- Open Access
Egg laying and incubation rhythm of the Chinese Grouse (Tetrastes sewerzowi) at Lianhuashan, Gansu, China
© The Author(s) 2019
- Received: 15 May 2019
- Accepted: 30 May 2019
- Published: 14 June 2019
Incubating birds must balance the conflict between thermal needs of the developing embryos and their self-maintenance needs for energy. The Chinese Grouse (Tetrastes sewerzowi) lives in high mountain conifer forests and faces energy stress, cold environment, and predation pressure. Females might adjust incubation rhythm to adapt to these constraints.
Two methods were used to investigate egg laying and incubation pattern of the Chinese Grouse; 25 nests were monitored by data loggers and 12 nests by infrared video cameras.
Female Chinese Grouses usually laid an egg every 2 days. The incubation period was 28–31 days. Overall incubation constancy for Chinese Grouse was 93%. The females took 5.0 recesses per day and 34% of all 1696 recesses were taken in the crepuscular period. The average recess duration was 20.3 min. Females took more and shorter recesses in the latter part of incubation. The females who allocated more time to foraging had a higher reproductive success.
Probably due to its high egg/body mass ratio, the Chinese Grouse has a long laying interval of 49 h. We suggest that, due to energy stress, females have relatively more recesses and they increase the number of recesses as incubation progresses. To compensate for the embryos’ thermal needs, they extend the incubation period and shorten the recess duration in this cold environment.
- Body mass
- Chinese Grouse
- Environment temperature
- Incubation pattern
- Nest attentiveness
In precocial birds, especially in those where only one sex incubates, egg laying and incubation are important stages of reproductive investment, and may represent critical energy bottlenecks, especially in harsh environments (Wiebe and Martin 1995, 1997, 2000). Incubating individuals must balance the conflict between thermal needs of the developing embryos and their self-maintenance needs by leaving the nest to forage (Wiebe and Martin 2000; Conway and Martin 2000a; Coates and Delehanty 2008). Also, incubating birds have to adjust their incubation rhythms based on physical conditions and environmental factors.
In smaller species, environmental factors have a greater effect on incubation rhythm and smaller birds are thought to have a greater need for food during incubation (Afton 1980). Large-bodied birds have greater energy reserves and can spend more time on the nest, but in periods of stress, small-bodied birds might not have enough nutrient reserves to complete incubation (Gloutney and Clark 1991) and need more time off nests for foraging (Manlove and Hepp 2000; Camfield et al. 2010). Also, birds living in areas with low temperatures have a higher daily energy expenditure, but foraging away from the nest is almost twice as costly as incubating a four-egg clutch (Piersma et al. 2003). Because low ambient temperatures allow eggs to cool quickly, birds might be required to show higher nest attentiveness in cold climates (Chalfoun and Martin 2007). Martin (2002) has shown that colder ambient temperatures can result in higher attentiveness, such as Anna’s (Calype anna) and Black-chinned Hummingbirds (Archilochus alexandri) nesting in California, which took longer nest attentiveness than Purple-crowned Fairy (Heliothryx barroti) in the warm lowland tropics of Panama (Vleck 1981).
The Chinese Grouse (Tetrastes sewerzowi) is an endemic bird distributed in Gansu, Qinghai, Sichuan, Yunnan, and Tibet in western China (Sun 2000), along the high mountain conifer forests at altitudes between 2700 and 4200 m on the eastern edge of the Tibetan Plateau. These birds typically experience a decrease in mass during reproduction, which is usually considered to be an indication of reproductive stress (Cucco and Malacarne 1997). The Chinese Grouse is the smallest grouse in the sub-family of Tetraonidae (Sun et al. 2005). On the other hand, nutritious foods are limited in spring, as willows (Salix spp.) are the main food resources for the birds (Zhao et al. 2017), so nutrient constraint possibly exists during the egg-formation and incubation periods (Wang et al. 2010). During the pre-incubation period, the proportion of time allocated for vigilance by male and time for foraging by female Chinese Grouse is the highest recorded among monogamous grouse species (Lou et al. 2017). This probably benefited the female by reducing the danger of predation, increasing her probability of survival, and allowing more time for her to forage for more nutritious food, such as herb leaves and insects, to increase her energy reserves (Lou et al. 2017). Good body condition at the beginning of the breeding season has been associated with large egg volumes and early laying and body mass is positively related to food abundance during the incubation of Wilson’s Storm Petrels (Oceanites oceanicus) (Quillfeldt et al. 2006).
