Fern Diversity in the Mid-Cretaceous Amber Forests Revealed by Exceptionally Preserved Sporangium Types — Oak Academic Publishing
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Fern Diversity in the Mid-Cretaceous Amber Forests Revealed by Exceptionally Preserved Sporangium Types
Department of Cenozoic Biological Evolution and Environment, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China
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Xiangxi Tujia and Miao Autonomous Prefecture Forest Resources Monitoring Center, Jishou, China
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Department of Cenozoic Biological Evolution and Environment, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China
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School of Resources and Earth Sciences, China University of Mining and Technology, Xuzhou, China
1 Department of Cenozoic Biological Evolution and Environment, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China
2 Xiangxi Tujia and Miao Autonomous Prefecture Forest Resources Monitoring Center, Jishou, China
3 Department of Cenozoic Biological Evolution and Environment, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China
4 School of Resources and Earth Sciences, China University of Mining and Technology, Xuzhou, China
The amber deposits from the Albian-Cenomanian in Myanmar have emerged as a pivotal source for exceptionally abundant fossil insect fauna since their initial discovery. Recent studies have increasingly focused on elucidating the fern inventory and examining newly available fossils from Myanmar amber, suggesting a diverse fern flora that once thrived in Cretaceous forests. Through investigations of amber collections, with particular emphasis on sporangium structures—especially the annulus types preserved in amber inclusions—this study revealed additional novelties within the Cyatheales and Schizaeales in mid-Cretaceous Myanmar amber forests. The described specimens and newly discovered fossils provide compelling evidence that Polypodiales were not only diverse and abundant but also that other fern lineages, such as Cyatheales and Schizaeales, coexisted in these ancient forest ecosystems. This study reveals the high diversity of ferns in the mid-Cretaceous Myanmar area, while also implying the paleoecological and paleogeographical significance of the Mesozoic Burmese amber forests.
Smith, A.R., Pryer, K.M., Schuettpelz, E., Korall, P. and Schneider, H. (2006) A Classification for Extant Ferns. Taxon , 55, 705-731. https://doi.org/10.2307/25065646
Ppg, I. (2016) A Community-Derived Classification for Extant Lycophytes and Ferns. Journal of Systematics and Evolution , 54, 563-603. https://doi.org/10.1111/jse.12229
Moran, R.C. (2008) Biogeography of Ferns and Lycophytes. In: Haufler, C. and Ranker, T.A., Eds., The Biology and Evolution of Ferns and Lycophytes , Cambridge University Press, Cambridge, 367-394. https://doi.org/10.1017/CBO9780511541827.015
Grimaldi, D.A. (2022) Evolutionary History of Interactions among Terrestrial Arthropods. Current Opinion in Insect Science , 51, Article ID: 100915. https://doi.org/10.1016/j.cois.2022.100915
Poinar Jr., G.O. (2021) A New Fern, Cladarastega burmanica gen. et sp. Nov. (Dennstaedtiaceae: Polypodiales) in Mid-Cretaceous Burmese Amber. Palaeodive r sity , 14, 153-160. https://doi.org/10.18476/pale.v14.a7
Poinar Jr., G.O. and Buckley, R. (2008) Cretacifilix fungiformis gen. and sp. nov., an Eupolypod Fern (Polypodiales) in Early Cretaceous Burmese Amber. Journal of the Botanical Research Institute of Texas , 2, 1175-1182.
