More than a simple egg: Underlying mechanisms of cold tolerance in avian embryos

Ibrahim M. Ahmad; Dongming Li

doi:10.1016/j.avrs.2023.100104

Volume 14 Issue 1

Feb. 2023

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Article Contents

Abstract

Author contributions

Ethics statement

Declaration of competing interests

Acknowledgements

Appendix A. Supplementary data

References

Avian Research > 2023 > 14(1): 100104. > DOI: 10.1016/j.avrs.2023.100104

Ibrahim M. Ahmad, Dongming Li. 2023: More than a simple egg: Underlying mechanisms of cold tolerance in avian embryos. Avian Research, 14(1): 100104. DOI: 10.1016/j.avrs.2023.100104

Citation:

Ibrahim M. Ahmad, Dongming Li. 2023: More than a simple egg: Underlying mechanisms of cold tolerance in avian embryos. Avian Research, 14(1): 100104. DOI: 10.1016/j.avrs.2023.100104

Citation:

Ibrahim M. Ahmad, Dongming Li. 2023: More than a simple egg: Underlying mechanisms of cold tolerance in avian embryos. Avian Research, 14(1): 100104. DOI: 10.1016/j.avrs.2023.100104

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More than a simple egg: Underlying mechanisms of cold tolerance in avian embryos

Ibrahim M. Ahmad^{a, b},
Dongming Li^{a, b, ,}

a.
Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang, 050024, China
b.
Hebei Collaborative Innovation Center for Eco-Environment, Hebei Normal University, Shijiazhuang, 050024, China

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Corresponding author:
Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang, 050024, China. E-mail address: lidongming@hebtu.edu.cn (D. Li)
Received Date: 02 Feb 2023
Rev Recd Date: 13 Apr 2023
Accepted Date: 17 Apr 2023
Available Online: 14 Jun 2023
Publish Date: 30 Apr 2023

Graphical Abstract

Abstract

Abstract

Avian embryos, which develop within eggs, exhibit remarkable tolerance to extremely low temperatures. Despite being a common trait among all birds, the mechanisms underlying this cold tolerance in avian embryos remain largely unknown. To gain a better understanding of this phenomenon and the coping mechanisms involved, we reviewed the literature on severe cold tolerance in embryos of both wild and domestic birds. We found that embryos of different bird orders exhibit tolerance to severe cold during their development. In response to cold stress, embryos slow down their heartbeat rates and metabolism. In severe cold temperatures, embryos can suspend these processes, entering a torpid-like state of cardiac arrest. To compensate for these developmental delays, embryos extend their regular incubation periods. Depending on their embryonic age, embryos of all bird species can tolerate acute severe cold regimes; only a few tolerate chronic severe cold regimes. We also discussed various extrinsic and intrinsic factors that affect the tolerance of bird embryos to low temperatures before and after incubation. Cold tolerance appears to be a heritable trait shared by wild and domestic embryos of all bird classes, regardless of egg size or development (altricial/precocial). Driven by environmental variability, cold tolerance in avian embryos is an optimal physiological and ecological strategy to mitigate the adverse effects of cold conditions on their development in response to fluctuating environmental temperatures.
- Acute cold tolerance,
- Avian embryo,
- Chronic cold tolerance,
- Embryonic development,
- Hatching success,
- Incubation period

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In sympatrical breeding, closely related bird species potentially compete for resources, including food, nest sites, song perches, and roost sites (Cody, 1969). This may result in interspecific territoriality and/or segregation in resource use. In addition, selection by predation may lead to maximizing the variance in nest sites of different species within avian communities (e.g., Martin, 1996). However, whether coexisting closely related species will converge or diverge in their traits has been a subject of debate (Murray, 1976). In addition, the most important studies attempting to demonstrate interspecific competition were performed on cavity nesters, where nest sites are a strongly limiting factor (Hill and Lein, 1989; Ye et al., 2019). Thus, more studies considering a range of open-nesting species are needed to resolve this issue.

The Buffy Laughingthrush (Garrulax berthemyi) is a species endemic to central and southeastern China (Zheng, 2017). The Red-tailed Laughingthrush (Trochalopteron milnei) is sympatric with the Buffy Laughingthrush in our study site and is distributed in southern China, northern Burma, and Indochina (Collar et al., 1994; Zheng, 2017). To our knowledge, there is little available data on the natural history of these two species. The two laughingthrush species breed in sympatry and share similar habitats in the Kuankuoshui Nature Reserve. The objectives of our work were to: (1) find and describe the nests, eggs, nestlings, and breeding behavior of the Buffy Laughingthrush and Red-tailed Laughingthrush; (2) survey their breeding densities and predation rates; and (3) compare the breeding ecology of these two sympatric species.

