Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China
b.
College of Life Science, University of Chinese Academy of Sciences, Beijing, 100049, China
c.
Center for Macroecology, Evolution and Climate, Globe Institute, University of Copenhagen, DK-2100, Copenhagen, Denmark
d.
Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, 650223, China
Funds: This study was financially supported by the National Key Research and Development Program of China (Grant No. 2022YFC2601601), the National Natural Science Foundation of China (Grant No. 31727901) and the China Scholarship Council (No. 2019–13045 to H.X.)
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China. E-mail address: leifm@ioz.ac.cn (F. Lei)
With the continued development of tracking technology and increasing interest in animal movement, our understanding of migration behavior has become more comprehensive. However, there are still many species that have not been well studied, particularly sea birds. Here, we present the first year-round Global Positioning System (GPS) tracking data of the Black-tailed Gull (Larus crassirostris) at the population level. We used solar-powered GPS-Global System for Mobile communication (GSM) loggers to successfully track 30 individuals breeding at Xingrentuo Islet, Liaoning Province, China, for 1–3 years. Except for one individual who roamed in the far north of the Yellow Sea during non-breeding period, all others did a directed southward migration. Migration routes and wintering sites differed among migrating gulls and between years for the birds tracked for two or more years. Additionally, during wintering, the migrating gulls were more likely to travel over a large body of water and shift sites, and some trajectories were quite complex, which was probably closely related to what we observed in the field about their boat-chasing behavior. Compared to wintering movements, the post-breeding movements ranged over a smaller area. Specifically, almost all of them had a long post-breeding period near the breeding islet (≥120 days, <220 km from the breeding islet), and 80% of the gulls who were tracked more than one year had at least one faithful post-breeding site. Compared to the post-breeding period, only approximately half of the migrating gulls had a pre-breeding period that was shorter (3–20 days) and closer to the breeding islet (≤80 km). Migration distance varied among migrating gulls (range 209–2405 km) and the gulls moved least distance during post-breeding period. Furthermore, we found that the southward movement of the migrating gulls occurred when the temperature near the breeding islet dropped; specifically, the gulls directly migrated southward away from the post-breeding site. Our results suggest that the Black-tailed Gull has a long post-breeding period but a short pre-breeding period near the breeding islet and high diversity of their migrating patterns (in especial migration routes and wintering sites).
Light is an essential environmental cue that affects the daily and seasonal activities of most free-living animals (Dixit and Singh, 2011; Dominoni, 2015; Grunst et al., 2023). Hence, the endogenous circadian clocks of animals are modulated to synchronize behavioral and physiological processes in response to exogenous diurnal cycles (Prabhat et al., 2020). However, changes in daily photoperiod regimes, such as exposure to artificial light at night, can disrupt this synchronization and lead to circadian rhythm desynchrony (Wyse et al., 2011; Spoelstra et al., 2018). This disparity between the internal physiology, behavior, and endogenous circadian clock of an animal can negatively affect its overall fitness, leading to energy loss, metabolic dysfunction, and neuroendocrinological disorders (Regas, 1998; West et al., 2017; Porcu et al., 2018). Body mass, behavioral activity, and core and peripheral body temperatures are primary indicators of energy metabolism and proper functioning of the neuroendocrinological system. By monitoring the changes in these parameters in response to abnormal photoperiod treatments, we can better understand the behavioral strategies and underlying metabolic mechanisms of animals. For example, the body temperature, body mass, and activity rhythms of birds may either be maintained or modified when the environmental photoperiod changes, especially under constant light (LL) or darkness (DD) conditions (Budki et al., 2012). However, the mechanisms by which birds adjust these parameters in response to abnormal photoperiod conditions are not fully understood.
