AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Avian Research Article
PDF (4.6 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Comparisons of microstructure and elemental composition of eggshells among wild plover populations

Langyu Gua,1, Hanyu Yangb,1, Canwei Xiac, Zitan Songd, Yachang Chengb, Chenjing Huangc, Yuelou Liub, Yang Liub( )
State Key Laboratory for Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, Guangdong, 510275, China
State Key Laboratory for Biocontrol, School of Ecology, Sun Yat-sen University, Shenzhen, 518017, China
Ministry of Education Key Laboratory for Biodiversity and Ecological Engineering, College of Life Sciences, Beijing Normal University, 100875, Beijing, China
Department for the Ecology of Animal Societies, Max Planck Institute of Animal Behavior, Konstanz, 78467, Germany

1 These authors contributed equally to this work.

Show Author Information

Abstract

Reproduction investment is a prominent trade-off in life-history theory and is subject to strong selection pressure. The avian eggshell, as a crucial barrier between the bird embryo and the surrounding environment, undergoes optimization under different environmental selection regimes to ensure the successful development of embryos, which can be linked to local adaptation. Therefore, understanding the variation in eggshell microstructure and composition in wild bird populations living in contrasting ambient environments is of great significance. In this study, we utilized electron microscope ultrastructure measurement and elemental analyses to measure and compare the microstructure and element composition of eggshells from three wild plover populations (Charadrius alexandrinus and C. dealbatus) residing in heterogeneous habitats across varied climatic zones. These populations include the high-altitude Qinghai Lake population, the temperate coastal Tangshan population, and the tropical coastal Zhanjiang population. Our findings revealed that the palisade layer was thinner in the Qinghai Lake population compared to its lowland populations. This difference might be attributed to hypoxia which facilitates the hatching process by allowing chicks to easily break through their shells. Additionally, the variations in the elemental composition of the eggshells among populations well reflected the distribution of element content in different geographical regions. The Qinghai Lake population displayed low zinc and low manganese levels but high calcium levels, while the Zhanjiang population exhibited high zinc, high iron, high manganese, and high phosphorus levels. Furthermore, these variations in elemental composition could also account for the observed microstructural differences among populations. Collectively, we propose that the dissimilarities in eggshell microstructure and elemental composition among populations could be attributed to adaptations to different environmental conditions. Our findings lay the groundwork for future research to explore the mechanisms behind the variations in eggshell characteristics among wild bird populations, and contribute to a broader understanding of biodiversity mechanisms.

Keywords

MicrostructureEggshellShorebirdReproductionPalisade layer

References

 

Alrashidi, M., Kosztolányi, A., Küpper, C., Cuthill, I.C., Javed, S., Székely, T., 2010. The influence of a hot environment on parental cooperation of a ground-nesting shorebird, the Kentish plover Charadrius alexandrinus. Front. Zool. 7, 1.
Crossref Google Scholar
 

Ar, A., Rahn, H., 1985. Pores in avian eggshells: gas conductance, gas exchange and embryonic growth rate. Respir. Physiol. 61, 1–20.
Crossref Google Scholar
 

Arad, Z., 1989. Changes in eggshell water vapour conductance during shell formation in the chicken. Respir. Physiol. 78, 197–206.
Crossref Google Scholar
 

Archer, G.S., 2019. How does red light affect layer production, fear, and stress? Poultry Sci. 98, 3–8.
Crossref Google Scholar
 

Bebout, D.E., Hempleman, S.C., 1994. Calcium deficient diet, acetazolamide and gas exchange characteristics of avian eggshells. Respir. Physiol. 95, 11–20.
Crossref Google Scholar
 

Bleu, J., Agostini, S., Angelier, F., Biard, C., 2019. Experimental increase in temperature affects eggshell thickness, and not egg mass, eggshell spottiness or egg composition in the great tit (Parus major). Gen. Comp. Endocrinol. 275, 73–81.
Crossref Google Scholar
 

Cao, H., Deng, Y., Chen, F., Pu, X., 2020. Analysis of trace element characteristics and ecological risk assessment in the surface of sediments in the Zhanjiang Bay. J. Ocean Technol. 2, 71–77.
Google Scholar
 

