The first discovery of non-avian dinosaur egg clutch (Macroolithus yaotunensis, Elongatoolithidae) from the Upper Cretaceous Qiupa Formation of Tantou Basin

doi:10.19615/j.cnki.2096-9899.250212

Abstract

Abstract:

The Upper Cretaceous of Tantou Basin in western Henan has yielded many vertebrate fossils, which are featured by several non-avian dinosaurs. Meanwhile, studies on their eggs were yet inadequate though many eggshells have been reported. The newly discovered material 41HⅤ0199 was excavated from the Upper Cretaceous Qiupa Formation in 2021. The block preserves eight complete eggs arranged in two partial rings that form a partial clutch, and there are some scattered eggshells preserved closely with the block, showing a concave-up to concave-down ratio of 54.5 : 45.5, which indicates that the scattered eggshells come from the clutch and the clutch had been partially broken before it was buried. Based on morphological and microstructural characteristics, the eggs and eggshells can be assigned to Macroolithus yaotunensis (Elongatoolithidae), an oospecies known to be related to oviraptorids, which leads Yulong mini to be its probable producer. Besides, some eggshells show microstructural signs indicating egg retention, which marks the second example of egg retention in the oofamily Elongatoolithidae.

Key words: Tantou Basin, Upper Cretaceous, Qiupa Formation, dinosaur egg, Macroolithus

摘要：

豫西潭头盆地上白垩统中已发现了多种脊椎动物化石，以数种非鸟恐龙类的发现为特点。盆地内也同时报道有大量的蛋壳，然而关于这些蛋壳的研究却还不足。新材料41HⅤ0199于2021年发掘自潭头盆地上白垩统秋扒组。岩石中保存了8枚完整蛋体，组成一不到一半的部分蛋窝，此外还保存有若干分散于围岩中的破碎蛋壳，其凹面向上与凹面向下者的比例为54.5∶45.5, 指示这些蛋壳可能直接来源于该蛋窝，且蛋窝在埋藏前发生了部分破碎。基于宏观形态与显微结构的特征，这些蛋和蛋壳可被归入长形蛋科的瑶屯巨形蛋(Macroolithus yaotunensis)。该蛋种已知与窃蛋龙类直接相关，而盆地内发现的迷你豫龙(Yulong mini) 可能是该蛋窝的产蛋者。此外，在个别蛋壳中还发现了指示蛋体滞留的显微结构，这是此类病态结构在长形蛋科中的第二例发现。

关键词: 潭头盆地, 上白垩统, 秋扒组, 恐龙蛋, 巨形蛋属

CLC Number:

Q915.21

ZHU Xu-Feng, CHANG Fei, LI Yu, ZHANG Xu-Huang, GAO Dian-Song, WANG Qiang, QIU Rui, WANG Xiao-Lin, LIU Di, JIA Song-Hai, JIA Guang-Hui, ZHANG Jian-Hua, XU Li. The first discovery of non-avian dinosaur egg clutch (Macroolithus yaotunensis, Elongatoolithidae) from the Upper Cretaceous Qiupa Formation of Tantou Basin. Vertebrata Palasiatica, 2025, 63(2): 159-172.

朱旭峰, 常飞, 李雨, 张旭晃, 高殿松, 王强, 裘锐, 汪筱林, 刘迪, 贾松海, 贾广辉, 张建华, 徐莉. 2025, 63(2): 159-172, 潭头盆地上白垩统秋扒组首次发现非鸟恐龙蛋窝(瑶屯巨形蛋，长形蛋科). 古脊椎动物学报.

Figures/Tables 6

Fig. 1 Geological map of the west part of Tantou Basin (modified from Wei et al., 2021) 1. Xionger Group; 2. Qiupa Formation; 3. Gaoyugou Formation; 4. Dazhang Formation;5. Tantou Formation; 6. Geological boundary; 7. Normal fault and its dip angle;8. Excavation site of 41HⅤ0199; 9. Settlement; 10. River system

Fig. 2 41HⅤ0199, a clutch of new Macroolithus yaotunensis material from Miaogou, Qiupa Town A. block containing the clutch, prepared from the bottom; B. sketch of A, showing eight remaining eggs (Ring 1: No. 1 to 4; Ring 2: No. 5 to 8) and 22 scattered in-situ eggshells, plus an unidentified bone fragment Note that those concave-up eggshells now have their outer surface towards our view;C. close view of egg No.1, showing nodular surface resembles dispersituberculate ornamentation;D. photo of the original block containing the clutch (center) during the field excavation