In vertebrates, the 24-h light–dark (LD) cycle is maintained through humoral and neural loops in a cascading manner (Tosini and Menaker, 1995; Buhr and Takahashi, 2013). The retinae, suprachiasmatic nuclei (SCN) of the hypothalamus, and pineal gland of non-mammalian vertebrates possess photoreceptors and are in close cooperation to ensure well-coordinated circadian precision and amplitude (Tosini and Menaker, 1995; Cassone et al., 2009; Cassone, 2014); in contrast, the SCN solely acts as the master pacemaker in mammals (Bronstein et al., 1990). Meanwhile, the hypothalamus and pineal gland of passerines play significant roles in resynchronizing their rhythms when the timing of LD cycles suddenly changes (Binkley and Mosher, 1986). On the other hand, the retina has a significant effect on the circadian rhythm of some non-passerine birds, such as the Japanese Quail (Coturnix japonica) and Rock Pigeon (Columba livia) (Brandstaetter, 2002). Generally, by integrating external LD cycles with humoral and neural loops, animals can predict and adapt to different times of the day (24 h) and, thus, maintain the circadian rhythms regulating their body mass, body temperature, and locomotion. Previous studies reported significant circadian rhythms influencing the locomotor activity and body temperature of mammals and birds (both passerines and non-passerines). A closely coupled oscillation between the core body temperature and the activity of an animal has been detected (Refinetti and Menaker, 1992; Depres-Brummer et al., 1995; Fonken et al., 2010). For example, improving the foraging success rate and utilization efficiency of food resources is closely synchronized with metabolism (Montoya et al., 2010), and the body temperature and activity of mammals were positively correlated (van Jaarsveld et al., 2019).
However, the behavioral and physiological rhythms of animals are disrupted under LL conditions (Le Tallec et al., 2013; Fonken and Nelson, 2014). The circadian rhythms of body temperature and daily activities are two fundamental variables derived from the radical changes in neuroendocrinology, metabolism (Zhang et al., 2019), and behavior (Jiang et al., 2020). For instance, the circadian rhythm affecting the activity and core body temperature of mammals becomes arrhythmic and dissociated under LL conditions (Depres-Brummer et al., 1995; Benstaali et al., 2001; Fonken et al., 2010). In contrast, the responses of birds to LL conditions are highly phylogeny-dependent. For example, in Columbiformes, Pigeons (Aplopelia Bonaparte) maintain activity and body temperature rhythm and closely coupled vibration under LL conditions, however, their rhythmicity is lost (Yamada et al., 1988). Moreover, passerines such as House Sparrows (Passer domesticus) lose their activity and body temperature rhythms (Binkley et al., 1971); however, White-crowned Sparrows (Zonotrichia leucophrys gambelii) retain their locomotor rhythms for the first three days (Coverdill et al., 2008). Similarly, the activity rhythms of Java Sparrows (Padda oryzivora) and Indian Weaverbirds (Ploceus philippinus) persist (Ebihara and Kawamura, 1981; Pandey and Bhardwaj, 2011). These findings indicate that activity and body temperature rhythms are tightly coupled in passerines; however, such a phenomenon has not been consistently observed in different passerine species.
Under DD conditions, some mammals maintain their circadian rhythm oscillations. For example, the diurnal Desert Goat (Capra hircus) maintains its activity and body temperature rhythms but exhibits a free-running circadian rhythm (Farsi et al., 2020). Nocturnal mice and rats also maintain the circadian rhythms of activity, body temperature, melatonin, and neurons under DD conditions (Wideman and Murphy, 2009b; Stenvers et al., 2016). Galliformes species such as the diurnal Japanese Quails (Underwood et al., 1999) and laying Hens (Gallus gallus domesticus) maintain the circadian rhythm of body temperature; however, the amount of locomotor activity was almost undetectable, and the activity rhythm was not sustained (Boshouwers and Nicaise, 1987). Passeriformes species such as diurnal House Sparrows exhibit rhythmic locomotor activity and body temperature (Gaston and Menaker, 1968), and diurnal European Starlings (Sturnus vulgaris) maintain their activity, feeding and melatonin rhythms (Gwinner, 1978). Therefore, nocturnal and diurnal animals can maintain circadian rhythms under DD conditions.
