Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-24T16:33:37.869Z Has data issue: false hasContentIssue false
  • English
  • Français

Exceptional preservation of clam shrimp (Branchiopoda, Eucrustacea) eggs from the Early Cretaceous Jehol Biota and implications for paleoecology and taphonomy

Published online by Cambridge University Press:  11 September 2015

Yanhong Pan ,
Yaqiong Wang ,
Jingeng Sha  and
Huanyu Liao
Yanhong Pan
Affiliation:
Key Laboratory of Economic Stratigraphy and Palaeogeography, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, East Beijing Road 39, Nanjing 210008, China
Yaqiong Wang
Affiliation:
Key Laboratory of Economic Stratigraphy and Palaeogeography, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, East Beijing Road 39, Nanjing 210008, China
Jingeng Sha
Affiliation:
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, East Beijing Road 39, Nanjing 21008, China 〈yhpan@nigpas.ac.cn〉, 〈yqwang@nigpas.ac.cn〉, 〈jgsha@nigpas.ac.cn〉, 〈hyliao@nigpas.ac.cn〉
Huanyu Liao
Affiliation:
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, East Beijing Road 39, Nanjing 21008, China 〈yhpan@nigpas.ac.cn〉, 〈yqwang@nigpas.ac.cn〉, 〈jgsha@nigpas.ac.cn〉, 〈hyliao@nigpas.ac.cn〉
Get access Rights & Permissions [Opens in a new window]

Abstract

Fossil eggs of clam shrimps (Spinicaudata) are rare and little attention has been paid to the study of their shape and microstructures. Here, we report the discovery of exceptionally preserved three-dimensional eggs from numerous specimens of Eosestheria elliptica Chen, 1976 from the lacustrine Early Cretaceous Yixian Formation in western Liaoning, China. These three-dimensionally preserved fossil eggs display a spherical shape with smooth surface, part of the tertiary envelope, and possibly the first embryonic cuticle, which were previously unknown or ambiguous. The eggs are abundant and assumed to be attached to the exopod as in extant Spinicaudata. Moreover, the exceptional three-dimensional preservation and delicate preparation of slices of the eggs allowed us to document the microstructures and elemental composition of fossil eggs of clam shrimps from the Jehol Biota. Energy dispersive spectroscopy of the fossilized envelope revealed a calcium phosphate composition. However, the egg contents display two completely different elemental compositions. Some exhibit the same elemental composition as the envelope, whereas others has been replaced by alumino-silicate. The taphonomic process is also briefly discussed in this paper.

Type
Articles
Information
Journal of Paleontology , Volume 89 , Issue 3 , May 2015 , pp. 369 - 376
Copyright
Copyright © 2015, The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Babcock, L.E., Isbell, J.L., Miller, M.F., and Hasiotis, S.T., 2002, New late Paleozoic conchostracan (Crustacea, p. Branchiopoda) from the Shackleton Glacier area, Antarctica, p. age and paleoenvironmental implications: Journal of Paleontology, v. 76, p. 70–75.2.0.CO;2>CrossRefGoogle Scholar
Belk, D., 1987, Embryonic cuticles of Artemia during diapause and hatching, p. insights from comparison with other brachiopoda: Journal of Crustacean Biology, v. 7, p. 691–696.CrossRefGoogle Scholar
Belk, D., 1989, Identification of species in the conchostracan genus Eulimnadia by egg shell morphology: Journal of Crustacean Biology, v. 9, p. 115–125.CrossRefGoogle Scholar
Bill, P.C., 1913, Über crustaceen aus dem voltziensandstein des elsasses: Mitteilungen der Geologischen Landesanstalt von Elsass-Lothringen, v. 8, p. 289–338.Google Scholar
