New insights into the affinities, autoecology, and habit of the Mesozoic fern Weichselia reticulata based on the revision of stems from Bernissart (Mons Basin, Belgium)
[en] The Mesozoic is a key period in fern evolution, with the rise of most modern families. Weichselia reticulata is a widely distributed Jurassic–Cretaceous fern that has been suggested to belong to the Matoniaceae or possibly the Marattiaceae. The most accepted classic whole-plant reconstruction for this species is based on stem and foliage material from the Barremian–Aptian locality of Négresse (Bernissart, Mons Basin, Belgium). In this work, two of these stems are revised and analysed using computed tomography, providing new information on their internal anatomy and external morphology. Weichselia reticulata has a unique anatomy, distinct from all other extant or fossil ferns. Stem external morphology suggests adaptations to stressful environments, due to the scale insertions, and a thick cortex. Especially noteworthy is the presence of structures interpreted as aerophores or nectaries at the base of putative roots and petioles that could suggest a need for extra ventilation of the frond or interactions with animals. Although these new results do not settle the question of the systematic affinities of Weichselia, they provide new information about its autoecology and allow us to test the validity of previous whole-plant reconstructions.
Blanco-Moreno, Candela ; Departamento de Biología, Universidad Autónoma de Madrid, Cantoblanco (Madrid), Spain
Decombeix, Anne-Laure ; AMAP, Université de Montpellier, CIRAD, CNRS, INRA, IRD, Montpellier, France
Prestianni, Cyrille ; Université de Liège - ULiège > Département de géologie > Evolution and diversity dynamics lab ; OD Earth & History of Life, Royal Belgian Institute of Natural Sciences, Brussels, Belgium
Language :
English
Title :
New insights into the affinities, autoecology, and habit of the Mesozoic fern Weichselia reticulata based on the revision of stems from Bernissart (Mons Basin, Belgium)
Bio-oriented Technology Research Advancement Institution
Funding text :
We would like to acknowledge the team managing the μCT scanner at the RBINS (Brussels, Belgium), especially Ulysse Lefevre for scanning and reconstructing the Y slices, and all his valuable help with all technical matters in this paper. We also acknowledge the Institut des Sciences de l'Evolution (Montpellier, France) and LabEx CeMEB (ANR‐10‐LABX‐0004) for assistance in the use of the Avizo software, and for use of their facilities. CB‐M is supported by an FPI‐UAM 2015 grant from the Universidad Autónoma de Madrid, and benefitted from a grant from the same organization for the work in Montpellier. Collections in the Royal Belgian Institute of Natural Sciences, Brussels, were studied with the support of a grant from the SYNTHESYS Project ( http://www.synthesys.info ) financed by the European Community Research Infrastructure Action under the FP7 Integrating Activities Program. CP is funded by the BRAIN project BR/143/A3/COLDCASE in the framework of which this research has been done. AMAP (Botany and Computational Plant Architecture) is a joint research unit associated with CIRAD (UMR51), CNRS (UMR5120), INRAE (UMR931), IRD (R123), and Montpellier University (UM). Finally, we would like to thank Professor G.W. Rothwell and an anonymous reviewer for their very helpful comments on an earlier draft of this manuscript.We would like to acknowledge the team managing the ?CT scanner at the RBINS (Brussels, Belgium), especially Ulysse Lefevre for scanning and reconstructing the Y slices, and all his valuable help with all technical matters in this paper. We also acknowledge the Institut des Sciences de l'Evolution (Montpellier, France) and LabEx CeMEB (ANR-10-LABX-0004) for assistance in the use of the Avizo software, and for use of their facilities. CB-M is supported by an FPI-UAM 2015 grant from the Universidad Aut?noma de Madrid, and benefitted from a grant from the same organization for the work in Montpellier. Collections in the Royal Belgian Institute of Natural Sciences, Brussels, were studied with the support of a grant from the SYNTHESYS Project (http://www.synthesys.info) financed by the European Community Research Infrastructure Action under the FP7 Integrating Activities Program. CP is funded by the BRAIN project BR/143/A3/COLDCASE in the framework of which this research has been done. AMAP (Botany and Computational Plant Architecture) is a joint research unit associated with CIRAD (UMR51), CNRS (UMR5120), INRAE (UMR931), IRD (R123), and Montpellier University (UM). Finally, we would like to thank Professor G.W. Rothwell and an anonymous reviewer for their very helpful comments on an earlier draft of this manuscript.