The Eurasian Tree Sparrow (Passer montanus, ETS) is a representative diurnal resident bird species that is widely distributed across Eurasia (Dixit and Singh, 2012). It is commonly used as a model species to investigate the circadian rhythms of avian behavior and physiology (Ravikumar and Tewary, 1990), seasonal rhythms of baseline and stress-induced corticosterone levels (Li et al., 2008, 2011), and testosterone and gonadal hormone-releasing hormone levels (Li et al., 2012, 2017; Dixit et al., 2022; Wang et al., 2022). They also exhibit a typical circadian rhythm of hormone secretion (Jiang et al., 2020). The closely related species of ETS, the House Sparrow lost its activity and body temperature rhythms under LL conditions (Binkley et al., 1971), but could maintain those under DD conditions (Gaston and Menaker, 1968). The ETSs are therefore predicted to exhibit a similar pattern of circadian rhythms of behavioral activity and body temperature under abnormal photoperiod conditions. To validate this hypothesis, we examined the circadian rhythms of activity and core and peripheral body temperatures of ETSs under LD, LL, and DD conditions. We predicted that the rhythmicity of activity and body temperature under the DD conditions could be maintained, but their rhythms would disappear under the LL conditions.
2.
Materials and methods
2.1
Bird collection
Through the use of mist nets, 21 free-living juvenile ETSs were caught in the wild in Shijiazhuang City, Hebei Province, China (38.03° N, 114.48° E; elevation: 112 m) in June 2018. After the ETSs were captured, they were randomly assigned to three groups (n = 7/group) and individually housed in similar-sized (width × length × height: 30 cm × 40 cm × 20 cm) cages. The ETSs were then acclimatized for five days under the normal LD cycle (12 h: 12 h) in three climate-controlled chambers under uniform temperature (28 ℃) and humidity (40–60%). Food (millets) and water were provided ad libitum. All protocols in this study were approved by the Institutional Animal Care and Use Committee and the Ethics and Animal Welfare Committee of Hebei Normal University, China.
2.2
Bird treatment
After acclimatization, the light cycles of one climate-controlled chamber remained unchanged (LD group). In contrast, the other two climate-controlled chambers were adjusted to either constant bright light (LL group) or constant darkness (DD group). The light intensity was 300–400 lx (similar to sunset and sunrise intensities) in the LL and LD groups. In order to record the activity, the DD group was exposed to 850 nm wavelength infrared light. The ZT0/ZT12 (zeitgeber, lights on/off) for the LD group was 6:40 and 18:40, respectively. Food and water were provided ad libitum to the ETSs in the three groups.
2.3
Body mass, activity, and body temperature monitoring
The core and peripheral body temperatures, activity, and body mass of the ETSs were monitored for seven consecutive days. The activity in the three groups was monitored for 24 h each day using a Big Brother circadian rhythm system (COULBOURN, ACT-400, Actimetrics, Wilmette, IL, USA). In each climate room, a surveillance camera was mounted to record the activity of the ETSs under dark conditions, and infrared light was irradiated to replenish light. The bird cages were placed on three 3D shelves, and the activity of each bird was monitored using cameras for 24 h for seven consecutive days. All data were exported to the Big Brother Viewer software, and the activity rhythms were analyzed. The body mass of each bird was measured using a portable digital balance (nearest to 0.01 g) at 2:00, 6:00, 10:00, 14:00, 18:00, and 22:00 each day. The temperature of the cloaca (representing the core body temperature) was measured using a handheld thermometer (nearest to 0.01 ℃; HH-25KC; Omega Engineering, Norwalk, CT, USA) at 2:00, 6:00, 10:00, 14:00, 18:00, and 22:00 each day. The eye and tarsometatarsus surface temperatures (representing the peripheral body temperature) were measured using an infrared thermal imager (TiS20+; Fluke Corporation, Everett, WA, USA) at 2:00, 6:00, 10:00, 14:00, 18:00, and 22:00 each day. To ensure accurate temperature measurements and obtain the best image quality, we preheated the thermal imager for 10 min before placing it on the eyes and tarsometatarsus.
