Transformative Paleobotany : Papers to Commemorate the Life and Legacy of Thomas N. Taylor [1 ed.] 9780128130124, 0128130121, 9780128130131, 012813013X

Table of contents :
EARLY LAND PLANTS: INNOVATIONS AND ADAPTATIONS 1. The evolutionary origin of the plant spore in relation to the antithetic origin of the plant sporophyte 2. Early Devonian woody plants and implications for the early evolution of vascular cambia 3. Using architecture modeling of the Devonian tree Pseudosporochnus to compute its biomass 4. The advantages and frustrations of a plant Lagerstatte as illustrated by a new taxon from the Lower Devonian of the Welsh Borderland, UK 5. Early Tracheophyte Phylogeny: A Preliminary Assessment of Homologies LATE PALEOZOIC AND MESOZOIC PLANTS AND FLORAS 6. Lower Permian flora of the Sanzenbacher Ranch, Clay County, Texas 7. Permian ginkgophytes of Angaraland 8. Glossopterid plant remains in permineralization: What do they tell us? 9. Pachytestopsis tayloriorum gen. et sp. nov., an anatomically preserved glossopterid seed from the Lopingian of Queensland, Australia 10. A Triassic Mystery Solved: Fertile Pekinopteris from the Triassic of North Carolina, U.S.A. 11. Enigmatic, structurally preserved stems from the Triassic of central Europe: A fern or not a fern? PALEOBIOGEOGRAPHY, BIOLOGY, AND PHYLOGENETIC RELATIONSHIPS OF PLANTS 12. A comprehensive assessment of the fossil record of liverworts in amber 13. Aerodynamics of Fossil Pollen: Implications for Understanding Pollination Biology in Extinct Plants 14. Escapia gen. nov.: Morphological evolution, paleogeographic diversification, and the environmental distribution of marattialean ferns through time 15. Heterosporous ferns from Patagonia: The case of Azolla 16. Why are bryophytes so rare in the fossil record? A spotlight on taphonomy and fossil preservation 17. Fossil seeds with affinities to Austrobaileyales and Nymphaeales from the Early Cretaceous (early to middle Albian) of Virginia and Maryland, U.S.A: new evidence for extensive extinction near the base of the angiosperm tree FOSSIL MICROORGANISMS 18. Reactive Oxygen Defense Against Cellular Endoparasites and the Origin of Eukaryotes 19. Fossils of arbuscular mycorrhizal fungi give insights into the history of a successful partnership with plants 20. Looking for arbuscular mycorrhizal fungi (AMF) in the fossil record - an illustrated guide 21. Exceptional preservation of sessile, long-stalked microorganisms in the Lower Devonian Windyfield chert (Scotland) 22. Morphological convergence in forest microfungi provides a proxy for Paleogene forest structure 23. Ediacarans, protolichens, and lichen-derived Penicillium: A critical reassessment of the evolution of lichenization in fungi ANTARCTIC PALEOBOTANY 24. Polar Regions of the Mesozoic-Paleogene greenhouse world as refugia for relict plant groups 25. Leaf venation density and calculated physiological characteristics of fossil leaves from the Permian of Gondwana 26. Functional significance of cambial development in Vertebraria roots: How do unusual xylem traits serve life at a high latitude? 27. Cretaceous to Paleogene vegetation transition in Antarctica

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Papers to Commemorate the Life and Legacy of Thomas N. Taylor Edited by Michael Krings SNSB-Bavarian State Collection for Pa laeontology and Geo logy Munich, Germany Ludvvig-Maxin1il ians-U niversitat Munchen Muni ch, Germany The Univers ity of Kansas La\vrence, Kansas, United States

Carla

J. Harper

The University of Kansas La\vrence, Kansas, United States SNSB-Bavarian State Collection for Pa laeonto logy and Geo logy Muni ch, Germany

Nestor Ruben Cuneo Museo Paleontol6gico Egidio Ferugl io, and National Research Counci l of Argentina Trelew, Chubut, Argentina

Gar W. Rothwell Oh io Univers ity Athens, Ohio, U nited States O regon State University Corvallis, Oregon, United States

ACADEMIC PRESS An in1print of Elsevi er

ELSEVIER

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Academic Press is an impri nt of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdo1n 525 B Street, Suite 1650, San Diego, CA 92101, United States 50 Hampshire Street, 5th Floor, Cambridge, Iv1A 02139, United States The Boulevard, La ngfo rd Lane, Kidli ngto n, Oxford O X5 J GB, Uni ted Kingdon1 Copyright © 20 18 Elsevier Inc. All rights reserved. No pan of this pu blication may be reprod uced or trans1nitted in any fonn or by any 1neans, electronic or 1nechanical, including photocopying, recording, or any infonnation storage and retrieval system, withou t pennission in writing fro1n the publisher. Details on ho\v to seek pern1issio n, fu rther inforn1 atio n about the Pu blisher's pern1issions policies and our arrangen1ents with organi zatio ns such as the Copyright Clearance Center and the Copyri ght Licensing Agency, ca n be foun d at ou r webs ite: \ V"W\V .elsevier .con1/penn.issions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as n1ay be noted herein).

Notices Kn owledge and best practice in this field are constantly changi ng. As new resea rch and experience broaden ou r understandi ng, changes in research n1ethods, professional practices, or n1edical treatrn ent n1 ay becon1e necessary. Practiti oners and researchers 1nust always rely on their O\ Vll experience and kno\vledge in evaluating and using any infonnation, 1nethods, co,npounds, or experi.Inents described herein . In usi.I1g such infonnation or 1nethods they should be 1nindful of thei.I" O\ Vll safety and die safety of others, i.I1cluding parties for who1n they have a professional responsibility. To the fullest extent of the Jaw, neither the Publisher nor the authors, contribu tors, or edi tors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or other•Nise, or from any use or operation of any n1ethods, products, instructions, or ideas contai ned in the material herein.

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Contents Contributo rs About the Editors Fo re\.vord Ac kn owledgments

XII I XVI I

. XXI

2. Early D evonian Woody Plants and Implications for the Early Evolution of Vascular Cambia

XXV

Patricia G. Gensel 1.

2.

Section I

2 .1

Early Land Plants: Innovations and Adaptations

3.

1. The Evolutionary Origin of the Plant Spore in Relation to the Antithetic Origin of th e Plant Sporophyte Paul K. Strother, Wilson A. Tavlor ,

1.

2.

3.

Introduction The Antithetic Theory as a Scaffold for Interpreting the Fossil Record of the Algal-Plant Transition Early Cryptospore Morphology

3 .1 3.2 3.3

3 .4

4.

5.

6.

7.

Introduction Background

Sporogenesis and Cryptospore M orpho logy Early Cryptospore Topology Spo re \Nal I Topology in Relation to the Sporopol lenin Tra nsfer H ypothesis The Evolutionary Developn1ental and Morpho logica l Significance of La mi nated Spore Wal l Structure

Cryptospores and the Origin of Meiosis in Plants The Stratigraphic Record of the Cryptospores as a Record of Sporophyte Evolution Interpreting Ordovician-Silurian Phytodebris as a Record of Sporophyte Evolution Conclusion Acknowledgments References

Plants W ith Secondary Xylem : Prel im inary Data

4. 5.

Comparisons Discussion

5.1 5.2 5.3

6 6

8

5.4 5.5

9

6. 1I 13

15

17 18 18 18

Previously Descri bed Occurrences of Secondary Xy lem in Fossi l Plants

22 Previously Described Early Devonian Taxa 22 3 .1 Armoricaphyton chateaupannense 23 U nnamed New Brunswick Plant A: 3.2 24 Prelirninary Data 3 .3 Franhueberia gerriennii, Ernsian, Gaspe 26 3.4 Additional Occurrences of E1nsian

3

4

21 21

lmpl icatio ns Evo lut io n of Cambiun1 lnfo rn1ati o n From D evelopn1ental Studies Psilophyton- One Taxon o r Several? Size is Decoupled Fro m Secondary Tissues in These Ear ly Plants

Conclusions Acknowledgments References

26 29 30 30 31 31 32

32 32 32 32

3. Using Architecture M odeling of the Devonian Tree Pseudosporochnus to Compute Its Biomass Anae1le Dambreville, Brigitte M eyer-Berthaud, Jean-Franc;ois Barczi, Anne-Laure Decon1beix, Sebastien Griffon, Herve Rey 1.

2.

Introduction Material

35 36

V

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vi

Contents

3.

Modeling Pseudosporochnus With AmapSim

3 .1 3.2

AmapSirn Software

Pseudosporoc hnus

37

3.3

38

3.4

Pseudosporochnus Pseudosporochnus

4.2

Biornass of a Tree Biomass of a Stand

6.

6.2 6.3

Con1puter Models of Fossil Plant A rchi tecture Model Accuracy Carbon A l location i n

Pseudosporochnus 6.4 7.

5.5

40

Acknowledgments References

Forest Biomass

Conclusions Supplementary Figure Acknowledgments References

40

2.

2 .1 2.2 3.

Geological Backgrou nd Note,vorthy Advances by Previous St udies

New Research 3. I Material and Methods

3.2 3.3 3.4

Morphology and Anatornica l Descriptions Comparisons and Systern atics Functional, Physiological, and Evolutionary Conundrurns

64 64 64 65 65

41 42 42 42

A Preliminary Assess,nent of Homol ogies Williarn L. Crepet, Karl J. Nik/as

1. 2.

Introduction Materials and Methods 2. I

2.2 43 44 45

46 46 46

2.3 3. 4.

4.2 4.3 4.4

5.

Taxa Selection Characters and Character Assignments Algori thn1s and Ph ilosophy

Results Discussion 4 .1

Jennifer L. Morris, Dianne Edwards, John 8. Richardson Introduction Geological Background and Previous Research

62 63 63 63 63

5. Early Tracheophyte Phylogeny:

4. The Advantages and Frustrations of a Plant Lagerstatte as Illustrated by a New Taxon From the Lower Devonian of the Welsh Borderland, UK

1.

61 61

40

Carbon A l location i n Carbon Content and Biomass of a Con1n1unity of Pseudosporochnus

New Localities Bu lk Maceration and Sorting Comprehensive Compari sons W ith the D ispersed Spore Record Technological Advances in A naton1 ica I Investigations Geochemical A pproaches

40

of

Discussion

6.1

5.4

Pseudosporochnus

Simu lating the Growth

Taphonomy Con1parisons Between D iffere nt Preservation Types Diversity

Future Research

5 .1 5.2 5.3

40

Pseudosporochnus 5.3

5.

Pseudosporochnus

Pseudosporochnus 5.2

4.3

40 40

Results 5. I

4 .1

Physiologica l

Computing Biomass

The Lirnitations of Charcoalified Lagerstatten

4.2

Unit Geometrical Parameters of

4. 1

5.

36 36

A rchitectural

Age Indexi ng 4.

4.

An Incomplete Fossi I Record An Insuffic ient Nurnber of Charac ters and Character States Rapid Radiations and Mosa ic Evolution The Problern of Honiology

Conclusions Appendices References Further Reading

69 70 70

70 76 76 79 81 82 82 82

88 88

91 92

49

52 52 53 54 54

Section 11 Late Paleozoic and Mesozoic Plants and Floras 6. Lower Permian Flora of the Sanzenbacher Ranch, Clay County, Texas

54 59

William A. DiMichele, Robert· W. Hook, Hans Kerp, Carol L. Hotton, Cindy V. Looy, Dan S. Chaney

60 1. 2.

Introduction Geology

95 95

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Contents

3. 4.

Collections Methods

4.1 4.2

s.

Results

5 .1 5 .2 6.

Taxonomic Composition of the Flora Quantitative Compositi on of the Flora

Discussion

6.1 6.2 6.3 7.

Macrofossils M ic rofossi ls

Collect ing Macrofl ora- Pa ly noflora (~o,npari son Broader Context of the Sanzenbacher Flora

Conclusions Acknowledgments References

97 98 98 101 103

9. Pachytestopsis tayloriorum ge n. et sp. nov., an Anatomically

103

Stephen Mcloughlin, Benjamin Bornfleur, Andrew N. Drinnan

114 117 117 120 121 123 124 124

Preserved G lossopterid Seed From the Lo pingian of Queensland, Australia

1.

2. 3. 4.

5.

1.

5.3 5.4 5.5 6.

2. 3.

4.

5.

Introduction Historical Background Materi al and Methods Results

127 130 130 131

4.1 4.2 4.3 4.4 4.5

131

Leaves of Psygmophyllo ids Sphenobaiera-L ike Leaves Grovvth Forms Fen,ale Reproductive ()rgans Male Fru cti fications/Pol Iin i ferous Organs

Discussion Acknowledgments References

133 133 137 137 139 141

Introduction Geological Setting Material and Methods Results Discussion

5 .1 5.2

7. Permian Ginkgophytes of Angaraland Serge V. Naugolnykh

Conclusions Acknowledgments References Appendix 1

1.

2. 3.

Introduction Geological Setting Material and Methods Discovery and Nature of the 3 .1

179 180 180

Specin1ens Preservat io n and M ethod s of Analysis

180

8. G lossopterid Plant Remains in 4. 5.

2. 3.

4.

Introduction Material and Methods Results Discussion

4.1

4.2

Comparison VVith Previously Described, Anatomi cal ly Preserved G lossopteri d Ovulate Structures and Ovu les Morpho logical Comparison of Glossopterid and Angiospern, Reproductive O rgans

Acknowledgments References

Systematic Paleontology Discussion

5 .1 5.2

Harufurni Nishida, Kathleen B. Pigg, M elanie L. Devore 1.

145

166 172 172 175 175 176 176 178

Brian Ax.smith, Judith Skog, Christian Pott

3 .2

Tell Us?

Affinities of t he Seeds Cornpari son With Other Pern1 ian Gondwanan Seeds (~ lossopterid Seed Character States Associated Pollen Taphonomy

155 155 156 156 165 165

10. A Triassic Mystery Solved : Fertil e Pekinopteris From th e Triass ic of North Carolina, United States

141

Permineralization : Wh at Do Th ey

vii

6.

146 146

Structure and Li fe H istory Con,parisons and Potential Phylogenetic lmpl ications

Conclusion Acknowledgmentu,'i asropcK1'1M npasoM

About the Editors

Michael Krings is the curator for fossil plants at the Bavarian State Collection for Palaeontology and Geology (SNSB-BSPG) in Munich, Germany, and a professor of plant paleobiology at the Ludwig-Maximilians-University Munich. He also holds an affiliate faculty position in the Departn1ent of Ecology and Evolutionary Biology at the University of Kansas. He received his PhD in botany fron1 the University of Munster, Germany, and was an Alexander von Humboldt-Foundation postdoctoral fellow at the University of Kansas. He is author of the paleobotany textbook Paleohotany. The Biology and Evolution of Fossil Plants (T.N. Taylor, E.L. Taylor & M. Krings, 2009) and the paleomycology book Fossil Fungi (T.N. Tay lor, M. K rings & E.L. Taylor, 20 I 5). His research interests include Carboniferous, Permian, and Triassic seed plants and the biology and ecology of microorganisms in ancient ecosystems.

Nestor Ruben Cuneo is the Museo Paleontol6gico Egidio Feruglio director and principal researcher of the National Research Council, Trelev,1, Chubut, Argentina. He also was an invited researcher for several years at the U.S. Antarctic Program and invited professor at the University of Patagonia. He received his PhD in geology from the Universidad de Buenos Ai.res, Argentina, and had a postdoctoral position at Ohio State U niversity under the guidance of Thomas N. Taylor. His research interests center on Gondwanan paleofloras, Patagonian Jurassic floras, and, 1nore recently, Cretaceous ecosystems.

Carla J. Harper is a National Science Foundation (NSF) Zygomycetes Genealogy of Life (ZyGoLife)- the Conundrum of Kingdon1 Fungi postdoctoral research fellow at the Biodiversity Institute and Natural History Museu1n at the University of Kansas. She ,vas an Alexander von Hu111boldt-Foundation postdoctoral research fellow (2015- 17) at the Bavarian State Collection for Palaeontology and Geology (SNSB-BSPG) and LudwigMax in1ilians-University Munich, Gern1any, and currently holds a research associate position at SNSB-BSPG. She received her PhD in ecology and evolutionary biology from the University of Kansas. Her research interests include the biology and ecology of 111icroorganisms and biotas in Pennian- Jurassic ecosysten1s of Antarctica and late Paleozoic of Europe, symbiotic systems through time, as well as the biology, geochemistry, and evolution of fossil tnicrobes.

Gar Rothwell is the Edwin and Ruth Kennedy Distinguished Professor of Environmental and Plant Biology, Emeritus, Ohio University, and Courtesy Professor of Botany and Plant Pathology, Oregon State University. He is past-president of the International Organisation of Palaeobotany, author of the paleobotany textbook Paleobotany and the Evolution of Plants (W.N. Stewart & G. W. Roth,vell, 1993), and editor of six previous volumes of studies in plant paleontology. His research focuses on the role of development in evolution and on the patten1s of organismal evolution and phylogeny among land plants, particularly lycophytes, equisetophytes, fe1ns, and seed plants. ••

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Thomas N. Taylor (1937- 2016)

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Foreword As natural history has progressively given way to newer approaches and avenues of inquiry in the fields of biology and geology during tbe past 60 years, the field of paleobotany has grown as a vibrant source of innovative science. To a certain extent, this resulted from the irreplaceable nature of data fi·om the fossil record. Of perhaps greater irnportance, this period has witnessed an unprecedented strea1n of new paleobiological approaches and techniques that have energized collaborative efforts \Vith a wide array of other disciplines. Together, these innovations have dramatically transformed traditional paleobotanical studies, fostered creative fusions of disciplines, and produced whole ne\V avenues of scientific inquiry. At the forefront of these transfonnative innovations are the studies of Thon1as N. (Torn) Taylor, \Vhose scholarship, insightful contributions, and scientific impact this cornpendiurn celebrates. Of perhaps even greater significance than the voluminous research personally developed and conducted by To1n Taylor are the colleagues he has inl'luenced and students he has inspired to extend our understanding of the evolution of life and to chrut the forthcoming directions of paleobiological research for the 21st century. Moreover, Ton, was transformative in b1inging together ideas and colleagues ti·om different disciplines to approach paleobotany. He also had foresight in rnany areas; while he certainly was not the first to explore the topics of paleomycology or Antarctic paleobotany, he brought those areas to the forefront because he knew at the ti1ne that they had tremendous potentiaJ, and he brought people together beyond the traditjonal boundaries. We envisage the present volun,e as a con1panion to T'Cim's most recent Paleobotany and Fossil F'ungi books and to exen1plify the vast body of accun1ulated research that is derived from Tom's influence. T he included report.s define and su1nmarize the breadth of scholarship that has result.eel fro1n Tom's scientjfic conl!ibutions to organisn1al and evolutionary biology, to the early evolution of land plants, to our understand.ing of fossil fu ngi and other rnicroorganisms, to syste1n atics and phylogeny of p lants and fungi, to biostratigraphy, to the evolution of organisn1al interactions, and to palynology and ultrastructure. The volun1e is divided into five sections to emphasize the most pron1jsing avenues of investigation that Ton, has

opened and to highlight the fruitful contributions that his influence has engende1:ed.

I. Early land plants: innovations and adaptationsUnanswered fundarnental questions about the origin and early evolution of land plants underlie Tom Taylor's overall scientific interests . From his earliest studies on the evolution of prin1jtive seeds, through his contributions to the evolution of spore and pollen ultrastructure, to bis pioneeriug work on the paleontological progression of plant/ microorganism interactions, his contributions have redefined the focus of early land plant studies. Ton1's en1phasis on evolutionary changes in structure/ultrastructure of Paleozoic spores is extended by Strother and W .A. Taylor, who use early Paleozoic evolution of e1nb ryophyte spores to e1nphasize life cycle changes leading to the origin of the sporo phyte phase of the plant life cycle. The roles of key evolutionary innovations in tissue development such as the vascular cambitun and in the architecture of the sporophyte and gametophyte plant bodies \Vere 1najor emphases of T·on,'s research. ,\dvancements are extended by Gensel's focus on the origin of wood in Early Devortiru1 plants, the architectural analysis of a Middle Devonian fern-like tree by Da1nbreville et aJ ., and the characterization of a plant ti·om a Lower Devonian Lagerstatte in the Welch Borderlands by Mo1Tis et al. As ernphasized by Ton1's focus on early land plant evolution, studies of these types rely heavi ly on our understanding of basic homologies, which is the focus of the final contribution in this section by Crepet and Niklas.

II. Late Paleozoic and Mesozoic plants and floras\Vhen Ton1 started to work in paleobotany, it \Vas not early land p lants or rnicrobial interactions he laid his eyes on, but rather the vast record or plant remains fro1n the late Paleozoic and i\1esozoic of North An1erica and Europe that were readily accessible in great nu1nbers, especially in the fonn of coal balls providing detailed insights into the internal organization and biology of Carboniferous coal swa1np plants. He stud.ied vruious fc111s and sphenophytes but then found the reproductive biology of late Paleozoic seed plants fascinat ing and wor'ked on Carboniferous seeds and pollen organs. The reports in this section emphasize Ton1's interest in the diversity and biology of vascular cryptogarns and seed plants in late Paleozoic and Iv1esozoic

.

XXI

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xxii

Foreword

ecosysten1s. DiMichele et al. describe an Early Pennian flora fron1 Clay County, Texas, v.1 hile Naugolnykh discusses the astonishingly diverse early foss il record of (putative) ginkgophytes in Angaraland. The third contribution in this section, by Nishida et al., discusses the value of pe1mineralized glossopte1idalean plant ren1ains, and the fou 1th, by M cloughlin et al., harks back to Toni' s interest in seed structure by describing a new glossopteridalean seed fron1 Australia and naming it in honor of To1n. The last tv.10 reports in this section focus on plants that have reinained rnysteries since their first discovery and description. Axsmith et al. resolve the systen1atic affinities and reproductive biology of Pekinopteris based on fertile 111aterial fro1n the North American Triassic, while Galtier et al. provide ev idence suggesting that the pennineralized stem Knorripteris fron1 the Triassic of central Europe belongs to the ferns .

ill. l'aleobiogeography, biology, and phylogenetic relationships of plants-One o f Tom's greatest conaibutions to the fi eld was the integration of ideas and people fro1n different fie lds of science to help answer paleobotanical questions and explain paleobotan ical discoveries. Therefore, it cornes as no surprise that one of the sections in this book brings together interdisciplinary studies with a focus on paleobotany concerning a wide range of different plant g roups and thei r dis tri bution in tin1e and space. The section is headed by a report by He inrichs et al. on the fossil record of liverworts in arnber and the value of these fossils in phylogenetic and tnolecu Jar clock analyses. Aerodyna1nics of fossil pollen (by Grega et al.) then shifts the focus to the connection between reproductive biology and biomechanics by assessing the aerodynamic effects of certain pollen characters through electron microscopy, 1nathen1atical mode ling, and experiments using scaled-up physical 1nodels. Rotl1\veJ1 et al. su1nn1arize and elaborate on the 1norpbological evolution, paleogeograpbic diversification, and environrnental distribution of rnarattialean ferns through time based on a new genus, Escapia, from the Early Cretaceous Apple Bay flora of Canada. The paleogeographic distribu tio n of certain ferns throug h tin1e is also the focus of the next repott (by De Benedetti et al.) that surveys the fossil record of Azolla in Pat.agonja. An entirely different question, raised by Tornescu et al., is connected then1atically with the first paper of the section by addressing the overall scarcity of bryophytes in the fossil record . Finally, Friis et al. describe Early Cretaceous seeds of North A.tnerica with affinities to Austrobaileyales and Ny111phaeales that provide new evidence for extensive extinction near the base of the angiospern1 tree. IV. Fossil microorganisms-Exanunation, description, evaluation, and biological characterization of microorganis,ns, especially fungi and fungus-like organisms and their various levels of biological interactions with plants, ani1nals, and other 1nicroorganisn1s frorn the Lower Devonian

Rhynie chert and other sources of histological preservation, \Vere an1ong To,n's favo ri te topics during the later years of his career. Microorganis1n s are key drivers in past and present-day ecosysten1s, and other organisrns wou ld not exist in the way they do without 1nicroorganisn1s. As a result, understanding the evolution of fossil plants for Torn required detailed attention to the microorganisn1s associated with the plants. Note\vo1thy an1ong To,n's 1nany contributions on Rhynie chert 1nicroorganis1n s, which he first studied with Winifred Re1ny of 1\1i.inster, Gern1any, are the accounts on the endon1ycorrhizas in sporophytes and garnetophytes of the land plant Aglaophyton majus. Because the Rhynie che,t ,vas one of To,n 's greatest scientific affections, it is not surprising that one of the contributions in this section (by Krings et al.) presents new findings fron1 the Rhynie chert and the nearby, coeval \Vindyfield chert, \vbile another, by Brundrett et al., uses the fossil record of arbuscular rnycorrhizas to elucidate the history of this successful partnership between fu ngi and plants. The next contribution, by Walker et al., looks at the characteristics of present-day mycorrhizas and 1nycorrhizal fung i, and the chances of recognizing these characteristics in fossils . Moreover, To1n's 1997 report on the Rbynie chert lichen ~Vinfrenatia reticul.ata represents a benchtnark contribution in the field of lichen evolution. The contribution by Li.icking and Nelson in this section takes the discussion of the orig in and early evolution of lichen syn1bioses yet a step further. T he two rernaining contributions in this section are great exarnples of how cooperation between paleobiologists and neonlicrobiologists has produced intellectual cross-fertilization resulting in an expanded knowledge base about the evolutionary history of eukaryotes (by \Vhi te et al.) and Paleogene forest structure (by Rikkinen and Schn1idt). V. Antarctic palcobotany-Tbe diversity of fossil rernains fro1n A11tarctica and the excellence of preservation of rnany of these fossils at sorne point caught Torn T aylor' s interest and, in the course of several expeditions to "the ice" that he and his wife Edie planned and conducted, Antarctica and Antarctic paleobotany developed into one of 'forn' s great scientific love affairs. Pernlian and Triassic chert (pennineralized peat) deposits fron1 A.t1tarctjca represent a particularly interesting setting for the study of plants and fungi because they preserve remains of distinctive high-latitude ecosystems with polar light regimens that underwent a profound climatic change fro,n icehouse to greenhouse conditions. Two of the conributions in this section focus on plants fro1n these cherts that were also studied by Torn. The first report assesses developrnental biology in glossopteridalean roots named Vertebraria (by Decombeix et al.). T\vo additional reports in this section deal with pe,iods of geological time that were not the p1irn ary focus of T·orn's work but that also have yielded nu1nerous and valuable fossils frorn A.t1tarctjca. Bornfleur

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Fo re word

et al. provide evidence of the function of polar regions of the tvlesozoic to Paleogene greenhouse world as refugia fo r rel ict p lant groups, including lycopsids, various "seed ferns," Bennettitales, and chei ro lepid conifers, wh ile Cantrill surveys the Cretaceous to Paleogene vegetation transition in Antarctica. Finally, Schv.1endernann investigates leaf venation density and calculated physiological characteristics of foss il leaves fron1 the Pern1ian of Gondwana. Paleobotany today is a highly integrated interdiscip linary endeavor. A paleobotanist 50 years ago needed only geology and plant biology to study fossil plants. However,

...

XXIII

"ve nO\V realize that research areas such as geochen1istry, n1olecular biology, n1icrobiology, biornechanics, phy logeny, etc. are transforn1ing our approaches to, and perception of, the analysis of fossi l plants and ecosyste,ns, and some of these once-so-rernote research areas are becorning increasingly in1portant for, and integral parts of, paleobotanical research. The present volu1ne exe1nplifies the potential of utilizing interdisciplinary research in the advancen1ent of paleobiological inquiry. As such, the volume represents a blueprint for paleobotany of the 21st century.

Marep1,1an, 3a1141,1114eHH1>u,'i asropcK1'1M npasoM

Acknowledgments We are deeply indebted to all ~rho, by contributing thei_r research , have filled this volu.n1e with life and provided a worthy fra1ne for the co1n1nemoration of Tom's life and legacy. We thank all chapter referees for their help and our colleagues, families, and f1iends for their unconditional support and loyalty . S .R. Ash • B.A . Atkinson • B .J . Axsn1ith • D .J. Batten • J.-F . B arczi • F . Baron • J . Bechteler • C.B . Beck • J'vl. Bergen • H.K. Bergernan • C.M. Berry • i\ .C. Bippus • B. Bo1nfleur • C.K. Boyce • P. Blomenkemper • L. Brindisi • M.C. Brundrett • D .J. Cantrill • D.S. Chaney • X . Chang • X . Chen • l\1.E. Collinson • P.R . Crane • D .J. Crawford • W .L. Crepet • C .P. Daghlian • A . Dan1brevillc • V . Daviero-Gomez • J .R. Dav is • F . De Benedetti • A .-L. Decombeix • T . Delevoryas • 1'1.L. De Yore • J. Dighton • W.A. Dil\1ichele • N. Dotzler • A.N . Drinnan • J.G. Duckett • D. Ecl\vards e l.H. Escapa • K . Feldberg • J'vl.J. Foster • E .-J'vl. Friis • J. Galt.ier • M .A . Gandolfo • J . G·arcfa Massini • P.G. Gensel • P. Genienne • L . Grega • S. G1i ffon • C. Grohn • H . Hass • B .C . Harper • D .B. Harper • C.H. Haufler • D.L. Hawksworth • J. Heilu·ichs • T.J. Hieger • C.C. Hoftnann • R.W. Hook • C .L. Hotton • M.S . lgnatov • B. I1semann • J.L. Isbell• D. Johanning • J.R . Keeler • H . Kerp • K . Kingsley • P .C . Klahs • A .H. Knoll • E. Kustatscher • A.B . Leslie • C.V. Looy • R. Lucking • 1-1. Iv1artin • T . Masselter • S. McLoughlin • B . l\1eyer-Berthaud • ,\ . M icci • M.A. J'vfillay • J. Moni s • P. Muller • S. Naugolnykh • M.P. Nelson • K . Nik.las • H. Nishida • A. Novotny • J.M. Osbo1n • K.R. Pedersen • K.B. Pigg • M.S . Pole • C . Pott • C. Presrianni • R. Prevec • L. Regalado • 1\1. Reich • M.I. Ren1shardt • J'vl.A.J'v1. Renner • H . Rey • J .B . Richardson • J. Rikkinen • R. R iiBler • N.P. Ro\ve • P.E. Ryberg • M .A. Savoretti • A. Schafer-Yer\vi1np • A.R. Schmidt • H . Schneider • A.B. Schwendemann • J. Skog • R. Sonnhof • S . S6nyi • T . Speck • C . Stabile • W .E. Stein • D .W . Stevenson • R .A . Stockey • P .K . S trother• Tassel Loafers • M .L. Taylor • \V. A. Taylor• A .J'vl.F . Tornescu • N.M. Varela-Gastel um • S .K. Venna • H. Voeks • C . Walker• S.A. Walker • C .H . Welhnan • J.F. White Jr. • P. Wilf • E. Wi1n 1ner • M. del C. Zamaloa • If we missed or accidently overlooked anyone, we sincerely apologize.

1'here are several people who \.Vere especially close to 'fon1. We \vould like to extend very speciaJ apprec.iation and thank you to: Editb L. 1'aylor is an esteem.e d colleague and friend and Tom's wife. Edie is a prolific and renowned paleobotanist and has ,vritten more than 200 publications and nine books or edi ted volumes. Together with Tom, the Taylors brought paleobotany to the University of Kansas (KU) in 1995 frotn The Ohio State University and established one of the largest paleobotanical collections in the United States. She was instrumental in securing the continuous National Science Foundation (NSF) Polar Progran1 grants to support the Taylors' legacy in Antarctic fi eldwork and research on fossil plants in Antarctica. Due to their continuous perseverance, K U today is hoine to the NSF National Repository of Antarctic Plant Fossils. Together, Tom and Edie have bad a lifetime of traveling around the vvorld conducting paleobotany research and b1i nging together 1nany inte1national collaborators, colleagues, postdoctorals, and graduate students, 1nany of whom have contributed to th.is volu1ne. Totn and Edie had unconditional support for one another through Life and career endeavors; the Taylors had a profoundly positive and transfo1mati ve impact on the science of paleobotany. Thank you, E{lie, for being a role model as a person, scientist, and f1iend to us all and for your support in this proj ect. W ith all our love and sincerest grati tude. Jeannie M. Houts began working at the KU Departn1ent of Ecology and Evolut.ionary Biology in the adnlinistrative office as a graduate coordinator, while Ton1 was the departn1ent chai r. Tom took notice of Jeannie's superior organizational skills and n1eticulous eye for detail and hi red her as his executive ad1ninistrati ve assistant when he was appointed to the U.S. National Science Board in 2006. Since that time, Jeannie has been invaluable not only to Ton1 and Edie but also to the s uccess and productivity of the paleobotany program at KU. S he helped the Taylors with all admi nistrative du ties and coordination of m ultiple textbooks (including the tedious task of add ing several thousand references), 111an uscripts, all travel-related items (domestic and international), the laborious task of coordinating nun1erous field expeditions to Antarctica, and n1uch

XXV

Marepi.1an. 381U"1lll0HHbliii asropcK"1M npasoM

xxvi Acknow ledgments

n1ore. Ton1 had a saying that Jeannie "knew where all the bodies were buried" because she had a hand in vi rtually every part of the paleobotany lab. She has been beh ind the scenes for longer than 12 years, allo,ving the progra1n to ru n s1noothly and gro,v, and set the standard for going above and beyond, as well as putting a system in place for the progran1 to thrive for years to con1e. Jeannie was instrumental in the coordination of 1nanv of the visits and ' success of collaborators \vorking at the KU paleobotany lab, 1nany of who1n are represented in this book. We are all indebted to you, Jeannie. T hank you for all that you have done. Rudolph Serbet has been an integral part of the Division of Paleobotany, Biodiversity Institute, at KU since he started \.VOrking with the Tay lors as collections manager in I 997 . When the Taylors moved the Ja111es l'vL Schopf collection frorn the Byrd Polar Institute, Ohio St.ate University, to KU, he had the arduous task of physically n1oving and organizing the entire collection. As a result, Rud y set forth a meticulous syste1n that has kept the KU collections going strong and in keeping ,vith the vision that the collections should continuously gro\.v and support research. Rudy created a database of the collections and provided the data online long before any other large collection in the United States had done so. Toni was a strong advocate for ahvays p rov iding a hon1e for orphaned paleobotan ical collections and, over the years, Rudy helped to integrate 1nany such col lections at KU. Rudy was insttutnental in co1npleting one of the Taylor's longstanding tnissions of further expanding the housing of the KU collections with a new state-of-the-art annex facility on

West Campus at KU. Rudy 1nanages the largest collection of Antarctic paleobotanical specin1ens in the world. Antarctica was one of Ton1 and Edie's true passions, and Rudy was fo rtunate enough to go to the ice with To1n during his last field season in 2010-201 l. Since then, Rud y has maintained this tradition of Antarctic collection and exploration and has Jed four subsequent expeditions. In addition, to his services as a collections manager, he still finds tin1e \Vith various outreach and 1nuseun1 activities to vigorously pro1note paleobotany to the public each year. Rudy has helped inunensely in 1nultiple projects and areas of paleobotany, including directly helping n1any of the con11ibutors and projects in this book. Taking an edited volu1ne fro1n concept phase to production is a tTemendous challenge and would not be possible without the dedication of 1nany people. \Ve acknowledge the assistance provided by Acaden1ic Press and Elsevier for support of this project fron1 the beginning. We are especially thankful to Kristi Gomez, \vho helped us i1n1nense ly in the early phases of this p roject, and to the helpful insig ht and comn1ents fro1n the anonymous reviewers of our book proposal. A special ack nowledgn1ent and en1phatic gratitude go to Pat Gonzales, editorial project 1nanager. Pat has, again, set the gold standard for book project 1nanagen1ent and consistently went above and beyond for al l contri butors to this volume. Pat, thank you fo r your patience and understanding, attention to detail, ans\vering every emai l pron1ptly and our questions \Vith poise, as well as your guidance and instrun1ental help throughout this project. We could not have cotnpleted this volume without you.

Marep1,1an, 3a1141,1114eHH1>u,'i asropcK1'1M npasoM

Chapter 1

The Evolutionary Origin of the Plant Spore in Relation to the Antithetic Origin of the Plant Sporophyte Paul K. Strother1 and Wilson A. Taylor2 1

Weston Observatory of Boston College, Weston, MA, United States; 2University of Wisconsin Eau Claire, Eau Claire, WI, United States

. the fossil record has so far been mute regarding the algaeeland plant transition. Graham (1996)

1. INTRODUCTION The origin of land plants from their algal ancestors involved an evolutionary transition from aquatic algae of relatively simple morphology to subaerial plants whose complex multicellular morphology was expressed, at least in part, through the development of a diploid embryo. For some authors, this transition represents one of a handful of fundamental evolutionary transitions in biology (Margulis and Schwartz, 1982; Smith and Szathmáry, 1995; Knoll, 2011); for others, the origin of embryophytes is represented as a bifurcation in a phylogeny (e.g., Kenrick and Crane, 1997a). But in all cases, the evolutionary origin of land plants most likely required the serial acquisition of a suite of novel characters, including the regulatory genome required for their assembly into a true land plant. The scarcity of any plant (mega)fossil record before the late Silurian traditionally led to the use of trilete spores as a proxy for the embryophytes (Chaloner, 1967), because trilete spores with sporopollenin-containing walls are not found in any green algal group, extant or fossil. The general acceptance that fossilized tetrahedral tetrads of tightly bound spores, such as Tetrahedraletes (Strother and Traverse, 1979) or Cryptotetras (Strother et al., 2015), also represent a good embryophyte proxy (Wellman and Gray, 2000; Edwards et al., 2014) has pushed the

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00001-2 Copyright © 2018 Elsevier Inc. All rights reserved.

putative age of land plant origins to the Darriwilian (Strother et al., 1996, 2015). It is important to note, however, that with respect to the fossil record of the embryophyte plant body, we have no evidence of bone fide embryophytes earlier than the reported Cooksonia axis from the Homerian of Ireland (Edwards et al., 1983). Bower (1908) developed the antithetic, or interpolational, hypothesis of the origin of the plant sporophyte as an explanation of how the land plants evolved from aquatic algal ancestors. The antithetic hypothesis of sporophyte origins has historically been contrasted with the homologous theory, or sporophyte origins from an isomorphic alternation of generations. The homologous theory remains of interest with regard to early vascular plants that display nearly isomorphic alternation of generations (Kenrick, 1994; Gerrienne and Gonez, 2011). But recent reviews (Blackwell, 2003; Haig, 2015) all favor Bower’s hypothesis, along with the supposition that the embryophytes evolved from a charophyte with a haplobiontic life cycle, in which individual zygotes were the only diploid (2n) cells. Bower’s key insights were that the embryophyte spore must have evolved first, with vegetative (somatic) sporophyte tissues evolving later in time, and that the entire sporophyte phase evolved in response to natural selection in subaerial settings. The land plant spore, then, represents a fundamental adaptation to the subaerial habitat in the application of heteropolymers to form a resistant wall surrounding the spore protoplast (Graham, 1996). That same feature, the evolution of a sporopollenin-containing wall, resulted in resistant walled spores, which, in turn, allowed for a fossil record of spore evolution in subaerial settings. In cases of

3

4 SECTION j I Early Land Plants: Innovations and Adaptations

exceptional preservation, both algal and plant vegetative tissues can be preserved as organic compressions or as petrifactions, but these are quite rare in comparison to the fossil record of dispersed spores, acting as organic sedimentary particles that are readily incorporated into the sedimentary rock record (Traverse, 1994). In this report, we review the palynological record of dispersed spores and spore-like microfossils leading up to the origin of the first plant sporophytes preserved in the fossil record. In this way, we hope to document evolutionary changes in spores that occurred during a time of transition from algal ancestors to bone fide embryophytes (land plants). But, more importantly, we hope to tie the morphological changes observed in the spore record into a larger, more general picture of the evolution of the plant sporophyte.

2. THE ANTITHETIC THEORY AS A SCAFFOLD FOR INTERPRETING THE FOSSIL RECORD OF THE ALGALePLANT TRANSITION The antithetic theory of Bower (1908, 1935) was presaged  in the work of Celakovsky (1874), who recognized that the sporophyte generation in plants was functionally and evolutionary distinct from the gametophytedhence, antithetic to the gametophytic generation (Qiu et al., 2012). Bower postulated that the ancestral sporophyte derived from zygotes that first delayed meiosis and divided mitotically to produce a multicellular set of (diploid) sporocytes, or sporogenous cells, each of which initially retained the ability to undergo meiosis to produce spores. Subsequently, some of these sporogenous cells underwent sterilization to become vegetative and, under the selective pressure associated with a subaerial existence, gradually evolved into the tissues and organs of a sporophyte plant body. The consequence of this idea is that spores (and sporangia) literally preceded sporophytes in evolutionary time, and that “. each fertile tract is a residuum left by advancing sterilization” (Bower, 1908, p. 248). Bower also suggested that the initial function of the earliest somatic (vegetative) cells would have been to both protect and nourish the sporogenous cells. Thus, the sporophyte would have evolved de novo through the ontogenetic interpolation of the vegetative plant body into the life cycle before meiotic spore production (sporogenesis). In contrast to the antithetic theory, the homologous theory, which posits an ancestral alga with isomorphic (or nearly so) alternation of free-living generations, is now considered important only in the context of the origin of the polysporangiates, not the embryophytes per se (Kenrick, 1994). The homologous theory, based, in part, on the isomorphic alternation of generations seen in some macroscopic marine algae such as Dictyota and Ulva,

appears to be somewhat of an historical footnote. It played heavily in the “transmigration” hypothesis of Church (1919), who considered the aquatic-to-terrestrial transmigration of plants to be evolutionarily parallel to that of animals. “As the highest type of marine animal (the vertebrate fish) led on to the higher animal organisms of the land, so land-flora has been undoubtedly produced from the highest plant-organism attained in the sea” (Church, 1919, p. 9). However, the fishetetrapod and charophytee embryophyte transitions are not evolutionarily equivalent events, despite the fact that they both produced higher organisms that were capable of living on land. In the fishetetrapod transition, morphologically differentiated species possessed exaptations that were modified later and assisted in survival on land (Janvier, 2010). In contrast, during the algaleplant transition, undifferentiated streptophyte algal species evolved complex multicellularity de novo as a solution to living in a subaerial setting. For animals, the evolution of complex multicellularity from unicellular protist ancestors probably took place entirely within the aquatic realm (Nielsen, 2008). But in plant evolution, the origin of complex multicellularity (and developmental patterning) took place during the transition itself. So the study of the origins of animal terrestrialization shows little or no parallel to that of the streptophyte terrestrialization. From a paleontological perspective, this is the legacy of Bower’s theorydwhile the origins of animals are shrouded in the deep time of the Precambrian, paleobotanists have the opportunity to sample the fossil record as a direct and tangible history of the evolution of complex multicellularity in the streptophyte lineage leading to the embryophytes. Conceptually, then, it should be possible to map out Bower’s interpolational scenario as a series of added character states and then compare that series with the tangible fossil record of cryptospores and phytodebris (sensu Gensel et al., 1990). This scaffolding technique allows for the interpretation of the fossil record as a proxy of sporophyte evolution. That tangible history begins with the origin of resistant walled spores from ancestral streptophyte algae. Intriguingly, the Cambrian cryptospore record has preserved a diverse range of spore wall ultrastructures and spore topologies, many of which may be interpreted as evolutionary responses to adaptations to subaerial lifestyles. The initial transformation, from charophytic, flagellated zoöspores to resistant walled meiospores, has been tied to a “sporopollenin-transfer” hypothesis (SPTH) (Graham, 1984, 1993, 1996; Hemsley, 1994). Sporopollenin, or sporopollenin-like substances, are known to occur in the zygote walls of extant Coleochaete (Delwiche et al., 1989). If the deposition of sporopollenin were to be developmentally delayed until after meiosis, this would effectively transfer an overwintering function of the zygote to the meiospores. Although this idea may seem speculative from

Spore Origins in Relation to Sporophyte Origins Chapter j 1

the standpoint of interpreting the fossil record, there is direct evidence of heterochrony, with respect to the deposition of sporopollenin, during the evolution of spore development in extant bryophytes (Brown and Lemmon, 2011). In essence, both the antithetic theory and the SPTH are well supported by the recognition of heterochrony in bryophyte sporogenesis (Brown and Lemmon, 2011). The antithetic theory, then, requires a sequence of added evolutionary novelties, which could occur de novo, be co-opted from a prior gametophytic genome, or some combination of both. To the extent that the sequence itself can be constrained, the order in which sporophytic characters evolved, regardless of their ultimate source, would present themselves in the same order of appearance in the fossil record. An attempt to construct such a sequence is presented in Table 1.1. For each proposed step in the evolutionary acquisition of sporophyte characters, as an extension of Bower’s hypothesis, the corresponding biological equivalent and potential fossil structures are presented. Thus, the first evidence of a transitional sequence might be seen as spore wall formation in streptophytic algae but one in which sporopollenin was retained in the wall of the resting zygote. The biological manifestation of this initial stage might be seen in the fossil record of resistant walls that surrounded either meiospores or multicellular sporogenous masses. And, indeed, the retention of a membrane surrounding fossil cryptospore dyads and tetrads has been cited as possible retention of either a resistant zygote wall (Taylor and Strother, 2008, 2009) or the resistant wall of a spore mother cell (SMC) (Strother and Traverse, 1979; Taylor and Strother, 2008). Taylor and Strother (2009) refer to preserved resistant walls that surround the earliest cryptospores as “synoecosporal walls,” a term reflecting the enclosed and endosporic nature of the dispersed, late Cambrian cryptospore Agamachates. After sporopollenin transfer, theoretically there should be a true spore record of dispersed, resistant walled spores,

5

and, in fact, there is such a recorddthe record of cryptospores. Bower did not anticipate the occurrence of spore dyads and tetrads but, as discussed next, aspects of cryptospore topology provide clues that support their inclusion in the interpolational hypothesis. In addition, cryptospores provide an important record of evolutionary change during the course of sporophyte evolution. For example, dispersed cryptospores provide our only evidence of sporocyte duplication (Strother et al., 2017), Bower’s next stage in which he proposed mitotic copies of fertilized zygotes as a means to increase the efficacy of rare fertilization events (Haig, 2008, 2015). Cryptospores from Cambrian and lower Ordovician strata show morphologies and topologies that appear more relevant to evolving streptophyte algal lineages than they do to living embryophytic spores. Ultimately, these differences can be traced to variations in ploidy levels that persist throughout their lifecycles as seen in charophytic algae today. Haig (2010) has pointed out that many charophyte lifecycles do not show a clear alternation between diploid and haploid phases. His observations, coupled with the documentation of DNA endoreduplication in Coleochaete (Hopkins and McBride, 1976), support the arguments of Taylor and Strother (2009) and Strother (2016), who have shown that cryptospore topologies of Cambrian taxa are consistent with spore-producing reduction divisions in which karyokinesis and cytokinesis are temporally decoupled. The canalization of meiosis, resulting in what is essentially a modern form of bryophytic sporogenesis, is seen clearly in the fossil record with the arrival of Tetrahedraletes grayae and Cryptotetras in the Darriwilian of Saudi Arabia (Strother et al., 2015). In terms of the interpolational hypothesis, the pre-Darriwilian fossil record represents a time during which the plant spore itself evolved from streptophyte algal ancestors. This can also be viewed in terms of the SPTH as a time during which the plant spore wall evolved. The fossil record does not provide very good direct evidence of Bower’s next phase, which is the existence of a

TABLE 1.1 Bower’s Interpolational Hypothesis as Working Scaffold for the Exploration of the Fossil Record of an Algal-Plant Transition Bower’s Sequence

Biological Manifestation

Fossil Record

1. Retained zygotes

Sporopollenin in zygote walls

Enclosed spores

2. Meiospores

Sporopollenin transfer

Free spores

3. Sporocyte duplications

Sporogenous tissue

Spore masses

4. Partial sterilization to generate vegetative cells

Vegetative 2n cells

Non-spore 2n tissues

5. Initial functional 2n tissue

Sporangial wall, haustorial tissue

Sporangia

6. Ancillary 2n tissue functions

Axial growth > transport cells

Elongate cells (tubes)

7. Genomic assembly

Embryo with apical cell

Axial plant body

6 SECTION j I Early Land Plants: Innovations and Adaptations

sporangium, or at least a sporocyte mass, which was surrounded by vegetative tissue. The homogeneous wall type seen in Cryptotetras erugata is consistent with a spore wall that was produced by tapetal secretion (Taylor et al., 2017). If this is true, it means that the earliest plant-like spores were produced in unilocular sporangia. Wellman et al. (2003) identified cryptospore masses from the Katian of Oman that were partially covered by acellular sheets, which they inferred to represent embryophytic sporangia. Intriguingly, some of these Late Ordovician spore masses were composed of dyads whose wall ultrastructure consisted of parallel laminae, this representing a second ultrastructural wall type found in association with Ordovician embryophytic sporangia. The next stages in Bower’s hypothesis have not really been explored in a paleobotanical context. The expectation is, of course, that the fossil record should contain a record of plant structures or tissues that evolved serially in association with the evolution of the sporophyte. This would necessarily have involved the evolution of vegetative tissues, such as mesophyll and cortical tissues, whose cells would have possessed cellulosic walls, which may not have been generally susceptible to preservation in the fossil record. There are some possible exceptions to this generalization, however, which include water-conducting cells, suberin-impregnated cell walls (such as endodermis), and impregnated (or coated) epidermal cells or cuticles. So, logically, we should look to later Ordovician and Silurian deposits to find this kind of plant-like cellular debris. This section of the column does contain such remains, but they have, for the most part, been thought of as belonging to the Nematophytales, and, with the caveat that the nematophytes are generally thought of as having a fungal (or lichen) affinity, their relevance to the origin of land plants, or embryophytes in general, has remained largely unexplored. Nevertheless, the recovery of any plant-like tissues in the DarriwilianeWenlock interval could be viewed in terms of the Bower model and, if so, potentially help to outline both the sequence and pathway taken during the evolution of the interpolational phases of sporophyte origins.

3. EARLY CRYPTOSPORE MORPHOLOGY 3.1 Sporogenesis and Cryptospore Morphology Miospore formation in spore-producing embryophytes has been well characterized in extant cryptogams. This includes, in addition to miospores that are shed as haploid spores (monads), spore tetrads in some hornworts and liverworts (Renzaglia et al., 2014) and, more recently, spore dyads in Haplomitrium (Renzaglia et al., 2015). The normal occurrence of meiosis in bryophytes and vascular

cryptogams results in four more-or-less morphologically identical miospores, whose derivation from a diploid sporocyte is often retained in the morphological details of the proximal facedespecially, the trilete mark. Fossilized cryptospores, as permanent dyads or tetrads, typically do not reveal such haptotypic features, but their derivation from a diploid sporocyte is revealed, in tetrahedral tetrads at least, by their common morphology and tetrahedral arrangement. The individual miospores in a cryptospore tetrad may be subtriangular in outline, as in Tetrahedraletes, or they may be more rounded, as is typically seen in Rimosotetras, which consist of more loosely arranged spores. But, in most cases, a combination of spore shape and position in a tetrad corroborates their meiotic derivation. As we discuss later, however, cryptospores from pre-Darriwilian strata do not generally show such morphological uniformity. Cambrian cryptospores do not occur exclusively in sets of four, so the normal relation between a single diploid sporocyte and four meiotically derived haploid spores as seen in all land plants today does not pertain to these more ancient forms. Neither do all Cambrian cryptospores possess rigid, uniform spore wallsdmany have undulating and somewhat irregularly shaped outlines. Fig. 1.1 represents an attempt to show some of these general differences in a graphic way by plotting images of key cryptospore taxa against a lower Paleozoic timeline. The images are plotted roughly in their correct stratigraphic position and are all to the same scale. What is immediately apparent is the general size difference between pre- and post-Darriwilian forms; as a general rule, Cambrian cryptospores are smaller. But the more irregular shapes and clustered habits of the pre-Darriwilian forms are also apparent. Because of such apparent differences between pre- and post-Darriwilian cryptospores, these more ancient forms have not been included in prior reviews of early land plant spores (e.g., Edwards et al., 2014), as they have been perceived as being of “algal” rather than “plant” origin (Wellman and Gray, 2000; Edwards and Wellman, 2001; Wellman, 2003). Strother (2016) has argued more recently that many of the morphological features seen in Cambrian cryptospores can be inferred to have evolved in response to natural selection in subaerial settings and that they are likely the remains of streptophytic, rather than chlorophytic, algae. These fossils may not be the remains of the direct ancestors of the embryophytes, but they probably do represent the remains of an evolving streptophyte algal complex that eventually did give rise to the earliest embryophytes. To process why pre-Darriwilian cryptospores are so different from embryophytic spores, we need to combine an accurate description of fossil morphology, topology, and wall ultrastructure, with an understanding of spore formation in living representatives of the streptophyte algae.