Aguirrezabala, L. M., Torres, J. A. and Viera, L. I. 1985. El Weald de Igea (Cameros-La Rioja). Sedimentología, bioestratigrafía y paleoicnología de grandes reptiles (dinosaurios). Munibe Ciencias Naturales, 37, 111–138.
Allison, H. E. 1913. On the vascular anatomy of the rhizome of Platycerium. New Phytologist, 12, 311–321.
Almendros, G., Zancada, M. C., González-Vila, F. J., Lesiak, M. A. and Álvarez-Ramis, C. 2005. Molecular features of fossil organic matter in remains of the Lower Cretaceous fern Weichselia reticulata from Przenosza basement (Poland). Organic Geochemistry, 36, 1108–1115.
Alvin, K. L. 1968. The spore-bearing organs of the Cretaceous fern Weichselia Stiehler. Botanical Journal of the Linnean Society, 61, 87–92.
Alvin, K. L. 1971. Weichselia reticulata (Stokes et Webb) Fontaine from the Wealden of Belgium. Mémoire de L'Institut Royal des Sciences Naturelles de Belgique, 166, 1–33.
Alvin, K. L. 1974. Leaf anatomy of Weichselia based on fusainized material. Palaeontology, 17, 587–598.
Arens, N. C. 1997. Responses of leaf anatomy to light environment in the tree fern Cyathea caracasana (Cyatheaceae) and its application to some ancient seed ferns. Palaios, 12, 84–94.
Arens, N. C. and Smith, A. R. 1998. Cyathea planadae, a remarkable new creeping tree fern from Colombia, South America. American Fern Journal, 88, 49–59.
BAELE, J. M., GODEFROIT, P., SPAGNA, P. and DUPUIS, C. 2012. A short introduction to the geology of the Mons Basin and the Iguanodon Sinkhole, Belgium. 35–42. In GODEFROIT, P. (ed.) Bernissart dinosaurs and Early Cretaceous terrestrial ecosystems. Indiana University Press, 629 pp.
Barale, G. 1979. Découverte de Weichselia reticulata (Stokes & Webb) Fontaine emend. Alvin, filicinée leptosporangiée, dans le Crétace Inférieur de la province de Lérida (Espagne): implications stratigraphiques et paléoécologiques. Geobios, 12, 313–319.
Barale, G. and Azar, D. 2004. Cuticules végétales dans le Crétacé inférieur du Sud du Liban. Comptes Rendus Palevol, 3, 119–124.
Barale, G. and Ouaja, M. 2001. Découverte de nouvelles flores avec des restes à affinités angiospermiennes dans le Crétacé inférieur du Sud tunisien. Cretaceous Research, 22, 131–143.
Barral, A., Gomez, B., Zorrilla, J. M., Serrano, J. M., Yans, J., Cazedebat, M., Daviero-Gomez, V., Ewin, T. A. M. and Lecuyer, C. 2016. Local-scale analysis of plant community from the Early Cretaceous riparian ecosystem of Hautrage, Belgium. Palaeogeography, Palaeoclimatology, Palaeoecology, 443, 107–122.
Barthel, K. W. and Boettcher, R. 1978. Abu Ballas Formation (Tithonian/Berriasian; Southwestern Desert, Egypt) a significant lithostratigraphic unit of the former ‘Nubian Series’. Mitteilungen der Bayerischen Staatssammlung für Paläontologie und Historische Geologie, 18, 153–166.
Batten, D. J. 1974. Wealden palaeoecology from the distribution of plant fossils. Proceedings of the Geologists’ Association, 85, 433–458.
Batten, D. J. 1998. Palaeoenvironmental implications of plant, insect and other organic-walled microfossils in the Weald Clay Formation (Lower Cretaceous) of southeast England. Cretaceous Research, 19, 279–315.
BIERHORST, D.W. 1971. Morphology of vascular plants. Macmillan, 560 pp.
Blanco-Moreno, C., Gomez, B. and Buscalioni, A. D. 2018. Palaeobiogeographic and metric analysis of the Mesozoic fern Weichselia. Geobios, 51, 571–578.