Regalado, L., Schneider, H., Mülle, P. and Schmidt, A.R. (2023) Character Evolution of Modern Eupolypods Supports the Assignment of the Fossil Fern Cretacifilix fu n gifor mis to Dryopteridaceae. Frontiers in Ecology and Evolution , 11, Article 1162577. https://doi.org/10.3389/fevo.2023.1162577
Li, C.X., Moran, R.C., Wang, Y.R., Li, Y. and Ma, J.Y. (2024) A New Fossil of Cy s todium (Cystodiaceae) from the Mid-Cretaceous Myanmar Amber. Cretaceous R e search , 160, Article ID: 105882. https://doi.org/10.1016/j.cretres.2024.105882
Regalado, L., Schmidt, A.R., Appelhans, M., Ilsemann, B., Schneider, H., Krings, M. and Heinrichs, J. (2017) A Fossil Species of the Enigmatic Early Polypod Fern Genus Cystodium (Cystodiaceae) in Cretaceous Amber from Myanmar. Scientific R e ports , 7, Article No. 14615. https://doi.org/10.1038/s41598-017-14985-7
Regalado, L., Schmidt, A.R., Müller, P., Niedermeier, L., Krings, M. and Schneider, H. (2019) Heinrichsia cheilanthoides gen. et sp. nov., a Fossil Fern in the Family Pteridaceae (Polypodiales) from the Cretaceous Amber Forests of Myanmar. Jou r nal of Systematics and Evolution , 57, 329-338. https://doi.org/10.1111/jse.12514
Regalado, L., Schmidt, A.R., Krings, M., Bechteler, J., Schneider, H. and Heinrichs, J. (2018) Fossil Evidence of Eupolypod Ferns in the Mid-Cretaceous of Myanmar. P lant Systematics and Evolution , 304, 1-13. https://doi.org/10.1007/s00606-017-1439-2
Schneider, H., Schmidt, A.R. and Heinrichs, J. (2016) Burmese Amber Fossils Bridge the Gap in the Cretaceous Record of Polypod Ferns. Perspectives in Plant Ecology , Evolution and Systematics , 18, 70-78. https://doi.org/10.1016/j.ppees.2016.01.003
Long, X., Peng, Y., Zhang, H., Fan, Y., Shi, C. and Wang, S. (2023) Microlepia bu r masia sp. nov., a New Fern Species from Mid-Cretaceous Kachin Amber of Northern Myanmar (Dennstaedtiaceae, Polypodiales). Cretaceous Research , 143, Article ID: 105417. https://doi.org/10.1016/j.cretres.2022.105417
Li, C.X., Moran, R.C., Ma, J.Y., Wang, B. and Hao, J.S. (2020) A New Fossil Record of Lindsaeaceae (Polypodiales) from the Mid-Cretaceous Amber of Myanmar. Cr e taceous Research , 105, Article ID: 104040. https://doi.org/10.1016/j.cretres.2018.12.010
Long, X.X., Peng, Y., Feng, Q., Engel, M.S., Shi, C. and Wang, S. (2023) A New Fossil Fern of the Dryopteridaceae (Polypodiales) from the Mid-Cretaceous Kachin Amber. Palaeobiodiversity and Palaeoenvironments , 103, 489-494. https://doi.org/10.1007/s12549-023-00572-4
Regalado, L., Schmidt, A.R., Müller, P., Kobbert, M.J., Schneider, H. and Heinrichs, J. (2017) The First Fossil of Lindsaeaceae (Polypodiales) from the Cretaceous Amber Forest of Myanmar. Cretaceous Research , 72, 8-12. https://doi.org/10.1016/j.cretres.2016.12.003
Li, C.X., Moran, R.C., Ma, J.Y., Wang, B., Hao, J.S. and Yang, Q. (2020) A Mid-Cretaceous Tree Fern of Thyrsopteridaceae (Cyatheales) Preserved in Myanmar Amber. Cretaceous Research , 105, Article ID: 104050. https://doi.org/10.1016/j.cretres.2019.01.002
Zhang, H.R., Shi, C., Long, X.X., Feng, Q., Cai, H.H., Lü, Y.T. and Wang, S. (2022) A New Fossil Record of Thyrsopteridaceae (Cyatheales) from the Mid-Cretaceous Amber of Myanmar. Palaeoworld , 31, 478-484. https://doi.org/10.1016/j.palwor.2021.09.002
Wang, S., Long, X.X., Zhang, H.R., Cai, H.H., Engel, M.S. and Shi, C. (2022) A Semi-Aquatic Fern (Marsileaceae) from the Mid-Cretaceous Amber of Northern Myanmar. Cretaceous Research , 133, Article ID: 105119. https://doi.org/10.1016/j.cretres.2021.105119
Li, Y., Wang, Y.D., Nosova, N., Lu, N. and Xu, Y.Y. (2022) Filmy Ferns (Hymenophyllaceae) and Associated Spike-Mosses (Selaginellaceae) from the Mid-Cretaceous Kachin Amber, Myanmar. Biology , 11, Article 1629. https://doi.org/10.3390/biology11111629
Nayar, B.K., Bajpai, N. and Chandra, S. (1968) Contributions to the Morphology of the Fern Genus Oleandra . Botanical Journal of the Linnean Society , 60, 265-282. https://doi.org/10.1111/j.1095-8339.1968.tb00089.x
Kramer, K.U. and Green, P.S. (1990) Pteridophytes and Gymnosperms. Springer, Berlin.
