Skip to main content

Endocrine response of early-hatching Asian Short-toed Lark nestlings exposed to cold temperature in a high-latitude grassland habitat

Abstract

Background

In high latitude grassland habitats, altricial nestlings hatching in open-cup nests early in the breeding season must cope with cold temperature challenges. Thyroid hormones (triiodothyronine, T3 and thyroxine, T4) and corticosterone play a crucial role in avian thermoregulation response to cold. Investigating the endocrine response of altricial nestlings to temperature variation is important for understanding the adaptive mechanisms of individual variation in the timing of breeding in birds.

Methods

We compared nest temperature, ambient temperature, body temperature, plasma T3, T4 and corticosterone levels in Asian Short-toed Lark (Alaudala cheleensis) nestlings hatching in the early-, middle-, and late-stages of the breeding season in Hulunbuir grassland, northeast China.

Results

Mean nest temperature in the early-, middle- and late-stage groups was − 1.85, 3.81 and 10.23 °C, respectively, for the 3-day-old nestlings, and 6.83, 10.41 and 11.81 °C, respectively, for the 6-day-old nestlings. The nest temperature significantly correlated with body temperature, plasma T3, T4 and corticosterone concentrations of nestlings. Body temperature of 3-day-old nestlings in the early and middle groups was significantly lower than that of the late group, but there was no significant difference between the nestlings in the early and middle groups. The T4 and T3 concentrations and the ratio of T3/T4 of both 3- and 6-day-old nestlings in the early-stage group were significantly higher compared to the middle and late groups. The corticosterone levels of 3-day-old nestlings were significantly higher in the early-stage group compared to the middle- and late-stage groups.

Conclusion

Nestlings hatching early responded to cold temperature by increasing thyroid hormones and corticosterone levels even in the early days of post hatching development when the endothermy has not been established. These hormones may play a physiological role in neonatal nestlings coping with cold temperature challenges.

Background

Timing of breeding is a key component of fitness for birds inhabiting highly seasonal environments. To enhance reproductive success, the development phase of nestlings tends to occur when environmental conditions are optimal. Nevertheless, there is significant within-year variation in the timing of breeding between individuals within populations (Arnold 1992; van der Jeugd and McCleery 2002; McCleery et al. 2004). Individuals that breed early in the season may benefit from acquiring better nesting locations and mates (Møller 1994; Smith and Moore 2005; Gunnarsson et al. 2006; Janiszewski et al. 2013). However, because altricial bird nestlings are featherless and unable to regulate their body temperature during the early stages of development (Pearson 1998; Østnes et al. 2001; Sirsat et al. 2016), one disadvantage of breeding early is that nestlings must deal with cold temperatures (Rotics et al. 2018). This is particularly the case for altricial nestlings raised in open-cup nests in exposed high latitude locations (MacDonald et al. 2013). Thus, understanding the adaptive mechanisms of individual variation in the breeding time of birds inhabiting highly seasonal environments requires determining how nestlings respond to cold ambient temperatures in early spring.

The endocrine system plays a crucial role in avian thermoregulation to cope with changes in external environments (Klandorf et al. 1981; Zheng et al. 2014). The most important hormone controlling thermogenesis is the thyroid hormones (triiodothyronine, T3 and thyroxine, T4) (Klandorf et al. 1981; Decuypere et al. 2005; Zheng et al. 2014). Cold exposure in adult birds can accelerate the conversion of T4 to T3 by deiodinase enzymes in tissues, particularly in the liver (Van der Geyten et al. 1999; Collin et al. 2003), resulting in higher circulating T3 levels. T3 binds to nuclear and mitochondrial receptors in tissues and influences gene expression thus modulating metabolic rates and respiration (Arieli and Berman 1979). Experimental elevation of thyroid hormones in blood has been shown to increase thermogenesis in Little Buntings (Emperiza pusilla) (Liu et al. 2006), and correlations between thyroid hormones and thermogenesis have been observed in Goldfinches (Carduelis tristis) (Dawson et al. 1992), Great Tits (Parus major) and Willow Tits (Parus montanus) (Silverin et al. 1989). Additionally, a positive correlation was observed between thyroid hormones and basal metabolic rate (BMR) in free-ranging bird populations (Chastel et al. 2003; Vézina et al. 2009). Cold temperature also can activate the hypothalamic pituitary adrenal axis and increase corticosterone secretion to regulate metabolism (Bruijn and Romero 2011; Wingfield et al. 2017; Blanca et al. 2018; Lassiter et al. 2018) and involved in thermoregulation of birds (Frigerio et al. 2004; Bize et al. 2010). Mitochondrial corticosterone receptors have recently been detected in avian muscle cells, suggesting corticosterone also play a role in regulating mitochondrial activity, thus energy production (Lassiter et al. 2018). Recent studies in Blue Tits (Cyanistes caeruleus) suggest there may be an association between baseline corticosterone, peripheral body temperature, and gradual changes in temperature over winter and summer (Jerem et al. 2018).

