoregulatory behaviour) or phenotypic plasticity (incubation temperatures directly modify hatchling behaviours). We tested this hypothesis with a montane scincid lizard (Bassiana duperreyi), using thermal-imaging methods to quantify temperatures (of both head and body) selected by hatchling lizards. The young lizards kept their heads cooler than their bodies, but mean selected temperatures did not differ among hatchlings from three populations with differing thermal regimes in natural nests, nor were they affected by thermal conditions during incubation. The conservatism of mean selected temperatures stands in strong contrast to the lability of many other phenotypic traits in response to incubation temperatures in this species.     

Body Temperature and Thermoregulatory Behaviour of the Lizard Ameiva ameiva in Central Amazonian Forests

Body temperatures and thermoregulatory behaviour of the teiid lizard Ameiva ameiva inhabiting the edge and the understory were studied in Central Amazonian forests. Despite of differences in the thermal profile of the habitats, the mean body temperature was the same for active lizards observed at the edge or inside the forest, where only slight peculiarities in thermoregulatory behaviour were observed. A. ameiva is capable of maintaining body temperature significantly above microhabitat temperature.     

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.     

Forest‐fire regimes affect thermoregulatory opportunities for terrestrial ectotherms

Fire‐induced changes in canopy openness may affect sunlight penetration to the forest floor, and thus the operative temperatures available to terrestrial ectotherms. We examined thermal regimes for two types of ectotherms: diurnally active species that utilize sun‐exposed patches to regulate their body temperatures, and nocturnally active species that depend upon solar radiation striking the rocks under which they shelter. We measured canopy openness, shrub height, radiation transmission and operative environmental temperatures in the open and inside reptile retreat‐sites, at 24 study sites in eucalypt forests in two regions (Gosford and Yengo) in south‐eastern Australia. All sites were last burnt in 2000–2001, but had experienced different fire frequencies (1–4 fires over the previous 37 years). In Gosford, higher fire frequencies reduced canopy openness and radiation transmission at ground and shrub level, and thus reduced environmental temperatures and the thermal quality of reptile habitats. Our modelling based on thermal preferenda of an endangered snake species (the broad‐headed snake Hoplocephalus bungaroides) suggests that increased fire frequency at Gosford halved the amount of time an animal could spend within its preferred (set‐point) range, regardless of whether it thermoregulated beneath rocks or basked out in the open. At Yengo, however, fire frequency did not affect the thermal quality of reptile habitats. Thus, the effects of fire frequency on forest structure and the thermal environment at ground level differed between adjacent areas, and relatively small changes in canopy openness translated into major effects on thermoregulatory opportunities for reptiles. Although fire is a useful management tool for creating open habitats, we need to understand more about the effects of fire frequency on vegetation structure and thermal environment before we can use fire to manage habitats for reptiles.     

Influence of altitude, habitat and microhabitat on thermal adaptation of cicadas from Southwest Texas (Hemiptera: Cicadidae)

The thermal responses of 12 cicada species inhabiting Big Bend National Park, Texas, USA are investigated to determine the influence of altitude, habitat and microhabitat. The park provides an opportunity to analyze the thermal responses in animals from a variety of habitats and altitudinal gradients within a limited geographic range. The data suggest that thermal responses of cicadas are adaptations to their specific habitats. No thermal responses are significantly correlated with body size. The maximum voluntary tolerance temperature (an upper behavioral thermoregulatory point) and heat torpor temperatures show significant correlations with altitude. Variability in thermal responses can also be related to the characteristics of the microhabitat selected or the behavioral pattern of a species.     

