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Type: Article
Published: 2024-10-30
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Arthropod coprolites and wound reaction in the late Paleozoic climbing fern Hansopteris

State Key Laboratory of Palaeobiology and Petroleum Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, No. 39 East Beijing Road, Nanjing 210008, China; University of Chinese Academy of Sciences, No. 19(A) Yuquan Road, Beijing 100049, China
Institute of Palaeontology, Yunnan Key Laboratory of Earth System Science, Yunnan Key Laboratory for Palaeobiology, MEC International Joint Laboratory for Palaeobiology and Palaeoenvironment, Yunnan University, Kunming 650500, China
State Key Laboratory of Palaeobiology and Petroleum Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, No. 39 East Beijing Road, Nanjing 210008, China; Centre of Palaeobiodiversity, West Bohemian Museum in Pilsen, Kopeckého sady 2, Plzeň 30100, Czech Republic
State Key Laboratory of Palaeobiology and Petroleum Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, No. 39 East Beijing Road, Nanjing 210008, China; University of Chinese Academy of Sciences, No. 19(A) Yuquan Road, Beijing 100049, China
State Key Laboratory of Palaeobiology and Petroleum Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, No. 39 East Beijing Road, Nanjing 210008, China; University of Chinese Academy of Sciences, No. 19(A) Yuquan Road, Beijing 100049, China
plant-arthropod interaction boring tunnel traumatic stimulus fossil climber pyrite framboid Wuda Tuff Flora

Abstract

Interactions between arthropods and plants have been documented extensively in late Paleozoic trees and ground cover plants, but they have rarely been recorded in late Paleozoic climbers. In this study, we present the second example of coprolites preserved within the plant tissue from the early Permian fossil Lagerstätte Wuda Tuff Flora. The host axis is identified as a phyllophore of the climbing fern Hansopteris uncinatus by the combined evidence of anatomy, morphology, and associated plants. Unlike the first coprolites, which were suggested to be produced by oribatid mites, the culprit of the studied coprolites was likely a myriapod or beetle, indicated by their slightly larger size and the boring behaviour. Furthermore, anomalous parenchymatous cells, sclerenchymatous cells, and metaxylem tracheids have been observed surrounding the tunnel, suggesting responses to traumatic stimulus caused by arthropod damage. This discovery provides an informative example of arthropod herbivory on late Paleozoic climbers and sheds light on how the host plant responded during the early stage of injury.

References

  1. Cai, C.Y., Tihelka, E., Giacomelli, M., Lawrence, J.F., Kundrata, R., Yamamoto, S., Thayer, M.K., Newton, A.F., Leschen, R.A.B., Gimmel, M.L., Lü, L., Engel, M.S., Bouchard, P., Huang, D.Y., Pisani, D. & Donoghue, P.C.J. (2022) Integrated phylogenomics and fossil data illuminate the evolution of beetles. Royal Society Open Science, 9 (3), 211771. https://doi.org/10.1098/rsos.211771
  2. Cheng, Y.M., Yang, X.N. & Liu, F.X. (2021) A permineralized thamnopteroid rhizome (Osmundaceae) with coprolites from the Permian of Heilongjiang Province, northeast China: The most primitive record of Osmundaceae in Asia. Review of Palaeobotany and Palynology, 290, 104425. https://doi.org/10.1016/j.revpalbo.2021.104425
  3. D’Rozario, A., Labandeira, C., Guo, W.Y., Yao, Y.F. & Li, C.S. (2011) Spatiotemporal extension of the Euramerican Psaronius component community to the Late Permian of Cathaysia: In situ coprolites in a P. housuoensis stem from Yunnan Province, southwest China. Palaeogeography, Palaeoclimatology, Palaeoecology, 306 (3-4), 127–133. https://doi.org/10.1016/j.palaeo.2011.04.009
  4. Dunlop, J.A. & Garwood, R.J. (2017) Terrestrial invertebrates in the Rhynie chert ecosystem. Philosophical Transactions of the Royal Society B-Biological Sciences, 373 (1739), 20160493. https://doi.org/10.1098/rstb.2016.0493