Blanco-Moreno, C., Gomez, B., Marugán-Lobón, J., Daviero-Gomez, V. and Buscalioni, A. D. 2019. A novel approach for the metric analysis of fern fronds: growth and architecture of the Mesozoic fern Weichselia reticulata in the light of modern ferns. PLoS One, 14, e0219192.
Blomquist, H. L. 1922. Vascular anatomy of Angiopteris evecta. Botanical Gazette, 73, 181–199.
Bommer, C. 1910. Contribution à l’étude du genre Weichselia. Bulletin de la Société Royale de Botanique de Belgique, 3, 296–304.
Bower, F. O. 1923. The ferns (Filicales): Analytical examination of the criteria of comparison. Vol. 1. Cambridge University Press, 359 pp.
Bower, F. O. 1926. The ferns (Filicales): The Eusporangiatae and other relatively primitive ferns. Vol. 2. Cambridge University Press, 344 pp.
Brouat, C., Gibernau, M., Amsellem, L. and McKey, D. 1998. Corner's rules revisited: ontogenetic and interspecific patterns in leaf–stem allometry. The New Phytologist, 139, 459–470.
Carpentier, A. 1927. La flore wealdienne de Féron-Glageon (Nord). Mémoires de la Société Géologique du Nord, 1, 1–151.
Cignoni, P., Callieri, M., Corsini, M., Dellepiane, M., Ganovelli, F. and Ranzuglia, G. 2008. Meshlab: an open-source mesh processing tool. 129–136. In Scarano, V., De Chiara, R. and Erra, U. (eds). Eurographics Italian Chapter Conference. The Eurographics Association.
Cornet, J. 1927. L’époque wealdienne dans le Hainaut. Annales de la Société Géologique de Belgique, Tome L., 161–164.
Cornet, J. and Schmitz, G. 1898. Les puits naturels du terrain houiller du Hainaut. Bulletin de la Société belge de Géologie, Paléontologie et Hydrologie, 12, 301-318.
Daber, R. 1968. A Weichselia–Stiehleria–Matoniaceae community within the Quedlinburg Estuary of Lower Cretaceous age. Botanical Journal of the Linnean Society, 61, 75–85.
Davies, K. L. 1991. A brief comparative survey of aerophore structure within the Filicopsida. Botanical Journal of the Linnean Society, 107, 115–137.
Dejax, J., Pons, D. and Yans, J. 2007. Palynology of the dinosaur-bearing Wealden facies in the natural pit of Bernissart (Belgium). Review of Palaeobotany & Palynology, 144, 25-38.
Delclòs, X. and Soriano, C. 2016. Insecta. 70–88. In Poyato-Ariza, F. J. and Buscalioni, A. (eds). Las Hoyas: A Cretaceous wetland. Verlag Dr Friedrich Pfeil, 262 pp.
Delmer, A. and Van Wichelen, P. 1980. Répertoire des puits naturels connus en terrain houiller du Hainaut. Geological Survey of Belgium Professional Papers, 172, 1–234.
Diéguez, M. C. and Meléndez, N. 2000. Early Cretaceous ferns from lacustrine limestones at Las Hoyas, Cuenca province, Spain. Palaeontology, 43, 1113–1141.
Diez, J., Sender, L., Villanueva-Amadoz, U., Ferrer, J. and Rubio, C. 2005. New data regarding Weichselia reticulata: soral clusters and the spore developmental process. Review of Palaeobotany & Palynology, 135, 99–107.
Durand, L. Z. and Goldstein, G. 2001. Growth, leaf characteristics, and spore production in native and invasive tree ferns in Hawaii. American Fern Journal, 91, 25–36.
Edwards, W. N. 1933. On the Cretaceous fern Paradoxopteris and its connexion with Weichselia. Annals of Botany, 47, 317–341.
El Atfy, H., Jasper, A. and Uhl, D. 2020. A new record of Paradoxopteris stromeri Hirmer 1927 (Monilophyta, incertae sedis) from the Cenomanian of Sinai, Egypt. Review of Palaeobotany & Palynology, 273, 104148.