Spore Origins in Relation to Sporophyte Origins Chapter j 1

b

7

Bloomsburg Fm - Pennsylvania, USA

a

c Tuscarora Fm - Pennsylvamia, USA d

f

e

g

h

i

Kosov Fm - Prague Basin Harnage Sh - UK

j 10 µm

k

Hanadir Sh - Saudi Arabia l

n

m

o

p

q Kanosh Sh - Utah, USA

s

r

t u

v

Lone Rock Fm - Wisconsin, USA

x

w

Conasauga Grp - Tenessee, USA

z

y

aa ac

ad

ae ag

ah

ab

af

Tonto Grp - Grand Canyon, USA Bloomington Fm - Idaho, USA Pioche Sh - Nevada, USA Rome Fm - Tennessee, USA

ai

10 µm FIGURE 1.1 Diagram showing the general character of pre- and post- Darriwilian cryptospores aligned roughly in stratigraphic order. All specimens are to the same scale, indicated by the 10 mm scale bars. (a) Ambitisporites avitus. (b) Ambitisporites avitus. (c) Rugosphaera sp. (d) Dyadospora murusdensa. (e) Rimosotetras sp. (f) Tetrahedraletes medinensis (holotype). (g) T. medinensis. (h) Velatitetras sp. (i) Tetrahedraletes grayae. (j) Tetrahedraletes sp. (k) Tetrahedraletes sp. (l) Didymospora luna. (m) Dyadospora cf. D. murusdensa. (n) Cryptotetras erugata. (o) C. erugata. (p) Tetrahedraletes grayae. (q) T. grayae. (r) cryptospore cluster. (s) planar cryptospore dyad pair. (t) small cryptospore planar tetrad. (u) Grododowon orthagonalis. (v) Agamachates casearius (holotype). (w) A. casearius. (x) small Rimosotetras sp. (y) Adinosporus geminus. (z) Adinosporus bullatus. (aa) Adinosporus voluminosus. (ab) Spissuspora laevigata. (ac) Adinosporus sp. (ad) Sphaerasaccus sp. (ae) Vidalgea maculata. (af) Vidalgea sp. (ag) cryptospore cluster. (ah) Adinosporus cf. A. voluminosus. (ai) Adinosporus cf. A. voluminosus.

8 SECTION j I Early Land Plants: Innovations and Adaptations

While we cannot guarantee that living representatives of the streptophyte algae possessed the same biology as their ancestors, spore formation in charophytes and, in particular, Coleochaete provides a starting point from which to interpret fossil sporogenesis. This uniformitarian approach has led to some key interpretations that have helped to clarify the seemingly messy morphology of these early cryptospores. In combination with a series of transmission electron microscope (TEM) studies (Strother et al., 2004; Taylor and Strother, 2008, 2009), we now possess a nascent understanding of how these spores formed, enough so, at least, to provide reasonable working hypotheses of sporogenesis in these transitional streptophytes. A key feature in the meiotic production of zoöspores in living Coleochaete is the recognition that karyokinesis and cytokinesis are temporally decoupled from each other. To be more precise, multiple rounds of DNA duplication, or endoreduplication, occur within the zygote before nucleation and cytokinesis. This was clarified by Hopkins and McBride (1976) who demonstrated that the nuclei in zygotes of C. scutata may contain up to eight copies (8C) of the haploid (1C) amount of DNA before perennation. After germination, Coleochaete zygotes produce up to 32 haploid (1n) zoöspores per original diploid (2n) zygote. Graham (1993) describes this form of sporogenesis as meiosis I, followed by multiple rounds of meiosis II. However, in a review of cell division in charophytes at large, Haig (2010) considers it unclear as to the nature of chromosomal pairing and karyokinesis in Coleochaete, leaving open the possibility that DNA replication occurred before the sorting of chromosomes into discrete nuclei. Haig (2015) points out that reduction division in Coleochaete does not correspond to either meiosis or mitosis, as seen in plants today. We will return to the nature of reduction division in Coleochaete later in the discussion in the canalization of meiosis, but for now, it is important to realize that many of the charophytes today, and Coleochaete in particular, do not possess a regularized version of reduction division, and, therefore, there is no reason to think that the Cambrian ancestors of these streptophyte algae did either. Cambrian cryptospore morphology can be characterized by two general features: (1) the close association of two or more spore-like bodies that do not retain regular geometric attachments and (2) the occurrence of multiple wall layers, including synoecosporal walls (Taylor and Strother, 2008), which enclose tightly clustered spores to form packets. Both of these features can be viewed in relation to the haphazard nature of spore development as characterized by zygotic germination in living charophytes (Haig, 2010). In addition, the persistence of multiple resistant walls, surrounding varying numbers of enclosed spore bodies, can be viewed as evidence of an on-going process of “sporopollenin transfer,” during

which sporopollenin deposition shifted from the zygote wall to the walls of the meiospores (Blackmore and Barnes, 1987; Graham, 1993; Hemsley, 1994).

3.2 Early Cryptospore Topology We use the term “topology” to refer to the geometric arrangement of spore bodies in combination with the pattern of enclosing walls. The topology of a cryptospore packet can be deconstructed as a combination of cell divisions (produced by cytokinesis) and wall constructions (produced by either centripetal or centrifugal deposition of wall material). The deconstruction methodology was originally applied to Agamachates casearius (Taylor and Strother, 2009), where we were able to demonstrate differences in the number of cell divisions that occurred during spore formation. Ultimately, these late Cambrian cryptospore packets were resolved down to sets of spore pairs, each of which corresponded to mitotic cytokinesis. The middle Cambrian sample at a depth of 1581 ft (482 m) in the JOY-2 core from Oak Ridge, Tennessee (Strother, 2016), contains a well-preserved cryptospore population that includes examples of spore dyads and tetrads enclosed within a common wall (Fig. 1.2). This structure was interpreted by Strother (2016) as an SMC, whose cell wall was preserved, and which had undergone endosporogenesis resulting in a spore tetrad (T) and a spore dyad (D)dboth of which were retained within the original SMC wall. If that is the case, then some form of successive meiosis must have occurred. Ignoring the question of ploidy level, it is possible to view the resultant topology as a series of nuclear division (K1, K2, K3) events, which are decoupled from cytokinesis (C1, C2) and spore wall formation, all occurring within the cell wall of the zygote initial. A first nuclear division (K1) results in two daughter nuclei (Fig. 1.2b). These daughter nuclei then separate (Fig. 1.2c) and each undergoes a second duplication (K2) to produce a zygote with four nuclei (Fig. 1.2d), one set of which duplicates again, resulting in six nuclei in total (Fig. 1.2e). At some time between K2 and K3, the first round of cytokinesis (C1) occurs. Likewise, a second series of cells, associated with the tetrad (T) are formed during cytokinesis (C2), but in this case, each nucleus eventually becomes associated with the deposition of a spore wall (Fig. 1.2f). The timing of C2 is not specified by nucleus number, except that it is preceded by C1 and is followed by the deposition of a spore wall. The above case demonstrates the importance of recognizing topology in the interpretation of early cryptospores. The key aspect of this, in practical terms, is the recognition that centrifugal spore wall formation only occurs at the level of the cell: if multiple spore-bodies are found enclosed with a (synoecosporal) wall, then those spore-bodies must have arisen after the formation of the enclosing cell wall.

Spore Origins in Relation to Sporophyte Origins Chapter j 1

9

- nucleus K - karyokinesis

K1

a

SMC

C - cytokinesis

wall

spore wall plasmalemma

T b

D C2 C1

c

K2

K3 f

d

e

FIGURE 1.2 Interpretative diagram showing the possible developmental pathway leading to a cryptospore dyad (D) and a cryptospore tetrad (T) being retained in a common generative cell (inferred to be a spore mother cell, SMC). See text for further explanation.

Thus, even if we are uncertain of the ploidy of a spore or spore-bodies in a cluster, we can still infer the sequence of endosporic cell divisions for any given topological arrangement of nested spore walls (Taylor and Strother, 2009).

3.3 Spore Wall Topology in Relation to the Sporopollenin Transfer Hypothesis The SPTH posits that sporopollenin deposition on the zygote wall in charophycean algae was developmentally delayed during evolution to be later deposited on meiospore walls (Brown and Lemmon, 2011). Sporopollenin deposition is initiated as a secretory process in the cytosol of the developing zygote and deposition occurs centrifugally to the outside of the cell to produce an encysted zygote. This is diagramed in Fig. 1.3, Series IA, which models reduction division in Coleochaete. The second stage in the SPTH, which is not seen in extant organisms, is modeled in Fig. 1.3, Series II, for both dyads (row B) and tetrads (row C). In this depiction of the model, Series II represents a hypothetical intermediate scenario in which sporopollenin deposition is retained both on the sporocyte wall and on the resultant meiospores. Meiospores are coated as centrifugal deposition of sporopollenin continues during meiotic cell divisions. The topology of sporopolleninous wall formation is constrained by the notion of centrifugal deposition: pulses of sporopollenin deposition can only occur as a coating of a single cell. In row B we have only shown sporopollenin deposition as occurring at the last stage of dyad development,

resulting in a dyad pair, however, one could also envisage sporopolleninous wall formation as occurring prior to M2, in which case each of the resultant dyad pairs would also be enclosed by an envelope. In any case, it is worth noting that the dispersed form of an enclosed dyad pair (Fig. 1.3, Series IIB) is not found in the post-Dapingian spore record. Thus, it is unclear whether or not the fossil record supports an intermediate phase in the SPTH in which sporopollenin is retained on both the sporocyte wall and the enclosed meiospore walls. For tetrads this determination of the retention of a sporopollenous sporocyte wall is bit trickier, because envelope-enclosed cryptospore tetrads (e.g., Velatitetras) are well known in post-Dapingian assemblages. Still, it is possible that an enclosing envelope in cryptospore tetrads may have been homologous to some form of perisporeda coating that was initiated centripetally from a surrounding tapetum, or tapetum-like inner sporangial lining. Series III in Fig. 1.3 depicts more evidence of the SPTH, but without hypothesizing retention of sporopollenin deposition in the initial sporocyte wall. The model depicts latent sporopollenin deposition as either occurring prior to M2 (row D) to produce pseudodyads, or after M2 (row E), in which case enclosed dyads are produced. What is intriguing here is that both of the topologies seen in the model are common in post-Dapingian cryptospore assemblages. Pseudodyads have always been somewhat problematic because they often do not display clear separations between the members of the dyad pair; Strother and Traverse (1979) originally interpreted them as diacrodioid acritarchs, mistaking internal thickening demarcating the

10

SECTION j I Early Land Plants: Innovations and Adaptations

meiotic development

I (A)

dispersed form (diaspore)

encysted zygote

zygote

zoöspores (8-32)

endoreduplication

(B)

sporocyte

M1

(C)

sporocyte

M1+M2

(D)

sporocyte

M1

(E)

sporocyte

M1

M2

enclosed dyads

(F)

sporocyte

M1

M2

free dyads

M2

enclosed dyad pair

II enclosed tetrad

M2

pseudo-dyads

III

IV (G)

sporocyte

free tetrad

M1+M2

plasmalemma

cell wall

sporopolleninous wall

FIGURE 1.3 Diagram showing possible developmental pathways involved in producing common cryptospore topologies in relation to the sporopollen in transfer hypothesis (SPTH). Series I A Model showing meiosis and zoöspore formation in Coleochaete. Here after DNA endoreduplication, 8e32 zoöspores are produced after cytokinesis occurs. Series II represents a hypothetical first step in the SPTH in which a sporopollenous wall is retained on the sporocyte initial. In row B, meiosis is successive, with the first meiotic division (M1) separated in time from the second meiotic division (M2). This results in an enclosed dyad pair. In row C, meiosis is simultaneous and an enclosed tetrad (¼Velatitetras) results. Series III posits the SPTH in an intermediate stage in which sporopollenin-containing walls are produced at different stages in successive meiosis. In row D, sporopollenin deposition occurs on the two intermediate cells that result from meiosis 1, but is incomplete or missing after meiosis 2 (M2), resulting in a pseudodyad. In row E, sporopollenin deposition takes place on both of the spores of the dyad pair, in addition, to the surrounding, intermediate wall. The resulting enclosed dyads may be free from the synoecosporal wall or attached, as depicted here in the dispersed form. Series IV demonstrates the completed SPTH state in which free dyads (row F) and free tetrads (row G) are the only cells with sporopollenin walls. See text for additional explanation.

Spore Origins in Relation to Sporophyte Origins Chapter j 1

two internal spore-bodies for external, arcuate folds. Basically, the exact nature of a contact surface between sporebodies in a pseudodyad is indeterminate. The individual spore-bodies are depicted here in Fig. 1.3 as consisting only of a plasmalemma, although, in many instances a cell wall probably was also in place. The wall topology of enclosed dyads can vary as well, as the outer wall (envelope) can either be free from the contact region, or converge at the contact area as depicted here at the end of row E in Fig. 1.3. Sporopollenin transfer is considered complete where there are no longer any intermediate traces of sporopollenin deposition in the morphology/topology of dispersed cryptospores. That is, sporopollenin walls occur only on the walls of meiospores, without any further envelopes or enclosing membranes. This is shown diagrammatically in Fig. 1.3, Series IV, in which row F represents the production of free dyads, and row G represents that of free tetrads. These forms first occur in the Darriwilian and persist well into the Devonian where they are found in the sporangia of cryptophytes and tracheophytes (Edwards et al., 2014).

3.4 The Evolutionary Developmental and Morphological Significance of Laminated Spore Wall Structure 3.4.1 The Primitive Nature of Laminated Sporoderm Based on developmental mechanisms in extant, sporebearing streptophytes, it is possible to identify two fundamental modes of constructing sporopollenin-containing walls. The first, and more primitive (Blackmore and Barnes, 1987), involves wefts of membrane, produced at the surface of the developing spore protoplast, that accumulate sporopollenin both on the inside (centripetally) and outside (centrifugally), but retain an electron-transparent center. These so-called tri partite lamellae (TPL) were among the first structural elements of the sporoderm to be identified using TEM. They are rarely thicker than about 20 nm, however, they can thicken as they move away from the membrane surface, resulting in the loss of the central lucent layer. Extant algal spores may secrete several successive layers of lamellae, and such layers are often continuous around the entire perimeter of the spore protoplast (Margulis et al., 1988). The second mechanism of sporopollenin deposition in the sporoderm involves the bulk formation and secretion of precursors by cells lining the sporangium cavity (tapetum). This mode of formation results in the masking of any original lamellated substructure. The process can result in thick, homogeneous, sporopollenin-containing walls; indeed this is the only known mechanism for the formation of such walls in extant developmental systems in sporebearing plants (see discussion below).

11

The discovery of laminae in the Ordovician/Silurian dyad, Dyadospora murusdensa Strother and Traverse emend. Burgess and Richardson (Taylor, 1995), led to comparisons between the then unknown producers of these ancient cryptospores and extant liverworts. This was based, in part, on the presence of laminae in the walls of mature spores in that group, and the basal position of the liverworts in land plant phylogenies (Kenrick and Crane, 1997b; Forrest et al., 2006). The subsequent discovery of charcoalified “Lilliputian” polysporangiates in the Devonian of the Welsh Borderlands, a subset of which possessed cryptospore dyads with laminated walls within terminal sporangia (Wellman et al., 1998), cemented the relationship between dispersed cryptospore dyads and true land plants (Edwards et al., 2014). The production of spore dyads in living embryophytes was not known at the time, and has only recently been documented in the living liverwort, Haplomitrium (Renzaglia et al., 2015). In any case, it is clear that some plant species produced meiotic dyads as a normal result of sporogenesis well into the early Devonian (Edwards et al., 2014), although this condition does not appear to have been common subsequently. Following Blackmore and Barnes’s designation of laminated spore walls as plesiomorphic (Blackmore and Barnes, 1987), it is not surprising that similarly, laminated sporoderm, which can be found in Cambrian spore-like microfossils, was later attributed to streptophytic algae, some of which were possibly ancestral to the embryophytes (Strother and Beck, 2000; Strother et al., 2004). There is now an extensive record of laminated spore walls found in specimens ranging in age from Cambrian Series 2 (Rome Fm) through the Darriwilian. Some walls comprise smooth laminae of uniform thickness that are continuous around the entire spore lumen (e.g., Plate I, 1). This basic, polylaminated construction can be derived from a series of successive pulses of resistant laminated membrane that exuded centrifugally from the entire surface of the developing spore protoplast. Such a process is consistent with developmental mechanisms amongst extant organisms, especially the green algae (Margulis et al., 1988), but certainly not limited to that group, as a similar mechanism has been implicated in the construction of the innermost laminated sporoderm in Sphagnum (Brown et al., 1982). A slightly variant system includes some Cambrian cryptospores that are surrounded by several continuous laminae that appear to be beaded, or to have occasional globular units between some laminae (Plate I, 2). This beadedwalled dyad was originally described from the middle Cambrian Bright Angel Shale (Strother et al., 2004). Although such ultrastructural wall features are unknown among extant green algae, it is not difficult to envision a phase of membrane bound droplets being secreted between the waves of laminae. The production of laminae with preformed globular units attached is less easily explained.

SECTION j I Early Land Plants: Innovations and Adaptations

12

1

2

3

5

4

PLATE I (1) Laminated wall ultrastructure detail showing smooth laminae of uniform thickness that are continuous around the entire spore lumen of a cryptospore polyad. Specimen GC2-2, Bright Angel Sh. Scale bar ¼ 200 nm. (2) Beaded-walled, “scabrate” dyad wall detail. Specimen GC1-2, Bright Angel Shale. Scale bar ¼ 400 nm. (3) Cryptospore dyad exhibiting multiple continuous laminae of variable thickness. Specimen GC1-4, Bright Angel Shale. Scale bar ¼ 100 nm. (4) Wall ultrastructure demonstrating continuous laminae of variable thickness similar to that seen in the extant liverwort Riccia. Specimen Rog2ox1-1, Rogersville Shale. Scale bar = 100 nm. (5) Wall ultrastructure demonstrating an anastomosing pattern of white lines reminiscent of tri-partite lamellae. Specimen GC2-4, Bright Angel Shale. Scale bar = 100 nm.

Spore Origins in Relation to Sporophyte Origins Chapter j 1

Finally, cryptospores found in both the Bright Angel Shale (Plate I, 3) and the Rogersville Shale (Plate I, 4) have a wall ultrastructure that consists of continuous laminae of variable thickness. These are strikingly similar to some extant liverworts (e.g., Riccia), but predate any other evidence of embryophytes by 50 million years. In general, the occurrence of resistant walled spores is rare among both extant freshwater and terrestrial algae. An extensive survey involving moribund unialgal cultures, as well as field-collected specimens from desiccating environmentsdall tested using acetolysis as a proxy for fossilization potential (and presence of sporopollenin)ddetected very few acetolysis resistant compounds (Taylor, unpublished data). And, the one extant algal system that was recognized as producing resistant walled spore-like bodies resembling some of those found in the Cambriandaeroterrestrial Coleochaetedis not a good match with the uniform separate laminae found in the Cambrian (Graham et al., 2012). As noted above, the production of a mature spore wall that lacks any laminated substructure and is substantially thicker than any single lamina (up to a full micrometer in thickness in some cases) only occurs in extant embryophytes through the action of a sporangium with an active tapetum. This is the basis for the claim that the first appearance of such a spore wall in the Darriwilian of Saudi Arabia (Taylor et al., 2017) marks the earliest indication of the existence of a unilocular sporangium that possessed a tapetum. This implies that by the middle Ordovician, an evolving sporophyte complex had achieved an early stage in sporophytic tissue differentiation that included some form of sporangial wall layer that enclosed a (sporopollenin-secreting) tapetal layer. But note that this precludes the indirect presence of liverworts, none of whose extant species possess an active tapetum.

3.4.2 Variation in Cambrian Spore Wall Lamination Our ongoing examination of Cambrian cryptospore wall ultrastructure continues to reveal a greater diversity than that represented by these two basic laminated and homogeneous types. Thus, it is not always clear how such walls were generated, especially when compared to modern analogs. Neither can we be certain as to the specific organisms that produced these various wall types, other than the assumption that these features are consistent with character state evolution within the streptophyte algae. Cryptospores from the lower Cambrian Series 2, Rome Fm in eastern Tennessee, which can be attributed to the genus, Adinosporus Strother, produced very thick walls consisting of a large number (as many as 40) continuous laminae. These laminae can be either beaded, or rucked up so they appear somewhat uneven in thickness in section view.

13

Some cryptospore dyads in the Bright Angel Shale (Cambrian Series 3) have walls constructed of discontinuous light zones in an otherwise dark matrix (Plate I, 5). These walls are reminiscent of previously mentioned TPL. Late Cambrian, packet-forming dyads of Agamachates casearius have a thin contact face wall that lacks evidence of multiple laminae, and a common outer wall (synoecosporal wall) that is completely homogenous. As noted above, there is no known algal system for producing such a wall. Overall lamination in various Cambrian cryptospores seems to vary from rather loosely arranged, individual laminae, characteristic of forms such as Adinosporus to more tightly-fused, anastomosing laminae of more-or-less uniform laminae, both of which are reminiscent of extant liverworts. This later form is also characteristic of dyads of Ordovician (Katian) age describe by Wellman et al. (2003). It is tempting to speculate that the plant spore wall began as a loose set of laminae, which evolved into a more compact and compressed form of anastomosing and/or parallel laminae, followed by thicker, homogeneous walls, eventually adorned with sculpture. However, the fact that loosely laminated and tightly laminated forms co-occur near the base of the cryptospore record precludes their utility as a stratophenetic marker of evolution.

4. CRYPTOSPORES AND THE ORIGIN OF MEIOSIS IN PLANTS Although we have stressed the probable homology between middle and late Cambrian cryptospore morphology and that of embryophytic spores, there are clear, generalized differences between pre- and post- Darriwilian cryptospore assemblages. Early reports of middle Cambrian cryptospores (Strother, 2000; Strother and Beck, 2000) were quickly rejected as evidence of embryophyte affinity (Steemans and Wellman, 2004), based, in part, on Wellman (2003), who noted that these earlier forms have thinner (less rigid) walls, lack geometric regularity, and are more loosely arranged than younger cryptospores that are unambiguously derived from embryophytes. Subsequent studies on Cambrian cryptospores (Strother et al., 2004), including systematic descriptions of new cryptospore species (Taylor and Strother, 2009; Strother, 2016), have not altered these facts. While Cambrian cryptospores are clearly “spore like” in overall character, they fundamentally lack the regular geometry that characterizes the tetrads and dyads of Darriwilian and younger cryptospores. These overall differences can be seen graphically in Fig. 1.1, which displays images of cryptospore taxa in a stratigraphical chart. There are obvious differences in the size and shapes of cryptospores that characterize pre- and post-Darriwilian assemblages. It seems apparent that a general change in the morphological regularity of dispersed spores occurred during Darriwilian time. The end result

14

SECTION j I Early Land Plants: Innovations and Adaptations

of that change was a shift from a highly variable spore morphology, such as that encapsulated by Adinosporus, to a much more regular geometric form, producing spores with robust walls and regular geometric arrangement (e.g., Cryptotetras). Since these later forms are convincingly of an embryophytic nature, we can infer that they were produced by plants that possessed an embryophytic form of sporogenesis. And, given that this would have included normal meiosis, we infer that a bryophyte-grade of meiotic sporogenesis was attained by Darriwilian time. The production of geometrically regular meiospores, which are derived from spore tetrads and dyads, has two biological components to it. The first is the observation that spore-bearing plants today undergo a rather elaborate series of cytoskeletal transformations in the cell cycle to guarantee that all four meiotic products are structurally and materially isomorphic. Spindle formation and cytokinesis during bryophytic sporogenesis use tubulin-based, preprophase bands to align the spindle and to ensure that the developing cell plates of the four meiospores form simultaneously and in a consistent, tetrahedral arrangement (Brown et al., 2010; Brown and Lemmon, 2011). Sporogenesis in all three extant bryophyte groups is often characterized by quadrilobing in the sporocyte itself (Shimamura et al., 2003). The lobes in the sporocyte wall predict the position taken by the four meiotic nuclei, each of which then establishes an isomorphic cytoskeletal domain. Once the four nuclei are in place, cytokinesis occurs simultaneously. These morphological features, which appear to have evolved de novo in the bryophytes, and are, therefore, plesiomorphic for all embryophytes, represent evidence of developmental processes that result in geometrically isomorphic spores. The second biological factor associated with the production of geometrically isomorphic meiospores is that individual sporocytes develop as separate cells that are freely suspended inside a unilocular sporangium. Each individual SMC is not constrained by adjoining walls of adjacent cellsdthey are free to ball up and develop in an isotropic medium. Sporogenous tissue, in other words, does not place a geometric constraint on the SMC shape because of rigid walls associated with neighboring cells. This, in part, allows the developing sporocyte to maintain a fundamentally spheroidal shape and, ultimately, produce geometrically regular meiospores. Strother (2016) has suggested that the Darriwilian origin of geometrically regular cryptospore tetrads represents the canalization of meiosis in the evolving lineage leading up to the origin of the plant sporophyte. This is consistent with the observations of Brown and Lemmon (2011), who see the origins of bryophytic sporogenesis as a combination of three examples of developmental heterochrony: (1) a delay in cytokinesis, (2) acceleration of

karyokinesis, and (3) a delay in the centrifugal application of sporopollenin to the sporoderm. This later process is effectively the “sporopollen-transfer hypothesis” as proposed by Graham (1984, 1993) and others (Blackmore and Barnes, 1987; Hemsley, 1994). In other words, spore development (ontogeny) in bryophytes has preserved the evolutionary pathway (phylogeny) by which streptophyte algae transitioned from using the zygote as the resting stage to using meiospores as the resting (and dispersal) stage the life cycle. This was seen by Brown and Lemmon (2011) as occurring as a result of subaerial adaptation during the early phases of the algal-plant transition, and as evidence that plant spores originally formed directly from a first (meiotic) division of the zygote, prior to the subsequent origin of the vegetative sporophyte. It is pretty clear, however, that the transfer of sporopollenin deposition from a streptophyte algal zygote to meiospore was already a work in progress by the middle Cambrian, as evidenced by the multilaminate sporoderm seen in many of the Cambrian cryptospores (Taylor and Strother, 2008). Thus, the shift in sporopollenin deposition from zygote wall to spore wall had already occurred prior to the Darriwilian origin of plant-like sporogenesis. The principal evolutionary novelty that is represented by the first occurrence of tetrahedral tetrads in the fossil record is the canalization of meiosis, during which a somewhat chaotic process of reduction division in streptophytic ancestors (Haig, 2010) became fixed into the diploid/haploid condition that characterizes all embryophytes today. The developmental heterochrony associated with the timing of nuclear and cell divisions during meiosis as seen in extant bryophytes, is integrated with cytoskeletal structures that constrain meiosis to form only four haploid spore domains. This shift occurred before there is any evidence in the fossil record of a vegetative sporophyte, although Taylor et al. (2017) argue that the homogeneous sporoderm that characterizes Cryptotetras constitutes indirect evidence of tapetal activity in the Darriwilian, which would imply the existence of vegetative sporophyte tissue, in the form of a sporangium, at that time. The first occurrence of geometrically regular cryptospore tetrads is not tracking the origin of the land plants per se, but rather, the advent of a modern form of embryophytic sporogenesis. In terms of a spores-before-sporophyte scenario, the canalization of plant meiosis would probably have occurred in an earlier, rather than later phase in the evolution of a plant sporophyte that included vegetative tissues beyond those immediately associated with spore production. This conclusion has the unsettling result of breaking with the generally accepted view that the tetrahedral tetrads stand as proof of the presence of true land plants. On the other hand, accepting that the evolution of plant-like spores and spore characters occurred earlier in the temporal sequence of sporophyte evolution, opens up the possibility that the fossil record may yet aid in establishing the order in

Spore Origins in Relation to Sporophyte Origins Chapter j 1

which the sporophyte characters were acquired. This would include developmental pathways associated with particular plant tissues, whether co-opted from prior algal genes or evolved de novo as part of the plant development toolkit.

5. THE STRATIGRAPHIC RECORD OF THE CRYPTOSPORES AS A RECORD OF SPOROPHYTE EVOLUTION It is now possible to propose a very basic sketch of sporophyte evolution based on the stratigraphic order in which cryptospores occur. This begins with cryptospores of early to middle Cambrian age (Strother, 2016), which appear to demonstrate that an evolving streptophytic algal complex had both adapted to subaerial conditions and begun a process of migrating sporopollenin deposition from the zygote wall to the spore wall. This included the fusion of centrifugally produced sporopollenin lamellae to form multilaminated spore walls. The process of sporopollenin transfer seems to have been completed by the Darriwilian, during which the establishment of a bryophytic style of meiosis became firmly established. But the Cambrian cryptospores also show some evidence of a relation between algal zygotes (as zoöspore producers) and sporocytes (as dispersed spore producers). Specifically, some cryptospore packets, recovered from Series 3 Rogersville Shale in Tennessee, are themselves preserved in loosely attached sets of six to eight packets, which show imperfect alignment in two parallel rows (Plate II, 1, 2, and 3). This is also the case for the holotype of Adinosporus voluminosus, which occurs as part of a loosely attached set of six packets (Strother, 2016). If such alignment reflects a vestigial representation of the original zygote position on a gametophytic thallus, then these forms might be evidence of zygote retention during the early phases of sporopollenin transfer. The issue of whether early zygotes were retained on a gametophyte thallus or freely dispersed as propagules prior to the initiation of meiosis has been addressed by Haig, who remarks that, “The retainedzygote hypothesis appears somewhat more plausible, although the dispersed-zygote hypothesis cannot be refuted definitively.” (Haig, 2008: p. 411). This issue is one whose resolution will require further fossil finds in the future. Palmelloid sheets of cryptospore dyads occur in Dapingian-Darriwilian boundary sediments of the Kanosh Formation at Fossil Mountain in Utah (Vecoli et al., 2015). These “spore-thalli” have been recently described as a new cryptospore taxon, Grododowon orthogonalis (Strother et al., 2017). The two-dimensional division patterns seen in Grododowon orthogonalis mimic basic palmelloid patterns seen in both chlorophyte (e.g., Prasiola) and charophyte (e.g., Coleochaete) algae. They include division sequences characterized by alternating orthogonal divisions to produce spore clusters and by serial (filamentous) divisions

15

that use both periclinal and anticlinal divisions to form circular rosettes. These cryptospores occur as tightly attached, geometrically regular planar clusters. They appear to have been formed through mitotic divisions of sporocytes, which, if true, would add support to Bower’s original hypothesis that the first divisions of an evolving sporophyte would have consisted only of cells capable of producing sporesdnot vegetative cell or tissues. It should be noted, however, that the palmelloid form of Grododowon orthogonalis does not represent an intermediate form of tissue in the construction of a sporophytic plant that was later incorporated into the plant developmental toolkit. Rather, it appears to have been a failed experiment in an evolving complex that had co-opted genes associated with vegetative gametophyte growth for mitotic expansion of a diploid phase of the life cycle. While this is speculative, it is an example of a fossil that can be interpreted both in light of Bower’s hypothesis and the probability that the evolving sporophyte evolved through the co-option of ancestral algal genes as part of the assembly of the plant developmental toolkit (Floyd and Bowman, 2007). The next stage in our brief timeline is the Darriwilian canalization of meiosis, resulting in the beginning of the tetrahedral cryptospore record (Fig. 1.1). From the standpoint of cryptospore evolution, this is probably the most significant evolutionary change seen in their fossil record. The Hanadir assemblage from Saudi Arabia represents the oldest example of well-documented taxa of tetrahedral tetrads, which include Cryptotetras and species of Tetrahedraletes and Rimosotetras. As discussed in Section 4, the thick, homogenous wall found in Cryptotetras is indirect evidence of the existence of a unilocular sporangium which possessed a tapetum, hence this represents both the origin of meiosis in the evolving sporophyte, and the first evidence of the vegetative sporophytic tissue. This level of sporophyte development has also been documented by Wellman et al. (2003) who reported on sporangial fragments from late Caradoc (now, Katian) sediments in Oman. Although the cellular nature of sporangial walls was not confirmed in these fragments, the authors argued that the amorphous material covering parts of these spore masses was likely sporopollenin that was of tapetal origin. In addition, some of the presumed sporangial spore masses contained cryptospore tetrads that possessed homogenous sporoderm, the characteristic form of plant sporoderm that is of tapetal origin today. Perhaps the last significant aspect of sporophyte that is tied directly to the cryptospore record is the timing of the origin of the trilete sporedlong thought to be indicative of not just embryophytes, but, more specifically of vascular plants themselves (Hoffmeister, 1959). This association between trilete spores and vascular plants is at the heart of an argument put forth by Steemans et al. (2009) who recovered ornamented trilete spores from shallow cores of latest Katian

SECTION j I Early Land Plants: Innovations and Adaptations

16

1

3

2

4

5

PLATE II (1) Aligned cluster of four cryptospore polyads. Rogersville Shale. Scale bar ¼ 10 mm. (2) Aligned cluster of six cryptospore tetrads. Rogersville Shale. Scale bar ¼ 10 mm. (3) Aligned cluster of eight cryptospore packets, Adinosporus voluminosus, Rogersville Shale. Scale bar ¼ 10 mm. (4) A cuticle fragment from rocks of Latest Ordovician to earliest Silurian age, showing the blocky character of cell shape. Power Glen Fm. Scale bar ¼ 100 mm. (5) Fibrillar nematoclast. Silurian, Mifflintown Fm. Scale bar ¼ 10 mm.

age from Saudi Arabia. Of course, fossil trilete spores are not, strictly speaking, a tracheophyte apomorphy, because they do occur in extant Sphagnum (Musci) and many hornworts. The fact that from the Llandovery onward, both trilete

spores and cryptospores occur together in palynomorph assemblages indicates that there was temporal overlap between cryptospore-producing and trilete-spore-producing plants. This has the effect of making the transition from tetrad

Spore Origins in Relation to Sporophyte Origins Chapter j 1

producers to trilete producers seem gradual. From an evodevo perspective the transition seems to be a case of heterochrony, wherein extended retention of the maturing sporocyte proceeds from the tetrad stage to the separated stage, prior to sporangial dehiscence. However, spore tetrad maturation in extant plants is a bit more complex than that, as both callose production and tapetally-derived sporopollenin deposition are involved in miospore development. In any case the shift from cryptospores to trilete spores appears to be a more or less gradual transition, reflecting, perhaps, evolution within one or more embryophyte lineages, and, eventually, by Lower Devonian time, residing in the tracheophytes.

6. INTERPRETING ORDOVICIANSILURIAN PHYTODEBRIS AS A RECORD OF SPOROPHYTE EVOLUTION It is probable that genes responsible for vegetative development of the gametophyte were co-opted to produce the vegetative sporophyte, whenever a free-living diploid plant evolved. Haig (2008: p. 411)

If we accept that the appearance of isometric, geometrically regular tetrads in the Darriwilian represents the evolutionary canalization of meiosis in plants, and not the origin of embryonic development in land plants per se, this opens up the possibility that the evolution of the plant sporophyte continued throughout the remainder of the Ordovician and on into the Silurian Period. In this scenario, the fossil record itself could contain evidence of novel character acquisition in association with sporophyte evolution during this interval. This might include plant-like cuticles as well as specialized tissues that are today associated with plant sporophytes of basal plant groups. These problematic, organic fragments have been termed, “phytodebris” (Gensel et al., 1990). Studies of Ordovician phytodebris are quite limited in extent. Perhaps the best known is the claim of sporangial masses from the Katian of Oman (Wellman et al., 2003). In this case an amorphous organic layer on top of a spore mass was considered to represent the remains of sporangial wall, however, neither the cellular nature, nor the overall geometric form of a sporangium was determined. Other authors have reported on “cuticle-like” debris, the oldest of which occurs in the Hanadir Shale of the Qasim Formation in Saudi Arabia (Strother et al., 1996). Similar, cuticular structures were illustrated by Gray et al. (1982) from Caradocian (now Katian-Hirnatian) rocks from Libya. These older “cuticles” tend to have very thick partitions, outlining generally isodiametric lumens, which, presumably represent

17

the positions of former epidermal cells. These few examples of Ordovician cuticle-like sheets are hardly distinguishable from the more common Nematothallus “cuticle” which is reasonably common in spore-rich palynological assemblages from Silurian and lower Devonian strata (Strother, 2010). However, Nematothallus, and related fossils are now generally believed to be lichens (Edwards and Axe, 2012; Edwards et al., 2013; Honegger et al., 2013), which would render them irrelevant with respect to sporophyte evolution. Silurian cuticles can be of varied morphology (and origins), however, so it is possible that a subset of these could be of plant origin. For example, Plate II, 4 shows a cuticle fragment from rocks of latest Ordovician to earliest Silurian age, in which the lumens are rectangular, rather than more rounded or isodiametric in shape. This pattern is more likely to represent cuticles derived from epidermal plant tissues. These are not common but their occurrence in the Llandovery could represent a stage in the development of plant epithelial tissue that is temporally intermediate between the origin of spores and full vascularization. Similar, rectangular patterned cuticles have been described by Edwards and Rose (1984) and Wellman (1995), all of whom noted that these rectangular forms could possibly belong to true plant cuticles. The so-called “banded tubes,” which were labeled nematoclasts by Gensel et al. (1990), are another class of potential plant structures that could represent intermediate stages in the assembly of the first plant sporophyte. As with the Nematothallus type cuticle, these mostly unbranched, resistant walled tubes are generally considered to be the remains of mycobionts in lichen associations (Wellman, 1995; Edwards and Wellman, 2001; Taylor and Wellman, 2009). Even after examination in TEM, Taylor and Wellman (2009) considered nematoclasts to be the remains of fungi, because they were not like coeval tracheids and they did not possess cross walls. In spite of this apparent general consensus, there are many doubts that remain with respect to the phylogenetic affinities of dispersed nematoclasts. For example, they do not persist in the fossil record after the Middle Devonian, their ultrastructure does not match that for known fungi, their lack of end walls (these are really, tubes), and their complete lack of clamp connections all add together to raise doubt as to their fungal affinity. The possibility that banded tubes could represent an early, evolving form of the plant tracheid has yet to be addressed, beyond an initial suggestion that they could belong to conducting or supporting structures derived from “. plants that were actively adapting to the selective pressures of a terrestrial environment” (Strother and Traverse, 1979). There are two aspects of banded nematoclast morphology that have been overlooked to some extent. One is the fibrillar nature of their primary wall construction, which, in theory, could be homologous with the fibrillar nature of cellulose fibril alignment in normal tracheid walls.

18

SECTION j I Early Land Plants: Innovations and Adaptations

This was not shown in the TEM work of Taylor and Wellman (2009) who found their samples to possess only walls of homogenous construction. Yet, it is quite easy to see the fibrillar nature of some nematoclasts (Gensel et al., 1990) and Plate II, 5 and 6. The second morphological parallel with true tracheids that has not received emphasis is the secondary nature of some internal thickenings. In some cases these have been shown in SEM to be peeling away from homogeneous primary walls (Strother and Traverse, 1979). These observations alone are enough to consider taking a closer look at the morphology and geological distribution of these fragments with respect to their possible origins as proto-tracheids in an evolving sporophyte lineage. Finally, nematoclasts have a stratigraphic distribution in the fossil record that aligns well with the stratigraphic record of a potential algal-plant transition. They first occur in the fossil record close to the Ordovician/Silurian boundary (Pratt et al., 1978; Strother and Traverse, 1979) and they seem to be at a maximal diversity during the Wenlock (Strother and Traverse, 1979; Gensel et al., 1990). Post-Silurian occurrences of nematoclasts seem to be confined to wefts of tubes that are associated with descriptions of tissues of nematophytes, and not as isolated elements.

7. CONCLUSION A review of the early streptophyte spore record supports an earlier SPTH (Graham, 1984; Blackmore and Barnes, 1987; Graham, 1993; Hemsley, 1994), but documentation of the details of this “transfer” do not present a simple, linear process. Cryptospore tetrads (and dyads) that were enveloped by a resistant wall were viewed as an intermediate form, in which both the sporocyte (as homologous to the primordial, sporopollenin-containing zygote) and the meiospores possessed a sporopollenin-containing wall. This notion is well-expressed in the stratophenetic diagrams of Wellman and Gray (Wellman and Gray, 2000; Wellman, 2010), but, as pointed out by Edwards et al. (2014) the “envelopes” that have been used to describe cryptospore taxa previously, probably do not represent homologous structures. Nevertheless, the variation that can be found in enclosed dyads (Fig. 1.3, Series III), which can be found well into the Silurian, seem to indicate an intermediate form of the SPTH in which sporopollenin was laid down onto synoecosporal walls that formed before the last mitotic division during successive meiosis. The application of Bower’s Theory to interpreting the fossil record leads to a transformative mindset in the paleobotanical approach to land plant origins, shifting focus away from “characters as proof or origin” toward one of “character acquisition and toolkit assembly.” This opens up the possibility that embryophyty itself evolvedda key to which is the observation that developmental regulation of the dividing

embryo initially specified meiospore development, but only later added vegetative tissue development. This was accomplished within an overarching program of heterochrony, where shifts in developmental timing became canalized as the evolving streptophyte lineage approached its modern state. These processes are demonstrated in the earliest fossil record of cryptospores, which do not show a precise alternation of diploid-haploid chromosome content during reduction division (meiosis). This stems from a charophyte-like ancestry in which variable levels of DNA endoreduplication preceded cell division during spore formation. Understanding extant plant development in the context of terrestrialization places some outside constraints on the evolutionary process leading to the origin of land plants. Some developmental components were probably inherited, or rather, co-opted, from previously evolved pathways in charophytic algae. Others evolved de novo after the basic developmental structure was in place (Floyd and Bowman, 2007; Niklas and Kutschera, 2009). But, however the basic developmental plant toolkit was constructed, it is unlikely that it was a simple linear process in which every step was retained in plant ontology. The fossil record, however, has already begun to show some of the basic components of the evolutionary construction of sporophyte development, especially with respect to spore development (Brown and Lemmon, 2011). If we can conclude anything from the application of the fossil record of cryptospores to the origin of land plants, it is that the origin of land plants was not a singularity in geologic time, but rather, a process of evolution of plant development that started with spores and ended with a fully developed sporophytic phase. This process had begun by middle Cambrian time and was completed by the middle Silurian.

ACKNOWLEDGMENTS This research has received prior funding from NSF and the Petroleum Research Fund of the American Chemical Society.

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Chapter 2

Early Devonian Woody Plants and Implications for the Early Evolution of Vascular Cambia Patricia G. Gensel University of North Carolina at Chapel Hill, Chapel Hill, NC, United States

1. INTRODUCTION The occurrence of small, 2- to 5-mm-diameter, ribbed axes of two plant types exhibiting aligned cells interpreted as secondary xylem, one from the Pragian of France and one from the Emsian of New Brunswick (Gerrienne et al., 2011), demonstrated the existence of a vascular cambium in the Early Devonian some 10 million years earlier than previously known (Gerrienne et al., 2011; Strullu-Derrien et al., 2014). This is a quite unexpected discovery that alters thinking about the timing of and some aspects of vascular cambium evolution given the small size of the plants involved. A third plant axis subsequently was described from the late Emsian of Gaspé by Hoffman and Tomescu (2013). The first two plants exhibit limited morphology, notably, narrow ribbed axes with at least two levels of dichotomous branching but lacking attached sporangia. The presence in all of these plants of centrarch haplostelic primary xylem with at least some tracheids exhibiting scalariform-bordered, multiaperturate pits (P-type of Kenrick and Crane, 1997) suggests these axes are allied to basal or early euphyllophytes. Reasons for regarding these aligned cells to be of secondary origin, hypotheses concerning possible causes for evolution of a vascular cambium, and impacts on hydraulics in these small plants have been proposed or discussed (Gerrienne et al., 2011; Hoffman and Tomescu, 2013; Strullu-Derrien et al., 2014; Gerrienne and Gensel, 2016). The use of new technologies for nondestructive sampling of specimens is advocated (Strullu-Derrien et al., 2014). These discoveries raise or renew many questions concerning the early evolution of the vascular cambium, including how to distinguish primary versus secondary tissues, how these

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00002-4 Copyright © 2018 Elsevier Inc. All rights reserved.

early cambia may have functioned, and why some (particularly unifacial) vascular cambia become determinate fairly quickly. The significance of these discoveries in relation to the several independent occurrences of the different types of vascular cambium activity in Paleozoic plants and to plant growth patterns needs reassessment. The purposes of this account are to summarize what is known about early Devonian plants with secondary tissues, to describe a fourth occurrence from the Early Devonian of New Brunswick, to present preliminary data on a complex of plants that resemble some species of Psilophyton but in which some axes possess aligned cells that may represent secondary tissue, and where possible, to discuss these issues. These Psilophyton-like plants again suggest that basal euphyllophytes at the trimerophyte grade (Psilophyton, Pertica-like plants) exhibit comparative morphological stasis or subtle morphological variation but differ considerably in anatomy. Reevaluation of which characters are now most effective for taxon delimitation and evaluation of phylogenetic relationships among basal euphyllophytes (trimerophytes) and their putative ancestors or descendants is needed.

2. BACKGROUND Because developmental or ontogenetic data are mostly lacking in fossil plants, some ambiguity exists in how to interpret aligned cells in the xylem of some steles. Criteria for distinguishing primary from secondary xylem in fossils that have been used in the absence of developmental information (Cichan and Taylor, 1990; Gerrienne et al., 2011; Hoffman and Tomescu, 2013 and other references included therein) include a combination of the following: (1) radially 21

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SECTION j I Early Land Plants: Innovations and Adaptations

aligned files of cells (tracheids), (2) the presence of both fusiform and ray initials that divide to produce mature cells of the vascular tissue, and (3) anticlinal (multiplicative) divisions in cells within these rows. Of these, aligned cell files developing into cells typical of vascular tissue and presence of rays has been used most extensively. The Early Devonian plants thus far described exhibit these features. Interestingly, anticlinal divisions apparently do not occur in the secondary xylem of those lepidodendrids that have been studied (Cichan, 1985) or in Sphenophyllum (Cichan and Taylor, 1982) but are important features in several others.

2.1 Previously Described Occurrences of Secondary Xylem in Fossil Plants Secondary xylem has been documented previously in several lineages within both the lycophyte and euphyllophyte clades of vascular plants from the Middle Devonian, as summarized by Hoffman and Tomescu (2013) and earlier researchers. In lycophytes, the earliest occurrence is in Longostachys latisporophyllus of Middle Devonian (Givetian) age, from Hunan, China (Cai and Chen, 1996), also one of the earliest upright lycopsids. Longostachys and several other Upper Devonian and Carboniferous upright lycopsids exhibit an unifacial vascular cambium. Unifacial vascular cambia also are found in Carboniferous calamitaleans and in the Upper Devonian Rhacophyton, which is of uncertain affinity and perhaps best treated as its own family, although similarities to some Iridopteridales as noted by Berry and Wang (2006) are intriguing. As mentioned, a limited amount of secondary xylem has been suggested to occur in some Devonian cladoxylopsids other than cf. Xenocladia (Meyer-Berthaud et al., 2004), with some considered to achieve large size by primary growth (Soria et al., 2001; Meyer-Berthaud et al., 2010). Devonian and Carboniferous stenokolealeans (Beck and Stein, 1993; Moment et al., 2016) and Carboniferous zygopteridealeans (Dennis, 1974; Phillips and Galtier, 2005) also exhibit a limited amount of secondary xylem. A bifacial vascular cambium appears first in Middle Devonian aneurophytalean progymnosperms and is also known in archaeopteridealeans, sphenophyllaleans, and seed plants. In a recent report of an early Late Devonian large permineralized cladoxylalean trunk Xinicaulis lignescens, Xu et al. (2017) document an unusual growth pattern involving secondary xylem and provide an interpretation of how early cladoxylopsid trees may have grown based on the new data. In Xinicaulis, numerous individual primary xylem strands are closely arrayed near the periphery of the stem, and some extend into the mostly parenchymatous stem center. Each primary xylem strand is surrounded by several growth increments of secondary xylem. These

strands separate, leaving outermost increments of secondary xylem of each strand intact until final division, and subsequently anastomose, resulting in a complex mesh-like vasculature. Evidence of expansion and proliferation of parenchyma cells within the xylem strand facilitates the splitting; parenchyma proliferation in the stem ground tissue also occurs. Vascular strands also supply the mantle of roots. These features, which compare fairly well with the limited anatomy and morphology known in the late Middle Devonian Eospermatopteris, form the basis for interpretation of growth in these early large trees and indicate yet another way a vascular cambium evolved. The authors note some similarity to cambial activity in certain modern palms. Proliferation of parenchyma also is a part of growth models suggested for lycopsid and calamitalean trees showing an unifacial cambium. This mode of expansion growth, present by the Middle Devonian, indicates both variability and disparity in growth patterns, given that the more standard form of secondary growth from a bifacial vascular cambium forming a single cylinder exists in coeval early lignophytes. In summary, vascular cambia arose more than once, in both lycopsids and euphyllophytes, and possibly several times within several lineages in the latter. Among early occurrences, several types of cambial organization are present, as noted earlier by Cichan and Taylor (1990) and in the more recent studies just cited. The early Devonian plant occurrences suggest that a vascular cambium arose before (or perhaps contemporaneous with) other plant organs (Hoffman and Tomescu, 2013). Because regions outside of the xylem are not preserved, it is unknown if the cambium in these Early Devonian plants is unifacial or bifacial. Phylogenetic relationships of basal members of both lycophyte and euphyllophyte lineages are unclear; thus, it is unknown if a cambium might have existed in the last common ancestor before the lycophyteeeuphyllophyte split (Hoffman and Tomescu, 2013). Cambial activity is unknown at present among early lycophytes before the Middle Devonian.

3. PREVIOUSLY DESCRIBED EARLY DEVONIAN TAXA Plants described as having secondary xylem are (1) axes from the Pragian age Chalonnes Formation, Anjou, France, that were later named Armoricaphyton chateaupannense (Strullu-Derrien et al., 2014); (2) axes from the Emsian Campbellton Formation of New Brunswick, Canada, as yet unnamed (Gerrienne et al., 2011; Gensel, in prep.); and (3) Franhueberia gerrienni, Emsian, Gaspé (Hoffman and Tomescu, 2013).

