Environmental temperature predicts resting metabolic rates in tropidurinae lizards.

Interspecific variation in metabolic rates may be associated with climate, habitat structure, and resource availability. Despite a strong link between ecology and physiology, there is a dearth in the understanding of how the costs of body maintenance change during ecological transitions. We focused on an ecologically diverse group of neotropical lizards (Tropidurinae) to investigate whether and how resting metabolic rate (RMR) evolved under divergent micro- and macrohabitat conditions. Using a phylogenetic framework, we tested whether species from hot and dry habitats had lower RMRs in relation to those from cooler and mesic habitats, and investigated whether microhabitat usage had an effect over body mass-adjusted RMRs. Our results suggest that RMRs are not phylogenetically structured in Tropidurinae. We found no correlation between metabolism, precipitation, and microhabitat usage. Species from warmer habitats had lower RMR compared to those from cooler habitats, supporting a mechanism of negative compensation in metabolic responses to temperature. Ectotherms from warmer habitats can limit energetic demand and expenditure through reduced RMR, whereas those from cooler habitats may sustain activity despite thermal constraints via increased RMR. Our work highlights the role of temperature in shaping metabolic responses in lizards, giving additional support to the notion that physiology and ecological contexts are intertwined.

Patterns of energetic substrate modifications in response to feeding in boas, Boa constrictor (Serpentes, Boidae).

Ambush-foraging snakes that ingest large meals might undergo several months without eating when they use the internal reserves to support the energetic costs of living. Then, morphological and physiological processes might be orchestrated during the transition from fasting to the postprandial period to rapidly use the energetic stores while the metabolic rate is elevated in response to food intake. To understand the patterns of substrates deposition after feeding, we accessed the morphological and biochemical response in Boa constrictor snakes after two months of fasting and six days after feeding. We followed the plasma levels of glucose, total proteins, and total lipids, and we performed the stereological ultrastructural analysis of the liver and the proximal region of the intestine to quantify glycogen granules and lipid droplets. In the same tissues and stomach, we measured the activity of the enzyme fructose-1,6-biphosphatase (FBPase1) involved in the gluconeogenic pathway, and we measured pyruvate kinase (PK) and lactate dehydrogenase (LDH) enzymatic activities involved in the anaerobic pathway in the liver. Briefly, our results indicated an increase in boas' plasma glucose one day after meal intake compared to unfed snakes. The hepatic glycogen reserves were continuously restored within days after feeding. Also, the enzymes involved in the energetic pathways increased activity six days after feeding in the liver. These findings suggest a quick restoring pattern of energetic stores during the postprandial period.

Feeding effects on liver mitochondrial bioenergetics of Boa constrictor (Serpentes: Boidae).

Snakes are interesting examples of taxa that can overcome energy metabolism challenges, as many species can endure long periods without feeding, and their eventual meals are of reasonably large sizes, thus exhibiting dual extreme adaptations. Consequently, metabolic rate increases considerably to attend to the energetic demand of digestion, absorption and protein synthesis. These animals should be adapted to transition from these two opposite states of energy fairly quickly, and therefore we investigated mitochondrial function plasticity in these states. Herein, we compared liver mitochondrial bioenergetics of the boid snake Boa constrictor during fasting and after meal intake. We fasted the snakes for 60 days, and then we fed a subgroup with 30% of their body size and evaluated their maximum postprandial response. We measured liver respiration rates from permeabilized tissue and isolated mitochondria. From isolated mitochondria, we also measured Ca2+ retention capacity and redox status. Mitochondrial respiration rates were maximized after feeding, reaching an approximately 60% increase from fasting levels when energized with complex I-linked substrates. Interestingly, fasting and fed snakes exhibited similar respiratory control ratios and citrate synthase activity. Furthermore, we found no differences in Ca2+ retention capacity, indicating no increase in susceptibility to mitochondrial permeability transition, and no changes in mitochondrial redox state, although fed animals exhibited increases in the release of H2O2. Thus, we conclude that liver mitochondria from B. constrictor snakes increase respiration rates during the postprandial period and quickly improve the bioenergetic capacity without compromising redox balance.

Thermal and salinity effects on locomotor performance of Thoropa taophora tadpoles (Anura, Cycloramphidae).

