Precocial birds hatch feathered and mobile, but when they become fully endothermic soon after hatching, their heat loss is high and they may become energy depleted. These chicks could benefit from using energy-conserving torpor, which is characterised by controlled reductions of metabolism and body temperature (Tb). We investigated at what age the precocial king quail Coturnix chinensis can defend a high Tb under a mild thermal challenge and whether they can express torpor soon after achieving endothermy to overcome energetic and thermal challenges. Measurements of surface temperature (Ts) using an infrared thermometer showed that king quail chicks are partially endothermic at 2–10 days, but can defend high Tb at a body mass of ∼13 g. Two chicks expressed shallow nocturnal torpor at 14 and 17 days for 4–5 h with a reduction of metabolism by >40% and another approached the torpor threshold. Although chicks were able to rewarm endogenously from the first torpor bout, metabolism and Ts decreased again by the end of the night, but they rewarmed passively when removed from the chamber. The total metabolic rate increased with body mass. All chicks measured showed a greater reduction of nocturnal metabolism than previously reported in quails. Our data show that shallow torpor can be expressed during the early postnatal phase of quails, when thermoregulatory efficiency is still developing, but heat loss is high. We suggest that torpor may be a common strategy for overcoming challenging conditions during development in small precocial and not only altricial birds.

The majority of mammals and birds are homeothermic endotherms as adults, and rely on endogenous heat production to keep a constant, high body temperature (Tb; Yahav, 2015). However, at birth or hatching, most endotherms are only partially endothermic (Dawson and Evans, 1960) and are unable to produce sufficient heat to maintain a high and constant Tb when exposed to temperatures below the thermal neutral zone (TNZ). Nevertheless, within thermoneutrality the heat produced by resting metabolic rate (RMR) is enough to maintain a normothermic Tb often even in the early stages of development (Price and Dzialowski, 2018). During exposure to cold, developing endotherms depend on parental heat production or heat conservation from insulated nests for maintenance of a high Tb (Ricklefs, 1984).

Endothermy is energetically demanding (Visser and Ricklefs, 1993) and in birds, it requires the maturation of the skeletal muscles for heat production (Sirsat et al., 2016; Hohtola and Visser, 1998). The age at which endothermy is established differs substantially within and among species, often reflecting the duration of the nestling period (Dunn, 1975; Ricklefs, 1974) and brood size (Andreasson et al., 2016). Most birds are altricial, featherless and immobile at hatching, and are unable to physiologically thermoregulate via internal heat production; their Tb and metabolic rate (MR) are a direct function of ambient temperature (Ta; Price and Dzialowski, 2018; Dawson and Evans, 1960). The age at which altricial species develop a strong endothermic metabolic response during cold exposure varies from several days in sparrows (Spizella passerina, Spizella pusilla and Pooecetes gramineus; Dawson and Evans, 1957, 1960) and storm petrel (Oceanodroma furcata; Boersma, 1986) to up to 3 weeks in large species, such as American white Pelicans (Pelecanus erythrorhynchos; Abraham and Evans, 1999) and double-crested cormorants (Phalacrocorax auritus; Dunn, 1976).

At the opposite end of the spectrum, a few species are precocial, fully feathered and mobile, and develop thermoregulation during the early postnatal phase (Nichelmann and Tzschentke, 2002). Many precocial species are able to maintain, rather than increase, metabolism under cold exposure at the time of hatching (Sirsat et al., 2016; Dzialowski et al., 2007), but can form an endothermic metabolic response soon after hatching (Brown and Prior, 1999; Tamura et al., 2003). Most small precocial birds are completely endothermic only from about 10 days of age (Nichelmann and Tzschentke, 2002), whereas large species can already thermoregulate efficiently 1 day after hatching (Brown and Prior, 1999; Tamura et al., 2003).

Once the young endotherms become thermally independent and can increase MR to defend their Tb at moderate Ta, they still may face excessive heat loss in the absence of parental heat transfer during brooding. This heat loss, mainly an issue for small species, must be compensated for via endogenous heat production, which can result in substantial loss of energy reserves. To overcome these energetic and thermal challenges, some developing altricial birds and mammals use torpor, which is characterised by controlled reductions of MR and Tb (Boersma, 1986; Renninger et al., 2020; Eichhorn et al., 2011). While there is more than one definition of torpor (Schleucher, 2004), a common definition is a reduction by >25% of RMR at the same Ta (Hudson and Scott, 1979), and/or a reduction by >5°C below the normothermic Tb at rest (Schleucher, 2004; Ruf and Geiser, 2015). To be able to use and benefit from torpor during development, young endotherms must not only establish the capability of active thermoregulation for maintenance of a high and stable Tb in the cold but also be able to actively rewarm and increase MR from torpor at low Tb at the end of the torpor bout (Geiser et al., 2014; Wacker et al., 2017).

While torpor can be an effective survival strategy, the reduced Tb and depressed physiological functions can have negative implications for young animals. These include increased predation risk for the inexperienced chicks (Eichhorn et al., 2011; Wheelwright and Boersma, 1979; Andreasson et al., 2019), possible metabolic imbalance (Jensen and Bech, 1992), and delayed prenatal and juvenile development (Boersma and Wheelwright, 1979; McAllan and Geiser, 2014). However, in many cases, the slow rate of development does not affect the chances of survival in offspring (McAllan and Geiser, 2014; Prinzinger and Siedle, 1988; Racey and Swift, 1981), or the mass gain of juveniles (Giroud et al., 2014), and therefore the ability to enter torpor during development is likely to increase fitness. Moreover, torpor has many other selective advantages beyond efficient energy conservation to survive the energetically challenging period of development (Boersma, 1986; Bae et al., 2003; Geiser et al., 2006; Giroud et al., 2014; Wacker et al., 2017; Geiser et al., 2019). For example, torpor has been shown to aid survival of bad weather and natural disasters (Nowack et al., 2017), delay hatching until conditions are favourable for parents and offspring (Geiser and Brigham, 2012) and enhance fat accumulation when food is scarce (Giroud et al., 2014).

Although a potentially crucial survival strategy for many endotherms, data on torpor during early stages of development are scarce and limited to only a few altricial mammalian and avian species (e.g. Nagel, 1977; Eichhorn et al., 2011; Giroud et al., 2014). Currently, data on torpor in precocial species are lacking entirely although the energetic and thermal demands during development are similarly excessive especially in small species. One of these, the precocial Japanese quail (Coturnix japonica) has been investigated as an adult with regard to thermal energetics: adult birds (body mass ∼150 g) entered shallow nocturnal torpor after food deprivation and reduced their Tb by 5°C (Hohtola et al., 1991). Although at hatching these quails weigh as little as 3.5 g, it has not been investigated whether torpor is used as a strategy to enhance survival during the early stages of development, around the time they become endothermic.