Unlike adult birds, thyroid function in altricial nestlings is weak upon hatching but increases over the first few days of development while the nestlings are still ectothermic (McNabb et al. 1984; Olson et al. 1999; Price and Dzialowski 2018). During nestling development, the size of the thyroid gland increases, with the fastest growth occurring just before the development of endothermy (McNabb and Cheng 1985). Consistent with the pattern of thyroid growth, thyroid hormones are low at hatching, then steadily increase immediately prior to, or concurrent with, the development of endothermy, e.g. in Ring-necked Doves (Streptopelia capicola; McNabb and Cheng 1985), European Starlings (Sturnus vulgaris; Schew et al. 1996; Výboh et al. 1996), and Great Tits (Silverin and Rudas 1996). The functional development of the thyroid is crucial for the development of endothermic capabilities, and thyroid hormones play an important role in endothermic responses to cold temperature (Price and Dzialowski 2018). Studies on nestlings of Black Kites (Milvus migrans) and Zebra Finches (Taeniopygia guttata) have shown that circulating corticosterone levels in nestlings often increases in response to cold stress, which suggests corticosterone plays a role in thermogenesis in nestlings (López-Jiménez et al. 2016; Crino et al. 2020). To date, thermoregulation in ectothermic nestlings is thought to rely largely on the warmth provided by adult birds and few field studies have tested whether ectothermic nestlings adapt to cold temperatures by enhancing thyroid hormones and corticosterone secretion. Understanding the physiological response of nestlings to cold temperatures is particularly important regarding altricial nestlings developing in open-cup nests as they are left exposed to the environments when adults leave the nest.

Asian Short-toed Larks (Alaudala cheleensis) are widely distributed across the Hulunbuir grassland in northeast China and provide an ideal model for studying the physiological response of altricial nestlings to variations in ambient temperature. Hulunbuir is a grassland ecosystem with a temperate continental climate where diurnal and seasonal variations in temperature are extreme (Yang 2014). Asian Short-toed Larks build open-cup nests on the ground in the open grassland (Tian 2015). Egg hatching in the Hulunbuir grassland population falls between mid-May and mid-June with hatch dates varying by up to 30 days between individuals and the ambient temperature gradually increases over the hatching period, exposing nestlings to different temperatures (Zhang et al. 2017a). Nestlings hatching earlier in spring must be able to deal with cold conditions to survive. The aim of our study was to determine whether Asian Short-toed Lark nestlings hatching at different stages regulate thyroid hormones and corticosterone secretion in response to changes in environment temperature.

In this paper, we hypothesized that nestlings hatching early in the breeding season have higher levels of thyroid hormones and corticosterone in response to cold temperatures. To investigate this, we compared nest temperature, ambient temperature, body temperature, plasma T4, T3 and corticosterone in Asian Short-toed Lark nestlings hatching in the early, middle and late stages of the breeding season in Hulunbuir grassland in 2019.

Methods

Study site and species

The study area was situated in the National Nature Reserve (47°45′50″N–49°20′20″N, 116°50′10″E–118°10′10″E) of Hulunbuir, in the northeastern portion of the Inner Mongolian Autonomous Region, China. This is a semiarid, steppe region where the mean annual temperature is − 0.6 °C and the average daily temperature in January and July is − 20.02 and 22.72 °C, respectively. The dominant plant species are Stipa krylovii, Leymus chinesis and Cleistogenes squarrosa. The Asian Short-toed Lark is the most common passerine species living on the Hulunbuir grasslands (Tian et al. 2015; Zhang et al. 2017a). This is an ideal species for testing our hypotheses as it raises a single brood in an open-cup nest on the ground, with egg laying dates varying between individuals within the population (Zhang et al. 2017a). The average clutch size is 3.05 ± 0.51, and nestlings remain in the nest for 8 days (Tian et al. 2015).

Field data and sample collection

Between 1 May and 20 June 2019, we monitored Asian Short-toed Lark nests daily to record hatching dates. The nestlings were divided into three 8-day groups according to their hatch date; an early-stage group (hatching between 10 and 17 May), a middle-stage group (hatching between 18 and 25 May), and a late-stage group (hatching between 26 May and 2 June). In total, 41 3-day-old (13 early, 15 middle, 13 late) and 48 6-day-old (14 early, 18 middle, 16 late) nestlings from different nests were monitored. A FLIR C3 (FLIR Systems, USA) infrared thermal imager was used to measure the nest temperature between 6:00 a.m. and 7:00 a.m. The thermal image was focused on the center of the nest, and nest temperature was calculated by taking the mean value of the temperature readings from the four corners of the image (thermal images are shown in Fig. 1). To prevent the influence of adult warming on the nest temperature measurement, we conducted a pre-experiment to determine the time it takes for the nest temperature to stabilize after the adult has left the nest. We did this by measuring the temperature of five nests where we observed the adult leaving the nest and found that the temperature reading became stable 20 min after the adult had left the nest. Thus, for our study, we waited 20 min before measuring the nest temperature to ensure that the adult had been absent from the nest for at least 20 min and that the temperature reading was not influenced by adult warming. After the nest temperature measurement, we collected approximately 100 μL of whole blood via brachial venipuncture from one 3-day-old and one 6-day-old nestlings from each nest. The blood was collected into heparinized microcapillary tubes and used to measure plasma T4, T3 and corticosterone levels. Immediately after blood collection, it was placed in an ice storage box then taken back to the lab at the study site within 1 h. Blood samples were centrifuged at 4000 rpm for 20 min. The resultant plasma was stored at − 20 °C until required for assays. After the blood sample collection, body temperature of 3- and 6-day-old nestlings were measured using a digital thermometer (UT325, Shenzhen Haixu Instrument, China) inserted into the cloaca. The daily minimum ambient temperature data were obtained from the Xinbarhu Meteorological Bureau.