Fig. 3 Scattered eggshells around the clutch showing variation of ornamentation and microstructure from Miaogou, Qiupa Town A. dispersituberculate; B. ramotuberculate; C. linearituberculate, ridge shaped; D. linearituberculate, chain shaped

Fig. 4 Microstructure of 41HⅤ0199 from Miaogou, Qiupa Town A-C. an eggshell from the equatorial region of egg No. 6 (Fig. 2B): A. radial view, showing undulating outer surface and a straight pore canal (black arrow); B. enlargement near the inner surface, polarized light, showing undulating and abrupt boundary between the mammillary layer (ML) and continuous layer (CL) The wedge shaped mammillae are closely arranged and the continuous layer shows irregular extinction;C. tangential view of the continuous layer, showing round to oval pore canals (white arrows) D, E. a scattered eggshell with abnormal structure: D. radial view of the eggshell, showing a black line (white arrow) near the outer surface; E. polarized light view of D,showing distinct change of extinction pattern after passing the dark line

Table 1 Comparison between 41HⅤ0199 and Macroolithus oospecies

Ootaxon/ Specimen	Length×equatorial diameter (cm)	Whole thickness (mm)	Mammillary layer thickness	Boundary between structure layers	Reference
M. rugustus	(16.5-18.1)× (7.5-8.5)	1.44-1.70	0.41	abrupt and flat	Zhao, 1975
M. yaotunensis	(17.6-20.8)× (6.7-9.4)	1.39-1.93	0.29-0.51	abrupt and undulating	Zhao, 1975
M. mutabilis	NA	1.3-2.0 (up to 2.3 with ornamentation)	NA	NA	Mikhailov, 1994
41HⅤ0199	(17.0-18.5)× (8.0-8.5)	0.84-1.54 (0.95-1.85 with ornamentation)	0.12-0.57	abrupt and undulating	This work

Table 2 Clutch comparison between 41HⅤ0199 and other Macroolithus clutches

Ootaxon	Specimen No.	Diameter (cm)*	Number of rings	Clutch size	References
M. rugustus	IVPP V 2788	53.4	3	18 (6+10+2)	Zhao, 1975
M. oosp.	41HⅤ0074 (HNM)	69.5	2-3	30 (12+16+2)	Yang et al., 2019
M. oosp.	DM-2014-P0154	~65.6	4	31 (8+13+?+?)	Yang et al., 2019
M. oosp.	PFMM-0014002972	65.4	3	32 (10+16+6)	Yang et al., 2019
M. oosp.	PFMM-0014004392	73.5	3	32 (10+18+4)	Yang et al., 2019
M. oosp.	PFMM-0014003019	68.7	3	35 (10+18+7)	Yang et al., 2019
M. yaotunensis	IVPP V 2784	71	2	20 (8+12)	Zhao, 1975
M. yaotunensis	LDNHMF2008	87.55	3	24 (3+9+12) incomplete	Bi et al., 2021; Hogan, 2024
M. yaotunensis	41HⅤ0199 (HNM)	45	2	8 preserved,26 (10+16) predicted	This work