Chang, G., Liu, N., Yang, W., Zhong, R., Ren, H., 2020. Characteristics and influencing factors of heavy metals in Tangshan Coastal environment. Front. Earth Sci. 10, 1042–1050.
Crossref Google Scholar
 

Chien, Y.-C., Hincke, M.T., McKee, M.D., 2009. Ultrastructure of avian eggshell during resorption following egg fertilization. J. Struct. Biol. 168, 527–538.
Crossref Google Scholar
 

Chien, Y.C., Hincke, M.T., Vali, H., McKee, M.D., 2008. Ultrastructural matrix-mineral relationships in avian eggshell, and effects of osteopontin on calcite growth in vitro. J. Struct. Biol. 163, 84–99.
Crossref Google Scholar
 

Dauphin, Y., Luquet, G., Perez-Huerta, A., Salomé, M., 2018. Biomineralization in modern avian calcified eggshells: similarity versus diversity. Connect. Tissue Res. 59, 67–73.
Crossref Google Scholar
 

Dieckert, J.W., Dieckert, M.C., Creger, C.R., 1989. Calcium reserve assembly: a basic structural unit of the calcium reserve system of the hen egg shell. Poultry Sci. 68, 1569–1584.
Crossref Google Scholar
 

Ding, J., Yang, W., Yang, Y., Ai, S., Bai, X., Zhang, Y., 2019. Variations in tree sparrow (Passer montanus) egg characteristics under environmental metal pollution. Sci. Total Environ. 687, 946–955.
Crossref Google Scholar
 

Ebeid, T.A., Suzuki, T., Sugiyama, T., 2012. High ambient temperature influences eggshell quality and calbindin-D28k localization of eggshell gland and all intestinal segments of laying hens. Poultry Sci. 91, 2282–2287.
Crossref Google Scholar
 

Flatt, T., Heyland, A., 2011. Mechanisms of Life History Evolution : the Genetics and Physiology of Life History Traits and Trade-Offs. Oxford University Press, Oxford.
Crossref
 

Gongruttananun, N., 2011. Influence of red light on reproductive performance, eggshell ultrastructure, and eye morphology in Thai-native hens. Poultry Sci. 90, 2855–2863.
Crossref Google Scholar
 

Halgrain, M., Bernardet, N., Crepeau, M., Même, N., Narcy, A., Hincke, M., et al., 2022. Eggshell decalcification and skeletal mineralization during chicken embryonic development: defining candidate genes in the chorioallantoic membrane. Poultry Sci. 101, 101622.
Crossref Google Scholar
 

Hempleman, S.C., Adamson, T.P., Bebout, D.E., 1993. Oxygen and avian eggshell formation at high altitude. Respir. Physiol. 92, 1–12.
Crossref Google Scholar
 

Huang, L., Shen, J., Feng, Y., Li, D., Wang, W., Yang, L., et al., 2020. Effect of dietary zinc level on egg production performance and eggshell quality characteristics in laying duck breeders in furnished cage system. Biol. Trace Elem. Res. 196, 597–606.
Crossref Google Scholar
 

Hung, C.-M., Tsao, S.-H., Chiang, P.-L., Wu, S.-P., Tuanmu, M.-N., Juang, J.-Y., 2022. Functional connections between bird eggshell stiffness and nest characteristics through risk of egg collision in nests. Ecol. Lett. 25, 1421–1431.
Crossref Google Scholar
 

Jetz, W., Sekercioglu, C.H., Böhning-Gaese, K., 2008. The worldwide variation in avian clutch size across species and space. PLoS Biol. 6, 2650–2657.
Crossref Google Scholar
 

Kamanlı, S., Demirtaş, Ş. E., Onbaşılar, E.E., Bakır, B., Yalçın, S., Göğer, H., et al., 2021. The effects of the breeder index value on the microscopic structure of egg shells, hatching results, and hybrid performance. Trop. Anim. Health Prod. 53, 557.
Crossref Google Scholar
 

Karlsson, O., Lilja, C., 2008. Eggshell structure, mode of development and growth rate in birds. Zoology (Jena) 111, 494–502.
Crossref Google Scholar
 

