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Compensation of thermal constraints along a natural environmental gradient in a Malagasy iguanid lizard (Oplurus quadrimaculatus)
Abstract
Physiological or behavioural adjustments are a prerequisite for ectotherms to cope with different thermal environments. One of the world's steepest environmental gradients in temperature and precipitation can be found in southeastern Madagascar. This unique gradient allowed us to study the compensation of thermal constraints in the heliothermic lizard Oplurus quadrimaculatus on a very small geographic scale. The lizard occurs from hot spiny forest to intermediate gallery and transitional forest to cooler rain forest and we investigated whether these habitat differences are compensated behaviourally or physiologically. To study activity skin temperature (as proxy for body temperature) and the activity time of lizards, we attached temperature loggers to individuals in three different habitats. In addition, we calculated field resting costs from field resting metabolic rate to compare energy expenditure along the environmental gradient. We found no variation in activity skin temperature, despite significant differences in operative environmental temperature among habitats. However, daily activity time and field resting costs were reduced by 35% and 28% in the cool rain forest compared to the hot spiny forest. Our study shows that O. quadrimaculatus relies on behavioural mechanisms rather than physiological adjustments to compensate thermal differences between habitats. Furthermore, its foraging activity in open, sun exposed habitats facilitates such a highly effective thermoregulation that cold operative temperature, not energetically expensive heat, presents a greater challenge for these lizards despite living in a hot environment.
... Through its impact on physiology, temperature is considered to be the 'abiotic master factor' for ectotherms (Dalvi et al., 2009;Turriago et al., 2015;Sunday et al., 2014;Berg et al., 2017;Theisinger et al., 2017). The tolerable thermal window of ectotherms is bracketed by critical temperatures (CT min and CT max ) beyond which survival is not possible and these limits occur where aerobic scope is either zero or (Holzman and McManus, 1973). ...
... As climate change is increasing mean environmental temperatures and the frequency of extreme thermal events (Pachauri et al., 2014;Gutiérrez-Pesquera et al., 2016;Theisinger et al., 2017), species with a limited capacity for acclimation will suffer from high maintenance costs as caused by the high SMRs. Especially in anuran larvae, having a low energy expenditure before and during metamorphosis is favorable since metamorphosis is a highly energyconsuming process (Orlofske and Hopkins, 2009). ...
... Consequently, larvae of X. laevis have the ability to compensate for changes in developmental temperature as they increased their thermal limits at warmer developmental temperatures (Schaefer and Ryan, 2006;Gunderson and Stillman, 2015;Little and Seebacher, 2016). The driver for this adjustment are changes in the thermal reaction norm and hence of physiological nature (Little and Seebacher, 2016;Theisinger et al., 2017). ...
Environmental variation induced by natural and anthropogenic processes including climate change may threaten species by causing environmental stress. Anuran larvae experiencing environmental stress may display altered thyroid hormone (TH) status with potential implications for physiological traits. Therefore, any capacity to adapt to environmental changes through plastic responses provides a key to determining species vulnerability to environmental variation. We investigated whether developmental temperature (Tdev), altered TH levels and whether the interactive effect of both affect standard metabolic rate (SMR), body condition (BC), survival and thermal tolerance in larvae of the African clawed frog (Xenopus laevis) reared at five temperatures with experimentally altered TH levels. At metamorphosis, SMR, BC and survival were significantly affected by Tdev, TH status and their interaction with the latter often intensified impacts. Larvae developing at warmer temperatures exhibited significantly higher SMRs and BC was reduced at warm Tdev and high TH levels suggesting decreased ability to acclimate to variation in temperature. Accordingly, tadpoles that developed at warm temperatures had higher maximum thermal limits but more narrow thermal tolerance windows. High and low TH levels decreased and increased upper thermal limits, respectively. Thus, when experiencing both warmer temperatures and environmental stress, larvae may be less able to compensate for changes in Tdev. Our results demonstrate that physiological traits in larvae of X. laevis are strongly affected by increased TH levels and warmer temperatures. Altered TH levels and increasing Tdev due to global change may result in a reduced capacity for physiological plasticity. This has far reaching consequences since the energetic requirement at the onset of metamorphosis is known to determine metamorphic success and thus, is indirectly linked to individual fitness in later life stages.
... High elevations generally denote low thermal quality habitat because the low temperatures diverge from the preferred body temperature of ectotherms (e.g., Brattstrom 1965Brattstrom , 1968Navas 1996;Diaz 1997), especially as preferred body temperatures of ectotherms tend to be phylogenetically conserved (e.g., Van Damme et al. 1989;Andrews 1998;Gvoždík & Castilla 2001;Theisinger et al. 2017;Díaz de la Vega-Pérez et al. 2019). The cool temperatures at high elevations may work to constrain time that can be allocated to activities such as foraging, territory defense, and mate searching, while simultaneously increasing time and effort required to behaviorally thermoregulate (Navas 1997, Nilson & Andren 1997Zamora-Camacho et al. 2013;Artacho et al. 2017;Theisinger et al. 2017;Díaz de la Vega-Pérez et al. 2019). ...
... High elevations generally denote low thermal quality habitat because the low temperatures diverge from the preferred body temperature of ectotherms (e.g., Brattstrom 1965Brattstrom , 1968Navas 1996;Diaz 1997), especially as preferred body temperatures of ectotherms tend to be phylogenetically conserved (e.g., Van Damme et al. 1989;Andrews 1998;Gvoždík & Castilla 2001;Theisinger et al. 2017;Díaz de la Vega-Pérez et al. 2019). The cool temperatures at high elevations may work to constrain time that can be allocated to activities such as foraging, territory defense, and mate searching, while simultaneously increasing time and effort required to behaviorally thermoregulate (Navas 1997, Nilson & Andren 1997Zamora-Camacho et al. 2013;Artacho et al. 2017;Theisinger et al. 2017;Díaz de la Vega-Pérez et al. 2019). We can expect that ectothermic organisms will either adapt or compensate for the thermal challenges associated with high elevations (Gurney & Middleton 1996;Herczeg et al. 2003;Toledo et al. 2008;Besson & Cree 2010;Aguado & Braña 2014;Zamora-Camacho et al. 2016). ...
Individuals that inhabit broad elevational ranges may experience unique environmental challenges. Because temperature decreases with increased elevation the ectotherms living at high elevations have to manage limited activity time and high thermoregulatory effort. The resting metabolic rate (RMR) of a postabsorptive animal is related to its total energy requirements as well as many other fitness traits. Mesquite lizards (Sceloporus grammicus, Wiegmann 1828) living on La Malinche Volcano, Mexico inhabit a wide elevational range with some populations apparently thriving above the tree line. We measured the RMR of lizards from different elevations (i.e., 2600 m, 3200 m, and 4100 m) at four ecologically relevant temperatures (i.e., 15, 25, 30, and 35°C) and found that RMR of mesquite lizards increased with temperature and body mass. More importantly, lizards from the high‐elevation population had mass specific RMR that was higher at all temperatures. While the higher RMRs of high‐elevation populations imply higher metabolic costs at a given temperature these lizards were also smaller. Both of these traits may allow these high elevation populations to thrive in the face of the thermal challenges imposed by their environment.
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... Species may present physiological compensation, plasticity and acclimatization as a supplementary mechanism to compensate thermal challenges (Putman and Clark, 2017;Theisinger et al., 2017). Stressful environmental temperatures may increase the energetic costs of metabolism maintenance during dormancy or nocturnal inactivity or reduce the quality of low-temperature thermoregulatory refugia (Lelièvre et al., 2013;Flesch et al., 2017). ...
... Martín and López (2013), Stahlschmidt et al. (2017) Squamata Thermal physiology Increase operative temperature Increase of energy expenditure and changes on thermoregulatory strategy Shade availability, use of refugies Weatherhead et al. (2012), Valenzuela-Ceballos et al. (2015), Basson et al. Trullas et al. (2011), Brischoux et al. (2015), Buckley et al. (2015), Ferri-Yáñez and Araújo (2015), Ortega et al. (2016b), Putman and Clark(2017),Theisinger et al. (2017) ...
In recent decades, changes in climate have caused impacts on natural and human systems on all continents and across the oceans and many species have shifted their geographic ranges, seasonal activities, migration patterns, abundances and interactions in response to these changes. Projections of future climate change are uncertain, but the Earth’s warming is likely to exceed 4.8°C by the end of 21th century. The vulnerability of a population, species, group
or system due to climate change is a function of impact of the changes on the evaluated system (exposure and sensitivity) and adaptive capacity as a response to this impact, and the relationship between these elements will determine the degree of species vulnerability. Predicting the potential future risks to biodiversity caused by climate change has become an extremely active field of research, and several studies in the last two decades had focused on determining possible impacts of climate change on Lepidosaurians, at a global, regional and local level. Here we conducted a systematic review of published studies in order to seek to what extent the accumulated knowledge currently allow us to identify potential trends or patterns regarding climate change effects on lizards, snakes, amphisbaenians and tuatara. We conducted a literature search among online literature databases/catalogues and recorded 255 studies addressing the influence of climate change on a total of 1918 species among 49 Lepidosaurian’s families. The first study addressing this subject is dated 1999. Most of the studies focused on species distribution, followed by thermal constraints, reproductive biology, behavior and genetics. We concluded that an integrative approach including most of these characteristics and also bioclimatic and environmental variables, may lead to consistent and truly effective strategies for species conservation, aiming to buffer the climate change effects on this group of reptiles.
