The Neuropteris ovata frond and its cyclopteroids: micromorphology-spectrochemistry-fractal taxonomy: Propositions for restructuring and taxonomy (Pennsylvanian, Canada)


Authors: Zodrow EL, D’Angelo JA, Cleal CJ

Published in: Bulletin of Geosciences, volume 91, issue 4; pages: 669 - 704; Received 18 March 2016; Accepted in revised form 13 October 2016; Online 13 January 2017

Keywords: morphology-chemistry, cyclopteroids, frond Aufbau, foliage, linkage, reconstruction,

full text (PDF, 11.98 MB)

Export to RIS



The primary study material consists of the 65-cm frond Neuropteris ovata (Hoffmann) var. simonii, associate petiole with organically attached cyclopteroid leaflets and trunk. Ancillary N. ovata material is used, all from the Asturian-Cantabrian strata of the Sydney Coalfield, Canada. This material is appropriate for the objective of the study to present an ovata-frond Aufbau in terms of micromorphology coupled with chemistry using an holistic sampling design (co-ordinating epidermal microscopy with chemistry per sample location). Chemical analyses were obtained by the reliable FTIR technique (Fourier transform infrared spectroscopy) and interpreted via chemometrics by methods of principal component analysis. Fractal geometry is introduced as a promising taxonomic parameter. The main conclusions include that the N. ovata plant can be characterized by three distinct epidermal structures: (1) rectangular elongate (trunk and petiole), (2) elongate (rachides of three orders), and (3) undulate (pinnule), which to a certain extent agrees with the chemistry of the frond Aufbau. The frond was also complex - architecturally, histologically, physiologically, chemically and autecologically. It was photosynthetic, had secretory organs (implying a characteristic plant aroma), supporting rodlets, divers epicuticular features, and a distinct chemical composition/structure. The frond was likely 4 m long with complex-pinnate cyclopteroid leaflets, fimbriate or entire-margined, below and above the main bifurcation, which begs the question of cyclopteroid definition and function. The overall results will be beneficial to taxonomy/systematics, and guide pteridospermous reconstruction into a new paradigm.


ADINEW, B. 2014. GC-MS and FT-IR analysis of constituents of essential oil from Cinnamon bark growing in south-west Ethiopia. International Journal of Herbal Medicine 1(6), 22-31.

ALVAREZ-CLARE, S. 2005. Biomechanical properties of tropical tree seedlings as a functional correlate of shade tolerance. xii + 83 pp. MSc. thesis, University of Florida, Florida.

BARTHEL, M. 1962. Epidermisuntersuchungen an einigen inkohlten Pteridospermenblättern des Oberkarbons und Perms. Geologie 11, Beiheft 33, 1-140.

BARTHEL, M. 1966. Johann Georg Bornemann - Begründer der Kutikularanalyse. Hallesches Jahrbuch Mitteldeutschlands Erdgeschichte 7, 7-10.

BEELER, H.E. 1983. Anatomy and frond architecture of Neuropteris ovata and N. scheuchzeri from the Upper Pennsylvanian of the Appalachian Basin. Canadian Journal of Botany 61(9), 2352-2368.View article

BELL, W.A. 1938. Fossil Flora of Sydney Coalfield, Nova Scotia. Geological Survey of Canada Memoir 215, 1-334.View article

BENÍTEZ, J., MATAS, A.J. & HEREDIA, A. 2004. Molecular characterization of the plant biopolymer cutin by AFM and spectroscopic techniques. Journal of Structural Biology 147, 179-184.View article

VAN BERGEN, P.F., BLOKKER, P., COLLINSON, M.E., SINNINGHE, DAMSTÉ, J.S. & DE LEEUW, J.W. 2004. Structural biomacromolecules in plants: what can be learnt from the fossil record?, 133-154. In HEMSLEY, A.R. & POOLE, A.I. (eds) The evolution of plant physiology. Elsevier Academy Press, Oxford.

VAN BERGEN, P.F., COLLINSON, M.E., SCOTT, A.C. & DE LEEUW, J.W. 1995. Unusual resin chemistry from Upper Carboniferous pteridosperm resin rodlets, 149-169. In ANDERSON, K.B. & CRELLING, J.C. (eds) Amber, resinite and fossil resins. Symposium Series 617. American Chemical Society, Washington D.C.

