The Paradox of Nocturnality in Lizards
Paradoxically, nocturnal lizards prefer substantially higher body temperatures than are achievable at night and are therefore active at thermally suboptimal temperatures. In this study, potential physiological mechanisms were examined that may enable nocturnal lizards to counteract the thermal handicap of activity at low temperatures: 1) daily rhythms of metabolic rate, 2) metabolic rate at low and high temperatures, 3) locomotor energetics, and 4) biochemical adaptation. A multi-species approach was used to separate evolutionary history of the species from any potential links between physiology and activity period. Four to eight species of lizards, encompassing nocturnal and diurnal lizards from the families Diplodactylidae and Scincidae, were used for all physiological measurements. Three daily patterns of metabolic rate (VO2) were apparent depending on the species: 24 h cycles, 12 h cycles, and no daily cycle. The daily patterns of VO2 and peak VO2 did not always coincide with the activity period of the species. All nocturnal lizards tested had a lower energetic cost of locomotion (Cmin) than diurnal lizards. Diurnal lizards from New Zealand also had low Cmin values when compared with nocturnal geckos and diurnal lizards from lower latitudes. Thus, a low Cmin appears to be related to activity at low temperatures rather than specifically to nocturnality. However, more data are required on lizards from high latitudes, including more New Zealand lizards, before the generality of this pattern can be confirmed. Also, based on correlations with lizards active at warmer temperatures, a low Cmin only partially offsets the thermal handicap imposed on lizards that are active at low temperatures. Nocturnal lizards were found to have lower thermal sensitivities of metabolism (lower Q10 values) than diurnal lizards, indicating that their energy-dependent activity was not as sensitive to changes in environmental temperature. The similarity of other metabolic processes among species with differing activity periods may be partly explained by the ability of nocturnal species to thermoregulate to achieve higher temperatures during the day. The amplitudes of daily VO2 cycles and mass-specific VO2 did not differ among nocturnal and diurnal New Zealand lizards at low temperatures. The specific activity of the glycolytic enzyme lactate dehydrogenase (LDH) isolated from the tail muscle of lizards was also comparable among nocturnal and diurnal lizards over a range of biologically relevant temperatures. Thus, activity of lizards at low temperatures is not enabled by lower energy requirements over a 24 h period, elevation of metabolic rates, or biochemical adaptation of LDH to specific temperatures. These results confirm that locomotion is more efficient in nocturnal lizards and diurnal lizards from New Zealand than lizards from elsewhere, but that other metabolic processes do not appear to differ among species. Additional physiological and behavioural adaptations may exist that complement the increased efficiency of locomotion, thus enabling nocturnal lizards to be active at low temperatures.