... Seasonal fRMR differs significantly at low T b for all thresholds ≤ 36°C (p < 0.05, df = 10). A T b of 36°C correspo nds to the l ower end of ac tivity T b i n O. quadrimaculatus and also marks a threshold for behavioral changes on sunny days (Theisinger et al. 2017), so a split of the dataset at 36°C also appears to be ecologically reasonable. Loess curves for Z. laticaudatus show no such clear pattern of diverging seasonal fRMR. ...
... O. quadrimaculatus shows clear seasonal differences in fRMR at T b below its range of activity T b but whether a rate Multiple fRMR records per T b from the same individual were averaged before plotting loess curves to avoid a bias in the weighting of data is elevated in one season or lowered in another (or both) can be difficult to assess in species that do not show seasonal reductions in activity (e.g., Zari 1996). O. quadrimaculatus does not seem to experience seasonal food or water restrictions and thermoregulates precisely to a narrow range of activity T b , at least on sunny days (Theisinger et al. 2017). It therefore seems reasonable to argue against a lowered fRMR as a measure for saving energy during the dry season. ...
The physiological compensation of animals in changing environments through acclimatization has long been considered to be of minor importance in tropical ectotherms due to more stable climatic conditions compared to temperate regions. Contrasting this assumption are reports about a range of metabolic adjustments in tropical species, especially during the last two decades from field acclimatized animals. Metabolic rates are strongly linked to temperature in ectotherms but they also reflect energetic requirements and restrictions. We therefore postulate that the observed variety of acclimatization patterns in tropical reptiles results from an interaction of multiple influences, including food and water availability, rather than from thermal constraints alone. We present new data from two sympatric Malagasy lizards with contrasting acclimatization patterns and, complemented with an extensive literature search, discuss the variety of acclimatization patterns in tropical reptiles with regard to thermal and energetic influences. This broad consideration of constraints allows a rearrangement of apparently controversial patterns into a scheme of decreasing metabolic costs, including two new categories for selective and selective inverse acclimatization, where metabolic shifts are restricted to body temperatures below those preferred during activity.
... Changes in T sel can help lizards adapt to new habitats (Bennett and Lenski 1993). In warming habitats, an increase in T sel can broaden the activity time window for ectotherms and may reduce the costs of behavioral thermoregulation (Gvoždík 2012;Theisinger et al. 2017). Indeed, the costs of thermoregulation largely depend on the thermal quality of habitats. ...
The survival of ectotherms worldwide is threatened by climate change. Whether increasing temperatures increase the vulnerability of ectotherms inhabiting temperate plateau areas remains unclear. To understand altitudinal variation in the vulnerability of plateau ectotherms to climate warming, Qinghai toad-headed lizards (Phrynocephalus vlangalii) were subjected to semi-natural enclosure experiments with simulated warming at high (2,600 m) and superhigh (3,600 m) elevations of the Dangjin Mountain, China. Our results revealed that the thermoregulatory effectiveness and warming tolerance (WT) of the toad-headed lizards were significantly affected by climate warming at both elevations, but their thermal sensitivity remained unchanged. After warming, the thermoregulatory effectiveness of lizards at superhigh elevations decreased because of the improved environmental thermal quality, whereas that of lizards at high-elevation conditions increased. Although the body temperature selected by high-elevation lizards was also significantly increased, the proportion of their active body temperature falling within the set-point temperature range decreased. This indicates that it is difficult for high-elevation lizards to adjust their body temperatures within a comfortable range under climate warming. Variations in the WT and thermal safety margin (TSM) under climate warming revealed that lizards at the superhigh elevation benefited from improved environmental thermal quality, whereas those at the high elevation originally on the edge of the TSM faced more severe threats and became more vulnerable. Our study highlights the importance of thermal biological traits in evaluating the vulnerability of ectotherms in temperate plateau regions.
... Body temperatures of reptiles and other ectotherms are dependent on the environment. An individual's body temperature influences its metabolism (Andrews & Pough, 1985;Sears, 2005;Theisinger et al., 2017), life history (Cadby et al., 2014;Meiri et al., 2013), behaviour (Gunderson & Leal, 2015;Henle, 1992;Ord & Stamps, 2017) and ecology (Niewiarowski & Waldschmidt, 1992;Pafilis et al., 2007;Van Damme et al., 1989. Consequently, body temperature plays a critical role in shaping ectotherm fitness (Angilletta, 2009;Angilletta et al., 2002;Cadby et al., 2014). ...
... Body temperatures of reptiles and other ectotherms are dependent on the environment. An individual's body temperature influences its metabolism (Andrews & Pough, 1985;Sears, 2005;Theisinger et al., 2017), life history (Cadby et al., 2014;Meiri et al., 2013), behaviour (Gunderson & Leal, 2015;Henle, 1992;Ord & Stamps, 2017) and ecology (Niewiarowski & Waldschmidt, 1992;Pafilis et al., 2007;Van Damme et al., 1989. Consequently, body temperature plays a critical role in shaping ectotherm fitness (Angilletta, 2009;Angilletta et al., 2002;Cadby et al., 2014). ...
Aim: Squamate fitness is affected by body temperature, which in turn is influenced by environmental temperatures and, in many species, by exposure to solar radiation. The biophysical drivers of body temperature have been widely studied, but we lack an integrative synthesis of actual body temperatures experienced in the field, and their relationships to environmental temperatures, across phylogeny, behaviour, and climate.
Location: Global (25 countries on six continents).
Taxa: Squamates (210 species, representing 25 families).
Methods: We measured the body temperatures of 20,231 individuals of squamates in the field while they were active. We examined how body temperatures vary with substrate and air temperatures across taxa, climates, and behaviours (basking and diel activity).
Results: Heliothermic lizards had the highest body temperatures. Their body temperatures were the most weakly correlated with substrate and air temperatures. Body temperatures of non-heliothermic diurnal lizards were similar to heliotherms in relation to air temperature, but similar to nocturnal species in relation to substrate temperatures. The correlation of body temperature with air and substrate temperatures was stronger in diurnal snakes and non-heliothermic lizards than in heliotherms. Body-substrate and body-air temperature correlations varied with mean annual temperatures in all diurnal squamates, especially in heliotherms. Thermal relations vary with behaviour (heliothermy, nocturnality) in cold climates but converge toward the same relation in warm climates. Non-heliotherms and nocturnal species body temperatures are better explained by substrate temperature than by air temperature. Body temperature distributions become left-skewed in warmer-bodied species, especially in colder climates.
Main conclusions: Squamate body temperatures, their frequency distributions, and their relation to environmental temperature, are globally influenced by behavioural and climatic factors. For all temperatures and climates, heliothermic species’ body temperatures are consistently higher and more stable than in other species, but in regions with warmer climate these differences become less pronounced. A comparable variation was found in non-heliotherms, but in not nocturnal species whose body temperatures were similar to air and substrate irrespective of the macroclimatic context.
... The transition between a unimodal and a bimodal pattern shows that lizards modify their behaviour in a plastic manner along a temporal axis, possibly because other behavioural options, such as posture modification, have already been depleted [100,101]. Similarly, species in wide altitudinal gradients rely on behavioural thermoregulation, modifying hourly activity [38,102]. T. spinulosus showed low activity levels when operative temperatures were outside the species' preferred range, which coincides with the pattern found in other ectotherms [103,104]. This finding suggests that high temperatures may constrain activity, as predicted by "medium constraint" theoretical models, which postulate restricted activity within the Tset boundaries [8, 105,106]. ...