Thermoregulatory differences in African mole-rat species from disparate habitats: Responses and limitations

Individuals and populations possess physiological adaptations to survive local environmental conditions. To occur in different regions where ambient temperature varies, animals must adopt appropriate thermoregulatory mechanisms. Failure to adjust to environmental challenges may result in species distributional range shifts or decreased viability. African mole-rats (Bathyergidae) occupy various habitats in sub-Saharan Africa from deserts to montane regions to mesic coastal areas. We examined thermoregulatory characteristics of three African mole-rat species originating from disparate (montane, savannah, and arid/semi-arid) habitats. Animals were exposed to various ambient temperatures, whilst core body temperature and the surface temperature of different body parts were measured. Oxygen consumption was determined as a measure of heat production. Core body temperatures of Natal (montane) mole-rats (Cryptomys hottentotus natalensis) increased significantly at ambient temperatures >24.5 °C, while those of the highveld (Cryptomys hottentotus pretoriae) (savannah) and Damaraland (Fukomys damarensis) (arid/semi-arid) mole-rats remained within narrower ranges. In terms of surface temperature variation, while pedal surfaces were important in regulating heat loss in Natal and Damaraland mole-rats at high ambient temperatures, the ventral surface was important for heat dissipation in Damaraland and highveld mole-rats. This study provides evidence of the variation and limitations of thermo-physiological mechanisms for three mole-rat species relative to their habitats. Information on physiological adaptations to particular habitats may inform predictive modelling of species movements, declines, and extinctions in response to a changing environment, such as climate change.     

Comparisons of behavioural and TRPA1 heat sensitivities in three sympatric Cuban Anolis lizards

Thermal tolerances of organisms play a role in defining geographic ranges and occurrence of species. In Cuba, three sympatric species of Anolis lizards (Anolis allogus, Anolis homolechis and Anolis sagrei) inhabit different thermal microhabitats. A previous study found that these species showed distinct gene expression patterns in response to temperature stimuli, suggesting the genetically distinct thermal physiology among species. To investigate whether the Anolis species inhabiting locally distinct thermal habitats diverge their thermal tolerances, we first conducted behavioural experiments to analyse the temperatures at which the three Anolis species escape from heat source. Then, for each of the three species, we isolated cDNA encoding a putative molecular heat sensor, transient receptor potential ion channel ankyrin 1 (TRPA1), which has been suggested to play a role on eliciting behavioural responses to heat stimuli. We performed electrophysiological analysis to quantify activation temperature of Anolis TRPA1 to see whether the pattern of divergence in TRPA1 responses is congruent with that of divergence in behavioural responses. We found that temperatures triggering behavioural and TRPA1 responses were significantly lower for shade‐dwelling species (A. allogus) than for sun‐dwelling species (A. homolechis and A. sagrei). The ambient temperature of shade habitats where A. allogus occurs stays relatively cool compared to that of open habitats where A. homolechis and A. sagrei occur and bask. The high temperature thresholds of A. homolechis and A. sagrei may reflect their heat tolerances that would benefit these species to inhabit the open habitats.     

Is increased maternal basking an adaptation or a pre-adaptation to viviparity in lizards?

Pregnant females modify their thermoregulatory behaviour in many species of viviparous (live-bearing) reptiles, typically maintaining higher and more stable body temperatures at this time. Such modifications often have been interpreted as adaptations to viviparity, functioning to accelerate embryonic development and/or modify phenotypic traits of hatchlings. An alternative possibility is that similar maternal thermophily may be widespread also in oviparous species and if so, would be a pre-adaptation (rather than an adaptation) to viviparity. Because eggs are retained in utero for a significant proportion of development even in oviparous reptiles, maternal thermophily might confer similar advantages in oviparous as in viviparous taxa. Experimental trials on montane oviparous scincid lizards (Bassiana duperreyi) support the pre-adaptation hypothesis. First, captive females (both reproductive and non-reproductive) selected higher temperatures than males. Second, experimentally imposing thermal regimes on pregnant females significantly affected their oviposition dates and the phenotypic traits (body shape, running speed) of their hatchlings. Thus, as for many other behavioural correlates of pregnancy in viviparous reptiles, maternal thermophily likely may have already been present in the ancestral oviparous taxa that gave rise to present-day viviparous forms.     