Kim, J.H., Kim, H.W., Kwon, C.H., Kwon, S.H., Kil, D.Y., 2023. Effects of dietary organic or inorganic iron concentrations on productive performance, egg quality, blood measurements, and tissue iron concentrations in aged laying hens. Anim. Sci. J. 94, e13817.
Crossref Google Scholar
 

Kosztolányi, A., Székely, T., Cuthill, I.C., Yilmaz, K.T., Berberoglu, S., 2006. Ecological constraints on breeding system evolution: the influence of habitat on brood desertion in Kentish plover. J. Anim. Ecol. 75, 257–265.
Crossref Google Scholar
 

Lee, J., McCurdy, C., Chae, C., Hwang, J., Karolak, M.C., Kim, D.-H., et al., 2021. Myostatin mutation in Japanese quail increased egg size but reduced eggshell thickness and strength. Animals 12, 47.
Crossref Google Scholar
 

Liao, X., Yan, J., Chen, J., Huang, Z., Xiao, T., Li, C., et al., 2022. A simple daily dynamic feeding regimen for reducing phosphorus consumption and excretion in laying hens. Anim. Nutr. 11, 132–141.
Crossref Google Scholar
 

Liu, J., Chai, Z., Wang, H., Ivanov, A., Kubelka, V., Freckleton, R., et al., 2023. Effects of feeding strategies on eggshell quality of laying hens during late laying period. Poultry Sci. 102, 102406.
Crossref Google Scholar
 

Mayer, A.N., Vieira, S.L., Berwanger, E., Angel, C.R., Kindlein, L., França, I., et al., 2019. Zinc requirements of broiler breeder hens. Poultry Sci. 98, 1288–1301.
Crossref Google Scholar
 

McClelland, S.C., Cassey, P., Maurer, G., Hauber, M.E., Portugal, S.J., 2021. How much calcium to shell out? Eggshell calcium carbonate content is greater in birds with thinner shells, larger clutches and longer lifespans. J. R. Soc. Interface 18, 20210502.
Crossref Google Scholar
 

Nakagawa, S., Schielzeth, H., 2017. rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol. Evol. 8, 1639–1644.
Crossref Google Scholar
 

Orłowski, G., Siebielec, G., Kasprzykowski, Z., Dobicki, W., Pokorny, P., Wuczyński, A., et al., 2016. Effect of spatial resolution of soil data on predictions of eggshell trace element levels in the Rook Corvus frugilegus. Environ. Pollut. 219, 288–295.
Crossref Google Scholar
 

Peebles, E.D., Brake, J., Gildersleeve, R.P., 1987. Effects of eggshell cuticle removal and incubation humidity on embryonic development and hatchability of broilers. Poultry Sci. 66, 834–840.
Crossref Google Scholar
 
Reynolds, S.J., Perrins, C.M., 2010. Dietary calcium availability and reproduction in birds. In: Current Ornithology, 17. Springer, New York, NY, pp. 31–74.
Crossref
 

Solomon, S.E., 2010. The eggshell: strength, structure and function. Br. Poultry Sci. 51(Suppl. 1), 52–59.
Crossref Google Scholar
 

Song, Z., Lin, X., Que, P., Halimubieke, N., Huang, Q., Zhang, Z., et al., 2020. The allocation between egg size and clutch size depends on local nest survival rate in a mean of bet-hedging in a shorebird. Avian Res. 11, 40.
Crossref Google Scholar
 
Song, Z., Que, P., Jones, W., Huang, C., Halimubieke, N., Ding, P., et al., 2023. Colder Ambient Temperatures Constrain Female Mate Preference for Ornamental Traits. Authorea.
Crossref
 

Sozcu, A., Ipek, A., 2015. Acute and chronic eggshell temperature manipulations during hatching term influence hatchability, broiler performance, and ascites incidence. Poultry Sci. 94, 319–327.
Crossref Google Scholar
 

Sözcü, A., İpek, A., van den Brand, H., 2022. Eggshell temperature during early and late incubation affects embryo and hatchling development in broiler chicks. Poultry Sci. 101, 102054.
Crossref Google Scholar
 

Stearns, S.C., 1989. Trade-offs in life-history evolution. Funct. Ecol. 3, 259.
Crossref Google Scholar
 