Early Devonian Woody Plants and Implications for the Early Evolution of Vascular Cambia Chapter j 2

3.1 Armoricaphyton chateaupannense (Strullu-Derrien et al., 2014) Considerable information about Pragian Armoricaphyton is now available (Gerrienne et al., 2011; Strullu-Derrien et al., 2013, 2014; Gerrienne and Gensel, 2016) and summarized here (Plate I). Adpressions of axes 1.5e2.5 mm wide and up to 15 cm long associated with the shorter lengths of permineralized ones branch up to two times and are strongly ribbed. Detached elongate, fusiform sporangia also occur associated with axes (Strullu-Derrien et al., 2014). The 1- to 7-cm-long permineralized axes of the same diameter sometimes exhibit at least one bifurcation. Axes are permineralized by pyrite (Plate I, 1e4). Data were obtained via polished thin sections, peels, and synchrotron

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microtomy. The latter two techniques are important in that these provided important details supporting the existence of rays. While usually only the xylem is preserved, in lateral branches one often finds one to three layers of thickened cortical cells, suggesting a sterome is present. There is no anatomical evidence of cell patterns that might be the cause of ribbing (see Gerrienne and Gensel, 2016). The primary xylem consists of a centrarch haplostele, with a central line or row of cells, 5e15 mm in diameter, interpreted as protoxylem, surrounded by polygonal-shaped metaxylem 10e50 mm in radial diameter and 7e30 mm in tangential diameter (Plate I, 1). Primary xylem is surrounded by a layer of radially aligned rows of square to rectangular aligned tracheids, up to 15 cells deep, interpreted as secondary xylem (Plate I, 1e4). These are 15e100 mm in

PLATE I Armoricaphyton chateaupannense. Pragian, France. (1) Peel of transverse section of axis showing protoxylem, metaxylem, and secondary xylem. Little or no evidence of a lateral trace beginning to form. Multiplicative divisions at arrows. R indicates probable ray. Ulg. CP 9-1-2-slide B2a. Scale bar ¼ 100 mm. (2) Transverse section of axis in which lateral trace formation has been initiated (arrow). Ulg. CP 8-2-4-1, slide B5. Scale bar ¼ 100 mm. (3) Transverse section of axis exhibiting a lateral trace just separating from axis. Ulg. CP 31-1-2a. Slide C9. Scale bar ¼ 100 mm. (4) Transverse section of axis in which lateral trace has departed (right) and outer cortical region is preserved. Ulg. CP 31-1-2a, slide B9. Scale bar ¼ 100 mm.

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SECTION j I Early Land Plants: Innovations and Adaptations

radial diameter and 8e5 mm in tangential diameter. Multiplicative divisions occur frequently, as do spaces lined by a single wall and interpreted as the site of rays. The latter vary in length, depth, and frequency. Support for interpreting the spaces as rays is derived from longitudinal sections (not shown here, but refer to Gerrienne et al., 2011; Gerrienne and Gensel, 2016) where the absence of walls or pitting on the space side suggest that parenchymatous cells may have occurred there but were not preserved. Variability in ray morphology, as demonstrated by Gerrienne et al. (2011: supplemental data), may be comparable to that documented in early secondary xylem of conifers (Bannan, 1934). P-type pitting is observed on radial and tangential walls of both primary and secondary xylems. Based on a study of serial peels from several different axes, Gerrienne and Gensel (2016) described changes in primary and secondary xylem cells as traces to lateral branches are emitted. Lateral trace formation involves an initial elongation of protoxylem, with a proliferation of primary and secondary xylem cells around it to form the incipient trace, in which the protoxylem and metaxylem plus associated secondary xylem appear distinct from that

of the parent axis (Plate I, 3). This is followed by separation of a smaller round lateral trace in which secondary xylem still surrounds primary xylem. More distally, lateral traces lack secondary xylem (Plate I, 4). The amount of secondary xylem relative to the size of primary xylem present within series of sections or between specimens varies, and a growth model, similar to that shown in other plants (epidogenetic, then menetogentic, apoxogenetic phases), was proposed to explain some of these variations.

3.2 Unnamed New Brunswick Plant A: Preliminary Data The second plant briefly described and figured by Gerrienne et al. (2011) is from the Emsian Campbellton Formation of northern New Brunswick, Canada (Fig. 2.1, lower left red square), and is as yet unnamed. Adpressions of smooth, ribbed axes up to 14 cm long and 3e7 mm wide produce several lateral branches. Up to three divisions of axes are known (Plate II, 1 and 2). Fertile regions are unknown. Some axes exhibit short lengths of permineralization, which show the following: (1) in some, an elongate

FIGURE 2.1 Map showing outcrops in northern New Brunswick (red square in lower left of large map) and Gaspé Bay area, Quebec (red square in upper right) from which plants described in sections 3.2, 3.4.1 and 3.4.2 were obtained. Inset shows northeastern US and southeastern Quebec, with square delimiting fossil-bearing sites.

Early Devonian Woody Plants and Implications for the Early Evolution of Vascular Cambia Chapter j 2

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PLATE II New Brunswick plant A, Emsian, New Brunswick. (1 and 2) Ribbed axes showing branching. (1) Highly unequal bifurcation producing main axis and a dividing lateral branch. (2) Less unequal bifurcation on axis to left. Axes identical to these contained varying amounts of pyritized regions which were removed for sectioning, so it is known the anatomy shown belongs to these axes. (1) Scale bar ¼ 5 mm. (2) Scale bar ¼ 10 mm. (3 and 4) Axial anatomy showing elongate primary xylem and two stages in lateral trace departure (arrows). Note differentially thickened sterome in (3). (3) Scale bar ¼ 5 mm. (4) Scale bar ¼ 0.5 mm. (5) Transverse section of axis in which secondary xylem also is present. Spaces which may represent rays present, multiplicative divisions at arrows. Scale bar ¼ 0.5. (6) Section in which some secondary xylem present, showing initiation of lateral trace at arrow. Note differentially thickened sterome. Scale bar ¼ 0.5. (7 and 8) Scanning electron microscopic images of tracheids exhibiting P-type tracheid wall thickening. (7) Walls of adjacent tracheids with scalariform bordered thickening and perforations. (8) Casts of the wall pattern. Scale bars ¼ 0.01 mm.

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SECTION j I Early Land Plants: Innovations and Adaptations

oval haplostele with a central, narrow elongate protoxylem is well preserved (Plate II, 3). Many exhibit stages in the formation of lateral branches from opposite ends of the haplostele, in a pattern similar to that described earlier (enlargement of protoxylem and metaxylem, formation of an incipient trace), and results in the production of an elongate lateral trace (Plate II, 3 and 4). (2) Others exhibit the same primary xylem configuration but are surrounded by up to 24 rows of radially aligned cells, in which multiplicative division occurs and spaces considered to correspond to rays are present (Plate II, 5 and 6). Primary xylem cells are polygonal and 30e50 mm wide radially and 20 mm tangentially. Secondary xylem cells are 30e40 mm wide radially and 20e40 mm tangentially but more rectangular in shape. The rays are more abundant than in Armoricaphyton. Early stages in lateral trace formation in the axes with secondary xylem are similar to those showing primary xylem only (Plate II, 6). Tracheids exhibit scalariform bordered pitting with multiperforate apertures (P-type) (Plate II, 7 and 8). All axes are bounded by one to several layers of very thick-walled cells (a sterome) that is at least three cell layers thick, with cells being about 60 mm in diameter (Plate II, 3 and 4). The sterome varies in thickness around the circumference and often is broken or separated by a space. The discontinuities may be regions where stomata occurred or alternatively, taphonomic, such as sites of thinner-walled cells that provided a point of breakage as stems were compressed. Finding these plants of small size, with both a thick sterome and a limited amount of secondary tissue, led Gerrienne et al. (2011) to postulate that an initial cause for development of secondary vascular tissue was not for support but rather for improved water conduction.

3.3 Franhueberia gerriennii, Emsian, Gaspe´ A third occurrence, Franhueberia gerriennii Hoffmann et Tomescu, is found permineralized in cobbles from the Emsian Battery Point Formation, near Douglastown, south shore of Gaspé Bay, Quebec, Canada, intermixed with numerous axes and sporangia identical to P. dawsonii (Hoffman and Tomescu, 2013). These axes are permineralized in calcium carbonateerich clays (Banks et al., 1975; Hoffman and Tomescu, 2013), and serial peels were obtained. The specimens consist only of xylem, with no external tissues preserved, and exhibit a centrarch haplostele, 1.9 mm in diameter, composed of three zones, the innermost one being a central protoxylem 0.5 mm in diameter overall, with cells 8 mm in diameter. Surrounding this are metaxylem cells 7e15 mm in diameter, both of these cells being more rounded. These in turn are surrounded by up to 25 aligned rectangular shaped cells, 8.4e28.5 mm wide radially, 21.6e40.8 mm tangentially, and with numerous narrow rays. Multiplicative divisions occur in these cell rows and, compared with several similar plants, are considered

sufficiently distinct to be a separate taxon. Of particular interest is that pitting in all but the outermost metaxylem is circular to oval bordered. Some P-type pitting occurs in the outermost metaxylem but mainly in secondary xylem, along with some oval to circular bordered pits near the tapered ends of tracheids. Hoffman and Tomescu (2013) provide a thorough comparison of these three plants relative to younger taxa.

3.4 Additional Occurrences of Emsian Plants With Secondary Xylem: Preliminary Data 3.4.1 New Brunswick: Unidentified Axis B Some isolated pyrite nodules from the same locality producing the unnamed plant A described in Section 3.2 from the Emsian Campbellton Formation, New Brunswick (Fig. 2.1, lower left red square), show significantly larger axes with a circular to broadly angular region of primary xylem and more abundant secondary xylem (Plate III). Tissues outside of the xylem are not preserved. It is difficult to discern many details about the primary xylem, including location of protoxylem, but cells adjacent to the secondary xylem are similar in size, suggesting centrarch maturation. Outermost primary xylem cells are about 40e50 mm in diameter (Plate III, 4). Rows of square, aligned tracheids, with at least 50 cells per row but incompletely preserved, surround the primary xylem (Plate III, 1, 2, 5, and 6). Cells are 30e40 mm in radial and tangential direction and square to slightly rectangular. Again, spaces occur between the tracheid rows; some are quite wide and may represent regions of nonpreservation, while other, narrower ones may represent rays (Plate III, 1e3, 5, and 6). Longitudinal sections prepared thus far are uninformative about rays. Numerous anticlinal divisions can be observed. Although only a limited number of sections of this type are available, some show an apparent dichotomy of the axis into two apparently unequal sized axes, each with a similar amount of aligned xylem (Plate III, 2 and 3). The large number of aligned cells/row and multiplicative division suggests these are of secondary origin but further proof of the presence of rays is needed. Relationship to plant A from the same locality is unclear.

3.4.2 North Shore, Gaspe, Quebec: A Puzzle to Be Solved A collection of loose blocks from the Battery Point Formation at Seal Rock West on the north shore of Gaspé Bay, Quebec (Fig. 2.1, upper right red square), yields branched axes of two size ranges, 4e5 and 7e11 mm. The smaller axes are mostly finely ribbed, while the larger ones exhibit broader ribbing (Plate IV, 1 and 2). The smaller axes branch anisotomously, and some terminate in paired, fusiform sporangia that twist around each other (Plate IV, 2).

Early Devonian Woody Plants and Implications for the Early Evolution of Vascular Cambia Chapter j 2

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PLATE III New Brunswick plant B, Emsian, New Brunswick. (1) Transverse section of axis with outer part of primary xylem preserved and significant secondary xylem. Region on right suggests possible early stage in formation of a dichotomy. Scale bar ¼ 0.5 mm. (2 and 3) Axes showing successive stages in dichotomizing, with a nearly equal sized axis the result. Scale bar ¼ 1 mm. (4) Detail of axis from Plate III, 1, arrow pointing to probable metaxylem cells, based on difference in size, shape, and orientation of cells. Scale bar ¼ 0.5 mm. (5) Transverse section, showing secondary xylem, arrows indicate regions of possible multiplicative division. Scale bar ¼ 0.5 mm. (6) Detail of secondary xylem from Plate II, 1 showing spaces. Narrow space on right may represent a region where a ray occurred; the wider space may represent region of breakage or nonpreservation. Scale bar ¼ 0.5 mm.

PLATE IV Large and small axes, possibly Psilophyton-type, Emsian, Gaspe. (1) Specimen showing wide broadly ribbed axis with narrow attached lateral branches (also ribbed). Scale bar ¼ 10 mm. (2) Psilophyton type fertile specimen bearing paired terminal fusiform sporangia from lateral branch. Axis permineralized from base of image (where permineralized part removed) to above level of lateral branch departure. Scale bar ¼ 10 mm. (3) Polished thin section showing main axis consisting of primary xylem and nearly departed lateral trace. While not from the specimen in Plate IV, 2, trace formation similar. Scale bar ¼ 5 mm. (4) View of whole permineralized axis, with differentially thickened sterome; note breakage on lower side, possibly as outer region collapsed during preservation. Primary xylem present. Smaller axis to left may represent a lateral branch. Scale bar ¼ 1 mm. (5) Detail of stele from Plate IV, 4, showing dark area where protoxylem is not preserved, surrounding metaxylem, and beginnings of lateral trace formation. Scale bar ¼ 1 mm. (6) Axis in which both primary and possible secondary xylem occur, showing lateral trace departing (arrow). Multiplicative division occurs at arrowhead. Scale bar ¼ 0.1 mm. (7) Unrelated axis in which protoxylem is preserved in center, surrounded by metaxylem and possible secondary xylem. Multiplicative divisions at arrows. Some spaces may represent rays but no corroborative LS sections obtained yet. Scale bar ¼ 0.1 mm. (8 and 9) Scanning electron microscopic images of tracheids from these specimens. (8) Pyrite casts of P-type pitting. (9) Cell wall showing same. Scale bar ¼ 0.01 mm.

Early Devonian Woody Plants and Implications for the Early Evolution of Vascular Cambia Chapter j 2

The larger, strongly ribbed axes branch anisotomously, the laterals being 2e3 mm wide, with up to three divisions observed thus far (Plate IV, 1). Laterals exhibit narrower ribs and lack terminations. No attached fertile structures have been found on laterals of larger axes. Two possibilities exist for these axes: (1) the narrow ones represent lateral or distal regions of the larger, strongly ribbed axes, given that the lateral branches attached to wide ribbed axes are similar in morphology and size to the isolated ones, or (2) the wider ribbed and narrow axes represent two different entities. Many of the narrower to mid-sized axes exhibit regions of permineralization by pyrite. Additionally, large pyrite nodules surround some axes in which cell structure is preserved, where axis width can be measured only in cross section. Most are 4e7 mm wide. Several have been sectioned into approximately 1-mm-thick wafers, polished and etched, and are currently being studied. Longitudinal sections are in preparation. Anatomy from the narrow axes (4 mm diameter) mostly exhibit a rounded haplostele, 0.54 mm wide, in which the central protoxylem is often represented by a line of smaller cells, which in turn is surrounded by metaxylem composed of polygonal shaped cells 20e30 mm in diameter radially and 10e20 mm tangentially (Plate IV, 3e5). Formation of lateral branches involves enlargement at one end of the linear protoxylem and associated metxaylem, followed by separation of a smaller, usually round to oval lateral trace (Plate IV, 3 and 5). Serial sections obtained from the fertile branch system, starting below lateral branch production and continuing through and past the departure of the lateral branch, show a similar organization, although the lateral trace, while initially round, becomes less so farther from the base. Details will be provided in a future report. Among the permineralized axes obtained from pyrite nodules are some that demonstrate aligned xylem, multiplicative divisions, and spaces that may represent putative rays (Plate IV, 6 and 7). Axis diameter measured in thin sections of these nodules ranges from 4 to 8 mm, thus falling in the upper range of smaller axes and the lower range of larger ribbed ones. The circular to oval centrarch haplostele has a central region of presumed protoxylem, often represented by a line, but in a few sections by an elongate oval region of small cells 8e14 mm (Plate IV, 7). This area is surrounded by metaxylem 20e40 mm in diameter radially and 22e39 mm in diameter tangentially. Surrounding these cells are larger, aligned, square tracheids, 18e44 mm in radial diameter, 17e25 mm in tangential diameter, and up to 15 cells deep. Anticlinal divisions occur within this layer frequently, some within the first few aligned cells. Spaces that could represent rays are also present, although not yet demonstrated as single walled in longitudinal section. A few sections exhibit the beginnings of lateral trace departure (Plate IV, 6). Protoxylem expands, metaxylem proliferates around it, and both

29

become separate from the remainder of the stele. The aligned cells rearrange to surround the trace, which now appears as a small bulge to one side of the stele. In one sequence, the bulge departs, forming a small circular lateral trace lacking any aligned cells. Preliminary scanning electron miroscopic studies demonstrate that scalariformbordered pits with multiperforate apertures, as well as circular or circular bordered pits, are present in metaxylem (Plate IV, 8 and 9). Additional investigation about pitting and other features is under way. 3.4.2.1 Extra-xylary tissues All of these axes consistently exhibit an outer region of at least four or five layers of thick-walled cells, the layers being differentially thickened and forming a scalloped pattern to the outside (¼ribbing?). Most are compressed, and on one side of the axis, this sterome typically is broken apart with thinner areas being sites of breaks (Plate IV, 4). Might the thinner areas represent sites of stomata? Where lateral branches are present, a similar sterome is observed. More data are needed in order to better understand the relationship between the two types of axes and anatomy, but this information strongly indicates they are parts of the same plant.

4. COMPARISONS Armoricaphyton is very similar in morphology, anatomy of primary tissues, pitting type, and mode of lateral trace formation to anatomy recorded for the genus Psilophyton, and the presence of secondary xylem was a major basis for recognizing these plants as a separate taxon. The amount of data available on anatomical variation, including details relating to lateral branch formation in many species of Psilophyton, is limited, with the exception of P. dawsonii and P. coniculum, both of which are mainly known from serial peels. Thus more detailed comparisons have not been possible (but see Gaspé plant later). The unnamed New Brunswick plant A differs considerably in shape of stele, and possibly in details of lateral trace emission from Psilophyton, although morphologically it is represented by slender ribbed axes similar in branching pattern to that taxon. It will be named a new genus in a future report. The second type of anatomy observed in nodules from New Brunswick (Section 3.4.1) is represented by a very limited number of sections and remains unnamed, pending obtaining additional data on pitting pattern and possible morphology. The anatomy is interesting in that it demonstrates much more probable secondary xylem than any of the previously described taxa. It is somewhat similar to Franhueberia, but cell size, available data about rays, and lack of information on pitting pattern and conclusive information on xylem maturation preclude closer comparison. Dichotomous division is unknown in Franheuberia.

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SECTION j I Early Land Plants: Innovations and Adaptations

In regard to the axes obtained from Gaspé (Section 3.4.2), additional preparations are needed to better understand if the large and small axes are related. The smaller ones appear very similar anatomically to Psilophyton species, while the ones with putative secondary tissues are more similar to Armoricaphyton, even though the former are younger. The Gaspé specimens differ, based on current information, in that the lateral traces do not exhibit any aligned cells at their base. If both wide and narrow axes of the Gaspé specimens are part of the same plant, it is reasonable to consider the possibility that some fossils included in the genus Psilophyton might possess more basal regions with secondary xylem, while more distal axes possess only primary xylem. Not finding this condition previously may be a result of which plant parts were sampled during sedimentation processes and burial and of which plant parts are collected and identified. There is a bias toward obtaining fertile axes since sporangial characters and position are conclusive characters in the absence of anatomy. Alternatively, very similar looking plants may possess sufficient anatomical differences (e.g., one with primary xylem only, the other with aligned/secondary xylem) to be recognized as separate taxa.

5. DISCUSSION 5.1 Implications Criteria for recognizing secondary xylem, as applied in instances of aligned cells in younger plants, are met by the already described Early Devonian plants, representing at least three different genera, with the material under study possibly adding more. Most exhibit pitting and/or other features (xylem maturation) that indicate they are likely basal euphyllophytes, at the trimerophyte grade. Franhueberia is interesting in that the P-type pitting is less predominant, with circular and circular bordered pitting being more predominant, especially in primary xylem tracheids, presaging the types of pitting patterns observed in younger plants. Pitting occurs on both radial and tangential walls in both primary and secondary xylem, in contrast to some younger plants (gymnosperms). It is unknown if the cambium producing secondary tissues in these plants is unifacial or bifacial and, if unifacial, determinate. Gerrienne et al. (2011: supplemental data) show cells that may represent cambial initials located outside of aligned ones in Armoricaphyton and New Brunswick plant A, but they are poorly preserved. For some younger plants, such as Rhacophyton, anticlinal divisions are not mentioned, the interpretation being based on presence of rays. Some lepidodendraleans and Sphenophyllum are interpreted as accommodating increasing circumference by tangential enlargement of cambial initials and, in some cases, apical intrusive growth (Cichan, 1985; Cichan and Taylor, 1990) rather than anticlinal divisions.

Cichan and Taylor (1990) note that plants with unifacial cambia exhibit different patterns of development in their secondary tissues. Additionally, such cambia in Carboniferous plants, and possibly others, appear determinate and are distinct from the bifacial cambia present in lignophytes, as best as has thus far been determined. Arrangement of secondary xylem in Xinicaulis shows that tracheids are very thick walled. Limited data about rays and pitting are presented, and no information on the presence/absence of anticlinal divisions is given. The splitting apart of a vascular strand, with proliferation of parenchyma, and emission of root traces or putative branch traces requires further description and interpretation but clearly is interesting and different developmental patterns are occurring in this plant.

5.1.1 Aligned Cells Considered Primary in Origin-Aligned Metaxylem Versus Vascular Cambium-Derived Secondary Tissues In the absence of multiplicative divisions or rays, aligned cells present in some living and fossil plants have been interpreted as aligned metaxylem. Explanations of how these are produced vary and are not always satisfactory. In living plants, broad apices in some plants have a primary thickening meristem that results in the production of aligned cells with specific orientations, clearly demonstrated in developmental studies (Esau, 1943; DeMason, 1983; Soh, 1990) as in many monocots and possibly Isoetes, and these appear very convincingly primary in origin. Interpretation of the limited amount of aligned xylem in the extant ophioglossalean Botrychium has been interpreted by some researchers as primary and by others as secondary. Recently, Rothwell and Karrfalt (2008) have interpreted them as primary, suggesting they result from a prolonged period of patterned apical cell division before differentiation of the procambium or any primary tissue (Rothwell and Karrfalt, 2008). Again, this is convincing, but why would such divisions occur? Are they tied to aspects of the overall unusual growth pattern observed in this taxon or to the type of apical meristem present? In fossils, aligned metaxylem (e.g., aligned cells but no rays) has been described in regions of P. dawsonii axes where considerable xylem expansion occurs before the emission of closely successive lateral branches (Banks et al., 1975). Radially aligned cells also are described from an isolated vascular strand of P. crenulatum (Doran, 1980). What mechanism(s) might have resulted in aligned cells in these comparatively slender axes, especially in only certain parts of the plant? Aligned cells that apparently lacked rays were similarly interpreted for the Late Devonian Rhacophyton zygopteroides by Leclercq (1951). However, Schultka (1978) and Dittrich et al. (1983) demonstrated the presence of rays

Early Devonian Woody Plants and Implications for the Early Evolution of Vascular Cambia Chapter j 2

among these aligned cells and currently R. zygopteroides, R. condrusorum, and R. ceratangium are interpreted as possessing a limited amount of secondary xylem. For some cladoxylopsids with complex multistranded steles, a limited amount of aligned xylem around each (or some) meristele(s) occurs, but in most taxa, it is unclear if it is primary or secondary (Boyer and Matten, 1996; Giesen and Berry, 2013). One cladoxylopsid, cf. Xenocladia sp. from the lower Upper Devonian (Meyer-Berthaud et al. 2004) of Morocco, exhibits aligned cells with rays and multiplicative divisions considered to be a result of vascular cambium activity. Other axes attributed to Xenocladia exhibit aligned cells that apparently do not demonstrate rays (Arnold, 1940, 1952; Mustafa, 1980; Lemoigne and Iurina, 1983). Further anatomical information would greatly contribute to better understanding whether these aligned cells are primary or secondary in origin. Such knowledge may also aid in understanding the growth pattern (or patterns) of the recently described Middle Devonian trees mostly related to cladoxylopsids, all of which are interpreted as having considerable parenchymatous tissue in their trunks and peripherally located xylem. Differing hypotheses on how these trees grew (Fairon-Demaret and Berry, 2002; Meyer-Berthaud et al., 2010; Giesen and Berry, 2013) provide varying ideas for nonlignophyte tree growth patterns. The Meyer-Berthaud et al. (2010) hypothesis involving predominantly primary growth is largely based on the noncladoxylopsid Pietszchia, although the authors include limited secondary tissues that did not result in stem diameter increase as part of the model. The Giesen and Berry (2013) hypothesis, superseding the Fairon-Demaret and Berry (2002) model for Pseudosporochnus, is based on compressions of Calamophyton trees (linked with Duisbergia trunks for which anatomy is known) and, to some extent, information about Eospermatopteris trunks, in which secondary growth (qualified as aligned xylem or secondary-like growth) is considered important in expansion of the basal region. Just what is the so-called secondary growth in these plants? This is addressed in part by the recent description of Xinicaulis (Xu et al., 2017), which indicates some plants presently included in cladoxylopsids exhibit considerable secondary growth in a unique fashion as described earlier.

5.1.2 Unifacial cambia In plants producing secondary xylem, especially those with an unifacial vascular cambium, only a limited amount of secondary xylem is produced. Why? Are they determinate in all cases as is suggested by the presence and pattern of cells outside the secondary xylem in lepidodendrids, calamites, and Sphenophyllum (Cichan and Taylor, 1990 and references therein)? Lack of preservation of tissues outside of xylem in other taxa precludes that or alternative interpretations.

31

Size does not appear to be a factor in the extent of cambial activity; discussion of growth models of these various plants might indicate that to some extent this is part of their intrinsic ontogenetic program. An additional question is, If developmental stages were available, might we be able to determine what cells in protostelic taxa regained stem cell function to become cambial initials?

5.2 Evolution of Cambium Gensel and Andrews (1984) suggested that cambial evolution might have occurred stepwise, with sequential acquisition of characters leading to the predominant forms known in plants today. It might be simplistic, but perhaps aligned cells considered primary in nature may provide evidence for an initial change in cell division rates or extent at the apex or in the procambium. Retention of residual procambial cells or signaling of some living cells to resume division predominantly periclinally might be needed to establish a cambium. Perhaps the anomalies cited by Hoffman and Tomescu (2013) such as sphenophylls sans multiplicative division, Botrychium with no rays, but only aligned xylem, support that this is one way a vascular cambium might have evolved. The nature of shoot apical meristem construction might be important in these plants.

5.3 Information From Developmental Studies Developmental data thus far suggest that auxins, cytokinins, and several other growth regulators influence transcription of genes and play an important role in vascular cambium initiation and function in the few extant model organisms thus far studied and that similar genes and transcription factors important in the functioning of meristems, as well as additional ones, are involved in the initiation and division of cambial initials and differentiation of their products (Spicer and Groover, 2010; Brackmann and Greb, 2014; Niemanen et al., 2015). It is interesting that in a small plant such as Arabidopsis, secondary xylem, when formed, lacks rays, although the latter will form under weight-induced conditions (Mazur and Kurczynska, 2012). It is unknown if they function as do rays in other seed plants. It is difficult to extrapolate from the small number of distantly related extant taxa to patterns that might be considered applicable to 400-milion-year-old plants. But as these studies progress, this information might aid in better understanding the existence and function of vascular cambia in general and of unifacial cambia as seen in fossils in particular. It also would be interesting to examine gene expression in living plants with aligned metaxylem to learn whether similar or different genetic mechanisms are involved.

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SECTION j I Early Land Plants: Innovations and Adaptations

5.4 Psilophyton- One Taxon or Several? Some of the plants described here again raise questions about the monophyly of species included in Psilophyton. It is increasingly evident that slender dichotomizing axes of a Psilophyton type may represent several different Early Devonian, presumably basal euphyllophyte taxa, differing in the type of anatomy and/or morphology present. It also is evident, as a result of cladistic studies, that the genus Psilophyton is paraphyletic (Kenrick and Crane, 1997) and, further, that some Psilophyton species not included in phylogenetic analyses differ in subtle details of branching architecture or are simply too poorly preserved to be attributed to that taxon (Wang and Berry, 2001; Hao and Xue, 2013; Gensel, 2017). A contributing factor to taxon delimitation is that extent and type of preservation are highly variable among those species described. Morphological resemblance of Armoricaphyton, the New Brunswick plant type A, and the Gaspé plant(s) to Psilophyton axes has already been noted. The new collections described here, containing a mixture of narrow and wide axes, with considerable anatomy preserved, adds further complexity to the problem of what these plants represent, because fertile specimens in the new collection, with narrow axes, strongly resemble those described as P. forbesii (Gensel, 1979).

5.5 Size is Decoupled From Secondary Tissues in These Early Plants A number of Early Devonian plants a magnitude larger, possessing axes 1 cm or more wide, and up to a least 1 m in height (probably more), with numerous lateral branches of varying length that occur singly or in pairs, exhibit a deeply lobed stele with only primary tissues. Examples include the new trimerophyte-like plant of Gensel (1984), cf. Pertica sp. (Gensel, unpublished data) and Gothanophyton (Remy and Hass, 1986). Branching architecture in these plants also is more predictable. This contributes to the variety of anatomical variation seen among different growth architectures in Early to Middle Devonian plants.

6. CONCLUSIONS The Late Early Devonian to Early Middle Devonian is a time of major change in plant types, architectures, and now occurrence of primary versus secondary tissues. It appears that larger size does not necessarily correlate with occurrence of “woody tissues.” But early stages in cambial evolution by Late Pragian at least alter thinking about the timing of evolution of the vascular cambium and may affect ideas about affinities and growth patterns in a variety of plants. There also appear to have been many “experiments” in cell types or mode of accommodating even minor

changes in stelar enlargement in plants with secondary tissues from Early Devonian to Carboniferous, with the Middle Devonian advent of a bifacial vascular cambium establishing a pattern that remains fairly consistent, at least in terms of cell types but perhaps not in ontogenetic patterns, throughout lignophytes. Clearly much remains to be learned about the early history of vascular cambia.

ACKNOWLEDGMENTS This work was supported by funds from the George W. Cooley Fund, North Carolina Botanical Garden, University of North Carolina, Chapel Hill, NC. The author acknowledges the assistance of Ms. Susan Whitfield for artwork and image advice and Brian Nalley for aid in macrophotography. Appreciation is extended to several colleagues for many stimulating discussions, and to P. Gerrienne for providing some images of Armoricaphyton.

REFERENCES Arnold, C.H., 1940. Structure and relationships of some Middle Devonian plants from Western New York. American Journal of Botany 27, 57e63. Arnold, C.H., 1952. Observations on fossil plants from the Devonian of Eastern North America. VI. Xenocladia medullosina Arnold. Contributions from the Museum of Paleontology. University of Michigan IX (10), 297e309. Banks, H.P., Leclercq, S., Hueber, F.M., 1975. Anatomy and morphology of Psilophyton dawsoni, sp. n. from the late Lower Devonian of Quebec (Gaspé) and Ontario, Canada. Palaeontographica Americana 8 (48), 77e127. Bannan, M., 1934. Origin and cellular character of xylem rays in gymnosperms. Botanical Gazette 96 (2), 260e281. Beck, C.B., Stein, W.E., 1993. Crossia virginiana gen. et sp. nov., a new member of the Stenokoleales from the Middle Devonian of southwestern Virginia. Palaeontographica B229, 115e134. Berry, C.M., Wang, Y., 2006. Eocladoxylon (Protopteridium) minutum (Halle) Koidzumi from the Middle Devonian of Yunnan, China: an early Rhacophyton-like plant? International Journal of Plant Sciences 167 (3), 551e566. Boyer, J.S., Matten, L.C., 1996. Anatomy of Eospermatopteris eriana from the Upper Middle Devonian (Givetian) of New York. International Organisation of Palaeobotany 5, 13. Brackmann, K., Greb, T., 2014. Long- and short-distance signaling in the regulation of lateral plant growth. Physiologia Plantarum 151, 134e141. Cai, C.-Y., Chen, L.-Z., 1996. On a Chinese Givetian lycopod, Longostachys latisporophyllus Zhu, Hu and Feng, emend: its morphology, anatomy and reconstruction. Palaeontographica Abt B 238, 1e43. Cichan, M., 1985. Vascular cambium and wood development in Carboniferous plants. I. Lepidodendrales. American Journal of Botany 72 (8), 1163e1176. Cichan, M.A., Taylor, T.N., 1982. Vascular cambium development in Sphenophyllum: a Carbonifeorus arthrophyte. International Association of Wood Anatomists Bulletin (3), 155e160. Cichan, M.A., Taylor, T.N., 1990. Evolution of cambium in geologic timea reappraisal. In: Iqbal, M. (Ed.), The Vascular Cambium. John Wiley and Sons Inc., New York, pp. 213e228.

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DeMason, D., 1983. The primary thickening meristem: definition and function in monocotyledons. American Journal of Botany 70 (6), 955e962. Dennis, R.L., 1974. Studies of paleozoic ferns: Zygopteris from the Middle and Upper Pennsylvanian of the United States. Palaeontographica B 148, 96e136. Dittrich, H.S., Matten, L.C., Phillips, T.L., 1983. Anatomy of Rhacophyton ceratangium from the Upper Devonian (Famennian) of West Virginia. Review of Palaeobotany and Palynology 40, 127e147. Doran, J.B., 1980. A new species of Psilophyton from the Lower Devonian of northern new Brunswick, Canada. Canadian Journal of Botany 58, 2241e2262. Esau, K., 1943. Origin and development of primary vascular tissues in seed plants. The Botanical Review 9 (3), 125e206. Fairon-Demaret, M., Berry, C.M., 2002. The architecture of Pseudosporochnus nodosus Leclercq et Banks: a Middle Devonian cladoxylopsid from Belgium. International Journal of Plant Sciences 163 (5), 699e713. Gensel, P.G., 1979. Two Psilophyton species from the Lower Devonian of Eastern Canada with a discussion of morphological variation within the genus. Palaeontographica B 168, 81e99. Gensel, P.G., 1984. A new Lower Devonian plant and the early evolution of leaves. Nature 309 (5871), 785e787. Gensel, P.G., Andrews, H.N., 1984. Plant Life in the Devonian. Praeger Press, New York, 380 pp. Gensel, P.G., 2017. Silurian-Devonian origins of ferns and lycophytes-what we know, what we need to find out. Fern Gazette 20 (6), 217e242. Gerrienne, P.M., Gensel, P.G., 2016. New data about anatomy, branching, and inferred growth patterns in the early Devonian plant Armoricaphyton chateaupannense, Montjean-sur-Loire, France. Review of Palaeobotany and Palynology 224, 38e53. Gerrienne, P., Gensel, P.G., Strullu-Derrien, C., Lardeux, H., Steemans, P., Prestianni, C., 2011. A simple type of wood in two early Devonian plants. Science 333 (6044), 837. Giesen, P., Berry, C.M., 2013. Reconstruction and growth of the early tree Calamophyton (Pseudosporochnales, Cladoxylopsida) based on exceptionally complete specimens from Lindlar, Germany (Mid-Devonian): organic connection of Calamophyton branches and Duisbergia trunks. International Journal of Plant Sciences 174 (4), 665e686. Hao, S.-G., Xue, J., 2013. The Early Devonian Posongchong Flora of Yunnan- a Contribution to an Understanding of the Evolution and Early Diversification of Vascular Plants. Science Press, 366 pp. Hoffman, L.A., Tomescu, A.M.F., 2013. An early origin of secondary growth: Franhueberia gerriennei gen. et sp. nov. from the Lower Devonian of Gaspé (Quebec, Canada). American Journal of Botany 100, 754e763. Kenrick, P., Crane, P.R., 1997. The Origin and Early Diversification of Land Plants: A Cladistic Study. Smithsonian, Washington. Leclercq, S., 1951. Étude morphologique et anatomique d’une Fougère du Dévonien Superieur. Annales de la Societe Geologique de Belgique, Memoires XIV (3), 39 pp. Lemoigne, Y., Iurina, A., 1983. Xenocladia medullosina CH.A. Arnold 1940, 1952 du Dévonien. Palaeontographica 186B, 81e120. Mazur, E., Kurczynska, E.U., 2012. Rays, intrusive growth, and storied cambium in the inflorescence stems of Arabidopsis thaliana (L.) Heynh. Protoplasma 249, 217e220.

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Meyer-Berthaud, B., Rücklin, M., Soria, A., Belka, A., Lardeux, H., 2004. Frasnian plants from the Dra valley, southern anti-atlas, Morocco. Geological Magazine 141 (6), 675e686. Meyer-Berthaud, B., Soria, A., Decombeix, A.-L., 2010. The land plant cover in the Devonian: a reassessment of the evolution of the tree habit. In: Vecoli, M., Clement, G., Meyer-Berthaud, B. (Eds.), The Terrestrialization Process: Modeling Complex Interactions at the Biospheregeosphere Interface. Geol. Soc. London, Spec. Pub. 339, pp. 59e70. Moment, N., Decombeix, A.-L., Gerrienne, P., Prestianni, C., 2016. New Information, including anatomy of the secondary xylem, on the genus Brabantophyton (Stenokoleales) from Ronquières (Middle Devonian, Belgium). Review of Palaeobotany and Palynology 234, 44e60. Mustafa, H., 1980. Beiträge zur Devonflora IV. Argumenta Palaeobotanica 6, 115e132. Niemanen, K., Blomster, T., Helariutta, Y., Mahonen, A., 2015. Vascular cambium development. In: The Arabidopsis Book. Amer. Soc. Pl. Phys, p. e0177. https://doi.org/10.1199/tab.0177. Phillips, T.L., Galtier, J., 2005. Evolutionary and ecological perspectives of Late Paleozoic ferns, Part 1. Review of Palaeobotany and Palynology 135 (3), 165e203. Remy, W., Hass, H., 1986. Gothanophyton zimmermanni nov.gen., nov. spec., eine Pflanze mit komplexem Stelar-Korper aus dem Emsian. Argumenta Palaeobotanica 7 (9), 9e69. Rothwell, G.W., Karrfalt, E.E., 2008. Growth, development, and systematics of ferns: does Botrychium s.l. (Ophioglossales) really produce secondary xylem? American Journal of Botany 95 (4), 414e423. Schultka, S., 1978. Beiträge zur Anatomie von Rhacophyton condrusorum Crepin, Argumenta Palaeobotanica 5, 11e22. Soh, W.Y., 1990. Origin and development of cambial cells. In: Iqbal, W. (Ed.), The Vascular Cambium, pp. 37e62. Soria, A., Meyer-Berthaud, B., Scheckler, S.E., 2001. Reconstructing the architecture and growth habit of Pietzschia levis sp. nov. (Cladoxylopsida_from the Late Devonian of southeastern Morocco. International Journal of Plant Sciences 162 (4), 911e926. Spicer, R., Groover, A., 2010. Evolution of development of vascular cambia and secondary growth. Tansley Review. New Phytologist 186, 577e592. Strullu-Derrien, C., Kenrick, P., Badel, E., Cochard, H., Tafforeau, P., 2013. An overview of the hydraulic systems in early land plants. IAWA Journal 34 (4), 333e351. Strullu-Derrien, C., Kenrick, P., Tafforeau, P., Cochard, H., Bonnemain, J.-L., Le Herisse, A., Lardeau, H., Badel, E., 2014. The earliest wood and its hydraulic properties documented in 407-millionyear-old fossils using synchrotron microtomography. Botanical Journal of the Linnean Society 175, 423e437. Wang, Y., Berry, C.M., 2001. A new plant from the Xichong formation (Middle Devonian) South China. Review of Palaeobotany and Palynology 116, 63e85. Xu, H.-H., Berry, C.M., Stein, W.E., Wang, Y., Tang, P., Fu, Q., 2017. Unique growth strategy in the Earth’s first trees revealed in silicified fossil trunks from China. Proceedings of the National Academy of Sciences of the United States of America 114 (45), 12009e12014.

Chapter 3

Using Architecture Modeling of the Devonian Tree Pseudosporochnus to Compute Its Biomass Anae¨lle Dambreville, Brigitte Meyer-Berthaud, Jean-Franc¸ois Barczi, Anne-Laure Decombeix, Se´bastien Griffon and Herve´ Rey AMAP, Université de Montpellier, Montpellier, France

1. INTRODUCTION Terrestrial ecosystems represent important carbon sinks that interact closely with the atmosphere. Exchanges between these two carbon pools (terrestrial ecosystems and the atmospheric carbon pool) are significant drivers of the global climate whose evolution is a major concern today. The largest fraction of terrestrial carbon is stored in tropical forests and a way of assessing how much carbon is held in terrestrial ecosystems consists of estimating the above-ground biomass of tropical forests (Chave et al., 2004, 2014). In the southern warm-temperate paleolatitudes during the Middle Devonian, the pseudosporochnaleans formed the major canopy components of the earliest forests, which inhabited coastal wetlands. The best evidence for this assessment was an extensive horizon of numerous stump casts of Wattieza/Eospermatopteris reported in growth position in the Riverside Quarry, Gilboa, New York (Stein et al., 2012). This exceptional site allowed for a detailed study of the composition, spatial organization, and environmental conditions of the Givetian forest. Several other horizons with preserved stump casts were described from the Gilboa area. However, they provided less informative data for the purpose of the present study due to their more limited extension and the uncertain stump cast identification (Driese et al., 1997; Mintz et al., 2010; Retallack and Huang, 2011). Despite the abundance and exceptional preservation of some specimens, such as the Calamophyton/Duisbergia whole plants reported from the middle Eifelian of Lindlar, Germany (Giesen and Berry, 2013), the European sites

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00003-6 Copyright © 2018 Elsevier Inc. All rights reserved.

yielding pseudosporochnaleans are generally allochthonous and do not provide any satisfying information about the actual composition and spatial organization of the forests. The Pseudosporochnales that thrived in the Middle Devonian include four whole-plant genera: Pseudosporochnus (Potonié and Bernard, 1904), Lorophyton (FaironDemaret and Li, 1993), Wattieza/Eospermatopteris (Stockmans, 1968; Berry, 2000; Stein et al., 2007), and Calamophyton/Duisbergia (Kräusel and Weyland in Weyland, 1925; Giesen and Berry, 2013). These pseudosporochnaleans show a wide range of sizes, from approximately 2 m high in Calamophyton (Giesen and Berry, 2013) to 10 m in Wattieza (Stein et al., 2007), but they all share a similar architecture (Berry and Fairon-Demaret, 2002). The Lorophyton type specimen, which may have slightly exceeded 20 cm high in life conditions, has been interpreted as an immature individual (Fairon-Demaret and Li, 1993). Above ground, pseudosporochnaleans show an upright trunk bearing densely arranged branches (PBs) that are short-lived and form a terminal crown. Branches are generally digitate, meaning that they produce several secondary branches (SBs) of comparable diameters at very close intervals. These SBs may divide again. All orders of branches bear three-dimensionally arranged lateral branching systems (LBSs) that are either sterile or fertile, the latter ending with paired sporangia (Leclercq and Banks, 1962; Berry and Fairon-Demaret, 1997, 2002). Apart from size, the main characters discriminating the pseudosporochnalean genera include the branching patterns of the branches and of the LBSs and the morphology of the

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SECTION j I Early Land Plants: Innovations and Adaptations

fertile appendages (Berry, 2000). Anatomically, the Pseudosporochnales are characterized by a highly dissected primary vascular system embedded within a parenchyma and surrounded by a cortex of primary origin (Leclercq and Banks, 1962; Leclercq and Lele, 1968; Mustafa, 1978a; Stein and Hueber, 1989; Meyer-Berthaud et al., 2010). A secondary xylem can be present around the individual strands of primary xylem in both the stems and the branches (Mustafa, 1978a,b). Pseudosporochnus Potonié and Bernard 1904 is the most widely distributed genus of Pseudosporochnales. It has been described from numerous Middle to early Late Devonian deposits of Europe and North America (Potonié and Bernard, 1904; Lang, 1927; Leclercq and Banks, 1962; Stein and Hueber, 1989; Edwards et al., 2000). It has also been mentioned in species lists from northern Russia (Orlova et al., 2016), Siberia (Gutak et al., 2011), Kazakhstan (Iurina, 1988), and south China (Xiong et al., 2013). These identifications, however, are not supported by photographic evidence. Pseudosporochnus has been one of the most thoroughly studied whole-plant genera within the Pseudosporochnales, and numerous articles have been devoted to the morphology and the anatomy of its various parts (Taylor et al., 2009). Several attempts have been made to reconstruct its architecture. Revising the collection of specimens of Pseudosporochnus nodosus Leclercq and Banks 1962 collected by S. Leclercq in the late Eifelian of Goé III in the Liège Province (Belgium), Berry and Fairon-Demaret (2002) questioned the previous reconstructions of Pseudosporochnus made since Zimmermann (1930), including the often-reproduced one proposed by Leclercq and Banks (1962). They showed that branches of P. nodosus were tightly packed in alternating verticils and that they were not a late production of the trunk, in the manner of some arborescent lycopsids. Pseudosporochnus branches were emitted continuously since the early stages of their development. They were shed regularly and left a pattern of contiguous hexagonal scars on the trunks when they abscised. Although Berry and Fairon-Demaret (2002) have reported the occurrence of a 15-cm-wide trunk of P. nodosus, they proposed a “conservative” (according to their own terms) reconstruction showing a tree with a 2.5- to 3-m-high trunk, about 10 cm in diameter proximally, and resembling the Lorophyton type specimen during its early growth stages. Our modeling of Pseudosporochnus is based on this reconstruction. The first goal of this report is to detail the different steps of the modeling of Pseudosporochnus and the simulation of its morphological changes during growth by using the AmapSim architectural simulator. A second goal is to provide a realistic estimate for the biomass of a Pseudosporochnus tree and of its individual components at each growth stage. The last objective is to extend these calculations at the

scale of a forest, as a preliminary step toward an estimate of the terrestrial carbon pool during the Middle Devonian, at a time when the atmospheric partial pressure of carbon dioxide is undertaking a significant decline.

2. MATERIAL Fifty-eight specimens of P. nodosus from the collections of the University of Liège were observed and measured: ULg11, 15, 15bis, 19, 23, 158, 217, 317, 339, 383, 473, 656, 695, 695bis, 699, 1410, 1412, 1413, 1416, 1417, 1420, 1422, 1423, 1426, 1428e1431, 1623, 1671B, 1679A, 1687A, 1688B, 1709, 1715, 1736, 1739A, 1741, 1744A, 1756B, 1761B, 1761Bbis, 4957, 4988, 4995, ULgX1-6, X8-10, and X12-15. They consist of fragments of trunks (T), PBs, SBs, and LBSs preserved as adpressions. They were collected by Suzanne Leclercq in the 1950s from the Brandt Quarry at Goé (Belgium). The lithology and age of the fossiliferous beds are detailed in Leclercq and Banks (1962) and Berry and Fairon-Demaret (1997, 2002).

3. MODELING PSEUDOSPOROCHNUS WITH AMAPSIM 3.1 AmapSim Software AmapSim proposes a conceptual model and a computer simulator based on plant architecture concepts to dynamically simulate tree growth (Barczi et al., 2008, http:// amapstudio.cirad.fr/soft/amapsim/start). Basic assumptions are the following: (1) a plant, and especially a tree, is a strongly organized three-dimensional branched system. It is made of the addition of elementary components corresponding to different levels of organization, such as axes, growth units when growth is rhythmic, and internodes (Barthelemy and Caraglio, 2007). (2) A plant grows during its entire life due to the coordinated functioning of its meristems. (3) Meristems contribute to apical growth (i.e., the addition of elementary components) and to branching. These processes cease when the meristems die or become inactive. (4) Every meristem has a specific capability to perform growth and branching and a specific probability to cease functioning. These properties may evolve along its life, and their combination is indexed with a numerical value called “physiological age.” Each meristem is born with an initial physiological age that depends on its location and on the developmental stage of the plant (i.e., juvenile, mature, senescent). This value fixes the initial vigor of the meristem. The physiological age value may change during the meristem life, thus providing changing properties to the basic processes of growth and branching. A plant is simulated as a collection of meristems that run the same algorithm with parameter values indexed on the current physiological age of each meristem. The outputs of

Modeling Pseudosporochnus Chapter j 3

AmapSim are three-dimensional botanically realistic plant shapes that may be drawn at all growth stages and that also may allow for some calculations on the virtual plants. The way to model a plant like Pseudosporochnus with AmapSim consists of designing its architectural unit, assessing the number of physiological age values necessary to parametrize the functioning of every meristem class along their lifespan, and inputting some control parameter values obtained from measurements.

FIGURE 3.1 Pseudosporochnus architectural unit. Diagram showing the topological arrangement of the tree components.

3.2 Pseudosporochnus Architectural Unit The architectural unit of Pseudosporochnus is defined by the number of axis categories recognized in this tree, their relative position, and their main morphological characters (Fig. 3.1, Table 3.1). Based on the information provided by Berry and FaironDemaret (2002) in their reconstruction of P. nodosus and our own observations and measurements, we recognize three categories of axes: (1) the trunk (abbreviated T), (2) the PBs, (3) the SBs resulting from the digitate branching of the PB axes (Fig. 3.1). SBs of Pseudosporochnus may branch dichotomously, but this pattern is not as common as in Calamophyton, for example. In this report, therefore, we do not take into account any additional category of branches. LBSs are borne on the PBs and the SBs (Fig. 3.1). They are considered as determinate organs (i.e., appendages consisting of a stalk and a branched part; Fig. 3.1). They are sterile (SLBS) or fertile (FLBS). Pseudosporochnus does not produce any leaves. Therefore, in our computer simulation, a trunk internode is considered to be the length between two successive verticils of PBs and a branch internode (PB or SB internode) is the length between two successive LBSs of this branch. Pseudosporochnus is considered as having an indeterminate trunk growth; growth is determinate for all the other categories of components (Table 3.1). The apical meristems of the PBs produce a succession of PB-type internodes up to the level of digitate branching. The apical meristems of the SBs produce a succession of SB-type internodes, whereas distally we assume that they lose part of their morphogenetic potential and produce LBSs. The trunk of Pseudosporochnus produces only PBs that are tightly arranged in alternating successive verticils (Table 3.1). Five contiguous PBs are borne per verticil as

TABLE 3.1 Pseudosporochnus Architectural Unit Trunk

Primary Branch (PB)

Secondary Branch (SB)

Lateral Branching System (LBS)

Growth

Indeterminate

Determinate

Determinate

Determinate

Abscission

e

Yes

No

Yes

Internode

Short (contiguous branches)

Shorter apically

Shorter apically

e

Branching

Bears PB only

Bears SBs distally, and sterile LBSs laterally

Bears sterile and fertile LBSs laterally and distally

e

Arrangement

Self-supporting

5 PBs per verticil

2e4 (mean 3) SBs digitately

Alternate

Geometry

Conical

Conical

Conical

Three-dimensional

Angle

Orthotropic

Acute then wide

Acute

Acute then wide

Morphological and developmental features of the tree components.

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SECTION j I Early Land Plants: Innovations and Adaptations

along the fragment used by Berry and Fairon-Demaret (2002) for their reconstruction. PBs produce digitately arranged SBs distally and sterile LBSs laterally (Fig. 3.1). Twenty specimens with PBs observed in the Liège collections produced two to four SBs arranged in a plane (Table 3.1). A single PB, considered as an exception, bears six SBs. SBs bear both SLBSs and FLBSs. All axes (T, PBs, SBs) taper distally and are conical. The LBSs are threedimensional (Table 3.1). In Lorophyton type specimen, the youngest PBs are borne acutely at the trunk apex; older ones are borne at a wider angle (Berry and Fairon-Demaret, 2002). This variation in the insertion angle of the PBs is also observable in the Wattieza specimen from Gilboa (Stein et al., 2007) and in the complete specimens of Calamophyton described from Lindlar (Giesen and Berry, 2013). In Pseudosporochnus, we hypothesize similar changes in the angle between the trunk and the PBs (a1 between T and PB in Fig. 3.1) and in the

angle between the SBs and the LBSs (a3 between SB and SLBS or FLBS in Fig. 3.1) (Table 3.1).

3.3 Geometrical Parameters of Pseudosporochnus The geometrical parameters of the model (diameter and length of the components, branching angles) are either assessed from previous reports (e.g., Leclercq and Banks, 1962; Berry and Fairon-Demaret, 1997, 2002) or calculated from our measurements on the specimens of P. nodosus (Fig. 3.1). These specimens are considered as representing mature growth stages. Initial values of the parameters (i.e., when the tree components are initiated and before they grow to their final size) are estimated by using the type specimen of Lorophyton. The values used here for modeling a 3-m-high Pseudosporochnus are summarized in Table 3.2.