Sexual selection often shapes social behavioural activities, such as movement in the environment to find possible partners, performance of displays to signal dominance and courtship behaviours. Such activities may be negatively influenced by increasing temperatures, especially in ectotherms, because individuals either have to withstand the unfavourable condition or are forced to allocate more time to thermoregulation by increasing shelter seeking behaviour. Thus, they “miss” opportunities for social and reproductive interactions. Moreover, behavioural displays of ectotherms closely depend on temperature; consequently, mate choice behaviours may be disrupted, ultimately modifying sexual selection patterns. Therefore, it would be interesting to elucidate how increasing temperatures associated with global warming may influence activity and social interactions in the species’ natural habitat and, specifically how high temperatures may modify intersexual interactions. Consequently, our aim was to explore differences in the daily pattern of social interactions in an ectotherm model, Tropidurus spinulosus, in two thermally different habitats and to determine how high temperatures modify mate choice. High environmental temperatures were found to be associated with a bimodal pattern in daily activity, which was closely linked to the daily variations in the thermal quality of the habitat; whereas the pattern and frequency of social displays showed less plasticity. The time allocated to mate choice generally decreased with increasing temperature since individuals increased the use of thermal refuges; this result supports the hypothesis of “missed opportunities”. Moreover, at high temperatures, both sexes showed changes in mate selection dynamics, with females possibly “rushing” mate choice and males showing an increase in intermale variability of reproductive displays. In our ectotherm model, plastic adjustments in the behavioural activity pattern induced by high temperatures, plus the modification of the displays during courtship may ultimately modify mate choice patterns and sexual selection dynamics.
... mantids (Hurd et al., 2020), and some species of lizards (Theisinger et al., 2017). ...
Species have different requirements for the habitat in which they live, depending on various biotic and abiotic factors. For sedentary predators such as antlion larvae, both factors are essential. In this study, we examined the preferred habitat choice concerning two abiotic factors, i.e., substrate and illumination, in two pit‐building antlions, Euroleon nostras and Myrmeleon formicarius , to determine whether choice changes during con‐ or heterospecific interactions. Both species preferred medium sand grains, i.e., 230–540 μm but differed in their choice of illumination. E. nostras preferred shade, while M. formicarius chose the illuminated part of the container. However, the choice changed, especially for M. formicarius during interactions with another individual. Abiotic factors took precedence over biotic factors in the choice of E. nostras when interactions were involved . M. formicarius avoided interactions and built pits in less suitable conditions when suitable locations were already occupied. The results can be applied to the species' natural habitat and life traits. We can confirm that E. nostras is a more competitive species when it comes to providing the most suitable abiotic conditions in the habitat for pit construction.
... Alternatively, short-term phenotypic plasticity in lizards in response to higher temperatures (heat hardening) can have multiple negative phenotypic side effects (e.g., Gilbert and Miles 2019). Likewise, behavioral shifts in response to elevated temperatures carry negative physiological consequences in lizards that can seriously impact fitness (e.g., Theisinger et al. 2017). ...
Global climate change has profound effects on species, especially those in habitats already altered by humans. Tropical ectotherms are predicted to be at high risk from global temperature increases, particularly those adapted to cooler temperatures at higher altitudes. We investigated how one such species, the water anole (Anolis aquaticus), is affected by temperature stress similar to that of a warming climate across a gradient of human-altered habitats at high elevation sites. We conducted a field survey on thermal traits and measured lizard critical thermal maxima across the sites. From the field survey, we found that (1) lizards from the least disturbed site and (2) operative temperature models of lizards placed in the least disturbed site had lower temperatures than those from sites with histories of human disturbance. Individuals from the least disturbed site also demonstrated greater tolerance to high temperatures than those from the more disturbed sites, in both their critical thermal maxima and the time spent at high temperatures prior to reaching critical thermal maxima. Our results demonstrate within-species variability in responses to high temperatures, depending on habitat type, and provide insight into how tropical reptiles may fare in a warming world.
... However, S. grammicus lizards are larger in the warmer elevations with higher whole organism RMR, and rather appear to lower energetic costs by lowering mass specific RMR, whereas S. grammicus at high (cold) elevations are much smaller (Table 1; see also Díaz de la Vega-Pérez et al. 2019) with lower whole organism RMR. Growth may be restricted by limited food abundance and short thermal windows for foraging at high elevations (Jin et al. 2007;Theisinger et al. 2017) and a small body size in ectotherms may favor thermoregulation by reducing heating time Žagar et al. 2018). Liolaemid lizards present smaller body size and tend to resort to herbivory at cold sites (Espinoza et al. 2004), which coincides with findings in S. grammicus that are small and include plants in their diet at the high elevation study site (Montoya-Ciriaco et al. 2020). ...
Body maintenance costs are often considered a proxy for performance in fitness traits. Maintenance energy requirements are measured as minimal metabolic rate of inactive, postabsorptive individuals in the laboratory. For mountain-dwelling species, translocation to the laboratory often means that they are also moved to another elevation. Due to physiological adaptations to local oxygen pressure, rapid elevational change can alter metabolic rate and translocation may result in erroneous estimates of body maintenance costs. In this study, we measured resting metabolic rate (RMR) of three populations of the Mesquite lizard (Sceloporus grammicus, Wiegmann 1828) at their native elevations (i.e., 2600, 3200 and 4100 m). Our results showed that at native elevations, mass specific RMR of lizards from the high elevation population (4100 m) did not differ from the RMR of the other populations (i.e., 2600 and 3200 m), whereas the lizards from the low elevation (2600 m) had lower RMR than those from the intermediate population. These results differ from a previous study in which the RMR of lizards from the same populations were reported to increase with native elevation when translocated and measured at an intermediate elevation. Hence, our results show that translocation in elevation can affect metabolic measures. We caution researchers that changes in elevation may preclude accurate measures of RMR in some animals and may therefore incorrectly predict performance of fitness-related traits.
... Dada a importância da temperatura para as reações bioquímicas, os impactos do clima são passíveis de se manifestar na maioria das funções fi siológicas. Além disso, as espécies podem apresentar plasticidade e aclimatação como mecanismos suplementares para lidar com desafi os térmicos (Theisinger et al. 2017). Temperaturas ambientais estressantes podem aumentar o custo da manutenção do metabolismo durante a dormência ou inatividade noturna e reduzir a qualidade do refúgio de termorregulação (Flesch et al. 2017). ...
Nas últimas décadas, as alterações climáticas vêm causado
impactos em sistemas naturais e humanos em todos os continentes e
oceanos. Projeções acerca do futuro são incertas, mas o aquecimento
global é passível de exceder 4,8 °C até o fi nal do século XXI. Muitos estudos têm focado em determinar os possíveis impactos das mudanças climáticas nos Lepidosauria, em uma escala global, regional e local. Neste capítulo buscamos identifi car possíveis tendências e padrões a respeito dos efeitos das mudanças climáticas nestes animais.
... This phenomenon has been particularly well studied in reptiles (Bogert, 1949;Caldwell, While, & Wapstra, 2017;Dubois, Blouin-Demers, Shipley, & Thomas, 2009;Seebacher, Grigg, & Beard, 1999). For example, it has been shown that some lizard species that occur across broad altitudinal gradients can use behavioural thermal regulation to compensate for the decrease in environmental temperature that accompanies increasing elevation (Hertz & Huey, 1981;Theisinger, Berg, & Dausmann, 2017). However, efficient behavioural thermal regulation might also constrain the evolution of other thermal physiological mechanisms that could contribute to species survival over the long term (Huey, Hertz, & Sinervo, 2003). ...
In ants, social thermal regulation is the collective maintenance of a nest temperature that is optimal for individual colony members. In the thermophilic ant Aphaenogaster iberica, two key behaviours regulate nest temperature: seasonal nest relocation and variable nest depth. Outside the nest, foragers must adapt their activity to avoid temperatures that exceed their thermal limits.
It has been suggested that social thermal regulation constrains physiological and morphological thermal adaptations at the individual level. We tested this hypothesis by examining the foraging rhythms of six populations of A. iberica, which were found at different elevations (from 100 to 2,000 m) in the Sierra Nevada mountain range of southern Spain. We tested the thermal resistance of individuals from these populations under controlled conditions.
Janzen's climatic variability hypothesis (CVH) states that greater climatic variability should select for organisms with broader temperature tolerances. We found that the A. iberica population at 1,300 m experienced the most extreme temperatures and that ants from this population had the highest heat tolerance (LT50 = 57.55°C). These results support CVH's validity at microclimatic scales, such as the one represented by the elevational gradient in this study.
Aphaenogaster iberica maintains colony food intake levels across different elevations and mean daily temperatures by shifting its rhythm of activity.
This efficient colony‐level thermal regulation and the significant differences in individual heat tolerance that we observed among the populations suggest that behaviourally controlled thermal regulation does not constrain individual physiological adaptations for coping with extreme temperatures.
... From all environmental stressors affecting growth and developmental rate in ectotherms such as anuran larvae, temperature is the most pervasive and arguably the most important (Dalvi et al., 2009;Berg et al., 2017). In ectotherms, body temperature fluctuates with ambient temperatures and the rates of most biochemical reactions and many biological processes exponentially increase with temperature (Harkey and Semlitsch, 1988;Zuo et al., 2012;Theisinger et al., 2017). Larval amphibians are especially likely to encounter variation in temperature because they live in a variety of aquatic habitats and often in shallow ephemeral ponds (Walsh et al., 2008;Yu et al., 2015) and are known to exhibit temperature-induced plasticity in growth and developmental rate as a response to temperature variation (rev. ...
