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

Abstract

SUMMARYThe 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(V̇O2=0.0636 ml g-1 h-1) and are nearly temperature insensitive over the range of 17-25°C (Q10=1.55). During dormancy, plasma glucose levels are 60% lower than those in active animals, while total protein, total lipids and β-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 V̇O2 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 β-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 V̇O2 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.

Seasonal Changes in Daily Metabolic Patterns of Tegu Lizards (Tupinambis merianae) Placed in the Cold (17°C) and Dark

“…While some species show metabolic acclimation/acclimatization to compensate for seasonal changes in temperature (Roberts 1968), other species downregulate physiological and biochemical processes and become dormant. The metabolic rate of tegus, like other lizards in this latter group, measured at a constant temperature falls progressively from summer to winter, and the magnitude of this fall is proportionately less at lower temperatures (Weigmann 1932;Moberly 1963;Mayhew 1965;Gelineo 1967;Bennett and Dawson 1976;Abe 1983Abe , 1993Abe , 1995de Souza et al 2004). As a consequence, the effect of temperature on metabolic rate (the Q 10 effect) is progressively reduced from summer to winter, and thus the metabolic rate of dormant lizards is much less temperature dependent (Abe 1983(Abe , 1993(Abe , 1995de Souza et al 2004).…”

“…The metabolic rate of tegus, like other lizards in this latter group, measured at a constant temperature falls progressively from summer to winter, and the magnitude of this fall is proportionately less at lower temperatures (Weigmann 1932;Moberly 1963;Mayhew 1965;Gelineo 1967;Bennett and Dawson 1976;Abe 1983Abe , 1993Abe , 1995de Souza et al 2004). As a consequence, the effect of temperature on metabolic rate (the Q 10 effect) is progressively reduced from summer to winter, and thus the metabolic rate of dormant lizards is much less temperature dependent (Abe 1983(Abe , 1993(Abe , 1995de Souza et al 2004). Indeed, preparation for dormancy may begin well before winter, and the loss of temperature sensitivity may occur in midautumn and precede the general decrease in levels of metabolism (Gelineo 1967).…”

“…Other studies, however, report that the Q 10 effect does not change with season (for review, see Bennett and Dawson 1976) or that Q 10 even increases during winter at higher temperatures in larger animals (Andrade and Abe 1999). Of particular note is that the effect of temperature on metabolic rate has been reported to be reduced, unchanged, or increased during winter all in the same species, Tupinambis merianae, in different studies (Abe 1983(Abe , 1993(Abe , 1995Andrade and Abe 1999;de Souza et al 2004;Toledo et al 2008).…”

“…The three most southerly occurring species (Tupinambis duseni, Tupinambis rufescens, and T. merianae) belong to one clade that can undergo seasonal dormancy (Köhler and Langerwerf 2000;Manzani and Abe 2002). One of them, T. merianae, has been the subject of a variety of studies that have examined patterns of daily and seasonal change in activity, body temperature, and metabolic rate (Abe 1983(Abe , 1993(Abe , 1995Andrade and Abe 1999;Andrade et al 2004;de Souza et al 2004;Klein et al 2006;Toledo et al 2008).…”

“…It is clear that metabolic suppression in reptiles is a complex phenomenon and is regulated by both endogenous and exogenous factors and that these factors fluctuate on both a daily and a seasonal basis (Guppy and Withers 1999;de Souza et al 2004). Given how little is known about these factors and their interactions, it is not surprising that such wide-ranging changes in oxygen consumption rate have been reported to occur as a function of season in different studies of the same species (Abe 1983(Abe , 1993(Abe , 1995Andrade and Abe 1999;de Souza et al 2004;Toledo et al 2008).…”