TABLE 3.2 Parameter Values and Physiological Ages of the Pseudosporochnus Components

Trunk (T)

Primary Branch (PB)

Secondary Branch (SB)

Sterile Lateral Branching Systems Borne on PBs (SLBS1)

Sterile Lateral Branching Systems Borne on SBs (SLBS2)

Fertile Lateral Branching Systems (FLBS)

0.51

0.89

1.61

1.81

2.94

3.66

Internode initial length (Li, cm)

1.50 (Berry and Fairon-Demaret, 2002)

0.69 (Lorophyton)

0.26

Internode final length (Lf, cm)

1.50 (Berry and Fairon-Demaret, 2002)

0.75

0.80

Internode initial diameter (di, cm)

1.50 (Lorophyton)

0.15 (Lorophyton)

0.14

Internode final diameter of T, PB, SB; width of SLBS1, SLBS2, FLBS (df, cm)

9.36

1.99

0.66

Conicity (mm/cm)

0.32

0.60 (basal) 0.55 (apical)

0.15

Final length (cm)

297

33.03

44.87

Number of internodes

198

48

84

Physiological age

1e99

101e148

201e284

301 and 501

302 and 502

303 and 401

10 (Lorophyton) to 40 (mature)

21.08 (apical zone of PBs)

40.00 (apical zone of PBs)

24.16 (apical zone of SB) to 36.24 (basal zone of SBs)

26.67 (apical zone of SB) to 38.18 (basal zone of SBs)



Insertion angle (a, )

Values in bold have been computed.

Modeling Pseudosporochnus Chapter j 3

3.3.1 Internode length and diameter (Fig. 3.2) Because branch scars are contiguous along the trunk specimens of P. nodosus, we assume that the increase in length of the trunk results mainly from the addition of internodes rather than from their increase in length. For that reason, the initial and final lengths of the trunk internodes are similar in our model. They correspond to the vertical dimension of a branch scar in the specimen used by Berry and Fairon-Demaret (2002) for their restoration. For the final diameter of the trunk internodes, we use the mean of the larger diameter of the trunks of the Liège collections. For the initial diameter of the trunk internodes, we use the diameter of the main stem of the Lorophyton type specimen just below the crown of branches. The final internode lengths of the PBs and SBs are calculated by dividing the preserved length of the branches by the number of LBSs they show. These measures are overestimated because the LBSs hidden in the matrix are not taken into account. For the final diameter of the PB and

39

SB internodes, we use the mean of the larger diameter of these branches. The Lorophyton type specimen that shows PBs but is devoid of SBs is used to infer the initial length and diameter of the PB internodes of Pseudosporochnus. The length and diameter of the smallest internodes of the SBs of Pseudosporochnus in the Liège collections are used for the initial length and diameter of the SB internodes.

3.3.2 Number of internodes in each axis category The mean length of an axis is calculated from its conicity and its basal diameter. The mean number of internodes produced by the trunk and branches of Pseudosporochnus is calculated by dividing the mean length of these axes by the final length of their internodes.

3.3.3 LBSs The size of the SLBSs and FLBSs is estimated by using their mean length and width. Their probability of being

FIGURE 3.2 Measurements of the initial and final length and diameter of the internodes of the trunk and branches of Pseudosporochnus. Some initial measures are inferred from the Lorophyton type specimen whose above-ground part only is schematized here. i1, i2, i3: internodes 1, 2, 3; Li: initial length; Lf: final length; di: initial diameter; df: final diameter. Adapted from Fairon-Demaret and Li (1993).

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SECTION j I Early Land Plants: Innovations and Adaptations

sterile or fertile is calculated from their proportions in the specimens from the Liège collections.

3.3.4 Relative growth speed of the trunk and branches In this work, we hypothesize that, at a juvenile stage, the model of Pseudosporochnus tree is similar in size and shape to the 20-cm-high Lorophyton type specimen illustrated by Fairon-Demaret and Li (1993) and reproduced in Fig. 3.2. At 13 cm high (i.e., 4% of the total height of the tree trunk), the Lorophyton main stem (T) bears a 5.3-cmlong PB, and at 20 cm high (i.e., 7% of the total height of the tree trunk), a 12-cm-long PB. A linear regression therefore indicates that the first mature PB of the model, which is 33 cm long (Table 3.2), is produced on the trunk at 16% of its height. There is little evidence provided by the fossils for estimating the relative growth speed of the trunk and branches. Here we hypothesize that a branch measuring 12 cm, like the longest one preserved on the Lorophyton type specimen, is produced while the trunk produces two internodes and, therefore, increases in length by 3 cm (see Lorophyton internode length in Table 3.2). In this case, branches grow four times more quickly than the trunk.

3.4 Pseudosporochnus Physiological Age Indexing In Pseudosporochnus, the trunk and branches are conical and the number and type of components they produce at each node differ on a proximal-distal basis. To account for such variations, we choose the following indexing (Table 3.2, Fig. 3.3): 99 physiological age values for the trunk (from 1 to 99), 48 physiological age values for the PBs (from 101 to 148), 84 physiological age values for the SBs (from 201 to 284), and 2 physiological age values for the LBSs.

4. COMPUTING BIOMASS

(1997), the marattialean tree fern Psaronius (DP ¼ 0.076 g C/cm3) and the pteridosperm Medullosa (DM ¼ 0.049 g C/cm3). Stems and branches in these taxa are broadly comparable to those of the pseudosporochnaleans by their relative abundance of parenchyma and low percentage of vascular tissues.

4.2 Biomass of a Pseudosporochnus Stand There is no available information about the structure and tree density of a Pseudosporochnus forest. To estimate the carbon composition of a stand of Pseudosporochnus, we hypothesize that the tree density and relative spacing between individual trees have been close to that in the Gilboa forest of the Riverside Quarry. This assumption is based on the fact that the Wattieza/Eospermatopteris trees had a similar morphology to Pseudosporochnus with comparably narrow crowns and root systems. Based on Stein et al. (2012, Fig. 2), we calculated that the tree density was (1) 985 trees/ha when considering only the stumps definitively identified as Eospermatopteris by these authors, (2) 1292 trees/ha when considering stumps identified with both high and intermediate confidence, and (3) 2324 trees/ha, when considering all stumps including those identified with low confidence.

5. RESULTS 5.1 Simulating the Growth of Pseudosporochnus The modeled Pseudosporochnus is visualized at different growth stages calculated here as a percentage of development (Fig. 3.4; Supplementary Figure). The individual is seen in juvenile stage at 10% and 16% of its development with only PBs and corresponding LBSs. The 16% state corresponds to the stage in which PBs reach their maximal length. At 50% and 99%, PBs and SBs are developed. The two latter stages show a similar crown, and they differ only in the trunk size.

4.1 Biomass of a Pseudosporochnus Tree

5.2 Carbon Allocation in Pseudosporochnus

The biomass of a tree, or of its trunk, branches and LBSs, is calculated at every stage of growth with use of the Xplo software improved with a dedicated Groovy script (Griffon and de Coligny, 2014; http://amapstudio.cirad.fr). It is obtained by multiplying the total volume of the tree, or of its components, by a carbon density. In this report, we estimate that the carbon density of the Pseudosporochnus components may have been in the range of the carbon densities of the stems of two permineralized taxa of Pennsylvanian age analyzed by Baker and DiMichele

Carbon allocation patterns in a Pseudosporochnus tree are illustrated in Fig. 3.5 with calculations made with the carbon density of Medullosa (0.049 g C/cm3). Carbon allocation patterns show the same trends when using the carbon density of Psaronius but with carbon values multiplied by a factor of 1.55 (i.e., 0.076/0.049). The Pseudosporochnus components that accumulate the largest carbon content in the early stages of development are the PBs, then the trunk (T) at 40% development. At 99%, 83% of the biomass is contained in the trunk.

Modeling Pseudosporochnus Chapter j 3

41

Branches (PBs þ SBs þ LBSs) reach their maximal length at about the 30% development stage. The carbon accumulated in the crown does not change in the later stages; this is due to the constant values of the rhythm of branch production and shedding in our model. Fig. 3.6 differs from the previous one by analyzing the cumulative amount of carbon allocated to the tree. Whatever the growth stage in a tree that would have retained all of its branches, there is less carbon contained in the trunk than in the branches (PBs þ SBs þ LBSs), even when these are separated into PBs and SBs. The branches being relatively short, this is due to high branch density. The standing biomass of a Pseudosporochnus tree in its latest stage of development (99%) is 1300 g C when using Psaronius carbon density and 837 g C with Medullosa carbon density (Baker and DiMichele, 1997). When considering the cumulative carbon tree content during its lifetime, the total biomass of a Pseudosporochnus tree is 6524 g C when using Psaronius carbon density and 4211 g C with Medullosa carbon density.

5.3 Carbon Content and Biomass of a Community of Pseudosporochnus FIGURE 3.3 Physiological age indexing of the components of the Pseudosporochnus architectural model.

Calculations of the carbon content and above-ground biomass of a Pseudosporochnus tree stand are based on

FIGURE 3.4 Visualization of Pseudosporochnus at 10%, 16%, 50%, and 99% of its development.

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SECTION j I Early Land Plants: Innovations and Adaptations

6. DISCUSSION 6.1 Computer Models of Fossil Plant Architecture

FIGURE 3.5 Changes in the carbon content of a Pseudosporochnus tree and its components during growth. Calculations use the carbon density of Medullosa.

FIGURE 3.6 Cumulative changes in the carbon content of a Pseudosporochnus tree and its components during growth. Calculations use the carbon density of Medullosa.

the following assumptions: (1) the tree density in a Pseudosporochnus stand is similar to that of Wattieza/ Eospermatopteris trees in Riverside Quarry, State of New York; (2) all trees of the stand are in their mature stage, Pseudoporochnus trees being about 3 m high at 99% of development; and (3) considering the above-ground part of a tree, the carbon content represents 50% of its biomass (Martin and Thomas, 2011). Results are summarized in Table 3.3.

There have been few attempts to compute architectural models of fossil plants (Daviero et al., 2000; Daviero and Lecoustre, 2000; Daviero-Gomez et al., 2005; Hinz et al., 2010). One reason is that plants are modular organisms that are generally fragmented in the depositional environments. Reconstructing whole plant morphologies with such a record appears much more difficult than with determinate organisms like animals. A second reason is that the available modeling approaches may appear complex to a wide range of paleobotanists. We hope that the details provided here on the different steps of our approach are clear enough to be reproduced. The simulation software, packaged with the Pseudosporochnus parameter file, is freely available after request to [email protected]. It is compatible with Windows 64 bits OS later than NT. A user manual is also available to enable users to self-simulate and eventually adapt the parameter files to specific applications. One interesting attempt was proposed by Hinz et al. (2010) who reconstructed the plants forming a Late Jurassic forest from northwest China using the Greenworks Xfrog 3.5 software. The modeling of the Araucaria trees at three different ages (young, middle-aged, mature) required to generate individual models for each growth stage. Earlier, the AMAP 1 software was used by Daviero and Lecoustre (2000) to model the architecture of the arborescent equisetopsid Calamites multiramis and by Daviero-Gomez et al. (2005) to reconstruct the early land plant Nothia aphylla. A significant advantage of Amap 1 and of the AmapSim software used here is that they provide dynamic models of plant growth. This requires a reasonably good understanding of the growth patterns governing the coordinated functioning of the plant meristems. This part of the modeling process is certainly the most challenging one when reconstructing fossil plants.

6.2 Model Accuracy The 3-m-high simulated Pseudosporochnus corresponds to the tree reconstructed by Berry and Fairon-Demaret (2002). These authors, however, recognized that this reconstruction does not take into account the largest specimens. The actual trunks of P. nodosus may have exceeded the trunk of our model in average size, and their contribution to the standing biomass of the tree may therefore be underestimated in this report. The number of LBSs borne on the PBs and SBs is also underestimated and its correct assessment requires some refinement. The contribution of these elements to the total biomass of Pseudosporochnus is clearly underestimated.

Modeling Pseudosporochnus Chapter j 3

43

TABLE 3.3 Estimated Amount of Carbon and Above-Ground Biomass in a Pseudosporochnus Stand Whose Tree Density Is Similar to That of the Riverside Quarry Forest; Pseudosporochnalean Trees Identified With High Confidence (HC), Intermediate Confidence (IC), Low Confidence (LC) (Stein et al., 2012) Tree Density HC 985 trees/ha

IC 1292 trees/ha

LC 2324 trees/ha

Carbon content of a Pseudosporochnus stand; trees with a Psaronius carbon density (0.076 g C/cm3)

6.50 t C/ha

8.53 t C/ha

15.31 t C/ha

Above-ground biomass of a Pseudosporochnus stand (Psaronius carbon density)

13 t/ha

17.06 t/ha

30.62 t/ha

Carbon content of a Pseudosporochnus stand; trees with a Medullosa carbon density (0.049 g C/cm3)

4.26 t C/ha

5.59 t C/ha

10.03 t C/ha

Above-ground biomass of a Pseudosporochnus stand (Medullosa carbon density)

8.52 t/ha

11.18 t/ha

20.06 t/ha

There is no available fossil showing the distal part of a Pseudosporochnus trunk and its crown of branches. The shape of the crown is determined by the number of branches retained on the trunk, their length, the angle they form with the trunk until they are abscised, and their rigidity. The shape of the crown varies in the Pseudosporochnales, with that of Calamophyton looking relatively thicker, with mature branches more widely opened than that of Wattieza and Lorophyton (Fairon-Demaret and Li, 1993; Stein et al., 2007; Giesen and Berry, 2013). We are relatively confident in our assessment of the branch lengths of Pseudosporochnus. The other geometrical and growth parameters used in our model have been hypothesized to model a crown broadly similar to that of the Lorophyton type specimen when juvenile and that of Wattieza later. If our estimation of the rate of production versus shedding of the branches, that determines the number of branches forming the crown, were inaccurate, this would affect the contribution of the crown to the total biomass of the tree. We parametrized the early growth stages of Pseudosporochnus with the only pseudosporochnalean fossil suspected to be a juvenile, the Lorophyton type specimen. This is another limitation of our work as we had to assume that the trunk diameter of Pseudosporochnus increased markedly during tree growth, a process supported by Berry and Fairon-Demaret (2002) but that has not yet been demonstrated (Meyer-Berthaud et al., 2010). The other uncertain parameters in our work are related to carbon density, especially our assumptions that (1) all the components of Pseudosporochnus had the same density and (2) this density may have fallen in the range of values shown by two phylogenetically unrelated plants, Psaronius and Medullosa. Yet, in the present state of knowledge, we had no better alternative.

Finally, our estimate of the carbon density of a Pseudosporochnus tree stand using the information about the Wattieza forest of Gilboa is rather crude. Moreover, it assumes that all trees were at a similar growth stage and does not take into account the fact that the forest probably contained smaller trees. This can easily be refined when information about the structure of a Pseudosporochnus forest will be available.

6.3 Carbon Allocation in Pseudosporochnus Modeling the growth of Pseudosporochnus provides for the first time a realistic estimation of the biomass of a Devonian tree and of its different organs, both through the life of an individual and at any given moment in its development. The cumulative analysis provides evidence that, when considering the total lifetime of a Pseudosporochnus tree, the biomass is mostly allocated to the branches. The latter are regularly shed and form a litter, which is of high importance for the functioning of Middle Devonian ecosystems as it provides both a microhabitat and a food source. This is especially significant when considering that, in a context where lignin degradation is not common or even absent (Stubblefield et al., 1985; Taylor et al., 2015), Pseudosporochnus branches contained a relatively high proportion of nonlignified tissues (Stein and Hueber, 1989). Mintz et al. (2010) studied a paleosol exposing Eospermatopteris casts near Gilboa and interpreted the forest paleoenvironment as resource limited and “not prone to produce a high volume of organics.” The large amount of litter produced by Pseudosporochnus and, potentially, by other pseudosporochnaleans with a comparable architecture challenges this interpretation.

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SECTION j I Early Land Plants: Innovations and Adaptations

While the branches represent the highest allocation of biomass through the life of a tree, the architecture of Pseudosporochnus is such that the trunk represents most of the standing biomass for the latter half of its lifetime. According to our model, after the tree reaches 30% of its development, the biomass of the crown of branches would remain more or less constant through the rest of its life, since old branches would be continuously abscised as new branches are formed. At the latest stage of development (i.e., 99%), the trunk of our Pseudosporochnus model represents 83% of the tree’s standing carbon mass. One can thus distinguish two major components of the tree: the lateral branches, which represent an important allocation of biomass with a fast turnover, and the trunk, which represents a lesser allocation of biomass but is accumulated over a longer time span. Pseudosporochnus has been reconstructed here as a tree about 3 m high, with mature individuals producing 837e1300 g C. This number only includes the aerial parts of the tree since the below-ground parts and roots are not taken into account in the present model. The content of carbon present in the aerial parts of living trees can be calculated using the fact that about half of the trees organic matter is carbon, with a small difference between angiosperms (48%) and gymnosperms (51%) (Brown and Lugo, 1984; Ritson and Sochacki, 2003; Martin and Thomas, 2011). Using this ratio, extant trees with a DBH (i.e., diameter at breast height) comparable to Pseudosporochnus have a much higher carbon mass. A cherry tree (Prunus virginiana) has a carbon content of 4193 g C, and a pine (Pinus strobus), 4670 g C. Trees like Quercus rubra or Alnus rugosa have a carbon content that is about 10 times that of Pseudosporochnus (9010 and 11,352 g C, respectively) (Ter-Mikaelian and Korzukhin, 1997). If one applies the ratio calculated for angiosperms and gymnosperms, the total biomass of a Pseudosporochnus tree would have been twice its mass in carbon: 1674e2600 g per tree. However, because Pseudosporochnus contained a lot more parenchymatous tissue than typical angiosperms or gymnosperms, we suspect that the ratio of carbon content to total biomass was different and that a better estimate would be provided by a comparison with living tree ferns (no value available).

6.4 Forest Biomass The appearance of the first trees and forests during the Devonian may have had a significant impact on the global carbon cycle (Algeo et al., 2001; Beerling and Berner, 2005; Le Hir et al., 2011). Combined with data on tree density, our carbon content estimates of Pseudosporochnus provide the first quantitative assessments for the amount of carbon stored by these fossil forests. For a Pseudosporochnus forest organized such as that of Riverside Quarry,

calculated values range from 4.3e to 15.3 t C/ha, depending on the tissue density used and the more or less conservative estimate of tree density (Table 3.3). Today, forest ecosystem productivity varies greatly depending on biome and tree species (Table 3.4). The highest carbon content in a natural system is found in Australian temperate forests of Eucalyptus regnans, with an average of 1053 t C/ha in living above-ground biomass (Keith et al., 2009). This is about 100 times higher than our highest estimates for a Pseudosporochnus forest. More typical ranges compiled by Keith et al. (2009) are 87e436 t C/ha for tropical forests, 85e678 t C/ha for temperate forests, and 11e149 t C/ha for boreal forests. A few types of forests can be compared with our highest estimates for Pseudosporochnus (Table 3.4). A Siberian stand of Larix gmelinii studied by Kajimoto et al. (1999) contains trees comparable in size to Pseudosporochnus, with an average DBH of 6.8 cm and an average tree height of 5.5 m. Its above-ground biomass is 22.4 t/ha, which corresponds to about 11 t C/ha for a ratio of carbon to total biomass of 50% (Martin and Thomas, 2011). Stems represent 81% of the standing aerial biomass, which is also comparable to values calculated for Pseudosporochnus trees. However, the Larix forest corresponds to old trees (240e280 years old) growing slowly, in a very constrained environment at about 64 N, which differs from the Devonian climatic conditions for Riverside Quarry and the other regions where pseudosporochnalean trees have been reported (Berry and Fairon-Demaret, 2001; Stein et al., 2012; Giesen and Berry, 2013). Savannas like the Brazilian cerrado (Table 3.4) are the only forested tropical ecosystems with standing aboveground carbon content values comparable to our Pseudosporochnus forests, with an average of 9 t C/ha (Grace et al., 2006). However, they represent again environments with strong environmental constraints, in that case aridity. This was probably not the case for the pseudosporochnalean forests whose environments were not limited in soil water availability (Stein et al., 2012; Giesen and Berry, 2013). Thickets of young beech trees in temperate forests (Table 3.4) are another example of a tree stand comparable in carbon content to our highest estimates for a Pseudosporochnus forest, with a value of about 9 t C/ha when trees are 8 years old (Huet et al., 2004). In that case, the trees are immature, and they have a DBH significantly smaller than Pseudosporochnus (1.5 cm) and a density much higher (16,815 trees/ha). As the trees get older, the values change rapidly to reach five times or more the carbon content reconstructed for a Pseudosporochnus forest. With the exception of very young stands or very constrained environments, our calculated values are, thus, lower than those found in the large majority of extant forest ecosystems (Table 3.4). They remain, however, higher than

Modeling Pseudosporochnus Chapter j 3

45

TABLE 3.4 Standing Aerial Biomass-Carbon by Area in a Reconstructed Pseudosporochnus Stand and in Selected Extant Ecosystems Tree

Source

Standing Aerial Biomass in t C/ ha

Pseudosporochnus

This study

4.3e6.5 (HC) 5.6e8.5 (MC) 10e15.3 (LC)

Eucalyptus regnans forests

Keith et al. (2009)

1053

Tropical forests

Keith et al. (2009)

87e436

Temperate forests

Keith et al. (2009)

85e678

Boreal forests

Keith et al. (2009)

11e149

Larix stand in central Siberia

Kajimoto et al. (1999)

11

Savanna ecosystems (average)

Grace et al. (2006)

9.4

Brazilian cerrado

Grace et al. (2006)

9.6e11

Natural savanna area of South Africa

Grace et al. (2006)

6.7

Open humid savanna, Cote d’Ivoire

Grace et al. (2006)

17.7

Beech thicket (8 years old)

Huet et al. (2004)*

9.5

Beech forest (25 years old)

Huet et al. (2004)*

53

Grasslands

Stypinski and Mastalerczuk (2006)

3.7e4.3

Temperate dwarf shrub heath

Alonso et al. (2012)

2

Temperate bog

Alonso et al. (2012)

2

* Where only biomass data were provided, a carbon concentration of 0.5 g C/g was used for conifers and 0.47 g C/g for angiosperms, following Martin and Thomas (2011).

in ecosystems such as bogs or grasslands in which the mean values for aerial parts do not exceed 4.3 t C/ha (Stypinski and Mastalerczuk, 2006). Given our hypotheses on the structure of a Pseudosporochnus stand, the closest extant forest analogs in terms of productivity are, thus, either young or environmentally constrained. This is significant when considering that Mintz et al. (2010) interpreted a pseudorochnalean habitat near Gilboa as stressful and limited in resources. Stein et al. (2012) viewed the forest at Riverside Quarry as highly disturbed. Giesen and Berry (2013) also interpreted the stands of Calamophyton from Lindlar as subject to catastrophic events.

7. CONCLUSIONS This report presents a three-dimensional architectural model of Pseudosporochnus, a major component of the earliest forests on Earth. The AmapSim software used to simulate the tree at all stages of growth also allows for the calculation of its carbon content and biomass. The accuracy

of the model requires a better assessment of the growth patterns of its components and of their carbon density, perhaps using that of living tree ferns. Despite these limitations and the possible underestimation of the carbon content of some components, the model makes a clear distinction between the trunk and the branches. Besides being regularly shed and forming a thick litter (Berry and Fairon-Demaret, 2002; Giesen and Berry, 2013), the latter accumulate the largest part of biomass synthesized by the tree during its entire lifetime. In terms of biomass, our calculations show, however, that Pseudosporochnus contains much less carbon than most living trees. The performances of the Pseudorochnales as primary producers, therefore, remain an open question. According to our model, the productivity of a Pseudosporochnus tree stand is comparable to that of environmentally constrained extant forests. The architectural traits of Pseudosporochnus may have favored the establishment of tree communities reasonably well adapted to constrained environments in the Devonian.

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SECTION j I Early Land Plants: Innovations and Adaptations

SUPPLEMENTARY FIGURE Supplementary data related to this article can be found online at https://doi.org/10.1016/B978-0-12-8130124.00003-6.

ACKNOWLEDGMENTS We are very much indebted to the editors for their invitation to participate in this volume. Early in his career, Prof. Thomas N. Taylor got off the beaten track and he had, since then, never ceased to propose a new and attractive vision of paleobotany. This work is a tribute to his creativity and courage. This report was greatly improved by three anonymous reviewers who provided very helpful comments and suggestions.

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Chave, J., Condit, R., Aguilar, S., Hernandez, A., Lao, S., Perez, R., 2004. Error propagation and scaling for tropical forest biomass estimates. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 359 (1443), 409e420. Chave, J., Réjou-Méchain, M., Búrquez, A., Chidumayo, E., Colgan, M.S., Delitti, W.B.C., Duque, A., Eid, T., Fearnside, P.M., Goodman, R.C., Henry, M., Martínez-Yrízar, A., Mugasha, W.A., MullerLandau, H.C., Mencuccini, M., Nelson, B.W., Ngomanda, A., Nogueira, E.M., Ortiz-Malavassi, E., Pélissier, R., Ploton, P., Ryan, C.M., Saldarriaga, J.G., Vieilledent, G., 2014. Improved allometric models to estimate the aboveground biomass of tropical trees. Global Change Biology 20 (10), 3177e3190. Daviero, V., Lecoustre, R., 2000. Computer simulation of sphenopsid architecture. II. Calamites multiramis Weiss, as an example of Late Paleozoic arborescent sphenopsids. Review of Palaeobotany and Palynology 109, 135e148. Daviero, V., Meyer-Berthaud, B., Lecoustre, R., 2000. Computer simulation of sphenopsid architecture. I. Principles and methodology. Review of Palaeobotany and Palynology 109, 121e134. Daviero-Gomez, V., Kerp, H., Hass, H., 2005. Nothia aphylla: the issue of clonal development in early land plants. International Journal of Plant Sciences 166 (2), 319e326. Driese, S.G., Mora, C.I., Elick, J.M., 1997. Morphology and taphonomy of root and stump casts of the earliest trees (Middle to Late Devonian), Pennsylvania and New York, USA. PALAIOS 12, 524e537. Edwards, D., Fairon-Demaret, M., Berry, C.M., 2000. Plant megafossils in Devonian stratigraphy: a progress report. Courier Forschunginstitut Senckenberg 220, 25e37. Fairon-Demaret, M., Li, C.-S., 1993. Lorophyton goense gen. et sp. nov. from the Lower Givetian of Belgium and a discussion of the Middle Devonian Cladoxylopsida. Review of Palaeobotany and Palynology 77, 1e22. Giesen, P., Berry, C.M., 2013. Reconstruction and growth of the early tree Calamophyton (Pseudosporochnales, Cladoxylopsida) based on exceptionally complete specimens from Lindlar, Germany (Mid-Devonian): organic connection of Calamophyton branches and Duisbergia trunks. International Journal of Plant Sciences 174 (4), 665e686. Grace, J., San Jose, J., Meir, P., Miranda, H.S., Montes, R.A., 2006. Productivity and carbon fluxes of tropical savannas. Journal of Biogeography 33, 387e400. Griffon, S., de Coligny, F., 2014. AMAPstudio: An editing and simulation software suite for plants architecture modelling. Ecological Modelling 290, 3e10. Gutak, J.M., Antonova, V.A., Ruban, D.A., 2011. Diversity and richness of the Devonian terrestrial plants in the Southeastern Mountainous Altay (Southern Siberia): regional versus global patterns. Palaeogeography, Palaeoclimatology, Palaeoecology 299 (1e2), 240e249. Hinz, J.K., Smith, I., Pfretzschner, H.-U., Wings, O., Sun, G., 2010. A high resolution three-dimensional reconstruction of a fossil forest (Upper Jurassic Shishugou Formation, Junggar Basin, Northwest China. Palaeobiodiversity and Palaeoenvironments 90, 215e240. Huet, S., Forgeard, F., Nys, C., 2004. Above- and belowground distribution of dry matter and carbon biomass of Atlantic beech (Fagus sylvatica L.) in a time sequence. Annals of Forest Science 61 (7), 683e694. Iurina, A., 1988. The Middle and Late Devonian floras of northern Eurasia. Transactions of the Palaeontological Institution (in Russian) 227, 1e175.

Modeling Pseudosporochnus Chapter j 3

Kajimoto, T., Matsuura, Y., Sofronov, M.A., Volokitina, A.V., Mori, S., Osawa, A., Abaimov, A.P., 1999. Above- and belowground biomass and net primary productivity of a Larix gmelinii stand near Tura, central Siberia. Tree Physiology 19, 815e822. Keith, H., Mackey, B.G., Lindenmayer, D.B., 2009. Re-evaluation of forest biomass carbon stocks and lessons from the world’s most carbon-dense forests. Proceedings of the National Academy of Sciences 106 (28), 11635e11640. Lang, W.H., 1927. Contributions to the study of the Old Red Sandstone flora of Scotland. VII. On a specimen of Pseudosporochnus from the Stromness beds. Transactions of the Royal Society of Edinburgh 55 (2), 453e454. Le Hir, G., Donnadieu, Y., Goddéris, Y., Meyer-Berthaud, B., Ramstein, G., Blakey, R.C., 2011. The climate change caused by the land plant invasion in the Devonian. Earth and Planetary Science Letters 310 (3e4), 203e212. Leclercq, S., Banks, H.P., 1962. Pseudosporochnus nodosus sp. nov., a Middle Devonian plant with cladoxylalean affinities. Palaeontographica Abt B 110, 1e34. Leclercq, S., Lele, K.M., 1968. Further investigation on the vascular system of Pseudosporochnus nodosus Leclercq et Banks. Palaeontographica Abt. B 123 (1e6), 97e112. Martin, A.R., Thomas, S.C., 2011. A reassessment of carbon content in tropical trees. PLoS ONE 6 (8), e23533. https://doi.org/10.1371/ journal.pone.0023533. Meyer-Berthaud, B., Soria, A., Decombeix, A.-L., 2010. The land plant cover in the Devonian: a reassessment of the evolution of the tree habit. In: Vecoli, M., Clément, G., Meyer-Berthaud, B. (Eds.), The Terrestrialization Process: Modelling Complex Interactions at the Biosphere-geosphere Interface. Geological Society, London, pp. 59e70. Special Publications 339. Mintz, J.S., Driese, S.G., White, J.D., 2010. Environmental and ecological variability of Middle Devonian (Givetian) forests in Appalachian basin paleosols, New York, United States. PALAIOS 25, 85e96. Mustafa, H., 1978a. Beiträge zur Devonflora II. Argumenta Palaeobotanica 5, 31e56. Mustafa, H., 1978b. Beiträge zur Devonflora III. Argumenta Palaeobotanica 5, 91e132. Orlova, O.A., Jurina, A.L., Snigirevsky, S.M., 2016. Late Devonian plant communities of North Russia. Review of Palaeobotany and Palynology 224 (1), 94e107. Potonié, H., Bernard, C., 1904. Flore dévonienne de l’étage H de Barrande. Charles Bellmann, Prague, 68 pp.

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Retallack, G.J., Huang, C., 2011. Ecology and evolution of Devonian trees in New York, USA. Palaeogeography, Palaeoclimatology, Palaeoecology 299 (1e2), 110e128. Ritson, P., Sochacki, S., 2003. Measurement and prediction of biomass and carbon content of Pinus pinaster trees in farm forestry plantations, southwestern Australia. Forest Ecology and Management 175 (1e3), 103e117. Stein, W.E., Hueber, F.M., 1989. The anatomy of Pseudosporochnus: P. hueberi from the Devonian of New York. Review of Palaeobotany and Palynology 60, 311e359. Stein, W.E., Berry, C.M., Hernick, L.V., Mannolini, F., 2012. Surprisingly complex community discovered in the mid-Devonian fossil forest at Gilboa. Nature 483 (7387), 78e81. Stein, W.E., Mannolini, F., Hernick, L.V., Landing, E., Berry, C.M., 2007. Giant cladoxylopsid trees resolve the enigma of the Earth’s earliest forest stumps at Gilboa. Nature 446 (7138), 904e907. Stockmans, F., 1968. Végétaux mésodévoniens récoltés aux confins du Massif du Brabant (Belgique). Institut Royal des Sciences Naturelles de Belgique, pp. 1e49. Mémoires 159. Stubblefield, S.P., Taylor, T.N., Beck, C.B., 1985. Studies of Paleozoic fungi: IV. Wood-decaying fungi in Callixylon newberryi from the Upper Devonian. American Journal of Botany 72, 1765e1774. Stypinski, P., Mastalerczuk, G., 2006. Carbon sequestration by Polish grassland biomass. In: Lloveras, J., González-Rodríguez, A., Vázquez-Yañez, O., Piñeiro, J., Santamaría, O., Olea, L., Poblaciones, M.J. (Eds.), Sustainable Grassland Productivity: Proceedings of the 21st General Meeting of the European Grassland Federation, pp. 763e765 (Badajoz, Spain). Taylor, T.N., Taylor, E.L., Krings, M., 2009. Paleobotany. The Biology and Evolution of Fossil Plants. Elsevier/Academic Press, Burlington MA, 1230 pp. Taylor, T.N., Krings, M., Taylor, E.L., 2015. Fossil Fungi. Elsevier/ Academic Press, Amsterdam, 382 pp. Ter-Mikaelian, M.T., Korzukhin, M.D., 1997. Biomass equations for sixty-five North American tree species. Forest Ecology and Management 97, 1e24. Weyland, H., 1925. Die Flora des Elberfelder Mitteldevons in ihrer Bedeutung für die Kenntnis der gesamten Devonflora. Jahresbericht des Naturwissenschaftlichen Vereins, Elberfeld 15, 33e47. Xiong, C., Wang, D., Wang, Q., Benton, M.J., Xue, J., Meng, M., Zhao, Q., Zhang, J., 2013. Diversity dynamics of SilurianeEarly Carboniferous land plants in South China. PLoS One 8 (9), e75706. Zimmermann, W., 1930. Die Phylogenie der Pflanzen. Gustav Fischer, Jena, 452 pp.

Chapter 4

The Advantages and Frustrations of a Plant Lagersta¨tte as Illustrated by a New Taxon From the Lower Devonian of the Welsh Borderland, UK Jennifer L. Morris1, Dianne Edwards1 and John B. Richardson2 1

Cardiff University, Cardiff, United Kingdom; 2Natural History Museum, London, United Kingdom

1. INTRODUCTION A Lagerstätte, a term first used in mining and roughly translated as a mother lode, is a locality yielding fossils with exceptional preservation via a number of different processes that have provided unique insights into the history of life on Earth. The majority of occurrences are zoological and were divided by Seilacher, who originally applied the term to fossils (Seilacher et al., 1985), into those that were aggregations of shells and/or bones (Konzentrat [concentration] Lagerstätten) and those where tissues of soft-bodied organisms (Konservat [conservation] Lagerstätten) are preserved (Allison, 1988; Allison and Briggs, 1993). The latter are particularly important for plants, where decay-resistant constituents are restricted to lignified tissues, cuticles, and spores, and where soft parts (e.g., parenchyma with cellulose plus cytoplasmic contents) are readily compressed and broken down via both biological and taphonomic processes. Examples are almost exclusively of permineralisations where coalified cell walls are preserved in a mineral matrix (e.g., the Lower Devonian Rhynie chert [silica]; Carboniferous coal balls [CaCO3]). Here we draw attention to the role of wildfires in producing Lagerstätten, with the best known preserving some of the earliest flowers as charcoal (Friis and Skarby, 1981). We focus on a Lower Devonian charcoal Lagerstätte, which has provided remarkable insights into herbaceous groundcovering vegetation some 415 million years ago (Edwards and Axe, 2004). Reflectance values indicate that the majority

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00004-8 Copyright © 2018 Elsevier Inc. All rights reserved.

of the plant remains were partially charred by lowtemperature smoldering wildfires (Glasspool et al., 2006), possibly initiated by lightning and facilitated by oxygen levels approximating those of the present day (Lenton et al., 2016). The plant fossils are found within siltstones of fluvial origin, often accumulated within ripple troughs and foreset laminations, and thus were transported away from their growth position and deposited elsewhere. Charcoalification of the plant material may have occurred before transportation (i.e., while still living) or most likely after their accumulation across exposed sedimentary surfaces. Preservation is exceptional, including the cellular structures of the sporangial and axial walls, internal anatomy, and in situ spores. Key discoveries include vascular tissue in Cooksonia axes (Edwards et al., 1992), the reunion of certain cryptospore taxa from the dispersed spore record with their parent plants (cryptophytes; Edwards et al., 2014), the recognition of fungal and lichen remains (Edwards et al., 2013; Honegger et al., 2013), and evidence for interactions between the plants and animals (Edwards et al., 1995a). Several novel embryophyte genera have been discovered from this assemblage (Table 4.1), and here we describe an additional new taxon with an unusual reproductive complex. However, studying charcoalified plant fossils, both in general and from this particular Lagerstätte, is not without challenges or frustrations, which we discuss later. Finally, we consider future lines of research, including the use of new technologies in the visualization and geochemical analyses of these exceptional fossils.

49

50

Lower MN Group

Taxon

TM

1

TR

Culullitheca richardsonii

Cryptophytes

Fusiformitheca fanningiae

x

Grisellatheca salopensis

x

Lenticulatheca spp.

x

Partitatheca spp.

BT

Upper MN 5

CM

Cooksonia cambrensis

(x)

x

Cooksonia hemisphaerica

x

x x

ND

BZ AD

8

RW

(x) x

x

x

(x) (x)

(x)

x

Electorotheca enigmatica

x c

cf. Aberlemnia caledonica

x

x

x

Monnowella bennettii

x

(x)

x

Resilitheca salopensis

x

Sporathylacium salopense

x

cf. Horneophyton sp.

x

Salopella allenii

x

x

Salopella marcensis

x

x

cf. Sporogonites sp.

x (x)

(x)

x

x

(x)

x

Tarrantia salopensis

x

Tortilicaulis offaeus

(x)

x

x x

Tortilicaulis transwalliensis

x

Uskiella reticulata

x

Uskiella spargens

7

x

Concavatheca banksii

Paracooksonia spp.

Elongate/oval

CR

6

x b

Cooksonia pertoni

Bivalved

NBCH

4

x a

Discoidal

3

x

Ficoiditheca aenigma

Rhyniophytoids

Middle MN 2

(x) x

(x) (x) x

9

MBQ10

SECTION j I Early Land Plants: Innovations and Adaptations

TABLE 4.1 Lochkovian Plant Body Fossils From the Anglo-Welsh Basin

Zosterophylls

Zosterophyllum cf. fertile

x

x

Deheubarthia splendens

x

x

Gosslingia breconensis

x

Craswallia haegensis Zosterophyllum sp.

Trimerophytes

x

x

x x x

Zosterophyllum llanoveranum

x

Dawsonites sp.

x

Crosses in brackets represent questionable assignment. Compiled from the following references: 1Tredomen Quarry: Morris et al., 2011a. 2Targrove: Lang, 1937; Edwards and Fanning, 1985; Fanning et al., 1988, 1992; Morris, 2009. 3North Brown Clee Hill: Fanning et al., 1988; Edwards et al., 1994, 1995b,c, 1999, 2001, 2012a, 2014; Edwards, 1996; Wellman et al., 1998a; Edwards and Richardson, 2000; Habgood et al., 2002; Morris et al., 2011b, 2012b; this report. 4Brynglas Tunnels, Newport: Wellman et al., 2000. 5Cwm Mill: Fanning, 1987; Kenrick, 1988. 6Craswall Quarry: Morris and Edwards, 2014. 7Newton Dingle: Edwards and Richardson, 1974; Morris and Edwards, 2014. 8Allt Ddu: Kenrick, 1988; Edwards et al., 1989. 9Rhiw Wen: Habgood, 2000. 10Mascle Bridge Quarry: Kenrick, 1988; Edwards et al., 1989; Wellman et al., 1998c. BZ, breconensisezavallatus Spore Assemblage Biozone; MN, micrornatusenewportensis Spore Assemblage Biozone. a Previously known as Fusitheca. b Previously assigned to Cooksonia banksii. c Previously assigned to cf. Cooksonia caledonica.

Advantages and Frustrations of a Plant Lagersta¨tte Chapter j 4 51

52

SECTION j I Early Land Plants: Innovations and Adaptations

2. GEOLOGICAL BACKGROUND AND PREVIOUS RESEARCH 2.1 Geological Background The Lagerstätte deposit is a gray siltstone horizon exposed in a stream section on the north side of Brown Clee Hill, Shropshire, UK (NBCH, Fig. 4.1) (Edwards et al., 1994). This horizon is part of a sequence of siltstones, sandstones, and calcretes that were assigned by Ball and Dineley (1961) to the lower Ditton Group, which is now known as the Freshwater West Formation, part of the Lower Old Red Sandstone of the Anglo-Welsh Basin (Barclay et al., 2015). This extramontane basin was located on the southern margins of Laurussia between the Late Silurian (Prídolí) to Early Devonian (Emsian) and was the depositional center for large southerly flowing fluvial systems that transported postorogenic detritus from the Caledonides mountain chain (Simon and Bluck, 1982; Allen and Crowley, 1983; Friend et al., 2000). Sedimentation was initially marine influenced, across low-lying tidal flats, but was wholly terrestrial by the Lochkovian, via braided and/or meandering fluvial systems. Fossil plants across the basin are most commonly preserved as coalified compressions, within gray to green fine-grained sandstones or siltstones that have sedimentary structures, such as cross-ripple lamination, which indicate deposition under relatively low flow strength and the accretion of in-channel bars (Morris et al., 2012a). These

deposits are often green due to the reduction of iron within the minerals, most likely because the original depositional environment was reducing and the sediments were buried rapidly. This not only inhibited plant decay but also promoted the crystallization of pyrite within intercellular spaces (Grimes et al., 2001). Preservation of plant material from the AngloWelsh Basin via pyritization has allowed for the characterization of the vascular tissues of some taxa (Edwards, 1981; Kenrick and Edwards, 1988) and the recognition of different tracheid types (Kenrick and Crane, 1991). Some pyrite crystallization has occurred within the Lagerstätte deposit, but its occurrence is patchy, often restricted to the axial parts of the plants. The main preservation process is charcoalification by low-temperature wildfires, either before or after the transportation and deposition of the plant remains within fluvial sediments. The fossils are preserved down to cellular level and in three dimensions, although they have also been subjected to varying degrees of shrinkage and compression (Edwards and Axe, 2004). Palynological assemblages from the Lagerstätte at Brown Clee Hill were studied by Richardson and McGregor and belong to the middle sub-zone of the micrornatuse newportensis Sporomorph Assemblage Biozone (Richardson and McGregor, 1986). This indicates an early Lochkovian (Early Devonian) age. Therefore, compared with other paleobotanical assemblages across the Anglo-Welsh Basin (Edwards and Richardson, 2004) (Fig. 4.1), it is contemporaneous with Targrove, Shropshire (Fanning et al., 1992), and

FIGURE 4.1 Gray shading indicates exposure of the Upper Silurian to Lower Devonian Anglo-Welsh Basin. Black dots indicate paleobotanical localities discussed in the text. Crossed boxes indicate towns. AD, Allt Ddu; BT, Bryn Glas Tunnels; CM, Cwm Mill; CR, Craswall; LL, Ludford Lane; MBQ, Mascle Bridge Quarry; ND, Newton Dingle; NBCH, North Brown Clee Hill; RW, Rhiw Wen; TR, Targrove; TM, Tredomen Quarry.

Advantages and Frustrations of a Plant Lagersta¨tte Chapter j 4

Bryn Glas Tunnels, Newport (Wellman et al., 2000) but younger than the assemblage at Tredomen Quarry (Morris et al., 2011a) (Table 4.1).

2.2 Noteworthy Advances by Previous Studies During the past 30 years, paleobotanical and palynological studies of the fossil assemblage from Brown Clee Hill have provided critical information about the detailed morphology and anatomy of the vegetation on land at this time, such as the nature of the vascular tissues, stomata, and in situ spores. The Lagerstätte consists of more plant taxa than any other locality in the Anglo-Welsh Basin (Table 4.1) and is still yielding new genera (e.g., Edwards et al., 2014). The following section highlights the most noteworthy advances in our understanding of the early embryophytes, the nonvascular nematophytes, and the interactions between early land plants and animals that have been provided by this Lagerstätte.

2.2.1 Embryophytes The embryophytes are represented in this assemblage by bifurcating axial vegetative organs and terminal sporangia. Charcoalification results in preservation of most tissue with some bias away from parenchyma. It has provided information on stomata, peripheral tissues, intercellular spaces, apices, and ultrastructure of conducting cells including plasmodesmata-derived pits. Very rarely do we have sufficient information, particularly on vascular tissues, in a single specimen to allow assignment to a higher taxonomic position than genus. Indeed, the classification of these early tracheophytes is in a state of flux. Traditionally placed in the subdivision Rhyniophytina (Banks, 1968), in a more recent classification (Hao and Xue, 2013) they were included in the class Rhyniopsida but excluded from the order Rhyniales and listed as cooksonioids and renalioids. Some members of the latter informal groupings had been considered as representing a basal grade of organization in the Lycophytina basal stem group (Kenrick and Crane, 1997). 1. Basal tracheophytes a. Cooksonioid complex i. Unequivocal demonstration of the vascular status of Cooksonia pertoni (Edwards et al., 1992) ii. Use of spore and sporangial characteristics in distinction of intraspecific variation in C. pertoni (Fanning et al., 1988) and erection of new cooksonioid genera (e.g., Concavatheca banksii; Morris et al., 2012a) iii. In situ spores consistently crassitate with bilayered walls (Edwards et al., 1995b)

53

Discovery of variation in the meiotic process with the production of both monads and dyads of distinctive ultrastructure in cooksonioid genera Paracooksonia and Lenticulatheca (Morris et al., 2011b), also recorded in the trilete monads of Cooksonia pertoni b. Renalioid complex i. Circumscription of isolated bivalved sporangia with variation in dehiscence features, spores, and stomatal distribution (e.g., Resilitheca, Edwards et al., 1995c; Sporathylacium, Edwards et al., 2001) ii. In situ spores consistently retusoid and typical of those from the zosterophylls (as in Gensel et al., 2013) c. Erection of a new species of Tortilicaulis with branching axes and in situ trilete spores, which provide evidence for its tracheophytic status (T. offaeus; Edwards et al., 1994) d. Demonstration of the distinctive emphanoid spores (e.g., Emphanisporites) in at least three different sporangial morphologies (Edwards and Richardson, 2000; Morris et al., 2012b) 2. Basal embryophytes (cryptophytes) a. Discovery and description of cryptospores (dyads and tetrads), similar to those in dispersed assemblages from the mid Ordovician, in sporangia (e.g., dyads in Culullitheca and Fusiformitheca, Wellman et al., 1998a; tetrads in Grisellatheca, Edwards et al., 1999) b. Distinction of a new lineage of basal embryophytes with valvate sporangia that terminated stomatiferous branching axes (Partitatheca, Edwards et al., 2012a), with a combination of characteristics not seen in extant tracheophytes and bryophytes 3. In situ spores a. Preliminary studies on the use of in situ spores in enhancing the role of the dispersed spore record for the analyses of regional variations in the composition of vegetation in the absence of megafossils b. Use of spore ultrastructure in detecting relationships from species to lineages (e.g., Morris et al., 2011b; Edwards et al., 2012a, 2014) c. Additional evidence for the detection of evolutionary trends, from intergraded morphological variation of spores (morphons) through time, specifically here the ornamentation of crassitate spores, recognized both in situ and in the dispersed record (Fanning et al., 1988; 1990; 1991a; Richardson, 1996a) iv.

2.2.2 Nematophytes (sensu Lang, 1937) 1. Linkages of dispersed cuticles such as Nematothallus and Cosmochlaina, to associations of hyphae-forming,

54

SECTION j I Early Land Plants: Innovations and Adaptations

encrusting fungal thalli, which were major components of early land vegetation (cryptogamic covers; Edwards et al., 2013) 2. Discovery of the earliest thalloid lichens (Honegger et al., 2013) 3. Confirmation of the relationship between Prototaxites and Nematoplexus and the formation of cords, which reinforce the fungal affinities of these taxa (Edwards and Axe, 2012)

2.2.3 PlanteAnimal Interactions Apart from cuticles of eurypterids, megafossils or microfossils of animals have not been isolated from the Lagerstätte, but some of the co-occurring fossils are coprolites. Based on their content and size, they were probably produced by millipedes consuming plant litter but excreting indigestible remains including, not surprisingly, spores (detritivores; Edwards et al., 1995a) and nematophytes (fungivores; Edwards et al., 2012b).

3. NEW RESEARCH 3.1 Material and Methods Research continues on the assemblage and here we describe a small collection of unusual sporangia which demonstrate inter alia further disparity and the problems of relating three dimensionally preserved material to compression fossils. Five specimens were released from the fine-grained siltstone using HCl/HF to dissolve the matrix, recovered by sieving and sorting and then examined by scanning electron microscopy (FEI ESEM-FEG), as described in detail in earlier studies from the locality (e.g., Edwards, 1996; Morris et al. 2011b). One specimen was initially isolated by Una Fanning about 30 years ago (NMW 2018.18G.1) (Fanning, 1987); four additional specimens have been isolated from more recent macerations ([NMW 2018.18G.2], [NMW 2018.18G.3], [NMW 2018.18G.4], and [NMW 2018.18G.5], the last as part of an undergraduate student project).

3.2 Morphology and Anatomical Descriptions The reconstruction in Fig. 4.2 is based on five fragmentary specimens, united in their possession of distinctive but concatenating morphological and superficial anatomical features, whose preservation states vary. The most complete specimen is NMW 2018.18G.1 (Plate I, 1e3). It provides the most comprehensive proximal view of a reproductive complex (c. 3.5 mm in total diameter) in which a compressed sporangium, almost circular in outline (diameter c. 1000 mm) with remnants of a subtending stem,

FIGURE 4.2 Reconstruction of Electorotheca, based on five fragmentary specimens. Modelled by Dianne Edwards and drawn by Brian Davies.

is centrally attached and distally expands into a circular planar structure with peripheral tapering projections, two of which were complete. A similar but less complete specimen [NMW 2018.18G.2] shows the considerable extent of the sporangial/stem junction, when viewed laterally (Plate I, 4), as does an additional specimen [NMW 2018.18G.5], where only the central body is preserved (Plate I, 5). Here the stalk tissues have collapsed, resulting in formation of radiating ridges and obliteration of any cellular detail. By contrast, in specimen NMW 2018.18G.1, the well-preserved elongate cells of the sporangial proximal surface pass without interruption into the more poorly preserved cells of the stem (Plate I, 3), where just one stoma has been recorded. The transversely fractured stem is laterally compressed, ranging between 250 and 300 mm in width, and lacks internal anatomy except for a peripheral zone of uniformly thickened, relatively thin-walled cells (Plate I, 2). The topography of the distal surface of the complex is uncertain: that preserved in specimen NMW 2018.18G.1 is disorganized, with superimposed but fused fragments (Plate II, 1). In the best specimen regarding cellular preservation [NMW 2018.18G.4], the central area that immediately overlies the sporangium is gently domed, with a slight central depression (Plate II, 2) and free projections that are flat or slightly reflexed at their bases (Plate II, 2). In specimen NMW 2018.18G.2, the superficial cells in the central region show signs of shrinkage (Plate II, 3) and the center of the structure is funnel shaped, as if collapsed (Plate II, 4). When intact, the cells in this region are superficially isodiametric (c. 45 mm in diameter) and of very regular appearance (Plate II, 5) with uniformly thickened walls but become more elongate in the vicinity of

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PLATE I (1e3) Specimen NMW 2018.18G.1. (1) The proximal side of the most complete specimen. Sporangial body is circular, with short subtending stem; attached centrally by overlying planar structure with peripheral tapering appendages. Scale bar ¼ 500 mm. (2) Fractured section of the subtending stem. Scale bar ¼ 100 mm. (3) Remnants of the subtending stem. Scale bar ¼ 100 mm. (4) Specimen NMW 2018.18G.2. Lateral view of specimen, showing the extent of the sporangial/stem junction. Scale bar ¼ 200 mm. (5) Specimen NMW 2018.18G.5. Proximal surface, showing radiating ridges that represent stalk tissue. Scale bar ¼ 300 mm.