BERLI, F., D’ANGELO, J.A., CAVAGNARO, B., BOTTINI, R., WUILLOUD, R. & SILVA, M. 2008. Phenolic composition in grape (Vitis vinifera L. Cv. Malbec) ripened with different solar UV-B radiation levels by capillary zone electrophoresis. Journal of Agricultural Food Chemistry 56, 2892-2898.View article

BERTRAND, P. 1930. Études des gîtes minéraux de la France. Bassin houiller de la Sarre et de la Lorraine. I. Flore fossile. 1er fascicule: Neuroptéridées. 58 pp. Imprimerie L. Danel, Lille.

BODE, H. 1958. Die floristische Gliederung des Oberkarbons der Vereinigten Staaten von Nordamerica. Zeitschrift der Deutscher Geologischen Gesellschaft 110, 217-259.

BOYCE, C.K., CODY, G.D., FOGEL, M.L., HAZEN, R.M., ALEXANDER, C.M. O’D. & KNOLL, A.H. 2003. Chemical evidence for cell wall lignification and the evolution of tracheids in early Devonian plants. International Journal of Plant Science 164, 691-702.View article

BRAUNE, W., LEMAN, A. & TAUBERT, H. 1999. Pflanzenanatomisches Praktikum I. 8th edition. 368 pp. Spektrum Akademischer Verlag, Heidelberg.

BROWN, C.A. 1960. Palynological techniques. 188 pp. C.A. Brown, publisher, Baton Rouge, Louisiana.

DE CANDOLLE, A.P. 1816. Essai sur les propriétés médicales des plantes, comparées avec leurs forms extérieures et leur classification, 2nd edition, revue et augmentée. Crochard, Paris.View article

CHEN, Y., ZOU, C., MASTALERZ, M., HU, S., GASAWAY, C. & TAO, X. 2015. Applications of micro-Fourier Transform Infrared spectroscopy (FTIR) in the geological sciences - A review. International Journal of Molecular Sciences 15, 30223-302550.View article

CLEAL, C.J. & SHUTE, C.H. 1995. A synopsis of neuropteroid foliage from the Carboniferous and Lower Permian of Europe. Bulletin of the British Museum (Natural History), Geology Series 51, 1-52.

CLEAL, C.J. & SHUTE, C.H. 2012. The systematic and palaeoecological value of foliage anatomy in Late Palaeozoic medullosalean seed-plants. Journal of Systematic Palaeontology 10, 765-800.View article

CLEAL, C.J. & THOMAS, B.A. 1994. Plant fossils of the British Coal Measures. 222 pp. Palaeontological Association, London.

CLEAL, C.J. & ZODROW, E.L. 1989. Epidermal structure of some medullosalean Neuropteris foliage from the Middle and Upper Carboniferous of Canada and Germany. Palaeontology 32, 837-882.

CLEAL, C.J., ZODROW, E.L. & MASTALERZ, M. 2010. An association of Alethopteris foliage, Trigonocarpus ovules and Bernaultia-like pollen organs from the Middle Pennsylvanian of Nova Scotia, Canada. Palaeontographica, Abteilung B 283, 73-97.

COLTHUP, N.B., DALY, L.H. & WIBERLEY, S.E. 1990. Introduction to infrared and Raman spectroscopy. 547 pp. Academic Press, New York.

D’ANGELO, J.A. 2006. Analysis by Fourier transform infrared spectroscopy of Johnstonia (Corystospermales, Corystospermaceae) cuticles and compressions from the Triassic of Cacheuta, Mendoza, Argentina. Ameghiniana 43, 669-685.