Micro-scale differences in thermal habitat quality and a possible case of evolutionary flexibility in the thermal physiology of lacertid lizards

We studied the thermal ecology of the lacertid lizards Lacerta oxycephala and Podarcis melisellensis on the Adriatic island of Vis (Croatia) during summer. These species obviously differ in microhabitat use: L. oxycephala climbs on rocks and stone walls, whereas P. melisellensis is mainly ground-dwelling in vegetation. Since theoretical considerations predict a difference in thermal quality between the species' microhabitats, this system seems to present a good opportunity to test the influence of thermal microhabitat quality on body temperature, thermoregulatory behaviour and evolution of thermal characteristics. Data on thermoregulatory behaviour, body temperatures (T_b) and habitat quality were collected in the field and selected temperatures (T_sel) were estimated in a laboratory thermogradient. Accuracy and effectiveness of thermoregulation were quantified. Thermoregulatory behaviour consisted of timing of activity, selection of places in full sun and near sun-shade transitions, and basking. As predicted, L. oxycephala occupied the microhabitat with the lower thermal quality and had on average a lower T_b. However, L. oxycephala also selected lower temperatures in the experimental thermogradient. Thus, if T_sel can be regarded as the thermoregulatory target, both species proved to be accurate and effective thermoregulators. These results corroborate the "labile view" on the evolution of thermal physiology: both L. oxcephala and P. melisellensis appear to be adapted to their respective thermal microhabitat. This is a surprising conclusion, since earlier studies have found the thermal characteristics of Lacertidae to be evolutionarily rigid.     

The ecological consequences of unpalatable prey: phytoplankton response to nutrient and predator additions

Thermoregulation is thought to be the most important factor influencing habitat selection by terrestrial ectotherms, at least in temperate climates. The cost-benefit model of thermoregulation predicts that ectotherms should invest more in thermoregulation when the costs of doing so are low (when the thermal quality of the habitat is high). However, the extent to which ectotherms vary their thermoregulatory behaviour according to the thermal quality of habitats is currently unknown. We studied the relationship between habitat use and thermoregulation in 53 black rat snakes using temperature-sensitive radio-transmitters. Among the habitats available to black rat snakes, edges had the highest thermal quality, retreat sites and forest were intermediate, and open habitats had the lowest thermal quality. Black rat snakes experienced more favourable body temperatures while in barns (retreat sites) than in edges, and in edges than in forest. During the day, the effectiveness and the extent of thermoregulation by the snakes were equal in barns and forest, but much lower in edges. In fact, black rat snakes selected thermally favourable microhabitats less than their availability while in edges. Therefore, more favourable body temperatures were not necessarily achieved in thermally superior habitats by increased thermoregulation, but simply because favourable temperatures were encountered more often in those habitats. This result is contrary to the central prediction of the cost-benefit model of thermoregulation and we suggest that this model should be modified to put more emphasis on other costs of thermoregulation, such as increased predation risk or lost foraging opportunities.     

Morphological evolution in Tropidurinae squamates: an integrated view along a continuum of ecological settings

Variation in squamate foot morphology is likely relevant during evolutionary processes of habitat colonization because distinct surfaces differ in energetic and functional demands for locomotion. We combined new foot morphological data with published information of limb and tail lengths to investigate evolutionary changes possibly associated with the differential usage of ecological settings by Tropidurinae species. Several traits exhibited significant phylogenetic signal, and we performed conventional and phylogenetic regressions of PC scores (retained from Principal Components Analyses of morphometric traits) on continuous ecological indices. Tropidurines from sandy habitats exhibit larger foot soles, opposite to the evolution of narrow feet in species that use branches and rocks. Also, species that usually move along trunks present longer femora. This study provides evidence for morphological adaptations associated with substrate usage in Tropidurinae, and suggests that opposite morphological profiles might evolve associated with the use of surfaces energetically and functionally contrasting, possibly leading to trade‐offs.     