References 45

[1]	Amo Sanjuán O, Canudo J I, Cuenca-Bescós G, 2000. First record of elongatoolithid eggshells from the Lower Barremian (Lower Cretaceous) of Europe (Cuesta Corrales 2, Galve Basin, Spain). In: Bravo A M, Reyes T eds. First International Symposium on Dinosaur Eggs and Babies Extended Abstracts. Isona i Conca Dellà. 7-14
[2]	Bi S D, Amiot R, Peyre de Fabrègues C et al., 2021. An oviraptorid preserved atop an embryo-bearing egg clutch sheds light on the reproductive biology of non-avialan theropod dinosaurs. Sci Bull, 66: 947-954 DOI PMID
[3]	Cheng Y N, Ji Q, Wu X C et al., 2008. Oviraptorosaurian eggs (Dinosauria) with embryonic skeletons discovered for the first time in China. Acta Geol Sin - Engl, 82: 1089-1094
[4]	Clark J M, Norell M A, Chiappe L M, 1999. An oviraptorid skeleton from the Late Cretaceous of Ukhaa Tolgod, Mongolia, preserved in an avianlike brooding position over an oviraptorid nest. Am Mus Novit, 3265: 1-36
[5]	Dong Z M, 1979. Dinosaur fossils from the Cretaceous of southern China. In: Institute of Vertebrate Paleontolgy and Paleoanthropology, Nanjing Institute of Geology and Paleontolgy eds. Mesozoic and Cenozoic Red Beds in Southern China. Beijing: Science Press. 342-350
[6]	Dong Z M, Currie P J, 1996. On the discovery of an oviraptorid skeleton on a nest of eggs at Bayan Mandahu, Inner Mongolia, People’s Republic of China. Can J Earth Sci, 33: 631-636
[7]	Ewert M A, Firth S J, Nelson C E, 1984. Normal and multiple eggshells in batagurine turtles and their implications for dinosaurs and other reptiles. Can J Zool, 62: 1834-1841
[8]	Grellet-Tinner G, Corsetti F, Buscalioni A D, 2010. The importance of microscopic examinations of eggshells: discrimination of bioalteration and diagenetic overprints from biological features. J Iber Geol, 36: 181-192
[9]	Hayward J L, Zelenitsky D K, Smith D L et al., 2000. Eggshell taphonomy at modern gull colonies and a dinosaur clutch site. Palaios, 15: 343-355
[10]	Henan Provincial Bureau of Geology and Mineral Resources, 1989. Regional Geology of Henan Province. Beijing: Geological Press. 1-722
[11]	Hogan J D, 2024. The egg-thief architect: experimental oviraptorosaur nesting physiology, the possibility of adult-mediated incubation, and the feasibility of indirect contact incubation. Paleobiology, 50: 108-122
[12]	Holtz T R, 2004. Tyrannosauroidea. In: Weishampel D B, Osmólska H, Dodson P eds. Dinosauria II. Berekley: Unversity of California. 111-136
[13]	Imai T, Varricchio D J, Cahoon J et al., 2015. Sedimentological analyses of eggshell transport and deposition: implication and application to eggshell taphonomy. Palaios, 30: 435-445
[14]	Jackson F D, Varricchio D J, 2003. Abnormal, multilayered eggshell in birds: implications for dinosaur reproductive anatomy. J Vert Paleont, 23: 699-702
[15]	Jackson F D, Schmitt J G, 2008. Recognition of vertebrate egg abnormalities in the Upper Cretaceous fossil record. Cretac Res, 29: 27-39
[16]	Jackson F D, Garrido A, Schmitt J G et al., 2004. Abnormal, multilayered titanosaur (Dinosauria: Sauropoda) eggs from in situ clutches at the Auca Mahuevo locality, Neuquén Province, Argentina. J Vert Paleont, 24: 913-922
[17]	Jensen J A, 1970. Fossil eggs in the Lower Cretaceous of Uath. Brigh Young Univ Geol Stud, 17: 51-65
[18]	Jia S H, Lü J C, Xu L et al., 2010. Discovery and significance of ankylosaur specimens from the Late Cretaceous Qiupa Formation in Luanchuan, Henan, China. Geol Bull China, 29: 483-487
[19]	Jin X S, Varricchio D J, Poust A W et al., 2020. An oviraptorosaur adult-egg association from the Cretaceous of Jiangxi Province, China. J Vert Paleont, 39: e1739060
[20]	Liang X Q, Wen S N, Yang D S et al., 2009. Dinosaur eggs and dinosaur egg-bearing deposits (Upper Cretaceous) of Henan Province, China: occurrences, palaeoenvironments, taphonomy and preservation. Prog Nat Sci, 19: 1587-1601
[21]	Lü J C, Xu L, Zhang X et al., 2007. New dromaeosaurid dinosaur from the Late Cretaceous Qiupa Formation of Luanchuan area, western Henan, China. Geol Bull China, 26: 777-786
[22]	Lü J C, Currie P J, Xu L et al., 2013. Chicken-sized oviraptorid dinosaurs from central China and their ontogenetic implications. Naturwissenschaften, 100: 165-175 DOI PMID