Kumar, K. (2001) Reproductive Biology of Pteridophytes. In: Ramawat, K.G., Mérillon, J.M. and Shivanna, K.R., Eds., Reproductive Biology of Plants , CRC Press, Boca Raton, 175-214. https://doi.org/10.1007/978-3-642-50133-3_9
Shen, H., Jin, D.M., Shu, J.P., Zhou, X.L., Lei, M., Wei, R., Shang, H., Wei, H.J., Zhang, R., Liu, L., Gu, Y.F., Zhang, X.C. and Yan, Y.H. (2018) Large-Scale Phylogenomic Analysis Resolves a Backbone Phylogeny in Ferns. GigaScience , 7, gix116. https://doi.org/10.1093/gigascience/gix116
Schneider, H., Smith, A.R. and Pryer, K.M. (2009) Is Morphology Really at Odds with Molecules in Estimating Fern Phylogeny? Systematic Botany , 34, 455-475. https://doi.org/10.1600/036364409789271209
Gifford, E.M. and Foster, A.S. (1989) Morphology and Evolution of Vascular Plants. 3rd Edition, Freeman W. H. and Co., New York.
Friis, E.M. and Pedersen, K.R. (1990) Structure of the Lower Cretaceous Fern On y chiopsis psilotoides from Bornholm, Denmark. Review of Palaeobotany and Pal y nology , 66, 47-63. https://doi.org/10.1016/0034-6667(90)90028-H
Grimaldi, D.A., Engel, M.S. and Nascimbene, P. (2002) Fossiliferous Cretaceous Amber from Myanmar (Burma): Its Rediscovery, Biotic Diversity, and Paleontological Significance. American Museum Novitates , 3361, 1-72. https://doi.org/10.1206/0003-0082(2002)361 2.0.CO;2
Cruickshank, R.D. and Ko, K. (2003) Geology of an Amber Locality in the Hukawng Valley, Northern Myanmar. Journal of Asian Earth Sciences , 21, 441-445. https://doi.org/10.1016/S1367-9120(02)00044-5
Shi, G.H., Grimaldi, D.A., Harlow, G.E., Wang, J., Wang, J., Yang, M.C., Lei, W.Y., Li, Q.L. and Li, X.H. (2012) Age Constraint on Burmese Amber Based on U-Pb Dating of Zircons. Cretaceous Research , 37, 155-163. https://doi.org/10.1016/j.cretres.2012.03.014
Yu, T., Kelly, R., Mu, L., Ross, A., Kennedy, J., Broly, P., Xia, F., Zhang, H., Wang, B. and Dilcher, D. (2019) An Ammonite Trapped in Burmese Amber. Proceedings of the National Academy of Sciences of the United States of America , 116, 11345-11350. https://doi.org/10.1073/pnas.1821292116
Pryer, K.M., Schneider, H., Smith, A.R., Cranfill, R., Wolf, P.G., Hunt, J.S. and Sipes, S.D. (2001) Horsetails and Ferns Are a Monophyletic Group and the Closest Living Relatives to Seed Plants. Nature , 409, 618-622. https://doi.org/10.1038/35054555
Pryer, K.M., Schuettpelz, E., Wolf, P.G., Schneider, H., Smith, A.R. and Cranfill, R. (2004) Phylogeny and Evolution of Ferns (Monilophytes) with a Focus on the Early Leptosporangiate Divergences. American Journal of Botany , 91, 1582-1598. https://doi.org/10.3732/ajb.91.10.1582
Schneider, H., Schuettpelz, E., Pryer, K.M., Cranfill, R., Magallon, S. and Lupia, R. (2004) Ferns Diversified in the Shadow of Angiosperms. Nature , 428, 553-557. https://doi.org/10.1038/nature02361
Schuettpelz, E. and Pryer, K.M. (2009) Evidence for a Cenozoic Radiation of Ferns in an Angiosperm-Dominated Canopy. Proceedings of the National Academy of Sciences of the United States of America , 106, 11200-11205. https://doi.org/10.1073/pnas.0811136106
Kuo, L. Y., Li, F.W., Chiou, W.L. and Wang, C.N. (2011) First Insights into Fern MatK Phylogeny. Molecular Phylogenetics and Evolution , 59, 556-566. https://doi.org/10.1016/j.ympev.2011.03.010
Rothfels, C.J., Li, F.W., Sigel, E.M., Huiet, L., Larsson, A., Burge, D.O., Ruhsam, M., Deyholos, M., Soltis, D.E., Stewart Jr., C.N. Shaw, S.W., Pokorny, L., Chen, T., DePamphilis, C., DeGironimo, L., Chen, L., Wei, X.F., Sun, X., Korall, P., Stevenson, D.W., Graham, S.W., Wong, G.K.S. and Pryer, K.M. (2015) The Evolutionary History of Ferns Inferred from 25 Low-Copy Nuclear Genes. American Journal of B o tany , 102, 1089-1107. https://doi.org/10.3732/ajb.1500089