Thermal ecology of the Australian agamid Pogona barbata

This study compares the thermal ecology of male bearded dragon lizards (Pogona barbata) from south-east Queensland across two seasons: summer (1994–1995) and autumn (1995). Seasonal patterns of body temperature (T _b) were explored in terms of changes in the physical properties of the thermal environment and thermoregulatory effort. To quantify thermoregulatory effort, we compared behavioral and physiological variables recorded for observed lizards with those estimated for a thermoconforming lizard. The study lizards' field T _bs varied seasonally (summer: grand daily mean (GDM) 34.6 ± 0.6°C, autumn: GDM 27.5 ± 0.3°C) as did maximum and minimum available operative temperatures (summer: GDM T _max 42.1 ± 1.7°C, T _min 32.2 ± 1.0°C, autumn: GDM T _max 31.7 ± 1.2°C, T _min 26.4 ± 0.5°C). Interestingly, the range of temperatures that lizards selected in a gradient (selected range) did not change seasonally. However, P. barbata thermoregulated more extensively and more accurately in summer than in autumn; lizards generally displayed behaviors affecting heat load nonrandomly in summer and randomly in autumn, leading to the GDM of the mean deviations of lizards' field T _bs from their selected ranges being only 2.1 ± 0.5°C in summer, compared to 4.4 ± 0.5°C in autumn. This seasonal difference was not a consequence of different heat availability in the two seasons, because the seasonally available ranges of operative temperatures rarely precluded lizards from attaining field T _bs within their selected range, should that have been the goal. Rather, thermal microhabitat distribution and social behavior appear to have had an important influence on seasonal levels of thermoregulatory effort. Received: 28 April 1997 / Accepted: 29 December 1997     

Relations between microhabitat use and limb shape in phrynosomatid lizards

With the exception of the well-documented case for anoline lizards, recent studies have found few evolutionary relationships between morphology and habitat use in lizards despite clear-cut biomechanical predictions. One of the factors typically hampering these analyses is the clustering of habitat use within evolutionary lineages. In the present study, body shape was quantified for male and female lizards of 30 species of phrynosomatid lizards. This group was selected as little clustering of ecological variables seemed to be present. The results of traditional analyses indicate that evolutionary correlates of habitat use were prominent in the hindlimbs of both sexes. Species living in open habitats are characterized by longer femurs, and longer hindlimbs relative to the forelimb. Moreover, males from ground-dwelling species utilizing open habitats have longer toes on the hind foot than males from climbing species. Phylogenetic analyses indicated strong evolutionary associations between habitat use and the relative length of front and hindlimbs, with species from open terrestrial habitats having significantly shorter frontlimbs relative to their hindlimb than rock or tree climbing species. Evolutionary associations between morphology and habitat use were generally stronger for male lizards, indicating a potentially important contribution of sexual selection to the evolution of differences in limb proportions.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 149–163.     

Miami heat: Urban heat islands influence the thermal suitability of habitats for ectotherms

The urban heat island effect, where urban areas exhibit higher temperatures than less‐developed suburban and natural habitats, occurs in cities across the globe and is well understood from a physical perspective and at broad spatial scales. However, very little is known about how thermal variation caused by urbanization influences the ability of organisms to live in cities. Ectotherms are sensitive to environmental changes that affect thermal conditions, and therefore, increased urban temperatures may pose significant challenges to thermoregulation and alter temperature‐dependent activity. To evaluate whether these changes to the thermal environment affect the persistence and dispersal of ectothermic species in urban areas, we studied two species of Anolis lizards (Anolis cristatellus and Anolis sagrei) introduced to Miami‐Dade County, FL, USA, where they occur in both urban and natural habitats. We calculated canopy openness and measured operative temperature (T_e), which estimates the distribution of body temperatures in a non‐thermoregulating population, in four urban and four natural sites. We also captured lizards throughout the day and recorded their internal body temperature (T_b). We found that urban areas had more open canopies and higher T_e compared to natural habitats. Laboratory trials showed that A. cristatellus preferred lower temperatures than A. sagrei. Urban sites currently occupied by each species appear to lower thermoregulatory costs for both species, but only A. sagreihad field T_b that were more often within their preferred temperature range in urban habitats compared to natural areas. Furthermore, based on available T_e within each species' preferred temperature range, urban sites with only A. sagrei appear less suitable for A. cristatellus, whereas natural sites with only A. cristatellus are less suitable for A. sagrei. These results highlight how the thermal properties of urban areas contribute to patterns of persistence and dispersal, particularly relevant for studying species invasions worldwide.     

