Phenotypic flexibility in heat production and heat loss in response to thermal and hydric acclimation in the zebra finch, a small arid-zone passerine

Abstract

To maintain constant body temperature (T_b) over a wide range of ambient temperatures (T_a) endothermic animals require large amounts of energy and water. In hot environments, the main threat to endothermic homeotherms is insufficient water to supply that necessary for thermoregulation. We investigated flexible adjustment of traits related to thermoregulation and water conservation during acclimation to hot conditions or restricted water availability, or both, in the zebra finch, Taeniopygia guttata a small arid-zone passerine. Using indirect calorimetry, we measured changes in whole animal metabolic rate (MR), evaporative heat loss (EHL) and T_b before and after acclimation to 23 or 40 °C, with different availability of water. Additionally, we quantified changes in partitioning of EHL into respiratory and cutaneous avenues in birds exposed to 25 and 40 °C. In response to heat and water restriction zebra finches decreased MR, which together with unchanged EHL resulted in increased efficiency of evaporative heat loss. This facilitated more precise T_b regulation in heat-acclimated birds. Acclimation temperature and water availability had no effect on the partitioning of EHL into cutaneous or respiratory avenues. At 25 °C, cutaneous EHL accounted for ~ 60% of total EHL, while at 40 °C, its contribution decreased to ~ 20%. Consistent among-individual differences in MR and EHL suggest that these traits, provided that they are heritable, may be a subject to natural selection. We conclude that phenotypic flexibility in metabolic heat production associated with acclimation to hot, water-scarce conditions is crucial in response to changing environmental conditions, especially in the face of current and predicted climate change.

Keywords: Energy metabolism; Evaporative heat loss; Passerine; Phenotypic flexibility; Thermoregulation.

Fig. 1

Metabolic rate (a), body temperature (b), evaporative heat loss (c) and efficiency of evaporative cooling (EHL/MR; d) as function of ambient temperature in zebra finches acclimated to T_a = 23 °C with unrestricted access to water. Data for initial acclimation are presented together as there was no difference between birds (GAMM: p > 0.1 for all variables). The solid line is the segmented linear regression model that provided the best fit. Different symbols stand for birds that were later assigned to different experimental acclimation

Fig. 2

The effect of experimental acclimation on zebra finch metabolic rate (W; a, b), body temperature (°C; c, d), evaporative heat loss (W; e, f) and efficiency of evaporative heat loss (EHL/MR; g, h) at T_a’s between 23 and 44 °C and above upper critical temperature (T_UC). Different symbols (estimated marginal mean ± SE) stand for birds from different experimental groups. T_b (between 23 and 44 °C) as well as EHL (at all T_a’s) of birds from different acclimation regimes did not differ (c, e, f) and thus groups were pooled together. Marginal means at T_a > T_UC were estimated at T_a = 44 °C. Asterisks indicate significant differences between measurements after initial and experimental acclimation (p < 0.0001)

Fig. 3

Thermal conductance (mW °C⁻¹ cm⁻²; estimated marginal mean ± SE) below lower critical temperature after initial and experimental acclimation. Different symbols stand for zebra finches from different acclimation regimes. Asterisks indicate significant differences within groups (p < 0.05)

Fig. 4

Respiratory (a) and cutaneous (b) evaporative heat loss (W; estimated marginal mean ± SE) at 25 and 40 °C in zebra finches after experimental acclimation. Different symbols stand for birds from different acclimation regimes. Note different scale of axes for parts at 25 and 40 °C at panel of respiratory EHL (a). Boxes at panel of cutaneous EHL (b) indicate 25th and 75th percentiles, solid line stands for median. Different symbols mark individual birds from different acclimation regimes. Inset: a schematic drawing of zebra finch in the polyethylene mask used for respiratory evaporative water loss measurements. Rubber band securing the mask (blue) was placed under feathers below the occipital region of the skull (color figure online)

Fig. 5

Respiratory to cutaneous evaporative heat loss (EHL) ratio (a), and contribution of cutaneous EHL to total EHL (b) at T_a of 25 and 40 °C. Boxes indicate 25th and 75th percentiles, solid lines stand for median. Different symbols indicate individual birds from different acclimation regimes

Fig. 6

Representative recording of body temperature (black line), metabolic rate (MR, grey line), total evaporative heat loss (total EHL, REHL + CEHL; pink line), respiratory evaporative heat loss (blue line), and cutaneous evaporative heat loss (red line) in one zebra finch measured at T_a = 40 °C. Black arrows indicate the time of wing drooping (color figure online)