Fig. 1
figure1

Infrared thermal images of Asian Short-toed Lark nests and nestlings. a1: nest and 3-day-old nestlings in the early-stage group (10–17 May); a2: nest and 3-day-old nestlings in the middle-stage group (18–25 May); a3: 3-day-old nestlings in the late-stage group (26 May–2 June); b1: nest and 6-day-old nestlings in the early-stage group; b2: nest and 6-day-old nestlings in the middle-stage group; b3: nest and 6-day-old nestlings in the late-stage group. The temperature range (°C) is indicated by the legend in each photograph

Hormone assay

Plasma T3, T4 and corticosterone levels were determined using enzyme-linked immunoassay kits (T3: Andy gene, AD0500Ch; T4: Andy gene, AD0499C; Corticosterone: Enzo, ADI-901-097). The kits have been validated for Asian Short-toed Larks by serial plasma dilutions following the method described in Zhang et al. (2017a). We followed the kit protocols, which included diluting 10 μL of the plasma samples with dilution buffer (1:5) for the assays. All samples were assayed in triplicate. The mean intra-assay coefficients of variation for T3 and T4 were less than 8% and the inter-assay coefficients were less than 10%, respectively. The intra- and inter plate coefficients of variation for corticosterone were 7.02% and 10.3%, respectively.

Data analysis

We used linear mixed models (LMMs) to analyze the effects of hatch stage (early, middle, and late), age (3- and 6-day-old), nest temperature, the interaction between age and hatch stage, and the interaction between age and nest temperature on plasma T3, T4, corticosterone concentrations, and body temperature. Age, nest temperature, hatch stage, and the interaction factors were modeled as fixed factors, with nest as a random factor. All the data was log transformed to correct for departures from normality and homogeneity of variance. For the factors showing a significant effect in the LMMs, we used a one-way ANOVA with a LSD multiple comparison test to determine the differences between groups or a Pearson correlation to determine the relationship between significant factors and dependent variables. All statistical analyses were performed in SPSS 22.0. P-values ≤ 0.05 were considered significant.

Results

Nest temperature and ambient temperature

The nest temperature for 3- and 6-day-old nestlings was significantly different between hatch groups (3-day-old: one-way ANOVA, F2,38 = 23.06, P < 0.001; 6-day-old: one-way ANOVA, F2,45 = 5.47, P < 0.01). The nest temperature in the early group was significantly lower than that of the middle- and late-stage groups (LSD test, P < 0.05), and for 3-day-old nestlings nest temperature was significantly lower in the middle-stage group compared to the late-stage group (LSD test, P < 0.05). Mean nest temperature in the early-, middle- and late-stage groups was − 1.85, 3.81 and 10.23 °C, respectively, for 3-day-old nestlings, and 6.83, 10.41 and 11.81 °C, respectively, for 6-day-old nestlings (Fig. 2). The minimum air temperature was significantly different between hatch stages (One way ANOVA, F2,22 = 4.598, P < 0.05). The air temperature of the early hatch stage was significantly lower than that of the middle and late stages (LSD test, P < 0.05) (Fig. 3).

Fig. 2
figure2

The nest temperature of 3- and 6-day-old Asian Short-toed Lark nestlings hatched in the early-stage (10–17 May), middle-stage (18–25 May) and late-stage (26 May–2 June). Different letters (a and b, b and c, a and c) indicate there are significant differences between groups (LSD test, P < 0.05), same letters (b and b) indicate there is no significant difference between groups (LSD test, P > 0.05)

Fig. 3
figure3

The minimum ambient temperature of the study area for early stage (10–17 May), middle stage (18–25 May) and late stage (26 May–2 June). Different letters (a and b) indicate there is significant difference between groups (LSD test, P < 0.05), and same letters (b and b) indicate there is no significant differences between groups (LSD test, P > 0.05)

Body temperature of nestlings

The Linear mixed model result for body temperature indicated that nest temperature, age, hatch stage, and the interactions between these factors, significantly influenced the body temperature of nestlings (Table 1). The body temperature of 3-day-old nestlings was positively correlated with nest temperature (Pearson correlation, r = 0.926, P < 0.001), but there was no significant correlation between body temperature and nest temperature for 6-d-old nestlings. Mean body temperature of 3- and 6-day-old nestlings was 27.4 and 37.9 °C, respectively (Fig. 4). The body temperature of 3-day-old nestlings was significantly different between the three hatch groups (one-way ANOVA, F2,38 = 18.37, P < 0.001). Body temperature of 3-day-old nestlings in the early and middle groups was significantly lower than that of the late group (LSD test, P < 0.05), while there was no significant difference between the early and middle groups (LSD test, P > 0.05) (Fig. 4). Nestling body temperature did not vary significantly with hatching stage in 6-day-old nestlings (Fig. 4).