Testo, W. and Sundue, M. (2016) A 4000-Species Dataset Provides New Insight into the Evolution of Ferns. Molecular Phylogenetics and Evolution , 105, 200-211. https://doi.org/10.1016/j.ympev.2016.09.003
Schneider, H. and Kenrick, P. (2001) An Early Cretaceous Root Climbing Epiphyte (Lindsaeaceae) and Its Significance for Calibrating the Diversification of Polypodiaceous Ferns. Review of Palaeobotany and Palynology , 115, 33-41. https://doi.org/10.1016/S0034-6667(01)00048-3
Deng, S.H. (2002) Ecology of the Early Cretaceous Ferns of Northeast China. R e view of Palaeobotany and Palynology , 119, 93-112. https://doi.org/10.1016/S0034-6667(01)00131-2
Tidwell, W.D. and Ash, S.R. (1994) A Review of Selected Triassic to Early Cretaceous Ferns. Journal of Plant Research , 107, 417-442. https://doi.org/10.1007/BF02344066
Collinson, M.E. (2001) Cainozoic Ferns and Their Distribution. Brittonia , 53, 173-235. https://doi.org/10.1007/BF02812700
Skog, J.E. (2001) Biogeography of Mesozoic Leptosporangiate Ferns Related to Extant Ferns. Brittonia , 53, 236-269. https://doi.org/10.1007/BF02812701
Bower, F.O. (1963) The Ferns (Filicales) Treated Comparatively with a View to Their Natural Classification. Today and Tomorrow’s Book Agency, New Delhi.
Korall, P., Pryer, K.M., Metzgar, J.S., Schneider, H. and Conant, D.S. (2006) Tree Ferns: Monophyletic Groups and Their Relationships AS Revealed By Four Protein-Coding Plastid Loci. Molecular Phylogenetics and Evolution , 39, 830-845. https://doi.org/10.1016/j.ympev.2006.01.001
Wolf, P.G., Sipes, S.D., White, M.R., Martines, M.L., Pryer, K.M., Smith, A.R. and Ueda, K. (1999) Phylogenetic Relationships of the Enigmatic Fern Families Hymenophyllopsidaceae and Lophosoriaceae: Evidence from RbcL Nucleotide Sequences. Plant Systematics and Evolution , 219, 263-270. https://doi.org/10.1007/BF00985583
Zhou, X.L. (2013) A Study on the Anatomy of Fern Sporangium and Its Relationship to the Leaf Vein. Master’s Thesis, Central South University of Forestry and Technology, Changsha.
Skog, J.E., Zimmer, E.A. and Mickel, J.T. (2002) Additional Support for Two Subgenera of Anemia (Schizaeaceae) from Data for the Chloroplast Intergenic Spacer Region TrnL-F and Morphology. American Fern Journal , 92, 119-130. https://doi.org/10.1640/0002-8444(2002)092[0119:ASFTSO]2.0.CO;2
Wikstrom, N., Kenrick, P. and Vogel, J.C. (2002) Schizaeaceae: A Phylogenetic Approach. Review of Palaeobotany and Palynology , 119, 35-50. https://doi.org/10.1016/S0034-6667(01)00128-2
Labiak, P.H., Mickel, J.T. and Hanks, J.G. (2015) Molecular Phylogeny and Character Evolution of Anemiaceae (Schizaeales). Taxon , 64, 1141-1158. https://doi.org/10.12705/646.3
Tryon, R.M. and Tryon, A.F. (1982) Ferns and Allied Plants with Special Reference to Tropical America. Springer, New York. https://doi.org/10.1007/978-1-4613-8162-4
Smith, R.D.A. and Ross, A.J. (2018) Amberground Pholadid Bivalve Borings and Inclusions in Burmese Amber: Implications for Proximity of Resin-Producing Forests to Brackish Waters, and the Age of the Amber. Earth and Environmental Science Transactions of the Royal Society of Edinburgh , 107, 239-247. https://doi.org/10.1017/S1755691017000287
Rothwell, R.W. and Stockey, R.A. (2008) Phylogeny and Evolution of Ferns: A Paleontological Perspective. In: Ranker, T.A. and Haufler, C.H., Eds., Biology an d Ev o lution of Ferns and Lycophytes , Cambridge University Press, Cambridge, 332-366. https://doi.org/10.1017/CBO9780511541827.014
Wang, Y.R. and Li, C.X. (2024) Inferring Eupolypods Divergence Time Using Bayesian Tip-Dating. Open Journal of Geology , 14, 247-258. https://doi.org/10.4236/ojg.2024.142013