The study was performed in the Kuankuoshui Nature Reserve, Guizhou province, southwestern China (28°10ʹ N, 107°10ʹ E) from April to July 2005–2009. The annual average temperature there is 13.6 ℃, and the average annual total precipitation is 1210 mm (Yang et al., 2020). The study site is situated in a subtropical moist broadleaf and mixed forest at an altitude of about 1500 m, and is interspersed with abandoned tea plantations, bamboo, and shrubby areas, and open fields used as cattle pastures. The breeding density for each of the two species was surveyed by the line transect method during the breeding season from 2005 to 2009. Five 100-m width sampling lines that covered the study site were arranged with a distance of 6 km for each line (Appendix Fig. S1). Every sampling line was surveyed five times (once each year) by walking at a speed of 1.5 km/h. Breeding density (number of pairs per km²) was averaged for the five yearly surveys.

Nests were found by systematically searching all typical and potential nest sites and by monitoring the activities of adults throughout the breeding season. We monitored nests daily by recording nest-building activity, the date of the first egg, egg color, clutch size, and nest habitat, and also calculated the predation rate. Nest failure was assumed to be due to predation if remains of eggs or nestlings were found in or beneath nests or if the entire contents disappeared, and due to desertion if eggs or young were present but unattended. Nestlings were assumed to have fledged if they were at least 12 d old and nests were found empty and undisturbed on or shortly after the anticipated fledging date. Because of the remoteness of some nest sites from our campsite, not all nests were inspected regularly, and sample sizes varied for different breeding parameters. Moreover, sample sizes of nests varied among years due to differences in time spent in the field. We thus pooled data from different years.

Egg size and mass were measured with an electronic caliper (precision 0.01 mm) and a portable electronic scale (precision 0.01 g), respectively, shortly after clutch completion or during early incubation. Egg volume was estimated by using the formula (0.51 × length × (width²)) of Hoyt (1979). The eggs were photographed in a standardized manner on a grey card using a Canon EOS 500D digital camera. When a nest was found during the incubation period, the eggs were floated to estimate the laying date (Hays and Lecroy, 1971). We also measured the nest size and nest height and estimated nest cover at 15 cm above the nest. Nest size and nest height above the ground were measured by a tape measure. Nest cover was visually estimated from 0% to 100%. Either Student's t-test or the χ² test was used for comparing the nest parameters between Red-tailed Laughingthrush and Buffy Laughingthrush. All statistical analyses were carried out by using SPSS 16.0 (SPSS Inc, Chicago, Illinois). Data are presented as mean ± SE (standard error), and the significance level is set to P < 0.05.

Our results showed that mean breeding densities of the Buffy Laughingthrush and Red-tailed Laughingthrush were 17.6 pairs/km² and 25.8 pairs/km², respectively. A total of 12 Buffy Laughingthrush and 27 Red-tailed Laughingthrush nests were found (yearly sample sizes = 5, 2, 2, 3, 0 and 6, 2, 3, 15, 1 in 2005–2009, respectively). The breeding time of these two laughingthrushes was from April to late July. The laying date of the first egg in Buffy and Red-tailed laughingthrushes was 3 May – 10 July and 1 May – 14 July, respectively. Buffy and Red-tailed Laughingthrushes built nests in bamboo or tree forests, with no significant interspecific differences in microhabitat choice or height of the nests above the ground (Table 1). However, the nest cover of the Buffy Laughingthrush was denser than that of the Red-tailed Laughingthrush (Table 1). Both laughingthrushes built cup-shaped nests out of bamboo or tree leaves, also adding some moss. The Buffy Laughingthrush used fibers or pine needles to line the nest cup, but the Red-tailed Laughingthrush used black fern roots. The nest size of Buffy Laughingthrushes was similar to that of Red-tailed Laughingthrushes in all dimensions except outer nest depth: Buffy Laughingthrush nest structures were higher than those of Red-tailed Laughingthrush nests (Table 1). The eggs of the two species did not differ significantly in size or mass (Table 1), but were dramatically different in coloration (Fig. 1). Buffy Laughingthrush eggs were plain blue, while those of the Red-tailed Laughingthrush were white with scarce maroon blotches (Fig. 1). In addition, the clutch sizes of the two laughingthrush species were also very similar (Table 1). Nest predation was the major cause of nest failure, taking a similar toll in both species (Table 1). The nestling gape pattern differed substantially between the two species (Fig. 1). The gape of Buffy Laughingthrush's nestlings was lemon-yellow. However, Red-tailed Laughingthrush nestlings had a conspicuous orange gape and were covered in golden-brown down on the head and the back (Fig. 1).