2.4
Statistical analysis
The effects of different light treatments and time points on the activity, body mass, core, tarsometatarsus, and eye temperatures of the ETSs were analyzed using a mixed linear model. Multiple comparisons in each treatment and six-time points were performed using Bonferroni post-hoc tests, with time points defined as repeating variables. The JTK_Cyclev.3.1 function in the R package (Hughes et al., 2010) was used to calculate the circadian rhythm parameters, including acrophase (φ), amplitude (A), and Benjamini–Hochberg Q value (BH.Q, a method for optimizing false discovery rates), for the activity, body mass, and core, eye, and tarsometatarsus temperatures. A BH.Q < 0.05 means that there is a significant circadian rhythm. All cosine curves were fitted using the formula f(t) = M + Acos (tπ/12−φ), including the mesor (M), amplitude (A), and acrophase (φ). All statistical analyses were performed in IBM SPSS Statistics v.23 (IBM Inc., NY, USA) and R 4.3.0 (Hughes et al., 2010). All figures were plotted using GraphPad Prism 8.0 (GraphPad Software, Inc., CA, USA). The data are expressed as the mean ± SEM.
3.
Results
3.1
Activity, body mass, and core and peripheral temperatures in response to abnormal photoperiod
The activity, body mass, and core, tarsometatarsus, and eye temperatures of the ETSs varied significantly with treatment, time, and the interaction between treatment and time; however, there was no significant change in body mass in response to the interaction between time and treatment (Table 1; Appendix Table S1). The post-hoc results revealed that regardless of time, the birds in the LL group were significantly more active than those in the LD and DD groups (Fig. 1; Table 2; Appendix Table S2). The birds in the LD group were significantly more active during the day and less active at 22:00 than those in the DD group; however, there was no significant difference in activity between the LD and DD groups at 2:00 and 6:00 (Fig. 1; Table 2; Appendix Table S2).
Table
1.
The statistical results of treatment, time, and the interaction of treatment and time on activity, body mass, core temperature, eye temperature, and tarsometatarsus temperature of Eurasian Tree Sparrows (Passer montanus) in mixed linear models.
Figure
1.
Changes of activity of Eurasian Tree Sparrows (Passer montanus) under constant light (LL) and darkness (DD), and normal light-dark conditions (LD). (A) Average activity of each bird for eight consecutive days under a 24-h cycle (2:00, 6:00, 10:00, 14:00, 18:00, and 22:00). (B) Double-plotted actogram of daily rhythms of activity under a 48-h cycle. The cosine curve fitted in the figure represents a significant rhythm (BH.Q < 0.05). Data are shown as means ± SEM.
Table
2.
Statistical results of the average of activity, body mass, core temperature, tarsometatarsus temperature, and eye temperature of Eurasian Tree Sparrows (Passer montanus) under constant light (LL) and darkness (DD), and normal light-dark conditions (LD) at different time points (2:00, 6:00, 10:00, 14:00, 18:00, and 22:00).
The initial body mass of the birds in the three groups did not significantly differ (F = 0.557, P = 0.583; Fig. 2). However, the birds in the DD group were significantly heavier than those in the LD and LL groups; meanwhile, the body mass of the birds in the LL and LD groups did not significantly differ at any time point (Fig. 2; Table 2; Appendix Table S2).
Figure
2.
Comparisons of initial body mass (A) and the changes of body mass (B) at six-time points (2:00, 6:00, 10:00, 14:00, 18:00, and 22:00) in a 24-h cycle under constant light (LL) and darkness (DD), and normal light-dark conditions (LD) of Eurasian Tree Sparrows (Passer montanus). Data are shown as means ± SEM.
The core temperature of the LL group was significantly higher than that of the DD group at 2:00 (P = 0.002), and that of the LD (P = 0.003) and DD groups (P = 0.001) at 22:00; in contrast, it was significantly lower than that of the LD group at 10:00 (P = 0.041). The core temperature of the three groups did not significantly differ at other time points (Fig. 3; Table 2; Appendix Table S2). Although there were no significant differences in tarsometatarsus temperature across the groups at other time points, the LL group had a significantly higher tarsometatarsus temperature than the LD group at 2:00, 6:00, and 22:00. The eye temperature of the LL and LD groups was significantly lower than that of the DD group at all time points; moreover, the eye temperature of the LL group was significantly higher than that of the LD group at all time points except at 10:00 (Fig. 3; Table 2; Appendix Table S2).