Environmental stress induced by natural and anthropogenic processes including climate change may threaten the productivity of species and persistence of populations. Ectotherms can potentially cope with stressful conditions such as extremes in temperature by exhibiting physiological plasticity. Amphibian larvae experiencing stressful environments display altered thyroid hormone (TH) status with potential implications for physiological traits and acclimation capacity. We investigated how developmental temperature (Tdev) and altered TH levels (simulating proximate effects of environmental stress) influence the standard metabolic rate (SMR), body condition (BC), and thermal tolerance in metamorphic and post-metamorphic anuran larvae of the common frog (Rana temporaria) reared at five constant temperatures (14–28 °C). At metamorphosis, larvae that developed at higher temperatures had higher maximum thermal limits but narrower ranges in thermal tolerance. Mean CTmax was 37.63 °C ± 0.14 (low TH), 36.49 °C ± 0.31 (control), and 36.43 °C ± 0.68 (high TH) in larvae acclimated to different temperatures. Larvae were able to acclimate to higher Tdev by adjusting their thermal tolerance, but not their SMR, and this effect was not impaired by altered TH levels. BC was reduced by 80% (metamorphic) and by 85% (post-metamorphic) at highest Tdev. The effect of stressful larval conditions (i.e., different developmental temperatures and, to some extent, altered TH levels) on SMR and particularly on BC at the onset of metamorphosis was carried over to froglets at the end of metamorphic climax. This has far reaching consequences, since body condition at metamorphosis is known to determine metamorphic success and, thus, is indirectly linked to individual fitness in later life stages.
The physiological compensation of animals in changing environments through acclimatization has long been considered to be of minor importance in tropical ectotherms due to more stable climatic conditions compared to temperate regions. Contrasting this assumption are reports about a range of metabolic adjustments in tropical species, especially during the last two decades from field acclimatized animals. Metabolic rates are strongly linked to temperature in ectotherms but they also reflect energetic requirements and restrictions. We therefore postulate that the observed variety of acclimatization patterns in tropical reptiles results from an interaction of multiple influences, including food and water availability, rather than from thermal constraints alone. We present new data from two sympatric Malagasy lizards with contrasting acclimatization patterns and, complemented with an extensive literature search, discuss the variety of acclimatization patterns in tropical reptiles with regard to thermal and energetic influences. This broad consideration of constraints allows a rearrangement of apparently controversial patterns into a scheme of decreasing metabolic costs, including two new categories for selective and selective inverse acclimatization, where metabolic shifts are restricted to body temperatures below those preferred during activity.
Global climate change is expected to have strong effects on the world’s flora and fauna. As a result, there has been a recent increase in the number of meta-analyses and mechanistic models that attempt to predict potential responses of mammals to changing climates. Many models that seek to explain the effects of environmental temperatures on mammalian energetics and survival assume a constant body temperature. However, despite generally being regarded as strict homeotherms, mammals demonstrate a large degree of daily variability in body temperature, as well as the ability to reduce metabolic costs either by entering torpor, or by increasing body temperatures at high ambient temperatures. Often, changes in body temperature variability are unpredictable, and happen in response to immediate changes in resource abundance or temperature. In this review we provide an overview of variability and unpredictability found in body temperatures of extant mammals, identify potential blind spots in the current literature, and discuss options for incorporating variability into predictive mechanistic models.
Body temperatures were positively correlated with corresponding mean air temperatures but were most elevated above ambient temperatures during cool early spring months. In early spring, body temperatures were considerably lower than those that the animals maintained in a laboratory thermal gradient (selected temperatures). During the colder months, time of activity was restricted, and lizards increased basking frequency and actively sought warmer microhabitats. A biophysical model was used to calculate equilibrium temperatures that a lizard could achieve by maximizing or minimizing its heat gain. Lizards regulated body temperatures near selected levels, or if these could not be achieved for physical reasons, they regulated near maximal operative temperatures. During the coolest periods, activity was highest in adult males. A main benefit of thermoregulation under these suboptimal conditions may be the maximization of mating success, through an increase of the rate of sperm development. -from Authors
Understanding how climate change affects natural populations remains one of the greatest challenges for ecology and management of natural resources. Animals can remodel their physiology to compensate for the effects of temperature variation, and this physiological plasticity, or acclimation, can confer resilience to climate change. The current lack of a comprehensive analysis of the capacity for physiological plasticity across taxonomic groups and geographic regions, however, constrains predictions of the impacts of climate change. Here, we assembled the largest database to date to establish the current state of knowledge of physiological plasticity in ectothermic animals. We show that acclimation decreases the sensitivity to temperature and climate change of freshwater and marine animals, but less so in terrestrial animals. Animals from more stable environments have greater capacity for acclimation, and there is a significant trend showing that the capacity for thermal acclimation increases with decreasing latitude. Despite the capacity for acclimation, climate change over the past 20 years has already resulted in increased physiological rates of up to 20%, and we predict further future increases under climate change. The generality of these predictions is limited, however, because much of the world is drastically undersampled in the literature, and these undersampled regions are the areas of greatest need for future research efforts.
Nocturnal geckos are active with body temperatures (Tb) that are low and variable relative to those of diurnal lizards. If the physiology of geckos is evolutionarily adapted to these low and variable Tb's, then the physiology of geckos should function best at relatively low and variable temperatures. In fact, optimal temperatures and performance breadths for sprinting of several geckos (Coleonyx brevis, C. variegatus, Hemidactylus frenatus, H. turcicus, Lepidodactylus lugubris) do not differ substantially from those of diurnal lizards from other families. As a result geckos normally forage at night at Tb's that should be suboptimal for sprinting. Potential evolutionary explanations (eg evolutionary inertia of thermal physiology, possible selection pressures favouring high optimal temperatures) for the similarity of the thermal dependence of sprinting of geckos and diurnal lizards are evaluated. -from Authors
In conclusion, our results show a close relationship and
high accuracy between Tsk and Tb in lizards of different body
sizes and thus a high applicability of both methods, ETLs and
IRTs. Considerable differences between Tsk and Tb occurred only
during phases of intense changes in Tb, and were detectable even
in lizards with a BM of ~20 g, suggesting that the thermal inertia
depends not only on body size but also on the rate of heating.
Both methods proved to be easy to use under field conditions
if certain limitations are considered. We therefore generally
validate the use of Tsk measurements as surrogates for cloacal
Tb measurements in small to medium sized reptiles (20–120 g)
also for field studies, but have to emphasize the importance of
restrictions related to the rate of heating, which is not necessarily
apparent under standardized lab conditions. The increasing
application of IRTs and other external measurements of body
temperature in reptiles will expand the potential of field studies
by facilitating repeated temperature records of undisturbed
animals, larger sample sizes and the collection of data over
several days including night times and in retreat sites.
Global warming is increasing the overheating risk for many organisms, though the potential for plasticity in thermal tolerance to mitigate this risk is largely unknown. In part, this shortcoming stems from a lack of knowledge about global and taxonomic patterns of variation in tolerance plasticity. To address this critical issue, we test leading hypotheses for broad-scale variation in ectotherm tolerance plasticity using a dataset that includes vertebrate and invertebrate taxa from terrestrial, freshwater and marine habitats. Contrary to expectation, plasticity in heat tolerance was unrelated to latitude or thermal seasonality. However, plasticity in cold tolerance is associated with thermal seasonality in some habitat types. In addition, aquatic taxa have approximately twice the plasticity of terrestrial taxa. Based on the observed patterns of variation in tolerance plasticity, we propose that limited potential for behavioural plasticity (i.e. behavioural thermoregulation) favours the evolution of greater plasticity in physiological traits, consistent with the 'Bogert effect'. Finally, we find that all ectotherms have relatively low acclimation in thermal tolerance and demonstrate that overheating risk will be minimally reduced by acclimation in even the most plastic groups. Our analysis indicates that behavioural and evolutionary mechanisms will be critical in allowing ectotherms to buffer themselves from extreme temperatures.
© 2015 The Author(s) Published by the Royal Society. All rights reserved.
We determined diurnal and seasonal patterns of body temperature ( T b) in Crocodylus johnstoni in the wild by monitoring T b and behavior of 15 crocodiles, as well as measuring water, air and ground temperatures, and solar radiation. Two fundamentally different diurnal patterns of T b occurred. One (pattern A) was similar to that described as typical for thermoregulating heliothermic reptiles, in that crocodiles shuttled between basking on land and cooling in water so that T b formed a plateau elevated above water temperature (Tw) during the day. In the other (pattern B), crocodiles did not leave the water, and T b equalled T w throughout the day. Some crocodiles showed either pattern A or pattern B throughout the year, and some behaved differently at different seasons. The preferred body temperature range (PBTR) of those crocodiles that thermoregulated for all or most of the year changed seasonally, parallelling seasonal changes in T w. The midpoint of the PBTR changed from approximately 29 C to 33 C, winter to summer. Intraspecific aggression prevented some crocodiles from thermoregulating effectively, and their PBTR was significantly lower when experiencing aggression from other crocodiles, compared with when undisturbed.