El-Khayal, A. 1985. Occurrence of a characteristic Wealden fern (Weichselia reticulata) in the Wasia Formation, central Saudi Arabia. Scrypta Geologica, 79, 75–88.
Evert, R. F. 2006. Esau's plant anatomy: Meristems, cells, and tissues of the plant body: Their structure, function, and development. John Wiley & Sons, Hoboken, NJ, 600 pp.
Fedorov, A., Beichel, R., Kalpathy-Cramer, J., Finet, J., Fillion-Robin, J. C., Pujol, S., Bauer, C., Jennings, D., Fennessy, F., Sonka, M. and Buatti, J. 2012. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magnetic Resonance Imaging, 30, 1323–1341.
Godefroit, P. 2012. Bernissart dinosaurs and Early Cretaceous terrestrial ecosystems. Indiana University Press, 629 pp.
Gomez, B., Thévenard, F., Fantin, M. and Giusberti, L. 2002. Late Cretaceous plants from the Bonarelli level of the Venetian Alps, northeastern Italy. Cretaceous Research, 23, 671–685.
Gomez, B., Gillot, T., Daviero-Gomez, V., Spagna, P. and Yans, J. 2008. Paleoflora from the Wealden facies strata of Belgium: mega-and meso-fossils of Hautrage (Mons Basin). Memoirs of the Geological Survey, 55, 53–60.
Grimaldi, D. and Agosti, D. 2000. A formicine in New Jersey Cretaceous amber (Hymenoptera: Formicidae) and early evolution of the ants. Proceedings of the National Academy of Sciences, 97, 13678–13683.
Halle, F. 1965. Les stolons de la fougère arborescente Cyathea manniana Hooker. Comptes Rendus de L'Académie des Sciences, 261, 2935–2938.
Halle, F. 1966. Étude de la ramification du tronc chez quelques fougères arborescentes. Adansonia, 6, 405–424.
Harris, T. M. 1981. Burnt ferns from the English Wealden. Proceedings of the Geologists’ Association, 92, 47–58.
Haushahn, T., Speck, T. and Masselter, T. 2014. Branching morphology of decapitated arborescent monocotyledons with secondary growth. American Journal of Botany, 101, 754–763.
Heil, M. 2015. Extrafloral nectar at the plant-insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs. Annual Review of Entomology, 60, 213–232.
Hesse, L., Masselter, T., Leupold, J., Spengler, N., Speck, T. and Korvink, J. G. 2016. Magnetic resonance imaging reveals functional anatomy and biomechanics of a living dragon tree. Scientific Reports, 6, 32685.
Hirmer, M. 1927. Handbuch der Paláobotanik. R. Oldenbourg, Berlin, 708 pp.
Jung, J., Lee, S. C. and Choi, H. 2008. Anatomical patterns of aerenchyma in aquatic and wetland plants. Journal of Plant Biology, 51, 428–439.
Karst, A. L. and Lechowicz, M. J. 2007. Are correlations among foliar traits in ferns consistent with those in the seed plants? New Phytologist, 173, 306–312.
Kato, M. 1993. A taxonomic study of the genus Matonia (Matoniaceae). Blumea: Biodiversity, Evolution & Biogeography of Plants, 38, 167–172.
Kessler, M., Siorak, Y., Wunderlich, M. and Wegner, C. 2007. Patterns of morphological leaf traits among pteridophytes along humidity and temperature gradients in the Bolivian Andes. Functional Plant Biology, 34, 963-971.
Koeniguer, J. C. 1966. Étude paléophytogéographique du Continental Intercalaire de l'Afrique Nord-Équatoriale. Sur de nouveaux échantillons du genre Paradoxopteris. Mémoires de la Société Géologique de France, 105, 100–112.
Koptur, S., Smith, A. R. and Baker, I. 1982. Nectaries in some neotropical species of Polypodium (Polypodiaceae): preliminary observations and analyses. Biotropica, 14, 108–113.
Koptur, S., Palacios-Rios, M., Díaz-Castelazo, C., MacKay, W. P. and Rico-Gray, V. 2013. Nectar secretion on fern fronds associated with lower levels of herbivore damage: field experiments with a widespread epiphyte of Mexican cloud forest remnants. Annals of Botany, 111, 1277–1283.