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SECTION j I Early Land Plants: Innovations and Adaptations

PLATE II (1) Specimen NMW 2018.18G.1. Distal surface, showing radially arranged appendages. Scale bar ¼ 500 mm. (2) Specimen NMW 2018.18G.4. Distal surface, showing flat or reflexed appendages and slightly domed central area. Scale bar ¼ 500 mm. (3 and 4) Specimen NMW 2018.18G.2. (3) Distal surface, showing the shrinkage of cells. Scale bar ¼ 200 mm. (4) Distal surface, where center of the structure is funnel-shaped. Scale bar ¼ 200 mm. (5e7) Specimen NMW 2018.18G.4. (5) Distal surface, showing central isodiametric superficial cells that become more elongate in the vicinity of the appendages. Arrow indicates stoma in transitional zone. Scale bar ¼ 200 mm. (6) Elongate superficial cells within the appendage. Arrow indicates where outer periclinal cell walls removed, revealing uniformly thickened cell walls. Scale bar ¼ 200 mm. (7) Stoma arrowed in (5). Scale bar ¼ 20 mm. (8) Specimen NMW 2018.18G.1. Fractured section through sporangial wall in the central region. Scale bar ¼ 100 mm. (9) Specimen NMW 2018.18G.2. Radiating cells on the proximal surface of the sporangium. Scale bar ¼ 200 mm.

Advantages and Frustrations of a Plant Lagersta¨tte Chapter j 4

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PLATE III (1) Specimen NMW 2018.18G.1. Raised clusters of isodiametric cells, surrounded by radiating cells (arrow). Scale bar ¼ 100 mm. (2) Specimen NMW 2018.18G.3. Fractured cross section through an appendage. Wall composed of two layers of cells, with evenly thickened walls. Scale bar ¼ 50 mm. (3) Specimen NMW 2018.18G.1. Fractured cross section through an appendage. Scale bar ¼ 30 mm. (4) Specimen NMW 2018.18G.4. Fractured cross section through an appendage. Contents of cells display strands consistent with charcoalification. Scale bar ¼ 20 mm. (5 and 6) Specimen NMW 2018.18G.3. (5) Appendage with a slightly recurved tip. Scale bar ¼ 100 mm. (6) Tip of appendage. Scale bar ¼ 20 mm. (7) Specimen NMW 2018.18G.1. Tip of an appendage that is either gaping or bifurcating. Scale bar ¼ 30 mm. (8) Specimen NMW 2018.18G.3. Bifurcating appendage. Scale bar ¼ 500 mm.

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SECTION j I Early Land Plants: Innovations and Adaptations

PLATE IV (1 and 2) Specimen NMW 2018.18G.1. (1) Stoma located on the sporangium. Scale bar ¼ 20 mm. (2) Stoma located on the sporangium; the periclinal cell walls of guard cells have not preserved. Scale bar ¼ 30 mm. (3e7) Specimen NMW 2018.18G.4. Laevigate, crassitate trilete spores within the sporangial cavity. (3) Scale bar ¼ 20 mm. (4) Arrow indicates internal pyrite crystals. Scale bar ¼ 10 mm. (5) Scale bar ¼ 5 mm. (6) Arrow indicates microconi-like protrusion, an artefact created where an external pyrite crystal has deformed the spore wall. Scale bar ¼ 10 mm. (7) Scale bar ¼ 10 mm. (8e10) Specimen NMW 2018.18G.5. (8) Fractured sporangium, with three-dimensional spores preserved within. Scale bar ¼ 200 mm. (9 and 10) Three dimensionally preserved spores, including one with a trilete mark, surrounded by disorganized tissue. (9) Scale bar ¼ 20 mm. (10) Scale bar ¼ 50 mm.

Advantages and Frustrations of a Plant Lagersta¨tte Chapter j 4

the appendages (Plate II, 6). Very rare stomata occur in the transition zone (Plate II, 7). Evidence from vertically fractured specimens suggests that the wall in the central region above the sporogenous zone consists of at least a single layer of cells (Plate II, 8). The radiating cells shown in Plate II, 9 are thought to represent the innermost part of the sporangial wall of the proximal surface. Additionally, two features occur toward the edge of the central area on the distal surface, close to the base of a projection. They consist of raised clusters of more or less isodiametric cells, which are much smaller than the surrounding, possibly radiating, cells of the surrounding epidermis (Plate III, 1). The projections are multilayered: the fractured transverse section close to the base shows at least two peripheral layers of similarly shaped cells with evenly thickened walls on both surfaces, although more deeply seated tissue is less well preserved (Plate III, 2) and is less common in distal regions (Plate III, 3). Obliquely fractured peripheral cells display contents characteristically associated with charcoalification (Plate III, 4) (Edwards and Axe, 2004). The tips of the appendages are rounded, possibly slightly recurved (Plate III, 5). The discontinuities seen in Plate III, 6 are considered preservational rather than an original anatomical feature. The tip of one isolated example is either gaping or bifurcating (Plate III, 7). Where complete, the projections are simple triangular structures, except for one fragment with excellent cellular preservation where a basal bifurcation is present (Plate III, 8). Because all five specimens are fragmentary, the number of appendages is conjectural, and in the reconstruction (Fig. 4.2) is estimated from their basal dimensions (recorded as 500e700 mm) and space available. Occasional, widely separated stomata are present among the elongate cells on both surfaces and from very limited observations, more on the lower than on the upper surface. The stomata possess two guard cells with circumporal thickenings (Plate IV, 1). Where the outer periclinal walls of the guard cells are not preserved, such thickenings are absent. Most stomatal complexes are longer than the almost isodiametric forms closer to the center of the specimens but are mostly of similar width (Plate IV, 2). Spores are present in two specimens. In the more conventionally preserved (Plate IV, 3), they are compressed, with subtriangular to circular ambs, convex sides, thick crassitudes (Plate IV, 4e7), and small diameters (15e18 mm). Laesurae are simple and vary in length (Plate IV, 6), some extending to the crassitude (Plate IV, 4, 7). The proximal surfaces appear to have murornate-verrucate sculpture (Plate IV, 5), and in one case micrograna-like protrusions (arrowed in Plate IV, 6), but these features are artefacts produced by large pyrite crystals, either externally to or within the spore bodies, as illustrated where slightly exposed (arrowed in Plate IV, 4). Both proximal and distal surfaces are laevigate.

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Fractured sporangia, such as seen in Plate IV, 8, are unique in our experience, because the contents are threedimensionally preserved as a solid mass (Plate IV, 9, 10) and, hence, not easily understood. Specimen NMW 2018.18G.5 consists of a small number of distorted or almost spherical voids in a matrix of very numerous small fragments (Plate IV, 9, 10). The former, one of which shows a small trilete mark, are interpreted as uncompressed spores, their size more or less equal to those described here earlier, whose walls are partially fused with the surrounding disorganized tissue. This tissue may represent immature, compressed, or fragmented spores or even the remains of precipitated locular fluid. The contents are irregularly distributed, with fewer “voids” in the peripheral region (Plate IV, 10). Because the spores are poorly preserved, precise assignment to a dispersed spore species is challenging, but they do show a characteristic equatorial crassitude similar to the in situ spores of other cooksonioids (Fanning et al., 1988, 1991a) and in the dispersed record (Richardson, 1996a). Absence of convincing evidence for sculpture allows assignment of the laevigate spores to Ambitisporites, but further comparison is hampered by poor preservation. However, their small size and wide crassitudes distinguish them from species of Ambitisporites recorded in the dispersed spore record.

3.3 Comparisons and Systematics 3.3.1 Comparisons With Other Rhyniophytoids The association of a sporangium with sterile appendages sets the new material apart from coeval trilete spore producers in Lochkovian sequences across the Anglo-Welsh Basin. There are coalified examples from older rocks (Prídolí) in the area, with substantial spinose projections, but these occur either over the entire surface of the discoidal sporangium of Pertonella dactylethra (Fanning et al., 1991b, Fig. 7) or as in Caia langii (Fanning et al., 1990, Fig. 5), where the sporangia are elongated and the projections are concentrated distally. The cellular construction of the spines in these compression fossils is unknown. Elsewhere and in younger strata, much smaller scattered spines occur on zosterophyll sporangia (e.g., Xitunia spinitheca, Lochkovian, Yunnan, China, Xue, 2009; Discalis longistipa, Pragian, Yunnan, China, Hao, 1989; Sawdonia ornata, Emsian, USA, Gensel et al., 1975). However, most relevant to this account are the terminal sporangia bearing triangular emergences of Eocooksonia sphaerica (Senkevich) Doweld (Doweld, 2000; Wang and Xu, 2011; Xue et al., 2015), earlier named Junggaria spinosa Dou by Cai et al. (1993), in compression fossils from the uppermost Silurian Wutubulake Formation in the

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Junggar Basin, north Xinjiang, China. These were initially described as possessing “more complex, indeed more enigmatic organization, than seen in most Silurian and Early Devonian rhyniophytoids” (Cai et al., 1993), and there remain some uncertainties relating to the nature of the central area and border, particularly in the positioning of the compressed triangular structures. All authors concurred that the compressed sporangia formed a circular central area composed of homogeneous coalified material associated with peripheral triangular emergences of varying lengths. Cai et al. (1993), in discussing the possibility that the central region was the sporogenous area with a border (possibly associated with dehiscence) or, alternatively, that the sporangium was columellate, were convinced that the border extended vertically over the sporangium. However, although the interpretative line drawings and illustrations in Xue et al. (2015, Figs. 1e3) appear to support this configuration, the authors concluded that the overall shape was a compressional artefact and that the specimens composed a central, probably discoidal, sporogenous region that was “covered by a distal surface wall with radiated elongate-triangular emergences.” Their resulting restoration therefore looks remarkably similar to that produced here (Fig. 4.2), except that the projections were more numerous and less regular. The Chinese restoration was based on two rare types of preservation, resulting in distal views. In the first, a few specimens show a border enclosing the central body for almost the entire circumference (Xue et al., 2015: Fig. 4, d, f, and Fig. 5, g, l), although this type of compression makes it impossible to distinguish the ends of the subtending axis and the actual emergences, as illustrated in Xue et al. (2015, Fig. 1, k). In the single example of the second type, the circumference of the sporangium is almost enclosed by six emergences with a further emergence extending over the central body in the vicinity of the subtending axis (Xue et al., 2015: Fig. 4, g, and Fig. 5, j). This is the only specimen where there is an emergence adjacent to the axis. All other specimens were interpreted as laterally compressed. In our opinion, lateral compression would have resulted in lens-shaped, originally discoidal, sporangia extended into emergences and, if indeed laterally compressed, the appearance of the sporangia must have been produced by tilting of almost all the sporangia on compression but with no instances of the emergences superimposed on the stalks. We consider it most unlikely that such orientation could have occurred consistently. While there are similarities at a glance between the Chinese material and the sporangia described here, these similarities are considered to have been taphonomically produced, and as there is no information on the threedimensional construction and anatomy in Eocooksonia, we choose to erect a new genus.

3.3.2 Systematic Paleontology Plantae: Incertae sedis Genus name: Electorotheca Morris, Edwards, and Richardson gen. nov Figures: Plates IeIV; Fig. 4.2 Derivation of name: from the Greek “Elektor,” meaning “the beaming sun,” in relation to the distal view of the complex Type species: Electorotheca enigmatica Morris, Edwards, and Richardson sp. nov Diagnosis: Sporangial complex composed of lenticular sporangium with proximal central stem and overlying planar extension with peripheral triangular projections. Both stem and extensions with stomata. Spores trilete Species name: Electorotheca enigmatica Morris, Edwards, and Richardson sp. nov Figures: Plates IeIV; Fig. 4.2. Derivation of name: Latinized from the Greek “ainigma,” meaning obscure, inexplicable Holotype: NMW 2018.18G.1 (lost; images only): Plate I, 1e3; Plate II, 1, 8; Plate III, 1, 3, 7; Plate IV, 1, 2 Neotype: NMW 2018.18G.4: Plate II, 2, 5e7; Plate III, 4; Plate IV, 3e7 Paratypes: NMW 2018.18G.2, NMW 2018.18G.3, NMW 2018.18G.5 Type locality and horizon: Stream section to the north of Brown Clee Hill, Shropshire, Welsh Borderland, UK. Freshwater West Formation, Anglo-Welsh Basin. Middle sub-biozone of the micrornatusenewportensis Sporomorph Assemblage Biozone, Lochkovian Stage, Lower Devonian Diagnosis: As for the genus. Complex at least 3 mm wide. Sporangia 600e1700 mm in diameter. Elongate triangular projections at least 1000 mm long. Spores trilete and crassitate, with laevigate distal and proximal surfaces; assigned to Ambitisporites. 15e18 mm in diameter Repository: All specimens were deposited in the National Museum of Wales, Cardiff

3.4 Functional, Physiological, and Evolutionary Conundrums The flat distal structure with projections, which distinguish this plant from the cooksonioid complex whose sporangia are similar in shape and in situ spores, presents some interesting challenges to hypotheses relating to its function. The multicellular construction of the projections indicates that they were quite substantial entities, and the presence of stomata, although rare, points to possible photosynthetic capacity that would have provided an immediate source of energy for a developing sporangium. However, such juxtapositioning raises questions as to how the spores were

Advantages and Frustrations of a Plant Lagersta¨tte Chapter j 4

dispersed. There is limited evidence that this may have occurred after breakdown of the distal central region (Plate II, 4), where at least a single layer is preserved above the sporogenous region. We have no evidence of any predetermined dehiscence structures, but some indications of shrinkage that may have led to eventual collapse of cells. Returning to the photosynthetic hypothesis, the positioning of the stomata and their rarity question a role in gas exchange, especially as their construction is similar to that on stems and sporangia of approximately coeval vascular plants (Edwards and Axe, 1992; Edwards, 1993; Edwards et al., 1998). Their absence from the distal central region of the complex can be explained by the lack of potentially chlorophyllous tissue beneath, but their very low density on the potentially photosynthetic projections is closer to that noted on naked stems and axes of early land plants preserved in the Rhynie Chert (Edwards, 2004). In commenting on the presence of stomata on coalified sporangia, Raven and Edwards (2004) speculated on a possible role in the creation of a transpiration stream for delivery of water and nutrients to an active metabolic region. Whether this is the case here is considered unlikely; we have no evidence of any vasculature between the distal structure and the supporting stem or fortuitous fractures that would reveal the nature of the tissue immediately below the stomata. A further possibility is that the stomata were involved in sporangial desiccation and, hence, spore liberation. This role was recently suggested for moss stomata, which look very similar to those of tracheophytes but are restricted to sporangia (Field et al., 2015). In these examples, it is hypothesized that opening of the stomata resulted in the drying out of previously liquid-filled intercellular spaces within the sporangial walls, thus setting up tensions that resulted in splitting and spore liberation. Here, it is difficult to see how so few and scattered stomata could have had a similar function. Indeed, in marchantioid liverworts, the peltate heads of the gametangiophores might have had a role in maintaining the hydration of the reproductive structures (Duckett and Pressel, 2009). Finally, in an evolutionary setting when much has been debated concerning the relationship between bryophytes (particularly hepatics) and the vascular plants, the association of a sporangium with a sterile laminate structure with peripheral projections (similar to a peltate head) recalls the arrangement characteristic of the gametangiophores of the marchantioid liverworts, particularly the archegoniophores. This raises the possibility of homology between sexual and asexual generations in the life cycle. However, these are superficial resemblances. Although photosynthesis occurs in the archeogoniophores (Duckett and Pressel, 2009), gaseous exchange occurs via open pores, while the presence of stomata and the typically tracheophytic spores in Electorotheca eliminates any phylogenetic relationships with liverworts.

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4. THE LIMITATIONS OF CHARCOALIFIED LAGERSTA¨TTEN In Section 2.2, we illustrate the benefits of exceptional preservation via charcoalification, here exemplified by the new genus Electorotheca. However, the account also highlights the frustrations of studying such a charcoalified Lagerstӓtte. The following limitations apply to Electorotheca and in general.

4.1 Taphonomy The most common taphonomic history of a fossil plant assemblage in the Anglo-Welsh Basin is as follows: transportation within fluvial channels; fragmentation; sorting and deposition via hydrodynamic partitioning; burial; and compression. For the Lagerstätte, the additional charcoalification process occurred either before transportation or after deposition, while the partial permineralization by pyrite crystals occurred during burial. The transportation of plant remains via fluvial currents resulted in fragmentation and a reduction of specimen size. The plants were then deposited within different size fractions as a result of hydrodynamic processes. Relatively large plant remains, such as Cooksonia hemisphaerica and Salopella allenii, were carried short distances by river currents and deposited across the bedding planes of sandy sediments that were accreting on the sides of channel bars (Morris et al. 2012a). In cases of minimal fragmentation, where the majority of the aerial parts have remained intact, taxonomic assignments based on overall morphology of the plants have been possible (Table 4.1). Smaller fractions of plant debris, a few millimeters in diameter, were deposited from suspension with silt-sized clasts or clay and include smaller fragments of once large plant remains together with minute plants, such as Electorotheca, Tortilicaulis offaeus, and the cryptophytes. Both size fractions are evident in the sandstones and siltstones at Tredomen Quarry (Morris et al., 2011a, 2012a; Tables 4.1 and 4.2). However, only the smaller fraction of plant debris is preserved in the siltstones at north Brown Clee Hill, while the larger plants are missing (Tables 4.1 and 4.2). In the Lagerstätte, fragmentation has been especially exaggerated due to the brittle nature of charcoal, and while anatomy has been preserved, we often lack any information on the subtending axes, branching patterns, and the overall size of the minute plants, as is the case in Electorotheca. Regarding the cooksonioids, there are compression fossils preserved elsewhere that indicate the relatively small stature of the plants (a few millimeters) (e.g., Fanning et al., 1992). This problem is particularly an issue when we were presented with the very small size of the cryptophytes, especially in the Partitatheca complex. The question then arose as to whether these sporangia terminated a small autonomous

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TABLE 4.2 Lochkovian Assemblages From the Anglo-Welsh Basin, Approximately in Stratigraphical Order From Oldest to Youngest (MNeBZ Sporomorph Assemblage Biozones) Stratigraphy

Geographical Area

Biozone/Age

Taphonomy

Freshwater West Fm.

Brecon Beacons

Lower MN Biozone; early Lochkovian

Compressions in distal fluviatile channel siltstones and sandstones1

Targrove

Clee Hills, Shropshire

Lower MN Biozone; early Lochkovian

Compressions in distal fluviatile channel and crevasse splay siltstones and sandstones2,3

North Brown Clee Hill

Clee Hills, Shropshire

Middle MN Biozone; middle Lochkovian

Charcoal in distal fluviatile siltstones4

Bryn Glas Tunnels

South Wales

Middle MN Biozone; middle Lochkovian

Compressions in distal fluviatile siltstones5

Cwm Mill

Black Mountains

Middle MN Biozone; middle Lochkovian

Compressions in distal fluviatile siltstones6

Craswall

Black Mountains

Middle-upper MN Biozone, middle-upper Lochkovian

Compressions in medial fluviatile siltstones and sandstones7

Newton Dingle

Clee Hills, Shropshire

Upper MN to BZ Biozone, late Lochkovian

Compressions in medial fluviatile sandstones8

Beacon Beacons

BZ Biozone, late Lochkovian

Compressions in medial fluviatile siltstones and sandstones9

Black Mountains

BZ Biozone, late Lochkovian

Compressions in medial fluviatile siltstones and sandstones9

Pembrokeshire

BZ Biozone, late Lochkovian

Compressions and permineralisations in medial fluviatile silty sandstones10

Locality Tredomen Quarry

Allt Ddu

Senni Fm.

Rhiw Wen Mascle Bridge Quarry

Llanstadwell Fm.

1

Morris et al., 2011a; 2Fanning et al., 1992; 3Morris, 2009; 4Edwards et al., 1994; 5Wellman et al., 2000; 6Kenrick, 1988; 7Morris and Edwards, 2014; Edwards and Richardson, 1974; 9Habgood, 2000; 10Edwards et al., 1989.

8

axial system or were the parts of a larger, multibranched sporophyte with decreasing axial diameter with each dichotomy. However, compressed sporangia of similar dimensions and shape have been recorded in the siltstones at Tredomen Quarry (Morris et al., 2011a), where they terminate small branching systems, thus confirming the existence of plants of such small stature. Conversely, because of their simplicity and lack of anatomical preservation, they could only be categorized by overall morphology and cannot be directly compared with the charcoalified taxa.

4.2 Comparisons Between Different Preservation Types The problem of comparing compression and charcoalified fossils is also encountered particularly when dealing with the morphological simplicity of the early tracheophytes, where anatomical details (e.g., spores and conducting tissues) are essential in detecting relationships. Comparisons

are more easily made between taxa with distinctive features, such as the reproductive complex of Electorotheca, but even here uncertainties arise from possible compressional artefacts as those highlighted when comparing the reproductive structures with those of Eocooksonia. More commonly, problems arise with compressions and permineralizations of sporangia of similar morphology. For example, the elongate fusiform sporangium of Aglaophyton have been compared with some compression fossils from Spain (Teruelia) on the basis of shape and twisting of sporangia (Cascales-Miñana and Gerrienne, 2017), despite the absence of any of the defining anatomical characteristics (spores and conducting tissues) in the Spanish fossils. Similarly shaped sporangia, again with an oblique dehiscence fracture, are seen in coeval Lochkovian material of Salopella allenii from the Welsh Borders (Edwards and Richardson, 1974; Morris et al., 2011a; Morris and Edwards, 2014), but, again, there are insufficient anatomical details to allow congeneric assessment. However, while small Salopella-shaped sporangia are recorded in

Advantages and Frustrations of a Plant Lagersta¨tte Chapter j 4

the Lagerstätte assemblage (Edwards et al., 1994), with information on spores and dehiscence, with possible compression counterparts in South Wales and the Welsh Borderland (S. marcensis; Fanning et al., 1992), they should still be distinguished from Aglaophyton in the absence of evidence for conducting cells. Where Cooksonia pertoni is recorded as a compression fossil, the subspecies would be impossible to identify in the absence of spores (Fanning et al., 1988). This is also the case for Paracooksonia and Lenticulatheca, which, if preserved as compression fossils, would look identical to C. pertoni but are distinguished from the latter based on the cellular construction of the sporangial walls and the in situ spores (Morris et al., 2011b). Therefore, our assessment of diversity is biased toward charcoalified and permineralized assemblages, with diversity “hidden” within compressed assemblages.

4.3 Diversity The Lagerstätte at north Brown Clee Hill has yielded more taxa than any other locality in the Anglo-Welsh Basin (Table 4.1). It has been particularly critical to the determination of the parent plants of cryptospores, because the exceptional preservation has allowed for the identification of the in situ spores of such small sporangia, which has yet to be achieved from compressed mesofossils. As such, it is the only Lochkovian assemblage where cryptophytes have been recognized, representing 37% of the formally described species present. The only other rocks in the Anglo-Welsh Basin to yield cryptophytes are the siltstones from Ludford Lane, Shropshire, of Prídolí age, where simple charcoalified spore masses have been described (Wellman et al., 1998b). This is because of the size fraction and the bias toward the anatomical preservation of very small plants by charcoalification, as discussed in Sections 4.1 and 4.2. Of the trilete-bearing plants, only small plants with sporangia less than about 2e3 mm in diameter are present in the Lagerstätte (e.g., C. pertoni, Tortilicaulis offaeus). The sporangia in the reproductive complexes of Electorotheca are among the largest found (Table 4. 1). Larger plants, such as Cooksonia hemisphaerica, Salopella allenii, and the zosterophylls, are absent, despite their widespread occurrences in other assemblages across the basin (Table 4.1).

5. FUTURE RESEARCH 5.1 New Localities The sedimentology of the Lower Devonian Anglo-Welsh Basin has been extensively studied and has produced comprehensive insights on the depositional environments across the basin, including the generation of

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palaeogeomorphological frameworks that reflect the landscape (e.g., Allen and Tarlo, 1963; Allen, 1964, 1974; Allen and Dineley, 1976; Allen and Williams, 1979; Marriott and Wright, 1996, 2004; Williams and Hillier, 2004; Hillier et al., 2007; Marriott and Hillier, 2014). Many studies focus on the extensive coastal outcrops of Pembrokeshire, SW Wales, while in the Brecon Beacons and Welsh Borderland, exposure is restricted to short stream sections, road cuttings, or small quarries (Barclay et al., 2005). The majority of the exposures in this region reveal fining-up sequences of sandstones and siltstones, with sedimentary structures indicative of fluvial deposition. As discussed in Section 4.1, the charcoalified mesofossils of the Lagerstätte were found in siltstones at the top of a fining-upward sequence that were deposited and/or buried under reducing conditions. This lithofacies commonly occurs in this region (Allen and Tarlo, 1963; Allen, 1974), and it is likely that similar associations with small plant fossils occur elsewhere within the basin. However, the minute size of the fossils means that they are barely visible with the naked eye while embedded in the matrix and are revealed after only maceration, making recognition in the field challenging. In addition, the fine-grained nature of the rock renders it very susceptible to erosion on exposure. Indeed, the Lagerstätte described here is at risk because its survival depends on the presence of a sandstone slab immediately above. Nevertheless, a combination of the abundance of siltstone beds and the tendency for wildfires to be widespread encourages the search for further charcoal-based Lagerstätten in the area.

5.2 Bulk Maceration and Sorting Since the discovery of the locality by J.B. Richardson in the mid-1980s, a succession of students and postdocs (Una Fanning, Charles Wellman, Kate Habgood, Elena Mendez) have studied the Lagerstätte at Cardiff University and, under the guidance of technician Lindsey Axe, have sifted through thousands of fragments before examination by scanning electron microscopy (SEM) and, to a lesser extent, transmission electron microscopy (TEM), undertaken by Kevin Davies. While some taxa (e.g., Cooksonia, Tortilicaulis, Pachytheca, Prototaxites/ Nematasketum) and coprolites are relatively frequent and represent a greater proportion of indeterminate fragments, some of the major advances have been made by the recovery of a single specimen, or certainly less than 10 specimens (e.g., Wellman et al., 1998a; Edwards et al., 1999). Most recently, these include the discovery of thalloid lichens (Honegger et al., 2013), the distinction of a new lineage of basal embryophytes (Edwards et al., 2012a), and a number of taxa containing cryptospores (Edwards et al., 2014). These essentially serendipitous discoveries, which continue to make breakthroughs after

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SECTION j I Early Land Plants: Innovations and Adaptations

30 years of study, demonstrate the need for continuing a routine sifting approach.

5.4 Technological Advances in Anatomical Investigations

critically, visualization of the internal anatomy. In a pilot project, in collaboration with Prof. Phil Donoghue at the University of Bristol, a selection of mesofossils from the north Brown Clee Hill locality were scanned at the TOMCAT beamline at the Swiss Light Source (Paul Scherrer Institute, Switzerland). Advantages of using SRXTM over SEM include minimal sample preparation (uncoated), quick scan times (approximately 6 minutes per specimen), and the visualization and reconstruction of internal anatomy in any orientation. However, initial results have highlighted some challenges, including those specific to the plant fossils from this Lagerstätte. First, their minute and brittle nature makes their transfer from sticky carbon SEM stubs to the brass pins used for SRXTM a risky procedure, in terms of accidental fragmentation or loss of the specimen. In particular, where axial specimens (i.e., narrow and long) are required to be orientated upright, they are at risk of overmanipulation and breakage. Second, in initial scans, to fit whole specimens within the field-of-view, the resolution was compromised. Higher magnification can be obtained with further scanning, with a reduction in the field-of-view, but this requires more beam time, which is restricted by expense and demand. Third, pyrite crystals are highly absorbing and as such appear very bright in the images, resulting in a comparative loss of contrast for the fossilized material, as well as causing streak artefacts. The inundation of pyrite crystals within some specimens hampers their visualization and reconstruction. However, once these challenges are overcome, SRXTM will be a powerful tool for the characterization of these early embryophyte fossils in the future.

5.4.1 Electron Microscopy and Synchrotron Tomography

5.4.2 Light Microscopy

5.3 Comprehensive Comparisons With the Dispersed Spore Record While the assemblage at north Brown Clee Hill has been very important to the understanding of early land plant anatomy and the recognition of early embryophyte lineages, it does not provide an accurate picture of the relative proportions of these lineages in the region during the Lochkovian. To gain a better understanding of the level of diversity captured by the Lagerstätte in comparison to other localities where body fossils are preserved differently and to the regional variation in vegetation, we turn to the dispersed spore record. While great advances have been made in identifying the diversity and patterns of evolution of dispersed spore taxa across the basin between the Wenlock ad Pragian (e.g., Richardson 1967, 1996b, 2007; Richardson and Lister 1969; Burgess and Richardson 1995; Wellman et al., 1998c), there is still key work to be done on a series of palynological assemblages systematically collected by John Richardson from near uninterrupted sequences between the Prídolí and upper Lochkovian in the Clee Hills and Welsh Borderland (J.B.R., unpublished work). Several taxa have been identified but have not yet been formally described.

Major advances in determining the anatomy and affinity of these fossils have been made by using SEM (most recently, field emission SEM), involving semidestructive invasive processes (e.g., splitting the specimen with the use of a razor blade to reveal the internal anatomy and then coating with gold palladium). More recently, the development of the helium ion microscopy (HIM) offers greater resolution without the coating, as trialed at NEXUS, based at Newcastle University, in collaboration with Dr. Geoff Abbott, but at very great expense for routine studies. An alternative approach is synchrotron radiation X-ray tomographic microscopy (SRXTM), whih allows us to characterize fossils in a noninvasive and nondestructive way, with a resolution to a submicron level, as has been demonstrated in the studies of other charcoalified plant fossils (e.g., Carboniferous seed fern fertile organs, Scott et al., 2009; angiosperms, Friis et al., 2014). SRXTM produces a large dataset of two-dimensional images through a scanned specimen, which allows for the threedimensional reconstruction of the whole fossil and, more

There has been some success in embedding the charcoalified specimens in resin and sectioning for spores via TEM (e.g., Edwards et al., 1995b, 1999, 2012a; Wellman et al., 1998a), but again this is a very labor-intensive and costly process. Semithin sections prepared in a similar way but for light microscopy have also yielded useful spore information, albeit at lower resolution (Morris et al., 2011b, 2012b; Edwards et al., 2012c), but this might be a sensible approach to the detection of vascular tissue in axial fossils. However, once again, there is the problem of pyrite crystals, causing difficulties in sectioning using diamond knives.

5.5 Geochemical Approaches Some progress has been made in the detection of elemental and molecular composition of carbonaceous fossils (e.g., alkenes, alkanes, alkylphenols) using flash pyrolysisegas chromatographyemass spectrometry (PyGC-MS) (Ewbank et al., 1996), with similar unpublished

Advantages and Frustrations of a Plant Lagersta¨tte Chapter j 4

results including the detection of nitrogen in charcoalified material. Refinement of this technique is ongoing, but a combination of X-ray photoelectron spectroscopy with time-of-flight secondary ion mass spectrometry (ToFSIMS) offers an alternative approach to characterize elemental signatures. ToF-SIMS also offers a method for molecular characterization for spatial imaging at submicron levels. A further nondestructive approach, which has already been applied to the charcoalified fossils by using the Berkeley synchrotron, in collaboration with George Cody and David Kilcoyne, has produced fascinating results in detecting organic matter in a variety of tissues. X-ray absorption near edge fine structure, in combination with scanning transmission X-ray microscopy, is a powerful experimental technique that produces spatially resolved images and chemical analysis. It clearly has potential in detecting affinities in extinct organisms (e.g., Pachytheca), although the extent to which original chemistry is modified during charcoalification requires further experimentation.

ACKNOWLEDGMENTS The authors thank Jamie Stanfield, who found one of the specimens as part of a M.Sc. student project and Dr. Una Fanning who initially described a specimen during her doctoral studies. This work has been funded by the Gatsby Charitable Foundation and the Leverhulme Trust. JLM was funded by NERC Standard Grant NE/N003438/1 (University of Bristol) at the time of preparation of the paper.

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Banks, H.P., 1968. The early history of land plants. In: Drake, E.T. (Ed.), Evolution and Environment: A Symposium Presented on the One Hundredth Anniversary of the Foundation of Peabody Museum of Natural History at Yale University. Yale University Press, New Haven, pp. 73e107. Barclay, W.J., Browne, M.A.E., McMillan, A.A., Pickett, E.A., Stone, P., Wilby, P.R., 2005. The Old Red Sandstone of Great Britain. Geological Conservation Review Series No. 31. Joint Nature Conservation Committee, 393 pp. Barclay, W.J., Davies, J.R., Hillier, R.D., Waters, R.A., 2015. Lithostratigraphy of the Old Red Sandstone Successions of the Anglo-Welsh Basin. British Geological Survey Research Report Rr/14/02. British Geological Survey, Keyworth, UK, pp. 1e196. Burgess, N.D., Richardson, J.B., 1995. Late Wenlock to Early Prídolí cryptospores and miospores from South and Southwest Wales, Great Britain. Palaeontographica Abteilung B 236, 1e44. Cai, C.-Y., Dou, Y.-W., Edwards, D., 1993. New observations on a Prídolí plant assemblage from north Xinjiang, northwest China, with comments on its evolutionary and palaeogeographical significance. Geological Magazine 130, 155e170. Cascales-Miñana, B., Gerrienne, P., 2017. Teruelia diezii gen. et sp. nov.: an early polysporangiate from the Lower Devonian of the Iberian Peninsula. Palaeontology 60, 199e212. Doweld, A.B., 2000. Eocooksonia, a new substitute name for Cooksonella (CooksoniaceaeeRhyniophyta). Taxon 49, 547. Duckett, J.G., Pressel, S., 2009. Extraordinary features of the reproductive biology of Marchantia at Thursley Common. Field Bryology 97, 2e11. Edwards, D., 1981. Studies on Lower Devonian petrifactions from Britain. 2. Sennicaulis, a new form genus for sterile axes based on pyrite and limonite petrifactions from the Senni Beds. Review of Palaeobotany and Palynology 32, 207e226. Edwards, D., 1993. Cells and tissues in the vegetative sporophyte of early land plants. New Phytologist 125, 225e247. Edwards, D., 1996. New insights into early land ecosystems: a glimpse of a Lilliputian world. Review of Palaeobotany and Palynology 90, 159e174. Edwards, D., 2004. Embryophytic sporophytes in the Rhynie and Windyfield cherts. Transactions of the Royal Society of Edinburgh Earth Sciences 94, 397e410. Edwards, D., Axe, L., 1992. Stomata and mechanics of stomatal functioning in some early land plants. Courier Forschungsinstitut Senckenberg 147, 59e73. Edwards, D., Axe, L., 2004. Anatomical evidence in the detection of the earliest wildfires. PALAIOS 19, 113e128. Edwards, D., Axe, L., 2012. Evidence for a fungal affinity for Nematasketum, a close ally of Prototaxites. Botanical Journal of the Linnean Society 168, 1e18. Edwards, D., Fanning, U., 1985. Evolution and environment in the Late Silurian e Early Devonian: the rise of the pteridophytes. Philosophical Transactions of the Royal Society of London B 309, 147e165. Edwards, D., Richardson, J.B., 1974. Lower Devonian (Dittonian) plants from the Welsh Borderland. Palaeontology 17, 311e324. Edwards, D., Richardson, J.B., 2000. Progress in reconstructing vegetation on the Old Red Sandstone continent: two Emphanisporites producers from the Lochkovian sequence of the Welsh Borderland. Geological Society, London, Special Publications 180, 355e370. Edwards, D., Richardson, J.B., 2004. Silurian and Lower Devonian plant assemblages from the Anglo-Welsh Basin: a palaeobotanical and palynological synthesis. Geological Journal 39, 375e402.

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Edwards, D., Kenrick, P., Carluccio, L.M., 1989. A reconsideration of cf. Psilophyton princeps (Croft and Lang, 1942), a zosterophyll widespread in the Lower Old Red Sandstone of South Wales. Botanical Journal of the Linnean Society 100, 293e318. Edwards, D., Davies, K.L., Axe, L., 1992. A vascular conducting strand in the early land plant Cooksonia. Nature 357, 683e685. Edwards, D., Fanning, U., Richardson, J.B., 1994. Lower Devonian coalified sporangia from Shropshire: Salopella Edwards & Richardson and Tortilicaulis Edwards. Botanical Journal of the Linnean Society 116, 89e110. Edwards, D., Selden, P.A., Richardson, J.B., Axe, L., 1995a. Coprolites as evidence for plant-animal interaction in Siluro-Devonian terrestrial ecosystems. Nature 377, 329e331. Edwards, D., Davies, K.L., Richardson, J.B., Axe, L., 1995b. The ultrastructure of spores of Cooksonia pertoni. Palaeontology 38, 153e168. Edwards, D., Fanning, U., Davies, K.L., Axe, L., Richardson, J.B., 1995c. Exceptional preservation in Lower Devonian coalified fossils from the Welsh Borderland: a new genus based on reniform sporangia lacking thickened borders. Botanical Journal of the Linnean Society 117, 233e254. Edwards, D., Kerp, H., Hass, H., 1998. Stomata in early land plants: an anatomical and ecophysiological approach. Journal of Experimental Botany 49, 255e278. Edwards, D., Wellman, C.H., Axe, L., 1999. Tetrads in sporangia and spore masses from the Upper Silurian and Lower Devonian of the Welsh Borderland. Botanical Journal of the Linnean Society 130, 111e156. Edwards, D., Axe, L., Mendez, E., 2001. A new genus for isolated bivalved sporangia with thickened margins from the Lower Devonian of the Welsh Borderland. Botanical Journal of the Linnean Society 137, 297e310. Edwards, D., Richardson, J.B., Axe, L., Davies, K.L., 2012a. A new group of Early Devonian plants with valvate sporangia containing sculptured permanent dyads. Botanical Journal of the Linnean Society 168, 229e257. Edwards, D., Selden, P.A., Axe, L., 2012b. Selective feeding in an Early Devonian terrestrial ecosystem. PALAIOS 27, 509e522. Edwards, D., Morris, J.L., Richardson, J.B., Axe, L., Davies, K.L., 2012c. Notes on sporangia and spore masses containing tetrads or monads from the Lower Devonian (Lochkovian) of the Welsh Borderland, U.K. Review of Palaeobotany and Palynology 179, 56e85. Edwards, D., Axe, L., Honegger, R., 2013. Contributions to the diversity in cryptogamic covers in the mid-Palaeozoic: Nematothallus revisited. Botanical Journal of the Linnean Society 173, 505e534. Edwards, D., Morris, J.L., Richardson, J.B., Kenrick, P., 2014. Cryptospores and cryptophytes reveal hidden diversity in early land floras. New Phytologist 202, 50e78. Ewbank, G., Edwards, D., Abbott, G.D., 1996. Chemical characterization of Lower Devonian vascular plants. Organic Geochemistry 25, 461e473. Fanning, U., 1987. Late Silurian e Early Devonian Plant Assemblages in the Welsh Borderland (Ph.D. thesis). University of Wales, Cardiff, UK. Fanning, U., Richardson, J.B., Edwards, D., 1988. Cryptic evolution in an early land plant. Evolutionary Trends in Plants 2, 13e24. Fanning, U., Edwards, D., Richardson, J.B., 1990. Further evidence for diversity in late Silurian land vegetation. Journal of the Geological Society, London 147, 725e728.

Fanning, U., Richardson, J.B., Edwards, D., 1991a. A review of in situ spores in Silurian land plants. In: Blackmore, S., Barnes, S.H. (Eds.), Pollen and Spores, Systematics Association, Special vol. 44. Clarendon Press, Oxford, pp. 22e47. Fanning, U., Edwards, D., Richardson, J.B., 1991b. A new rhyniophytoid from the late Silurian of the Welsh Borderland. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 183, 37e47. Fanning, U., Edwards, D., Richardson, J.B., 1992. A diverse assemblage of early land plants from the Lower Devonian of the Welsh Borderland. Botanical Journal of the Linnean Society 109, 161e188. Field, K.J., Duckett, J.G., Cameron, D.D., Pressel, S., 2015. Stomatal density and aperture in non-vascular land plants are non-responsive to above-ambient atmospheric CO2 concentrations. Annals of Botany 115, 915e922. Friend, P.F., Williams, B.P.J., Ford, M., Williams, E.A., 2000. Kinematics and dynamics of Old Red Sandstone basins. In: Friend, P.F., Williams, B.P.J. (Eds.), New Perspectives on the Old Red Sandstone, pp. 29e60. Geological Society, London, Special Publications 180. Friis, E.M., Skarby, A., 1981. Structurally preserved angiosperm flowers from the Upper Cretaceous of southern Sweden. Nature 291, 484e486. Friis, E.M., Marone, F., Pedersen, K.R., Crane, P.R., Stampanoni, M., 2014. Three-dimensional visualization of fossil flowers, fruits, seeds, and other plant remains using synchrotron radiation X-ray tomographic microscopy (SRXTM): new insights into Cretaceous plant diversity. Journal of Palaeontology 88, 684e701. Gensel, P.G., Andrews, H.N., Forbes, W.H., 1975. A new species of Sawdonia with notes on the origin of microphylls and lateral sporangia. Botanical Gazette 136, 50e62. Gensel, P.G., Wellman, C.H., Taylor, W.A., 2013. Spore wall ultrastructure of the Lower Devonian zosterophylls Renalia hueberi and Zosterophyllum divaricatum. International Journal of Plant Sciences 174, 1302e1313. Glasspool, I.J., Edwards, D., Axe, L., 2006. Charcoal in the Early Devonian: a wildfire-derived Konservat-Lagerstätte. Review of Palaeobotany and Palynology 142, 131e136. Grimes, S.T., Brock, F., Rickard, D., Davies, K.L., Edwards, D., Briggs, D.E.G., Parkes, R.J., 2001. Understanding fossilization: experimental pyritization of plants. Geology 29, 123e126. Habgood, K.S., 2000. Integrated approaches to the cycling of primary productivity in early terrestrial ecosystems (Ph.D. thesis). Cardiff University, UK. Habgood, K.S., Edwards, D., Axe, L., 2002. New perspectives on Cooksonia from the Lower Devonian of the Welsh Borderland. Botanical Journal of the Linnean Society 139, 339e359. Hao, S.G., 1989. A new zosterophyll from the Lower Devonian (Siegenian) of Yunnan, China. Review of Palaeobotany and Palynology 57, 155e171. Hao, S.G., Xue, J.Z., 2013. The Early Devonian Posongchong Flora of Yunnan e A Contribution to an Understanding of the Evolution and Early Diversification of Vascular Plants. Science Press, Beijing, 366 pp. Hillier, R.D., Marriott, S.B., Williams, B.P.J., Wright, V.P., 2007. Possible climate variability in the Lower Old Red Sandstone Conigar Pit Sandstone Member (Early Devonian), South Wales, UK. Sedimentary Geology 202, 35e57. Honegger, R., Edwards, D., Axe, L., 2013. The earliest records of internally stratified cyanobacterial and algal lichens from the Lower Devonian of the Welsh Borderland. New Phytologist 197, 264e275.

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Kenrick, P., 1988. Studies on Lower Devonian Plants from South Wales (Ph.D. thesis). University of Wales, Cardiff, UK. Kenrick, P., Crane, P.R., 1991. Water-conducting cells in early land plants: implications for the early evolution of tracheophytes. Botanical Gazette 152, 335e356. Kenrick, P., Crane, P.R., 1997. The Origin and Early Diversification of Land Plants: A Cladistic Study. Smithsonian Institution Scholarly Press, Washington, 456 pp. Kenrick, P., Edwards, D., 1988. The anatomy of Lower Devonian Gosslingia breconensis Heard based on pyritized axes, with some comments on the permineralization process. Botanical Journal of the Linnean Society 97, 95e123. Lang, W.H., 1937. On the plant-remains from the Downtonian of England and Wales. Philosophical Transactions of the Royal Society of London B 227, 245e291. Lenton, T.M., Dahl, T.W., Daines, S.J., Mills, B.J.W., Ozaki, K., Saltzman, M.R., Porada, P., 2016. Earliest land plants created modern levels of atmospheric oxygen. Proceedings of the National Academy of Sciences of the United States of America 113, 9704e9709. Marriott, S.B., Hillier, R.D., 2014. Fluvial style in the Lower Old Red Sandstone: examples from Southwest Wales, UK. Proceedings of the Geologists’ Association 125, 534e547. Marriott, S.B., Wright, V.P., 1996. Sediment recycling on Siluro-Devonian floodplains. Journal of the Geological Society, London 153, 661e664. Marriott, S.B., Wright, V.P., 2004. Mudrock deposition in an ancient dryland system: Moor Cliffs Formation, Lower Old Red Sandstone, Southwest Wales, UK. Geological Journal 39, 277e298. Morris, J.L., 2009. Integrated approaches to the reconstruction of early land vegetation and environments from Lower Devonian strata, Central South Wales (Ph.D. thesis). Cardiff University, UK. Morris, J.L., Edwards, D., 2014. An analysis of vegetational change in the Lower Devonian: new data from the Lochkovian of the Welsh Borderland, U.K. Review of Palaeobotany and Palynology 211, 28e54. Morris, J.L., Richardson, J.B., Edwards, D., 2011a. Lower Devonian plant and spore assemblages from Lower Old Red Sandstone strata of Tredomen Quarry, South Wales. Review of Palaeobotany and Palynology 165, 183e208. Morris, J.L., Edwards, D., Richardson, J.B., Axe, L., Davies, K.L., 2011b. New plant taxa from the Lower Devonian (Lochkovian) of the Welsh Borderland, with a hypothesis on the relationship between hilate and trilete spore producers. Review of Palaeobotany and Palynology 167, 51e81. Morris, J.L., Wright, V.P., Edwards, D., 2012a. Siluro-Devonian landscapes of southern Britain: the stability and nature of early vascular plant habitats. Journal of the Geological Society, London 169, 173e190. Morris, J.L., Edwards, D., Richardson, J.B., Axe, L., Davies, K.L., 2012b. Further insights into trilete spore producers from the Early Devonian (Lochkovian) of the Welsh Borderland, U.K. Review of Palaeobotany and Palynology 185, 35e63. Raven, J.A., Edwards, D., 2004. Physiological evolution of lower embryophytes: adaptations to the terrestrial environment. In: Hemsley, A.R., Poole, I. (Eds.), The Evolution of Plant Physiology: From Whole Plants to Ecosystems. Linnean Society Symposium Series 21. Elsevier Academic Press, London, pp. 17e41. Richardson, J.B., 1967. Some British Lower Devonian spore assemblages and their stratigraphic significance. Review of Palaeobotany and Palynology 1, 111e129.

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Richardson, J.B., 1996a. Lower and Middle Palaeozoic record of terrestrial palynomorphs. In: Jansonius, J., McGregor, D.C. (Eds.), Palynology: Principles and Applications, vol. 2. American Association of Stratigraphical Palynologists Foundation, Dallas, pp. 555e574 (Chapter 18A). Richardson, J.B., 1996b. Taxonomy and classification of some new Early Devonian cryptospores from England. Special Papers in Palaeontology 55, 7e40. Richardson, J.B., 2007. Cryptospores and miospores, their distribution patterns in the Lower Old Red Sandstone of the Anglo-Welsh Basin, and the habitat of their parent plants. Bulletin of Geosciences 82, 355e364. Richardson, J.B., Lister, T.R., 1969. Upper Silurian and Lower Devonian spore assemblages from the Welsh Borderland and South Wales. Palaeontology 12, 201e252. Richardson, J.B., McGregor, D.C., 1986. Silurian and Devonian spore zones of the Old Red Sandstone Continent and adjacent regions. Bulletin of the Geological Survey of Canada 364, 1e79. Scott, A.C., Galtier, J., Gosling, N.J., Smith, S.Y., Collinson, M.E., Stampanoni, M., Marone, F., Donoghue, P.C., Bengtson, S., 2009. Scanning electron microscopy and synchrotron radiation x-ray tomographic microscopy of 330 million year old charcoalified seed fern fertile organs. Microscopy and Microanalysis 15, 166e173. Seilacher, A., Reif, W.-E., Westphal, F., 1985. Sedimentological, ecological and temporal patterns of fossils Lagerstätten. Philosophical Transactions of the Royal Society of London B 311, 5e23. Simon, J.B., Bluck, B.J., 1982. Palaeodrainage of the southern margin of the Caledonian mountain chain in the northern British Isles. Transactions of the Royal Society of Edinburgh Earth Sciences 73, 11e15. Wang, Q., Xu, H.H., 2011. A nomenclatural note on the Late Silurian rhyniophytoid Junggaria. Acta Palaeontologica Sinica 50, 326e329 (in Chinese with English abstract). Wellman, C.H., Edwards, D., Axe, L., 1998a. Permanent dyads in sporangia and spore masses from the Lower Devonian of the Welsh Borderland. Botanical Journal of the Linnean Society 127, 117e147. Wellman, C.H., Edwards, D., Axe, L., 1998b. Ultrastructure of laevigate hilate spores in sporangia and spore masses from the Upper Silurian and Lower Devonian of the Welsh Borderland. Philosophical Transactions of the Royal Society B 353, 1983e2004. Wellman, C.H., Thomas, R.G., Edwards, D., Kenrick, P., 1998c. The Coheston Group (Lower Old Red Sandstone) in Southwest Wales: age, correlation and palaeobotanical significance. Geological Magazine 135, 397e412. Wellman, C.H., Habgood, K., Jenkins, G., Richardson, J.B., 2000. A new plant assemblage (microfossil and megafossil) from the Lower Old Red Sandstone of the Anglo-Welsh Basin: its implications for the palaeoecology of early terrestrial ecosystems. Review of Palaeobotany and Palynology 109, 161e196. Williams, B.P.J., Hillier, R.D., 2004. Variable alluvial sandstone architecture within the Lower Old Red Sandstone, Southwest Wales. Geological Journal 39, 257e275. Xue, J.Z., 2009. Two zosterophyll plants from the Lower Devonian (Lochkovian) Xitun Formation of Northeastern Yunnan, China. Acta Geologica Sinica 83, 504e512. Xue, J.Z., Wang, Q., Wang, D., Wang, Y., Hao, S.G., 2015. New observations of the early land plant Eocooksonia Doweld from the Prídolí (Upper Silurian) of Xinjiang, China. Journal of Asian Earth Sciences 101, 30e38.

Chapter 5

Early Tracheophyte Phylogeny: A Preliminary Assessment of Homologies William L. Crepet and Karl J. Niklas Cornell University, Ithaca, NY, United States

The task of explaining the connection between the several groups [of vascular cryptogams] has been rendered difficult by the present state of the terminology, which is one of transition. We may hope however that the terminology will soon be greatly simplified and cleared up by applying the acknowledged homologies. Karl R. von Goebel (1882)

1. INTRODUCTION The history of investigating the explosive SilurianDevonian diversification of the land plants is replete with the fastidious examination of pivotal fossil plants beginning with the studies of Kidston and Lang (1917), concomitant comparative analyses of extant plants, particularly those of F.O. Bower (1908) and D.H. Campbell (1940), and inspired hypotheses about the phylogeny of early Paleozoic plants (Zimmermann, 1930, 1959; Banks, 1968, 1975; Stewart, 1993). Most recently, Kenrick and Crane (1997) provided a rigorous and thoughtful analysis of Devonian plants with historical context, explication of relevant characters, and a number of phylogenetic hypotheses, including an overall analysis of the phylogenetic relationships among 34 key taxa using 31 characters. They also provided detailed analyses of individual major lineages including additional fossil taxa represented in each of the species-groupings. In addition, Kenrick and Crane (1997) identified major questions surrounding the diversification of Devonian plants that extend to understanding extant plant diversity and phylogeny.

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00005-X Copyright © 2018 Elsevier Inc. All rights reserved.

As in all examinations of fossil materials, unavoidable limitations were imposed on their analyses. For example, the computational ability of the phylogenetic algorithms available at the time was insufficient to cope with the fact that many important fossil taxa had relatively few diagnostic characters, which resulted in many missing character states that had unavoidably deleterious effects on any phylogenetic analyses (e.g., Nixon and Davis, 1991). In addition, the algorithms available to Kenrick and Crane (1997) were severely limited in their ability to generate trees in a timely fashion. Currently, much more rapid analytical techniques with which to construct phylogenetic hypotheses are now available. In addition, more data on some of the fossil taxa used in their analyses have come to light, and many newly discovered taxa offer the hope of constructing transformational series among lineages. Nonetheless, our understanding of the anatomy, morphology, and reproductive biology of SilurianDevonian land plants is still far from comprehensive because of their incomplete states of fossilization and taphonomic biases that limit our cognizance of floristic diversity, particularly that of upland communities. Perhaps most vexing is the resolution of organographic homologies among ancient organisms that had yet to evolve clear anatomical and reproductive differences among their body parts, a problem that is all the more concerning owing to the high probability of mosaic and convergent evolution. Our objective in this chapter is to explore the effects of these and other limitations on the interpretation of early tracheophyte phylogeny as well as to offer some tentative hypotheses about their phylogeny from the perspective of interpreting homologies among phenotypically simple plants. Indeed, we recognize this as a principal challenge.