  5. Falcon-Lang, H.J., Labandeira, C. & Kirk, R. (2015) Herbivorous and detritivorous arthropod trace fossils associated with subhumid vegetation in the Middle Pennsylvanian of Southern Britain. Palaios, 30 (3), 192–206. https://doi.org/10.2110/palo.2014.082
  6. Fang, Y.H., Qin, X., Liao, Q.G., Du, R., Luo, X.Z., Zhou, Q., Li, Z., Chen, H.C., Jin, W.T., Yuan, Y.N., Sun, P.B., Zhang, R., Zhang, J., Wang, L., Cheng, S.F., Yang, X.Y., Yan, Y.H., Zhang, X.T., Zhang, Z.H., Bai, S.N., Van de Peer, Y., Lucas, W.J., Huang, S.W. & Yan, J.B. (2021) The genome of homosporous maidenhair fern sheds light on the euphyllophyte evolution and defences. Nature Plants, 8 (9), 1024–1037. https://doi.org/10.1038/s41477-022-01222-x
  7. Feng, Z., Bertling, M., Noll, R., Ślipiński, A. & Rößler, R. (2019) Beetle borings in wood with host response in early Permian conifers from Germany. Paläontologische Zeitschrift, 93 (3), 409–421. https://doi.org/10.1007/s12542-019-00476-9
  8. Feng, Z., Wang, J., Rößler, R., Ślipiński, A. & Labandeira, C. (2017) Late Permian wood-borings reveal an intricate network of ecological relationships. Nature Communications, 8, 556. https://doi.org/10.1038/s41467-017-00696-0
  9. Feng, Z., Wang, J., Zhou, W.M., Wan, M.L. & Pšenička, J. (2021) Plant-insect interactions in the early Permian Wuda Tuff Flora, North China. Review of Palaeobotany and Palynology, 294, 104269. https://doi.org/10.1016/j.revpalbo.2020.104269
  10. Fletcher, T.L. & Salisbury, S.W. (2014) Probable oribatid mite (Acari: Oribatida) tunnels and faecal pellets in silicified conifer wood from the Upper Cretaceous (Cenomanian—Turonian) portion of the Winton Formation, central–western Queensland, Australia. Alcheringa, 38 (4), 541–545. https://doi.org/10.1080/03115518.2014.912557
  11. Galtier, J. & Phillips, T.L. (2014) Evolutionary and ecological perspectives of Late Paleozoic ferns. Part III. Anachoropterid ferns (including Anachoropteris, Tubicaulis, the Sermayaceae, Kaplanopteridaceae and Psalixochlaenaceae). Review of Palaeobotany and Palynology, 205, 31–73. https://doi.org/10.1016/j.revpalbo.2014.02.012
  12. Goto, H.E. (1972) On the structure and function of the mouthparts of the soil-inhabiting collembolan Folsomia candida. Biological Journal of the Linnean Society, 4 (2), 147–168. https://doi.org/10.1111/j.1095-8312.1972.tb00693.x
  13. Hendrix, S.D. (1980) An evolutionary and ecological perspective of the insect fauna of ferns. The American Naturalist, 115 (2), 171–196. https://doi.org/10.1086/283554
  14. Holden, H.S. (1910) Note on a wounded Myeloxylon. New Phytologist, 9 (6-7), 253–257. https://doi.org/10.1111/j.1469-8137.1910.tb05573.x
  15. Holden, H.S. (1912) Some wound reactions in filicinean petioles. Annals of Botany, 26 (3), 777–794. https://doi.org/10.1093/oxfordjournals.aob.a089416
  16. Holden, H.S. (1931) Some observations on the wound reactions of Ankyropteris corrugata. Botanical Journal of the Linnean Society, 48 (325), 643–655. https://doi.org/10.1111/j.1095-8339.1931.tb00597.x
  17. Kim, K.W., Hyun, J.W. & Park, E.W. (2004) Cytology of cork layer formation of citrus and limited growth of Elsinoe fawcettii in scab lesions. European Journal of Plant Pathology, 110 (2), 129–138. https://doi.org/10.1023/B:EJPP.0000015330.21280.4c
  18. Krings, M., Dotzler, N., Galtier, J. & Taylor, T.N. (2011) Oldest fossil basidiomycete clamp connections. Mycoscience, 52 (1), 18–23. https://doi.org/10.1007/s10267-010-0065-4
  19. Laaß, M., Kretschmer, S., Leipner, A. & Hauschke, N. (2020) First evidence of arthropod herbivory in calamitalean stems from the Pennsylvanian of Germany. Annales Societatis Geologorum Poloniae, 90 (3), 219–246. https://doi.org/10.14241/asgp.2020.14
  20. Labandeira, C.C. (2006) The four phases of plant-arthropod associations in deep time. Geologica Acta, 4 (4), 409–438.