D’ANGELO, J.A., ESCUDERO, L., VOLKHEIMER, W. & ZODROW, E.L. 2011. Chemometric analysis of functional groups in fossil remains of the Dicroidium flora (Cacheuta, Mendoza, Argentina): Implications for kerogen formation. International Journal of Coal Geology 87, 97-111.View article

D’ANGELO, J.A. & ZODROW, E.L. 2011. Chemometric study of functional groups in different layers of Trigonocarpus grandis ovules (Pennsylvanian seed fern, Canada). Organic Geochemistry 42, 1039-1054.View article

D’ANGELO, J.A. & ZODROW, E.L. 2015. Chemometric study of structural groups in medullosalean foliage (Carboniferous, fossil Lagerstätte, Canada): Chemotaxonomic implications. International Journal of Coal Geology 138, 42-54.View article

D’ANGELO, J.A. & ZODROW, E.L. 2016. 3-D chemical map and a theoretical life model for Neuropteris ovata var. simonii index fossil Asturian, Late Pennsylvanian, Canada). International Journal of Coal Geology 153, 12-27.View article

D’ANGELO, J.A., ZODROW, E.L. & MASTALERZ, M. 2012. Compression map, functional groups and fossilization: A chemometric approach (Pennsylvanian neuropteroid foliage, Canada). International Journal of Coal Geology 90-91, 149-155.View article

DARRAH, W.C. 1969. A critical review of the Upper Pennsylvanian floras of Eastern United States with notes on the Mazon Creek flora of Illinois. Privately printed. Library of Congress Catalog Card Number 74-113602. USA.

DUSTIN, C. & COOPER-DRIVER, G. 1993. Changes in phenolic production in the hay-scented fern (Dennstaedtia punctilobula) in relation to resource availability. Biochemical Systematics and Ecology 20, 99-106.View article

FAHN, A. 1979. Secretory tissues in plants. 302 pp. Academic Press, New York. FLORIN, R. 1925. Zur Kenntnis einiger Cyclopteriden des Oberkarbons. Geologiska Föreningens i Stockholm Förhandlingar 47, 223-244.View article

FORGERON, S., MACKENZIE, B. & MACPHERSON, K. 1986. The effects of geological features on coal mining, Sydney coalfield, Nova Scotia. CIM Bulletin 79(891), 79-87.

GANZ, H. & KALKREUTH, W. 1987. Application of infrared spectroscopy to the classification of kerogen types and the evolution of source rock and oil shale potentials. Fuel 66, 708-711.View article

GIBLING, M.R., LANGENBERG, W., KALKREUTH, W.D., WALDRON, J.W.F., COURTNEY, R., PAUL, J. & GRIST, A.M. 2002. Deformation of Upper Carboniferous coal measures in the Sydney Basin: evidence for late Alleghanian tectonism in Atlantic Canada. Canadian Journal of Earth Sciences 39, 79-93.View article

GOTHAN, W. 1913. Die Oberschlesische Steinkohlenflora. 1. Teil. Farne und farnähnliche Gewächse. Abhandlungen der Königlich Preussischen Geologischen Landesanstalt, Neue Folge 75.

GOTHAN, W. 1916. Über die Epidermen einiger Neuropteriden des Carbons. Jahrbuch der Königlich Preussischen Geologischen Landesanstalt 35, Teil II, 373-381.

GRESHOFF-HAAG, M. 1893. Gedanken über Pflanzenkräfte und phytochemische Verwandtschaft, Berichte der Pharmaceutischen Gesellschaft 3, 191-204.

GUO, Y. & BUSTIN, R.M. 1998. Micro-FTIR spectroscopy of liptinite macerals in coal. International Journal of Coal Geology 36, 259-275.View article

HACQUEBARD, P.A. 1984. Coal rank changes in the Sydney and Pictou coalfields of Nova Scotia; cause and economic significance. CIM Bulletin 77, 33-40.

HEGGIE, M. & ZODROW, E.L. 1994. Fractal lobatopterid frond (Upper Carboniferous marattialean tree fern). Palaeontographica, Abteilung B 232, 35-57.

HEGNAUER, R. 1986. Phytochemistry and plant-taxonomy - An essay on the chemotaxonomy of higher plants. Phytochemistry 25, 1519-1535.View article

HEITNER, C., DIMMEL, D. & SCHMIDT, J.A. 2010. Lignin and Lignans: Advances in chemistry. 683 pp. CRC Press, Taylor & Francis Group. Florida.