The impact of anthropogenic climate change on terrestrial organisms is often predicted to increase with latitude, in parallel with the rate of warming. Yet the biological impact of rising temperatures also depends on the physiological sensitivity of organisms to temperature change. We integrate empirical fitness curves describing the thermal tolerance of terrestrial insects from around the world with the projected geographic distribution of climate change for the next century to estimate the direct impact of warming on insect fitness across latitude. The results show that warming in the tropics, although relatively small in magnitude, is likely to have the most deleterious consequences because tropical insects are relatively sensitive to temperature change and are currently living very close to their optimal temperature. In contrast, species at higher latitudes have broader thermal tolerance and are living in climates that are currently cooler than their physiological optima, so that warming may even enhance their fitness. Available thermal tolerance data for several vertebrate taxa exhibit similar patterns, suggesting that these results are general for terrestrial ectotherms. Our analyses imply that, in the absence of ameliorating factors such as migration and adaptation, the greatest extinction risks from global warming may be in the tropics, where biological diversity is also greatest.
• biodiversity
• fitness
• global warming
• physiology
• tropical
Thermal trait variation is of fundamental importance to forecasting the impacts of environmental change on lizard diversity. Here, we review the literature for patterns of variation in traits of upper and lower sub-lethal temperature limits, temperature preference and active body temperature in the field, in relation to space, time and phylogeny. Through time, we focus on the direction and magnitude of trait change within days, among seasons and as a consequence of acclimation. Across space, we examine altitudinal and latitudinal patterns, incorporating inter-specific analyses at regional and global scales. This synthesis highlights the consistency or lack thereof, of thermal trait responses, the relative magnitude of change among traits and several knowledge gaps identified in the relationships examined. We suggest that physiological information is becoming essential for forecasting environmental change sensitivity of lizards by providing estimates of plasticity and evolutionary scope.
We investigated whether the thermal history of Black Rat Snakes (Elaphe obsoleta) and Northern Water Snakes (Nerodia sipedon) during development affected their preferred body temperatures (PBT) after hatching or birth. Eggs of black rat snakes were incubated at high or low temperatures. Gravid female water snakes were main- tained in rooms under low, medium, or high ambient temperatures. PBT of neonates were measured in a controlled thermal gradient. We only found plasticity in PBT with developmental temperature for northern water snakes, where offspring that developed under warmer temperatures demonstrated a significant preference for warmer temperatures. Our results suggest that PBT are plastic in only some species of snakes and may explain some of the individual variation in PBT observed in adult snakes.
We studied the impact of restrictions by the thermal environments on body temperatures (Tbs) and microhabitat use of the lacertid lizards Podarcis melisellensis and Podarcis muralis in a Mediterranean area (Croatia) during autumn. The thermal conditions at available microhabitats were assessed with copper models that measured the operative temperatures (Te) at different sites. We estimated the thermal suitability of microhabitats by quantifying the extent of similarity between the Tes and the range of selected temperatures (i.e., the Tbs that lizards maintain in zero-cost conditions in a laboratory thermogradient; Tsel). Both species maintained, throughout most of day, Tbs that were on average 2–4 C below both Tsel and the Tbs recorded in the field during summer. Nevertheless, the Tbs measured during autumn were in the upper range of available Tes and were much closer to the Tsel than were the Tes. In addition, lizards were most often observed in the warmest microhabitats and were often seen basking. These results indicate that lizards were actively thermoregulating. The Te measurements show that lizards encounter suitable thermal conditions (i.e., where Tes is within Tsel) in only a restricted subset of the available microhabitats and during only a relatively short period of the day. Thus, lizards are constrained to maintain relatively low Tbs during autumn by the generally low available Tes. Although lizards were clearly thermoregulating, they appeared to accept lower Tbs during activity in autumn than in summer. A possible reason for this seasonal shift in activity Tbs is that achievement of higher Tbs during autumn is only feasible by confining activities to some specific microhabitats, which may severely constrain other behaviors, such as foraging.
Behavioural regulation of body temperature in thermally heterogeneous habitats requires different amounts of time that could otherwise be dedicated to foraging and social activities. In this study I examined how four populations of the lizard Zootoca vivipara along an altitudinal gradient (250-1450 m) adjust their thermal-physiology traits and thermoregulatory behaviour to compensate for increasing time costs of thermoregulation. I focused on variation in several physiological (set-point temperature, heating rate) and behavioural traits (microhabitat selection, basking frequency, extent of thermoregulation). To estimate potential time spent basking and foraging by lizards that were not employing any behavioural compensatory mechanism, I used a simple biophysical model of thermoregulation, including information about operative temperatures at the study sites, selected temperature range, and heating/cooling rates. Time costs of thermoregulation for each population were calculated as potential time spent basking relative to time spent foraging. Operative temperatures varied among study sites, resulting in different time costs of thermoregulation. Lizards at 1450 m should spend about 50% more time basking than those at 250 m. I found that the only mechanism which potentially compensated for the higher time costs incurred at high altitudes was a shift in the choice of basking sites. Lizards thermoregulated with similar accuracy and effectiveness over the 1200-m altitudinal range, indicating that there were no adjustments in the extent of thermoregulation. The observed basking frequencies of lizards were highly correlated with potential time spent basking without behavioural adjustments, suggesting a minor compensatory effect of thermoregulatory behaviour. Lizards responded to higher time costs of thermoregulation primarily by allocating different amounts of time to basking. These results suggest that Z. vivipara regulated body temperature at the expense of time that could be devoted to other activities.
The measurement of metabolic rates is important in many areas of science. Examples range from ecology through a broad spectrum of physiological disciplines to biomedical fields such as genetic screening, obesity, and trauma research. The organisms being measured range in size from bacteria through insects to whales, and many different measurement methodologies have developed over the years, most of which are famously difficult for the novice to master. This book covers a wide range of metabolic measurement techniques, giving background and applications information for each, with enough practical detail to allow for accurate and informed measurements with minimal trial-and-error. Much tribal wisdom, passed down from professors to students and between scientific peers, is included. A broad range of techniques is covered, including Gilson and Warburg respirometry and their modern derivatives; direct calorimetry; stable isotope work; coulometric respirometry; aquatic respirometry; and practically every variation of field and laboratory flow-through respirometry, including complex, computer-driven multi-animal systems. Characteristics of the different varieties of gas analyzers, flow measurement systems, and so on are evaluated in detail. The book brings to the task over two decades of experience in practically every type of respirometry, from laboratory settings to the jungles of Panama and the deserts of Namibia.
It is predicted that climate change will cause species extinctions and distributional shifts in coming decades, but data to
validate these predictions are relatively scarce. Here, we compare recent and historical surveys for 48 Mexican lizard species
at 200 sites. Since 1975, 12% of local populations have gone extinct. We verified physiological models of extinction risk
with observed local extinctions and extended projections worldwide. Since 1975, we estimate that 4% of local populations have
gone extinct worldwide, but by 2080 local extinctions are projected to reach 39% worldwide, and species extinctions may reach
20%. Global extinction projections were validated with local extinctions observed from 1975 to 2009 for regional biotas on
four other continents, suggesting that lizards have already crossed a threshold for extinctions caused by climate change.
Abstract The predominant view is that the thermal physiology of tropical ectotherms, including lizards, is not labile over ecological timescales. We used the recent introduction (∼35 years ago) of the Puerto Rican lizard Anolis cristatellus to Miami, Florida, to test this thermal rigidity hypothesis. We measured lower (critical thermal minimum [CT(min)]) and upper (critical thermal maximum [CT(max)]) thermal tolerances and found that the introduced population tolerates significantly colder temperatures (by ∼3°C) than does the Puerto Rican source population; however, CT(max) did not differ. These results mirror the thermal regimes experienced by each population: Miami reaches colder ambient temperatures than Puerto Rico, but maximum ambient temperatures are similar. The differences in CT(min) were observed even though lizards from both sites experienced nearly identical conditions for 49 days before CT(min) measurement. Our results demonstrate that changes in thermal tolerance occurred relatively rapidly (∼35 generations), which strongly suggests that the thermal physiology of tropical lizards is more labile than previously proposed.
We studied the thermal consequences of microhabitat selection by Psammodromus algirus lizards by combining data on the frequency of use and relative availability of three different types of microhabitats, with information about the environmental operative temperatures, and their deviations from the lizards' selected thermal range, available in these microhabitats. In both seasons, lizards preferred holm oak shrubs and avoided rockrose shrubs and open areas. However, the thermal suitability of holm oaks was highest in July but lowest in May. We suggest that microhabitat preferences were more related to other aspects of lizard ecology (e.g. antipredator behaviour) than to thermal requirements.
