Physiological thermal responses of three Mexican snakes with distinct lifestyles.

The impact of temperature on reptile physiology has been examined through two main parameters: locomotor performance and metabolic rates. Among reptiles, different species may respond to environmental temperatures in distinct ways, depending on their thermal sensitivity. Such variation can be linked to the ecological lifestyle of the species and needs to be taken into consideration when assessing the thermal influence on physiology. This is particularly relevant for snakes, which are a very functionally diverse group. In this study, our aim was to analyze the thermal sensitivity of locomotor performance and resting metabolic rate (RMR) in three snake species from central Mexico (Crotalus polystictus, Conopsis lineata, and Thamnophis melanogaster), highlighting how it is influenced by their distinctive behavioral and ecological traits. We tested both physiological parameters in five thermal treatments: 15 °C, 25 °C, 30 °C, 33 °C, and 36 °C. Using the performance data, we developed thermal performance curves (TPCs) for each species and analyzed the RMR data using generalized linear mixed models. The optimal temperature for locomotion of C. polystictus falls near its critical thermal maximum, suggesting that it can maintain performance at high temperatures but with a narrow thermal safety margin. T. melanogaster exhibited the fastest swimming speeds and the highest mass-adjusted RMR. This aligns with our expectations since it is an active forager, a high energy demand mode. The three species have a wide performance breadth, which suggests that they are thermal generalists that can maintain performance over a wide interval of temperatures. This can be beneficial to C. lineata in its cold habitat, since such a characteristic has been found to allow some species to maintain adequate performance levels in suboptimal temperatures. RMR increased along with temperature, but the proportional surge was not uniform since thermal sensitivity measured through Q10 increased at the low and high thermal treatments. High Q10 at low temperatures could be an adaptation to maintain favorable performance in suboptimal temperatures, whereas high Q10 at high temperatures could facilitate physiological responses to heat stress. Overall, our results show different physiological adaptations of the three species to the environments they inhabit. Their different activity patterns and foraging habits are closely linked to these adaptations. Further studies of other populations with different climatic conditions would provide valuable information to complement our current understanding of the effect of environmental properties on snake physiology.

Flexibility in thermal requirements: a comparative analysis of the wide-spread lizard genus Sceloporus.

Adaptation or acclimation of thermal requirements to environmental conditions can reduce thermoregulation costs and increase fitness, especially in ectotherms, which rely heavily on environmental temperatures for thermoregulation. Insight into how thermal niches have shaped thermal requirements across evolutionary history may help predict the survival of species during climate change. The lizard genus Sceloporus has a widespread distribution and inhabits an ample variety of habitats. We evaluated the effects of geographical gradients (i.e. elevation and latitude) and local environmental temperatures on thermal requirements (i.e. preferred body temperature, active body temperature in the field, and critical thermal limits) of Sceloporus species using published and field-collected data and performing phylogenetic comparative analyses. To contrast macro- and micro-evolutional patterns, we also performed intra-specific analyses when sufficient reports existed for a species. We found that preferred body temperature increased with elevation, whereas body temperature in the field decreased with elevation and increased with local environmental temperatures. Critical thermal limits were not related to the geographic gradient or environmental temperatures. The apparent lack of relation of thermal requirements to geographic gradient may increase vulnerability to extinction due to climate change. However, local and temporal variations in thermal landscape determine thermoregulation opportunities and may not be well represented by geographic gradient and mean environmental temperatures. Results showed that Sceloporus lizards are excellent thermoregulators, have wide thermal tolerance ranges, and the preferred temperature was labile. Our results suggest that Sceloporus lizards can adjust to different thermal landscapes, highlighting opportunities for continuous survival in changing thermal environments.

Seasonal and altitudinal variation in dorsal skin reflectance and thermic rates in a high-altitude montane lizard.