In this study, we first aimed to determine at what age the king quail Coturnix chinensis (adult body mass ∼50 g), a close relative to the Japanese quail, develops competent endothermic thermoregulation, and is able to defend a high Tb when thermally challenged. Second, we aimed to test the hypothesis that precocial king quail can use torpor soon after achieving endothermy. To quantify this, we measured MR as the rate of oxygen consumption. Metabolic reduction is regarded as a more reliable indicator of torpor than reduction in Tb (Hiebert, 1993; McKechnie and Lovegrove, 2002; Willis, 2007) and is relevant when determining torpor, because the purpose of torpor is energy conservation and not Tb reduction. Moreover, entry into torpor usually requires a calm and undisturbed animal. Because of their small size, implanting temperature-sensitive devices in the king quail chicks was not possible, and the use of external devices to measure Tb or surface temperature (Ts) would disturb the birds, and may interrupt torpor, whereas MR measurements can be conducted non-invasively while the bird is resting. Measurements were conducted overnight when torpor is more likely to be used by diurnal birds.

Experimental animals

King quails, Coturnix chinensis (Linnaeus 1766), occur widely from India to Southeast Asia, Indonesia, New Guinea, and the northern and eastern coast of Australia, and are also a popular aviary bird. For our study, fertile quail eggs were obtained from commercial breeders on the Northern Tablelands in northern New South Wales. Eggs were incubated (LUMIA 8 incubator in heat-resistant ABS, Borroto, Buttapietra; Verona, Italy) at 37.7°C, and humidity was 50%. The photoperiod was 12 h light:12 h dark with lights on from 06:00 h to 18:00 h. Nine chicks hatched after 18 days of incubation and were kept in a temperature-controlled room at Ta=22.0±0.1°C. Chicks were randomly assigned to two brooders made of plastic cages (43.3×80×51 cm H×W×D), bedded with pine shavings and heated with a ceramic lamp suspended above the middle of the cage to create a thermal gradient. Chicks were identified by a marker on the back of their head. Four chicks were housed in one cage and five in the other. The Ta in the cage was 35°C below the heating lamp and 25±1°C at the edges of the cage, furthest from the lamp. Chicks could therefore move around in the thermal gradient to behaviourally regulate their Tb. Commercial game birds starter (28% protein, 3% fat) and fresh water were provided ad libitum, except during cooling and respirometry measurements.

Cooling measurements

From the time when the chicks were 2 days old, 2–4 individuals were removed from the brooder between 09:30 h and 11:00 h and placed individually into a paper cup at Ta=22.0±0.1°C. Immediately upon removal from the brooder, Ts was measured under the wing to the nearest 0.1°C (Tstart) using an infrared thermometer (Digitech, QM-7218), and then at 10 min intervals until the last measurement after 40 min (Tend). Previous studies found the difference between Ts and cloacal Tb to be ∼0.4°C in an 8 g bat (Bondarenco et al., 2014), less than 2°C in a 50 g common poorwill (Brigham, 1992) and less than 4°C in an 80 g owl (Smit and McKechnie, 2010) and nightjar (McKechnie et al., 2007). It is therefore likely that in the small king quail chicks, the difference between Tb and Ts does not exceed 1–2°C. Animals were weighed with an electronic balance at the end of the cooling experiment to the nearest 0.1 g. These measurements were conducted until 12 days of age, when the Ts change over 40 min was no longer significant. Each chick was measured between 3 and 4 times during the cooling experiment, and always had at least 1 day for recovery between measurements.

RMR

Oxygen consumption measurements using open-flow respirometry of chicks in the TNZ were conducted from 3 to 12 days of age. Two animals were measured concurrently and were placed individually into 500 ml metabolic chambers in a temperature-controlled cabinet at Ta=30±1.1°C, thermoneutral conditions for adult king quail (28–35°C; Roberts and Baudinette, 1986), for at least 60 min to determine RMR. The Ta was measured to the nearest 0.1°C in the respirometry chambers using calibrated thermocouples. Dried outside air was pumped through these chambers at a rate of approximately 300 ml min−1. By employing two-way solenoid valves, reference outside air and the air from the metabolic chambers was measured sequentially every 9 min (3 min for each channel). Air exiting the chambers was again dried and flow rate was measured with a mass flow meter (Omega FMA-5606); the oxygen content in a 100 ml min−1 subsample was then determined with an O2 analyser (FXO301-01R field oxygen analysis system version 1.01, Sable Systems International). Outputs from the flow meter and the thermocouples from each respirometry chamber were digitized via a 14 bit A/D converter (Data Taker DT100), whereas the O2 analyser was interfaced with the PC directly via a serial port. Temperature control within the climatic chamber, channel switching, calculations and data storage were performed with a custom program written by G.K. in Visual Basic 6 (Microsoft Inc.). Oxygen consumption was calculated based on flow rate and the O2 differential between reference and chamber air using Eqn 3a from Withers (1977) assuming a respiratory quotient (RQ) of 0.85. This RQ would result in a maximum error of 3% if the RQ was actually 0.7 or 1 (Withers, 1977). Prior to measurements, the span of the O2 analyser was set against outside air and the mass flow meter was calibrated with a custom-made bubble meter (Levy, 1964).

Determination of torpor expression

Once the chicks were 12 days of age, and able to maintain a constant Ts over 40 min at Ta=22.0±0.1°C, we tested whether they could use torpor. Chicks were removed from the brooder between 16:00 h and 16:30 h and placed individually into the respirometry chamber overnight for approximately 15 h on a 12 h light:12 dark cycle, without food and water. We then measured MR as the rate of oxygen consumption using the respirometry equipment described above. In the first two nights of metabolic measurements, the chicks were measured at Ta=22.0±0.3°C and from the third night onwards, we decreased the Ta to 18.0±0.3°C, both well below the TNZ (Roberts and Baudinette, 1986).

The minimum and maximum metabolic rate (MRmin and MRmax) were calculated as the lowest and the highest mean rate of O2, respectively, measured consecutively over a 36 min period (i.e. 4 consecutive values). Chicks were weighed to the nearest 0.1 g before and after each respirometry measurement. We assumed a linear mass loss to calculate the mass-specific MR.