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For this purpose, we present a set of analyses of 36 critical and well-preserved early Paleozoic land plants and the extant taxon Equisetum. As will be shown, these analyses identify highly resolved phylogenetic trees that share a core branching topology consistent with broadly held views about early land plant diversification. Yet, at more finegrained levels of analyses, tree topologies identify surprising deviations from this core topology, raising intriguing questions about prior interpretations of land plant phylogeny. Of particular interest is the placement of Equisetum with fossil taxa that have been described as ferns and fernlike plants. As in prior studies of this kind, we present and discuss our analyses fully recognizing their preliminary and mercurial status and cognizant of the difficulties of coding characters for organisms manifesting poorly delineated organographic distinguishing features.

2. MATERIALS AND METHODS 2.1 Taxa Selection With one exception (i.e., Equisetum), the taxa used in our analyses span the SilurianeDevonian time interval, and, in three cases, the Carboniferous, to include important taxa emanating from well-recognized (e.g., Lepidodendron and Lyginopteris) or uncertain (e.g., Calamites) late Devonian lineages (Table 1). In addition, to its perceived importance as a key representative of a major lineage, each species was selected because it represented the best state of preservation for its genus. Thus, fossil taxa were selected based on two criteria: (1) they must provide an adequate representation of the major lineages to which they are assigned during the target geological interval, and (2) they must provide as many characters as possible to reduce the negative effects of missing characters on resolving phylogenetic relationships. We included additional taxa that did not meet these two criteria because they are the only representatives of interesting lineages (e.g., Nothia, Elkinsia, and EospermatopterisþWattieza). Consequently, the effect of missing characters on tree topologies was not totally avoided because the majority of the taxa in our matrices are known exclusively from aerial axes bereft of roots or rhizomes and, in some cases, even reproductive organs. The absence of anchorage organs has sometimes resulted in misinterpretations of the nature of what were thought to be relatively well-known plants. For example, Aneurophyton was considered to be arborescent because of its secondary growth. Yet, a newly discovered lagenstrattan has revealed that it was rhizomatous (Stein et al., 2012). The study of early Paleozoic fossil plants is particularly prone to “missing data” owing to the tendency of plants to fragment during transport and subsequent deposition. The phylogenetic placement of Equisetum was explored because of the controversy regarding its affiliation with

extant ferns. This controversy is addressed here by incorporating Equisetum in the extended matrix for 36 fossil taxa. As will be seen, an analysis of this matrix places Equisetum in an unresolved polytomy containing fossils that have been conventionally classified as ferns or fernlike plants (i.e., Calamophyton [Bonamo and Banks, 1966], Eospermatopteris, and Pseudosporochnus [Stein and Hueber, 1989]) along with representative fossil sphenophytes (i.e., Calamites and Archaecalamites). In total, four matrices were analyzed, one containing 33 fossil taxa (Table 1) rooted with Aglaophyton or Cooksonia at the base, another containing an additional three fossil taxa (i.e., Stauropteris, Archaeopteris, and Lyginopteris), and both the 33 and 36 matrices containing the extant genus Equisteum. The two matrices with only fossil taxa were used to determine the sensitivity of tree topologies to the inclusion or exclusion of evolutionarily important or interesting fossil taxa from an analysis. The matrix containing Stauropteris, Archaeopteris, and Lyginopteris was used to test the sensitivity of the 33 matrix tree topology to the inclusion of taxa. Stauropteris was selected because it is heterosporous, has microspores and megaspores within the same sporangium, and has sporangia with a micropyle like extension. Archaeopteris was included because of its arborescent growth habit, heterospory, exquisitely preserved anatomy, and critical phyletic importance in understanding progymnosperms. Finally, Lyginopteris was selected because it is an important and well-studied example of the seed ferns and because of its unusual anatomy and complex vegetative architecture.

2.2 Characters and Character Assignments As noted, for the purposes of this study, we ran two data sets composed exclusively of fossil taxa (Tables 1 and 2). In each case, character selection was challenging because there are numerous characters that are inapplicable to certain taxa, particularly in an analysis with a broad taxonomic scope and temporal range. This limitation is manifest even in the detailed analysis of Kenrick and Crane (1997), which used a set of characters for determining overall (“polysporangiophyte”) relationships among early land plants. To cope with this unavoidable limitation on the study of a phylogenetically broad spectrum of fossil taxa, these authors then used separate, more fine-grained sets of characters for analyzing the phylogenetic relationships within what were identified a priori as monophyletic groups (e.g., Zosterophyllopsida and Lycopsida [Grierson and Banks, 1963]). In contrast, our approach was to include characters that applied as broadly as possible to the majority of early Paleozoic plants and to minimize the number of characters that would be inapplicable only to various subsets or presumed monophyletic groups (although it was impossible to

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TABLE 1 Character Matrix 1 for Analyses 1, 1.1, and 1.2dAll Fossil Taxa

completely eliminate subsets or monophyletic groups in view of the increasing complexity of vascular plants as they radiated throughout the Devonian). The challenge was to construct matrices with as many homologous characters as possible while minimizing the number of characters that did not apply to progressively more complex groups and vice versa. This challenge was complicated further by details of anatomy that were at times ambiguous, conflated definitions of lateral structures (e.g., enations vs. leaves and

sporangia), differing branching pattern terminologies, and the interpretation of planarity among lateral organs (e.g., DiMichele et al., 2001; Rothwell and Nixon, 2006; Corvez et al., 2012). Inclusion of Equisetum was particularly challenging because of its idiosyncratic anatomy. For example, the Equisetum stele has been described as an ectophloic (solenoxylic) siphonostele (Bower, 1930, 1935), as a perforated ectophloic siphonostele (Schmidt, 1983), and simply as a siphonostele (Smith, 1955). An analogy

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TABLE 2 Character Matrix 2 for Analyses 2, 2.1, and 2.2 Extended Fossil Taxa

Continued

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TABLE 2 Character Matrix 2 for Analyses 2, 2.1, and 2.2 Extended Fossil Taxadcont’d

with the seed plant eustele has also been suggested (Niklas, 1997). The ambiguity of how to classify this type of stele is so great that Bold (1967) and Bierhorst (1971) avoided any terminological assignment. Nevertheless, many of the characters in the four matrices have been traditionally used to define Devonian plant groups even before phylogenetic methodologies were

available (e.g., Banks, 1968, 1975) and continue to be used in organizing discussions and descriptions of Devonian plant groups (e.g., Taylor et al., 2009). Accordingly, we have used these characters as well as a selection of those used by Kenrick and Crane in their comprehensive analysis of extant plants as well as early Paleozoic plants (Tables 1e3).

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TABLE 3 Character Matrix 2 With Equisetum Added

Continued

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TABLE 3 Character Matrix 2 With Equisetum Addeddcont’d

We have also tried to distinguish among variants of what others have taken as a single character as, for example, among the characteristics of the primary vascular tissue (e.g., characters 49e52, Tables 1e3). With respect to branching patterns, we have used some characters typically

employed in defining Devonian and post-Devonian plant groups but also tried to identify additional characters within those usually used to define branching (e.g., our characters include those related to dorsiventrality in fronds or lateral branching systems; see Corvez et al., 2012).

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2.3 Algorithms and Philosophy

3. RESULTS

Extensive analyses were performed on evolving matrices. In total, >100 iterations of the matrices used in our study were computed. Although the numbers and nature of characters and character states changed and some taxa were added or removed, we found surprising uniformity in critical aspects of tree topologies. With respect to the analyses themselves, all maximum parsimony phylogenetic analyses (heuristic search; maximum number of trees to keep ¼ 5,000,000; number of replications ¼ 400) were performed by using the program NONA (Goloboff, 1999), spawned through the program Winclada (Asado, version 1.1 beta, by K. Nixon, Cornell University). Characters were all unweighted. Winclada treats inapplicable characters (-) and unknown characters (?) in the same way. Winclada and parsimony were used because this analytical technique is most appropriate for relatively small data sets based on morphological characters. Some characters were coded as ordered or additive if they seemed unambiguously so based on either patterns in the fossil record, or on the logical consequences of plant development. To assess the sensitivity of analyses to the manner in which characters were coded, we coded 3/53 characters (Appendices 1 and 2) as additive according to criteria discussed herein but ran the same matrix (Matrix 1, Table 1) with all characters unordered or nonadditive and repeated the process for the other larger matrices (Matrices 2 and 3, Tables 2 and 3). We found that there were fewer most parsimonious trees in cases where a subset of characters was additive (2 fewer for Matrix 1, without differences in the consensus trees) but found that there were fewer most parsimonious trees when 10 additive characters in Matrix 2 were changed to nonadditive for the analysis (8 vs. 16), again without substantial changes to the trees. With one exception (i.e., Equisetum), extant taxa were omitted from our analyses because their frequently highly derived character states not found in fossils in the time interval of interest here would result in numerous missing characters (for the fossil taxa) and can alter phylogenetic interpretations of fossil organisms. Moreover, analyses using larger data sets containing extant taxa are likely to place fossil organisms on trees whose topologies are largely defined by the characters associated with extant organisms. Under these circumstances, the placement of fossil organisms on tree topologies is biased simply because of the sheer number of characters derived from extant organisms. In addition, our primary objective was to explore the possibility that matrices composed exclusively of fossil organisms might provide new insights into vascular plant history.

Each matrix was analyzed with or without Equisetum and established a core tree topology that complies remarkably well with the rhyniophyte-trimerophyte-zosterophyllophytelycophyte classification system of Banks (1968, 1975) as well as with aspects of the classification systems established by Kenrick and Crane (1997) and Taylor et al. (2009) (Figs. 5.1e5.4). They also produce trees that are remarkably stable even when rooted differently (e.g., using Aglaophyton vs. Cooksonia as the root taxon) (Figs. 5.1e5.2). The zosterophyllophytes-lycophytes are identified as a monophyletic group in all cases as well as a sequence of branches consisting of euphyllophytes among which the progymnosperms appear as either a monophyletic or paraphyletic species-group (e.g., Aneurophyton, Rellimia, and Tetraxylopteris) (compare Figs. 5.1 and 5.3). These branches are all subtended either by Oocampsa (which has been postulated as in a transformational series from the trimerophytes to the progymnosperms; Andrews et al., 1975) or by a trimerophyte (compare Figs. 5.1e5.3). Analyses further define a cluster of euphyllophyte lignophytes containing taxa with secondary growth (postulated for Calamophyton [Giesen and Berry, 2013], uncertain in Eospermatopteris and possibly lost in Pseudosporochnus) and an arborescent growth habit, with or without rhizomatous growth (e.g., Calamophyton and EospermatopterisþWattieza, respectively). Tree topologies also contain a series of fernlike taxa and seed plants between the trimerophytes and the lignophytes (e.g., Rhacophyton and Elkinsia). The matrices also identify trees that appear to suggest a number of hypotheses. Among the more intriguing of these is the location of Renalia, which is classified as a rhyniophyte (Gensel, 1976) with the combination of pseudomonopodial branching and reniform sporangia at the base of the euphyllophyte branch, the placement of Estinnophyton (a poorly understood taxon formerly considered to be a protolepidodendriod or even a sphenopsid, Hao et al., 2004; Taylor et al., 2009) within the zosterophyllophyte þ lycophyte cluster, and the location of the purported seed plant Elkinsia (which otherwise manifests a fern-like morphology) within a series of other fernlike taxa (Figs. 5.1e5.3). Most surprising is the consistent grouping of the sphenopsids (Calamites and Archaecalamites) with EospermatopterisþWattieza and PseudosporochnusþPietzchia (see Stein et al, 1984, for a detailed discussion of sphenophyte evolution). These arguably unexpected associations of taxa draw attention to two obvious yet important possibilities: (1) either characters states in our matrix have been improperly defined or coded or (2), unbeknown to us, important

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Aglaophyton Cooksonia P. Nothia aphylla

“rhyniophytes”

Rhynia Horneophyton Barinophyton obscurum Estinnophyton Zosterophyllum fertile Crenaticualis Gosslingia

“zosterophyllophytes”

Asteroxylon machiei

“lycophytes”

Baragwanathia Drepanophycus spinaeformis Clwydia Colpodexylon Leclercqia Lepidodendron Renalia

“trimerophytes”

Hsua Psilophyton dawsonii Rhacophyton

Elkinsia Yiduxylon Ibyka Oocampsa Aneurophyton Tetraxylopteris

“progymnosperms”

Rellimia Archaecalamites Calamites

“lignophytes”

Calamophyton Eospermatopteris+Wattieza Pseudosporochnus--Pietzchia

FIGURE 5.1 Consensus tree of 20 most parsimonious trees with 33 taxa rooted with Aglaophyton (L ¼ 180, Ci ¼ 53, Ri ¼ 71).

characters have been omitted from our analyses. If neither is true, it follows that aspects of traditional classification schemes are in need of further scrutiny. The former two possibilities must be freely acknowledged because (1) the manner in which some characters should be coded is always subject to change in light of new discoveries (e.g., the nonvascular nature of Aglaophyton and the rhizomatous nature of Aneurophyton) and because (2), as noted earlier, a number of important characters are currently unknown owing to incomplete states of preservation (e.g., the basal body parts of many taxa remain unknown). Another confounding problem is whether some taxa are form taxa (e.g., given the tremendous diversity of sporangial shapes and geometries, it would not be unreasonable to argue that Cooksonia is not a natural taxon, see Kenrick and Crane, 1997). Finally, we attempted to select a set of characters that would to the extent possible, minimize the

number of inapplicable character states associated with the breadth of taxa we incorporate in our analyses, and again, with the exception of Equisetum in some of our analyses, our approach was to include fossils only. As noted and discussed, this approach makes our analyses more vulnerable to unwanted effects associated with missing characters. Clearly, it is best to be conservative when evaluating the phylogenetic implications that our matrix generates. By the same token, we believe a fruitful dialogue can be gained by considering alternative phylogenetic relationships, particularly for taxa that have been the subject of extensive debate. As noted in Section 2, we examined the effects of including additional taxa on trees (Fig. 5.3) with what appear to have robust topologies. For this purpose, Stauropteris, Archaeopteris, and Lyginopteris were added to the matrix giving rise to the previously described trees (Fig. 5.3). The trees resulting from this sensitivity analysis

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---> Cooksonia P. Cooksonia Aglaophyton

“rhyniophytes”

Barinophyton obscurum

Crenaticualis

“zosterophyllophytes”

Asteroxylon machiei

“lycophytes”

Baragwanathia

Clwydia Colpodexylon

Leclercqia

“trimerophytes”

Aneurophyton

“progymnosperms” Archaecalamites Calamites

“lignophytes”

Calamophyton

FIGURE 5.2 Consensus tree of 20 most parsimonious trees with 33 taxa rooted with Cooksonia (L ¼ 180, Ci ¼ 52, Ri ¼ 71).

maintained topologies that conformed with those shown in Figs. 5.1 and 5.2 but nevertheless contained notable differences in the placement of some evolutionarily important taxa. Specifically, the consensus tree for the 36 taxa matrix has a topology reasonably reminiscent of the rhyniophytetrimerophyte-zosterophyllophyte-lycophyte classification system of Banks (1968, 1975) as well as critical aspects of the classification systems established by Kenrick and Crane (1997) and Taylor et al. (2009) (Fig. 5.5). Cooksonia and rhyniophytes are positioned at the base of the tree, and taxa traditionally classified as zosterophyllophytes and lycophytes are grouped as a single early divergent clade. As in the previously described trees, trimerophyte taxa are positioned at the base of a series of branches including fern-like taxa and culminating in euphyllophyte lignophytes (Fig. 5.3). Nevertheless, comparisons between the topologies of trees emerging from the 33 and 36 taxon matrices reveal notable differences. For example, Ibyka and Oocampsa

are more firmly associated and include a branch terminating with Stauropteris. Other differences from the 33 matrix trees include the locations of Rhacophyton, Elkinsia, and Yiduxylon. Aneurophyton, Rellimia, and Tetraxylopteris are shown to be even more paraphyletic than in previous analyses with the addition of Archaeopteris (which is distant from the progymnosperm “cohort”). The position of Rhacophyton is elevated in this tree topology (Fig. 5.3). These and other differences between the topologies of the consensus trees emerging from the 33 taxa matrix and 36 taxa matrices suffice to show that the results of our analyses are demonstrably sensitive to the exclusion or inclusion of taxa (as well as how taxa and characters are selected and how character states are coded). These differences in topologies are sufficient to show clearly that the interpretation of phylogenetic trees with limited numbers of morphological characters must be approached with considerable caution.

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Aglaophyton Cooksonia P. Horneophyton

“rhyniophytes”

Nothia aphylla Rhynia Asteroxylon machiei Baragwanathia Drepanophycus spinaeformis Barinophyton obscurum Crenaticualis Gosslingia

“zosterophyllophytes”

Zosterophyllum fertile

“lycophytes”

Estinnophyton Colpodexylon Clwydia Leclercqia Lepidodendron Renalia

“trimerophytes”

Hsua Psilophyton dawsonii Ibyka

Oocampsa Stauropteris Aneurophyton

“progymnosperms”

Rellimia Tetraxylopteris

Rhacophyton Elkinsia Yiduxylon Calamophyton Archaeopteris Lyginopteris Eospermatopteris+Wattieza Pseudosporochnus--Pietzchia

“lignophytes”

Archaeocalamites Calamites

FIGURE 5.3 Consensus of 16 most parsimonious trees with 36 taxa rooted with Aglaophyton (L ¼ 214, Ci ¼ 45, Ri ¼ 70).

Finally, the consensus tree for the 36 fossil taxa and Equisetum contains a terminal polytomy containing ArchaeopteriseLyginopteris, EospermatopterisþWattiezae PseudosporochnusþPietzchia, and Calamophytone EquisetumeCalamiteseArchaeocalamites (Fig. 5.4). This polytomy is subtended by a series of branches composed of ElkinsiaeYiduxylon and Rhacophyton that is in turn subtended by taxa traditionally assigned to the progymnosperms (Fig. 5.4).

4. DISCUSSION Perhaps the most controversial aspect of our analyses is the placement of the extant genus Equisetum with fossil taxa that have been described traditionally as ferns or fernlike plants (see Fig. 5.4). In this context, we note that the fossil record shows that modern ferns are polyphyletic and that, with the exception of the zosterophyllophytes and lycophytes, all vascular plant lineages are likely the

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“rhyniophytes”

“zosterophyllophytes” “lycophytes”

“trimerophytes”

“progymnosperms”

“lignophytes” Equisetum

Calamites

FIGURE 5.4 Consensus of 16 most parsimonious trees with 36 taxa and Equisetum rooted with Aglaophyton (L ¼ 219, Ci ¼ 44, Ri ¼ 70).

descendants of a trimerophytelike ancestral plexus of plants. In this respect, the consensus tree for the extended analysis including Equisetum mirrors this conventional wisdom because (1) the trimerophytes included in our analyses are basal to the euphyllophytes in all of the tree topologies, (2) fossils that have been traditionally described as “ferns” or fernlike organisms are demonstrably paraphyletic, and (3) Equisetum is positioned on a terminal branch of an otherwise early vascular plant phylogeny. Whether Equisetum is called a “fern” is

irrelevant in the present context because this designation is taxonomically and phylogenetically meaningless or, at best, ambiguous. We hold to the idea that Equisetum is the last survivor of a once morphologically, anatomically, and reproductively diverse clade that traces its origins to a group that (by definition) was the last common ancestor to all other euphyllophyte lineages (i.e., a trimerophyte plexus of early vascular plants including Calamophyton whose association with the sphenophytes is supported in our analyses (Fig. 5.4).

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FIGURE 5.5 Schematic of major anatomical, morphological, and reproductive evolutionary features achieved during the early course of vascular land plant evolution. These include the appearance of xylem preceded by the appearance of banded tube-like structures (a), cooksonoid-branching with terminal sporangia (b), stomata (c), unequal pseudomonopodial branching (d), vascularized lycophylls (e), trimerophyte branching (f), planated lateral branches (g), complex stelar anatomy (h), metaphyll (i), secondary growth (j), and the seed habit (k). The earliest occurrences of these features in the fossil record are minimum ages, since future discoveries may extend the age of any “first occurrence.” Data taken from the primary literature and Taylor et al. (2009).

However, it is important to reiterate that every phylogenetic tree must be considered an evolutionary hypothesis and that the outcome of every phylogenetic analysis depends on the taxa that are used and on how characters are selected and coded that, in turn, depends on a priori hypotheses about homology. In the parlance of mathematics, each phylogenetic tree must be considered an opaque modelda model that reveals the logical consequences of the assumptions used to construct it. Nonetheless, each putatively homologous character can be evaluated in the context of the overall phylogeny to determine if the apparent a priori determination of homology (determined first by criteria in the sense of Owen) also conforms to the phylogenetic definition, that is, characters derived from a last common ancestor. For these reasons, we present our analyses not as affirmations about the phylogenetic relationships among the taxa included in our analyses but rather as an illustration of the challenging limitations on identifying valid phylogenetic relationships among early land plants. Specifically, our analyses serve to show that attempts to resolve early land plant phylogenetic relationships are inevitably problematic for the following five reasons: (1) only a small fraction of taxa is preserved in the fossil record, (2) the numbers of diagnostic characters (and character states) preserved in the fossil record, even for the best described key taxa are insufficient, (3) all of the organographic, anatomical, and reproductive characteristics that are conventionally used to distinguish among extant plant lineages had not yet evolved, (4) mosaic evolution is

particularly evident during the Siluro-Devonian time period, as is (5) convergent evolution, and (6) phylogenetic analyses of fossil organisms require assumptions about homology, but these are testable in overall phylogenetic context as noted earlier. We discuss each of these limitations in the following sections but emphasize immediately that our concerns about these limitations should not be interpreted as a resignation or a call to abandon future attempts to resolve the phylogenetic enigmas of the early Paleozoicdquite the contrary. Much can be learned from opaque mathematic models because their predictions often challenge the assumptions underlying conveyed wisdom, particularly those about organic homologies.

4.1 An Incomplete Fossil Record It is clear that the fossil record is incomplete in its taxonomic representation and that what is preserved is biased taphonomically and ecologically. It is estimated that >90% of all organisms that ever existed in the past are absent from the fossil record. Thus, our view of past life is extraordinarily narrow in much the same way that extant organisms represent the tips of a much more massive tree of life. One consequence of the incomplete representation of past life is the general absence of complete transformational series among taxa in the same lineage, which clouds our ability to draw reasonable inferences about homologies. Taphonomic and ecological biases contribute in no small ways to furthering this limitation. The former puts constraints on

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the preservation of taxonomically critical diagnostic features, whereas the latter limits the sampling of different kinds of communities. The Rhynie Chert is a classic example. Although the states of preservation in this Lagerstätten permit the identification of extremely fine cellular details, the taxonomic and ecological inferences that can be drawn from this locality are likely not representative of the Devonian flora at this time because there can be little doubt that the vascular plants preserved in the Rhynie Chert were highly specialized. Yet another taphonomic limitation is the fragmentary nature of plant preservation. With very few exceptions, fossil plants are typically found as fragments of the whole body plan. Reproductive and underground parts may be lost during transport to depositional environments, or they may be so damaged as to make their organographic identities doubtful or impossible to surmise.

4.2 An Insufficient Number of Characters and Character States It is a truism to say that the ability to resolve phylogenetic relationships among any group of organisms is proportional to the signal:noise ratio, which increases as the number of characters distinguishing among taxa increase in relationship to the number of taxa being studied. Attempts to resolve the phylogenetic relationships among early vascular land plants are not immune to this limitation. Unfortunately, the signal:noise ratio for early Paleozoic land plants is extremely low for a number of reasons. For example, (1) there are comparatively few diagnostic features with which to evaluate the phylogenetic relationship among early vascular plants because organographic and anatomical distinctions among body parts have yet to evolve, (2) the fragmentary nature of preservation and the effects of diagenetic processes have artificially increased the number of “taxa” that have been described, and they have (3) eliminated key diagnostic features in some critical taxa. Other factors contributing to the low signal:noise ratio are discussed next.

4.3 Rapid Radiations and Mosaic Evolution The Siluro-Devonian time period experienced the most rapid evolutionary radiations in the history of the land plants. At the closure of a period spanning w17% of the entire history of the embryophytes, every major morphological, anatomical, and reproductive innovation made its appearance or prefigured subsequent important phenotypic characteristics (Fig. 5.5, Plates IeIV). One of the consequences of this rapid (presumably adaptive) radiation was the appearance of differential character evolution as, for example, the elaboration of anatomical features during periods of conservative morphological diversity. For

example, the earliest trimerophytes were characterized by pseudomonopodial vertical axes bearing more or less helically arranged sterile and reproductive dichotomously branching lateral axes, an architecture that was shared by Middle Devonian lignophytes that were far more anatomically complex. Likewise, it is clear that in some cases reproductive innovation has exceeded vegetative or anatomical innovation, whereas in other cases the reverse is true. For example, consider the diversity of sporangial size, shape, and geometry reported for the iconic oldest known vascular plant, Cooksonia, or the morphological and anatomical complexity of Archaeopteris in stark contrast to its comparatively ancient fernlike reproductive biology. These and other examples of disparity among morphological, anatomical, and reproductive rates of evolution serve to confound attempts to define clear-cut phenotypic boundaries separating early divergent tracheophyte lineages.

4.4 The Problem of Homology Perhaps the most serious challenge to any attempt to establish phylogenetic relationships among early Paleozoic plant fossils is the inferences regarding homology, which are exceedingly difficult because the oldest of plant fossils are incomplete and poorly preserved and manifest few clearly defined phenotypic traits (e.g., Tomescu, 2009). Hence, the principal difficulty in assessing relationships among early land plants lies in identifying sufficient numbers of and informative homologous characters. In addition, as noted, there is the likelihood of mosaic evolution and homoplasy; the tree topologies obtained with our matrices indicate that heterospory, secondary growth, and leaves (here defined as appendicular surficial structures produced by a shoot apical meristem) evolved at least twice, once within the lycophyte clade and a second time in the euphyllophytes clade. Aside from the disparity in the numbers of characters between base sequence data from modern taxa and the relatively few structural characters available from fossils, inferences about the phylogeny of early Paleozoic tracheophytes based on comparative studies of extant taxa are equally suspect because homology at the molecular level (sometimes difficult to determine) does not provide irrefutable evidence for homology at the morphological or anatomical level of organization. For example, the fact that sporangia and leaves may express the same components in similar gene expression patterns does not provide sufficient evidence that sporangia and leaves are homologous because both of these organs involve hypodermal cellular activity and because gene regulatory networks can be coopted to perform dissimilar developmental consequences. This caveat is illustrated by studies of the MADS box gene called LEAFY (LFY), which is found in mosses, ferns, gymnosperms, and angiosperms. Among

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PLATE I Illustrations of key fossil taxa from the Cornell research and teaching collections. (1) Polished surface of petrified Rhynie Chert showing Aglaophyton axes, Cornell University Paleobotany Teaching Collection (CUPTC). Scale bar ¼ 0.5 cm. (2) Thin section of Rhynia gwynne-vaughanii, scale bar ¼ 500 mm, Cornell University Paleobotany Collection (CUPC). (3) Compression fossil of Cooksonia (CUPC 40999), scale bar ¼ 5 mm. (4) Thin section of Horneophyton (CUPTC), scale bar ¼ 500 mm. (5) Zosterophyllum sp. (CUPC 1167, collected by Harlan P. Banks in 1935), scale bar ¼ 5 mm. (6) Stem section of Asteroxylon mackeii, Rhynie Chert (CUPTC), scale bar ¼ 500 mm. (7) Compression of Baragwanathia longifolia (CUPC 2105, collected by H.P. Banks in Wilson Creek Australia, 1973), scale bar ¼ 1 cm. (8) Drepanophycus colophyllus transfer preparation of type specimen (Grierson and Banks, 1963), scale bar ¼ 1 cm. (9) Clwydia compression (Archaeosigillaria vanuxemi, [CUPTC] collected by Petry and Banks, Gilboa NY), scale bar ¼ 1 cm. (10) Colpodexylon deatsii compression (CUPC 1163, Pond Eddy NY collected by Harlan P. Banks). Scale bar ¼ 1 cm.

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PLATE II Illustrations of key fossil taxa from the Cornell research and teaching collections. (1) Leclercqia complexa compression (CUPTC), scale bar ¼ 1 cm. (2) Lepidodendron cast with carbonized leaf bases (CUPTC, gift of T. Delevoryas, Yale), scale bar ¼ 2 cm. (3) Stigmaria rootstock and rootlets compression (CUPTC), scale bar ¼ 3 cm. (4) Psilophyton dawsoni peel of type specimen. Scale bar ¼ 500 mm. (5) Psilophyton crenulatum isolated from matrix and embedded in plastic (CUPTC, gift of J. Doran), scale bar ¼ 1 cm. (6) Ibyka amphikoma (paratype, collected by H.P. Banks, J. Skog, R. Baschnagel, and F. Essig, 1969), scale bar ¼ 3 cm.

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PLATE III Illustrations of key fossil taxa from the Cornell research and teaching collections. (1) Tetraxylopteris schmidtii, Hawks Nest NY (CUPC 529(26) paratype, collected by H. P. Banks), scale bar ¼ 1 cm. (2) Transfer of Tetraxylopteris fertile branches (Bonamo and Banks, 1967), scale bar ¼ 1 cm. (3) Archaeopteris macilenta, sterile branch (CUPTC), scale bar ¼ 1 cm. (4) Rhacophyton ceratangium fertile branches (on loan, University of Connecticut Paleobotany Collection), scale bar ¼ 2 cm. (5) Rhacophyton ceratangium closer view of sterile branchlets with terminal appendages (on loan, University of Connecticut Paleobotany Collection), scale bar ¼ 1 cm. (6) Fertile branch of Calamophyton (CUPC 1617, collected by Harlan P. Banks and H.N. Andrews, Goé Belgium June 1959), scale bar ¼ 1 cm.

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PLATE IV Illustrations of key fossil taxa from the Cornell research and teaching collections. (1) Sterile branch of Hyenia (Calamophyton) (CUPC 1617, collected by Harlan P. Banks and H.N. Andrews, Goé Belgium June 1959), scale bar ¼ 1 cm. (2) Section of Stauropteris showing the stelar configuration and branch traces (CUPTC), scale bar ¼ 500 mm. (3) Asterophyllites branch (CUPTC), scale bar ¼ 1 cm. (4) Calamites cone (Palaeostachya, CUPTC). Scale bar ¼ 1 cm. (5) A frond of Sphenopteris (Lyginopteris) (CUPTC), scale bar ¼ 1 cm.

Early Tracheophyte Phylogeny: A Preliminary Assessment of Homologies Chapter j 5

flowering plants, the single LFY gene product binds to sequences in the enhancers of several homeotic floral genes (as, e.g., APETALA1). Among nonflowering plants, several LFY gene products control more general and manifold aspects of the life cycle. The LFY DNA binding domain is strongly conserved across all taxa. But the LFY protein as a whole has diverged in activity across taxa from mosses to angiosperms, which is indicated by the ability of LFY cDNAs (isolated from mosses, ferns, and various gymnosperms linked to the Arabidopsis LFY promoter) to progressively recover the lfy mutant of Arabidopsis. However, an important pattern of recovery emerges when the phyletic relationship among the different land plant lineages is considered. The ability to recover the mutant mirrors the phyletic distances of the mosses, ferns, and gymnosperms from the angiospermseethe success of recovery decreases the more distant the lineage used to construct the LFY cDNA is from Arabidopsis. Two possible explanations for this phenomenon exist. LFY either controls similar gene networks that have coevolved with target genes that have themselves become modified during plant diversification, or the function of LFY in early divergent plant lineages (mosses and ferns) and late divergent lineages (angiosperm) has changed as a result of the recruitment or intercalation of new target genes. In either case, it is clear that understanding phenotypic evolution requires thinking both within and outside the paradigm of transcription factors (Niklas et al., 2015; Yruela et al., 2017). As noted, the difficulties underlying the establishment of organic homologies are not confined to the present study. The evolution of organic form involves the nonrandom, lineage-specific ordering and reordering of structural parts. Any legitimate evolutionary-developmental theory must account for the generation of new structural parts, the fixation and combination of parts, and their subsequent modification (including their possible loss and reappearance). The neo-Darwinian theory of evolution accounts for some but not all of the necessary elements of a legitimate evo-devo theory. Specifically, it accounts for the modification of preexisting parts (by means of natural selection). However, neo-Darwinian theory fails to explain the appearance of new (truly novel) parts or the reappearance of parts previously lost (the Lazarus effect). Natural selection has no generative capabilities. It eliminates or maintains what exists. The relevance of the concept and application of homology becomes apparent when we consider that homology is the manifestation of structural organization, the processes from which it emerges, and the processes that maintain it. Unfortunately, homology has been defined in a variety of ways, some ranging from idealistic (lacking a formal definition) to methodological (as in cladistic analyses). Some of these definitions emerge from the idealistic morphology of the 18th century (as, e.g., in Goethe’s

87

Versuch die Metamorphose der Pflanzen zu erklaren). What is arguably (and historically) the most concise and precise definition for initial assertion of homology (as well as the first) was offered in 1843 by Sir Richard Owen (1804e92): “The same organ in different animals under every variety of form and function.” A generalized restatement of Owen’s concept is “[t]he same trait in different but related lineages under every variety of form and function.” Note that this definition does not present criteria whereby homologous traits can be identified. More important perhaps is that, in the parlance of cladistics, homologues are often synapomorphies (although synplesiomorphies may also be homologues), although the reverse is not true. A character state shared by two or more species sharing a most recent common ancestor need not be a homologue. For example, the absence of an organ found in a common ancestor may appear to be a synapomorphy, but it cannot be a homologue because the part does not exist and one cannot rule out the possibility that the loss represents the results of two separate events. One of the difficulties of this (or any) approach to homology is that it has an element of circular reasoning in the sense that it requires us to identify a character and to infer that two or more different kinds of organisms possess it. The leaves of lycopods and the leaves of ferns were called “leaves” by the earliest plant morphologists. However, subsequent studies show that these structures evolved independently, just as roots have in different plant lineages, and it would be inaccurate to identify these as homologues for a single character. A more challenging example is multicellularity that has evolved independently in different lineages by means of similar developmental modules, which are nevertheless clearly not homologous. The homology concept of Owen has been extended to other levels of biological organization, often with considerable success. However, problems arise when homologies are drawn across different levels of organization. For example, a morphologically homologous character, such as a leaf or root, across different taxa does not provide prima facie evidence that the trait is generated by the same developmental or genomic processes, nor do developmental or genomic homologies guarantee morphological homology. Although it is certainly true that the assessment of homology benefits inordinately the more levels of biological organization that are compared, the strongest evidence for homology comes from comparisons between comparable levels, which can be extended, albeit carefully, to cover all of the relevant levels of comparison. And, with respect to problems briefly discussed here, modern phylogenetic approaches to homology determination address this issue. Homologous characters, identified by Owen (1843) and enhanced by considerations of Lankester (1870) and Hennig (1966) who introduced the concept of evolution to Owen’s definition based on

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SECTION j I Early Land Plants: Innovations and Adaptations

position, common function, and ontogeny, may be defined, then confirmed, as those demonstrating shared similarity due to common ancestry in phylogenetic context. The illuminating and character testing power of such context has been the subject of an extensive discourse (e.g., see Nixon and Carpenter, 2011 for a discussion of homology and the history of the concept), and is generally regarded as appropriate in evaluation of assertions of homology for particular characters.

5. CONCLUSIONS We return to our previous assertion that every phylogenetic analysis is a hypothesis generated by an opaque model. Nevertheless, it should be clear that all of the challenges to establishing unambiguous phylogenetic relationships among early tracheophytes should not deter attempts to explore the relationships identified by phylogenetic analyses. Although this statement may seem counterintuitive, particularly in light of our hesitancy to make any claims about the virtues of the analyses presented here, it must be clear that different phylogenetic relationships emerging from different character state assignments (i.e., different hypotheses about homology and therefore character selection) can inform and refine our perception about early land plant evolution and generate new search images for seeking and identifying transformational series in the fossil record. In turn, new fossil discoveries can inform hypotheses about homology based on prior phylogenetic analyses. In this way, hypotheses about homology are elevated from circular reasoning.

APPENDICES Appendix 1: Character List for Matrix 1 0. 1. 2. 3.

4.

5. 6.

7.

Peripheral loops: absent ¼ 0; present ¼ 1. Secondary growth: absent ¼ 0; present ¼ 1. Vascular cambium: unifacial ¼ 0; bifacial ¼ 1. Xylem conductive elements: unornamented ¼ 0; S-type ¼ 1; G-type ¼ 2; P-type ¼ 3; Recent type ¼ 4 [additive]. Metaxylem tracheid secondary wall thickenings: annular spiral ¼ 0; scalariform ¼ 1; scalariform pitted ¼ 2; circular bordered pitted ¼ 3 [nonadditive]. Pith: absent ¼ 0; present ¼ 1; unnamed state ¼ 2 [nonadditive]. Microphyllous leaves: simple ¼ 0; forked ¼ 1; trifurcate ¼ 2; with more than three lobes ¼ 3 [nonadditive]. Growth Habit: procumbent dichotomous with upright branches (rhizomatous) ¼ 0; upright/pseudo/monopodial ¼ 1; arborescent ¼ 2 [nonadditive].

8. Axes: naked ¼ 0; bearing appendages ¼ 1. 9. Ultimate branchlets: straight ¼ 0; recurved ¼ 1. 10. Ultimate branchlet geometry: three dimensional ¼ 0; planar ¼ 1. 11. Planar ultimate branchlets: unwebbed ¼ 0; incompletely webbed ¼ 1; webbed ¼ 2 [nonadditive]. 12. Sporangial position: terminal ¼ 0; lateral ¼ 1; axillary ¼ 2; adaxial-sporophyll ¼ 3 [nonadditive]. 13. Lateral sporangial aggregation: scattered ¼ 0; aggregated ¼ 1; in strobili ¼ 2 [nonadditive]. 14. Spores: homosporous ¼ 0; heterosporous ¼ 1. 15. Megaspore number: numerous ¼ 0; one ¼ 1. 16. Ligules: absent ¼ 0; present ¼ 1. 17. Circinate vernation: absent ¼ 0; present ¼ 1. 18. Unequal branching: absent ¼ 0; pseudomonopodial ¼ 1; monopodial ¼ 2 [nonadditive]. 19. Sterile lateral branches: absent ¼ 0; present ¼ 1. 20. Determinate lateral branches: absent ¼ 0; present ¼ 1. 21. Axis cross-sectional shape: terete ¼ 0; flattened ¼ 1. 22. Axillary branching: absent ¼ 0; present ¼ 1; tubercle or other axillary associated but diminutive structure ¼ 2 [nonadditive]. 23. Sporangial configuration: spheroid ¼ 0; fusiform absc vertical ¼ 1; reniform absc lateral ¼ 2; modified reniform ¼ 3 [additive]. 24. Sporangial spines/papillae: absent ¼ 0. 25. Noneterminal-sporangial arrangement: not in rows ¼ 0; in rows ¼ 1. 26. Sporangia: not aggregated ¼ 0; aggregated ¼ 1; loosely aggregated ¼ 2; cones ¼ 3 [nonadditive]. 27. Aggregated lateral sporangia: distichously arranged ¼ 0; spirally arranged ¼ 1; in whorls ¼ 2 [nonadditive]. 28. Strobili: absent ¼ 0; present ¼ 1. 29. Lateral sporangia stalked: no ¼ 0; yes ¼ 1. 30. Terminal sporangium present in aggregated (lateral) sporangia: no ¼ 0. 31. H or K branching: absent ¼ 0. 32. Secondary branches: spiral ¼ 0; whorled ¼ 1. 33. Bulbous unlobed base: absent ¼ 0; present ¼ 1. 34. Abscising lateral branches: absent ¼ 0; present ¼ 1. 35. Tubercles at branching points: absent ¼ 0; present ¼ 1. 36. Leaves: microphylls ¼ 0; megaphylls ¼ 1. 37. Spore micromorphology: smooth ¼ 0; echinate ¼ 1; coni ¼ 2; elaters ¼ 3; grana ¼ 4 [nonadditive]. 38. Gametophyte: bisexual ¼ 0; unisexual ¼ 1. 39. Sporangium symmetry: radial ¼ 0; bilateral ¼ 1. 40. Branching orders: no digitate orders ¼ 0; some digitate orders ¼ 1. 41. Rhizoids (only) or roots: rhizoids ¼ 0; roots ¼ 1. 42. Spore walls: uniformly appressed ¼ 0; separated ¼ 1; saccate ¼ 2 [nonadditive]. 43. Secondary growth in arborescent taxa: absent ¼ 0; present ¼ 1.

Early Tracheophyte Phylogeny: A Preliminary Assessment of Homologies Chapter j 5

44. Branching planarity: dichotomous-all threedimensional ¼ 0; pseudomonopodial all threedimensional ¼ 1; pseudomonopodial 2/3 planar ¼ 2; monopodial all three-dimensional ¼ 3; monopodial 2/3 planar ¼ 4; monopodial 3 and above planar ¼ 5 [nonadditive]. 45. Sterome: absent ¼ 0; continuous ¼ 1; discontinuous ¼ 2 [nonadditive]. 46. Primary xylem development: centrach-mesarch ¼ 0; exarch mesarch ¼ 1; endarch ¼ 2 [nonadditive]. 47. Exarch-mesarch primary xylem cross section: elliptical ¼ 0; stellate ¼ 1; divided ¼ 2; ridged ¼ 3 [no-nadditive]. 48. Centrarch mesarch primary xylem cross section: circular ¼ 0; stellate ¼ 1; clepsydroid ¼ 2; stellate/ clepsydroid ¼ 3; separate strands ¼ 4 [nonadditive]. 49. Protoxylem shape in cross section: circular ¼ 0; tangential arc ¼ 1; separate but embedded in common procambium ¼ 2; clepsydroid ¼ 3; three armed ¼ 4; four armed ¼ 5; separate concentric bundles ¼ 6 [nonadditive]. 50. Primary xylem shape in cross section: circular ¼ 0; elliptical ¼ 1; oblong ¼ 2; stellate ¼ 3; concentric strands ¼ 4 [additive]. 51. Direction of differentiation from protoxylem: radial ¼ 0; principally bidirectional ¼ 1; centripetal ¼ 2; centrifugal ¼ 3 [nonadditive]. 52. Symmetry of the protoxylem point arrangement: one point only ¼ 0; radial/more or less concentric ¼ 1; bilateral ¼ 2; indefinite ¼ 3 [nonadditive].

Appendix 2: Character List for Matrix 2 0. 1. 2. 3.

4.

5. 6.

7.

8. 9.

Peripheral loops: absent ¼ 0; present ¼ 1. Secondary growth: absent ¼ 0; present ¼ 1. Vascular cambium: unifacial ¼ 0; bifacial ¼ 1. Xylem conductive elements: unornamented ¼ 0; S-type ¼ 1; G-type ¼ 2; P-type ¼ 3; recent type ¼ 4 [additive]. Metaxylem tracheid secondary wall thickenings: annular spiral ¼ 0; scalariform ¼ 1; scalariform pitted ¼ 2; circular bordered pitted ¼ 3 [additive]. Pith: absent ¼ 0; present ¼ 1; unnamed state ¼ 2 [additive]. Microphyllous leaves: simple ¼ 0; forked ¼ 1; trifurcate ¼ 2; with more than three lobes ¼ 3 [nonadditive]. Growth habit: procumbent dichotomous with upright branches (rhizomatous) ¼ 0; upright/pseudo/monopodial ¼ 1; arborescent ¼ 2 [additive]. Axes: naked ¼ 0; bearing appendages ¼ 1; bearing trichomes ¼ 2 [additive]. Ultimate branchlets: straight ¼ 0; recurved ¼ 1.

89

10. Ultimate branchlet geometry: three dimensional ¼ 0; planar ¼ 1. 11. Planar ultimate branchlets: unwebbed ¼ 0; incompletely webbed ¼ 1; webbed ¼ 2 [additive]. 12. Sporangial position: terminal ¼ 0; lateral ¼ 1; axillary ¼ 2; adaxial-sporophyll ¼ 3 [additive]. 13. Lateral sporangial aggregation: scattered ¼ 0; aggregated ¼ 1; in strobili ¼ 2 [additive]. 14. Spores: homosporous ¼ 0; heterosporous ¼ 1. 15. Megaspore number: numerous ¼ 0; one ¼ 1. 16. Ligules: absent ¼ 0; present ¼ 1. 17. Development by circinate vernation: absent ¼ 0; present ¼ 1. 18. Unequal branching: absent ¼ 0; pseudomonopodial ¼ 1; monopodial ¼ 2 [additive]. 19. Sterile lateral branches: absent ¼ 0; present ¼ 1. 20. Determinate lateral branches: absent ¼ 0; present ¼ 1. 21. Axis cross-sectional shape: terete ¼ 0; flattened ¼ 1. 22. Axillary branching: absent ¼ 0; present ¼ 1; tubercle or other axillary associated but diminutive structure ¼ 2 [nonadditive]. 23. Sporangial spines/papillae: absent ¼ 0. 24. Noneterminal-sporangial arrangement: not in rows ¼ 0; in rows ¼ 1. 25. Sporangia: not aggregated ¼ 0; aggregated ¼ 1; loosely aggregated ¼ 2; cones ¼ 3 [additive]. 26. Aggregated (lateral) sporangia?: distichously arranged ¼ 0; spirally arranged ¼ 1; in whorls ¼ 2; unnamed state ¼ 3 [nonadditive]. 27. Strobili: absent ¼ 0; present ¼ 1. 28. Lateral sporangia stalked: no ¼ 0; yes ¼ 1. 29. Terminal sporangium present in aggregated (lateral) sporangia: no ¼ 0. 30. H or K branching: absent ¼ 0. 31. Secondary branches: spiral ¼ 0; whorled ¼ 1; distichous ¼ 2; quadriseriate ¼ 3 [nonadditive]. 32. Bulbous unlobed base: absent ¼ 0; present ¼ 1. 33. Abscising lateral branches: absent ¼ 0; present ¼ 1. 34. Tubercles at branching points: absent ¼ 0; present ¼ 1. 35. Spore micromorphology: smooth ¼ 0; echinate ¼ 1; coni ¼ 2; elaters ¼ 3; grana ¼ 4 [nonadditive]. 36. Gametophyte: bisexual ¼ 0; unisexual ¼ 1. 37. Sporangium symmetry: radial ¼ 0; bilateral ¼ 1. 38. Branching orders: no digitate orders ¼ 0; some digitate orders ¼ 1. 39. Rhizoids (only) or roots: rhizoids ¼ 0; roots ¼ 1. 40. Spore walls: uniformly appressed ¼ 0; separated ¼ 1; saccate ¼ 2 [additive]. 41. Secondary growth in arborescent taxa: absent ¼ 0; present ¼ 1. 42. Branching planarity: unnamed state ¼ 0; unnamed state ¼ 1; unnamed state ¼ 2; unnamed state ¼ 3; unnamed state ¼ 4; unnamed state ¼ 5 [additive].

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SECTION j I Early Land Plants: Innovations and Adaptations

43. Sterome: absent ¼ 0; continuous ¼ 1; discontinuous ¼ 2 [nonadditive]. 44. Primary xylem development: centrarch-mesarch ¼ 0; exarch-mesarch ¼ 1; endarch ¼ 2 [nonadditive]. 45. Exarch-mesarch primary xylem cross section: elliptical ¼ 0; stellate ¼ 1; divided ¼ 2; ridged ¼ 3 [nonadditive]. 46. Centrarch-mesarch primary xylem cross section: circular ¼ 0; stellate ¼ 1; clepsydroid ¼ 2; stellate/ clepsydroid ¼ 3; separate strands ¼ 4 [nonadditive]. 47. Protoxylem shape in cross section: circular ¼ 0; tangential arc ¼ 1; separate embedded in common procambium ¼ 2; clepsydroid ¼ 3; three armed ¼ 4; four armed ¼ 5; unnamed state ¼ 6 [nonadditive]. 48. Primary xylem shape in cross section: circular ¼ 0; elliptical ¼ 1; oblong ¼ 2; stellate ¼ 3; concentric strands ¼ 4 [nonadditive]. 49. Symmetry of protoxylem point arrangement: one point only ¼ 0; radial/more or less concentric ¼ 1; bilateral ¼ 2; indefinite ¼ 3 [nonadditive]. 50. Stem with ridges and furrows: absent ¼ 0; present ¼ 1. 51. Branches subtended by two aphledae-like structures: absent ¼ 0; present ¼ 1. 52. One functional megaspore or seeds: absent ¼ 0; present ¼ 1. 53. Fronds: absent ¼ 0; present ¼ 1. 54. Sporangial trusses: not subtended by whorled sterile bracts ¼ 0; subtended by whorled sterile bracts ¼ 1.

Appendix 3: Character List for Matrix 3 0. 1. 2. 3.

4.

5. 6.

7.

8. 9. 10.

Peripheral loops: absent ¼ 0; present ¼ 1. Secondary growth: absent ¼ 0; present ¼ 1. Vascular cambium: unifacial ¼ 0; bifacial ¼ 1. Xylem conductive elements: unornamented ¼ 0; S-type ¼ 1; G-type ¼ 2; P-type ¼ 3; recent type ¼ 4 [additive]. Metaxylem tracheid secondary wall thickenings: annular spiral ¼ 0; scalariform ¼ 1; scalariform pitted ¼ 2; circular bordered pitted ¼ 3 [additive]. Pith: absent ¼ 0; present ¼ 1. Microphyllous leaves: simple ¼ 0; forked ¼ 1; trifurcate ¼ 2; with more than three lobes ¼ 3 [nonadditive]. Growth habit: procumbent dichotomous with upright branches (rhizomatous) ¼ 0; upright/pseudo/monopodial ¼ 1; arborescent ¼ 2 [additive]. Axes: naked ¼ 0; bearing appendages ¼ 1; bearing trichomes ¼ 2 [additive]. Ultimate branchlets: straight ¼ 0; recurved ¼ 1. Ultimate branchlet geometry: three dimensional ¼ 0; planar ¼ 1.

