{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,12]],"date-time":"2026-10-12T18:41:41Z","timestamp":1791830501677,"version":"4.3.4"},"reference-count":41,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2023,4,19]],"date-time":"2023-04-19T00:00:00Z","timestamp":1681862400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Natural Science Foundation of China","award":["no. 32000355 (Tao Pan)"],"award-info":[{"award-number":["no. 32000355 (Tao Pan)"]}]},{"name":"National Natural Science Foundation of China","award":["31872253"],"award-info":[{"award-number":["31872253"]}]},{"name":"National Natural Science Foundation of China","award":["32170525 (Xiaobing Wu)"],"award-info":[{"award-number":["32170525 (Xiaobing Wu)"]}]},{"name":"National Natural Science Foundation of China","award":["AHLYCX-2021-01"],"award-info":[{"award-number":["AHLYCX-2021-01"]}]},{"name":"National Natural Science Foundation of China","award":["1908085QC127"],"award-info":[{"award-number":["1908085QC127"]}]},{"name":"National Natural Science Foundation of China","award":["2019HJ2096001006"],"award-info":[{"award-number":["2019HJ2096001006"]}]},{"name":"Anhui Forestry Science and Technology Innovation Project","award":["no. 32000355 (Tao Pan)"],"award-info":[{"award-number":["no. 32000355 (Tao Pan)"]}]},{"name":"Anhui Forestry Science and Technology Innovation Project","award":["31872253"],"award-info":[{"award-number":["31872253"]}]},{"name":"Anhui Forestry Science and Technology Innovation Project","award":["32170525 (Xiaobing Wu)"],"award-info":[{"award-number":["32170525 (Xiaobing Wu)"]}]},{"name":"Anhui Forestry Science and Technology Innovation Project","award":["AHLYCX-2021-01"],"award-info":[{"award-number":["AHLYCX-2021-01"]}]},{"name":"Anhui Forestry Science and Technology Innovation Project","award":["1908085QC127"],"award-info":[{"award-number":["1908085QC127"]}]},{"name":"Anhui Forestry Science and Technology Innovation Project","award":["2019HJ2096001006"],"award-info":[{"award-number":["2019HJ2096001006"]}]},{"name":"Anhui Natural Science Foundation","award":["no. 32000355 (Tao Pan)"],"award-info":[{"award-number":["no. 32000355 (Tao Pan)"]}]},{"name":"Anhui Natural Science Foundation","award":["31872253"],"award-info":[{"award-number":["31872253"]}]},{"name":"Anhui Natural Science Foundation","award":["32170525 (Xiaobing Wu)"],"award-info":[{"award-number":["32170525 (Xiaobing Wu)"]}]},{"name":"Anhui Natural Science Foundation","award":["AHLYCX-2021-01"],"award-info":[{"award-number":["AHLYCX-2021-01"]}]},{"name":"Anhui Natural Science Foundation","award":["1908085QC127"],"award-info":[{"award-number":["1908085QC127"]}]},{"name":"Anhui Natural Science Foundation","award":["2019HJ2096001006"],"award-info":[{"award-number":["2019HJ2096001006"]}]},{"name":"Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment","award":["no. 32000355 (Tao Pan)"],"award-info":[{"award-number":["no. 32000355 (Tao Pan)"]}]},{"name":"Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment","award":["31872253"],"award-info":[{"award-number":["31872253"]}]},{"name":"Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment","award":["32170525 (Xiaobing Wu)"],"award-info":[{"award-number":["32170525 (Xiaobing Wu)"]}]},{"name":"Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment","award":["AHLYCX-2021-01"],"award-info":[{"award-number":["AHLYCX-2021-01"]}]},{"name":"Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment","award":["1908085QC127"],"award-info":[{"award-number":["1908085QC127"]}]},{"name":"Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment","award":["2019HJ2096001006"],"award-info":[{"award-number":["2019HJ2096001006"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>The Chinese alligator (Alligator sinensis), found only in a small region in southeastern Anhui Province, is listed as critically endangered (CR) by the International Union for Conservation of Nature (IUCN) due to its current declining population trend. Any abnormalities in the physical properties of an egg can decrease the hatching rate. In particular, eggshells play an essential role in embryo development, motivating us to analyze the microstructures of the eggshells of Chinese alligators. In this study, we categorized the eggshells into two groups, based on the hatching rates, and analyzed the relationship between the eggshell parameters (eggshell thickness, calcium content, and number of pores in erosion craters) and the hatching rate, as well as the relationships between the eggshell parameters. We