To determine torpor occurrence in king quail, we calculated the individual expected RMR as:
formula
(1)
where C is the wet thermal conductance, calculated using the equation for the active phase C=0.994M−0.509 (where M is mass in g; Schleucher and Withers, 2001) and Tc,lower is the lower critical temperature: Tc,lower=Tb−4.24M0.317 (Swanson and Weinacht, 1997). Individual basal metabolic rate (BMR, in ml g−1 h−1; because the chicks were still growing) was calculated using the equation for non-passerines birds: logBMR=0.699×logM−1.371 (McKechnie et al., 2006). A chick was deemed to be torpid if MR during the rest phase fell >25% below the expected RMR (Hudson and Scott, 1979).

We measured Ts under the wing using an infrared thermometer in four individuals at 22:00 h during the metabolic measurements when the chicks were 17, 18 and 19 days old. These Ts measurements were completed within no more than 30 s of removing the chick from the respirometry chamber and subsequently returning it. We defined torpor as a reduction of Ts by >5°C below the resting Ts (Schleucher, 2004; Ruf and Geiser, 2015).

All experiments were approved by the University of New England Animal Ethics Committee (Authority No. AEC19-079), and were conducted in conformity with the NHMRC Australian Code of Practice for the Care and Use of Animals for Scientific Purposes.

Statistical analysis

Growth rate

A Gompertz growth curve (Tsoularis and Wallace, 2002) was fitted through the individual body masses with the non-linear model, according to the formula:
formula
(2)
where M(t) is body mass (g) at age t (days), A is asymptotic body mass (g), k is Gompertz growth constant (days−1) and ti is the age at the inflection point (days). We used the function grow_gompertz from the R package ‘growth rates’ (https://CRAN.R-project.org/package=growthrates).

Changes in Ts

We applied a general additive model (GAM) to describe temporal changes in Ts because the increase in Ts with age is not linear. The GAM approach is an extension of the general linear model (GLM) and is well suited for non-linear trends. The model included log of body mass and age as the response variables, with Ts as the dependent variable.

Cooling experiment

We fitted a general linear mixed-effect model with individual as a random effect to analyse the change in Ts over time with age and body mass. We set the difference between Ts at the start of the experiment (Tstart, at time zero) and Ts at the end of the experiment (Tend, after 40 min) as the dependent variable, in relation to age and body mass. In addition, we divided the dataset into four different body mass groups (<5, 5–<8, 8–13 and >13 g) and fitted a general linear mixed-effect model with individual as a random effect in each body mass group to determine the body mass at which chicks develop endothermy. We set Ts before and after the cooling experiment (at time zero and after 40 min) as the dependent variable in relation to time (start and end of the experiment). Finally, we calculated an index of homeothermy for nestlings following Ricklefs (1987) and Visser and Ricklefs (1993). This index measures the gradient between equilibrium Tb and the environmental temperature, and thus indicates the degree of homeothermy. We calculated the index (H) by dividing the final temperature difference between Ts and Ta by the initial difference:
formula
(3)
where Tstart and Tend are Ts at time of extraction from brooder and after 40 min of cooling at Ta=22°C, respectively. When H=1, a chick defends its initial Ts and when H=0, Ts drops to Ta within 40 min.

RMR in the TNZ

We used general linear modelling with individual as a random effect to examine the effect of body mass on RMR at TNZ (Ta=30°C) in the 3–12 day old chicks. RMR was calculated as the lowest mean rate of O2, measured consecutively over a 27 min period (i.e. 3 consecutive values). We analysed both total and mass-specific RMR.

Overnight MR below the TNZ

We analysed the effect of age and body mass on the difference between MR during the active and rest phases (MRmax−MRmin) under mild cold exposure (Ta=18 or 22°C). For this purpose, we fitted a general linear mixed-effect model with individual as a random effect.

Variables were excluded from models using ANOVA Type III, based on a threshold significance level set to P=0.05. We confirmed the use of random effect in the model by comparing the AIC of the best model with and without random effect using the REML method (Zuur et al., 2009). The R function lme in the R package ‘nlme’ (https://CRAN.R-project.org/package=nlme) was used to perform mixed-effect models with the function visreg in the ‘visreg’ package for visualization (https://CRAN.R-project.org/package=visreg). All statistical analyses were conducted using R version 3.3.0 (http://www.R-project.org/).

Numeric values are presented as means±s.d for the number of individuals (N) measured n=number of measurements.

Body mass (M) and growth rate

Mean chick body mass was 3.9±0.5 g, 24 h after hatching (n=5, N=5), 8.7±1.5 g at 7 days (n=4 measurements, N=4 individuals), and 19±2.6 g at 15 days (n=8, N=8). By the end of the experiment, at 22 days, the mean body mass was 27.8±1.7 g (n=7, N=7; Fig. 1). Adult feathers were visible at 5 days.

Ts

The mean Ts of chicks measured immediately after removal from the brooder at thermoneutrality increased with age from 34.6±2.2°C at 2–5 days, to 36.9±0.7°C at 3–8 days, 38.6±0.7°C at 6–12 days and 40.1±0.4°C at 10–15 days (Table 1). The increase was significantly and non-linearly correlated with age (F=30.12, P<0.001); body mass was not significant, probably because the importance of age was greater, and was removed from the model.

Changes in Ts during cooling in young chicks

The change in Ts over the 40 min of the cooling experiment at Ta=22°C was correlated with body mass (t=−9.28, P<0.001). In chicks with a body mass <5 g, mean Ts decreased from Tstart (34.6±2.2°C) to 24.8±1.3°C after 40 min (Tend), and these means differed significantly (t=9.26, P<0.001). The chicks were already able to visibly shiver when they were 2 days old. Chicks with a body mass between 5 and 13 g had slower rates of cooling than the previous group (<5 g). Consequently, Tend was 28.9±2.4°C at 5–8 g, whereas at 8–13 g, Tend was rather high at 35.2±1.8°C, but still significantly lower than Tstart. Chicks weighing >13 g, at 10–15 days were able to defend their Tb, and the mean Tstart was indistinguishable from Tend (39.8±1.5°C, P=0.74; Table 1 and Fig. 2).

Metabolic trials

MR in the TNZ

At 3–12 days, all chicks showed a substantial drop of MR at night with a minimum soon after midnight. Mass-specific mean RMR of all chicks was 4.2±0.99 ml O2 g−1 h−1 at Ta=30°C, ranging between 3.14 and 6.04 ml O2 g−1 h−1 (with one value of 1.97 ml O2 g−1 h−1 in one individual at 5.3 g). The mean total RMR was 38.43±15.64 ml O2 h−1 (Table 2). Mass-specific RMR was independent of body mass. Total RMR (ml O2 h−1) significantly increased with body mass (total RMR=1.43+4M; t=8.94, P<0.001).