Figure
3.
Daily changes of average values in core temperature (A), tarsometatarsus temperature (B), and eye temperature (C) at six-time points (2:00, 6:00, 10:00, 14:00, 18:00, and 22:00) under constant light (LL) and darkness (DD), and normal light-dark conditions (LD) of Eurasian Tree Sparrows (Passer montanus). The cosine curve fitted in the figure represents a significant rhythm (BH.Q < 0.05). Data are shown as means ± SEM.
3.2
Circadian rhythms of activity, body mass, and core and peripheral temperatures in response to constant photoperiod
Except for body mass, the ETSs in the LD group exhibited significant circadian rhythms in activity and core and tarsometatarsus temperatures, with acrophase at 12:00, and in eye temperature, with acrophase at 14:00 (Table 3). The rhythmicity of these measured parameters varied with the treatment duration. There were no significant circadian rhythms in the activity, body mass, and tarsometatarsus and eye temperatures in the LL group; however, the core temperature exhibited significant rhythmicity, with acrophase at 14:00 (delayed by 2 h relative to the LD group; Table 3). Lastly, there were no significant circadian rhythms in the activity, body mass, and eye temperature in the DD group; however, the core and tarsometatarsus temperatures exhibited significant rhythmicity, with acrophases at 12:00 and 16:00, respectively (Table 3). Compared with the LD group, the amplitudes of all measured parameters decreased in the LL and DD groups (Table 3).
Table
3.
Circadian rhythm parameters of activity, body mass, core temperature, tarsometatarsus temperature, and eye temperature of Eurasian Tree Sparrows (Passer montanus) under constant light (LL) and darkness (DD), and normal light-dark cycle (LD) conditions.
Factors
Variable
BH.Q
ADJ.P
Acrophase (φ, h)
Amplitude (A)
df
F
P
Activity
LL
1.000
1.000
22
6.393
5275
0.725
0.606
LD
< 0.05
< 0.001
12
34.850
5276
24.163
< 0.001
DD
0.072
0.035
12
5.922
5276
1.184
0.323
Body mass
LL
1.000
0.759
16
0.362
5364
3.027
0.013
LD
0.679
0.144
16
0.540
5372
8.655
< 0.001
DD
1.000
0.882
16
0.360
5401
2.089
0.071
Core temperature
LL
< 0.05
< 0.001
14
0.478
5413
7.669
< 0.001
LD
< 0.05
< 0.001
12
0.889
5422
37.124
< 0.001
DD
< 0.05
< 0.001
12
0.714
5444
32.552
< 0.001
Tarsometatarsus temperature
LL
1.000
1.000
12
0.191
5391
0.480
0.790
LD
< 0.05
< 0.001
12
1.332
5363
9.814
< 0.001
DD
0.029
0.019
16
0.470
5190
0.878
0.502
Eye temperature
LL
0.170
0.113
18
0.452
5388
0.587
0.710
LD
< 0.05
< 0.001
14
1.048
5363
24.730
< 0.001
DD
0.793
0.793
14
0.171
5190
0.243
0.941
Significant values (BH.Q < 0.05; P < 0.05) are shown in bold.
As predicted, the activity, core and peripheral body temperatures of the ETSs had significant circadian rhythms and were closely coupled under LD conditions; however, eye temperature was acrophase-delayed by approximately 2 h. In response to an abnormal photoperiod, the amplitude of concussion for each index under all treatments weakened. Under LL conditions, only the core temperature exhibited significant rhythmicity, whereas under DD conditions, the core and tarsometatarsus temperatures displayed significant rhythmicity. These results indicate that the circadian rhythm of the core body temperature of ETSs is endogenous, well-maintained, and independent of the photoperiod.