It is well known that environmental temperature influences several biological functions of ectotherms, notably in amphibians. The high permeability of anuran skin, associated with the effect of elevated environmental temperature, potentiates the dehydration process and this combination may restrict locomotor performance. Thoropa taophora is an endemic species from the Atlantic Rainforest whose tadpoles are semiterrestrial and predominantly diurnal, and are found in rocky seashores where they are exposed to sea spray and high temperatures. In this study we investigated how temperature and salinity conditions affect the locomotor performance in Thoropa taophora tadpoles. We also assessed how different osmotic concentrations affect the activity of the metabolic pathways that support muscle function. We measured the sprint speed of tadpoles of various sizes at different temperatures and salinities in the field. We also measured the activity of the enzymes pyruvate kinase (PK), lactate dehydrogenase (LDH) and citrate synthase (CS) in different temperatures and osmotic concentrations, and calculated the thermal sensitivity and the activity constants for each osmolality. Our results showed that, in general, sprint speed decreased with increasing temperature and salinity. However, whereas the effect of increased salinity was similar in smaller and larger tadpoles, increased temperature had a higher negative impact on sprint speed of larger tadpoles, thus indicating low thermal sensitivity of small tadpoles. PK and LDH thermal sensitivities and LDH constant of activity decreased as the osmolality increased. In conclusion, the locomotor capacity of tadpoles was decreased by temperature and salinity, which may be related to a decrease in anaerobic metabolism both in terms of sensitivity and total energy turnover through enzymatic activity. We discuss the ecological consequences, including the potential impacts on predator escape behavior promoted by changes in metabolism and locomotor performance in an early stage of development of this species.

Phylogenetic analysis of standard metabolic rate of snakes: a new proposal for the understanding of interspecific variation in feeding behavior.

The current proposal about the variation of standard metabolic rates (SMR) in snakes predicts that SMR is influenced by the feeding frequency (frequent or infrequent feeders). However, feeding frequency in snakes is poorly studied and hard to quantify under natural conditions. Alternatively, foraging strategy was studied for a large number of species and is usually related to the feeding frequency. In this work, we performed a meta-analysis on the SMR of compiled data from 74 species of snakes obtained from the literature and five more different species of lanceheads (genus Bothrops), after categorization according to the foraging mode (ambush or active foraging) and regarding their phylogenetic history. We tested the hypothesis that foraging mode (FM) is a determinant factor on the interspecific variation of SMR despite the phylogenetic relationship among species. We demonstrated that FM predicted SMR, but there is also a partial phylogenetic structuration of SMR in snakes. We also detected that evolution rates of SMR in active foragers seem to be higher than ambush-hunting snakes. We suggested that foraging mode has a major effect over the evolution of SMR in snakes, which could represent an ecophysiological co-adaptation, since ambush hunters (with low feeding rates) present a lower maintenance energetic cost (SMR) when compared to active foragers. The higher SMR evolution rates for active foraging snakes could be related to a higher heterogeny in the degree of activity during hunting by active foragers when compared to ambush-hunting snakes.

Beyond body size: muscle biochemistry and body shape explain ontogenetic variation of anti-predatory behaviour in the lizard Salvator merianae.

Anti-predatory behaviour evolves under the strong action of natural selection because the success of individuals avoiding predation essentially defines their fitness. Choice of anti-predatory strategies is defined by prey characteristics as well as environmental temperature. An additional dimension often relegated in this multilevel equation is the ontogenetic component. In the tegu Salvator merianae, adults run away from predators at high temperatures but prefer fighting when it is cold, whereas juveniles exhibit the same flight strategy within a wide thermal range. Here, we integrate physiology and morphology to understand ontogenetic variation in the temperature-dependent shift of anti-predatory behaviour in these lizards. We compiled data for body shape and size, and quantified enzyme activity in hindlimb and head muscles, testing the hypothesis that morphophysiological models explain ontogenetic variation in behavioural associations. Our prediction is that juveniles exhibit body shape and muscle biochemistry that enhance flight strategies. We identified biochemical differences between muscles mainly in the LDH:CS ratio, whereby hindlimb muscles were more glycolytic than the jaw musculature. Juveniles, which often use evasive strategies to avoid predation, have more glycolytic hindlimb muscles and are much smaller when compared with adults 1-2 years old. Ontogenetic differences in body shape were identified but marginally contributed to behavioural variation between juvenile and adult tegus, and variation in anti-predatory behaviour in these lizards resides mainly in associations between body size and muscle biochemistry. Our results are discussed in the ecological context of predator avoidance by individuals differing in body size living at temperature-variable environments, where restrictions imposed by the cold could be compensated by specific phenotypes.