Determination of torpor expression

At 12–22 days, the mean decrease of rest phase MR (RMRmin) for all chicks was 39.2% of the active phase MR (MRmax) at Ta=18–22°C. The average nightly reduction in mass-specific MR was 2.1±0.62 ml O2 g−1 h−1 or 43.81±9.55 ml O2 h−1 in total MR (Table 3; Table S1). Generally, MR started to decrease soon after lights off (at 18:00 h), and increased again at approximately 02:00 h, 4 h before lights on (Fig. 3). Mass loss during the night ranged between 2.96 and 4.6 g, with an average mass loss of 3.84±0.48 g (Table S1), which to some extent was due to loss of faeces. The differential between both total and mass-specific MRmin and MRmax was significantly and negatively related to body mass (Fig. 4, Table 4), with this differential being smaller in heavier birds.

Two of the chicks expressed shallow nocturnal torpor and one additional chick approached the RMR torpor threshold. Chick 1 exposed to Ta=22°C at 14 days, with a body mass of 14.2 g, steadily reduced MR from 6.31 ml O2 g−1 h−1 after being placed into the respirometer in the afternoon to a minimum of 2.39 ml O2 g−1 h−1 (60% of predicted RMR and slightly below the predicted BMR of 2.6 ml O2 g−1 h−1) at around 01:00 h, after which MR increased again to 4.46 ml O2 g−1 h−1 at around 04:00 h. After this increase, MR plummeted to 1.15 ml O2 g−1 h−1 and when the animal was removed at 07:30 h, its Ts was 26.2°C and the chick was returned to the brooder under the heat lamp. The MR of chick 1 remained below the torpor threshold for 5 h (from 22:00 h until 03:00 h; Fig. 3A, Table 3). Similarly, chick 2 (body mass 16.1 g) exposed to Ta=18°C at 17 days steadily reduced MR from ∼5.5 ml O2 g−1 h−1 after lights off. The Ts measured at 22:00 h was 33.8°C, 6.2°C below the starting Ts, with a MR at 3.39 ml O2 g−1 h−1. After a brief increase to 4.09 ml O2 g−1 h−1, MR continued to decline until it reached 2.72 ml O2 g−1 h−1 at approximately 01:30 h (59% of the predicted RMR, but 35% above the BMR). MR then increased briefly to 3.93 ml O2 g−1 h−1 at around 04:00 h, but then again decreased until it reached 1.60 ml O2 g−1 h−1 at 07:30 h, when the animal was removed from the chamber, and its Ts was 25.6°C. The MR of chick 2 remained below the torpor threshold for 4 h (from 00:00 h until 04:00 h; Fig. 3B, Table 3). Both chicks did not enter torpor on the second trial at Ta=18°C at 21 days (Fig. 3C,D). Chick 5 at Ta=22°C at 14 days reduced MR to values very close to the torpor threshold (2.77 ml O2 g−1 h−1, 77% of the predicted RMR), but not during the second trial at Ta=18°C (figure not shown).

We measured Ts in four chicks at 22:00 h while they were in the respirometry chamber on days 17, 18 and 19. The mean Ts of all chicks at the age of 12–22 days, before the respirometry measurements, was 40.2±0.6°C. The Ts of chicks 2, 4, 5 and 7 was 33.8, 35.4, 35.6 and 37.8°C, respectively, which was 6.2, 5.6, 5.4 and 2.8°C below their initial Ts, respectively. Except for chick 2 (details above), all the chicks rewarmed (to 38.8, 36.6 and 37.8°C for chicks 4, 5 and 7) when they were removed from the chambers at around 07:30 h.

We provide the first evidence of shallow nocturnal torpor expression in a developing precocial endotherm. King quail chicks develop endothermy and are able to defend their Tb at between 12 and 17 days, and at 30% of adult body mass. The chicks reduced MR by up to 41% below the predicted RMR, almost twice below the torpor threshold of 25% below RMR. Two chicks remained in shallow torpor for nearly half the night, and all chicks displayed a day–night oscillation in MR, with an average reduction of metabolism and Ts greater than previously reported for the heavier adult Japanese quail (Hohtola et al., 1991).

Ts and the development of endothermy

The Ts of king quail chicks in our study increased from 32.6°C at hatching to a maximum of ∼41°C at approximately 15 days. The latter is in line with the value of Tb=41.7°C reported in the TNZ by Roberts and Baudinette (1986) for the same species. This increase in Tb with development is well documented, and initially when chicks are small, it allows them to reduce energy expended for thermoregulation, by lowering Tb and reducing the differential between Ta and Tb (Hissa et al., 1983; Tzschentke and Nichelmann, 1999; Pis, 2003; Freeman, 1964). While most precocial birds are completely endothermic at 10 days of age (Nichelmann and Tzschentke, 2002), the age of onset of endothermy was positively correlated with growth rate (Dunn, 1975). Therefore, it is difficult to determine a specific age at which a species becomes fully endothermic because of individual variation in growth rates and probably also environmental variables (Beintema and Visser, 1989). However, the results of our study indicate that the crucial period for the onset of endothermy in king quail chicks is between 11 and 15 days, or when body mass reaches ∼13 g. This age range for this species is in agreement with Pearson (1994); however, Pis and Luśnia (2005) reported the onset of endothermy between 16 and 19 days in the king quail. Spiers et al. (1974) report 13–15 days for the Japanese quail Coturnix coturnix japonica, and 14 days for the Bobwhite quail Colinus virginianus (Spiers et al., 1985). Although quails are rather similar with regard to the development of thermoregulatory efficiency, this varies between precocial avian species, and is especially affected by size. In large ostrich and emu chicks, for example, homeothermy is well developed, and they are able to maintain a constant Tb soon after hatching (Tamura et al., 2003; Brown and Prior, 1999).