The fundamental niche can be viewed as the set of conditions and resources that allow a given organism to survive and reproduce in the absence of biotic interactions. Quantitative descriptions of the environmental variables with which organisms are asso-ciated are becoming common with the advent of geographic information systems (GIS). Although such descriptive approaches to the niche are useful for interpolating species distributions, they implicitly incorporate biotic interactions and therefore do not represent the fundamental niche. A mechanistic understanding of the fundamental niche, when com-bined with GIS data, can provide us with greater insight into the causes of distribution and abundance, a solid foundation for exploring the role of biotic interactions, and greater confidence in extrapolating to novel circumstances such as climate change and species introductions. We apply such a mechanistic approach to study the climatic component of the fundamental niche of a nocturnal lizard, Heteronotia binoei, across an entire continent. We combine physiological measurements of this species (thermal requirements for egg development, thermal preferences and tolerances, metabolic and evaporative water loss rates), and high-resolution climatic data for the Australian continent (air temperature, cloud cover, wind speed, humidity, and radiation), with biophysical models to calculate the cli-matic component of the fundamental niche of this lizard and map it onto the Australian landscape at high resolution. We also use this approach to predict the effects of a mild global warming on the degree-days in the soil for egg development and the potential for aboveground activity of the study organism.
We studied, in the field and laboratory, aspects of the thermal biology in two populations of the lizard Podarcis tiliguerta along a 1450 m altitudinal gradient. Body temperatures (Tb) at high altitudes average lower, are more variable, but are more elevated above environmental temperatures than at sea level. Lizards partially reduced the impact of altitudinal changes in thermal loads through presumable subtle behavioural adjustments. A comparison of the thermal preferences in the laboratory, the maximal operative temperatures predicted from a biophysical model, and the activity Tb's at both sites, indicates that the main response to changing environmental conditions is an active shift in thermoregulatory set points. Integration of field Tb's and laboratory data on temperature specific sprint speeds, predicts that the mountainous lizards experience reduced running abilities that are especially acute in the early morning. Despite this impairment of running performance, the thermal sensitivity of running speed has not evolved to match the Tb's experienced by both populations. This result supports the view that the thermal physiology of this lizard is evolutionarily conservative, but the lack of information on the relation between running performance and fitness components impedes rejection of alternative hypotheses.
In the last two decades, interest in species distribution models (SDMs) of plants and animals has grown dramatically. Recent advances in SDMs allow us to potentially forecast anthropogenic effects on patterns of biodiversity at different spatial scales. However, some limitations still preclude the use of SDMs in many theoretical and practical applications. Here, we provide an overview of recent advances in this field, discuss the ecological principles and assumptions underpinning SDMs, and highlight critical limitations and decisions inherent in the construction and evaluation of SDMs. Particular emphasis is given to the use of SDMs for the assessment of climate change impacts and conservation management issues. We suggest new avenues for incorporating species migration, population dynamics, biotic interactions and community ecology into SDMs at multiple spatial scales. Addressing all these issues requires a better integration of SDMs with ecological theory.
A recently developed integrative framework proposes that the vulnerability of a species to environmental change depends on the species' exposure and sensitivity to environmental change, its resilience to perturbations and its potential to adapt to change. These vulnerability criteria require behavioural, physiological and genetic data. With this information in hand, biologists can predict organisms most at risk from environmental change. Biologists and managers can then target organisms and habitats most at risk. Unfortunately, the required data (e.g. optimal physiological temperatures) are rarely available. Here, we evaluate the reliability of potential proxies (e.g. critical temperatures) that are often available for some groups. Several proxies for ectotherms are promising, but analogous ones for endotherms are lacking. We also develop a simple graphical model of how behavioural thermoregulation, acclimation and adaptation may interact to influence vulnerability over time. After considering this model together with the proxies available for physiological sensitivity to climate change, we conclude that ectotherms sharing vulnerability traits seem concentrated in lowland tropical forests. Their vulnerability may be exacerbated by negative biotic interactions. Whether tropical forest (or other) species can adapt to warming environments is unclear, as genetic and selective data are scant. Nevertheless, the prospects for tropical forest ectotherms appear grim.
Diet composition can affect body temperatures selected by lizards in a thermal gradient (SBT) but there is very little evidence to support a similar effect due to fasting. The latter could represent a means of energy conservation during periods of low food availability. This study investigated the impact of short-term food deprivation (5 days) on diurnal thermal preferences of male (n=10) and non-reproductive female (n=22) Anolis carolinensis using a repeated measures design. Mean SBT varied significantly over the 4 h measurement period, and was higher for males than females, overall. A small but significant change in SBT was detected between the two feeding treatments, with food deprivation leading to a mean decrease ranging from 0.43±0.55 to 0.72±0.46 °C (at different times of day) in females and from 0.61±0.71 to 2.13±0.76 °C in males. Previous studies may have failed to detect such subtle trends due to a lack of statistical power arising from small sample sizes. An explanation of these differences is they represent a feeding status dependent trade-off for maintenance of energy balance versus optimal food assimilation. However, (1) the estimated energy saving, and (2) the impact on food assimilation appear rather negligible even assuming that the observed decrease in SBT produces a similar lowering of field body temperature in the wild.
Metabolic rates of the western fence lizard Sceloporus occidentalis (Sauria: Iguanidae) were measured in the laboratory by gas exchange, and in the field with doubly labeled H 2 O. Field metabolic rates of adults during the spring reproductive season (0.22 ml CO 2 g — ¹ h — ¹ or 141.4j g — ¹ day — ¹ ) were not different from those during the fall nonreproductive season (0.20 ml CO 2 g — ¹ h — ¹ or 127.2j g — ¹ day — ¹ ). Field and laboratory metabolic rates of @V @V were not different from those of ♀ ♀ in spring or fall. Average daily field metabolic rates were 2.0 to 2.5 x resting laboratory rates measured on a simulated normal thermal cycle; estimated rates during the field activity period were 2.5 to 3.1 x resting levels measured at 35°C. Only 11 to 17% of total daily energy expenditure was used while lizards were inactive in their burrows. Daily field metabolism of this lizard is only 3 to 4% that of a bird or mammal of equal size.
We compared preferred body temperatures, critical thermal minima, and maxima, and tolerance ranges among four populations of Zootoca vivipara (formerly Lacerta vivipara) distributed along an altitudinal gradient (250-1450 m) to examine whether different thermal environments have induced a change in these thermal characteristics. Lizards in all populations had similar preferred body temperatures and critical thermal limits, suggesting that acclimation or adaptation of these traits to different thermal environments did not occur. Subadult females and gravid females preferred lower body temperatures than nongravid females and subadult and adult males. Preferred body temperatures differed among individuals of the same age and sex within a particular population. In contrast to the negligible among-population variation, preferred body temperatures varied considerably within populations in Z. vivipara
Thermoregulatory behaviour represents an important component of ectotherm non-genetic adaptive capacity that mitigates the impact of ongoing climate change. The buffering role of behavioural thermoregulation has been attributed solely to the ability to maintain near optimal body temperature for sufficiently extended periods under altered thermal conditions. The widespread occurrence of plastic modification of target temperatures that an ectotherm aims to achieve (preferred body temperatures) has been largely overlooked. I argue that plasticity of target temperatures may significantly contribute to an ectotherm's adaptive capacity. Its contribution to population persistence depends on both the effectiveness of acute thermoregulatory adjustments (reactivity) in buffering selection pressures in a changing thermal environment, and the total costs of thermoregulation (i.e. reactivity and plasticity) in a given environment. The direction and magnitude of plastic shifts in preferred body temperatures can be incorporated into mechanistic models, to improve predictions of the impact of global climate change on ectotherm populations.
Synopsis In 1967 Daniel Janzen published an influential paper titled "Why Mountain Passes Are Higher in the Tropics." Janzen derived a simple climatic-physiological model predicting that tropical mountain passes would be more effective barriers to organismal dispersal than would temperate-zone passes of equivalent altitude. This prediction derived from a recognition that the annual variation in ambient temperature at any site is relatively low in the tropics. Such low variation within sites not only reduces the seasonal overlap in thermal regimes between low- and high-altitude sites, but should also select for organisms with narrow physiological tolerances to temperature. As a result, Janzen predicted that tropical lowland organisms are more likely to encounter a mountain pass as a physiological barrier to dispersal (hence "higher"), which should in turn favor smaller distributions and an increase in species turnover along altitudinal gradients. This synthetic hypothesis has long been at the center of discussions of latitudinal patterns of physiological adaptation and of species diversity. Here we review some of the key assumptions and predictions of Janzen's hypothesis. We find general support for many assumptions and predictions, but call attention to several issues that somewhat ameliorate the generality of Janzen's classic hypothesis.