Stefanello, C., Santos, T.C., Murakami, A.E., Martins, E.N., Carneiro, T.C., 2014. Productive performance, eggshell quality, and eggshell ultrastructure of laying hens fed diets supplemented with organic trace minerals. Poultry Sci. 93, 104–113.
Crossref Google Scholar
 

Stoddard, M.C., Yong, E.H., Akkaynak, D., Sheard, C., Tobias, J.A., Mahadevan, L., 2017. Avian egg shape: Form, function, and evolution. Science 356, 1249–1254.
Crossref Google Scholar
 

Stoewsand, G.S., Anderson, J.L., Gutenmann, W.H., Lisk, D.J., 1978. Influence of dietary calcium selenium and methylmercury on eggshell thickness in Japanese quail. Bull. Environ. Contam. Toxicol. 20, 135–142.
Crossref Google Scholar
 

Stoffel, M.A., Nakagawa, S., Schielzeth, H., 2017. rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol. Evol. 8, 1639–1644.
Crossref Google Scholar
 
Székely, T., Kosztolányi, A., Küpper, C., 2008. Practical Guide for Investigating Breeding Ecology of Kentish Plover Charadrius Alexandrinus. Unpublished Report, University of Bath. https://www.researchgate.net/publication/228494424_Practical_guide_for_investigating_breeding_ecology_of_Kentish_plover_Charadrius_alexandrinus.
 

van der Pol, C.W., van Roovert-Reijrink, I.A.M., Maatjens, C.M., van den Brand, H., Molenaar, R., 2013. Effect of relative humidity during incubation at a set eggshell temperature and brooding temperature posthatch on embryonic mortality and chick quality. Poultry Sci. 92, 2145–2155.
Crossref Google Scholar
 

Vincze, O., Székely, T., Küpper, C., Alrashidi, M., Amat, J.A., Ticó, A.A., et al., 2013. Local environment but not genetic differentiation influences biparental care in ten plover populations. PLoS One 8, e60998.
Crossref Google Scholar
 

Wang, P., Cao, J.-J., Wu, F., 2010. Environmental background values and its impact factors of topsoil within the Lake Qinghai catchment, Northeast Tibetan Plateau, China. J. Earth Environ. 3, 189–200.
Google Scholar
 

Wang, X., Que, P., Heckel, G., Hu, J., Zhang, X., Chiang, C.Y., et al., 2019. Genetic, phenotypic and ecological differentiation suggests incipient speciation in two Charadrius plovers along the Chinese coast. BMC Evol. Biol. 19, 1–18.
Crossref Google Scholar
 

Xin, Q., Wang, M., Jiao, H., Zhao, J., Li, H., Wang, X., et al., 2021. Prolonged scotophase within a 24 hour light regime improves eggshell quality by enhancing calcium deposition in laying hens. Poultry Sci. 100, 101098.
Crossref Google Scholar
 

Yang, C., Huang, Q., Wang, L., Du, W.-G., Liang, W., Møller, A.P., 2018. Keeping eggs warm: thermal and developmental advantages for parasitic cuckoos of laying unusually thick-shelled eggs. Naturwissenschaften 105, 10.
Crossref Google Scholar
 

Zhang, Y.N., Zhang, H.J., Wu, S.G., Wang, J., Qi, G.H., 2017. Dietary manganese supplementation modulated mechanical and ultrastructural changes during eggshell formation in laying hens. Poultry Sci. 96, 2699–2707.
Crossref Google Scholar
Avian Research
Volume 14 Issue 4,
December 2023
Article number: 100146
DOI: 10.1016/j.avrs.2023.100146
Cite this article:
Gu L, Yang H, Xia C, et al. Comparisons of microstructure and elemental composition of eggshells among wild plover populations. Avian Research, 2023, 14(4): 100146. https://doi.org/10.1016/j.avrs.2023.100146

160

Views

8

Downloads

0

Crossref

0

Web of Science

0

Scopus

0

CSCD

Altmetrics
Received: 11 July 2023
Revised: 05 October 2023
Accepted: 30 October 2023
Published: 06 November 2023
© 2023 The Authors.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Return