found that the shells of the eggs with high hatching rates were thicker than those of the eggs with low hatching rates. There were also fewer erosion-crater pores on the surfaces of the eggs with high hatching rates than on the surfaces of the eggs with low hatching rates. Moreover, the shell Ca content was significantly higher in the eggs with high hatching rates than in the eggs with low hatching rates. Cluster modeling indicated that the highest hatching rate occurred when the eggshell thickness was 200\u2013380 \u00b5m and there were 1\u201312 pores. These results suggest that eggs with adequate Ca contents, thicker shells, and less air permeability are more likely to hatch. Furthermore, our findings can inform future studies, which will be vital for the survival of the critically endangered Chinese alligator species.<\/jats:p>","DOI":"10.3390\/ani13081405","type":"journal-article","created":{"date-parts":[[2023,4,20]],"date-time":"2023-04-20T01:42:39Z","timestamp":1681954959000},"page":"1405","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Effects of Eggshell Thickness, Calcium Content, and Number of Pores in Erosion Craters on Hatching Rate of Chinese Alligator Eggs"],"prefix":"10.3390","volume":"13","author":[{"given":"Naijing","family":"Zhang","sequence":"first","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"},{"name":"Anhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huabin","family":"Zhang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"},{"name":"Anhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guangwei","family":"Fan","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"},{"name":"Anhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ke","family":"Sun","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"},{"name":"Anhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingqing","family":"Jiang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhuowen","family":"Lv","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Boyang","family":"Han","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhenyuan","family":"Nie","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yujie","family":"Shao","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yongkang","family":"Zhou","sequence":"additional","affiliation":[{"name":"Anhui Chinese Alligator National Nature Reserve, Xuancheng 242099, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Baowei","family":"Zhang","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Anhui University, Hefei 230039, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaobing","family":"Wu","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"},{"name":"Anhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tao","family":"Pan","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Anhui Normal University, Wuhu 241000, China"},{"name":"Anhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2710","DOI":"10.3382\/ps.2011-01878","article-title":"Fuzzy modeling to predict chicken egg hatchability in commercial hatchery","volume":"91","author":"Peruzzi","year":"2012","journal-title":"Poult. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2735","DOI":"10.3382\/ps.2009-00403","article-title":"Hatching egg characteristics, chick quality, and broiler performance at 2 breeder flock ages and from 3 egg weights","volume":"89","author":"Fasenko","year":"2010","journal-title":"Poult. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1079\/WPS20020023","article-title":"Egg physical characteristics and hatchability","volume":"58","author":"Narushin","year":"2002","journal-title":"Worlds Poult. Sci. J."},{"key":"ref_4","first-page":"54","article-title":"Correlation of some quality traits of hens\u2019 eggs and the level of hens\u2019 productivity with chick hatchability","volume":"Volume 2","author":"Moiseyeva","year":"1968","journal-title":"Papers on Genetics and Immunogenetics of Animals, Eggs and Chicks Hatchability"},{"key":"ref_5","unstructured":"Tsarenko, P.P., and Kurova, G.M. (1989). Effective Technologies of Poultry Production, Agropromizdat."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1114","DOI":"10.14202\/vetworld.2017.1114-1117","article-title":"The effect of eggshell thickness on hatchability of quail eggs","volume":"10","author":"Ergun","year":"2017","journal-title":"Vet. World."},{"key":"ref_7","first-page":"20162675","article-title":"Eggshell structure in Caiman latirostris eggs improves embryo survival during nest inundation","volume":"284","author":"Simoncini","year":"2017","journal-title":"Proc. Biol. Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1539","DOI":"10.4315\/0362-028X-69.7.1539","article-title":"Influence of eggshell condensation on eggshell penetration and whole egg contamination with Salmonella enterica serovar Enteritidis","volume":"69","author":"Koen","year":"2006","journal-title":"J. Food Prot."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.cbpa.2012.03.013","article-title":"Effects of dehydration on cardiovascular development in the embryonic American alligator (Alligator mississipiensis)","volume":"162","author":"Tate","year":"2012","journal-title":"Comp. Biochem. Physiol. A"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1111\/1749-4877.12269","article-title":"Reduced egg shell permeability affects embryonic development and hatchling traits in Lycodon rufozonatum and Pelodiscus sinensis","volume":"13","author":"Tang","year":"2018","journal-title":"Integr. Zool."},{"key":"ref_11","first-page":"330","article-title":"The reproductive biology and embryology of the crocodilians","volume":"12","author":"Ferguson","year":"1981","journal-title":"Biol. Reptilia"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"159","DOI":"10.3382\/ps.0240159","article-title":"Carbonic anhydrase in the calcification of the egg shell","volume":"24","author":"Gutowska","year":"1945","journal-title":"Poultry Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1139\/z91-049","article-title":"Structure of shells from eggs of the Australian lizard Amphibolurus barbatus","volume":"69","author":"Packard","year":"1991","journal-title":"Can. J. Zool."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1086\/652425","article-title":"The role of python eggshell permeability dynamics in a respiration-hydration trade-off","volume":"83","author":"Stahlschmidt","year":"2010","journal-title":"Physiol. Biochem. Zool."},{"key":"ref_15","unstructured":"Andrews, R. (2004). Reptilian Incubation: Environment, Evolution and Behaviour, Biologist."},{"key":"ref_16","unstructured":"Vleck, C.M., and Hoyt, D.F. (1991). Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles, Cambridge University Press."},{"key":"ref_17","unstructured":"Thompson, M.B. (1985). Biology of Australasian Frogs and Reptiles, Royal Zoological Society of New South Wales."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1242\/jeb.01355","article-title":"Cardiovascular development in embryos of the American alligator (Alligator mississippiensis): Effects of chronic and acute hypoxia","volume":"208","author":"Crossley","year":"2005","journal-title":"J. Exp. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1203\/00006450-199709000-00008","article-title":"Changes in mean chorioallantoic artery blood flow and heart rate produced by hypoxia in the developing chick embryo","volume":"42","author":"Mulder","year":"1997","journal-title":"Pediatr. Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/0034-5687(93)90033-7","article-title":"Physiological effects of hypoxia on metabolism and growth of turtle embryos","volume":"92","author":"Kam","year":"1993","journal-title":"Respir. Physiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.resp.2011.04.003","article-title":"Physiological responses to acute changes in temperature and oxygenation in bird and reptile embryos","volume":"178","author":"Nechaeva","year":"2011","journal-title":"Respir. Physiol. Neurobiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1744","DOI":"10.1139\/z83-225","article-title":"Selenium, vitamin E, and trace elements in the plasma of wild and farm-reared alligators during the reproductive cycle","volume":"61","author":"Lance","year":"1983","journal-title":"Can. J. Zool."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"3403","DOI":"10.1111\/are.14675","article-title":"Calcium and phosphorus in unbanded eggs of the Nile crocodile (Crocodylus niloticus)","volume":"51","author":"Brown","year":"2020","journal-title":"Aquac. Res."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Huchzermeyer, F.W. (2003). Crocodiles: Biology, Husbandry and Diseases, CABI.","DOI":"10.1079\/9780851996561.0000"},{"key":"ref_25","unstructured":"Lane, T.J., and Ruppert, K.C. (1981). Alligator Farming Production Review, Institute of Food and Agricultural Sciences, Universtiy of Florida, Florida Cooperative Extension Service."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1242\/jeb.147.1.203","article-title":"Control of metabolism and growth in embryonic turtles: A test of the urea hypothesis","volume":"147","author":"Packard","year":"1989","journal-title":"J. Exp. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"159","DOI":"10.3724\/issn1000-3207-2006-2-159-l","article-title":"Parameter Analysis and Population Growth Prediction of Chinese Alligator Breeding Population in Anhui Province","volume":"30","author":"Wu","year":"2006","journal-title":"Acta Hydrobiol. Sin."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1002\/jmor.1052030105","article-title":"Porosity of eggshells from wild and captive, pen-reared alligators (Alligator mississippiensis)","volume":"203","author":"Wink","year":"1990","journal-title":"J. Morphol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"12A","DOI":"10.1021\/ac00001a711","article-title":"Elemental analysis using icp-oes and icp\/ms","volume":"63","author":"Olesik","year":"1991","journal-title":"Anal. Chem."},{"key":"ref_30","first-page":"13","article-title":"Investigation of correlation between some morphological parameters and hatching quality of turkey eggs","volume":"25","author":"Sharlanov","year":"1988","journal-title":"Zhivotnovudni Nauki"},{"key":"ref_31","first-page":"28","article-title":"Quality of goose eggs and their selection for incubation","volume":"1","author":"Tsarenko","year":"1978","journal-title":"Ptitsevodstvo"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"153","DOI":"10.2307\/1366725","article-title":"The avian egg: Water vapor conductance, shell thickness, and functional pore area","volume":"76","author":"Ar","year":"1974","journal-title":"The Condor"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/j.ecoenv.2013.08.022","article-title":"The eggshell features and clutch viability of the broad-snouted caiman (Caiman latirostris) are associated with the egg burden of organochlorine compounds","volume":"98","author":"Stoker","year":"2013","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"299","DOI":"10.17221\/46\/2015-CJAS","article-title":"Eggshell structure, measurements, and quality-affecting factors in laying hens: A review","volume":"61","author":"Ketta","year":"2016","journal-title":"Czech J. Anim. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1111\/age.12071","article-title":"Enhancing the egg\u2019s natural defence against bacterial penetration by increasing cuticle deposition","volume":"44","author":"Bain","year":"2013","journal-title":"Anim. Genet."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1742-9994-10-23","article-title":"The effect of hydration state and energy balance on innate immunity of a desert reptile","volume":"10","author":"Moeller","year":"2013","journal-title":"Front. Zool."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1016\/j.cbpa.2009.02.041","article-title":"Gas exchange in avian embryos and hatchlings","volume":"153","author":"Mortola","year":"2009","journal-title":"Comp. Biochem. Phys. A"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1086\/515860","article-title":"Gas permeability of American alligator eggs and its anatomical basis","volume":"70","author":"Kern","year":"1997","journal-title":"Physiol. Zool."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1016\/j.cbpa.2007.08.005","article-title":"Oxygen consumption as related to the development of the extraembryonic membranes and cardiovascular system in the European pond turtle (Emys orbicularis) embryogenesis","volume":"148","author":"Nechaeva","year":"2007","journal-title":"Comp. Biochem. Phys. A"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1086\/physzool.69.2.30164194","article-title":"Aspects of calcium regulation in embryonic lepidosaurians and chelonians and a review of calcium regulation in embryonic archosaurians","volume":"69","author":"Packard","year":"1996","journal-title":"Physiol. Zool."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"R1541","DOI":"10.1152\/ajpregu.1989.257.6.R1541","article-title":"Mobilization of calcium, phosphorus, and magnesium by embryonic alligators (Alligator mississippiensis)","volume":"257","author":"Packard","year":"1989","journal-title":"Am. J. Physiol. -Regul. Integr. Comp. Physiol."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/8\/1405\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:19:07Z","timestamp":1760123947000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/8\/1405"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,19]]},"references-count":41,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["ani13081405"],"URL":"https:\/\/doi.org\/10.3390\/ani13081405","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,19]]}}}