Temperature is one of the most important factors in the life histories of ectotherms, as body temperature has an undeniable effect on growth, activity, and reproduction. Lizards have a wide variety of strategies to acquire and maintain body temperature in an optimal range. The "Thermal Melanism Hypothesis" proposes that individuals with lower skin reflectance can heat up faster as a result of absorbing more solar radiation compared to lighter conspecifics. Therefore, having a darker coloration might be advantageous in cold habitats. Dorsal skin reflectance has been found to change rapidly with body temperature in several lizard species, and it can also vary over longer, seasonal time scales. These variations may be important in thermoregulation, especially in lizards that inhabit areas with a large temperature variation during the year. Here, we study how dorsal reflectance fluctuates with body temperature and varies among seasons. We compared dorsal skin reflectance at three body temperature treatments, and measured thermal rates (i.e., heat and cool rate, thermic lapse, and net heat gain) by elevation (2500-4100 m) and seasons (spring, summer, and autumn) in the mesquite lizard, Sceloporus grammicus. Our results show that lizards were darker at high elevations and during the months with the lowest environmental temperatures. The rate of obtaining and retaining heat also varied during the year and was highest during the reproductive season. Our results indicate that the variation of dorsal skin reflectance and thermal rates follows a complex pattern in lizard populations and is affected by both elevation and season.

Avoiding the effects of translocation on the estimates of the metabolic rates across an elevational gradient.

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.

Resting metabolic rates increase with elevation in a mountain-dwelling lizard.

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) 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., 2,600, 3,200, and 4,100 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.

Feeling the heat: Extreme temperatures compromise constitutive innate humoral immunity and skin color in a desert dwelling lizard.

Environmental temperature, particularly in habitats with extreme temperature fluctuations, may shape selection pressures on life history traits. Especially in ectotherms, temperature affects performance, physiology, and in some species, skin color. Skin color can be a sexual ornament signaling the bearer's ability to resist infections, when only high-quality individuals are able to invest both in high immune defense and elaborate ornament expression. However, how the information content of these sexual traits may vary with environmental conditions has been less studied. Dickerson's collared lizard (Crotaphytus dickersonae) males are blue and have a black and white collar. This conspicuous coloration signals performance and immune response, and is related to body temperature. Here, by maintaining males at higher, lower, and mean environmental temperatures we evaluated whether temperature variation influences color and constitutive innate humoral immunity (agglutination and lysis titers, estimated through hemolysis-hemagglutination assays), and whether extreme temperatures impose trade-offs between color and humoral immunity. We found that at low and high temperature treatments males had lower agglutination and lysis titers, and at low temperature, blue chroma from the dorsum declined and males became greener. Interestingly, at low and control temperature treatments, agglutination titer and blue coloration were positively correlated, whereas high temperatures revealed a trade-off between increasing agglutination titers and displaying bluer skin color. Our results suggest that in the Dickerson collared lizard even short-term variation of environmental temperature affects performance of constitutive innate humoral immunity and the brilliant blue skin color. Particularly, high temperatures may compromise some components of male's immunity and sexual signaling.

Environmental temperature alters the overall digestive energetics and differentially affects dietary protein and lipid use in a lizard.

Processing food (e.g. ingestion, digestion, assimilation) requires energy referred to as specific dynamic action (SDA) and is at least partially fuelled by oxidation of the nutrients (e.g. proteins and lipids) within the recently ingested meal. In ectotherms, environmental temperature can affect the magnitude and/or duration of the SDA, but is likely to also alter the mixture of nutrients that are oxidized to cover these costs. Here, we examined metabolic rate, gut passage time, assimilation efficiency and fuel use in the lizard Agama atra digesting cricket meals at three ecologically relevant temperatures (20, 25 and 32°C). Crickets were isotopically enriched with 13C-leucine or 13C-palmitic-acid tracers to distinguish between protein and lipid oxidation, respectively. Our results show that higher temperatures increased the magnitude of the SDA peak (by 318% between 32 and 20°C) and gut passage rate (63%), and decreased the duration of the SDA response (by 20% for males and 48% for females). Peak rate of dietary protein oxidation occurred sooner than peak lipid oxidation at all temperatures (70, 60 and 31 h earlier for 20, 25 and 32°C, respectively). Assimilation efficiency of proteins, but not lipids, was positively related to temperature. Interestingly, the SDA response exhibited a notable circadian rhythm. These results show that temperature has a pronounced effect on digestive energetics in A.atra, and that this effect differs between nutrient classes. Variation in environmental temperatures may thus alter the energy budget and nutrient reserves of these animals.