Table 1 Results of linear mixed models for the effects of hatch stage (early, middle and late), age (3- and 6-day-old), nest temperature on body temperature, blood thyroid hormones (triiodothyronine, T3 and thyroxine, T4) and corticosterone concentration in wild Asian Short-toed Lark (Alaudala cheleensis) nestlings captured in Hulun Lake Nature Reserve, Inner Mongolia, China
Fig. 4
figure4

The body temperature of 3- and 6-day-old Asian Short-toed Lark nestlings hatched in the early-stage (10–17 May), middle-stage (18–25 May) and late-stage (26 May–2 June). Different letters (a and b) indicate there are significant differences between groups (LSD test, P < 0.05), same letters (b and b) indicate there is no significant difference between groups (LSD test, P > 0.05). There is no significant difference between hatch stage groups of 6-day-old nestlings

Plasma T4 and T3 concentration of nestlings

Linear mixed model results indicated that nest temperature, age, hatch stage, and the interaction between age and hatch stage, all significantly influenced nestling plasma T4 levels (Table 1). The T4 level of both 3- and 6-day-old nestlings was negatively correlated with nest temperature (Pearson correlation, 3-day-old: r =  − 0.842; P < 0.001; 6-day-old: r =  − 0.335, P < 0.05). There was a significant difference in plasma T4 concentration in 3- and 6-day-old nestlings hatched at different hatch stages (3-day-old: one way ANOVA, F2,38 = 13.39, P < 0.001; 6-day-old: one way ANOVA, F2,45 = 5.03, P < 0.05). The T4 concentration of 3- and 6-day-old nestlings in the early-stage group was significantly higher than that in the middle and late groups (LSD test, P < 0.05) (Fig. 5).

Fig. 5
figure5

The plasma T4 concentration of 3- and 6-day-old Asian Short-toed Lark nestlings hatched in the early-stage (10–17 May), middle-stage (18–25 May) and late-stage (26 May–2 June). Different letters (a and b) indicate there are significant differences between groups (LSD test, P < 0.05), same letters (b and b) indicate there is no significant difference between groups (LSD test, P > 0.05)

The linear mixed model results indicated that nest temperature and the interaction between age and hatch stage also significantly influenced nestling plasma T3 levels (Table 1). The T3 level of both 3- and 6-day-old nestlings was negatively correlated with nest temperature (Pearson correlation, 3-day-old: r =  − 0.921; P < 0.001; 6-day-old: r =  − 0.683, P < 0.001). There was a significant difference between hatch stages in plasma T3 concentration for 3-day-old nestlings (one way ANOVA, F2,38 = 15.44, P < 0.001). T3 concentration of nestlings in the early-stage group was significantly higher than that in the middle and late groups (LSD test, P < 0.05), and T3 concentration in the middle group was significantly higher than that in the late group (LSD test, P < 0.05) (Fig. 6).

Fig. 6
figure6

The plasma T3 concentration of 3- and 6-day-old Asian Short-toed Lark nestlings hatched in the early-stage (10–17 May), middle-stage (18–25 May) and late-stage (26 May–2 June). Different letters (a and b, a and c, b and c) indicate there are significant differences between groups (LSD test, P < 0.05), same letters (b and b) indicate there is no significant difference between groups (LSD test, P > 0.05)

There was a significant difference between hatch stages in plasma T3/T4 ratio of nestlings (3-day-old: one way ANOVA, F2,38 = 13.393, P < 0.001; 6-day-old: one way ANOVA, F2,38 = 3.885, P < 0.05). The T3/T4 ratio of 3-day old and 6-day old nestlings in the early-stage group was significantly higher than that in the middle and late groups (LSD test, P < 0.05), and the T3/T4 ratio of 3-day old nestlings in the middle stage was significantly higher than that in the late group (LSD test, P < 0.05) (Fig. 7).

Fig. 7
figure7

The plasma T3/T4 ratio of 3- and 6-day-old Asian Short-toed Lark nestlings hatched in the early-stage (10–17 May), middle-stage (18–25 May) and late-stage (26 May–2 June). Different letters (a and b, a and c, b and c) indicate there are significant differences between groups (LSD test, P < 0.05), same letters (b and b) indicate there is no significant difference between groups (LSD test, P > 0.05)

Plasma corticosterone of nestlings

The Linear mixed model result for corticosterone indicated that nest temperature and the interaction between age and hatch stage significantly influenced the concentration of plasma corticosterone in nestlings (Table 1). The corticosterone concentration in 3-day-old nestlings was negatively correlated with nest temperature (Pearson correlation, r =  − 0.825; P < 0.001). There was a significant difference between hatch stages in the plasma corticosterone concentration of 3-day-old nestlings (one way ANOVA, F2,38 = 6.7, P < 0.001). The corticosterone concentration of nestlings in the early-stage group was significantly higher than that in the middle and late groups (LSD test, P < 0.05) (Fig. 8).