How does the Chinese Grouse deal with the cold weather, high altitude, short breeding time, and nutrient stress during the egg-laying and incubation period? In this study, we explored the egg-laying and incubation rhythms of Chinese Grouse and analyzed the strategies Chinese Grouse uses to deal with these disadvantages. We predicted that more feeding during incubation is important for Chinese Grouse reproductive success.
We conducted the study during 1999–2016 at the Lianhuashan Nature Reserve (34°45ʹ–35°06ʹN, 103°27ʹ–103°51ʹE) in southern Gansu Province, central China. Our research station was at the altitude of 2850 m, surrounded by forest dominated by fir (Abies fargesii), spruce (Picea asperata), birch (Betula utilis), and many species of willow. The average annual temperature in the reserve is 5.1–6.0 °C, with recorded extremes of 34.0 °C and − 27.1 °C at an altitude of 2100 m. For more information, see Sun et al. (2003).
The nests of Chinese Grouse are located at the bases of fir, spruce, birch and willow trees. Nesting materials are mainly mosses, leaves and dry twigs. Nests were found by locating radio-tracked females, searching paired males’ territories or from reports by local people, who received a reward (Sun et al. 2003; Zhao et al. 2018).
We equipped 25 nests with data loggers (Germin Data Loggers LTD, UK, Tiny Talk II) to record the egg temperatures when the females were on and off their nests, when the temperatures were higher and lower, respectively. In 1999, we equipped 4 nests with thermo-sensors fixed at the bottom of the nests, with a cable (length < 3 m) connected to the data loggers. The temperature data recorded in this way were generally lower than the temperature of the egg. However, changes in data logger temperatures should be proportional to those of the eggs, so we could record the nest attendance of the females. In 2000 and 2001, we placed artificial eggs in the center of 16 nests for monitoring both nest attendance and egg temperature. The artificial eggs were from abandoned clutches, and filled with paraffin wax, and thermo-sensors were buried in it (Persson and Göransson 1999). This arrangement did not seem to affect the behaviour of the females, as no females abandoned their nests after we placed the dummy eggs in their nests. We put the thermo-sensors or dummy eggs into the nests as soon as we located them. If the clutch was unfinished, we could record the egg laying intervals. The data loggers were kept dry and covered in plastic boxes. The data loggers were programmed to record temperatures every 6.0 min. In 2010, we monitored 5 nests. The other operations were the same as in 2000, except that the data loggers were programmed to record temperatures every minute. We revisited the nests every 7 days to download the data and restart the loading, mostly without disturbing the hens from the nests. If we disturbed the hens while downloading the data, we excluded the results from that day from the analyses.
The timing and duration of recesses were interpreted from changes in egg (n = 21) or nest (n = 4) temperatures associated with the departure and return of the females, as shown on the strip charts. Short temperature drops (lasting only one measurement, 6 min) were likely a result of females repositioning themselves on the nest and moving the eggs; they were not considered to be recesses. Four irregular records from three nests were recorded (two at day time from one nest: 186, 1068 min; two at night from two nests: 186, 205 min). All three nests hatched successfully. These were most likely associated with predation attempts and all data from these days were excluded from analyses. We defined the overall incubation constancy as the percentage of the time the females spent on the nests during the entire incubation period. Partial incubation was a less regular form of incubation that can occur from the beginning of egg laying to shortly after clutch completion (Wang and Beissinger 2011). Nests were regarded as successful when at least one egg was hatched. We determined nest age by considering that eggs were laid every other day with a mean incubation period of 28 days for successful nests (Sun et al. 2003). For the unsuccessful nests that had been found during incubation, we speculated nest age as Zhao et al. (2019).
In both 2000 and 2001, one data logger was used to record the forest temperature in our study area during the laying and incubating period. All monitored nests were located throughout the study area, so we selected a nest randomly to record the environment temperature. To avoid disturbing the incubating female, thermo-sensors and data logger were hung on a tree 1.5 m high from the ground and 50 m away from the Chinese Grouse nest. Nest site temperatures might differ from our data logger records. However, as the Chinese Grouse made open nests without much concealment, we assumed that there was not a big difference.