Kramer, K. U. 1990. Matoniaceae. 183–185. In Kramer, K. U. and Green, P. S. (eds). Pteridophytes and gymnosperms. Springer, 404 pp.
Lehtonen, S., Silvestro, D., Karger, D. N., Scotese, C., Tuomisto, H., Kessler, M., Peña, C., Wahlberg, N. and Antonelli, A. 2017. Environmentally driven extinction and opportunistic origination explain fern diversification patterns. Scientific Reports, 7, 1–12.
Lyon, M. A., Johnson, K., Wing, S., Nicholas, D., Lacovara, K. and Smith, J. 2001. Late Cretaceous equatorial coastal vegetation: new megaflora associated with dinosaur finds in the Bahariya oasis, Egypt. Geological Society of America Abstracts With Programs, 33, 1179.
Morgan, E. J. 1959. The morphology and anatomy of American species of the genus Psaronius. Illinois Biological Monographs, 27, 1–108.
Niklas, K. J. 1978. Morphometric relationships and rates of evolution among Paleozoic vascular plants. Evolutionary Biology, 11, 509–543.
Niklas, K. J. 1991. Flexural stiffness allometries of angiosperm and fern petioles and rachises: evidence for biomechanical convergence. Evolution, 45, 734–750.
Niklas, K. J. 1994. Predicting the height of fossil plant remains: an allometric approach to an old problem. American Journal of Botany, 81, 1235–1242.
Niklas, K. J., Tiffney, B. H. and Knoll, A. H. 1983. Patterns in vascular land plant diversification. Nature, 303, 614–616.
Ough, K. and Murphy, A. 2004. Decline in tree-fern abundance after clearfell harvesting. Forest Ecology & Management, 199, 153–163.
Peppe, D. J., Lemons, C. R., Royer, D. L., Wing, S. L., Wright, I. J., Lusk, C. H. and Rhoden, C. H. 2014. Biomechanical and leaf–climate relationships: a comparison of ferns and seed plants. American Journal of Botany, 101, 338–347.
Poorter, H., Niinemets, U., Poorter, L., Wright, I. J. and Villar, R. 2009. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist, 182, 565–588.
Poyato-Ariza, F. J. and Buscalioni, A. D. 2016. Las Hoyas: A Cretaceous wetland. Verlag Dr Friedrich Pfeil, 262 pp.
PPG I 2016. A community-derived classification for extant lycophytes and ferns. Journal of Systematics & Evolution, 54, 563–603.
QUINIF, Y. and LICOURT, L. 2012. The karstic phenomenon of the Iguanodon Sinkhole and the geomorphological situation of the Mons Basin during the Early Cretaceous. 51–61. In GODEFROIT, P. (ed.) Bernissart dinosaurs and Early Cretaceous terrestrial ecosystems. Indiana University Press, 629 pp.
Rolleri, C. H. 2002. Caracteres diagnósticos y taxonomía en el género Angiopteris Hoffm. (Marattiaceae Bercht. & JS Presl): I, los caracteres. Revista del Museo de La Plata, 15, 23–49.
Rolleri, C. H. 2004. Revisión del género Danaea (Marattiaceae-Pteridophyta). Darwiniana, Nueva Serie, 42, 217–301.
Román Gómez, P. 1986. Nota sobre la macroflora del Cretácico inferior de la Cuenca de Préjano (LaRioja). Coloquios de Paleontología, 41, 35–40.
Ross, A. J. and Cook, E. 1995. The stratigraphy and palaeontology of the Upper Weald Clay (Barremian) at Smokejacks Brickworks, Ockley, Surrey, England. Cretaceous Research, 16, 705–716.
Rothwell, G. W. and Blickle, A. H. 1982. Psaronius magnificus n. comb., a marattialean fern from the Upper Pennsylvanian of North America. Journal of Paleontology, 56, 459–468.
Schneider, C. A., Rasband, W. S. and Eliceri, K. W. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671.
Schnyder, J., Dejax, J., Keppens, E., Tu, T. T. N., Spagna, P., Boulila, S., Galbrun, B., Riboulleau, A., Thsibangu, J. P. and Yans, J. 2009. An Early Cretaceous lacustrine record: organic matter and organic carbon isotopes at Bernissart (Mons Basin, Belgium). Palaeogeography, Palaeoclimatology, Palaeoecology, 281, 79-91.