HEREDIA-GUERRERO, J.A., BENETÍZ, J.J., DOMÍNGUEZ, E., BAYER, I.S., CINGOLANI, R., ATHANASSIOU, A. & HEREDIA, A. 2014. Infrared and Raman spectroscopic features of plant cuticles: a review. Frontiers in Plant Science 5(305), 1-14.View article

HERNES, P.J., BENNER, R., COWIE, G., GONI, M.A., BERGAMASCHI, B.A. & HEDGES, J.I. 2001. Tannin diagenesis in mangrove leaves from a tropical estuary: A novel molecular approach. Geochimica et Cosmochimica Acta 65, 3109-3122.View article

HOFFMANN, F. 1826. Über die Pflanzenreste des Kohlengebirges von Ibbenbühren und vom Piesberge bei Osnabrück, 150-160. In KEFERSTEIN, C. (ed.) Teutschland geognostisch-geologisch dargestellt und mit Charten und Zeichnungen erläutert 4(2).

JONGMANS, W.J. 1952. Some problems on Carboniferous stratigraphy, 295-306. In 3e Congres pour l’Avancement des Études de Stratigraphie et de Géologie du Carbonifere, Heerlen 25-30 Juin, 1951. Compte Rendu 1. Ernest van Aelst, Maestricht.

KHAN, A.M., BERA, S., GHOSH, R., SPICER, R.A. & SPICER, T.E.V. 2015. Leaf cuticular morphology of some angiosperm taxa from the Siwalik sediments (middle Miocene to lower Pleistocene) of Arunachal Pradesh, eastern Himalaya: Systematic and palaeoclimatic implications. Review of Palaeobotany and Palynology 214, 9-26.View article

KLASSEN, H. (ed.) 1984. Geologie des Osnabrücker Berglandes. 672 pp. Naturwissenschaftliches Museum, Osnabrück.

KRUMBEIN, W.C. & GARRELS, R.M. 1952. Origin and classification of chemical sediments in terms of pH and oxidation-reduction potentials. Journal of Geology 52, 1-33.View article

LAVEINE, J.P. 1967. Contribution a l’étude de la flore du terrain houiller. Les Neuroptéridées du Nord de la France: 1. Flore fossiles, 5e fascicule. Études Géologiques pour l’Atlas de Topographie Souterraine, Houilleres du bassin du Nord et du Pas-de-Calais. Service géologique 1(5), 1-344.

LAVEINE, J.P. 1977. Report on the Westphalian D, 71-81. In HOLUB, V.M. & WAGNER, R.H. (eds) Symposium on Carboniferous stratigraphy. Czech Geological Survey, Prague.

LAVEINE, J.P. 1997. Synthetic analysis of the Neuropterids. Their interest for the decipherment of Carboniferous palaeogeography. Review of Palaeobotany and Palynology 95, 155-189.View article

LAVEINE, J.P., KAHLERT, E. & SCHULTKA, S. 2005. Frond architecture of two specimens of the pteridosperm Laveineopteris rarinervis from the Late Carboniferous (early Westphalian D) of Piesberg near Osnabrück (Germany): morphological implications. Revue de Paléobiologie 24, 489-504.

DE LEEUW, J.W., VERSTEEGH, G.J.M. & VAN BERGEN, P.F. 2006. Biomacromolecules of algae and plants and their fossil analogs. Plant Ecology 182, 209-233.View article

LIN, R. & RITZ, G.P. 1993a. Reflectance FT-IR microspectroscopy of fossil algae contained in organic-rich shale. Applied Spectroscopy 47, 265-271.View article

LIN, R. & RITZ, G.P. 1993b. Studying individual macerals using i.r. microspectroscopy, and implications on oil versus gas/condensate proneness and “low-rank” generation. Organic Geochemistry 20, 695-706.View article

LUCAS, P.W., TURNER, I.M., DOMINY, N.J. & YAMASHITA, N. 2000. Mechanical defenses to herbivory. Annals of Botany 86, 913-920.View article

LYONS, P.C., FINKELMAN, R.B., THOMPSON, C.L., BROWN, F.W. & HATCHER, P.G. 1982. Properties, origin and nomenclature of rodlets of the inertinite maceral group in coals of the Central Appalachian Basin, U.S.A. International Journal of Coal Geology 1, 313-346.View article

LYONS, P.C. & LAVEINE, J.P. 2005. Association of entire orbicular cyclopterids with Neuropteris ovata pinnate foliage from the Late Pennsylvanian (Stephanian) of West Virginia, USA: taxonomical implications. Revue de Paléobiologie 24, 505-514.