During 2013 to 2016, we monitored 12 nests with infrared video cameras (The Ltl Acorn Ltl-6210 M). With its highly sensitive passive Infra-Red sensor, the camera detects the sudden change of ambient temperature caused by moving animals in a region of interest, triggering the camera to take pictures/videos. Thus when a female moved, we obtained videos. By this means, we knew the exact time that a female left and arrived at a nest. We mounted cameras on trunks about 0.5 m away from the nests. The video lasted 10 s for every triggering and 3 pictures for confirmation. We recorded date, time, and frame number on video images electronically.
Data from nests monitored less than 7 days were not included in calculating the recess rates and incubation constancy. We excluded video footages that were interrupted by camera malfunction, loss of power, or disturbance from changing batteries, memory cards, and long-time recess because of predation. Nineteen samples using the data logger and nine from the video camera were included in our analyses. All recesses occurred from 05:30 to 20:30. Nest constancy was calculated in days, and the average was taken.
We conducted a mixed effects linear model, the daily number of recesses as the dependent variable and year, method, nest age, recess duration as fixed factors, with individual as a random factor. And we used a mixed effects linear model to test how the fixed factors year, method, nest age, hour and number of recesses affected recess duration, with individual as a random factor. There was a correlation between year and method. To exclude the effect of method on year, we separated all data to three groups: datalog6, datalog1 and camera, then reanalyzed. To examine how incubating females adjusted recess timing, we grouped all individuals into these groups: reproduction successful and failed, tracked and untracked. We used t tests to test the difference in incubation patterns between groups. The data were analyzed using the program R. All values were expressed as mean ± SD.
We monitored the egg laying of 8 females. Females laid eggs at midday, between 10:59 and 15:45 (time arriving at nest, n = 16), except for one female that arrived at the nest at 07:27 and spent 6 h there when laying its sixth egg. The laying time of all six of one female’s eggs occurred within two and half hours (12:32–15:11). Females usually laid one egg every 2 days, except for one instance of 3 days. The laying intervals of five females were 49.0 ± 1.3 h (n = 18). Females spent variable amounts of time on the nests when laying eggs. Less time was spent when laying the first four eggs (71.3 ± 19.8 min, n = 9) than for laying the fifth and sixth eggs (162.8 ± 89.0 min, n = 8). Full incubation started in the early morning (6:30–8:30, n = 8). Two females started right after laying the sixth egg, five on the next day, and one on the third day.
The number of daily recesses and nest constancy of Chinese Grouse females during the incubation period at Lianhuashan Nature Reserve, Gansu, China
Number of daily recessesa
Recess duration (min)b
Nest constancy (%)c
5.36 ± 1.16 (23)
28.93 ± 7.59 (129)
89.16 ± 1.96
4.83 ± 0.79 (12)
22.84 ± 5.49 (57)
92.31 ± 1.17
5.57 ± 0.82 (7)
22.76 ± 10.23 (39)
91.19 ± 1.62
3.56 ± 0.53 (9)
21.48 ± 7.06 (31)
94.72 ± 1.18
5.25 ± 0.61 (24)
18.87 ± 6.66 (126)
93.12 ± 1.16
4.84 ± 0.96 (19)
20.66 ± 6.67 (92)
93.05 ± 1.22
4.67 ± 0.87 (24)
23.52 ± 7.93 (113)
92.40 ± 1.29
4.69 ± 0.63 (13)
22.78 ± 7.42 (64)
92.66 ± 1.07
6.15 ± 0.81 (13)
21.19 ± 6.31 (78)
91.30 ± 1.69