4.1
Circadian rhythms under normal conditions
Under LD conditions, the ETSs were extremely active during the day and inactive at night; in particular, locomotor activity was significantly rhythmic and acrophased at approximately 12:00. They fed during the day, significantly gained weight while fasting, and lost weight at night. Unlike nocturnal animals, diurnal animals forage, digest food, and absorb nutrients to promote anabolism during the day (Wideman and Murphy, 2009). Diurnal birds are inactive at night and rely on the mobilization of their glycogen and fat stores to enhance catabolism (Lucia et al., 2010). Our results confirm that diurnal animals are highly photosensitive: their activities rapidly increase when lights are on, but their activities end when lights are off (Dawson et al., 2001; Trivedi et al., 2005; Dawson and Sharp, 2007). Although no significant rhythmicity was detected in the body mass of the ETSs, there were significant differences in body mass at daytime and nighttime. Our results are congruent with the reports that Light-vented Bulbul (Pycnonotus sinensis), White-throated Sparrow (Z. albicollis) (Kontogiannis, 1967), and Marsh Tit (Poecile palustris) (Hurly, 1992) gained weight during the day, but lost weight at night. Such circadian rhythms in activity and the corresponding changes in body mass indicate endogenous behavioral and physiological processes of animals to adapt to the external diurnal cycles of light signals (Prabhat et al., 2020).
Meanwhile, we found that both the core and peripheral body temperatures—tarsometatarsus and eye temperatures—were remarkably rhythmic, with highly synchronized acrophases at 12:00 and 14:00, respectively. The core body temperature rhythm was synchronized with locomotor activity, indicating that they are highly coupled. The tarsometatarsus temperature had a higher amplitude and reached its peak synchronizing with the core body temperature, while the eye temperature reached its peak approximately 2 h later. Although birds can maintain an equilibrium of heat production and loss at a constant temperature in their surrounding environment, heat loss generally lags behind the core temperature (Giloh et al., 2012). Since the core body temperature is coupled with metabolic rate, the synchronicity of body temperature with locomotor activity is essential in controlling metabolic processes, ensuring that endogenous shock is synchronized with the external environment (Al-Hasani et al., 2003). All these temporal synchronizations to predictable LD cycles are essential in optimizing the fitness of organisms (Ramkisoensing and Meijer, 2015; Plano et al., 2017).
4.2
Circadian rhythms under constant light conditions
Compared with the birds under LD conditions, the birds under LL conditions lost the rhythmicity of their locomotor activity. Our results indicate that their activities are highly light signal–dependent (Dawson et al., 2001). Furthermore, our results are consistent with the findings for other avian species such as Rock Pigeons (Yamada et al., 1988), Domestic Chicken (Gallus domesticus), Ptarmigans (Lagopus muta) (Appenroth et al., 2021), and resident House Sparrows (Binkley et al., 1971). However, our results differ from the finding for migratory White-crowned Sparrows: under LL conditions, they maintain the rhythmicity of their locomotor activity for three days (Coverdill et al., 2008). Therefore, it seems that migratory and resident passerines exhibit different behavioral strategies in response to certain environmental signal changes that may be caused by different interactions between the output of the circadian oscillation and light signal.
The ETSs under LL conditions had significantly higher core and peripheral body temperatures during the subjective night than those of the LD group during the dark period. However, their body mass did not change. Increased body temperature and activity, coupled with constant body mass, denote that the ETSs increased their food intake under constant light conditions at night; however, they demonstrated a similar trend under normal conditions. In contrast, nocturnal mice increased food intake and gained weight under light-disturbed conditions (Coomans et al., 2013). Furthermore, the core body temperature of the ETSs remained rhythmic, consistent with those of Pigeons (Ebihara et al., 1984; Oshima et al., 1989). However, the peripheral body temperature was arrhythmic. These results indicate that the rhythmicity of the core body temperature is endogenous, and peripheral body temperatures and activity can be decoupled under LL conditions. Relative to normal light conditions, the core body temperature of the ETSs under LL conditions was acrophase-delayed for approximately 2 h, indicating that its rhythmicity was affected by light, and its oscillation process was under the strict control of the endogenous biological clock. The core body temperature of the ETSs in the LL group during the subjective night was higher than that in the LD group, and the trough of the core body temperature rhythm occurred during the subjective night. This downregulation of metabolism has also been observed in nocturnal rats exposed to dim light (Borniger et al., 2014). In terms of energy expenditure, constant light exposure is a costly inconvenience because core body temperature rhythms can help an animal conserve energy; for example, a rhythmic core temperature helps House Sparrows save 7% of their energy (Regas, 1998).