  21. Labandeira, C.C. & Phillips, T.L. (1996) Insect fluid-feeding on Upper Pennsylvanian tree ferns (Palaeodictyoptera, Marattiales) and the early history of the piercing-and-sucking functional feeding group. Annals of the Entomological Society of America, 89 (2), 157–183. https://doi.org/10.1093/aesa/89.2.157
  22. Labandeira, C.C., Phillips, T.L. & Norton, R.A. (1997) Oribatid mites and the decomposition of plant tissues in Paleozoic coal-swamp forests. Palaios, 12 (4), 319–353. https://doi.org/10.2307/3515334
  23. Lesnikowska, A.D. (1990) Evidence of herbivory in tree-fern petioles from the Calhoun Coal (Upper Pennsylvanian) of Illinois. Palaios, 5 (1), 76–80. https://doi.org/10.2307/3514997
  24. Nejat, N. & Mantri, N. (2017) Plant immune system: Crosstalk between responses to biotic and abiotic stresses the missing link in understanding plant defence. Current Issues in Molecular Biology, 23, 1–16. https://doi.org/10.21775/cimb.023.001
  25. Ozeretskovskaya, O.L., Vasyukova, N.I., Chalenko, G.I., Gerasimova, N.G., Revina, T.A. & Valueva, T.A. (2009) Wound healing and induced resistance in potato tubers. Applied Biochemistry and Microbiology, 45 (2), 199–203. https://doi.org/10.1134/S0003683809020148
  26. Pšenička, J., Wang, J., Bek, J., Pfefferkorn, H.W., Opluštil, S., Zhou, W.M., Frojdová, J.V. & Libertín, M. (2021) A zygopterid fern with fertile and vegetative parts in anatomical and compression preservation from the earliest Permian of Inner Mongolia, China. Review of Palaeobotany and Palynology, 294, 104382. https://doi.org/10.1016/j.revpalbo.2021.104382
  27. Putz, F.E. (1980) Lianas vs. trees. Biotropica, 12 (3), 224–225. https://doi.org/10.2307/2387978
  28. Rex, G.M. (1986) The preservation and paleoecology of the Lower Carboniferous silicified plant deposits at Esnost, near Autun, France. Geobios, 19 (6), 773–800. https://doi.org/10.1016/s0016-6995(86)80107-3
  29. Rößler, R. (2000) The late Palaeozoic tree fern Psaronius: An ecosystem unto itself. Review of Palaeobotany and Palynology, 108 (1-2), 55–74. https://doi.org/10.1016/s0034-6667(99)00033-0
  30. Rößler, R., Feng, Z. & Noll, R. (2012) The largest calamite and its growth architecture—Arthropitys bistriata from the Early Permian Petrified Forest of Chemnitz. Review of Palaeobotany and Palynology, 185, 64–78. https://doi.org/10.1016/j.revpalbo.2012.07.018
  31. Sagasti, A.J. & Bodnar, J. (2023) Biological decay by microorganisms in stems from the Upper Triassic Ischigualasto Formation (San Juan Province, Argentina): A striking microbial diversity in Carnian-Norian terrestrial ecosystems. Review of Palaeobotany and Palynology, 315, 104915. https://doi.org/10.1016/j.revpalbo.2023.104915
  32. Schmitz, M.D., Pfefferkorn, H.W., Shen, S.Z. & Wang, J. (2021) A volcanic tuff near the Carboniferous-Permian boundary, Taiyuan Formation, North China: Radioisotopic dating and global correlation. Review of Palaeobotany and Palynology, 294, 1–6. https://doi.org/10.1016/j.revpalbo.2020.104244
  33. Scott, A.C., Stephenson, J. & Chaloner, W.G. (1992) Interaction and coevolution of plants and arthropods during the Paleozoic and Mesozoic. Philosophical Transactions of the Royal Society B-Biological Sciences, 335 (1274), 129–165. https://doi.org/10.1098/rstb.1992.0016
  34. Scott, A.C. & Taylor, T.N. (1983) Plant animal interactions during the Upper Carboniferous. The Botanical Review, 49 (3), 259–307. https://doi.org/10.1007/bf02861089
  35. Slater, B.J., McLoughlin, S. & Hilton, J. (2012) Animal-plant interactions in a Middle Permian permineralised peat of the Bainmedart Coal Measures, Prince Charles Mountains, Antarctica. Palaeogeography, Palaeoclimatology, Palaeoecology, 363, 109–126. https://doi.org/10.1016/j.palaeo.2012.08.018
  36. Stopes, M.C. (1907) A note on wounded calamites. Annals of Botany, 21 (81-84), 277–281. https://doi.org/10.1093/oxfordjournals.aob.a089133
  37. Wang, J., Pfefferkorn, H.W., Oplustil, S. & Kerp, H. (2021) Permian “vegetational Pompeii”: A peat-forming in situ preserved forest from the Wuda Coalfield, Inner Mongolia, China—Introduction to a volume of detailed studies. Review of Palaeobotany and Palynology, 294, 104502. https://doi.org/10.1016/j.revpalbo.2021.104502
  38. Weaver, L., McLoughlin, S. & Drinnan, A.N. (1997) Fossil woods from the Upper Permian Bainmedart Coal Measures, northern Prince Charles Mountains, East Antarctica. AGSO Journal of Australian Geology and Geophysics, 16 (5), 655–676.