MR

The RMR of king quail chicks under thermoneutral conditions at a body mass of 3.6–14.8 g in our study (Table 2) is similar to reports on the same species at 6–10 days, ranging between 4 and 7 ml O2 g−1 h−1 (Pearson, 1994). Bernstein (1973) reported lower values of RMR in king quail chicks at a body mass of 3–9 g, but a RMR of 6.3 ml O2 g−1 h−1 in a 6.8 g chick at Ta=25°C. Both studies reported an increase in RMR from the minimum value at hatching to a maximum shortly after hatching, indicating an increase in the capacity for heat production with growth, followed by a decrease, reflecting a decrease in the metabolic requirements for heat production (Bernstein, 1973; Pearson, 1994). The same polynomial relationship between body mass and oxygen consumption has also been reported in other bird species (domestic pigeon: Riddle et al., 1932; red-necked pheasant, domestic fowl and California quail: Koskimies 1962). The changes in RMR in the chicks aged 3–12 days in our study was highly variable and independent of body mass. Bernstein (1973) reported lowest values of MR in the first days after hatching, at a body mass <4 g, maximum RMR at about 4–12 g and a decrease starting at about 15 g (fig. 3 in Bernstein, 1973). Our MR trial period was shorter than in the other king quail studies, and started only on day 3, at a body mass of almost 4 g, so the lower values are probably missing from our data. Our data of RMR at 3–12 days, therefore, probably depicted the peak values of RMR, between the phases of low RMR just after hatching and later at the decrease of metabolic requirement, and therefore were not explained by body mass.

Torpor

The fast development of thermoregulation in the precocial king quail is followed by the ability to express shallow torpor at a young age under mild thermal conditions. The king quail chicks in our study expressed torpor between the ages of 14 and 17 days for a brief window during their development, when their ability to defend high Tb was rather limited. Torpor was characterised by a substantial but reversible reduction in MR around and soon after midnight. Although chicks were able to rewarm from the first torpor bout via an increase in MR independently of Ta (a controlled response, hence defined as torpor), their MR and Ts decreased again by the end of the night, but they rewarmed passively only after extraction from the chamber. They were therefore deemed to be hypothermic (Geiser et al., 2014). Similar behaviour was observed in young crimson chat (Epthianura tricolor) and captive young banded whiteface (Aphelocephala nigricincta) by Ives (1973), that spent the night appearing to be in a state of torpor. When they were handled in the morning, they were still inert, and passively rewarmed gradually with increasing morning warmth (Ives, 1973). More anecdotal evidence on passive arousal from torpor in birds has been reported for white-backed swallow (Cheramoeca leucosternum; Serventy, 1970) and welcome swallow (Hirundo neoxena; Dove, 1923). Marsupial dunnarts (Sminthopsis crassicaudata) also had an intermittent phase between a poikilothermic phase and a completely endothermic phase, in which the young enter into what appears to be torpor, but could only rewarm passively when basking under a heat lamp (Wacker et al., 2017).

Our data suggest that torpor can be expressed when quail chicks are at their early postnatal phase, where thermoregulatory efficiency is still developing, but heat loss is high (Nichelmann and Tzschentke, 2002). Indeed, the chicks expressing torpor also had the slowest growth rate (Fig. 1), supporting the occurrence of torpor during this time only in those chicks that developed competent endothermy later than the others. The flexible thermoenergetics obtained at this point was apparently used as a survival strategy in response to the mild thermal challenge. However, the rapid fall of MR after the increase during rewarming from torpor before the end of the dark phase implies an exhaustion of their energy reserves as they appeared unable to maintain a high Tb at Ta lower than thermoneutrality. When the chicks were more mature (on the second night of measurements on day 21), they no longer expressed torpor, but maintained a high MR throughout the night. This sequence of expressing torpor immediately when the animal is able to control Tb varies among species. Some mammalian and avian species may express torpor at early stages of development and decrease torpor frequency with age (Renninger et al., 2020; Geiser et al., 2019; Geiser, 1988; Prinzinger and Siedle, 1988), whereas some placental mammals appear to express torpor only after a transient homeothermic phase, where Tb is high and constant following the poikilothermic phase (Bae et al., 2003; Geiser and Kenagy, 1990).

Those chicks that did not express torpor, according to our definition, still reduced metabolism and Ts during the rest phase, but not to the extent that we can define it as torpor. We did not measure Ts during the night in all birds to avoid interference with the MR measurements and risk that this interference would prevent torpor, but also because we were more interested in the energy currency, rather than the reduction of their Tb. However, we did measure Ts in four birds and can also calculate the expected Ts given the MR measurements. The amplitude of Ts fluctuation for the three chicks that were measured at 22:00 h (and did not express torpor according to our MR definition), was 5.6, 5.4 and 2.8°C. This fluctuation is much larger than the 1°C difference in Tb between the active and rest phases that has been reported in adult Japanese quails under normothermic conditions (Hohtola et al., 1991). Prinzinger et al. (1991) suggested a normal range of Tb fluctuation (day/night) of 2.48–1.25°C for birds weighing between 10 and 100,000 g, decreasing with increasing body mass. While a reduction of Tb may provide a potential definition of torpor accompanying the reduction in metabolic rate, it is first necessary to determine the rest phase values as a standard reference to be able to define it (Schleucher, 2004). Considering a rest phase Tb of 38.9°C in birds from the order Galliformes (Prinzinger et al., 1991), the Tb reductions in the three chicks that did not express torpor would only be 3.5, 3.3 and 1.1°C, all smaller than the 5°C Tb reduction torpor threshold (Ruf and Geiser, 2015), and 5.1°C in the chick that did express torpor, before MR reached the lowest value. However, if we calculate the Ts for the minimum MR for the chicks that expressed torpor using thermal conductance (Schleucher and Withers, 2001), the Ts calculated is 29.2 and 31.8°C in chicks 2 and 1, respectively. These calculated values are 4.7 and 2.1°C below the torpor threshold of 33.9°C, and 7–10°C below the resting phase Tb.

Torpor may be used at times of energetic emergency, such as starvation, and not as a developmental strategy to save energy while encountering a minor thermal challenge. Fork-tailed storm petrel, Wilson’ storm petrels (Oceanites oceanicus) and house martin (Delichon u. urbica) chicks expressed torpor only after a period of food shortage or starvation (Boersma, 1986; Prinzinger and Siedle, 1988; Kuepper et al., 2018), while Antarctic petrel chicks (Thalassoica antarctica) maintained high Tb (>36°C) throughout the day even if Ta decreased below −15°C (Bech et al., 1991). Juvenile garden dormice (Eliomys quercinus), exposed to an intermittent starvation trial, expressed torpor at about 6 weeks of age, gained mass at the same rate as juveniles fed ad libitum, and reached similar pre-hibernation fattening (Giroud et al., 2014). The juveniles fed ad libitum at Ta=6°C entered torpor only after gaining maximum body mass at the age of about 12 weeks (Giroud et al., 2012; Giroud et al., 2014). It is therefore likely that because of the risk of slower growth rate as a result of reduced Tb (McAllan and Geiser, 2014; Racey and Swift, 1981), chicks do not use torpor as a regular developmental strategy to save energy, but rather as a strategy to overcome extreme challenges such as starvation. A greater thermal challenge, or prolonged starvation, as in Alpine swift (Apus melba) chicks (Bize et al., 2007), may possibly trigger chicks in older age groups to use torpor.