4.50 ± 0.53 (8)
18.83 ± 4.34 (36)
94.11 ± 0.75
4.36 ± 0.67 (11)
19.38 ± 6.69 (48)
94.13 ± 1.09
6.07 ± 0.70 (15)
15.9 ± 5.06 (92)
93.39 ± 1.08
5.19 ± 0.75 (16)
16.36 ± 6.48 (84)
94.11 ± 1.20
4.29 ± 0.49 (7)
22.32 ± 5.06 (25)
93.54 ± 0.57
4.54 ± 0.66 (13)
21.97 ± 5.48 (59)
93.08 ± 1.26
4.64 ± 0.58 (22)
14.38 ± 4.09 (101)
95.42 ± 0.73
4.75 ± 0.71 (8)
23.56 ± 8.94 (36)
92.27 ± 1.60
4.89 ± 0.78 (9)
22.37 ± 7.4 (43)
92.42 ± 0.91
5.30 ± 0.82 (10)
20.55 ± 5.71 (52)
92.58 ± 1.17
4.41 ± 0.79 (15)
21.09 ± 7.38 (52)
93.29 ± 1.91
4.45 ± 0.52 (11)
23.6 ± 9.36 (10)
93.08 ± 2.65
5.18 ± 0.60 (11)
19.86 ± 8.8 (43)
93.02 ± 1.68
4.15 ± 0.69 (11)
18.28 ± 5.78 (39)
94.56 ± 1.48
5.90 ± 0.88 (10)
18.71 ± 9.61 (45)
92.32 ± 1.76
4.29 ± 0.49 (7)
17.64 ± 4.93 (28)
94.85 ± 0.86
6.00 ± 0.76 (7)
18.21 ± 7.56 (29)
92.96 ± 1.29
6.13 ± 0.85 (24)
16.24 ± 7.51 (109)
93.53 ± 1.81
4.33 ± 0.49 (12)
16.28 ± 4.22 (36)
95.21 ± 0.71
Of the 28 females yielding data on incubation rhythm, 18 females were successful in hatching. Recess duration and number of recesses were significantly different between the successful and unsuccessful females (df = 1512, t = 3.131, p = 0.002 and df = 338.771, t = 2.863, p = 0.005 respectively, Tsuccessful = 20.7 ± 8.2 min, Tunsuccessful19.5 ± 6.7 min, Nsuccessful = 5.1, Nunsuccessful = 4.8). Successful females took more and longer recesses. Twenty of 28 females were followed with transmitters. There was no difference in number of recesses between those that were tracked and those that were not (Ntracked = 5.0, Nuntracked = 5.1, df = 188.791, t = –1.024, p = 0.299), however, tracked individuals had longer recess durations (Ttracked = 20.8, Tuntracked = 19.0, df = 1063.200, t = 4.591, p < 0.001).
Reported reproductive parameters between grouse species
Body weight (g)
Egg laying interval (h)
Egg weight (g)
Incubation constancy (%)
Number of daily recesses
Recess duration (min)
Chinese Grouse (Tetrastes sewerzowi)
Willow Ptarmigan (Lagopus lagopus)
White-tailed Ptarmigan (Lagopus leucurus)
2, 3, 4
Rock Ptarmigan (Lagopus mutus)
Ruffed Grouse (Bonasa umbellus)
2, 6, 7
Hazel Grouse (Tetrastes bonasia)
2, 8, 9
Blue Grouse (Dendragapus obscurus)
Greater Sage-grouse (Centrocercus urophasianus)
Spruce Grouse (Dendragapus canadensis)
Capercaillie (Tetrao urogallus)
The laying time of Chinese Grouse was concentrated around noon. It is different from Hazel Grouse, which lays their eggs during 04:00–20:00 (Semenov-Tyan-Shanskii 1960) and the ptarmigans, which lay eggs during 07:00–19:00 (Wiebe and Martin 1995). In 11% failed nests, we identified three nest predator species using infrared video cameras: Asian Badger (Meles leucurus) accounting for three nest failures, Hog Badger (Arctonyx collaris) for one nest failure, and Blue-eared Pheasant (Crossoptillon auritum) for one nest failure. Badgers, the main nest predators in our study area were active in the evening-night period, so around noon might be the safest time for the Chinese Grouse to visit their nests. The length of the egg-laying interval (around 48 h) also permitted all eggs to be laid around noon. Partial incubation existed especially in the late period of egg laying. White-tailed Ptarmigan and Spruce Grouse (Dendragapus canadensis) also showed this pattern (McCourt et al. 1973; Giesen and Braun 1979). In anseriforms and galliforms species, incubation starts during the laying period without causing hatching asynchrony (Wang and Beissinger 2011). Partial incubation thus shortens the incubation period and benefits incubating females (Wang and Beissinger 2011).