Aggressive behavior and performance in the Tegu lizard Tupinambis merianae.

Aggression is an important component of behavior in many animals and may be crucial to providing individuals with a competitive advantage when resources are limited. Although much is known about the effects of catecholamines and hormones on aggression, relatively few studies have examined the effects of physical performance on aggression. Here we use a large, sexually dimorphic teiid lizard to test whether individuals that show high levels of physical performance (bite force) are also more aggressive toward a potential threat (i.e., a human approaching the lizard). Our results show that independent of their sex, larger individuals with higher bite forces were indeed more aggressive. Moreover, our data show that individuals with higher bite forces tend to show decreased escape responses and are slower, providing evidence for a trade-off between fight and flight abilities. As bite force increased dramatically with body size, we suggest that large body size and bite force may reduce the threshold for an individual to engage in an aggressive encounter, allowing it to potentially gain or maintain resources and fight off predators while minimizing the risk of injury.

Seasonal metabolic changes in a year-round reproductively active subtropical tree-frog (Hypsiboas prasinus).

Although seasonal metabolic variation in ectothermic tetrapods has been investigated primarily in the context of species showing some level of metabolic depression during winter, but several species of anurans maintain their activity patterns throughout the year in tropical and subtropical areas. The tree-frog Hypsiboas prasinus occurs in the subtropical Atlantic Forest and remains reproductively active during winter, at temperatures below 10 degrees C. We compared males calling in summer and winter, and found that males of H. prasinus exhibit seasonal adjustments in metabolic and morphometric variables. Individuals calling during winter were larger and showed higher resting metabolic rates than those calling during summer. Calling rates were not affected by season. Winter animals showed lower liver and heart activity level of citrate synthase (CS), partially compensated by larger liver mass. Winter individuals also showed higher activity of pyruvate kinase (PK) and lower activity of CS in trunk muscles, and higher activity of CS in leg muscles. Winter metabolic adjustments seem to be achieved by both compensatory mechanisms to the lower environmental temperature and a seasonally oriented aerobic depression of several organs. The impact of seasonal metabolic changes on calling performance and the capacity of subtropical anurans for metabolic thermal acclimatization are also discussed.

Seasonal metabolic depression, substrate utilisation and changes in scaling patterns during the first year cycle of tegu lizards (Tupinambis merianae).

The tegus increase in body mass after hatching until early autumn, when the energy intake becomes gradually reduced. Resting rates of oxygen consumption in winter drop to 20% of the values in the active season ((O(2))=0.0636 ml g(-1) h(-1)) and are nearly temperature insensitive over the range of 17-25 degrees C (Q(10)=1.55). During dormancy, plasma glucose levels are 60% lower than those in active animals, while total protein, total lipids and beta-hydroxybutyrate are elevated by 24%, 43% and 113%, respectively. In addition, a significant depletion of liver carbohydrate (50%) and of fat deposited in the visceral fat bodies (24%) and in the tail (25%) and a slight loss of skeletal muscle protein (14%) were measured halfway through the inactive period. Otherwise, glycogen content is increased 4-fold in the brain and 2.3-fold in the heart of dormant lizards, declining by the onset of arousal. During early arousal, the young tegus are still anorexic, although (O(2)) is significantly greater than winter rates. The fat deposits analysed are further reduced (62% and 45%, respectively) and there is a large decrease in tail muscle protein (50%) together with a significant increase in glycogen (2-3-fold) and an increase in plasma glucose (40%), which suggests a role for gluconeogenesis as a supplementary energy source in arousing animals. No change is detectable in citrate synthase activity, but beta-hydroxyacyl CoA dehydrogenase activities are strongly affected by season, reaching a 3-fold and 5-fold increase in the liver tissue of winter and arousing animals, respectively, and becoming reduced by half in skeletal muscle and heart of winter animals compared with late fall or spring active individuals. From hatching to late autumn, the increase of the fat body mass relatively to body mass is disproportionate (b=1.44), and the mass exponent changes significantly to close to 1.0 during the fasting period. The concomitant shift in the (O(2)) mass exponent in early autumn (b=0.75) to values significantly greater than 1.0 in late autumn and during winter dormancy indicates an allometric effect on the degree of metabolic depression related to the size of the fat stores and suggests greater energy conservation in the smaller young.