Generally, light signals can serve as external stimuli that induce internal physiological and behavioral changes by acting on the retinal photoreceptors of birds. When continuously exposed to constant light, the ETSs demonstrated behavioral changes and a higher level of activity, resulting in increased metabolic heat production and peripheral temperature. Unlike the core body temperature, controlled by the endogenous biological clock, the peripheral temperature strongly depends on exogenous light. Under LL conditions, the surface body temperature of the ETSs remained high, which could be induced by the increased activity at subjective night and enhanced thermogenesis through catabolism (Hohtola and Stevens, 1986). Therefore, the activity and body temperature rhythms of birds are disrupted under continuous exposure to intense light. Such a disruption may alter the homeostasis of energy metabolism and further impair the overall health of an organism. Considering the limited information on variations in peripheral body temperature, the underlying mechanisms of the decoupled relationship between peripheral and core body temperature require further investigation.
4.3
Circadian rhythms in constant dark conditions
The ETSs remained inactive at all time points and lost their activity rhythm under DD conditions. Similarly, White-crowned Sparrows lose their activity rhythm under dim light conditions; however, they maintain a high level of activity for night migration (McMillan, 1972; Coverdill et al., 2008). Our results differ from the findings that locomotor activity rhythms are maintained under DD conditions in House Sparrows (Cassone, 2014) and European Starlings (Gwinner, 1978). These results indicate that maintaining the activity rhythm under DD conditions is largely species-specific, not phylogenetic-dependent. In particular, the ETSs in the DD group were significantly heavier than those in the LD and LL groups, although they exhibited a similar trend in body mass as those in the LD group. Despite the disruption of their activity and foraging rhythms, an endogenous pattern of weight loss and gain was observed when the activities and energy consumption levels of the ETSs were low. The mechanism behind this phenomenon remains largely unknown and should be determined through ecological and physiological research.
The ETSs in the DD group had comparable core body and tarsometatarsus temperatures with those in the LD and LL groups; however, their eye temperature was significantly higher than those in the other two groups. Owing to weak vision under dark conditions, an increase in eye temperature under DD conditions is critical for better foraging, thereby ensuring adequate food intake and maintenance of energy balance (Harmening, 2017). Furthermore, the core body and tarsometatarsus temperatures exhibited a significant circadian rhythm, whereas eye temperature did not. Similarly, the circadian rhythm of the core body temperature under DD conditions has been observed in Japanese Quails and House Sparrows (Gaston and Menaker, 1968; Underwood et al., 1999). The core temperature of the ETSs with an acrophase at 12:00 indicates that constant darkness is not necessary to induce changes in the rhythmicity of the core body temperature of birds because it is controlled by an endogenous clock. However, our results showed that the acrophase of the tarsometatarsus temperature was delayed by 4 h relative to the core body temperature. Although birds can maintain an equilibrium of heat production and loss at a constant temperature in their surrounding environment, heat loss generally lags behind the core temperature (Giloh et al., 2012). In birds, the tarsometatarsus is a vital organ that regulates thermal dissipation (Mosher and White, 1978). Considering that limited information is available on the circadian rhythm of tarsometatarsus temperature under dark conditions, how birds regulate their thermal equilibrium by adjusting the surface temperature of their peripheral organs remains to be elucidated.
5.