Fig. 8
figure8

The plasma corticosterone concentration of 3- and 6-day-old Asian Short-toed Lark nestlings hatched in the early-stage (10–17 May), middle-stage (18–25 May) and late-stage (26 May–2 June). Different letters (a and b) indicate there is significant difference between groups (LSD test, P < 0.05), same letters (b and b) indicate there is no significant difference between groups (LSD test, P > 0.05). There is no significant difference between hatch stage groups of 6-day-old nestlings

Discussion

The nest temperature in the early-stage hatch group was significantly lower than that of the middle- and late-stage groups, which is consistent with the local ambient temperature variation trend. Nestlings hatching early in the breeding season are potentially exposed to sub-zero temperatures, while the temperature towards the middle and late stages of the breeding season is relatively mild, thus early hatching nestlings face greater cold temperature challenges. The significantly higher body temperature of 3-day-old nestlings hatching in the late-stage group compared to the early and middle stages indicates that nestlings of Asian Short-toed Larks are ectothermic during early development. The body temperature of nestlings in the three hatch stages increased significantly on day 6 after hatching and remained stable during all hatch stages at this age, a finding consistent with the thermogenesis development pattern seen in altricial birds in general (Price and Dzialowski 2018). Despite this overall trend, the body temperature data suggest that early hatched nestlings may have some capacity for thermogenesis, as evidenced by the fact that there was no significant difference in body temperature between the early and middle groups of 3-day-old nestlings, despite a significantly lower nest temperature during the early stage compared to the middle stage. Therefore, some minor capacity for thermogenesis may play a physiological role in early hatched nestlings coping with cold environment challenges.

Thyroid hormones can influence respiratory and metabolic levels in birds by regulating mitochondrial function and therefore regulating thermogenesis (Lassiter et al. 2018). We found T4 levels were higher in 6-day-old than 3-day-old nestlings suggesting that thyroid function is weak in newly hatched chicks, consistent with previous research on other altricial bird species (McNabb et al. 1984; Olson et al. 1999). However, the significantly higher T4 level in 3-day-old nestlings from the early hatch group indicates chicks hatching earlier in the breeding season tend to increase thyroid hormone secretion to cope with cold stress even though their thyroid function is still developing. The significantly higher T3 level and T3/T4 ratio observed in nestlings in the early hatch group compared to the middle and late groups indicates that nestlings hatching earlier in the season, when conditions are colder, have higher T4 to T3 conversion rates. T3 binds to both nuclear and mitochondrial receptors to modulate metabolic rates and respiration (Arieli and Berman 1979), therefore nestlings hatching in the early stage could increase thermogenesis by increasing thyroid hormone secretion. These results support our hypothesis that nestlings hatching early in the breeding season tend to have increased thyroid hormone secretion and conversion, which may speed up thermogenesis development in response to cold conditions. Additionally, T4 and T3 are also involved in regulating the growth of post-hatch nestlings (Schew et al. 1996). Therefore, higher levels of T4 and T3 may improve the growth rate of nestlings hatched at an early stage, something that should be tested in the future using growth data.

Our results showed that plasma corticosterone concentrations in 3-day-old nestlings in the early stage of the breeding season was significantly higher than that in the middle and late stages and corticosterone level in 3-day-old nestlings were negatively correlated with nest temperature, indicating that the activity of the HPA axis and therefore the secretion of corticosterone was greater in 3-day-old nestlings hatching in cold temperatures. An active HPA axis enables chicks to respond to cold environments by increasing mitochondrial activity (Lassiter et al. 2018), thus enhancing thermogenesis. However, we found no significant difference in corticosterone levels between the hatching stages for 6-day-old nestlings, indicating that the HPA axis’s regulatory effect on thermogenesis may weaken with maturation of the thyroid. The significant differences we observed in the levels of T3, T4, and corticosterone between the different stage hatch groups, suggests that the HPA axis in Asian Short-toed Lark nestlings may rapidly increase the function of the HPT axis during early development to the point where the HPT axis may function independently to regulate heat production. Additionally, higher corticosterone levels may increase the ability of newly hatched chicks to cope with cold conditions in the earlier stages of the breeding season.