The incubation period of Chinese Grouse (around 28–31 days) was relatively long compared to Blue Grouse (Dendragapus obscurus, 26 days) Greater Sage-grouse (Centrocercus urophasianus, 26.5 days) Hazel Grouse (23-27 days) and Spruce Grouse (21-25 days) (Johnsgard 1983) (Table 2). During incubation period, female Chinese Grouse spent on average 92.8% of their time per day on nest, which was lowest in grouse species: Ruffed Grouse (96%, Maxson 1977), White-tailed Ptarmigan (95.7% and 93.9%, Wiebe and Martin 1997), Greater Sage-Grouse (96.1%, Coates and Delehanty 2008) and Hazel Grouse (95%, Semenov-Tyan-Shanskii 1960) (Table 2). The number of daily recesses taken by Chinese Grouse females averaged 5.0, much higher than that of the Hazel Grouse (2.0, Müller 1992), and White-tailed Ptarmigan (3.07, Wiebe and Martin 1997). The average recess duration of Chinese Grouse was 20.25 min, shorter than that of Spruce Grouse (26.4 min, Naylor et al. 1988), Hazel Grouse (33 min, Müller 1992), Capercaillie (Tetrao urogallus) (35 min), and Ruffed Grouse (20–40 min, Johnsgard 1983) (Table 2). And our result showed the number of recesses was negatively related to recess duration. The incubating females might adjust recess duration to guarantee incubation attendance. Chinese Grouse therefore showed a pattern of a long incubation period with low incubation constancy, and more and shorter recesses.
Theory predicts shorter embryonic periods in species with smaller body size (Martin et al. 2007). However, Martin (2002) found no relationship between body mass and incubation period, and proposed that longer incubation periods were associated with lower attentiveness. Deeming et al. (2006) also believed that nest attentiveness affected egg temperature maintenance, and resulted in incubation period variation. Cartar and Montgomerie (1985) suggested that small-bodied incubators have a low fasting endurance and modified nest attentiveness by adjusting the frequency of recesses. Our results support their proposals. With small body mass, females have less endogenous reserves and more nutritional requirements (Demment and Vansoest 1985; Swenson et al. 1994). Limited by energy reserve, they have to leave their nests more often for foraging. Studies have documented that parents compensate for energy demands by reducing nest attentiveness (MacDonald et al. 2014). These might be the reasons why breeding success was related to more and longer recesses in Chinese Grouse females.
Females who were tracked by transmitters (weighing about 12 g, or 3–4% of their body weights, Sun et al. 2003) required longer recesses, presumably for more foraging. However, low attentiveness can decrease reproductive success (Mallory 2009; Shoji et al. 2011). Although we found no significant difference on reproductive success between tracked and untracked females, we believe that the additional burden of the transmitters might have adverse effects on the tracked females during incubation.
Our results showed differences in recess duration between years, which might be affected by environment temperatures and different monitoring methods. Method does affect recess duration (one-way ANOVA, F = 16.37, p < 0.001, Tdatalog6 = 21.32, Tdatalog1 = 19.34, Tcamera = 18.21). Data logger could overestimate the recess duration because of delayed temperature recording. But recess duration still has significant difference among years, when we excluded the effect of method. Many studies have shown that females take more and shorter recesses in cold environments (Conway and Martin 2000b; Londono et al. 2008; Reneerkens et al. 2011; MacDonald et al. 2014). The recess length of Chinese Grouse in 2001 (17.37 ± 6.23 min) was shorter than that in 2000 (21.06 ± 7.06 min) (t test, both p < 0.001). We recorded the air temperature in 2000 and 2001. The daily average air temperature during incubation was significantly lower in 2001 (5.4 ± 1.6 °C) than in 2000 (8.5 ± 2.1 °C) (t test, p < 0.001). As the daily number of recesses was higher in 2001 (5.37 ± 0.96, n = 249) than in 2000 (5.09 ± 0.95, n = 540) (t test, p = 0.093), we suggest that the Chinese grouse females adjust incubation rhythm to adapt environment constraints. This correlation has also been found in other grouse species, such as the Spruce Grouse (Naylor et al. 1988). However, studies on the Capercaillie showed that cold weather did not affect the number and length of recesses for this largest grouse (Semenov-Tyan-Shanskii 1960).
Fluctuations in temperature are more detrimental to eggs as incubation progresses (Webb 1987). Meanwhile, the rate of heat loss from eggs increases with embryo age (Cooper and Voss 2013). Female Black-capped Chickadee (Poecile atricapillus) responds to increased egg cooling rates by altering incubation rhythms (with more frequent and shorter on- and off-bouts) (Cooper and Voss 2013). The Chinese Grouse females also reduced the recess length as the incubation progressed. However, the daily inattentive period did not differ. For incubating females, body mass has been associated with food abundance (Quillfeldt et al. 2006), and positively related to reproductive success (Gloutney and Clark 1991). In the latter period of incubation, their foraging requirement might be more urgent, as adequate feeding is essential for reproductive success. So, female Chinese Grouse might increase the frequency of recesses and shorten recess duration. Similar results were also found in the Wood Duck (Aix spons) (Hepp et al. 1990).