  39. Wei, H.B., Gou, X.D., Yang, J.Y. & Feng, Z. (2019) Fungi-plant-arthropods interactions in a new conifer wood from the uppermost Permian of China reveal complex ecological relationships and trophic networks. Review of Palaeobotany and Palynology, 271, 104100. https://doi.org/10.1016/j.revpalbo.2019.07.005
  40. Zhou, W.M., He, X.Y., Wang, S.J., Pšenička, J., Rößler, R., Rothwell, G.W., Galtier, J., Hilton, J. & Wang, J. (2023a) (3005) Proposal to conserve the name Botryopteris Renault (fossil Pteridophyta) against Botryopteris C. Presl (Ophioglossaceae). Taxon, 72 (6), 1377–1379. https://doi.org/10.1002/tax.13097
  41. Zhou, W.M., Li, D.D., Pšenička, J., Boyce, C.K. & Wang, J. (2019) A left-handed fern twiner in a Permian swamp forest. Current Biology, 29 (22), R1172–R1173. https://doi.org/10.1016/j.cub.2019.10.005
  42. Zhou, W.M., Li, D.D., Pšenička, J., Boyce, C.K., Wang, S.J. & Wang, J. (2022a) Diodonopteris virgulata sp. nov., a climbing fern from the early Permian Wuda Tuff Flora and its paleoecology. Review of Palaeobotany and Palynology, 304, 104699. https://doi.org/10.1016/j.revpalbo.2022.104699
  43. Zhou, W.M., Pšenička, J., Bek, J., Libertin, M., Wang, S.J. & Wang, J. (2023b) A new species of Botryopteridium Doweld from the early Permian Wuda Tuff Flora and its evolutionary significance. Review of Palaeobotany and Palynology, 311, 104849. https://doi.org/10.1016/j.revpalbo.2023.104849
  44. Zhou, W.M., Pšenička, J., Bek, J., Wan, M.L., Boyce, C.K. & Wang, J. (2021) A new anachoropterid fern from the Asselian (Cisuralian) Wuda Tuff Flora. Review of Palaeobotany and Palynology, 294, 104346. https://doi.org/10.1016/j.revpalbo.2020.104346
  45. Zhou, W.M., Pšenička, J., Frojdová, J.V., Wang, J., Wan, M.L. & Feng, Z. (2024) Two anachoropterid fern rachises from the in situ volcanic ash of the Whetstone Horizon (Kladno Formation, Pennsylvanian), Radnice Basin, Czech Republic. Palaeoworld, 33 (2), 341–362. https://doi.org/10.1016/j.palwor.2023.02.003
  46. Zhou, W.M., Wan, M.L., Pšenička, J. & Wang, J. (2022b) Discovery of coprolites in an Early Permian fern mesophyll. Palaeoentomology, 5 (1), 1–5. https://doi.org/10.11646/palaeoentomology.5.1.1
  47. Zodrow, E.L. & Mastalerz, M. (2009) A proposed origin for fossilized Pennsylvanian plant cuticles by pyrite oxidation (Sydney Coalfield, Nova Scotia, Canada). Bulletin of Geosciences, 84 (2), 227–240. https://doi.org/10.3140/bull.geosci.1094