Mobile ectothermic animals can control their body temperatures by selecting specific thermal conditions in the environment, but embryos--trapped within an immobile egg and lacking locomotor structures--have been assumed to lack that ability. Falsifying that assumption, our experimental studies show that even early stage turtle embryos move within the egg to exploit small-scale spatial thermal heterogeneity. Behavioral thermoregulation is not restricted to posthatching life and instead may be an important tactic in every life-history stage.
Biological impacts of climate warming are predicted to increase with latitude, paralleling increases in warming. However, the magnitude of impacts depends not only on the degree of warming but also on the number of species at risk, their physiological sensitivity to warming and their options for behavioural and physiological compensation. Lizards are useful for evaluating risks of warming because their thermal biology is well studied. We conducted macrophysiological analyses of diurnal lizards from diverse latitudes plus focal species analyses of Puerto Rican Anolis and Sphaerodactyus. Although tropical lowland lizards live in environments that are warm all year, macrophysiological analyses indicate that some tropical lineages (thermoconformers that live in forests) are active at low body temperature and are intolerant of warm temperatures. Focal species analyses show that some tropical forest lizards were already experiencing stressful body temperatures in summer when studied several decades ago. Simulations suggest that warming will not only further depress their physiological performance in summer, but will also enable warm-adapted, open-habitat competitors and predators to invade forests. Forest lizards are key components of tropical ecosystems, but appear vulnerable to the cascading physiological and ecological effects of climate warming, even though rates of tropical warming may be relatively low.
Increasing concern about the impacts of global warming on biodiversity has stimulated extensive discussion, but methods to translate broad-scale shifts in climate into direct impacts on living animals remain simplistic. A key missing element from models of climatic change impacts on animals is the buffering influence of behavioral thermoregulation. Here, we show how behavioral and mass/energy balance models can be combined with spatial data on climate, topography, and vegetation to predict impacts of increased air temperature on thermoregulating ectotherms such as reptiles and insects (a large portion of global biodiversity). We show that for most "cold-blooded" terrestrial animals, the primary thermal challenge is not to attain high body temperatures (although this is important in temperate environments) but to stay cool (particularly in tropical and desert areas, where ectotherm biodiversity is greatest). The impact of climate warming on thermoregulating ectotherms will depend critically on how changes in vegetation cover alter the availability of shade as well as the animals' capacities to alter their seasonal timing of activity and reproduction. Warmer environments also may increase maintenance energy costs while simultaneously constraining activity time, putting pressure on mass and energy budgets. Energy- and mass-balance models provide a general method to integrate the complexity of these direct interactions between organisms and climate into spatial predictions of the impact of climate change on biodiversity. This methodology allows quantitative organism- and habitat-specific assessments of climate change impacts.
Thermochron iButtons are being used increasingly by animal physiologists to measure long-term patterns of body temperature in reptiles, birds and mammals. Typically, iButtons are surgically implanted into the intraperitoneal cavity where they measure and store body temperature together with the date and time from an onboard real-time clock. In 16-bit resolution, the DS1922L iButton can store a total of 4,096 data points over pre-determined sampling intervals. iButtons have proved invaluable in measuring patterns of torpor and hibernation in animals larger than 70 g. Weighing around 3.5 g after potting with wax, iButtons are too heavy and large to implant into animals smaller than 70 g because their weight exceeds 5% of the animal's total body weight. This paper describes how the stainless steel canister housing the DS 1922L iButton battery and circuit board can be removed to reduce the weight of the components to 1.49 g after waxing (ready for implantation) without compromising the function or battery life of the iButton. The modified iButton can be implanted into animals as small as 20-30 g. Calibration data revealed an offset of ca. 1 degrees C on average, confirming that iButtons must be calibrated prior to implantation.
Behavioural regulation of body temperature in thermally heterogeneous habitats requires different amounts of time that could otherwise be dedicated to foraging and social activities. In this study I examined how four populations of the lizard Zootoca vivipara along an altitudinal gradient (250-1450 m) adjust their thermal-physiology traits and thermoregulatory behaviour to compensate for increasing time costs of thermoregulation. I focused on variation in several physiological (set-point temperature, heating rate) and behavioural traits (microhabitat selection, basking frequency, extent of thermoregulation). To estimate potential time spent basking and foraging by lizards that were not employing any behavioural compensatory mechanism, I used a simple biophysical model of thermoregulation, including information about operative temperatures at the study sites, selected temperature range, and heating/cooling rates. Time costs of thermoregulation for each population were calculated as potential time spent basking relative to time spent foraging. Operative temperatures varied among study sites, resulting in different time costs of thermoregulation. Lizards at 1450 m should spend about 50% more time basking than those at 250 m. I found that the only mechanism which potentially compensated for the higher time costs incurred at high altitudes was a shift in the choice of basking sites. Lizards thermoregulated with similar accuracy and effectiveness over the 1200-m altitudinal range, indicating that there were no adjustments in the extent of thermoregulation. The observed basking frequencies of lizards were highly correlated with potential time spent basking without behavioural adjustments, suggesting a minor compensatory effect of thermoregulatory behaviour. Lizards responded to higher time costs of thermoregulation primarily by allocating different amounts of time to basking. These results suggest that Z. vivipara regulated body temperature at the expense of time that could be devoted to other activities.
Temperature pervasively impacts the phenotypes and distributions of organisms. These thermal effects generate strong selective pressures on behaviour, physiology, and life history when environmental temperatures vary over space and time. Despite this fact, progress toward a quantitative theory of thermal adaptation has lagged behind empirical descriptions of patterns and processes. This book draws on current evolutionary paradigms (optimization, quantitative genetics, and genetic algorithms) to establish a theory of thermal adaptation. It initially focuses on simple models that describe the evolution of thermosensitivity, thermoregulation, or acclimation. Later chapters focus on more complex models describing the coadaptation of traits or the coevolution of species. Throughout the book, various lines of evidence are used to question the major assumptions of these models. Furthermore, the predictions of these models are confronted with experimental and comparative data. Empirical examples represent a wide range of taxa, including bacteria, plants, fungi, and animals. The result is a synthesis of theoretical and empirical studies of thermal biology that offers insights about evolutionary processes.
Standard metabolic rates (SMR) are frequently used to estimate the maintenance costs of free-ranging ectotherms. Ecologically relevant sources of variation in the rate of metabolism not accounted for by SMR (e.g. nutritional status, time of day) can significantly affect estimates of the maintenance costs of free-ranging ectotherms. This study reports the effects of temperature, sex, population and time of day on the rate of oxygen consumption of resting Sceloporus merriami. The rate of oxygen consumption of fasted lizards (standard conditions) was strongly dependent on temperature, sex and population, and it was not constant over the inactive period (scotophase). Average rates of oxygen consumption were as much as four times higher than the minimal rate (SMR) for all individuals. Our results indicate that the cost of maintenance of S. merriami calculated using SMR is from two to four times lower than the cost estimated from the average rates of oxygen consumption of fasted lizards. These results have important implications for ecologists interested in comparing lizard productivity with similarly sized endotherms. Rates of oxygen consumption at 32 and 37-degrees-C increased by as much as 37% after lizards were fed 10-15% of their live mass in crickets. This effect was not observed at 25-degrees-C. Because oxygen consumption is not constant over the scotophase and because free-ranging lizards usually have food in their guts, we conclude that when estimating the energy budgets of free-ranging lizards ecologists should use the rate of oxygen consumption averaged over the scotophase of fed animals, not SMR.
In recent years, ecologists have stepped up to address the challenges imposed by rapidly changing climates. Some researchers have developed niche-based methods to predict how species will shift their ranges. Such methods have evolved rapidly, resulting in models that incorporate physiological and behavioral mechanisms. Despite their sophistication, these models fail to account for environmental heterogeneity at the scale of an organism. We used an individual-based model to quantify the effects of operative environmental temperatures, as well as their heterogeneity and spatial structure, on the thermoregulation, movement, and energetics of ectotherms. Our simulations showed that heterogeneity and spatial structure of a thermal landscape is as important as its mean temperature. In fact, temperature and heterogeneity interact to determine organismal performance. Consequently, the popular index of environmental quality (de), which ignores variance and spatial structure, is inherently flawed as a descriptor of thermal quality of an environment. Future efforts to model species' distributions should link thermoregulation and activity to environmental heterogeneity at fine scales.
Modelling thermal environments at high resolution becomes simpler when using operative temperature, which condenses microclimate and morphology into an index of thermal stress. Operative temperature can be mapped using large numbers of ‘operative temperature thermometers’, hollow models that duplicate external properties of the animal.
As climatologists predict that air will warm by 2–4 °C by 2100, biologists must be able to distinguish climate change from systematic errors in operative temperature of the same magnitude.