Our study shows that king quail chicks may express torpor soon after developing endothermy. Although they were able to increase metabolism and rewarm from the torpor bout at night, they were unable to maintain a high MR until the following morning, suggesting their energy reserves were depleted when exposed to a minor thermal challenge. Our data therefore suggest that this heterothermic step requires that king quail chicks have access to a parental or other external heat source to rewarm and benefit from torpor to overcome energetically challenging periods. Our study is the first to show torpor in the early stages of development in a precocial bird, and suggests that torpor may be a more common strategy during challenging conditions for developing birds, which deserves to be investigated further.

Author contributions

Conceptualization: Y.A., G.K., F.G.; Methodology: Y.A., G.K., C.W., F.G.; Software: G.K.; Formal analysis: Y.A.; Investigation: Y.A.; Writing - original draft: Y.A.; Writing - review & editing: G.K., C.W., F.G.; Supervision: F.G.; Project administration: Y.A.; Funding acquisition: Y.A.

Funding

This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Data availability

The datasets generated during the current study are available from Dryad (Aharon-Rotman et al., 2020): dryad.brv15dv80

Abraham
,
C. L.
and
Evans
,
R. M.
(
1999
).
The development of endothermy in American white pelicans
.
The Condor
101
,
832
-
841
.
Aharon-Rotman
,
Y.
,
Körtner
,
G.
,
Wacker
,
C. B.
and
Geiser
,
F.
(
2020
).
Metabolic rates and growth data for: Do small precocial birds enter torpor to conserve energy during development? Dryad Dataset
.
Andreasson
,
F.
,
Nord
,
A.
and
Nilsson
,
J.-Å.
(
2016
).
Brood size constrains the development of endothermy in blue tits
.
J. Exp. Biol.
219
,
2212
-
2219
.
Andreasson
,
F.
,
Nord
,
A.
and
Nilsson
,
J.-Å.
(
2019
).
Age-dependent effects of predation risk on night-time hypothermia in two wintering passerine species
.
Oecologia
189
,
329
-
337
.
Bae
,
H. H.
,
Larkin
,
J. E.
and
Zucker
,
I.
(
2003
).
Juvenile Siberian hamsters display torpor and modified locomotor activity and body temperature rhythms in response to reduced food availability
.
Physiol. Biochem. Zool.
76
,
858
-
867
.
Bech
,
C.
,
Mehlum
,
F.
and
Haftorn
,
S.
(
1991
).
Thermoregulatory abilities in chicks of the Antarctic Petrel Thalassoica antarctica
.
Polar Biol.
11
,
233
-
238
.
Beintema
,
A.
and
Visser
,
G. H.
(
1989
).
The effect of weather on time budgets and development of chicks of meadow birds
.
Ardea
77
,
181
-
192
.
Bernstein
,
M. H.
(
1973
).
Development of thermoregulation in painted quail, Excalfactoria chinensis
.
Comparative Biochemistry and Physiology Part A: Physiology
44
,
355
-
366
.
Bize
,
P.
,
Klopfenstein
,
A.
,
Jeanneret
,
C.
and
Roulin
,
A.
(
2007
).
Intra-individual variation in body temperature and pectoral muscle size in nestling Alpine swifts Apus melba in response to an episode of inclement weather
.
Journal of Ornithology
148
,
387
-
393
.
Boersma
,
P. D.
(
1986
).
Body temperature, torpor, and growth in chicks of fork-tailed storm-petrels (Oceanodroma furcata)
.
Physiol. Zool.
59
,
10
-
19
.
Boersma
,
P. D.
and
Wheelwright
,
N. T.
(
1979
).
Egg neglect in the Procellariiformes: reproductive adaptations in the Fork-tailed Storm-Petrel
.
The Condor
81
,
157
-
165
.
Bondarenco
,
A.
,
Körtner
,
G.
and
Geiser
,
F.
(
2014
).
Hot bats: extreme thermal tolerance in a desert heat wave
.
Naturwissenschaften
101
,
679
-
685
.
Brigham
,
R. M.
(
1992
).
Daily torpor in a free-ranging goatsucker, the common poorwill (Phalaenoptilus nuttallii)
.
Physiol. Zool.
65
,
457
-
472
.
Brown
,
C.
and
Prior
,
S.
(
1999
).
Development of body temperature regulation in ostrich chicks
.
Br. Poult. Sci.
40
,
529
-
535
.
Dawson
,
W. R.
and
Evans
,
F. C.
(
1957
).
Relation of growth and development to temperature regulation in nestling field and chipping sparrows
.
Physiol. Zool.
30
,
315
-
327
.
Dawson
,
W. R.
and
Evans
,
F. C.
(
1960
).
Relation of growth and development to temperature regulation in nestling Vesper Sparrows
.
The Condor
62
,
329
-
340
.
Dove
,
S.
(
1923
).
Semi-Hibernation of Swallows
.
Emu-Austral Ornithology
23
,
149
.
Dunn
,
E. H.
(
1975
).
The timing of endothermy in the development of altrical birds
.
The Condor
77
,
288
-
293
.
Dunn
,
E. H.
(
1976
).
Development of endothermy and existence energy expenditure of nestling Double-crested Cormorants
.
The Condor
78
,
350
-
356
.
Dzialowski
,
E.
,
Burggren
,
W.
,
Komoro
,
T.
and
Tazawa
,
H.
(
2007
).
Development of endothermic metabolic response in embryos and hatchlings of the emu (Dromaius novaehollandiae)
.
Respir. Physiol. Neurobiol.
155
,
286
-
292
.
Eichhorn
,
G.
,
Groscolas
,
R.
,
Le Glaunec
,
G.
,
Parisel
,
C.
,
Arnold
,
L.
,
Medina
,
P.
and
Handrich
,
Y.
(
2011
).
Heterothermy in growing king penguins
.
Nat. Commun.
2
,
1
-
7
.
Freeman
,
B.
(
1964
).
The emergence of the homeothermic-metabolic response in the fowl (Gallus domesticus)
.
Comp. Biochem. Physiol.
13
,
413
-
422
.
Geiser
,
F.
(
1988
).