Visser (1998) found that nestlings of altricial bird species did not respond to cold exposure with metabolic heat production during early development. Furthermore, in altricial species such as Ring-necked Doves, European Starlings and Great Tits, studies have found that thyroid hormone levels are very low at hatching, but steadily increase just prior to or simultaneously with the development of endothermy (McNabb and Cheng 1985; Schew et al. 1996; Silverin and Rudas 1996; Výboh et al. 1996). Our results for 3-day-old nestlings of Asian Short-toed Larks suggest that nestlings can increase thyroid hormone secretion during early development. This trait may be correlated with open-cup nesting and colder environments. To escape predators or inclement weather, rapid growth and physiological development is crucial for the survival of open-cup altricial nestlings (Camfield and Martin 2009; Coslovsky and Richner 2011; Cheng and Martin 2012). This concept is supported by our thyroid hormone results which demonstrate rapid thermogenesis development in Asian Short-toed Lark nestlings enabling them to leave the nest as young as 8 days old.

In this study, we looked at how three hormones in nestlings varied over three hatch stages. However, our findings cannot confirm whether the variation observed is due to phenotypic plasticity or genetic adaptation. The Clock gene poly-Q region has been found to be polymorphic in passerine populations and the length polymorphism in the Clock gene poly-Q region is positively correlated with the laying and hatching date for passerine birds (Liedvogel et al. 2009; Caprioli et al. 2012). Our previous study on Asian Short-toed Larks found that the shorter an individual’s Clock gene poly-Q mean allele length, the earlier its plasma LH, testosterone and estradiol values peaked. Additionally, Clock gene poly-Q allele length of nestlings in the same nest was positively correlated with the standardized laying date of the first egg in that nest (Zhang et al. 2017b). These results suggest that individual variation in the timing of reproduction may have a genetic basis. Therefore, the early hatched nestlings may have a genetic adaptation to cold temperature in the early stage of the breeding season. However, further research is required to support this theory.

Conclusions

Our findings suggest that nestlings hatching during the early stages of the breeding season can deal with cold temperatures by increasing activity of the hypothalamic-pituitary-thyroid axis and hypothalamic–pituitary–adrenal axis, even during early development when their body temperature is unstable. Because of the shorter breeding season typical of high latitude grasslands, there is a limited amount of time available for birds to breed. Within populations, individuals that breed early in the season can avoid competition for nest sites and food resources but face worse weather conditions as a consequence. Thyroid hormones and corticosterone may play a physiological function in nestlings enabling them to cope with cold temperature challenges, ensuring individuals can maximize breeding opportunities within a limited season.

Availability of data and materials

The data used in the present study are available from the corresponding author on reasonable request.

References

  1. Arieli A, Berman A. The effect of thyroxine on thermoregulation in the mature domestic fowl (Gallus domesticus). J Therm Biol. 1979;4:247–9.

    CAS  Article  Google Scholar 

  2. Arnold TW. Variation in laying date, clutch size, egg size, and egg composition of yellow-headed blackbirds (Xanthocephalus xanthocephalus): a supplemental feeding experiment. Can J Zool. 1992;70:1904–11.

    Article  Google Scholar 

  3. Bize P, Stocker A, Jenni-Eiermann S, Gasparini J, Roulin A. Sudden weather deterioration but not brood size affects baseline corticosterone levels in nestling Alpine swifts. Horm Behav. 2010;58:591–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  4. Blanca J, Michaela H, Simon V. Glucocorticoid-temperature association is shaped by foraging costs in individual zebra finches. J Exp Biol. 2018;221:23.

    Google Scholar 

  5. Bruijn RD, Romero LM. Behavioral and physiological responses of wild-caught European starlings (Sturnus vulgaris) to a minor, rapid change in ambient temperature. Comp Biochem Physiol A Mol Integr Physiol. 2011;160:260–6.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  6. Camfield AF, Martin K. The influence of ambient temperature on horned lark incubation behaviour in an alpine environment. Behaviour. 2009;146:1615–33.

    Article  Google Scholar 

  7. Caprioli M, Ambrosini R, Boncoraglio G, Gatti E, Romano A, Romano M, et al. Clock gene variation is associated with breeding phenology and maybe under directional selection in the migratory barn swallow. PLoS ONE. 2012;7:e35-140.

    Article  Google Scholar 

  8. Chastel O, Lacroix A, Kersten M. Pre-breeding energy requirements: thyroid hormone, metabolism and the timing of reproduction in house sparrows Passer domesticus. J Avian Biol. 2003;34:298–306.

    Article  Google Scholar 

  9. Cheng YR, Martin TE. Nest predation risk and growth strategies of passerine species: grow fast or develop traits to escape risk? Am Nat. 2012;180:285–95.

    PubMed  Article  PubMed Central  Google Scholar 

  10. Collin A, Buyse J, As PV, Darras VM, Malheiros RD, Moraes VMB, et al. Cold-induced enhancement of avian uncoupling protein expression, heat production, and triiodothyronine concentrations in broiler chicks. Gen Comp Endocrinol. 2003;130:70–7.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. Coslovsky M, Richner H. Predation risk affects offspring growth via maternal effects. Funct Ecol. 2011;25:878–88.

    Article  Google Scholar 

  12. Crinoa OL, Driscollb SC, Brandl HB, Buchanana KL, Griffith SC. Under the weather: corticosterone levels in wild nestlings are associated with ambient temperature and wind. Gen Comp Endocrinol. 2020;285:113247.