Briggs, D.E.G., 2003, The role of decay and mineralization in the preservation of soft-bodied fossils: Annual Reviews of Earth Planetary Science, v. 31, p. 275–301.CrossRefGoogle Scholar
Browe, W.E., Price, A.L., Gerberding, M., and Patel, N.H., 2005, Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis: Genesis, v. 42, p. 124–149.CrossRefGoogle Scholar
Bruner, E., Costantini, D., and Mura, G., 2013, Fractal analysis of the egg shell ornamentation in anostracans cysts: a quantitative approach to the morphological variations in Chirocephalus ruffoi: Hydrobiologia, v. 705, p. 1–8.CrossRefGoogle Scholar
Chernyshev, B.I., 1940, Mesozoic branchiopoda from Turkestan and Transbaikal: Akademiya Nauk Ukrainskoj SSR, Geologicheskij Zhurnal, v. 7, p. 5–43. (in Russian)Google Scholar
Clegg, J.S., 2005, Desiccation tolerance in encysted embryos of the animal extremophile, Artemia: Integrative and Comparative Biology, v. 45, p. 715–724.CrossRefGoogle ScholarPubMed
De Walsche, D., Munuswamy, N., and Dumont, H.J., 1991, Structural differences between the cyst walls of Streptocephalus dichotomus (Baird), S. torvicornis (Waga), and Thamnocephalus platyurus (Packard) (Crustacea: Anostraca), and a comparison with other genera and species: Hydrobiologia, v. 212, p. 195–202.CrossRefGoogle Scholar
Dechaseaux, C., 1951, Contribution a la connaissance des esthéries fossils: Annales de Paléontologie, v. 37, p. 125–132.Google Scholar
Dudich, E., 1931, Systematische und biologische untersuchungen über die kalkeinlagerungen des crustaceenpanzers in polarisiertem lichte: Zoologica, v. 80, p. 1–154.Google Scholar
Dumont, H.J., and Negrea, S.V., 2002. Branchiopoda: Leiden, Backhuys Publishers, 398 p.Google Scholar
Feys, R., 1985, A propos du limbe des Estheries: Estheria cebennensis G. E.: Bulletin trimestriel de la Société d’Histoire Naturelle et des Amis du Museum d’Autun, v. 115, p. 61–65.Google Scholar
Fürsich, F.T., Sha, J.G., Jiang, B.Y., and Pan, Y.H., 2007, High resolution palaeoecological and taphonomic analysis of Early Cretaceous lake biota, western Liaoning (NE-China): Palaeogeography, Palaeoclimatology, Palaeoecology, v. 253, p. 434–457.CrossRefGoogle Scholar
Gall, J.C., 1971, Faunes et paysages du Grès à Voltzia du nord des Vosges, Essai paléoécologique sur le Buntsandstein supérieur: Mémoire du Service de la Carte Géologique d’Alsace et de Lorraine, v. 34, p. 1–318.Google Scholar
Gilchrist, B.M., 1978, Scanning electron microscope studies of the egg shell in some Anostraca (Crustacea: Branchiopoda): Cell and Tissue Research, v. 193, p. 337–351.CrossRefGoogle ScholarPubMed
Grauvogel, L., 1947, Sur quelques types de pontes du Grès à Voltzia (Trias inférieur des Vosges): Compte Rendus Hebdomadaires des Seances de l’Academie des Sciences, v. 225, p. 1165–1167.Google Scholar
Hathaway, S.A., Sheehan, D.P., and Simovich, M.A., 1996, Vulnerability of branchiopod cysts to crushing: Journal of Crustacean Biology, v. 16, p. 448–452.CrossRefGoogle Scholar
Hethke, M., Fürsich, F.T., Jiang, B.Y., and Pan, Y.H., 2013, Seasonal to sub-seasonal palaeoenvironmental changes in Lake Sihetun (Lower Cretaceous Yixian Formation, NE China): International Journal of Earth Science, v. 102, p. 351–378.CrossRefGoogle Scholar
Hill, R.E., and Shepard, W.D., 1997, Observations on the identification of California anostracan cysts: Hydrobiologia, v. 359, p. 113–123.CrossRefGoogle Scholar
Jones, T.R., 1862. A monograph of the fossil Estheriae: London, Palaeontographical Society, London, 132 p.CrossRefGoogle Scholar