LYONS, P.C., OREM, W.H., MASTALERZ, M., ZODROW, E.L., VIETH-REDEMANN, A. & BUSTIN, R.M. 1995. 13CMR, micro-FTIR and fluorescence spectra, and pyrolysis-gas chromatograms of coalified foliage of late Carboniferous medullosan seed ferns, Nova Scotia, Canada: Implications for coalification and chemotaxonomy. International Journal of Coal Geology 27, 227-248.View article

MANDELBROT, B.B. 1983. The fractal geometry of nature. 498 pp. W.H. Freeman & Co., New York.

MIRANDA, V., BAKER, N.R. & LONG, S.P. 1981. Anatomical variation along the length of the Zea mays leaf in relation to photosynthesis. New Phytologist 88, 595-605.View article

NIKLAS, K.J. 1992. Plant Biomechanics: An engineering approach to plant form and function. 622 pp. University of Chicago Press, Chicago.

DE OLIVEIRA PLOTZE, R., FALVO, M., PÁDUA, J.G., BERNACCI, L.C., VIEIRA, M.L.C., OLIVEIRA, G.C.X. & BRUNO, O.M. 2005. Leaf shape analysis using multiscale Minkowski fractal dimension, a new morphometric methods: a study with Passiflora (Passifloraceae). Canadian Journal of Botany 83, 287-301.View article

PETERSEN, H.I. & NYTOFT, H.P. 2006. Oil generation capacity of coals as a function of coal age and aliphatic structure. Organic Geochemistry 37, 558-583.View article

PETERSEN, H.I., ROSENBERG, P. & NYTOFT, H.P. 2008. Oxygen groups in coals and alginite-rich kerogen revisited. International Journal of Coal Geology 74, 93-113.View article

ROCHLEDER, F. 1854. Phytochemie, 257-308. Über den Zusammenhang zwischen der Form and Zusammensetzung der Gewächse, 3. Abschnitt. Wilhelm Engelmann, Leipzig.

ROTHWELL, G.W. 1985. The role of comparative morphology and anatomy in interpreting the systematics of fossil gymnosperms. The Botanical Review 51, 319-327.View article

SALTZWEDEL, K. 1968. Revision der Imparipteris ovata (Hoffmann) Gothan, ihre Lebensdauer und stratigraphische Bedeutung in den westeuropäischen Varisziden. 169 pp. Inaugural Dissertation, Universität von Münster, Münster.

SALTZWEDEL, K. 1969. Revision der Imparipteris ovata (Hoffmann) Gothan. 1. Teil: Typus- und Typoid-Material vom locus typicus. Argumenta Palaeobotanica 3, 131-162.

SEIGLER, D.S. 2012. Plant secondary metabolism. 759 pp. Springer Science & Business Media, New York.View article

SHUTE, C.H. & CLEAL, C.J. 2002. Ecology and growth habit of Laveineopteris: a gymnosperm from the Late Carboniferous tropical rain forests. Palaeontology 45, 943-972.View article

ŠIMŮNEK, Z & CLEAL, C.J. 2016. The systematic and palaeoecological significance of Neuropteris ovata (Medullosales) cuticles from the Stephanian Stage of the Puertollano Basin, Spain. Spanish Journal of Palaeontology 31, 231-244.

SMITH, B.C. 1996. Fundamentals of Fourier transform infrared spectroscopy. 202 pp. CRC Press, New York.

SMITH, T.G., LANGE, G.D. & MARKS, W.B. 1996. Fractal methods and results in cellular morphology - dimensions, lacunarity and multifractals. Journal of Neuroscience Methods 69, 123-136.View article

STACE, C.A. 1984. The taxonomic importance of the leaf surface, 67-94. In HEYWOOD, H. & MOORE, D.M. (eds) Current concepts in plant taxonomy. Systematics Association, London (Special Volume 25). Clarendon Press, Oxford.