    Article  CAS  Google Scholar 

  13. Dawson WR, Carey C, Van’t Hof TJ, et al. Metabolic aspects of shivering thermogenesis in passerines during winter. Ornis Scand. 1992;23:381–7.

    Article  Google Scholar 

  14. Decuypere E, As PV, Geyten SVD, Darras VM. Thyroid hormone availability and activity in avian species: a review. Domest Anim Endocrinol. 2005;29:63–77.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  15. Frigerio D, Dittami J, Möstl E, Kotrschal K. Excreted corticosterone metabolites co-vary with ambient temperature and air pressure in male Greylag geese (Anser anser). Gen Comp Endocrinol. 2004;137:29–36.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  16. Gunnarsson TG, Gill JA, Atkinson PW, Gélinaud G, Potts PM, Croger RE, et al. Population-scale drivers of individual arrival times in migratory birds. J Anim Ecol. 2006;75:1119–27.

    PubMed  Article  PubMed Central  Google Scholar 

  17. Janiszewski T, Minias P, Wojciechowski Z. Reproductive consequences of early arrival at breeding grounds in the White Stork Ciconia ciconia. Bird Study. 2013;60:280–4.

    Article  Google Scholar 

  18. Jerem P, Jenni-Eiermann S, Herborn K, McKeegan D, McCafferty DJ, Nager RG. Eye region surface temperature reflects both energy reserves and circulating glucocorticoids in a wild bird. Sci Rep. 2018;8:1907.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  19. Klandorf H, Sharp PJ, Macleod MG. The relationship between heat production and concentrations of plasma thyroid hormones in the domestic hen. Gen Comp Endocrinol. 1981;45:513–20.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. Lassiter K, Dridi S, Greene E, Kong B, Bottje WG. Identification of mitochondrial hormone receptors in avian muscle cells. Poult Sci. 2018;97:2926–33.

    CAS  PubMed  Article  Google Scholar 

  21. Liedvogel M, Szulkin M, Knowles SCL, Wood MJ, Sheldon BC. Phenotypic correlates of Clock gene variation in a wild blue tit population: evidence for a role in seasonal timing of reproduction. Mol Ecol. 2009;18:2444–56.

    PubMed  Article  Google Scholar 

  22. Liu JS, Chen YQ, Li M. Thyroid hormones increase liver and muscle thermogenic capacity in the little buntings (Emberiza pusilla). J Therm Biol. 2006;31:386–93.

    CAS  Article  Google Scholar 

  23. López-Jiménez L, Blas J, Tanferna A, Cabezas S, Marchant T, Hiraldo F, et al. Ambient temperature, body condition and sibling rivalry explain feather corticosterone levels in developing black kites. Funct Ecol. 2016;30:605–13.

    Article  Google Scholar 

  24. MacDonald EC, Camfield AF, Jankowski JE, Martin K. Extended incubation recesses by alpine-breeding Horned larks: a strategy for dealing with inclement weather? J Field Ornithol. 2013;84:58–68.

    Article  Google Scholar 

  25. McCleery RH, Pettifor RA, Armbruster P, Meyer K, Sheldon BC, Perrins CM. Components of variance underlying fitness in a natural population of the great tit Parus major. Am Nat. 2004;164:E62–72.

    CAS  PubMed  Article  Google Scholar 

  26. McNabb FM, Cheng MF. Thyroid development in altricial Ring doves Streptopelia Risoria. Gen Comp Endocrinol. 1985;58:243–51.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. McNabb FM, Lyons LJ, Hughes TE. Free thyroid hormones in altricial (ring doves) versus precocial (Japanese quail) development. Endocrinology. 1984;115:2133–6.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  28. Møller AP. Phenotype-dependent arrival time and its consequences in a migratory bird. Behav Ecol Sociobiol. 1994;35:115–22.

    Article  Google Scholar 

  29. Olson JM, McNabb FMA, Jablonski MS, Ferris DV. Thyroid development in relation to the development of endothermy in the Red-Winged Blackbird (Agelaius phoeniceus). Gen Comp Endocrinol. 1999;116:204–12.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. Østnes JE, Jenssen BM, Bech C. Growth and development of homeothermy in nestling European shags (Phalacrocorax aristotelis). Ornithology. 2001;118:983–95.

    Article  Google Scholar 

  31. Pearson JT. Development of thermoregulation and post hatching growth in the altricial cockatiel Nymphicus hollandicus. Physiol Zool. 1998;71:237–44.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  32. Price ER, Dzialowski EM. Development of endothermy in birds: patterns and mechanisms. J Comp Physiol B. 2018;188:373–91.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. Rotics S, Kaatz M, Turjeman S, Zurell D, Wikelski M, Sapir N, et al. Early arrival at breeding grounds: Causes, costs and a trade-off with overwintering latitude. J Anim Ecol. 2018;87:1627–38.