Table 1. Differences in breeding parameters between Buffy Laughingthrush and Red-tailed Laughingthrush.

Parameters	Red-tailed Laughingthrush	Buffy Laughingthrush	Statistics^a	P
Egg coloration	White + brown spots	Immaculate blue	–	–
Clutch size	2.75 ± 0.25 (12)	3.78 ± 0.15 (9)	– 3.24	0.004^*
Egg size (cm³)	6.87 ± 0.18 (12)	6.77 ± 0.21 (9)	0.38	0.709
Cup diameter (cm)	8.62 ± 0.27 (6)	9.20 ± 0.38 (5)	– 1.30	0.225
Nest diameter (cm)	11.6 ± 2.13 (6)	13.4 ± 0.51 (5)	– 0.75	0.472
Cup depth (cm)	6.05 ± 0.28 (6)	4.90 ± 0.25 (5)	3.04	0.014^*
Nest depth (cm)	10.18 ± 0.26 (5)	10.60 ± 1.17 (5)	– 0.35	0.735
Nest height (m)	2.24 ± 0.16 (25)	2.37 ± 0.09 (12)	– 0.54	0.594
Nest cover (%)	58.95 ± 5.22 (19)	70.00 ± 6.57 (11)	– 1.30	0.204
Habitat (%)	93% bamboo, 7% tree (27)	17% shrub, 25% bamboo, 58% tree (12)	17.68^ψ	< 0.001^*
Predation rate (%)	57.14 (21)	40.00 (10)	0.80^ψ	0.458
Data are presented as means ± SE (sample size). ^a Comparisons were made using either Student's t-test or the Chi-square test (indicated by "ψ"). * Statistically significant (P < 0.05).

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Figure 1. Nests, eggs, and nestlings (7 days old) of Buffy Laughingthrushes (upper row) and Red-tailed Laughingthrushes (lower row) in Kuankuoshui NR, southwestern China (Photographs by Canchao Yang).

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In the Buffy Laughingthrush, we found one case in which more than two adults fed the nestlings at the same nest. One adult brooded the nestlings while two others fed them. Furthermore, occasionally more than two birds were observed to be mobbing the observer in the vicinity of their nests. Our detailed comparison of two closely related and sympatric species of laughingthrush revealed few differences in their breeding ecology, but the nest cover, egg color, and nestling gape morphology were found to differ between the two species. Wallace (1889) hypothesized that the ancestral white egg has been retained by species whose nests are safe from predator attacks (cavity nesters), while species with more vulnerable nest sites are more likely to lay pigmented eggs. Blue-green egg coloration is thought to be camouflaging in forest environments where greenish light is filtered out by the canopy (Lack, 1968). Furthermore, the Buffy Laughingthrush and Red-tailed Laughingthrush laid blue and white eggs, respectively, and bred in similar habitats. However, Red-tailed Laughingthrushes chose nest sites significantly more concealed from above compared to Buffy Laughingthrushes, suggesting a possible explanation for differences in egg appearance of the two species. Predation rates in these two species were not significantly different, but this may have been due to the adjustment of nest site cover and egg color, or perhaps that the effect is slight, thus requiring larger samples to be detected. Finally, more than two adults of the Buffy Laughingthrush were observed feeding the nestlings in the same nest. This phenomenon indicated that cooperative breeding may exist in the population of Buffy Laughingthrush, but more data are needed to confirm this behavior.

Author contributions

CY conceived and designed the study. CY and PY conducted the investigation in the field, analyzed the data and drafted the manuscript. XY, GL and WL assisted the field work. All authors read and approved the final manuscript.

Ethics statement

Fieldwork was carried out under the permission from Kuankuoshui National Nature Reserve, China. Experimental procedures were in agreement with the Animal Research Ethics Committee of Hainan Provincial Education Centre for Ecology and Environment, Hainan Normal University (permit no. HNECEE-2011-001).

Declaration of competing interests

The authors declare that they have no competing interests.

Acknowledgements

We thank the Forestry Department of Guizhou Province and Kuankuoshui National Nature Reserves for support and permission to carry out this study. Financial support has been provided by Hainan Provincial Natural Science Foundation of China (320CXTD437 and 2019RC189 to CY), and Hainan Provincial Innovative Research Program for Graduates (Hyb2021-7 to XY) National Natural Science Foundation of China (No. 31672303 to CY and No. 31970427 to WL).

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.avrs.2022.100024.

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More than a simple egg: Underlying mechanisms of cold tolerance in avian embryos