11. Planar ultimate branchlets: unwebbed ¼ 0; incompletely webbed ¼ 1; webbed ¼ 2 [additive]. 12. Sporangial position: terminal ¼ 0; lateral ¼ 1; axillary ¼ 2; adaxial-sporophyll ¼ 3 [additive]. 13. Lateral sporangial aggregation: scattered ¼ 0; aggregated ¼ 1; in strobili ¼ 2 [additive]. 14. Spores: homosporous ¼ 0; heterosporous ¼ 1. 15. Megaspore number: numerous ¼ 0; one ¼ 1. 16. Ligules: absent ¼ 0; present ¼ 1. 17. Development by circinate vernation: absent ¼ 0; present ¼ 1. 18. Unequal branching: absent ¼ 0; pseudomonopodial ¼ 1; monopodial ¼ 2 [additive]. 19. Sterile lateral branches: absent ¼ 0; present ¼ 1. 20. Determinate lateral branches: absent ¼ 0; present ¼ 1. 21. Axis cross-sectional shape: terete ¼ 0; flattened ¼ 1. 22. Axillary branching: absent ¼ 0; present ¼ 1; tubercle or other axillary associated but diminutive structure ¼ 2 [nonadditive]. 23. Sporangial spines/papillae: absent ¼ 0. 24. Noneterminal-sporangial arrangement: not in rows ¼ 0; in rows ¼ 1. 25. Sporangia: not aggregated ¼ 0; aggregated ¼ 1; loosely aggregated ¼ 2; cones ¼ 3 [additive]. 26. Aggregated (lateral) sporangia?: distichously arranged ¼ 0; spirally arranged ¼ 1; in whorls ¼ 2; unnamed state ¼ 3 [nonadditive]. 27. Strobili: absent ¼ 0; present ¼ 1. 28. Lateral sporangia stalked: no ¼ 0; yes ¼ 1. 29. Terminal sporangium present in aggregated (lateral) sporangia: no ¼ 0. 30. H or K branching: absent ¼ 0. 31. Secondary branches: spiral ¼ 0; whorled ¼ 1; distichous ¼ 2; quadriseriate ¼ 3 [nonadditive]. 32. Bulbous unlobed base: absent ¼ 0; present ¼ 1. 33. Abscising lateral branches: absent ¼ 0; present ¼ 1. 34. Tubercles at branching points: absent ¼ 0; present ¼ 1. 35. Spore micromorphology: smooth ¼ 0; echinate ¼ 1; coni ¼ 2; elaters ¼ 3; grana ¼ 4 [nonadditive]. 36. Gametophyte: bisexual ¼ 0; unisexual ¼ 1. 37. Sporangium symmetry: radial ¼ 0; bilateral ¼ 1. 38. Branching orders: no digitate orders ¼ 0; some digitate orders ¼ 1. 39. Rhizoids (only) or roots: rhizoids ¼ 0; roots ¼ 1. 40. Spore walls: uniformly appressed ¼ 0; separated ¼ 1; saccate ¼ 2 [additive]. 41. Secondary growth in arborescent taxa: absent ¼ 0; present ¼ 1. 42. Branching Planarity: unnamed state ¼ 0; unnamed state ¼ 1; unnamed state ¼ 2; unnamed state ¼ 3; unnamed state ¼ 4; unnamed state ¼ 5 [additive]. 43. Sterome: absent ¼ 0; continuous ¼ 1; discontinuous ¼ 2 [nonadditive].

Early Tracheophyte Phylogeny: A Preliminary Assessment of Homologies Chapter j 5

44. Primary xylem development: centrarch-mesarch ¼ 0; exarch-mesarch ¼ 1; endarch ¼ 2 [nonadditive]. 45. Exarch-mesarch primary xylem cross section: elliptical ¼ 0; stellate ¼ 1; divided ¼ 2; ridged ¼ 3 [nonadditive]. 46. Centrarch-mesarch primary xylem cross section: circular ¼ 0; stellate ¼ 1; clepsydroid ¼ 2; stellate/ clepsydroid ¼ 3; separate strands ¼ 4 [nonadditive]. 47. Protoxylem shape in cross section: circular ¼ 0; tangential arc ¼ 1; separate embedded in common procambium ¼ 2; clepsydroid ¼ 3; three armed ¼ 4; four armed ¼ 5; unnamed state ¼ 6 [nonadditive]. 48. Primary xylem shape in cross section: circular ¼ 0; elliptical ¼ 1; oblong ¼ 2; stellate ¼ 3; concentric strands ¼ 4 [nonadditive]. 49. Symmetry of protoxylem point arrangement: one point only ¼ 0; radial/more or less concentric ¼ 1; bilateral ¼ 2; indefinite ¼ 3 [nonadditive]. 50. Stem with ridges and furrows: absent ¼ 0; present ¼ 1. 51. Branches subtended by two aphledae-like structures: absent ¼ 0; present ¼ 1. 52. One functional megaspore or seeds: absent ¼ 0; present ¼ 1. 53. Fronds: absent ¼ 0; present ¼ 1. 54. Sporangial trusses: not subtended by whorled sterile bracts ¼ 0; subtended by whorled sterile bracts ¼ 1.

REFERENCES Andrews, H.N., Gensel, P.G., Kasper, A.E., 1975. A new fossil of probable intermediate affinities (Trimerophyte-Progymnosperm). Canadian Journal of Botany 53, 1719e1728. Banks, H.P., 1968. The early history of land plants. In: Drake, E.T. (Ed.), Evolution and Environment. Yale University Press, New Haven. Banks, H.P., 1975. Reclassification of psilophyta. Taxon 24, 401e413. Bierhorst, D.W., 1971. Morphology of Vascular Plants. Macmillan, New York. Bold, H.G., 1967. Morphology of Plants. Harper and Row, New York. Bonamo, P.M., Banks, H.P., 1966. Calamophyton in the Middle Devonian of New York State. American Journal of Botany 53, 778e791. Bonamo, P.M., Banks, H.P., 1967. Tetraxylopteris schmidtii: its fertile parts and its relationships within the Aneurophytales. American Journal of Botany 54, 755e768. Bower, F.O., 1908. The Origin of a Land Flora. MacMillan, London. Bower, F.O., 1930. Size and Form in Plants, with Special Reference to the Primary Conducting Tracts. MacMillan, London. Bower, F.O., 1935. Primitive Land Plants, also Known as the Archgoniatae. MacMillan, London. Campbell, D.H., 1940. The Evolution of the Land Plants (Embryophyte). Stanford University Press, California. Corvez, A., Barriel, V., Dubuisson, J.-V., 2012. Diversity and Evolution of the megaphylly in Eupyllophytes: Phylogenetic hypotheses and the problem of foliar organ definition. Comptes Rendu Paleo 11, 403e418.

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DiMichele, W.A., Stein, W.E., Bateman, R.M., 2001. Ecological Sorting of Vascular Plant Classes during the Paleozoic Evolutionary Radiation. Columbia University Press New York. Gensel, P.G., 1976. Renalia hueberi, a new plant from the lower Devonian of Gaspé. Review of Palaeobotany and Palynology 22, 19e37. Goloboff, P.A., 1999. Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15, 415e428. Grierson, J.D., Banks, H.P., 1963. Lycopods of the Devonian of New York State. Palaeontographica Americana 4, 220e295. Hennig, W., 1966. Phylogenetic Systematics. University of Illinois Press, Urbana. Kenrick and Crane, 1997. The Origin and Early Diversification of Early Land Plants, a Cladistics Study. Smithsonian Institution Press, Washington D.C., 441 pp. Kidston, R., Lang, W.H., 1917. On Old Red Sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire. Part IV. Restorations of the vascular cryptogams, and discussion of their bearing on the general morphology of the Pteridophyta and the origin of the organisation of land plants. Transactions of the Royal Society Edinburgh 52, 831e854. Lankester, E.R., 1870. On the use of the term homology in modern zoology, and the distinction between homogenetic and homoplastic agreements. Annals and Magazine of Natural History Series 4 (6), 34e43. Niklas, K.J., 1997. The Evolutionary Biology of Plants. University of Chicago Press, Chicago. Niklas, K.J., Bondos, S.E., Dunker, A.K., Newman, S.A., February 2015. Rethinking gene regulatory network theory in light of alternative splicing, intrinsically disordered protein domains, and posttranslational modifications. Frontiers in Cell and Developmental Biology, Section Evolutionary Developmental Biology 26. Nixon, K.C., Davis, J.I., 1991. Polymorphic taxa, missing values and cladistic analysis. Cladistics 7, 233e241. Nixon, K.C., Carpenter, J.M., 2011. On homology. Cladistics 28, 160e169. Owen, R., 1843. Lectures on the Comparative Anatomy and Physiology of the Invertebrate Animals. Longman, Brown, Green and Longmans, London. Rothwell, G.W., Nixon, K.C., 2006. How does the inclusion of fossil data change our conclusions about the phylogenetic history of euphyllophytes? International Journal of Plant Sciences 167, 737e749. Schmidt, R., 1983. The terminology and classification of steles: Historical perspective and the outlines of a system. The Botanical Review 48, 817e931. Smith, G.M., 1955. Cryptogamic Botany. In: Bryophytes and Pteridophytes, vol. II. McGraw-Hill, New York. Stein, W.E., Berry, C.M., Hernick, L.V.A., Mannolini, F., 2012. Surprisingly complex community discovered in the mid-Devonian fossil forest at Gilboa. Nature 483.7387, 78e81. Stein, W.E., Hueber, F.M., 1989. The anatomy of Pseudosporochnus: P. hueberi from the Devonian of New York. Review of Palaeobotany and Palynology 60, 311e359. Stein, W.E., Wight, D.C., Beck, C.B., 1984. Possible alternatives for the origin of Sphenopsida. Systematic Botany 9, 102e118. Stewart, W.N., Rothwell, G.W., 1993. Paleobotany and the Evolution of Plants. Cambridge University Press. Taylor, T.N., Taylor, E.L., Krings, M., 2009. Paleobotany: the biology and evolution of fossil plants. Elsevier, Amsterdam.

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Tomescu, A.M.F., 2009. Megaphylls, microphylls and the evolution of leaf development. Trends in Plant Science 14, 5e12. Yruela, I., Oldfield, C.J., Niklas, J.K., Dunker, A.K., 2017. Evidence for a strong correlation between transcription factor protein disorder and organismic complexity. Genome Biology and Evolution 9 (S), 1248e1265. Zimmermann, W. Die Phylogenie der Pflanzen, second ed. (Fischer, Stuttgart, 1959). Zimmermann, W., 1930. Die Phylogenie der Pflanzen: ein Überblick über Tatsachen und Probleme. Verlag von Gustav Fischer, Jena.

FURTHER READING Banks, H.P., Bonamo, P.M., Grierson, J.D., 1972. Leclercqia complexa gen. et sp. nov., a new Lycopod from the late middle Devonian of

eastern New York. Review of Palaeobotany and Palynology 14, 19e40. Campbell, D.H., 1905. The Structure and Development of Mosses and Ferns. MacMillan, New York. Darwin, C., 1859. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, London. Donoghue, M.J., Sanderson, M.J., 1994. Complexity and homology in plants. In: Hall, B.K. (Ed.), Homology: The Hierarchical Basis of Comparative Biology. Academic Press, San Diego, pp. 393e421. Gensel, P.G., Berry, C.M., 2001. Early lycophyte evolution. American Fern Journal 91, 74e98. Stein, W.E., Mannolini, F., Hernick, L.V., Landing, E., Berry, C.M., 2007. Giant cladoxylopsid trees resolve the enigma of the Earth’s earliest forest stumps at Gilboa. Nature 446, 904e907.

Chapter 10

A Triassic Mystery Solved: Fertile Pekinopteris From the Triassic of North Carolina, United States Brian Axsmith1, Judith Skog2 and Christian Pott3, 4 1

University of South Alabama, Mobile, AL, United States; 2George Mason University, Fairfax, VA, United States; 3Swedish Museum of Natural

History, Stockholm, Sweden; 4LWL-Museum für Naturkunde, Münster, Germany

1. INTRODUCTION Pekinopteris auriculata was first described as a new genus and species of vascular plant fossil based on isolated pinnate fronds from the now classic Boren Clay Products pit locality in the Upper Triassic of the Deep River Basin in North Carolina, United States (Hope and Patterson, 1970). The Boren locality exposes sediments of the middle Pekin Formation, and has produced a diverse paleoflora (Gensel, 1986). Pekinopteris is one of the most abundant plant fossils from this site. Hope and Patterson (1970) noted that a plant possibly representing this species was confusingly described, and perhaps intermixed, with Cladophlebis reticulata specimens from the New Oxford Formation in the Upper Triassic Gettysburg Basin of York County, Pennsylvania by Fontaine and Wanner (1900); however, the precise identity and provenance of this material are unclear. The first author has collected extensively in the New Oxford Formation and has found no evidence of Pekinopteris. If it did occur outside of the Deep River Basin area, it was rare. One of the most intriguing aspects of Pekinopteris is that it has been known only from sterile specimens since its initial description. Therefore, the true affinities of this plant have been a persistent enigma to researchers concerned with the Triassic paleobotany of eastern North America (Hope and Patterson, 1970; Delevoryas and Hope, 1978; Gensel, 1986). Despite the lack of fertile material, Hope and Patterson (1970) suggested assignment of Pekinopteris to the ferns based on the apparently delicate texture of the

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00010-3 Copyright © 2018 Elsevier Inc. All rights reserved.

pinnae along with the presence of occasional circinnate fronds, but they noted that pteridosperm or cycadalean affinities could not be entirely ruled out. Based on the later discovery of abundant new specimens from the Boren locality, Delevoryas and Hope (1978) described its growth habit based on fronds attached to creeping rhizomes with adventitious roots, and provided additional details of the morphology. A reconstruction of the plant was presented to show the overall growth form. Although the combination of thin, pinnate fronds with circinnate vernation and a creeping rhizomatous growth pattern supported assignment to the ferns, the absence of fertile material was still problematical, especially considering that other ferns from the Boren locality are known from abundant fertile specimens despite being less common (Axsmith et al., 2001). We have recently reexamined the Boren locality material now housed at the University of Kansas, Lawrence, Kansas, and have discovered the fertile portion of the fronds of Pekinopteris auriculata. These fertile parts are rare and mostly detached but are found in association with the abundant sterile fronds. This may be the reason they went unrecognized as parts of Pekinopteris for so long. However, three specimens show unambiguous attachment to sterile frond material. These newly recognized specimens confirm assignment to the ferns and indicate a relationship to the Schizaeales based on the structure of the sporangia. This material is described herein, and the possible relationships are discussed in greater detail. An updated reconstruction is also presented.

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2. GEOLOGICAL SETTING

3.2 Preservation and Methods of Analysis

All the described material was recovered from the Boren Clay Products pit locality 2.5 km northwest of Gulf, central North Carolina, which occurs along the western margin of the Sanford sub-basin of the Deep River Basin of the Newark Supergroup (Hope and Patterson, 1970). This locality exposes part of the middle Pekin Formation, which is the lowest formation in the Deep River Basin, and is considered Late Carnian in age (about 226e228 Ma) based on correlation with paleomagnetically dated cores (Whiteside et al., 2011). The fossils occur mainly in a gray and dusky siltstone deposited near the paleoequator by meandering streams on an alluvial plain. The paleoclimate has been interpreted as warm and moist with seasonal rainfall (Gensel, 1986). Based on the articulation of many of the plant fossils, including delicate forms like the filmy fern Hopetedia (Axsmith et al., 2001), the depositional environment was probably relatively undisturbed. This locality has produced one of the most diverse and currently well-studied floras from the Triassic of eastern North America. It includes many well-articulated ferns, bennettitaleans, conifers, and cycads, and their study has had a major impact on our general understanding of Triassic plant diversity and evolution (Gensel, 1986; Axsmith et al., 1995; Axsmith et al., 2001; Pott and Axsmith, 2015).

Most of the fossils are preserved as impressions, with a few possessing limited compressed organic material that is highly coalified. Most of the salient features could be observed under light microscopy (Nikon SMZ 1500) with minimal preparation required. Although the preservation of the fronds is generally satisfactory in terms of articulation and overall morphology, the sporangia were difficult to study and photograph. This is due mainly to their highly compressed state and the relatively large annuli that obscure the proximal sporangial morphology. Nevertheless, there were regions on most of the fertile specimens with sufficient preservation to reveal the basic structure of the annuli. Also, a few sporangia have coalified residue on the annular cell walls, making them easier to examine and photograph. Side lighting and cross-polarized light were sometimes used to aid in imaging the sporangia and pinna venation. Attempts to make transfers of the sporangia were unsuccessful due to the paucity of organic residue. Attempts were made to treat the rare organic remains to recover spores and cuticles, but they were unsuccessful. These included several standard maceration procedures (e.g., Pott and McLoughlin, 2009), transfers, and epifluorescence microscopy. Photographs were taken with a Pentax K20 digital SLR with a ring flash, and a Nikon DS-Ri1 digital camera attached to the SMZ 1500 dissecting microscope. Images were processed in Photoshop CS5.

3. MATERIAL AND METHODS 3.1 Discovery and Nature of the Specimens This analysis is based entirely on fossils from the Boren locality collected mainly by R.C. Hope, O.F. Patterson, and T. Delevoryas during the 1960s and 1970s, when the pit was most active for mining purposes. Although fossils can still be obtained from the now defunct pit, the most productive unit was largely collected out in a salvage effort at that time (R.C. Hope, 1995, personal communication). More recently, this material was incorporated into the University of Kansas paleobotanical collections in Lawrence, Kansas, including all the figured specimens. This allowed examination of the entire collection under ideal conditions, which is significant as some of the specimens were still wrapped since being originally collected. In addition to facilitating the reexamination of the previously described sterile fronds and rhizomes (Delevoryas and Hope, 1978), this allowed recognition of the fertile pinnae that form the basis of this study. These rare fertile specimens include five isolated pinnae along with two slabs showing fertile pinnae in attachment to sterile frond sections, proving that they belong to Pekinopteris. The specimen numbers and repository details are presented here in the systematic paleontology section.

4. SYSTEMATIC PALEONTOLOGY Class Polypodiopsida PPG I 2016 Subclass Polypodiideae PPG I 2016 Order Schizaeales PPG I 2016 Family cf. Cynepteridaceae Ash 1970 Genus Pekinopteris R.C. Hope et O.F. Patt. 1970 Species Pekinopteris auriculata, R.C. Hope et O.F. Patt. emend. B. Axsmith, J.E. Skog et C. Pott e the genus is monotypic. Emended diagnosis: Plant has once pinnately compound fronds. Pinnae have opposite-to-subopposite arrangement on the rachis, attached with a narrow base, but attachment often is covered by an auricle, with attachment angle variable from perpendicular to about 45 degrees. Pinnae margins have ascending, acute teeth formed where lateral veins enter the margin. Pinnae venation includes a prominent midvein at the base, becoming less distinct distally; one lateral vein arises directly from the rachis just above the midvein, branches and enters the auricle; auricle is less obvious on narrower pinnae. Pinnae lateral vein systems consist of one order of anastomosing veins forming long and slender areoles. Rhizome creeping and branching at irregular intervals, with a diameter from 6 mm to 1 cm; leaf bases often persistent on rhizome; adventitious roots

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occur along the rhizome. Fertile segment of the frond consists of an extended apical pinna about 1 cm wide and exceeding 18 cm long with marginal teeth and a strong midvein. Sporangia are tightly packed and entirely cover the abaxial surface of the apical fertile pinna; individual sporangia with an apical, mostly uniserriate annular ring with small cells in center; annulus averaging about 2 mm in diameter with about 30 thick-walled cells. Spores unknown. Material studied: Most of the figured sterile material occurs on fronds from slab T5353 (Plate I, 1, 2, 6). Two slabs contain fertile specimens showing attachment to sterile frond sections. T5374 (Plate I, 3e5, 7) is a slab with two partially overlapping frond apices, and T5376 (Plate II, 1e6) has a single fertile apical pinna. Most of figured sporangia details come from T5374, as it has the best preservation (Plate II, 3e6). Isolate fertile pinna T5296 is illustrated to show the marginal teeth (Plate I, 8). Additional studied but unfigured isolated fertile pinnae include specimens T5369, T5372, T5365, and T5367b. The specimens listed here represent all the known fertile material in the collection. Repository: All the studied and figured specimens are housed in the Natural History Museum and Biodiversity Institute, Division of Paleobotany Collections (KUPB), University of Kansas (KU), Lawrence, Kansas, USA. Type locality and horizon: Former Boren Clay Products pit locality, 2.5 km northwest of Gulf, North Carolina, USA, middle Pekin Formation, Deep River Basin in the Newark Supergroup. Late Carnian (about 226e228 Ma). Description and interpretation: The Pekinopteris plant has a creeping rhizome about 1 cm in diameter that branches at irregular intervals. The leaf bases are often persistent on the rhizome, and adventitious roots occur scattered along the rhizome. The pinnately compound fronds often exceed 40 cm in length (Plate I, 1, 2). The pinnae have an opposite-to-subopposite arrangement on the rachis and average 5e6 cm in length (up to 12 cm) and 2e9 mm in width, and are attached with a narrow base. However, this attachment is often obscured by an auricle, giving the superficial appearance of broad attachment. Therefore, it is likely that the wide attachment described by Hope and Patterson (1970) was a preservational artifact caused by the auricle flattened against the rachis. Delevoryas and Hope (1978) noted that the attachment was more variable in their material, but we believe that a narrow attachment was typical. The pinnae margins show ascending, acute teeth formed where lateral veins enter the margin (Plate I, 6). The venation includes a prominent midvein at the base, which becomes less distinct distally, and many lateral veins. One lateral vein arises directly from the rachis just above the midvein and then divides and enters the auricle. The auricle is less obvious on narrower pinnae. The lateral vein systems of the pinnae consist of

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one order of anastomosing veins forming long and slender areoles (Plate I, 6, 7). The fertile segment of the frond consists of an extended apical pinna about 1 cm wide and exceeding 18 cm long with small marginal teeth (Plate I, 3, 4, 7; Plate II, 1, 2). The teeth are not always visible due to preservational factors. Typical sterile pinnae as found on sterile fronds are laterally attached just below the fertile pinna base (Plate I, 3, 4, 7; Plate II, 1, 2). No complete fertile fronds are known, but based on the apices of the three known attached specimens, the proximal parts of the fertile fronds were probably like the sterile specimens. The midvein of the apical fertile pinna is easily distinguished. The sporangia are often tightly packed and entirely cover the abaxial side of the apical fertile pinna (Plate I, 3e5; Plate II, 1e6). Lateral venation of the fertile pinnae is uncertain due to being obscured by the abundant sporangia (Plate II, 3, 4). The sporangia have an apical, cap-like, mostly uniserriate annulus with small cells in the center surrounded by approximately 30 thick-walled annulus cells (Plate II, 5, 6). The annular rings average about 2 mm in diameter. Details of the sporangia below the annulus could not be clearly documented, as the apical annulus is relatively large, and in the vertically compressed condition of these fossils obscures the regions below. Spores have not been obtained from any specimens. Remarks: Although this study is mainly focused on the discovery and description of the fertile material, characteristics of the sterile parts are repeated here for completeness and in part to rectify the lack of an emended diagnosis in the Delevoryas and Hope (1978) report. The basic description of the sterile material by Hope and Patterson (1970) along with the additional details from Delevoryas and Hope (1978) are confirmed by our study, with minor changes mostly involving pinnae attachment as described earlier. See Delevoryas and Hope (1978) for additional figures and details of the fronds (including croziers) and the rhizomes, which are not refigured here. A reconstruction based on our revised concept of P. auriculata, including the fertile pinnae and an enlargement of the sporangia, is presented in Fig. 10.1.

5. DISCUSSION 5.1 Structure and Life History The recognition of fertile pinnae with sporangia bearing an annulus as described here unambiguously verifies the position of Pekinopteris auriculata as a fern, as previously suspected based on sterile frond characteristics and a rhizomatous growth habit (Hope and Patterson, 1970; Delevoryas and Hope, 1978). Part of the reason the fertile apical pinnae went unrecognized may be because they detached easily from the rest of the frond despite the rather thick rachis; however, a more significant factor may simply

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PLATE I Sterile and fertile fronds of Pekinopteris auriculata, R.C. Hope et O.F. Patt. emend. B. Axsmith, J.E. Skog et C. Pott from the Upper Triassic Pekin Formation of North Carolina, USA. (1 and 2) Two adjacent, well-articulated sterile fronds from one slab showing the basic morphology. No. T5353; scale bar ¼ 1 cm. (3) Two overlapping fertile frond apices showing lateral pinnae (darts) attached to the rachis below the elongate, terminal fertile pinnae. No. T5374; scale bar ¼ 1 cm. (4) Detail of fertile frond apices from the region indicated by the darts in Plate I, 3 showing lateral sterile pinnae identical to those of sterile fronds. No. T5374; scale bar ¼ 1 cm. (5) Detail of the abaxial surfaces of the two overlapping fertile pinnae. The small crowded structures are the sporangia. See Plate II, 5 for a detail. No. T5374; scale bar ¼ 1 cm. (6) Detail of sterile pinna showing the venation and marginal teeth; No. T5374; scale bar ¼ 1 cm. (7) Detail of lateral sterile pinnae from Plate I, 4 showing the venation (compare with pinna from the sterile frond in Plate I, 6) and attachment to the rachis (r) just below the apical fertile pinna. No. T5374; scale bar ¼ 1 cm. (8) Detail of an isolated fertile pinna margin showing the margin teeth. No. T5296; scale bar ¼ 1 mm.

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PLATE II Fertile pinnae and sporangial details of Pekinopteris auriculata. (1) Fertile frond apex showing a terminal fertile pinna and poorly preserved but recognizable sterile lateral pinnae attached below (dart). Additional unmarked lateral pinnae occur all along the rachis below. No. T5376; scale bar ¼ 1 cm. (2) Detail of attachment point of fertile pinnae and bases of uppermost lateral sterile pinnae. Dart indicates false margin that obscures the teeth. Dark spots in this region are the crowded sporangia. No. T5376; scale bar ¼ 1 cm. (3 and 4) Detail of an isolated fertile pinna abaxial surface showing the crowded sporangia. No. T5372; scale bar ¼ 1 mm. (5) Abaxial surface of the rightmost attached fertile pinna from Plate 1, 3e5 showing the crowded sporangia with cap-like, apical annuli. No. T 5374. Scale bar ¼ 100 mm. (6) Detail of the sporangia (darts). The dark, organic residue on these specimens shows the annuli relatively clearly. The proximal parts of the sporangia are obscured by the compressed annuli. No. T5372; Scale bar ¼ 100 mm.

be their overall rarity. After extensive examination of the entire University of Kansas collection from the Boren pit locality, we have identified only six fertile pinnae. Considering how common the sterile remains of Pekinopteris are, such a paucity of fertile specimens is remarkable and somewhat perplexing. Perhaps reproduction via spores occurred over a relatively short season, resulting in fewer fossils yielding fertile pinnae; however, this is less likely as most other ferns from the Boren locality are frequently found with sporangia (Hope and Patterson, 1970; Axsmith et al., 2001). Instead, we suspect that spore production was relatively rare in this plant and that most of the reproduction was via rhizome fragmentation or some other mechanism of vegetative reproduction. In any case, it is clear that the ground cover vegetation of the floodplain that supported most of the Boren Pit flora was dominated by Pekinopteris, supplemented by smaller but still

substantial populations of other basal leptosporangiate ferns of the Dipteridaceae, Hymenophyllaceae, Matoniaceae, and Osmundaceae (Axsmith et al., 2001).

5.2 Comparisons and Potential Phylogenetic Implications The structure of the sporangia of Pekinopteris auriculatad including the presence of a large, uniseriate, cap-like annulusdstrongly indicates affinity with the order Schizaeales; however, its relationships to other extinct and extant families of this group are unclear and underscore the morphological diversity of these ferns. Reticulate venation (e.g., Lygodium venustrum) and scattered sporangia (e.g., Mohria species) do occur is some species of the extant families, but they are not found in combination (Tryon and Tryon, 1982). However, these are key features in all species of

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FIGURE 10.1 A suggested reconstruction of Pekinopteris auriculata based in part on that of Delevoryas and Hope (1978), with additions and modifications based on this study. Additions include the apical fertile pinnae; modifications include relatively longer lateral pinnae and depiction of the narrow lateral pinnae attachment. Roots were not included, as this reconstruction is intended to depict the plant in life as it would appear on the ground surface. The upper right inset depicts details of the sterile lateral pinnae showing the narrow but relatively short attachment. The circular insets depict details of the abaxial side of the fertile pinnae showing the crowded sporangia (right) and annuli (left). Illustrations by Pollyanna von Knorring, Stockholm, Sweden.

the Triassic genus Cynepteris of the monogeneric family Cynepteridaceae (Ash, 1970). Also, the more densely packed sporangia covering the abaxial pinnae surfaces of Cynepteris bolichii (Axsmith, 2009) are particularly reminiscent of the condition in Pekinopteris, and are a major reason we suggest placement of Pekinopteris in Cynepteridaceae. We still consider this determination tentative (thus the “cf.” designation in the systematics section), though, as fertile/sterile frond dimorphism or partial dimorphism is unknown in any other species of the family. It is also possible that the Triassic Cynepteridaceae, either including or excluding Pekinopteris, does not represent a distinct monophyletic group so much as a complex of forms diverging before the modern schizaealean families (i.e., it represents stem group members), as well as some forms that left no extant representatives. There

are some features of Pekinopteris suggesting that it could represent a link to the modern Schizaeales. For example, the occurrence of an apical fertile segment is a feature commonly seen in fronds of the extant genera Schizaea, Actinostachys, and Lygodium. The presence of reticulate venation in some extant species has already been mentioned. In the Cynepteridaceae, including Pekinopteris, the sporangia are scattered on the fertile pinnules in all cases. In the modern Schizaeales, sporangia occur in a variety of positions, from scattered to clustered around veins to the specialized sorophores of Lygodium. It is interesting to surmise that the fertile apical pinnule of Pekinopteris might represent a similar evolutionary event to the development of the sorophore in extant Lygodium or the apical fertile part of the Schizaea frond. Development of such a form in the Triassic argues for a reconsideration

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of the phylogeny of the Schizaeales, at least in terms of character evolution, but that is beyond the scope of this report. Previously, the fossil history of the Schizaeales has generally been accepted as dating from the Jurassic, with representatives including Klukia, Stachypteris, and Klukiopteris (Skog, 1993; Tidwell and Ash, 1994). These genera have been suggested as being allied more closely to extant Lygodium than to Anemia or Schizaea. Spores attributed to the Schizaeales also date from the Jurassic (Bolkhovitina, 1961; Van Konijnenburg-van Cittert, 2002), and none are recorded before this time. It is now clear that the Schizaeales had representatives in the Triassic in the form of the Cynepteridaceae (Axsmith, 2009) and specifically Pekinopteris but possessed some unique character combinations not seen in extant forms. They also apparently had not yet evolved the distinctive spore morphology seen in Jurassic to recent representatives. Molecular and morphological phylogenies based on modern ferns support the critical position of the Schizaeales and related forms for understanding the radiation of the leptosporangiate clades (PPG I, 2016), which underscores the need for more paleobotanical information from the late Paleozoic and early Mesozoic (Wikström et al., 2002). For example, Pryer et al. (2004) resolved the Osmundales as the earliest diverging leptosporangiates, next a clade of gleichenioid ferns diverged, followed by a schizaeoid group as sister to the core leptosporangiates. They state that “Although it remains to be seen if our grouping of gleichenioid and filmy ferns will stand the test of time, it is worth noting that what were once thought to be distantly related and successive grades of taxa at the base of the leptosporangiate ferns, may in fact be closely related members of a single clade that diversified in the Late Paleozoic/Early Mesozoic” (Pryer et al., 2004: p. 1591). More recent molecular analyses indicate that the Osmundales represent the first divergence, but following this there is less certainty for the relationships between Schizaeales, Gleicheniales, and the filmy ferns (Rothfels et al., 2015, Testo and Sundue, 2016). Testo and Sundue (2016) also estimate an earlier divergence time for the basal leptosporangiates with clear extant representatives, as their suggested date for the Osmundales divergence is 357 Ma.

6. CONCLUSION Regardless of the various proposed ages of origin for the major leptosporangiate fern groups as discussed here, it is significant that most analyses converge on the same basic relationships, with the most recent studies showing that the gleichenioid and schizaeoid ferns were among the first

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to diverge after the Osmundales (e.g., Pryer et al., 2004; Testo and Sundue, 2016; PPG I, 2016). This, along with what is known so far about the late Paleozoic and early Mesozoic fossil record, indicates that forms with unexpected character combinations were part of this evolutionary radiation (Axsmith, 2009). Our description of the Triassic Pekinopteris and the Cynepteridaceae as forms showing such unique character combinationsdbut with several frond and sporangial characteristics of the extant Schizaealesd supports the concept of a complex of early Mesozoic ferns diverging before the extant families, with some representing possible stem group members. Continued efforts at reconstructing fossil ferns as whole plants are needed before most of them can be confidently incorporated into phylogenic analyses along with modern ferns to rigorously test these ideas. As demonstrated here for Pekinopteris. auriculata, such reconstructions can entail a long, difficult, cumulative effort involving many researchers but will be crucial to the development of a more complete understanding of fern phylogeny and character evolution. Future avenues of research on Pekinoperis. auriculata that could provide needed information include better preserved sporangia showing their morphology below the annulus, spores, and cuticles. Documentation of the internal anatomy would be particularly informative but is unlikely to be forthcoming, at least from the Boren locality. In any event, the documentation of the fertile parts of Pekinopteris presented here not only verifies its status as a fern but also represents another major step in the development of a whole plant concept. This allows it to join the ranks of other well-reconstructed vascular plants that have made the Boren pit locality one of the most significant from the Triassic of North America.

ACKNOWLEDGMENTS This research would not have been possible without the successful efforts of Thomas N. Taylor at bringing the Patterson, Hope, and Delevoryas Boren pit fossils to the University of Kansas when he was curator of the fossil plants. We dedicate this work to his memory and acknowledge his influence as a friend, colleague, and in the case of the first author, a mentor. We also thank Edith L. Taylor, current curator of the collections, and collections manager Rudolph Serbet for facilitating continued access to these materials. Robert C. Hope and the late Theodore Delevoryas provide encouragement and valuable information on the Boren locality and its flora. We also recognize their pioneering work on Pekinopteris. We gratefully acknowledge the comments and information provided by Sidney Ash. This research was funded in part by a University of South Alabama Research Council grant to B.A. We are grateful to Pollyanna von Knorring, Swedish Museum of Natural History, Stockholm, Sweden, for the excellent reconstruction of Pekinopteris auriculata. C.P. acknowledges funding from the Swedish Research Council (Vetenskapsrådet), Stockholm, Sweden.

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REFERENCES Ash, S.R., 1970. Ferns from the Chinle formation (Upper Triassic) in the Fort Wingate area, New Mexico. U. S. Geological Survey Professional Paper 613D, 1e40. Axsmith, B.J., 2009. A new Cynepteris from the upper Triassic of Arizona: potential implications for the early diversification of Schizaealean ferns. International Journal of Plant Sciences 170, 657e665. Axsmith, B.J., Krings, M., Taylor, T.N., 2001. A filmy fern from the Upper Triassic of North Carolina (USA). American Journal of Botany 88, 1558e1567. Axsmith, B.J., Taylor, T.N., Delevoryas, T., Hope, R.C., 1995. A new species of Eoginkgoites from the Upper Triassic of North Carolina, USA. Review of Palaeobotany and Palynology 85, 189e198. Bolkhovitina, N.A., 1961. Fossil and recent spores of the family Schizaeaceae. Proceedings of the Geological Institute of the Russian Academy of Science 40, 1e176. Delevoryas, T., Hope, R.C., 1978. Habit of the Upper Triassic Pekinopteris auriculata. Canadian Journal of Botany 56, 3129e3135. Fontaine, W.M., Wanner, A., 1900. Triassic flora of York County, Pennsylvania. U.S. Geological Survey Annual Report 2 (pt. 2), 233e255. Gensel, P., 1986. Plant fossils of the Upper Triassic deep river basin. In: Gore, P.J.W. (Ed.), Depositional Framework of a Triassic Rift Basin: The Durham and Sanford Sub-Basins of the Deep River Basin, North Carolina, vol. 3. Society of Economic Paleontologists and Mineralogists Field Trip, pp. 82e86. Hope, R.C., Patterson, O.F., 1970. Pekinopteris auriculata: a new plant from the North Carolina Triassic. Journal of Paleontology 1137e1139. Pott, C., McLoughlin, S., 2009. Bennettitalean foliage in the Rhaetiane Bajocian (latest Triassicemiddle Jurassic) floras of Scania, Southern Sweden. Review of Palaeobotany and Palynology 158, 117e166. Pott, C., Axsmith, B.J., 2015. Williamsonia carolinensis sp. nov. and associated Eoginkgoites foliage from the Upper Triassic Pekin

Formation, North Carolina: implications for early evolution in the Williamsoniaceae (Bennettitales). International Journal of Plant Sciences 176, 174e185. PPG I, 2016. A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54, 563e603. Pryer, K.M., Schuettpelz, E., Wolf, P.G., Schneider, H., Smith, A.R., Cranfill, R., 2004. Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. American Journal of Botany 91, 1582e1598. Rothfels, C.J., Li, F.W., Sigel, E.M., Huiet, L., Larsson, A., Burge, D.O., Ruhsam, M., Deyholos, M., Soltis, D.E., Stewart, C.N., Shaw, S.W., 2015. The evolutionary history of ferns inferred from 25 low-copy nuclear genes. American Journal of Botany 102, 1089e1107. Skog, J.E., 1993. The relationship of the fossil fern Schizaeaopsis Berry to modern genera in the Schizaeaceae. American Fern Journal 83, 20e29. Testo, W., Sundue, M., 2016. A 4000-species dataset provides new insight into the evolution of ferns. Molecular Phylogenetics and Evolution 105, 200e211. Tidwell, W.D., Ash, S.R., 1994. A review of selected Triassic to early Cretaceous ferns. Journal of Plant Research 107, 417e442. Tryon, R.M., Tryon, A.F., 1982. Ferns and allied plants: with special reference to Tropical America. Springer Verlag, New York, NY, p. 857. Van Konijnenburg-van Cittern, J.H.A., 1991. Diversification of spores in fossil and extant Schizaeaceae. In: Blackmore, S., Barnes, S.H. (Eds.), Pollen and Spores. Systematics Association Special Volume 44. Clarendon Press, Oxford, pp. 103e118. Whiteside, J.H., Grogan, D.S., Olsen, P.E., Kent, D.V., 2011. Climatically driven biogeographic provinces of Late Triassic tropical Pangea. Proceedings of the National Academy of Sciences 108, 972e8977. Wikström, N., Kenrick, P., Vogel, J.C., 2002. Schizaeaceae: a phylogenetic approach. Review of Palaeobotany and Palynology 119, 35e50.

Chapter 9

Pachytestopsis tayloriorum gen. et sp. nov., an Anatomically Preserved Glossopterid Seed From the Lopingian of Queensland, Australia Stephen McLoughlin1, Benjamin Bomfleur2 and Andrew N. Drinnan3 1

Swedish Museum of Natural History, Stockholm, Sweden; 2Westfälische Wilhelms-Universität, Münster, Germany; 3The University of Melbourne,

Parkville, VIC, Australia

1. INTRODUCTION Permian plant-bearing deposits of Gondwana contain a broad array of isolated, dispersed seeds with uncertain affinities. Pant et al. (1985) recognized more than 30 genera and more than 90 species of dispersed seeds from the Permian of Gondwana, and several more have been described and illustrated subsequently (e.g., McLoughlin, 1992; Bordy and Prevec, 2008; de Souza and Iannuzzi, 2009; Tewari et al., 2012; Edirisooriya et al., 2018). In most cases, these seeds are preserved as adpressions and provide only very limited information on external morphology, detracting from their systematic appraisal and inhibiting confident association with co-occurring foliage or fructifications. Anatomically preserved Gondwanan Permian seeds are rare and confined to a few exceptional deposits of silicified peat in Antarctica and eastern Australia (Gould and Delevoryas, 1977; McLoughlin, 1990c, 1992; Pigg and Trivett, 1994; Holdgate et al., 2005; Ryberg, 2010; Ryberg and Taylor, 2013). Anatomically preserved seeds recovered from one Lopingian (upper Permian) silicified peat bed at the Homevale locality in the Bowen Basin, Australia, offer an opportunity to resolve the architecture of probable glossopterid disseminules and to infer associations with enigmatic glossopterid fructifications. Recent cladistic analyses of major seed-plant groups highlight seed architectural features (e.g., platyspermy versus radiospermy and number and structure of integumentary layers) as key characters for differentiating

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00009-7 Copyright © 2018 Elsevier Inc. All rights reserved.

gymnosperm clades (Crane, 1985; Nixon et al., 1994; Rothwell and Serbet, 1994; Doyle, 2006; Hilton and Bateman, 2006). Therefore, a thorough understanding of seed architecture may help clarify the relationships between glossopterids and other seed plants and provide insights into the anatomical diversity and ecological strategies of this enigmatic plant group. Here, we describe a new anatomically preserved seed that is substantially larger than forms recorded previously from the Homevale permineralized peat deposits. We also document the presence of pollen entrapped in the micropyle of the seeds. Based on these observations, we infer affinities of the seeds and discuss the implications for coding of characters in gymnosperm phylogenies.

2. GEOLOGICAL SETTING The studied fossil material derives from the Fort Cooper Coal Measures, the middle coal-bearing unit of the Lopingian (upper Permian) Blackwater Group in the HomevaleeHail Creek area of the northeastern part of the Bowen Basin, Queensland, Australia. The Fort Cooper Coal Measures are around 400 m thick in the Homevale and Hail Creek areas and consist predominantly of green, volcanolithic sandstone, carbonaceous and siliceous shale, numerous thin tuff beds, and minor coal, silicified peat, and conglomerate (Goscombe, 1975; Hutton et al., 1991). Exposures are discontinuous and best represented by the more erosion-resistant silicified beds that form low

155

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SECTION j II Late Paleozoic and Mesozoic Plants and Floras

strike-ridges. The silicified peat hosting the fossil seeds described in this study occurs as a thin lens within a siltstoneand sandstone-dominated succession rich in volcanogenic detritus. Siltstones adjacent to the silicified peat lens are rich in impressions of foliage, stems, and roots of glossopterid gymnosperms and osmundaceous ferns. The abundance of tuffaceous beds is the principal feature used to correlate the upper part of the Fort Cooper Coal Measures with the Burngrove Formation in the central part of the Bowen Basin, the upper Black Alley Shale or lower Bandanna Formation in the southwestern sector of the basin, and the Kaloola Member of the Baralaba Coal Measures in the southeastern part of the basin (Koppe, 1978; Fielding et al., 1990; Matheson, 1990). Equivalent plant macrofossil assemblages are also represented in these units (Rigby, 1972; Gould and Delevoryas, 1977; McLoughlin, 1990c, 1992, 1994a,b). The lower part of the Fort Cooper Coal Measures is possibly correlative with the Fair Hill and upper Peawaddy formations in the central and southwestern Bowen Basin, respectively. A Lopingian (late Permian) age has been proposed for the tuffrich interval of the Blackwater Group throughout the Bowen Basin based on palynomorph assemblages assignable to the upper Stage 5bec (Microreticulatisporites bitriangularise Triplexisporites playfordii) Palynozone of Price (1983) or the APP5 Zone of Price (1997). Draper et al. (1990), Briggs (1991), and Shi et al. (2010) tentatively assigned these formations to the MaokouaneWuchiapingian stages. However, recent radiometric dates (CA-IDTIMS UePb dating of zircons from tuffs) obtained by Laurie et al. (2016) for these units in the southern Bowen Basin are in the range of 254.10
0.09e252.54
0.05 Ma, indicating a Changhsingian age. The Fort Cooper Coal Measures are interpreted to have been deposited within predominantly small-scale fluvial channels and extensive low-energy, lacustrine and paludal environments subject to regular extensive blanketing by air-fall tuffs (Hutton et al., 1991). Palaeocurrent data from the Hail Creek area indicate variable sediment transport directions to the southwest and southeast (Jensen, 1975). Silicified peat lenses in the Homevale to Hail Creek areas have been studied since the early 1970s as a source of anatomically preserved plant fossils. Taxa previously described from the silicified peats near Homevale include the osmundaceous fern axis Palaeosmunda williamsii Gould (1970), glossopterid root Vertebraria indica Royle (Gould, 1975), leaf Glossopteris homevalensis Pigg and McLoughlin (1997), an ovuliferous Dictyopteridium-like fructification Homevaleia gouldii Nishida et al. (2007), and a microsporangiate organ Ediea homevalensis Nishida et al. (2013), together with various dispersed, unnamed sporangia (Gould and Delevoryas, 1977) and shoot apices (see Chapter 8). However, significant assemblages of as yet undescribed plant and fungal remains are preserved anatomically in the permineralized peats and as impressions in overlying siltstones at this locality (McLoughlin, 1990c).

3. MATERIAL AND METHODS The material was collected during field work by S.M. and A.N.D. in February 1994 and is held in the palaeontological collections of the Swedish Museum of Natural History, Stockholm. It appears that material cited to be from Homevale in some previous investigations derives from different peat lenses within the Fort Cooper Coal Measures located approximately 2e3 km to the southwest of the source of material in the present study and close to the operational area of Rio Tinto’s Hail Creek Coal Mine (Nishida et al., 2007). Material in our study derives from a lens of silicified peat extending laterally over several meters and with a vertical extent of 5% frequency, and one is calamitalean foliage, which duplicates the occurrence of stem remains at higher frequency. When the taxonomic composition of these collections is considered, sharp differences emerge. Autunia conferta is the most consistently abundant, ranking first in two of the

three (USGS and USNM) and second in the third (NPL). Walchian conifers dominate the NPL collection, occur at slightly more than 5% of the USGS collection, and are a minor element of the USNM collection. Sphenopteris germanica occurs consistently in all three collections at >5% frequency. However, other significant taxa, those occurring at >5% average frequency, are present in only one assemblage: marattialean ferns, calamitalean sphenopsids, the pteridosperm species Odontopteris subcrenulata and Neurodontopteris auriculata, and cordaitalean foliage.

5.2.2 Palynological Quantitative Composition The quantitative composition of the palynological floras is summarized in Table 6.4 for the major groups and Table 6.5 for the detailed breakdown. As noted earlier, pteridosperms dominate the flora, accounting on average for 70%e80% of each assemblage. Most of this abundance is accounted for by species of Vesicaspora, which is present at approximately 30%e50% of each flora and probably can be attributed to the callipterids. Wilsonites spp., attributable to the peltasperms, and Anguisporites intonsus, of uncertain but likely seed plant affinity, also are common elements. Other relatively abundant elements include marattialean fern spores

Lower Permian Sanzenbacher Flora Chapter j 6

117

TABLE 6.4 Major Palynological Groups, Palynomorph Counts, and Percentage of Total Count for Each of the Three Sanzenbacher Samples USGS 9999

USNM 40600

NPL 53178B

Taxa

Group Count

Group %

Group Count

Group %

Group Count

Group %

Lycopsids

5

1.66

3

1.00

4

1.33

Sphenopsids

9

2.99

3

1.00

4

1.33

Marattiales

9

2.99

28

9.36

26

8.67

Other ferns

16

5.32

6

2.01

8

2.67

Cordaitaleans

5

1.66

7

2.34

5

1.67

Conifers

10

3.32

14

4.68

20

6.67

Pteridosperms

234

77.74

219

73.24

211

70.33

Anguisporites intonsus

37

12.29

50

16.72

19

6.33

Vesicapora spp.

144

47.84

95

31.77

145

48.33

Wilsonites spp.

29

9.63

60

20.07

18

6.00

Taeniates

13

4.32

19

6.35

22

7.33

TOTAL

301

100

299

100

300

100

Pteridosperms are subdivided into the most abundant taxa. Taeniates encompass ? Voltziales and Peltaspermales, not including Vittatina. Major groups in bold typeface; individual pteridosperm taxa in italics.

(w3%e9% abundance), conifer pollen (w3%e5% abundance), and taeniates, pollen of uncertain affinity but thought to be from dryland plants (w4%e7% abundance). Sample size emphasizes a distinct advantage of the palynofloral record. At least 64 distinct taxa occur in a mere 900-grain count. We project total diversity to exceed 100 taxa in the many thousands of grains available for observation. Most elements of the palynoflora are rare (Table 6.5). Thirty-eight taxa are present in only one of three collections, which is approximately 60% of the flora. Twenty-one of these single site occurrences are represented by a single grain, 33% of the flora. Many of these rare elements are thought to be derived from small ferns, but such patterns of rarity are found in all the major groups of plants.

6. DISCUSSION Three principal points can be made about the Sanzenbacher flora. The first has to do with sampling of fossil floras: the three, separate Sanzenbacher collections, all made from the same strata at the same location, differ significantly. The second point addresses the relationship between macroflora and palynoflora: recent studies have found these two to differ in unexpected ways (Mander et al., 2010; Looy et al., 2014; Looy and Hotton, 2014). However, at Sanzenbacher, they appear to be broadly congruent. The final point is the similarity of the Sanzenbacher flora to floras of presumed similar age elsewhere in the United States and western

Europe, indicative of broad geographic ranges and extensive species populations across the Pangean equatorial region.

6.1 Collecting The Sanzenbacher collections offer a rare opportunity to assess paleobotanical sampling biases. Although the three collections were made successively 20 and 30 years apart, there was overlap, and discussion, among the collectors. Witte, the original lead collector and supervisor of the 1940s WPA crew, directed Mamay to the site in 1961; Mamay returned to the site in 1991 with three of the authors, thus ensuring continuity of collecting location and strata. In addition, the three collections are of similar size, each approximately 250 hand-sample specimens. We can speak directly to the 1991 USNM collection, which was made in the course of 1 day by four collectors who worked alongside each other. The collection is effectively unbiased: plants were relatively sparse in the matrix, and anything that looked even remotely identifiable was collected. Given what we know of Mamay’s collecting methods elsewhere (the USNM holdings abound with his collections, and we had ample opportunity to discuss his methods in the field and in the museum collections), he retained everything regardless of completeness or perceived taxonomic significance. Thus, the 1961 USGS collection resembles the 1991 USNM collection in terms of lithofacies, the size range of specimens, and specimen quality.

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SECTION j II Late Paleozoic and Mesozoic Plants and Floras

TABLE 6.5 Palynoflora Quantitative Data From Each of the Three Sanzenbacher Collections

Taxa

USGS 9999-1

USNM 40600-1

NPL 53178B-1

Count

Count

Count

3

4

Lycopsids Crassispora kosankei

2

Endosporites globiformis

3

Cadiospora magna Sphenopsids Calamospora cf. breviradiatus Columinisporites ovalis

2 9

1

Laevigatosporites minor

3 1

Marattiales Cyclogranisporites cf. minutus

2

Cyclogranisporites obliquus

1

Cyclogranisporites indet.

2

Dictyomonolites sp.

5 1

Fabasporites cf. pallidus

8

5

Laevigatosporites medius

4

4

Punctatisporites glaber

1

Punctatosporites cf. granifer

2

Punctatisporites cf. minutus

1

Punctatosporites minutus

8

Punctatisporites/Punctatosporites indet.

6

Puncatisporites obesus

2

4

Punctatisporites cf. nudus Leioaletes circularis

5

1 1

Other Ferns Anapiculatasporites sp. A (G18/4)

1

Camptotriletes triangularis

2

Convolutispora cf. florida

1

Convolutispora mellita

1

Convolutispora sp. B (W19)

1

Convolutispora sp. C (F19) Deltoidospora sphaerotriangula

1 5

Granulatisporites indet. Lophotriletes microsaetosus

1 1

Raistrickia cf. aculeata

1

Raistrickia cf. protensa

1

Raistrickia indet.

1

Savitrisporites nux

1

1

1

Lower Permian Sanzenbacher Flora Chapter j 6

TABLE 6.5 Palynoflora Quantitative Data From Each of the Three Sanzenbacher Collectionsdcont’d USGS 9999-1

USNM 40600-1

NPL 53178B-1

Taxa

Count

Count

Count

Triquitrites sculptilis

2

3

1

Verrucosisporites verrucosus

1

Verrucosisporites cf. insuetus (Q18/2)

1 1

Cordaitaleans Cannanoropollis cf. janakii Florinites millottii

1 2

Florinites mediapudens

1

Florinites occultus Florinites indet.

1

1 3

4

4

14

20

Conifers Tinnulisporites microsaccus

1

Potonieisporites species complex

9

Seed Ferns Alisporites cf. plicatus

2

Colatisporites decorus/Anguisporites intonsus

37

Falcisporites cf. stabilis

2

50

4

19

Falcisporites cf. zapfei

5

Falcisporites indet.

2

5

Klausipollenites cf. staplinii

3

Paravesicaspora splendens

2

Platysaccus cf. papilionis

4

4

Platysaccus cf. saarensis

1

6

19

Pityosporites ’clepsydroid’

1

2

Schopfipollenites ellipsoideus

4

Vesicapora species complex

144

95

145

1

Wilsonites species complex

29

60

18

6

5

7

Taeniates Illinites unicus Illinites cf. talchirensis Kosankeisporites cf. elegans

1 1

Protohaploxypinus sp. A Striatoabieites richteri

4 3

12

Strotersporites communis

4 1

Vittatina costabilis

1

1

3

Vittatina lata

1

1

2

TOTAL

299

300

300

Numbers represent the counts of each palynomorph taxon identified.