    PubMed  Article  PubMed Central  Google Scholar 

  34. Schew WA, McNabb FMA, Scanes CG. Comparison of the ontogenesis of thyroid hormones, growth hormone and insulin-like growth factor-I in ad libitum and food restricted (altricial) European starlings and (precocial) Japanese quail. Gen Comp Endocrinol. 1996;101:304–16.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  35. Silverin B, Rudas P. Thyroid hormones in nestling Great Tits (Parus major). Gen Comp Endocrinol. 1996;103:138–41.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  36. Silverin B, Viebke PA, Westin J, Scanes CG. Seasonal changes in body weight, fat depots, and plasma levels of thyroxine and growth hormone in free-living great tits (Parus major) and willow tits (P. montanus). Gen Comp Endocrinol. 1989;73:404–16.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  37. Sirsat SKG, Sirsat TS, Crossley JL, Sotherland PR, Dzialowski EM. The 12-day thermoregulatory metamorphosis of Redwinged Blackbirds (Agelaius phoeniceus). J Comp Physiol B. 2016;186:651–63.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  38. Smith RJ, Moore FR. Arrival timing and seasonal reproductive performance in a long-distance migratory landbird. Behav Ecol Sociobiol. 2005;57:231–9.

    Article  Google Scholar 

  39. Tian S, Wang W, Zhang S. The breeding ecology of Asian short toed lark Callendrella cheleensis in Dalai Lake National Nature Reserve of Inner Mongolia. Sichuan J Zool. 2015;34:453–7.

    Google Scholar 

  40. Van der Jeugd HP, McCleery R. Effects of spatial autocorrelation, natal philopatry and phenotypic plasticity on the heritability of laying date. J Evolution Biol. 2002;15:380–7.

    Article  Google Scholar 

  41. Van der Geyten S, Van Rompaey V, Sanders JP, Visser TJ, Kühn ER, Darraset VM. Regulation of thyroid hormone metabolism during fasting and refeeding in chicken. Gen Comp Endocrinol. 1999;116:272–80.

    PubMed  Article  CAS  Google Scholar 

  42. Vézina F, Gustowska A, Jalvingh KM, Chastel O, Piersma T. Hormonal correlates and thermoregulatory consequences of molting on metabolic rate in a northerly wintering shorebird. Physiol Biochem Zool. 2009;82:129–42.

    PubMed  Article  CAS  Google Scholar 

  43. Visser GH. Development of temperature regulation. In: Starck JM, Ricklefs RE, editors. Avian growth and development. New York: Oxford University Press; 1998. p. 117–56.

    Google Scholar 

  44. Výboh P, Zeman M, Juráni M, Buyse J, Decuypere E. Plasma thyroid hormone and growth hormone patterns in precocial Japanese quail and altricial European starlings during postnatal development. Comp Biochem Phys c. 1996;114:23–7.

    Google Scholar 

  45. Wingfield JC, Pérez JH, Krause JS, Word KR, González-Gómez PL, Lisovski S, et al. How birds cope physiologically and behaviourally with extreme climatic events. Philos T R Soc b. 2017;372:1723.

    Article  Google Scholar 

  46. Yang J. Analysis on extreme temperature change in Inner Mongolia from 1961 to 2013 Years. Meteorol J Inner Mongol. 2014;3:17–20.

    Google Scholar 

  47. Zhang S, Xu X, Wang W, Zhao L, Gao L, Yang W. Annual variation in the reproductive hormone and behavior rhythm in a population of the Asian short-toed lark: can spring temperature influence activation of the HPG axis of wild birds? Horm Behav. 2017a;95:76–84.

    CAS  PubMed  Article  Google Scholar 

  48. Zhang S, Xu X, Wang W, Yang W, Liang W. Clock gene is associated with individual variation in the activation of reproductive endocrine and behavior of Asian short-toed lark. Sci Rep. 2017b;7:15002.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  49. Zheng W, Li M, Liu J, Shao S, Xu X. Seasonal variation of metabolic thermogenesis in Eurasian tree sparrows (Passer montanus) over a latitudinal gradient. Physiol Biochem Zool. 2014;87:704–18.

    PubMed  Article  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to Huashan Dou, Songtao Liu in Hulun Lake National Nature Reserve for their help with fieldwork.

Funding

This study was supported by the National Natural Science Foundation of China (No. 32071515).

Author information

Affiliations

Authors

Contributions

SZ conceived the study and designed the experiments. JS, LZ and XL conducted the experiments. JS wrote the first draft of the article. SZ supervised the research and revised the draft. All authors read and approved final manuscript.

Corresponding author

Correspondence to Shuping Zhang.

Ethics declarations

Ethics approval and consent to participate

Permission to handle our study animals was given by Hulun Lake National Reserve Administration (2018-10-20).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Shang, J., Zhang, L., Li, X. et al. Endocrine response of early-hatching Asian Short-toed Lark nestlings exposed to cold temperature in a high-latitude grassland habitat. Avian Res 12, 55 (2021). https://doi.org/10.1186/s40657-021-00291-4

Download citation