A bimodal pattern of recess timing may not be driven primarily by predation pressure, but by physiological needs of the incubating female (Winder et al. 2016). Female grouse may have a greater energy demand at dawn after fasting overnight, and take recesses at dusk to obtain energy reserves for overnight hours (Wiebe and Martin 1997). Successful females took more and longer recesses, which is at odds with the view that fewer trips to and from the nest may attract fewer predators to the eggs (Ghalambor and Martin 2002). In addition, radio-tracked females increased food intake to cover the additional burden of carrying the transmitter. We suggest that the energy needs of the incubating female are more important than egg chilling and predation risk. We conclude that the egg laying and incubation rhythm of the Chinese Grouse is an adaption mainly to deal with energy stress, with predation risk being of less importance.
We conclude that the egg laying and incubation rhythms of Chinese Grouse are driven by energy constraints. Compared with other grouse, female Chinese Grouse take longer egg laying intervals, leave nests more times per day with lower incubation attentiveness and longer incubation period to balance the thermal needs of the developing embryos and their self-maintenance needs.
We thank people in the Lianhuashan Natural Reserve for their great helps. Prof. Kathy Martin gave us great comments on our manuscript. We appreciate all these help for the improvement of this paper.
This study was supported by grants of the National Natural Science Foundation of China (31520103903, 31172099), CAS Innovation Program and Deutsche Forschungs-emeinschaft and World Pheasant Association.
MS and YHS conceived and designed the idea. YF, JMZ, YXJ and MS performed the field work. MS, JS and SK analyzed the data. MS and YHS wrote the paper. All authors contributed critically to the manuscript and gave final approval for publication. All authors read and approved the final manuscript.
Ethics approval and consent to participate
All capture, radio-tag and tracking procedures on Chinese Grouse used in the present study had been given prior approval and were supervised by the Animal Care and Use Committee of the Institute of Zoology, the Chinese Academy of Sciences (Project No. 2008/73).
Consent for publication
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
- Afton AD. Factors affecting incubation rhythms of Northern Shovelers. Condor. 1980;82:132–7.View ArticleGoogle Scholar
- Bump GR, Darrow W, Edminster FC, Crissey WF. The Ruffed Grouse. Buffalo: Holling Press; 1947.Google Scholar
- Camfield AF, Pearson SF, Martin K. Life history variation between high and low elevation subspecies of horned larks Eremophila spp. J Avian Biol. 2010;41:273–81.View ArticleGoogle Scholar
- Carey C, Rahn H, Parisi P. Calories, water, lipid and yolk in avian eggs. Condor. 1980;82:335–43.View ArticleGoogle Scholar
- Cartar RV, Montgomerie RD. The influence of weather on incubation scheduling of the white-rumped sandpiper (Calidris fuscicollis): a uniparental incubator in a cold environment. Behaviour. 1985;95:261–89.View ArticleGoogle Scholar
- Chalfoun AD, Martin TE. Latitudinal variation in avian incubation attentiveness and a test of the food limitation hypothesis. Anim Behav. 2007;73:579–85.View ArticleGoogle Scholar
- Clark AB, Wilson DS. Avian breeding adaptations: hatching asynchrony, brooding reduction, and nest failure. Q Rev Biol. 1981;56:253–77.View ArticleGoogle Scholar
- Coates PS, Delehanty DJ. Effects of environmental factors on incubation patterns of Greater Sage-Grouse. Condor. 2008;110:627–38.View ArticleGoogle Scholar
- Conway CJ, Martin TE. Effects of ambient temperature on avian incubation behavior. Behav Ecol. 2000a;11:178–88.View ArticleGoogle Scholar