Lee, K.W., Gouthro, M.A., Belk, D., and Rosowski, J.R., 1994, Ultrastructure features of the tertiary envelope in the cyst of the brine shrimp Artemia franciscana (Anostraca), in Bailey, G.W., and Garratt-Reed, A.J., eds., Proceedings of the 52nd Annual Meeting of the Microscopy Society of America: San Francisco, San Francisco Press, p. 362–363.Google Scholar
Liu, Y.L., Zhao, Y., and Dai, Z.M., 2009, Formation of diapause cyst shell in brine shrimp, Artemia parthenogenetica, and its resistance role in environmental stresses: The Journal of Biological Chemistry, v. 284, p. 16931–16938.CrossRefGoogle ScholarPubMed
Martens, T., 1983, Zur Taxonomie und Biostratigraphie der Conchostraca (Phyllopoda, Crustacea) des Jungpaläozoikums der DDR, Teil 1: Freiberger Forschungshefte C, v. 382, p. 7–105.Google Scholar
Martin, J.W., 1989, Eulimnadia belki, a new clam shrimp from Cozumel, Mexico (Conchostraca, p. Limnadiidae), with a review of central and south American species of the genus Eulimnadia: Journal of Crustacean Biology, v. 9, p. 104–114.CrossRefGoogle Scholar
Martin, D., Briggs, D.E.G., and Parkes, R.J., 2003, Experimental mineralization of invertebrate eggs and the preservation of Neoproterozoic embryos: Geology, v. 31, p. 39–42.2.0.CO;2>CrossRefGoogle Scholar
Morris, J.E., and Afzelius, B.A., 1967, The structure of the shell and outer membranes in encysted Artemia salina Embryos during cryptobiosis and development: Journal of Ultrastructure Research, v. 20, p. 244–259.CrossRefGoogle Scholar
Munuswamy, N., and Subramoniam, T., 1984, Egg envelopes of Streptocephalus dichotomus Baird: a structural and histochemical study: Hydrobiologia, v. 114, p. 17–28.CrossRefGoogle Scholar
Mura, G., 1991, SEM morphology of resting eggs in the species of the genus Branchinecta from North America: Journal of Crustacean Biology, v. 11, p. 432–436.CrossRefGoogle Scholar
Mura, G., and Rossetti, G., 2010, Intraspecific morphological diversity of anostracan resting eggs: Chirocephalus ruffoi Cottarelli & Mura, 1984 as a study case: Journal of Biological Research-Thessaloniki, v. 14, p. 137–150.Google Scholar
Olesen, J., 1998, A phylogenetic analysis of the Conchostraca and Cladocera (Crustacea, Branchiopoda, Diplostraca): Zoological Journal of the Linnean Society, v. 122, p. 491–536.CrossRefGoogle Scholar
Orr, P.J., Briggs, D.E.G., and Kearns, S.L., 2008, Taphonomy of exceptionally preserved crustaceans from the Upper Carboniferous of Southeastern Ireland: Palaios, v. 23, p. 298–312.CrossRefGoogle Scholar
Pan, Y.H., Sha, J.G., Fürsich, F.T., Wang, Y.Q., Zhang, X.L., and Yao, X.G., 2012, Dynamics of the lacustrine fauna from the Early Cretaceous Yixian Formation, China: implications of volcanic and climatic factors: Lethaia, v. 45, p. 299–314.CrossRefGoogle Scholar
Pruvost, P., 1919. Introduction à l’étude du terrain du Nord et du Pas-de-Calais: Paris, Mémoires pour server à l’explication de la carte géologique détaillée de la France, 584 p.Google Scholar
Rabet, N., 2010, Revision of the egg morphology of Eulimnadia (Crustacea, Branchiopoda, Spinicaudata): Zoosystema, v. 32, p. 373–391.CrossRefGoogle Scholar
Rieder, N., Abaffy, P., Hauf, A., Lindel, M., and Weishäupl, H., 1984, Funktionsmorphologische Untersuchungen an den Conchostracen Leptestheria dahalacensis und Limnadia lenticularis (Crustacea, Phyllopoda, Conchostraca): Zoologische Beiträge, v. 28, p. 417–444.Google Scholar
Rosowski, J.R., Belk, D., Gouthro, M.A., and Lee, K.W., 1997, Ultrastructure of the cyst shell and underlying membranes of the brine shrimp Artemia franciscana Kellogg (Anostraca) during postencystic development, emergence, and hatching: Journal of Shellfish Research, v. 16, p. 233–249.Google Scholar