STAFLEU, F.A. 1966. Brongniart’s Histoire des Végétaux fossiles. 2 vols 1828-1837. Reimpression A. Asher & Co., Amsterdam 1965.

TRAVERSE, A. 2008. Paleopalynology. Second edition. 813 pp. Springer, Berlin.View article

WAGNER, R.H. 1984. Megafloral zones of the Carboniferous. Compte Rendu 9e Congres de stratigraphie et de géologie du Carbonifere (Washington-Urbana, 1979) 2, 109-134.

WERNER-ZWANZIGER, U., BANGHAO CHEN, & ZODROW, E.L. 2009. 13C NMR study of gymnospermous cuticles and associated coals from Late Pennsylvanian seed ferns and cordaites. Poster 341, 50th Experimental Nuclear Magnetic Resonance Conference, Asilomar, CA, USA, March 29-April 3, 2009.

WESTAD, F. 2002. Parsimonious models in chemometrics. The North American Chapter of the International Chemometrics Society, Newsletter 22, 10-13.

WHEELER, Q.D. 2008. The new taxonomy. 256 pp. CRC Press, New York.View article

ZODROW, E.L. & CLEAL, C.J. 1985. Phyto- and chronostratigraphical correlations between the late Pennsylvanian Morien Group (Sydney, Nova Scotia) and the Silesian Pennant Measures (south Wales). Canadian Journal of Earth Sciences 22, 1465-1473.View article

ZODROW, E.L. & CLEAL, C.J. 1988. The structure of the Carboniferous pteridosperm frond Neuropteris ovata Hoffmann. Palaeontographica B 208, 105-124.

ZODROW, E.L. & D’ANGELO, J.A. 2013. Digital compression maps: an improved method for studying Carboniferous foliage. Atlantic Geology 49, 126-130.View article

ZODROW, E.L., D’ANGELO, J.A., MASTALERZ, M. & KEEFE, D. 2009. Compression-cuticle relationship of seed ferns: Insights from liquid-solid states FTIR (Late Palaeozoic-Early Mesozoic, Canada-Spain-Argentina). International Journal of Coal Geology 79, 61-73.View article

ZODROW, E.L., D’ANGELO, J.A., TAYLOR, W.A., CATENALI, T., HEREDIA-GUERRERO, J.A. & MASTALERZ, M. 2016. Secretory organs: Implications for lipoid taxonomy and kerogen formation (seed ferns, Pennsylvanian, Canada). International Journal of Coal Geology 167, 184-200.View article

ZODROW, E.L., D’ANGELO, J.A., WERNER-ZWANZIGER, U. & BANGHAO, C. 2014. Hair-trichomes-files, and spectrochemistry of Macroneuropteris scheuchzeri (Basal Cantabrian, Sydney Coalfield, Canada). Palaeontographica B 290, 141-153.

ZODROW, E.L., HELLEUR, R., WERNER-ZWANZIGER, U., BANGHAO, C. & D’ANGELO, J.A. 2013. Spectrochemical study of coalified Trigonocarpus grandis (Pennsylvanian tree-fern ovule, Canada): Implications for fossil-organ linkage. International Journal of Coal Geology 109-110, 24-35.View article

ZODROW, E.L. & MASTALERZ, M. 2001. Chemotaxonomy for naturally macerated tree-fern cuticles (Medullosales and Marattiales), Carboniferous Sydney and Mabou Sub-Basins, Nova Scotia, Canada. International Journal of Coal Geology 47, 255-275.View article

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.View article

ZODROW, E.L., MASTALERZ, M., WERNER-ZWANZIGER, U. & D’ANGELO, J.A. 2010. Medullosalean fusain trunk from the roof rocks of a coal seam: Insight from FTIR and NMR (Pennsylvanian Sydney Coalfield, Canada. International Journal of Coal Geology 82, 116-124.View article

ZODROW, E.L., ŠIMŮNEK, Z. & BASHFORTH, A.R. 2000. New cuticular morphotypes of Cordaites principalis from the Canadian Carboniferous Maritimes Basin. Canadian Journal of Botany 78(2), 135-148.View article