- Conway CJ, Martin TE. Evolution of passerine incubation behavior: Influence of food, temperature, and nest predation. Evolution. 2000b;54:670–85.View ArticleGoogle Scholar
- Cooper CB, Voss MA. Avian incubation patterns reflect temporal changes in developing clutches. PLoS ONE. 2013;8(6):1–6.Google Scholar
- Cucco M, Malacarne G. The effect of supplemental food on time budget and body condition in the Black Redstart Phoenicurus ochruros. Ardea. 1997;85(2):211–21.Google Scholar
- Deeming DC, Birchard GF, Crafer R, Eady PE. Egg mass and incubation period allometry in birds and reptiles: effects of phylogeny. J Zool. 2006;270(2):209–18.View ArticleGoogle Scholar
- Demment MW, Vansoest PJ. A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am Nat. 1985;125(5):641–72.View ArticleGoogle Scholar
- Ghalambor CK, Martin TE. Comparative manipulation of predation risk in incubating birds reveals variability in the plasticity of responses. Behav Ecol. 2002;13(1):101–8.View ArticleGoogle Scholar
- Giesen KM, Braun CE. Nesting behaviour of the female white-tailed ptarmigan in Colorado. Condor. 1979;81:215–7.View ArticleGoogle Scholar
- Gloutney ML, Clark RG. The significance of body-mass to female Dabbling Ducks during late incubation. Condor. 1991;93:811–6.View ArticleGoogle Scholar
- Hepp GR, Kennamer RA, Harvey WF. Incubation as a reproductive cost in female wood ducks. Auk. 1990;107:756–64.View ArticleGoogle Scholar
- Johnsgard PA. The grouse of the world. Lincoln: University of Nebraska Press; 1983. p. 13–9.Google Scholar
- Londono GA, Levey DJ, Robinson SK. Effects of temperature and food on incubation behaviour of the northern mockingbird, Mimus polyglottos. Anim Behav. 2008;76:669–77.View ArticleGoogle Scholar
- Lou YQ, Shi M, Fang Y, Swenson JE, Lyu N, Sun YH. Male vigilance and presence are important for foraging by female Chinese grouse in the pre-incubation period. Wildl Biol. 2017;1(Suppl):1–6.Google Scholar
- MacDonald EC, Camfield AF, Jankowski JE, Martin K. An alpine-breeding songbird can adjust dawn incubation rhythms to annual thermal regimes. Auk. 2014;131:495–506.View ArticleGoogle Scholar
- Mallory ML. Incubation scheduling by Northern Fulmars (Fulmarus glacialis) in the Canadian High Arctic. J Ornithol. 2009;150:175–81.View ArticleGoogle Scholar
- Manlove CA, Hepp GR. Patterns of nest attendance in female wood ducks. Condor. 2000;102:286–91.View ArticleGoogle Scholar
- Martin K, Hannon SJ, Rockwell RF. Clutch size variation and patterns of attrition in fecundity of Willow Ptarmigan. Ecology. 1989;70:1788–99.View ArticleGoogle Scholar
- Martin TE, Auer SK, Bassar RD, Niklison AM, Lloyd P. Geographic variation in avian incubation periods and parental influences on embryonic temperature. Evolution. 2007;61:2558–69.View ArticleGoogle Scholar
- Martin TE. A new view of avian life-history evolution tested on an incubation paradox. Proc R Soc B Biol Sci. 2002;269:309–16.View ArticleGoogle Scholar
- Maxson SJ. Activity patterns of female ruffed grouse during the breeding season. Wilson Bull. 1977;89:439–55.Google Scholar
- McCourt KH, Boag DA, Keppie DM. Female spruce grouse activities during laying and incubation. Auk. 1973;90:619–23.View ArticleGoogle Scholar
- Müller U. Aktivitätsuntersuchungen an freilebenden Haselhühnern (Bonasa bonasia L. 1758). Diplomarbeit. Freiburg, Germany: University of Freiburg. 1992.Google Scholar
- Naylor BJ, Szuba KJ, Bendell JF. Nest cooling and recess length of incubating spruce grouse. Condor. 1988;90:489–92.View ArticleGoogle Scholar
- Persson I, Göransson G. Nest attendance during egg laying in pheasants. Anim Behav. 1999;58:159–64.View ArticleGoogle Scholar
- Piersma T, Lindstrom A, Drent RH, Tulp I, Jukema J, Morrison RIG, Reneerkens J, Schekkerman H, Visser GH. High daily energy expenditure of incubating shorebirds on High Arctic tundra: a circumpolar study. Funct Ecol. 2003;17:356–62.View ArticleGoogle Scholar