Daily torpor and thermoregulation in Antechinus (Marsupialia): influence of body mass, season, development, reproduction, and sex
.
Oecologia
77
,
395
-
399
.
Geiser
,
F.
, and
Brigham
,
R. M.,
(
2012
).
The other functions of torpor
. In
Living in a seasonal world
(eds
T.
Ruf
,
C.
Bieber
,
W.
Arnold
and
E.
Millesi
), pp.
109
-
121
.
Berlin
:
Springer
.
Geiser
,
F.
and
Kenagy
,
G.
(
1990
).
Development of thermoregulation and torpor in the golden-mantled ground squirrel Spermophilus saturatus
.
J. Mammal.
71
,
286
-
290
.
Geiser
,
F.
,
Westman
,
W.
,
McAllan
,
B. M.
and
Brigham
,
R. M.
(
2006
).
Development of thermoregulation and torpor in a marsupial: energetic and evolutionary implications
.
Journal of Comparative Physiology B
176
,
107
-
116
.
Geiser
,
F.
,
Currie
,
S. E.
,
O'Shea
,
K. A.
and
Hiebert
,
S. M.
(
2014
).
Torpor and hypothermia: reversed hysteresis of metabolic rate and body temperature
.
American Journal of Physiology-Regulatory, Integrative and Comparative Physiology
307
,
R1324
-
R1329
.
Geiser
,
F.
,
Wen
,
J.
,
Sukhchuluun
,
G.
,
Chi
,
Q.-S.
and
Wang
,
D.-H.
(
2019
).
Precocious torpor in an altricial mammal: the functional implications of heterothermy during development
.
Frontiers in Physiology
10
,
469
.
Giroud
,
S.
,
Turbill
,
C.
and
Ruf
,
T.
(
2012
).
Torpor use and body mass gain during pre-hibernation in late-born juvenile garden dormice exposed to food shortage
. In
Living in a Seasonal World
(eds
T.
Ruf
,
C.
Bieber
,
W.
Arnold
and
E.
Millesi
), pp.
481
-
491
.
Berlin
:
Springer
.
Giroud
,
S.
,
Zahn
,
S.
,
Criscuolo
,
F.
,
Chery
,
I.
,
Blanc
,
S.
,
Turbill
,
C.
and
Ruf
,
T.
(
2014
).
Late-born intermittently fasted juvenile garden dormice use torpor to grow and fatten prior to hibernation: consequences for ageing processes
.
Proc. R. Soc. B
281
,
20141131
.
Hiebert
,
S.
(
1993
).
Seasonal changes in body mass and use of torpor in a migratory hummingbird
.
The Auk
110
,
787
-
797
.
Hissa
,
R.
,
Saarela
,
S.
,
Rintamäki
,
H.
,
Lindén
,
H.
and
Hohtola
,
E.
(
1983
).
Energetics and development of temperature regulation in capercaillie Tetrao urogallus
.
Physiol. Zool.
56
,
142
-
151
.
Hohtola
,
E.
and
Visser
,
G. H.
(
1998
).
Development of locomotion and endothermy in altricial and precocial birds
.
Oxf. Ornithol. Ser.
8
,
57
-
173
.
Hohtola
,
E.
,
Hissa
,
R.
,
Pyörnilä
,
A.
,
Rintamäki
,
H.
and
Saarela
,
S.
(
1991
).
Nocturnal hypothermia in fasting Japanese quail: the effect of ambient temperature
.
Physiol. Behav.
49
,
563
-
567
.
Hudson
,
J. W.
and
Scott
,
I. M.
(
1979
).
Daily torpor in the laboratory mouse, Mus musculus var. albino
.
Physiol. Zool.
52
,
205
-
218
.
Ives
,
N.
(
1973
).
Overnight torpidity in Australian arid-country birds
.
Emu-Austral Ornithology
73
, 140.
Jensen
,
C.
and
Bech
,
C.
(
1992
).
Oxygen consumption and acid-base balance during shallow hypothermia in the pigeon
.
Respiration Physiology
88
,
193
-
204
.
Koskimies
,
J.
(
1962
).
Ontogeny of thermoregulation and energy metabolism in some gallinaceous birds
.
Ricerche Zool Appl Caccia
4
,
149
-
160
.
Kuepper
,
N. D.
,
Marek
,
C.
,
Coria
,
N.
,
Libertelli
,
M. M.
and
Quillfeldt
,
P.
(
2018
).
Facultative hypothermia as a survival strategy during snowstorm induced food shortages in Antarctic storm-petrel chicks
.
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
224
,
76
-
83
.
Levy
,
A.
(
1964
).
The accuracy of the bubble meter method for gas flow measurements
.
Journal of Scientific Instruments
41
,
449
.
McAllan
,
B. M.
and
Geiser
,
F.
(
2014
).
Torpor during reproduction in mammals and birds: dealing with an energetic conundrum
.
Integrative and Comparative Biology
54
,
516
-
532
.
McKechnie
,
A. E.
and
Lovegrove
,
B. G.
(
2002
).
Avian facultative hypothermic responses: a review
.
The Condor
104
,
705
-
724
.
McKechnie
,
A. E.
,
Freckleton
,
R. P.
and
Jetz
,
W.
(
2006
).
Phenotypic plasticity in the scaling of avian basal metabolic rate
.
Proc. R. Soc. B
273
,
931
-
993
.
McKechnie
,
A. E.
,
Ashdown
,
R. A.
,
Christian
,
M. B.
and
Brigham
,
R. M.
(
2007
).
Torpor in an African caprimulgid, the freckled nightjar Caprimulgus tristigma
.
J. Avian Biol.
38
,
261
-
266
.
Nagel
,
A.
(
1977
).
Torpor in the European white-toothed shrews
.
Experientia
33
,
1455
-
1456
.
Nichelmann
,
M.
and
Tzschentke
,
B.
(
2002
).
Ontogeny of thermoregulation in precocial birds
.
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
131
,
751
-
763
.
Nowack
,
J.
,
Stawski
,
C.
and
Geiser
,
F.
(
2017
).
More functions of torpor and their roles in a changing world
.
Journal of Comparative Physiology B
187
,
889
-
897
.
Pearson
,
J.
(
1994
).
Oxygen consumption rates of adults and chicks during brooding in king quail (Coturnix chinensis)
.
Journal of Comparative Physiology B
164
,
415
-
424
.
Pis
,
T.
(
2003
).
Energy metabolism and thermoregulation in hand-reared chukars (Alectoris chukar)
.
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
136
,
757
-
770
.
Pis
,
T.
and
Luśnia
,
D.
(
2005
).
Growth rate and thermoregulation in reared king quails (Coturnix chinensis)
.
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