Shen, Y.B., Chen, P.J., and Huang, D.Y., 2003, Age of the fossil clam shrimps from Daohugou of Ningcheng, Inner Mongolia: Journal of Stratigraphy, v. 27, p. 310–313. (in Chinese)Google Scholar
Shen, Y.B., and Huang, D.Y., 2008, Extant clam shrimp egg morphology: taxonomy and comparison with other fossil branchiopod eggs: Journal of Crustacean Biology, v. 28, p. 352–360.Google Scholar
Shen, 2011, Soft body preservation in the conchostracan Eosestheria lingyuanensis Chen from the Jehol Biota and its taxonomic significance: Acta Palaeontologica Sinica, v. 50, p. 275–283. (in Chinese)Google Scholar
Spotte, S., and Anderson, G., 1988, Chemical decapsulation of resting cysts of the Anostracans Artemia franciscana and Streptocephalus seali as revealed by scanning electron microscopy: Journal of Crustacean Biology, v. 8, p. 221–231.CrossRefGoogle Scholar
Stigall, A.L., Babcock, L.E., Briggs, D.E.G., and Leslie, S.A., 2008, Taphonomy of lacustrine interbeds in the Kirkpatrick Basalt (Jurassic), Antarctica: Palaios, v. 23, p. 344–355.CrossRefGoogle Scholar
Tasch, P., 1969, Branchiopoda, in Moore, R.C., ed., Treatise on invertebrate paleontology, part R, Arthropoda 4, Crustacea (except Oxtracoda): Boulder, Colorado, Geological Society of America and the University of Kansas, p. 128–191.Google Scholar
Tasch, P., 1984, Central Transantarctic Mountains nonmarine deposits: American Geophysical Union, Antarctic Research Series, v. 36, p. 75–96.Google Scholar
Tasch, P., 1987, Fossil Conchostraca of the Southern Hemisphere and continental drift: Geological Society of America Memoir, v. 165, p. 1–290.Google Scholar
Thiéry, A., and Gasc, C., 1991, Resting eggs of Anostraca, Notostraca and Spinicaudata (Crustacea, Branchiopoda) occurring in France: identification and taxonomical value: Hydrobiologia, v. 212, p. 245–259.CrossRefGoogle Scholar
Tintori, A., 1990, Estherids from the Kalkschiefer zone (Triassic) of Lombardy (N. Italy), in Robba, E., ed., Atti del Quarto Simposio di Ecologia e Paleoecologia della Comunita Bentoniche: Torino, Museo Regionale di Scienze Naturali, p. 95–105.Google Scholar
Tommasini, S., and Sabelli, F.S., 1989, Eggshell origin and structure in two species of conchostraca (Crustacea, Phyllopoda): Zoomorphology, v. 109, p. 33–37.Google Scholar
Trusova, E.K., 1974, The traces of life of Phyllopod Crustaceans: Palaeontologicheskiy Sbornik, v. 10, p. 83–87. (in Russian)Google Scholar
Vannier, J., Thiéry, A., and Racheboeuf, P.R., 2003, Spinicaudatans and ostracods (Crustacea) from the Montceau Lagestätte (Late Carboniferous, France): morphology and palaeonenvironmental significance: Palaeontology, v. 46, p. 999–1030.CrossRefGoogle Scholar
Zarattini, P., Mura, G., and Ketmaier, V., 2013, Intra-specific variability in the thirteen known populations of the fairy shrimp Chirocephalus ruffoi (Crustacea: Anostraca): resting egg morphometrics and mitochondrial DNA reveal decoupled patterns of deep divergence: Hydrobiologia, v. 713, p. 19–34.CrossRefGoogle Scholar
Zhang, W.T., Shen, Y.B., and Niu, S.W., 1987, Discovery of Jurassic conchostracans with well-preserved soft parts and notes on its biological significance: Acta Palaeontologica Sinica, v. 26, p. 111–129. (in Chinese)Google Scholar
Zhang, W.T., Shen, Y.B., and Niu, S.W., 1990, Discovery of Jurassic clam shrimps with well-preserved soft parts and notes on its biological significance: Palaeontologia Cathayana, v. 5, p. 311–352.CrossRefGoogle Scholar
Zhang, W.T., Chen, P.J., and Shen, Y.B., 1976. Fossil Conchostraca of China: Beijing, Science Press, 325 p. (in Chinese)Google Scholar