Conclusions
In this study, we examined the circadian rhythms of activity, body mass, and core and peripheral body temperatures of ETS in response to LD, LL, and DD conditions. We found that the core body temperature maintained significant rhythmicity when the external photoperiods changed; however, the amplitude of the concussion of each index under all treatments weakened, indicating that the core body temperature is an endogenous index. The peripheral body temperature and activity decoupled when the sparrows were exposed to constant light, whereas increased eye temperature enabled adequate food intake to maintain an energy balance under DD conditions. Therefore, our results suggest that the maintenance of the core body temperature rhythm is highly rhythmic and endogenous—it is not completely dependent on light; however, but the activity and peripheral body temperature rhythms are greatly affected by photoperiod. Our results differ from the research findings for other diurnal passerines such as House Sparrows and White-throated Sparrows. These discrepancies suggest that the coping mechanisms of body condition and core and peripheral body temperatures in response to constant light signals are species-dependent, not phylogeny-dependent. Our results contribute to a better understanding of the diversity and plasticity of physiology and behavior of passerines under abnormal photoperiods. The underlying causes of such species-dependent variations in the rhythmicity of physiology and behavior in response to unfavorable photoperiod warrant further study.
CRediT authorship contribution statement
Lirong Zuo: Formal analysis, Writing original draft, Writing review & editing. Ibrahim M. Ahmad: Formal analysis, Writing original draft, Writing review & editing. Yuanyuan Liu: Investigation, Methodology. Limin Wang: Investigation, Methodology. Shu Fang: Investigation, Methodology. Dongming Li: Conceptualization, Supervision, Funding acquisition, Writing review & editing.
Ethics statements
All experimental materials were conducted in accordance with the Institutional Committee for Animal Care and Use of Hebei Normal University, China, and was carried out under the auspices of scientific collecting permits issued by the Departments of Wildlife Conservation (Forestry Bureau) of Hebei Province, China.
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Table
1.
The statistical results of treatment, time, and the interaction of treatment and time on activity, body mass, core temperature, eye temperature, and tarsometatarsus temperature of Eurasian Tree Sparrows (Passer montanus) in mixed linear models.
Table
2.
Statistical results of the average of activity, body mass, core temperature, tarsometatarsus temperature, and eye temperature of Eurasian Tree Sparrows (Passer montanus) under constant light (LL) and darkness (DD), and normal light-dark conditions (LD) at different time points (2:00, 6:00, 10:00, 14:00, 18:00, and 22:00).
Table
3.
Circadian rhythm parameters of activity, body mass, core temperature, tarsometatarsus temperature, and eye temperature of Eurasian Tree Sparrows (Passer montanus) under constant light (LL) and darkness (DD), and normal light-dark cycle (LD) conditions.
Factors
Variable
BH.Q
ADJ.P
Acrophase (φ, h)
Amplitude (A)
df
F
P
Activity
LL
1.000
1.000
22
6.393
5275
0.725
0.606
LD
< 0.05
< 0.001
12
34.850
5276
24.163
< 0.001
DD
0.072
0.035
12
5.922
5276
1.184
0.323
Body mass
LL
1.000
0.759
16
0.362
5364
3.027
0.013
LD
0.679
0.144
16
0.540
5372
8.655
< 0.001
DD
1.000
0.882
16
0.360
5401
2.089
0.071
Core temperature
LL
< 0.05
< 0.001
14
0.478
5413
7.669
< 0.001
LD
< 0.05
< 0.001
12
0.889
5422
37.124
< 0.001
DD
< 0.05
< 0.001
12
0.714
5444
32.552
< 0.001
Tarsometatarsus temperature
LL
1.000
1.000
12
0.191
5391
0.480
0.790
LD
< 0.05
< 0.001
12
1.332
5363
9.814
< 0.001
DD
0.029
0.019
16
0.470
5190
0.878
0.502
Eye temperature
LL
0.170
0.113
18
0.452
5388
0.587
0.710
LD
< 0.05
< 0.001
14
1.048
5363
24.730
< 0.001
DD
0.793
0.793
14
0.171
5190
0.243
0.941
Significant values (BH.Q < 0.05; P < 0.05) are shown in bold.
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