- Pynnönen A. Beiträge zur Kenntnis der Lebensweise des Haselhuhns, Tetrastes bonasia (L.). Pap Game Res. 1954;12:1–90.Google Scholar
- Quillfeldt P, Masello JF, Lubjuhn T. Variation in the adult body mass of Wilson’s storm petrels Oceanites oceanicus during breeding. Polar Biol. 2006;29:372–8.View ArticleGoogle Scholar
- Reneerkens J, Grond K, Schekkerman H, Tulp I, Piersma T. Do Uniparental Sanderlings Calidris alba increase egg heat input to compensate for low nest attentiveness? PLoS ONE. 2011;6:1–9.View ArticleGoogle Scholar
- Schubert CA, Cooke F. Egg-laying intervals in the Lesser Snow Goose. Wilson Bull. 1993;105:414–26.Google Scholar
- Semenov-Tyan-Shanskii O. Ekologiya teterevinykh ptits. Trudy Laplandskogo Gosudarstvennogo Zapovednika. 1960;5:1–318 (in Russian).Google Scholar
- Shoji A, Elliott KH, Aris-Brosou S, Crump D, Gaston AJ. Incubation patterns in a central-place forager affect lifetime reproductive success: Scaling of patterns from a foraging bout to a lifetime. PLoS ONE. 2011;6:1–10.Google Scholar
- Sun YH. Distribution and status of the Chinese grouse Bonasa sewerzowi. Wildl Biol. 2000;6:271–5.View ArticleGoogle Scholar
- Sun YH, Swenson JE, Fang Y, Klaus S, Scherzinger W. Population ecology of the Chinese grouse, Bonasa sewerzowi, in a fragmented landscape. Biol Conserv. 2003;110:177–84.View ArticleGoogle Scholar
- Sun YH, Fang Y, Swenson JE, Klaus S, Zheng GM. Morphometrics of the Chinese grouse Bonasa sewerzowi. J Ornithol. 2005;146:24–6.View ArticleGoogle Scholar
- Swenson JE, Saari L, Bonczar Z. Effects of weather on Hazel Grouse reproduction—an allometric perspective. J Avian Biol. 1994;25:8–14.View ArticleGoogle Scholar
- Vleck CM. Hummingbird incubation—female attentiveness and egg temperature. Oecologia. 1981;51:199–205.View ArticleGoogle Scholar
- Watson A. The behaviour of the ptarmigan. Brit Birds. 1972;65:6–26.Google Scholar
- Wang J, Chen Y, Lu N, Fang Y, Sun YH. Diet of Chinese Grouse (Tetrastes sewerzowi) during preincubation. Wilson J Ornithol. 2010;122:177–80.View ArticleGoogle Scholar
- Wang JM, Beissinger SR. Partial incubation in birds: its occurrence, function, and quantification. Auk. 2011;128:454–66.View ArticleGoogle Scholar
- Webb DR. Thermal tolerance of avian embryos: a review. Condor. 1987;97:708–17.Google Scholar
- Wiebe K, Martin K. Ecological and physiological effects on egg laying intervals in ptarmigan. Condor. 1995;97:708–17.View ArticleGoogle Scholar
- Wiebe K, Martin K. Effects of predation, body condition and temperature on incubation rhythms of white-tailed ptarmigan Lagopus leucurus. Wildl Biol. 1997;3:219–27.View ArticleGoogle Scholar
- Wiebe K, Martin K. The use of incubation behaviour to adjust avian reproductive costs after egg laying. Behav Ecol Sociobiol. 2000;48:463–70.View ArticleGoogle Scholar
- Winder VL, Herse MR, Hunt LM, Gregory AJ, McNew LB, Sandercock BK. Patterns of nest attendance by female Greater Prairie-Chickens (Tympanuchus cupido) in northcentral Kansas. J Ornithol. 2016;157(3):733–45.View ArticleGoogle Scholar
- Zhao JM, Fang Y, Ma YH, Sun YH. The importance of willow to the Chinese Grouse: evidence from analysis on their breeding territories at Lianhuashan, China. Avian Res. 2017;8:32.View ArticleGoogle Scholar
- Zhao JM, Fang Y, Lou YQ, Swenson JE, Sun YH. Brood rearing has an immediate survival cost for female Chinese grouse tetrastes sewerzowi. J Ornithol. 2018;159:1019–29.View ArticleGoogle Scholar
- Zhao JM, Yang C, Lou YQ, Shi M, Fang Y, Sun YH. Nesting season, nest age and disturbance, but not habitat characteristics affect nest survival of Chinese grouse. Curr Zool. 2019. https://doi.org/10.1093/cz/zoz024.View ArticlePubMedGoogle Scholar