140
,
101
-
109
.
Price
,
E. R.
and
Dzialowski
,
E. M.
(
2018
).
Development of endothermy in birds: patterns and mechanisms
.
Journal of Comparative Physiology B
188
,
373
-
391
.
Prinzinger
,
R.
and
Siedle
,
K.
(
1988
).
Ontogeny of metabolism, thermoregulation and torpor in the house martin Delichon u. urbica (L.) and its ecological significance
.
Oecologia
76
,
307
-
312
.
Prinzinger
,
R.
,
Preßmar
,
A.
and
Schleucher
,
E.
(
1991
).
Body temperature in birds
.
Comparative Biochemistry and Physiology Part A: Physiology
99
,
499
-
506
.
Racey
,
P.
and
Swift
,
S. M.
(
1981
).
Variations in gestation length in a colony of pipistrelle bats (Pipistrellus pipistrellus) from year to year
.
Reproduction
61
,
123
-
129
.
Renninger
,
M.
,
Sprau
,
L.
and
Geiser
,
F.
(
2020
).
White mouse pups can use torpor for energy conservation
.
Journal of Comparative Physiology B
190
,
253
-
259
.
Ricklefs
,
R. E.
(
1974
).
The energetics of reproduction in birds
.
Avian Energetics
15
,
152
-
297
.
Ricklefs
,
R. E.
(
1984
).
The optimization of growth rate in altricial birds
.
Ecology
65
,
1602
-
1616
.
Ricklefs
,
R. E.
(
1987
).
Characterizing the development of homeothermy by rate of body cooling
.
Funct. Ecol.
1
,
151
-
157
.
Riddle
,
O.
,
Nussmann
,
T. C.
and
Benedict
,
F. G.
(
1932
).
Metabolism during growth in a common pigeon
.
American Journal of Physiology-Legacy Content
101
,
251
-
259
.
Roberts
,
J. R.
and
Baudinette
,
R. V.
(
1986
).
Thermoregulation, oxygen-consumption and water turnover in stubble quail, Coturnix pectoralis, and king quail, Coturnix chinensis
.
Aust. J. Zool.
34
,
25
-
33
.
Ruf
,
T.
and
Geiser
,
F.
(
2015
).
Daily torpor and hibernation in birds and mammals
.
Biol. Rev.
90
,
891
-
926
.
Schleucher
,
E.
(
2004
).
Torpor in birds: taxonomy, energetics, and ecology
.
Physiol. Biochem. Zool.
77
,
942
-
949
.
Schleucher
,
E.
and
Withers
,
P. C.
(
2001
).
Re-evaluation of the allometry of wet thermal conductance for birds
.
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
129
,
821
-
827
.
Serventy
,
D. L.
(
1970
).
Torpidity in the white-backed swallow
.
Emu-Austral Ornithology
70
,
27
-
28
.
Sirsat
,
S. K.
,
Sirsat
,
T. S.
,
Faber
,
A.
,
Duquaine
,
A.
,
Winnick
,
S.
,
Sotherland
,
P. R.
and
Dzialowski
,
E. M.
(
2016
).
Development of endothermy and concomitant increases in cardiac and skeletal muscle mitochondrial respiration in the precocial Pekin duck (Anas platyrhynchos domestica)
.
J. Exp. Biol.
219
,
1214
-
1223
.
Smit
,
B.
and
McKechnie
,
A. E.
(
2010
).
Do owls use torpor? Winter thermoregulation in free-ranging pearl-spotted owlets and African scops-owls
.
Physiol. Biochem. Zool.
83
,
149
-
156
.
Spiers
,
D. E.
,
McNabb
,
R. A.
and
McNabb
,
F. A.
(
1974
).
The development of thermoregulatory ability, heat seeking activities, and thyroid function in hatchling Japanese quail (Coturnix coturnix japonica)
.
J. Comp. Physiol.
89
,
159
-
174
.
Spiers
,
D. E.
,
Adams
,
T.
and
Ringer
,
R. K.
(
1985
).
Homeothermic development in the bobwhite (Colinus virginianus)
.
Comparative Biochemistry and Physiology Part A: Physiology
81
,
921
-
927
.
Swanson
,
D. L.
and
Weinacht
,
D. P.
(
1997
).
Seasonal effects on metabolism and thermoregulation in northern bobwhite
.
The Condor
99
,
478
-
489
.
Tamura
,
A.
,
Akiyama
,
R.
,
Chiba
,
Y.
,
Moriya
,
K.
,
Dzialowski
,
E.
,
Burggren
,
W.
and
Tazawa
,
H.
(
2003
).
Heart rate responses to cooling in emu hatchlings
.
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
134
,
829
-
838
.
Tsoularis
,
A.
and
Wallace
,
J.
(
2002
).
Analysis of logistic growth models
.
Math. Biosci.
179
,
21
-
55
.
Tzschentke
,
B.
and
Nichelmann
,
M.
(
1999
).
Development of avian thermoregulatory system during the early postnatal period: development of the thermoregulatory set-point
.
Ornis Fenn.
76
,
189
-
198
.
Visser
,
G. H.
and
Ricklefs
,
R. E.
(
1993
).
Development of temperature regulation in shorebirds
.
Physiol. Zool.
66
,
771
-
792
.
Wacker
,
C. B.
,
McAllan
,
B. M.
,
Körtner
,
G.
and
Geiser
,
F.
(
2017
).
The role of basking in the development of endothermy and torpor in a marsupial
.
Journal of Comparative Physiology B
187
,
1029
-
1038
.
Wheelwright
,
N. T.
and
Boersma
,
P. D.
(
1979
).
Egg chilling and the thermal environment of the Fork-tailed Storm Petrel (Oceanodroma furcata) nest
.
Physiol. Zool.
52
,
231
-
239
.
Willis
,
C. K. R.
(
2007
).
An energy-based body temperature threshold between torpor and normothermia for small mammals
.
Physiol. Biochem. Zool.
80
,
643
-
651
.
Withers
,
P. C.
(
1977
).
Measurement of VO2, VCO2, and evaporative water loss with a flow-through mask
.
J. Appl. Physiol.
42
,
120
-
123
.
Yahav
,
S.
(
2015
).
Regulation of body temperature: strategies and mechanisms
. In
Sturkie's Avian Physiology
, pp.
869
-
905
.
Elsevier
.
Zuur
,
A.
,
Ieno
,
E. N.
,
Walker
,
N.
,
Saveliev
,
A. A.
and
Smith
,
G. M.
(
2009
).
Mixed effects models and extensions in ecology with R
.
Springer Science & Business Media
.

Competing interests

The authors declare no competing or financial interests.

Supplementary information