EVOLUTIONARY PATTERNS OF THE THERMAL SENSITIVITY OF SPRINT SPEED IN ANOLIS LIZARDS

I present evidence that the thermal sensitivity of sprint speed of Anolis lizards has evolved to match the activity body temperatures (T_b) experienced by local populations in nature. Anolis lizards from a range of altitudes in Costa Rica have limited thermoregulatory abilities and consequently have field T_b that differ substantially in median and interquartile distance (a measure of variability). Experimentally determined maximal sprint temperatures (T_b at which lizards run fastest) were positively correlated with median field T_b, and performance breadths (ranges of T_b over which lizards run well) were correlated with the variability (interquartile distance) of field T_b in the species I examined. Such correlations would be expected if the thermal sensitivity of sprint speed and field T_b had evolved together to improve the sprint performance of lizards in nature. Integration of laboratory and field studies indicates that several species of Anolis regularly experience impaired sprint speeds in the field, despite apparent evolutionary modification of their thermal physiologies. However, this impairment would have been more severe if the thermal sensitivities of sprint speed had not evolved. Data from other groups of lizards indicate that the thermal sensitivity of sprint speed has not evolved to match T_b of local populations (Hertz et al., 1983; Crowley, 1985). These lizards experience less variable T_b and less impairment of sprint speeds in the field than do the anoles. Thus, selection for modification of the thermal sensitivity of sprint speed might have been stronger for anoles than for other groups of lizards.     

The highest kingdom of Anolis: Thermal biology of the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) over an elevational gradient in the Eastern Cordillera of Colombia

Vertebrate ectotherms may deal with changes of environmental temperatures by behavioral and/or physiological mechanisms. Reptiles inhabiting tropical highlands face extreme fluctuating daily temperatures, and extreme values and intervals of fluctuations vary with altitude. Anolis heterodermus occurs between 1800 m to 3750 m elevation in the tropical Andes, and is the Anolis species found at the highest altitude known. We evaluated which strategies populations from elevations of 2200 m, 2650 m and 3400 m use to cope with environmental temperatures. We measured body, preferred, critical maximum and minimum temperatures, and sprint speed at different body temperatures of individuals, as well as operative temperatures. Anolis heterodermus exhibits behavioral adjustments in response to changes in environmental temperatures across altitudes. Likewise, physiological traits exhibit intrapopulation variations, but they are similar among populations, tended to the “static” side of the evolution of thermal traits spectrum. The thermoregulatory behavioral strategy in this species is extremely plastic, and lizards adjust even to fluctuating environmental conditions from day to day. Unlike other Anolis species, at low thermal quality of the habitat, lizards are thermoconformers, particularly at the highest altitudes, where cloudy days can intensify this strategy even more. Our study reveals that the pattern of strategies for dealing with thermal ambient variations and their relation to extinction risks in the tropics that are caused by global warming is perhaps more complex for lizards than previously thought.     

Coalescence patterns of endemic Tibetan species of stream salamanders (Hynobiidae: Batrachuperus)

Orogenesis of topographically diverse montane regions often drives complex evolutionary histories of species. The extensive biodiversity of the eastern edge of the Tibetan Plateau, which gradually decreases eastwardly, facilitates a comparison of historical patterns. We use coalescence methods to compare species of stream salamanders (Batrachuperus) that occur at high and low elevations. Coalescent simulations reveal that closely related species are likely to have been influenced by different drivers of diversification. Species living in the western high‐elevation region with its northsouth extending mountains appear to have experienced colonization via dispersal followed by isolation and divergence. In contrast, species on the eastern low‐elevation region, which has many discontinuous mountain ranges, appear to have experienced fragmentation, sometimes staged, of wide‐ranging ancestral populations. The two groups of species appear to have been affected differently by glaciation. High‐elevation species, which are more resistant to cooler temperatures, appear to have experienced population declines as recently as the last glaciation (0.016–0.032 Ma). In contrast, salamanders dwelling in the warmer and wetter habitats at low‐elevation environs appear to have been affected less by the relatively recent, milder glaciation, and more so by harsher, extensive glaciations (0.5–0.175 Ma). Thus, elevation, topography and cold tolerance appear to drive evolutionary patterns of diversification and demography even among closely related taxa. The comparison of multiple species in genealogical analyses can lead to an understanding of the evolutionary drivers.