[23]	Lü J C, Xu L, Chang H L et al., 2018. A new alvarezsaurid dinosaur from the Late Cretaceous Qiupa Formation of Luanchuan, Henan Province, central China. China Geol, 1: 28-35
[24]	Mao Z F, Zhou H R, Li S J et al., 2012. Palaeoclimates in the Tantou Basin, Luanchuan, western Henan during the Cretaceous-Palaeogene. Sedi Geol & Teth Geol, 33: 18-24
[25]	Mikhailov K E, 1994. Theropod and protoceratopsian dinosaur eggs from the Cretaceous of Mongolia and Kazakhstan. Paleontol J, 28: 101-120
[26]	Mikhailov K E, 1997. Fossil and recent eggshell in amniotic vertebrates: fine structure, comparative morphology and classification. Spec Pap Palaeontol, 56: 1-80
[27]	Mohabey D M, 1998. Systematics of Indian Upper Cretaceous dinosaur and chelonian eggshells. J Vert Paleont, 18: 348-362
[28]	Moreno-Azanza M, Canudo J I, Gasca J M, 2014. Spheroolithid eggshells in the Lower Cretaceous of Europe: implications for eggshell evolution in ornithischian dinosaurs. Cretac Res, 51: 75-87
[29]	Norell M A, Clark J M, Demberelyin D et al., 1994. A theropod dinosaur embryo and the affinities of the flaming cliffs dinosaur eggs. Science, 266: 779-782 PMID
[30]	Sato T, Cheng Y N, Wu X C et al., 2005. A pair of shelled eggs inside a female dinosaur. Science, 308: 375-375 PMID
[31]	Simon D J, Varricchio D J, Jin X S et al., 2019. Microstructural overlap of Macroelongatoolithus eggs from Asia and North America expands the occurrence of colossal oviraptorosaurs. J Vert Paleont, 38: e1553046
[32]	Tanaka K, Lü J C, Kobayashi Y et al., 2011. Description and phylogenetic position of dinosaur eggshells from the Luanchuan area of western Henan Province, China. Acta Geol Sin - Engl, 85: 66-74
[33]	Wang Q, Zhao Z K, Wang X L et al., 2013. A new form of Elongatoolithidae, Undulatoolithus pengi oogen. et oosp. nov. from Pingxiang, Jiangxi, China. Zootaxa, 3746: 194-200
[34]	Wang S, Zhang S K, Sullivan C et al., 2016. Elongatoolithid eggs containing oviraptorid (Theropoda, Oviraptorosauria) embryos from the Upper Cretaceous of Southern China. BMC Evol Biol, 16: 67 DOI PMID
[35]	Wei X F, Kundrát M, Xu L et al., 2022. A new subadult specimen of oviraptorid Yulong mini (Theropoda: Oviraptorosauria) from the Upper Cretaceous Qiupa Formation of Luanchuan, central China. Cretac Res, 138: 105261
[36]	Wei X F, Xia M L, Xu L et al., 2021. Advances of the studies on Late Cretaceous vertebrate fauna from Luanchuan in Henan Province. Geol Bull China, 40: 1178-1188
[37]	Weishampel D B, Fastovsky D E, Watabe M et al., 2008. New oviraptorid embryos from Bugin-Tsav, Nemegt Formation (Upper Cretaceous), Mongolia, with insights into their habitat and growth. J Vert Paleont, 28: 1110-1119
[38]	Xu L, Buffetaut E, O’Connor J K et al., 2021. A new, remarkably preserved, enantiornithine bird from the Upper Cretaceous Qiupa Formation of Henan (central China) and convergent evolution between enantiornithines and modern birds. Geol Mag, 158: 2087-2094
[39]	Xu L, Kobayashi Y, Lü J C et al., 2011. A new ornithomimid dinosaur with North American affinities from the Late Cretaceous Qiupa Formation in Henan Province of China. Cretac Res, 32: 213-222
[40]	Yang T R, Wiemann J, Xu L et al., 2019. Reconstruction of oviraptorid clutches illuminates their unique nesting biology. Acta Palaeontol Pol, 64: 581-596
[41]	Zelenitsky D K, Hills L V, 1997. Normal and pathological eggshells of Spheroolithus albertensis, oosp. nov., from the Oldman Formation (Judith River Group, Late Campanian), southern Alberta. J Vert Paleont, 17: 167-171
[42]	Zhao Z K, 1975. The microstructure of fossil dinosaur eggs from Nanxiong County, Guangdong Province: concurrent with a discussion on the problem of the classification of dinosaur eggs. Vert PalAsiat, 13: 105-117
[43]	Zhao Z K, Wang Q, Zhang S K, 2015. Dinosaur Eggs. Beijing: Science Press. 1-163
[44]	Zhou S Q, Feng Z J, 2002. Studies on the occurrence beds of oölithus and their relations to the upper-lower boundaries in Henan Province. Res Surv Environ, 23: 68-76
[45]	Zhu X F, Wang Q, Wang X L, 2024. Electron backscatter diffraction (EBSD) study of elongatoolithid eggs from China with microstructural and parataxonomic implications. Paleobiology, 50: 330-345