Scott, A. C., Cripps, J. A., Collinson, M. E. and Nichols, G. J. 2000. The taphonomy of charcoal following a recent heathland fire and some implications for the interpretation of fossil charcoal deposits. Palaeogeography, Palaeoclimatology, Palaeoecology, 164, 1–31.
Sender, L. M., Villanueva-Amadoz, U., Pons, D., Diez, J. B., García-Ávila, M. and Ferrer, J. 2015. New reconstruction of Weichselia reticulata (Stokes et Webb) Fontaine in Ward emend. Alvin, 1971 based on fertile remains from the middle Albian of Spain. Historical Biology, 27, 460–468.
Seward, A. C. 1900. La flore wealdienne de Bernissart. Mémoire du Muséum D'Histoire Naturelle de Belgique, 1, 1–37.
Shinaq, R. and Bandel, K. 1998. The flora of an estuarine channel margin in the Early Cretaceous of Jordan. Freiberger Forschungshefte C 474, Paläontologie, Stratigraphie, Fazies, 6, 39–57.
Silantieva, N. and Krassilov, V. 2006. Weichselia Stiehler from Lower Cretaceous of Makhtesh Ramon, Israel: new morphological interpretation and taxonomical affinities. Acta Palaeobotanica Krakow, 46, 119–135.
Smith, A. R., Pryer, K. M., Schettpelz, E., Korall, P., Schneider, H. and Wolf, P. G. 2006. A classification for extant ferns. Taxon, 55, 705–731.
SPAGNA, P., YANS, J., SCHNYDER, J. and DUPUIS, C. 2012. The palaeoenvironment of the Bernissart iguanodons: sedimentological analysis of the Lower Cretaceous Wealden facies in the Bernissart area. 87–96. In GODEFROIT, P. (ed.) Bernissart dinosaurs and Early Cretaceous terrestrial ecosystems. Indiana University Press, 629 pp.
Stokes, C. and Webb, P. B. 1824. Description of some fossil vegetables of the Tilgate Forest in Sussex. Transactions of the Geological Society of London, Series 2, 1, 421–424.
Tanner, E. V. J. 1983. Leaf demography and growth of the tree-fern Cyathea pubescens Mett. ex Kuhn in Jamaica. Botanical Journal of the Linnean Society, 87, 213–227.
Tidwell, W. D. and Ash, S. R. 1994. A review of selected Triassic to Early Cretaceous ferns. Journal of Plant Research, 107, 417–442.
Van den Broeck, E. 1898. Les coupes du gisement de Bernissart. Caractères et dispositions sedimentaires de l'argile ossifere du cran aux Iguanodons. Bulletin de la Societé Belge de Géologie de Paleontologie et de Hydrologie, 12, 216–243.
Van Konijnenburg-Van Cittert, J. H. A. 1993. A review of the Matoniaceae based on in situ spores. Review of Palaeobotany & Palynology, 7, 235–267.
Watson, J. and Alvin, K. L. 1996. An English Wealden floral list, with comments on possible environmental indicators. Cretaceous Research, 17, 5–26.
West, C. 1915. On the structure and development of the secretory tissues of the Marattiaceae. Annals of Botany, 29, 409–422.
White, R. A. and Turner, M. D. 2012. The anatomy and occurrence of foliar nectaries in Cyathea (Cyatheaceae). American Fern Journal, 102, 91–114.
White, R. A. and Turner, M. D. 2017. The comparative anatomy of Hymenophyllopsis and Cyathea (Cyatheaceae): a striking case of heterochrony in fern evolution. American Fern Journal, 107, 30–57.
YANS, J., ROBASZYNSKI, F. and MASURE, E. 2012. Biostratigraphy of the Cretaceous sediments overlying the Wealden facies in the Iguanodon sinkhole at Bernissart. 87–96. In GODEFROIT, P. (ed.) Bernissart dinosaurs and Early Cretaceous terrestrial ecosystems. Indiana University Press, 629 pp.
Zeiller, R. 1914. Sur quelques plantes wealdiennes recueillies au Pérou par M. le Capitaine Berthon. Revue Générale de Botanique, 25, 647–674.