A systematic error in operative temperature of 2 °C or a similar amount of climate warming can change predicted surface activity and indices of habitat quality, thermoregulatory precision and predation risk by 5–12%, and in some cases more than 30%.
As construction details of operative temperature thermometers can affect their accuracy by 2 °C or more, biologists should use detailed physical models calibrated against living animals over potential ranges of postures, orientations and microclimates.
Water‐filled models do not measure operative temperature correctly, fail to capture thermal extremes and are an unnecessary complication as one can easily compute the body temperature of moving or stationary animals from body mass and the spatio‐temporal distribution of operative temperatures .
Temperature profoundly affects the rate and trajectory of embryonic development, and thermal extremes can be fatal. In viviparous species, maternal behaviour and physiology can buffer the embryo from thermal fluctuations; but in oviparous animals (like most reptiles and all birds), an embryo is likely to encounter unpredictable periods when incubation temperatures are unfavourable. Thus, we might expect natural selection to have favoured traits that enable embryos to maintain development despite those fluctuations. Our review of recent research identifies three main routes that embryos use in this way. Extreme temperatures (i) can be avoided (e.g. by accelerating hatching, by moving within the egg, by cooling the egg by enhanced rates of evaporation, or by hysteresis in rates of heating versus cooling); (ii) can be tolerated (e.g. by entering diapause, by producing heat-shock proteins, or by changing oxygen use); or (iii) the embryo can adjust its physiology and/or developmental trajectory in ways that reduce the fitness penalties of unfavourable thermal conditions (e.g. by acclimating, by exploiting brief windows of favourable conditions, or by producing the hatchling phenotype best suited to those incubation conditions). Embryos are not simply passive victims of ambient conditions. Like free-living stages of the life cycle, embryos exhibit behavioural and physiological plasticity that enables them to deal with unpredictable abiotic challenges.
Correlative analyses predict that anthropogenic climate warming will cause widespread extinction but the nature and generality of the underlying mechanisms is unclear. Warming-induced activity restriction has been proposed as a general explanatory mechanism for recent population extinctions in lizards, and has been used to forecast future extinction. Here, I test this hypothesis using globally applied biophysical calculations of the effects of warming and shade reduction on potential activity time and whole-life-cycle energy budgets. These 'thermodynamic niche' analyses show that activity restriction from climate warming is unlikely to provide a general explanation of recent extinctions, and that loss of shade is viable alternative explanation. Climate warming could cause population declines, even under increased activity potential, through joint impacts on fecundity and mortality rates. However, such responses depend strongly on behaviour, habitat (shade, food) and life history, all of which should be explicitly incorporated in mechanistic forecasts of extinction risk under climate change.
Antipredatory behaviour may be temperature dependent in ectotherms because locomotor capacity varies with temperature, affecting ability to escape. I studied thermal dependence of escape by the keeled earless lizard, Holbrookia propinqua. Distance to refuge and distance from an approaching predator at which escape was initiated (approach distance) increased with substrate temperature, but distance fled was unaffected by temperature. Approach distance in other species decreases with temperature increases, which has been explained by decreased risk due to greater speed for warmer lizards. However, H. propinqua maintains nearly constant mean body temperature from completion of post-emergence basking until it retires for the night. Increase in approach distance with substrate temperature in this species may reflect occupation of or flight to more open sites where the probability of being detected increases. Other risk factors that vary with temperature may affect escape decisions. The lizards used burrows of the Mexican ground squirrel Citellus mexicanus as refuges only at substrate temperatures < 31°C and > 50°C. Shortly after they emerge in the morning, lizards remaining closer to refuge may have a greater probability of escape when slowed by low body temperature. After warming to preferred body temperature, they refuse to enter burrows when chased until environmental temperatures become high enough to place them in danger of heat exhaustion. Effects of temperature on risk and escape costs, and consequent effects on optimal escape by ectotherms are discussed.
Eastern fence lizards (Sceloporus undulatus) exhibit a distinct thermal preference that might be related to the thermal optimum for physiological performance. Sprint speed and treadmill endurance of S. undulatus were insensitive to body temperature in the ranges of 28–38°C and 25–36°C, respectively. Both locomotor and digestive performances are optimized at the preferred body temperature of S. undulatus, but thermoregulatory behavior is more closely related to the thermal sensitivity of digestive performance than that of locomotor performance.
In order to use counts of active animals to estimate population parameters (abundance, sex ratio, age structure), we need to understand the factors that bias such counts. For many taxa, the main problems involve behavioural differences among age/sex classes, and the effects of local conditions on activity levels. A unique opportunity to quantify such effects on snakes occurs on Shedao, a small island in the Bohai Sea off north-eastern China. The island contains an extraordinary density of endemic pit-vipers (Gloydius shedaoensis), that feed primarily on migrating passerine birds. Over an 8-year period we walked the same 540-m path on 936 mornings during bird-migration periods, counted all pit-vipers within a 3-m-wide transect, and recorded the animals’ sex and age class (adult vs juvenile). Total numbers of snakes averaged 40.6 per survey (0.31 per m): thus, the data set contains 37,980 records of sightings of snakes. The total numbers and the composition (sex ratio, age structure) of snakes seen in a morning differed among segments of the path, differed between seasons (spring versus autumn), differed with time within each season, and were influenced by weather conditions (temperature, wind speed, relative humidity). For example, more snakes were seen on days that were hot, with little wind. The proportion of juvenile snakes in the sample decreased on hot, dry, windy days. Sex ratios shifted with time and air temperature. Interactions between these factors were also significant. Overall, census conditions (date, weather) had more influence on total numbers of snakes seen than on age structure or sex ratio in the samples. However, visual censuses strongly under-represented the proportion of adult (vs juvenile) snakes, and the numbers of male compared to female snakes. These analyses provide a strong cautionary message for researchers who use census data to infer underlying demographic traits. At the same time, they show that census data can be informative about abundance and demography as long as one understands the nature and magnitude of biases introduced by conditions prevailing during data aquisition.
Operative temperature (Te) and standard operative temperature (Tes) models have been used to address ecological questions about the thermal biology of ectotherms and endotherms for over 25 years. This review focuses on the accuracy and use of Te and Tes models in ecological and physiological studies. The utility of Te and Tes models lie in the fact that they take a multivariate problem involving inputs of air temperature, ground temperature, solar radiation, and wind speed and map them into a single thermal metric on a spatial scale appropriate for the animal. The most reliable Te models are copper casts that mimic the morphology and absorptivity of an animal. Simplified Te models such as cylinders and spheres have been shown to produce errors in Te as large as 12 °C under certain conditions and should only be used after careful calibration against a live animal. The accuracy of heated Tes models has been addressed in much less detail then that of Te models. When calibrated and used under conditions of low solar radiation, heated taxidermic mounts and simplified Tes models produce errors in net heat production on the order of 5% or less. In order to provide reliable data, all types of models must be calibrated over an ecologically realistic range of environmental conditions experienced by the animal. This advice has been largely ignored in the literature, where 61% of the of studies examined failed to properly calibrate the models prior to use. Additionally, studies using these models tend to lack experimental rigor, using only one or two models to make measurements on 1 or 2 days of the active season. When used correctly, Te and Tes models can be powerful tools for integrating the thermal environment experienced by an animal into a single metric that can address questions regarding the ecology, physiology, and behavior of endotherms and ectotherms. However, until investigators make the effort to use these models in a scientifically valid manner with proper calibration and experimental design their value to thermal biologists will be limited.
Varanus mertensi is a semiaquatic lizard that lives near permanent water in northern Australia. During the wet and dry seasons, we measured the field metabolic rate (FMR) and water flux rates of animals in the field and standard metabolic rates across a range of body temperatures (18-96 C) in the laboratory. We combined these data to divide the FMR into energy expended during periods of rest and activity. The FMR was significantly higher in the wet season (120.7 kJ kg(-1) day(-1)) than in the dry season (81.1 kJ kg(-1) day(-1)). There was no difference in the water flux rate between the wet (63.2 ml kg(-1) day(-1)) and dry (66.5 ml kg(-1) day(-1)) seasons. The FMR during the wet season is greater than that predicted for a similarly sized iguanid lizard, but the 95% confidence interval around the mean FMR in the dry season overlaps the predicted iguanid value. The calculated percent of the FMR devoted to activity is high for both seasons (70-73%) compared to other lizards, as is the calculated sustainab
Most ectothermal animals have variable body temperatures. Because physiological rates are temperature sensitive, an ectotherm's behavioural and ecological performance - even its fitness - can be influenced by body temperature. As a result, the thermal sensitivity of ectotherm performance is relevant to diverse issues in physiology, ecology and evolution. This review formalizes an emerging framework for investigating the evolution of thermal sensitivity, outlines some functional and genetical constraints on that evolution, and summarizes comparative and experimental advances in this field.