119

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SECTION j II Late Paleozoic and Mesozoic Plants and Floras

Aspects of the NPL collection, on the other hand, suggest a focus on particularly fossil-rich zones within the exposure, not accompanied by intentional taxonomic or specimen-size filtering on outcrop but, rather, a focus on productive layers at the expense of less productive zones. A very large number of specimens appear to be from a layer 30% of the flora among the three collections that occur only once. In addition, only Autunia conferta occurs at >10% frequency in all three collections, and only A. conferta, Sphenopteris germanica, and Neurodontopteris auriculata have a CV (10) of 5%. Only four taxa in the entire Sanzenbacher sample have a CV 5% frequency in all three collections. The problematic taxon Anguisporites intonsus (w6%e17% of the flora) cannot be compared well with the macroflora

Lower Permian Sanzenbacher Flora Chapter j 6

due to its unknown affinities. Conifer prepollen, Potonieisporites, represented by at least two morphospecies, is relatively uncommon but always present, ranging from 3% to almost 7% of the palynoflora. The greatest palynofloral and macrofloral abundance of walchian conifers occurs in the NPL 1161 samples. The abundance of calamitaleans in the NPL 1161 macroflora is not matched in the palynoflora, however, which may reflect the overrepresentation of this group in the macroflora, as discussed earlier. Most elements of the palynoflora are uncommon. This generally includes probable spores of Marattiales, although these are most abundant and diverse in USNM 40600, which also has the most abundant marattialean remains in the macroflora. Many of the rare spore morphotypes probably represent herbaceous ferns, which are similarly rare in the macroflora. A similar pattern can be found in the palynomorphs of cordaitaleans and lycopsids. Incongruence between macrofloral and palynofloral assemblages does occur. For example, lycopsids are rare but persistent in the palynofloral assemblage (Cadiospora, Crassispora ¼ Sigillaria; Endosporites ¼ Chaloneria) but do not occur in the macroflora. Schopfipollenites (¼ Medullosaceae) is rare but present in all three assemblages, in contrast to the importance of medullosans in the macrofossil assemblages. The reasons for this latter mismatch are not clear but probably relate to the large size of medullosan prepollen, as noted earlier. We did not attempt to characterize the entire flora for this analysis. Nonetheless, the notably higher diversity of the palynological taxa shows that the macroflora significantly underestimates total floral diversity. Rare palynomorphs likely represent plants rare on the landscape, those occupying interfluves, and those growing at different times (due to seasonal variation or short-term fluctuations in weather patterns). In contrast, herbaceous forms, which may be present in the palynoflora, are less likely to be represented in the macroflora compared with arborescent plants (e.g., Scheihing, 1980; Scheihing and Pfefferkorn, 1984).

6.3 Broader Context of the Sanzenbacher Flora 6.3.1 Palynoflora in Context Pennsylvanian-Permian transition palynofloras of the Euramerican province display broadly similar patterns: relict Pennsylvanian wetland taxa in coals and conifer/seedfern dominance in siliciclastic rocks. Palynofloral assemblages from the uppermost Pennsylvanian siliciclastic beds in Texas (Gupta, 1977; Pashuck and Gupta, 1979; Looy and Hotton, 2014) and from Pennsylvanian-Permian strata

121

of New Mexico (Utting et al., 2004; Utting and Lucas, 2010) are similar to the Sanzenbacher palynoflora. All contain significant quantities of Potonieisporites spp., Vesicaspora spp., including the globose form, none taeniate bisaccates (Platysaccus spp., Pityosporites spp.), and relatively small numbers of taeniate pollen (notably Vittatina costabilis, Illinites unicus, Striatoabieites richteri). The enigmatic palynomorph Anguisporites intonsus (sometimes reported as Colatisporites decorus) is also a common component of these floras. Marattialian spores (Punctatisporites minutus, Punctatosporites spp., Cyclogranisporites aureus, Cyclogranisporites minutus, Laevigatosporites medius, Laevigatosporites ovatus) are also present, as well as such herbaceous fern taxa as Convolutisporites spp., Lophotriletes commisuralis, Raistrickia spp. Triquitrites sculptilis, Triquitrites spp., and Deltoidospora (Leiotriletes) spp. These latter taxa are typical of Late Pennsylvanian assemblages and tend to be abundant in coals and subordinate in siliciclastics. Curiously, Savitrisporites nux, which otherwise disappears at the top of the Bolsovian, is described as common in the latest Pennsylvanian of Canyon del Cobre, New Mexico (Utting and Lucas, 2010). Savitrisporites nux also appears (rarely) in the Sanzenbacher palynoflora, where its occurrence could be dismissed as reworking, except for its possible correlation with the Canyon del Cobre assemblage. Most of the palynological studies of Upper Pennsylvanian and lower Permian strata in Kansas, Arizona, and Oklahoma have not attempted to describe a complete assemblage but have rather focused on distinctive species (literature summarized in Lupia and Armitage, 2013). Nevertheless, many of the species described in these reports are a close match to those in the Sanzenbacher assemblage. Lupia and Armitage (2013) also present their own analysis of cores from north central Oklahoma ranging in age from Gzhelian through Kungurian (Virgilian through Leonardian). They do not present taxonomic details, but the overall pattern appears quite similar to that seen at Sanzenbacher. For example, monosaccate prepollen (Potonieisporites) and nontaeniate pollen are moderately abundant, in contrast to taeniate pollen, which does not become abundant until significantly higher in the section, near the top of the Wolfcampian. We have noticed a similar pattern in samples from north central Texas (Hotton and Looy, unpublished data). A notable difference can be seen in the high percentage of trilete spores reported from the lower Asselian Grenola Formation (Lupia and Armitage, 2013). This could be due to sampling of a wet interval, or it could be because the authors treat Anguisporites as a trilete spore e without taxonomic and sedimentological details, the pattern is difficult to interpret. The palynoflora of the Dunkard Group in the Central Appalachian Basin contains many of the typical Late

122

SECTION j II Late Paleozoic and Mesozoic Plants and Floras

Pennsylvanian species described from Sanzenbacher and assemblages of similar age (Clendening, 1975; Eble et al., 2013). Taking into account variance in taxonomic concepts, up to half of the spore morphospecies may be in common between the two floras. However, unlike the Sanzenbacher palynoflora, pollen species such as Potonieisporites spp. and Vesicaspora wilsonii are extremely sporadic in the upper Dunkard (Greene Formation, of likely Asselian age [Tibert et al., 2011, 2013]) and taeniate forms do not appear until near the top of the Greene Formation. The disparity seems clearly controlled by facies: the Dunkard palynoflora was collected from coals, as noted by Eble et al. (2013), whereas the Pennsylvanian-Permian samples described here are derived from siliciclastic deposits. Further evidence of this coalesiliciclastic disparity comes from an uppermost Pennsylvanian coal from the Bursum Formation, New Mexico, dominated by typical Late Pennsylvanian wetland taxa (although also including significant amounts of Vesicaspora) (DiMichele et al., 2016), similar to a coal of similar age described from north central Texas (Looy and Hotton, 2014). European palynological assemblages display a broadly similar pattern, although specific morphotaxa vary, exaggerated by disparities in palynological nomenclature. The Vittatina costabilis zone of Clayton et al. (1977), considered lower Autunian, is characterized by abundant Potonieisporites and Vittatina costabilis (although not their first appearance) and a pronounced decrease in abundance of typical wetland flora. Typical Permian forms (taeniate bisaccates) and virtual disappearance of monolete spores (¼ Marattiales and sphenopsids) mark the Disaccites striatiti Zone (Clayton et al., 1977), corresponding to the upper Autunian. Similar patterns are seen elsewhere across the Euramerican floral realm. The Sanzenbacher palynofloral assemblage is most notable for being composed primarily of Late Pennsylvanian palynomorphs. Even so-called Permian elements occur, though rarely, in the Pennsylvanian. The paleobotanist A.T. Cross noted with regard to the Dunkard flora that it was “essentially a reduced remnant of late Pennsylvanian time with a few Permian precursors being introduced” (paraphrased from Clendening and Gillespie, 1972) e this comment can be applied to almost any known PennsylvanianePermian transition flora. As has been noted many times before, terrestrial vegetation in the Late Pennsylvanianeearly Permian closely tracked climate conditions and is clearly controlled by depositional environment. The absence of novel plant macrofloral or palynofloral taxa at the PennsylvanianePermian boundary, here as well as globally, renders it very difficult to define the stratigraphic boundary in terrestrial strata using plant fossils.

6.3.2 Macroflora in Broader Context The Sanzenbacher flora compares most closely to several floras from the lower part of the Cisuralian Epoch, the

Asselian, and lower Sakmarian Stages, which correlate with the lower Wolfcampian Stage in U.S. regional terminology. Comparability is strengthened by similarity of depositional environments, particularly the absence of coal beds or other lithofacies indicators of extensive wetlands. Three floras from central New Mexico and one from southwest Texas are discussed next, followed by comments on the lower Permian floras known from the eastern United States. In the United States, the closest comparison, stratigraphically and paleoenvironmentally, is with the flora of Carrizo Arroyo (Tidwell and Ash, 2004), from the Red Tanks Member of the Bursum Formation, central New Mexico. The age of this flora is well constrained by conodonts and fusulinids from limestones (Lucas et al., 2013) to the early Wolfcampian. Environmentally, the Bursum Formation in the Carrizo Arroyo vicinity has been interpreted to be a coastal plain in which the remains of plants and freshwater to terrestrial invertebrates accumulated in standing water, possibly a large lake. Comparison is impeded to some extent by the differences in taxonomic names for what, by comparison of illustrations, appear to be the same taxa. Common elements include Autunia conferta, Walchia schneideri, Rhachiphyllum schenkii, Sphenopteris germanica, an Odontopteris that is very similar to O. subcrenulata, Dicranophyllum (identified as lycopsid leaves in the Carrizo Arroyo flora), Cordaites, calamitaleans, and possibly Neurodontopteris auriculata. Carrizo Arroyo has a greater diversity of conifers and includes the noeggerathialean Charliea; however, it lacks marattialean foliage, which is part of the Sanzenbacher flora. A flora from the “Red Magdalena” (terminology of C.B. Read, 1941, notes with USNM collection) also likely is from the Bursum Formation but exposed in Abo Pass, central New Mexico (DiMichele et al., 2017). The deposit probably formed in a brackish-water lagoon surrounding a seasonally dry coastline; brackish-to-marine depositional conditions are suggested by the suite of invertebrates preserved with the plants. Floral overlap with Sanzenbacher is minimal in detail but, as noted for Spanish Queen, later, there is a general similarity in the dominance of taxa regarded as xeromorphic forms, including small numbers of Rhachiphyllum, Taeniopteris, and Odontopteris, within a dominant framework of various walchian conifers, with none like that at Sanzenbacher. No marattialean ferns are present in the “Red Magdalena” collection. In many respects, the Spanish Queen Mine flora of the terrestrial Abo Formation, also from central New Mexico (Lucas et al., 2012) and of early middle Wolfcampian age (likely Sakmarian), likewise, is similar to Sanzenbacher. The flora occurs in gray siltstones with abundant comminuted plant debris, concentrated in pockets or troughs, and deposited in an active fluvial channel. Similar elements include Rhachiphyllum schenkii, Neurodontopteris auriculata, Annularia spicata, Taeniopteris, marattialean

Lower Permian Sanzenbacher Flora Chapter j 6

foliage, including Polymorphopteris sp., and walchian conifers (although different from those of Sanzenbacher). Noncomparable elements include the callipterid Dichophyllum, and the medullosan Alethopteris schneideri. An early Wolfcampian flora from the Neal Ranch Formation of Brewster County in southwest Texas (Glasspool et al., 2013) is comparable to Sanzenbacher despite considerable paleoenvironmental differences. The Brewster County plant remains were deposited in a prodeltaic marine setting and are accompanied by marine invertebrate fossils. Like Sanzenbacher, and the above floras from central New Mexico, the Neal Ranch flora is a mixture of plants characteristic of a variety of soil moisture regimens including xeromorphic elements such as walchian conifers (none in common with Sanzenbacher), callipterids (none in common with Sanzenbacher), medullosan pteridosperms (including Neurodontopteris auriculata), and the incertae sedis elements Taeniopteris and Sphenopteris germanica. However, the flora also includes a large array of wetland plants, such as the lycopsid Sigillaria, marattialean ferns, calamitaleans (including Annularia spicata), and a variety of small fern foliage. American floras of similar age but associated with coal beds contrast compositionally with the Sanzenbacher flora. From Carrizo Arroyo in central New Mexico, small numbers of plant macrofossils have been collected immediately above and below a thin coal bed from very close to the CarboniferousePermian boundary (DiMichele et al., 2016). These are similar to Sanzenbacher in dominance of drought tolerant taxa, primarily walchian conifers, although there is no overlap in species with those from Sanzenbacher, and small numbers of Rhachiphyllum, Taeniopteris, Odontopteris, and calamitalean stems are present. Marattialean ferns dominate the coal palynoflora and are present in the palynofloras of mudrocks above and below the coal, but no macrofossils of these plants were found. From the eastern United States, the flora of the Dunkard Group in West Virginia, Pennsylvania, and Ohio contrasts sharply with all the western U.S., early Wolfcampian assemblages. The age of the Dunkard is debated because it lacks the marine beds and their faunas, used in correlation to regional or global stratigraphies. Recent studies of nonmarine ostracodes suggest an earliest Permian age for the Greene Formation (Tibert et al., 2011, 2013), thus making it of comparable age to Sanzenbacher. The Dunkard flora, however, is overwhelmingly dominated by plants typical of wetland habitats (Blake and Gillespie, 2011), as known from floras in the latest Carboniferous and earliest Permian of Europe (Wagner and Lyons, 1997). Callipterids make their first appearance in the Appalachian Basin in these strata (Washington and Greene Formations of the Dunkard Group: DiMichele et al., 2013) and conifers are known to occur sporadically throughout the Dunkard but also, similarly, sporadically, throughout Upper

123

Pennsylvanian strata in the Appalachians (Lyons and Darrah, 1989; McComas, 1988; Martino, 2017). Wagner and Lyons (1997) provide a cogent analysis of these records and note that environmental changes during the CarboniferousePermian transition make this boundary difficult to determine with plant fossils and that the time of appearance of xeromorphic elements across Euramerica is highly variable. Much more is known of floras from the CarboniferousePermian transition in Europe than in the United States. The boundary is, again, difficult to identify there due to the extreme continentality of the geological successions, although recent radiometric age dates have been correlated to the floral succession, providing hope for a greatly improved understanding and basis for correlation (Oplustil et al., 2016). Nonetheless, there are well-studied and highly diverse floral successions to which the Sanzenbacher flora is compositionally similar, if less diverse. Recently, Wagner and Álvarez-Vázquez (2010) proposed a new floral zone for the uppermost Carboniferous, the Annularia spicata floral zone, to which the Sanzenbacher flora is similar. This would fall under the Autunia conferta floral zone as presented in Oplustil et al. (2016), which spans the CarboniferousePermian boundary in Europe. Comparable floras, differing to varying degrees in the relative abundance of taxa but with the same basic floristic composition, are reported from Scotland (Wagner, 1983), southwestern Spain (Broutin, 1986, Wagner and Mayoral, 2007), northern Spain (Wagner and Martínez García, 1982), France (Steyer et al., 2000), Germany (Kerp and Fichter, 1985; Barthel, 2009), the Czech Republic  unek and Martínek, 2009; Oplustil et al., 2017), and (Sim Romania (Popa, 1999), and this is a small representative selection of published floras.

7. CONCLUSIONS The Sanzenbacher flora is one of the few early Wolfcampian (Asselian) floras to be reported from north central Texas, an area well known for its Permian vertebrate fossils. As such, it serves as a point of comparison to other floras from the early Permian of western Pangea. Comparison with several described floras indicates considerable variation in space and time. However, similarities also are revealed, including the consistent mixture of plants interpreted to have grown in wetter and more water-stressed substrates. Drought-tolerant taxa, including conifers, callipterids, taeniopterids, and certain of the medullosan pteridosperm groups (particularly Neurodontopteris and Neurocallipteris), occur widely among these floras intermixed with more mesomorphic to hygromorphic plant groups, such as marattialean tree ferns and calamitaleans. The Sanzenbacher flora is one of many floras collected for the first time by the WPA, during the late 1930s and

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early 1940s. These floras guided our initial collecting efforts in north central Texas, and we anticipate future research on other localities discovered by the WPA in Clay Couty and adjacent counties. It is our hope that this continuing work will further enhance our understanding of early Permian floras and environments.

ACKNOWLEDGMENTS We thank the late Ann M. Molineux, The University of Texas, Jackson School, Non-vertebrate Paleontology Laboratory, for making collections available for our study. The management and staff of Central Transportation Systems generously facilitated our work while the Sanzenbacher collection was stored temporarily in their Austin warehouse. We are indebted to Dale Coleman for access to the former Sanzenbacher property in 1991. The previous year, Christopher J. Durden provided access to the WPA collections, then held by the Texas Memorial Museum in Austin. Matthew A. Brown, James C. Sagebiel, and Steven May, all of the VPL, along with Steven K. Madsen, assisted our research on the WPA and Adolph Witte. We gratefully acknowledge the significant contributions of the late Sergius Mamay to our research. We thank Arden Bashforth for his review of an earlier version of this report. The research of Carol Hotton was supported in part by the Intramural Research Program of the National Institutes of Health, National Library of Medicine. This report is dedicated to the memory of Thomas N. Taylor, a leading voice for paleobotany internationally and a strong and tireless advocate of empirical research.

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Chapter 11

Enigmatic, Structurally Preserved Stems From the Triassic of Central Europe: A Fern or Not a Fern? Jean Galtier1, Carla J. Harper3, 4, Ronny Ro¨ßler5, 6, Evelyn Kustatscher2, 7 and Michael Krings2, 3, 4 1

UMR AMAP, CIRAD, Montpellier, France; 2Ludwig-Maximilians-Universität München, Munich, Germany; 3SNSB-Bavarian State Collection for

Palaeontology and Geology, Munich, Germany; 4University of Kansas, Lawrence, KS, United States; 5Museum für Naturkunde Chemnitz, Chemnitz, Germany; 6TU Bergakademie Freiberg, Freiberg, Germany; 7Museum of Nature South Tyrol, Bozen/Bolzano, Italy

1. INTRODUCTION Ferns constitute one of the largest and most diverse lineages of vascular plants; today, they are second only to the angiosperms in number of species (Pimm and Raven, 2017). Despite the large number of modern and innumerable fossil species that have been formally described over time and documented in great detail, the evolutionary history and phylogeny of the ferns remain poorly understood to date, and conflicting ideas and scenarios exist in the literature. Molecular analyses have contributed greatly to resolve some of the open questions but have also added to the confusion, especially through the constant introduction of new combinations. For example, the recent, comprehensive phylogenetic classification of fern (and lycophyte) genera by PPG I (2016) maintains continuity in the naming and circumscription of families and genera as recognized by most pteridologists before the molecular revolution (e.g., Kramer and Green, 1990) and thus continues the approach used in most phylogenetic classifications (e.g., Smith et al., 2006; Christenhusz and Schneider, 2011; Christenhusz et al., 2011; Rothfels et al., 2012). However, PPG I (2016) differs from other phylogenetic classifications that favor a reduction in the number of taxa recognized (e.g., Christenhusz and Chase, 2014). The study by PPG I (2016) focuses exclusively on present-day taxa, due primarily to the many challenges of incorporating fossils. Although some fossils could easily be accommodated, the phylogenetic affinities of most extinct forms remain

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00011-5 Copyright © 2018 Elsevier Inc. All rights reserved.

unresolved. Moreover, “. many fossil taxa represent distinct evolutionary lineages and their inclusion in the PPG I classification would not only require revised circumscriptions, but almost certainly the recognition of new families, orders, and even classes.” (PPG I, 2016). Ferns sensu lato have a copious fossil record that extends back to the Devonian and indicates considerable systematic turnover through geologic time (Rothwell, 1999). However, a large proportion of the evidence of the ferns of the geologic past comes from impression and compression specimens, as well as dispersed spores, which are often problematic because not all of the characters commonly used in the determination of the systematic affinities are available. Conversely, anatomically preserved material often provides an opportunity to study internal structural detail as well as external form and therefore is generally better suited to gather a broad spectrum of systematically informative characters (Pigg and Rothwell, 2001). Stelar organization is not normally used by neobotanists to assess the systematic position of vascular plants because the outer boundary of the stele is often difficult to determine and stelar configuration varies at different stages of development. However, the stele has been very useful in comparative and phylogenetic studies of fossil vascular plants, especially ferns (Schmid, 1982). Nevertheless, stelar organization can be assessed only from structurally preserved fern fossils, which frequently occur in the late Paleozoic of Europe, North and South America, and China

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(e.g., Galtier and Taylor, 1994; Stockey et al., 1999; Collinson, 2001; Pigg and Rothwell, 2001; Phillips and Galtier, 2005, 2011; Galtier and Phillips, 2014); the Southern Hemisphere Mesozoic (e.g., Tidwell and Rozefelds, 1990; Yao et al., 1991; Delevoryas et al., 1992; Rothwell et al., 2002; Vera, 2013); and the Northern Hemisphere (NH) Jurassic to Cretaceous (e.g., Stockey et al., 2006; Bomfleur et al., 2015). If structurally preserved material is not available, such as from the Triassic of the NH, stelar organization cannot be used to assess affinities (Daugherty, 1960). On the other hand, if structurally preserved Triassic NH fern fossils are discovered, the integration of these fossils into the systematic classification is even more difficult because, if nothing closely related is known, then it usually goes into the literature as a curiosity and is often left obscure. Several excellently preserved fossils, but of dubious affinities, remain ignored and passed more or less unnoticed in the botanical literature. For example, certain exquisitely preserved, permineralized Triassic stems were initially described from France (Renault, 1879, 1901) and Upper Silesia (Michael, 1895; Potonié, 1899) and interpreted as lycopsids, then as putative ferns, under the name of Knorripteris jutieri. The most recent references to these stems (attributed to the family Knorripteridaceae Hörich, 1912) in paleobotanical textbooks are found in Gothan and Weyland (1964) and Emberger (1968); later reviews and textbooks no longer mention these taxa (e.g., Stewart and Rothwell, 1993; Taylor and Taylor, 1993; Taylor et al., 2009). In this report, we describe several permineralized stems from the Triassic of central Europe that are characterized by complements of structural features unknown in any fossil or extant taxon except Knorripteris. The stele and the leaf trace anatomy are unique among the ferns. For example, the primary vascular system neither fits with current concepts of stelar evolution or with the nodal structure (with or without leaf gaps) occurring in pteridophytes as summarized in Beck et al. (1982) and Beck (2005). Rather, the central vascular system consists of a discontinuous phloem cylinder and of xylem strands, in continuity of leaf traces, which extend down to, and converge at the center of, the stem. This renews an interesting question from the old botanical literature: How much of the primary vascular system is foliar in origin, and how much of it is cauline? The stelar theory supports an evolutionary series of the cauline vascular system from a protostele to a eustele. The eustele of lignophytes, long considered as having evolved from a precursor with dictyostelic condition (Jeffrey, 1902), is now interpreted as a system of discrete sympodia, each consisting of an axial bundle from which leaf traces diverge without leaf gaps (cf. Beck et al., 1982). We discuss how the stelar organization of the new Knorripteris specimens may be interpreted in comparison to the common

dictyostelic type of ferns (see White and Weidlich, 1995) and to the nonhomologous eustelic pattern. Moreover, we speculate on the affinities of Knorripteris. Although we are unable to provide a satisfying answer to the question “a fern or not a fern?” this study is important because it adds critical information and sheds new light on (putative) fern fossils that have remained largely obscure for more than 50 years, but that may be highly significant.

2. HISTORICAL BACKGROUND The fossils presented in this study resemble several permineralized stem portions from the Triassic of France and Upper Silesia (an area in central Europe today located mostly in Poland, with small portions in the Czech Republic) that were studied in the late 19th century. For example, Renault (1879) briefly described a conical fragment of a stem found under a dolmen in Alsace, France (Fig. 11.1AeC). Based on external morphology, in particular the helical arrangement of leaf base-like protuberances, Renault suggested lepidodendroid affinities for the stem that he named Lepidodendron jutieri. A second specimen, discovered from the Muschelkalk of Upper Silesia, was described by Michael (1895) and named Knorria mariana, likewise in reference to lepidodendroid external characters or Knorria-type preservation. In 1899, Potonié reassessed the specimen described by Michael (1895; Fig. 11.1D) and provided, but did not illustrate, information on the heterogeneous cortex, the leaf traces, and the central void region containing narrow cylindrical bundles. Potonié attributed the stem to the ferns, despite the Knorria mode of preservation, and proposed the new genus Knorripteris for the specimen. However, neither Michael (1895) nor Potonié (1899) mentions the study by Renault (1879). Equally strange is the fact that Renault did not mention the reports by Michael (1895) and Potonié (1899) in his detailed analysis of the French specimen that included the first photographic images of the fossil (Renault, 1901). Renault was authorized to prepare new thin sections, which provided a wealth of new details, including the central region of the stem that was occupied by what he termed “vasiform” cells surrounding small vascular strands, which correspond to decurrent traces. Moreover, Renault confirmed photographically that each xylem strand consisted of five small tracheid bundles, as suggested previously by Potonié (1899). Based on the new data collected from the vascular system, Renault (1901) rejected lepidodendroid affinities and renamed the stem Adelophyton jutieri (from the Greek adelos ¼ little known), thus acknowledging the uncertainties that remained regarding the “extraordinary structure” of this plant and its interpretation as an “incontestable fern.” A few years later, Bertrand (1907) revisited the material of A. jutieri from the Renault slide collection and prepared

Enigmatic, Structurally Preserved Stems Chapter j 11

(A)

(B)

(D)

(C) (H)

(F)

(I)

(G) (E)

FIGURE 11.1 Comparison of historical and new specimens of Knorripteris. (AeC) Knorripteris jutieri, surface views (A and B) and transverse section (C). (D) Knorripteris jutieri, external surface. (E) Knorripteris jutieri, transverse section. (FeH) Knorripteris taylorii holotype; external surface (F), longitudinal (G) and transverse (H) sections. (I) Knorripteris taylorii paratype; transverse section. All figures at the same magnification, except Fig. 11.1E. Scale bars ¼ 1 cm. (AeC) Redrawn from Renault, B. 1901. Sur un nouveau genre de tige fossile. Bulletin/ Société d’histoire naturelle d’Autun 13: 405e645, Plates VI, 1,2 and VII, 1. (D) Redrawn from Potonié, H. 1899. Lehrbuch der Pflanzenpalaeontologie mit besonderer Rücksicht auf die Bedürfnisse des Geologen 1. Ferd, Dümmlers Verlagsbuchhandlung, Berlin, Germany. pp. 68e69; 76e77, Fig. 35. (E) Redrawn from Rudolph, K. 1937. Ein neues Exemplar von Knorripteris jutieri Renault spec. Palaeontographica B 82: 143e171, Plate 14, 2.

a reconstruction of the vascular system, which depicts a helicoidal xylem reparatory strand (or “sympode”) formed by the fusion of successive xylem traces. On the other hand, the phloem according to this reconstruction constitutes of a massive, discontinuous cylinder interrupted at the level of divergence at each leaf trace xylem. The opening is caused by the departure of the phloem with the corresponding leaf trace. Bertrand (1907) emphasized the “unique independence” of the phloem and xylem in this plant, except in leaf traces extending through the cortex. He also confirmed that

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the leaf trace xylem was composed of five metaxylem tracheid bundles with no identifiable protoxylem ad provided details on the sclerenchymatous inner cortex, and the aerenchymatous ground cortex. Finally, based on the anatomical structure, he interpreted the plant as a fern with no modern analog. Hörich (1910) then restudied the specimen of K. mariana and presented the first photographic images of the stem that confirmed similarities with A. jutieri with regard to the xylem and phloem strands, leaf traces, bizoned cortex, and the “spirally thickened elements” (¼vasiform cells of Renault, 1901). However, Hörich suggested that the xylem strands ended blindly in the center of the stem and dismissed the existence of the helical xylem sympodia described by Bertrand (1907). Finally, he suggested that A. jutieri and K. mariana are conspecific and presented a generic diagnosis for Knorripteris that was not very informative regarding the complex vascular system. Based on the information provided by Hörich (1910), Bertrand (1911) agreed that the French and the Upper Silesian specimens probably belong to the same species but corrected the taxonomy; according to the rules of priority, the fossil must be named K. jutieri. This was subsequently accepted by Hörich (1912), who then also proposed the new fern family Knorripteridaceae, which was accepted by Potonié (1921). The systematic affinities of the stems remain controversial. For example, Posthumus (1924) suggested affinities with the seed plants, while Hirmer (1927) listed the stems as a fern incertae sedis. In 1929, Jongmans summarized the published accounts, argued in favor of the name K. jutieri, and interpreted the plant simply as a fern. Moreover, he noted that the French specimen is likely from the Muschelkalk of the Vosges Mountains. Seward (1931) lists the stem as a fern incertae sedis and as a good example of a fossil plant that cannot be attributed to any modern plant family. Finally, von Wettstein (1937) cautiously states that K. jutieri might have affinities with the Filicales but also emphasizes that any assignment to a present-day lineage remains conjectural. A little later, yet another stem portion (Fig. 11.1E) of unknown provenance, from the holdings of the Geological Institute in Prague, was described in great detail and attributed to K. jutieri by Rudolph (1937). This author prepared serial transverse sections and reconstructed the hollow cylinder of phloem interrupted by leaf traces in a meshwork-like fashion. He interpreted the xylem of leaf traces ending blindly in the center of the stem, even though he illustrated serial sections showing two successive and converging xylem traces in close contact. Finally, he considered that the vascular system was derived from a primal protostele with a cauline phloem mantle/meshwork, while the primary xylem is completely replaced by medullary parenchyma (not preserved), creating space for the

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French specimen 1879 Renault description of Lepidodendron jutieri

1901 Renault rejects L. jutieri and proposes Adelophyton jutieri (Figs 1A-C)

Upper Silesian specimen

1895 Michael description of Knorria mariana 1899 Potonié description of Knorripteris mariana (Fig. 1D)

1907 Bertrand detailed study on phloem of Adelophyton jutieri (Figs 5A-B, 7A)

1910 Hörich proposed to keep Knorripteris as

1911 Bertrand agrees; proposes to use Knorripteris jutieri

study (Fig. 5C) 1912 Hörich agrees; new fern family, Knorripteridaceae erected 1921 Potonié accepts Knorripteridaceae 1924 Posthumus suggests seed plant affinity

taxonomic description or change in depth study of stele discussion of systematic affinities

1927 Hirmer 1929 Jongmans 1931 Seward

state affinity in ferns incertae sedis

1937 Rudolph detailed stele; emphasized unique phloem (Figs 1E, 5D) 1938 Posthumus discusses ontogeny of vasculature

FIGURE 11.2 Summary timeline of historical background of Knorripteris jutieri. Corresponding line drawings that were reproduced in this study are noted. See text Section 2 for details.

extension of leaf trace xylems in the center of the stem. In a short communication, Posthumus (1938) summarizes and emphasizes the importance of the work by Rudolph (1937), especially with regard to the extraordinarily detailed description of the position of the phloem. Also mentioned was Rudolph’s thorough discussion of the affinities of K. jutieri, which range from the osmundaceous and filicalean ferns to seed plants. The historical account of K. jutieri is a convoluted story of multiple parallel studies from France and Upper Silesia that resulted in more questions than answers (see summary timeline for historical background in Fig. 11.2).

3. GEOLOGICAL SETTINGS This study presents two stem portions that are similar in size and overall internal organization to Knorripteris jutieri, one from the collections of the SNSB-Bayerische Staatssammlung für Paläontologie und Geologie (BSPG) in Munich, Germany (henceforth denoted “Munich fossil”),

and one from the Museum für Naturkunde in Chemnitz, Germany (denoted “Chemnitz fossil”). The Munich specimen was discovered about 50 years ago and, according to the label attached to it, was collected east of the city of Schweinfurt (Schonunger Bucht), N-Bavaria, Germany, from sands deposited along the left bank of the river Main (see Harper et al., 2018, Fig. 11.1). Unfortunately, more precise locality information is not available; therefore, the stratigraphic age of the fossil is difficult to resolve. The Schonunger Bucht is a series of abandoned sand excavation sites along the river Main that today are filled with water, and the “sands” mentioned in the label might refer to these fluvial deposits that occur along the river (Ziegler, 1990; Bormann et al., 2011). The original label states that the specimen likely is from the uppermost Muschelkalk or lowermost Keuper, and thus possibly Ladinian (242e237 Ma) in age (Deutsche Stratigraphische Kommission, 2016). However, we cannot rule out that the fossil was reworked and hence might be still older. Likewise, provenance and precise geological age cannot be determined for the Chemnitz fossil. The only information available states that the fossil was collected between 1980 and 1983 in Knetzgau, Germany (approximately 30 km east of Schweinfurt), from the Kümmel gravel plant, located within an embankment area along the river Main.

4. MATERIAL AND METHODS The Munich fossil (Plates I, III, and V, 4e10; Figs. 11.1FeH, 11.3A,B, and 11.4) was cut into five pieces (designated letters AeE in Plate I, 1); one slice (transverse section) was cut off the top of the specimen (B, Plate I, 1) and the remaining stem portion was then cut longitudinally, resulting in one half representing a median longitudinal section (A, Plate I, 1) and the other half that was further divided into three parts, i.e., top, middle, and basal (CeE, Plate I, 1) longitudinal sections. Thin sections were prepared by cementing thin slices (wafers) of the specimen to glass slides and then grinding with silicon carbide powder until the section was thin enough to transmit light. All specimen pieces and thin sections are deposited in the SNSB-BSPG in Munich, Germany, under acquisitions SNSB-BSPG 1968 I 97AeE (specimen pieces) and SNSBBSPG 1968 I (ex 97) 269e273 (thin sections); specifically, letter B in Plate I, 1 corresponds to slides SNSB-BSPG 1968 I (ex 97) 269 and 270, letter C in Plate I, 1 to slide SNSB-BSPG 1968 I (ex 97) 271, letter D in Plate I, 1 to slide SNSB-BSPG 1968 I (ex 97) 272, and letter E in Plate I, 1 to slide SNSB-BSPG 1968 I (ex 97) 273. The Chemnitz fossil (Plates II, IV, and V, 1e3; Figs. 11.1I and 11.3C,D) was cut into three pieces (designated letters AeC in Plate II); one slice (transverse section) was cut off of the top of the specimen (A, Plate II), the

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PLATE I Knorripteris taylorii sp. nov. holotype (Munich fossil). (1) Overview and sectioning of specimen into five pieces (AeE). (A) Piece separated by longitudinal axial section (see Plate I, 2). (B) Top transverse section corresponding to slide SNSB-BSPG 1968 I (ex 97) 269. (C) Top longitudinal section corresponding to slide ee271. (D) Middle longitudinal section corresponding to slide ee272. (E) Piece remaining after preparation of transverse section slide ee270 and longitudinal section slide ee273. Scale bar ¼ 1 cm. (2) Longitudinal axial surface of piece A in Plate I, 1, showing acropetal decrease in diameter of central stelar zone. Scale bar ¼ 1 cm. (3) Cast of specimen before sectioning, showing helically arranged elongate leaf scars. Scale bar ¼ 1 cm. (4) Rounded base of specimen before sectioning, showing central scar surrounded by leaf bases (arrows). (5) Longitudinal section of proximal region (piece E in Plate I, 1), showing cortex, broad stelar zone, and departing horizontal-oblique leaf traces (arrows). Slide SNSB-BSPG 1968 I (ex 97) 273. Scale bar ¼ 5 mm. (6) Transverse section of top of proximal region (piece E in Plate I, 1), showing cortex with numerous obliquely sectioned leaf traces, darkened inner cortex (ic), and central stelar zone with numerous xylem strands. BSPG 1968 I (ex 97) 270. Scale bar ¼ 5 mm. (7) Radial longitudinal section of central region (piece D in Plate I, 1), showing wide cortex, darkened inner cortex (ic), and stelar zone with oblique xylem strands converging to center (see detail on Fig. 11.4). Slide SNSB-BSPG 1968 I (ex 97) 272. Scale bar ¼ 5 mm. (8) Radial longitudinal section of upper region (piece C in Plate I, 1), showing wide cortex with oblique to nearly vertical xylem strands and leaf trace (arrow) and stelar zone. Slide SNSB-BSPG 1968 I (ex 97) 271. Scale bar ¼ 5 mm.

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(A) i (B)

(C)

ii

PLATE II Knorripteris taylorii sp. nov., paratype (Chemnitz fossil). (1) (A) Thin transverse cut of top of specimen; specimen K4549A. (B) One-quarter cut of specimen; specimen K4549B; “i” corresponds to top of slice B for transverse thin section; slide K4549-DS1. (C) Remaining portion of stem; specimen K4549C; “ii” corresponds to near midpoint of specimen for transverse thin section; slide K4549-DS2. Scale bar ¼ 1 cm.

remaining stem portion was then cut into two parts (both transverse sections), a one-quarter portion of the stem (B, Plate II) and the leftover three-quarter piece (C, Plate II). One thin section was prepared from the top of portion B (cut denoted “i” in Plate II) and a second section from near midway of portion C (cut denoted “ii” in Plate II). All specimen pieces and thin sections are housed in the Museum für Naturkunde in Chemnitz, Germany, under acquisition numbers K4549A (A, Plate II), K4549B (B0, Plate II), and K4549C (C, Plate II) (specimen pieces); “i” in Plate II corresponds to thin section K4549-DS1 and “ii” in Plate II to thin section K4549-DS2. Additional specimens used for comparison (but not figured) of the morphology and anatomy of the Munich and Chemnitz fossils come from the private collections of Mr. Raimund Rojko (Mönchengladbach, Germany) and Mr. Robert Noll (Tiefenthal, Germany). Thin sections were examined with a Leica DMLB2 transmitted light microscope and photographed using a Leica DFC480 digital camera; images were processed

minimally (i.e., to adjust brightness and contrast) in Adobe Photoshop CS6. All thin sections obtained from the stem were first imaged at low magnification. Overview images (i.e., Plates I, 5e8, II, i,ii, III, 1,2, and IV 1,2; Fig. 11.4B) were captured with a Keyence VHX-5000 digital microscope using two-dimensional panorama with a 10 objective and processed in Adobe Photoshop CS6. In addition, large mosaic composite images were produced in Adobe Photoshop CS6 (e.g., Fig. 11.3B,D); however, free and open-source image editing software such as GNU Image Manipulation Program can also be used. The mosaic images represent composites of 150e170 images stitched together by slightly overlapping shared edges (Kerp and Bomfleur, 2011). To obtain detailed images of the individual structures, images of the same specimen were recorded at multiple focal planes and stacked to produce composite images (Plates III, 3e9, IV, 3e9, and V, 4e10); measurements were taken using Adobe Photoshop CS6. All line drawings (Figs. 11.1, 11.2, 11.3A,C, 11.4A, 11.5, and 11.6) were produced in Adobe Illustrator CS6.

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PLATE III Knorripteris taylorii sp. nov., holotype (Munich fossil). (1) Transverse section near top of stem, showing the wide homogeneous cortex with numerous leaf traces. One leaf parastichy (of a set of five) is drawn with a dashed line. Numbered leaf traces are illustrated in detail in Plate III, 3e6, the central stelar zone is shown in detail in Fig. 11.3A,B. Slide SNSB-BSPG 1968 I (ex 97) 269. Scale bar ¼ 5 mm. (2) Longitudinal section of upper region of stem (detail of Plate I, 8), showing wide parenchymatous cortex of rectangular cells, occasionally in vertical files. One very oblique leaf trace is visible. On right side, elongate phloem strands. Slide SNSB-BSPG 1968 I (ex 97) 271. Scale bar ¼ 1 mm. (3e6) Detail of transverse sections of leaf traces 15, 19, 29, and 49 from Plate III, 1. All from slide SNSB-BSPG 1968 I (ex 97) 269. All scale bars ¼ 500 mm. (3) Leaf trace 15 in phloem zone, showing elongate tracheid xylem strand abaxially curved; note that leaf trace is clearly separated from small phloem bundle (PH) by small-celled parenchyma. (4) Leaf trace 19 with crescent shaped xylem strand still separated from phloem bundle (PH) by multilayered parenchyma (MP). (5) Leaf trace 29, showing smaller xylem strand with well-preserved abaxial protoxylem (arrow) and larger phloem bundle with probable protophloem dark zone; note narrow zone of small cells separating phloem from xylem and surrounding xylem. (6) Leaf trace 49 showing still smaller xylem tracheid strand; abaxial xylem zone is decayed and crescent shaped phloem bundle also partly decayed. (7) Longitudinal section in basal region of a leaf trace diverging in inner cortex. From top to bottom left: scalariform tracheid strand (TR), abaxial xylem parenchyma (XP), narrow zone of small parenchyma cells (MP) separating xylem from phloem (PH) with sieve cells (SC), and cortical parenchyma (CP). Slide SNSB-BSPG 1968 I (ex 97) 273. Scale bar ¼ 100 mm. (8) Detail of scalariform tracheids and adjacent CP in longitudinal section. Slide SNSB-BSPG 1968 I (ex 97) 271. Scale bar ¼ 100 mm. (9) Detail of phloem zone with nicely preserved SC showing sieve areas (arrows). Slide SNSB-BSPG 1968 I (ex 97) 272. Scale bar ¼ 100 mm.

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PLATE IV Knorripteris taylorii sp. nov., paratype (Chemnitz fossil) ((1e6), slide K4549-DS2), and tyloses in paratype and holotype specimens ((7, 9) slide K4549-DS1; (8) Slide SNSB-BSPG 1968 I (ex 97) 269). (1) Transverse section, showing wide parenchymatous cortex with >70 leaf traces, numerous protruding small leaf bases, and central stelar zone. Numbered leaf traces (13, 19, 37, 78) are detailed in Plate IV, 3e6. Scale bar ¼ 1 cm. (2) Detail Plate IV, 1, showing massive, homogeneous cortex, leaf traces, and one protruding leaf base (arrow). Scale bar ¼ 5 mm. (3e6) Details of leaf traces orientated with adaxial side down to fit with the adjacent Plate IV, 2. All scale bars ¼ 500 mm. (3) Leaf trace 13 in phloem zone; wide C-shaped xylem strand is surrounded by very small parenchyma cells. (4) Leaf trace 19 with smaller xylem tracheid strand and nicely preserved phloem. Whole leaf trace is surrounded by cortex with large parenchyma cells. (5) Leaf trace 37 from middle cortex; xylem strand is significantly smaller; abaxial region and large phloem bundle decayed. (6) Outermost leaf trace 78 within a leaf base; xylem and phloem are decayed and show small lacunae. (7e9) Tyloses in leaf trace xylem. (7) Detail of xylem of leaf trace within innermost cortex; tyloses with “banded” appearance begin to develop (arrows) from abaxial zone of small cells at right. Scale bar ¼ 250 mm. (8) Detail of xylem strand with vesicular tyloses inside abaxial concavity. Scale bar ¼ 250 mm. (9) Leaf trace xylem showing abaxial concavity fully occluded by elongate tyloses. Scale bar ¼ 125 mm.

PLATE V Knorripteris taylorii sp. nov., Chemnitz and Munich fossils. Details of the central stelar zone. (1) Transverse section across phloem zone showing one large phloem strand partly decayed (PH) in front of the elongated xylem strand (6) with abaxial protoxylem (PX). There are two older leaf traces (11 and 14) on both sides of the phloem strand. Note parenchyma of very small cells extending between phloem and xylem and internally around xylem strand (6). Arrows designate accumulations of “transfusion tissue.” Note stem center situated near top of figure. Slide K4549-DS2. Scale bar ¼ 1 mm. (2) Another area across the phloem zone of the same section, showing younger xylem strand (4) in front of two phloem strands (IX and X) closing gap left by departure of leaf trace (17) at left. Note that traces 4 and 17 belong to the same parastichy of a set of 13. Stem center is toward the right of the figure. Slide K4549-DS2. Scale bar ¼ 1 mm. (3) Central area of the same section, showing the 3 youngest xylem strands (0, 1, 2) helically arranged, in contact by their parenchyma envelope (p) but around a central triangular void. Slide K4549-DS2. Scale bar ¼ 1 mm. (4) Longitudinal section of entire stelar zone, showing, on each side, several superposed phloem strands and, in the middle, numerous decurrent xylem strands obliquely orientated and converging toward axial center of stem. Holotype, detail of basal area of surface A shown in Plate I, 2. Scale bar ¼ 1 mm. (5) Same section as Plate V, 4, detail of median axial zone showing converging xylem strands radially or tangentially sectioned (arrows) and very close to each other. Scale bar ¼ 1 mm. (6) Same section as Plate V, 4, adjacent area showing converging xylem strands with better radial section and changing in orientation from oblique to vertical (arrows). Note occurrence of “transfusion tissue” around the proximal extremities of xylem strands. Scale bar ¼ 1 mm. (7) Longitudinal section of tracheid xylem strand (X) crossing phloem zone before turning down obliquely toward stem center. Note undulating pattern of tracheids adjacent to palisade-like parenchyma (arrows). Transfusion tissue (TT) cells are present. Slide SNSB-BSPG 1968 I (ex 97) 273. Scale bar ¼ 500 mm. (8) Same section as Plate V, 7, detail of xylem strand entering obliquely in the central zone. The tracheid strand (X) is surrounded by several layers of small parenchymatous cells (P) with an outer, dark “epidermis-like” layer (E). Accumulation of TT in axil of xylem strand. Slide SNSB-BSPG 1968 I (ex 97) 273. Scale bar ¼ 500 mm. (9) Longitudinal section showing detail of TT cells proliferating from the inner layer (arrows) of xylem parenchyma. Slide SNSB-BSPG 1968 I (ex 97) 272. Scale bar ¼ 250 mm. (10) Accumulation of transfusion tissue cells showing spiral thickenings. SNSB-BSPG 1968 I (ex 97) 271. Scale bar ¼ 100 mm.

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5. SYSTEMATIC PALEONTOLOGY Incertae sedis Pteridophyta Kramer et Green, 1990 Family Knorripteridaceae Hörich, 1912 Genus Knorripteris Potonié, 1899 Emended diagnosis: Stem is erect with helically arranged leaf bases. There is massive ground tissue with numerous cauline leaf traces. Central vascular system consists of a discontinuous cylinder of phloem surrounding a complex central xylem zone. The largest trilobed phloem strands divide into three with the median, and smallest strand, becoming the phloem of the next departing leaf trace. Xylem of leaf traces extends down as cauline xylem strands are helically arranged and converge to the very center of stem. There is a broadly circular central zone, with most tissues decayed except the decurrent xylem strands and accumulations of cells with spiral thickenings or “transfusion tissue.” Xylem is in leaf traces and cauline strands with abaxial protoxylem. Progressive decrease in width of the xylem of leaf traces during their outgoing course across the cortex. Notable absence of roots. Type species: Knorripteris jutieri (Renault) Bertrand Synonyms 1879 Lepidodendron jutieri Renault; Renault, p. 258 1895 Knorria mariana Michael; Michael, p. 491 1899 Knorripteris mariana Potonié; Potonié, p. 68, Fig. 35 1901 Adelophyton jutieri Renault; Renault, p. 22, Plates 8e10 1911 Knorripteris jutieri Bertrand; Bertrand, p. 278 Knorripteris taylorii Galtier, Harper, Rössler, Kustatscher et Krings sp. nov Specific diagnosis: Stems up to 60 mm in diameter show acropetal decrease in diameter. Rounded base with central vascularized scar is suggestive of a zone of attachment in one specimen 8.5 mm long. Leaf bases are recognizable as narrow ridges (2 mm wide), helically arranged. Prominent parenchymatous cortex up to 25 mm thick, relatively uniform, has no evidence of zonation. Parenchyma cells are polygonal, often isodiametric, and sometimes showing vertical alignment. Cells vary in diameter from 10 to >200 mm; intercellular spaces exceed 100 mm diameter. Smallest cells (10e20 mm) occur in leaf bases, around the outgoing leaf traces, and in continuous darker zone bounding phloem. Discontinuous phloem cylinder (2 mm thick and 8e16 mm diameter) composed of >10 irregularly shaped strands (each up to 2 mm wide) of thinwalled cells, generally decayed. Phloem parenchyma of small cells (10e20 mm diameter) extend around phloem strands and departing leaf traces, in continuity with innermost cortex. Central circular xylem zone 5e10 mm in diameter, containing numerous flattened strands (up to

2.2 mm wide) of scalariform tracheids surrounded by small-celled parenchyma. Xylem strands, in the continuity of the leaf trace xylem, extend down to center of stem where up to three small strands occur in close contact. There is no evidence of lateral fusion of tracheid bundles, which are enveloped by parenchyma and associated with transfusion tissue. Innermost layers of continuous xylem parenchyma proliferate into cells (20e50 mm diameter and up to 100 mm long) with spiral thickenings (transfusion tissue). Accumulations of this tissue are present only in central “lacunar” xylem zone. Transverse sections of cortex with up to 70 leaf traces are arranged in sets of five, eight, or 13 parastichies. Leaf traces are oval (approximately 1 mm radially  0.5 mm), with the same overall dimensions throughout the cortex. Continuous, multilayered zone of small parenchyma cells encircles and separates tracheid xylem bundles from phloem. Departing leaf traces with xylem bundle are initially flattened, becoming crescent shaped, abaxially curved with abaxial protoxylem. Xylem bundle up to 2 mm wide in phloem zone decreases significantly to 200 mm. Intercellular spaces of >100 mm in diameter are common in the parenchyma (Plate III, 5 and 6). The smallest cells (10e20 mm diameter) occur in leaf bases, around the outgoing leaf traces (Plates I, 6 and III, 3e6), and in a continuous, darker narrow zone bounding the phloem that is interpreted as the inner cortex (ic, Plate I, 6 and 7). The inner cortex also has the highest concentration of fungal hyphae (Harper et al., 2018). Primary pit fields are common in medium-sized cortical cells. 6.1.1.2 The Chemnitz Fossil This Chemnitz specimen is slightly larger than the Munich fossil, with a stem diameter of 5.7  5.9 cm, and the cortex is up to 25 mm wide (Plate IV, 1). The excellent preservation permits recognition of several protruding leaf bases around the periphery of the stem; for one example, see Plate IV, arrow in 2; high magnification in 6. The leaf bases are approximately 3 mm wide, suggesting that the attached leaf or petiole was rather small compared with the overall stem diameter. Correspondences with the Munich specimen include the uniformity of the parenchymatous cortical tissue without zonation (Plate IV, 2) and medium-sized cells of >100 mm in diameter (Plate IV, 4 and 5). On the other hand, the cells of the inner cortex (Plate IV, 3) and leaf bases (Plate IV, 6) are variable in size and shape in the Chemnitz fossil.

6.1.2 Leaf Traces A maximum of 60 leaf traces are recognizable in the transverse section at the top portion of the Munich fossil (Plate III, 1), while there are up to 78 leaf traces in the Chemnitz fossil (Plate IV, 1). In both specimens, there is a similar leaf arrangement in sets of 5, 8, or 13 parastichies winding in opposite directions. This implies that leaves were in a 5/13 phyllotaxy. For example, leaf traces 19, 29, and 49 in the Munich fossil (illustrated in detail in Plate III, 4e6) belong to the same parastichy (of a set of five) as shown by the dashed line in Plate III, 1. Their comparison illustrates progressive modifications of the outgoing leaf traces. 6.1.2.1 Detail of Xylem and Phloem Leaf trace 15 within the phloem zone of the Munich fossil (circled in Plate III, 3; Fig. 11.3A,B) shows a flattened, elongate C-shaped xylem strand 1.2 mm wide and 400% in Gothania), the sacci probably do not play as significant a role in increasing the buoyancy force as do the other saccate grains. Based on its extremely small-predicted settling speeds (Table 13.2), Caytonanthus pollen grains will remain airborne much longer than the other fossil grains. This may have actually had an adverse impact on the grain, as it would increase the possibility of dehydration before

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reaching the ovulate organs. Its extremely small size may also limit the pollen grain’s ability to stay hydrated.

and necessary, in many cases, to understand complex paleobotanical systems, such as pollination biology.

4.3 Monoletes

ACKNOWLEDGMENTS

Monoletes was the largest pollen type of those investigated in this study. It was also the only nonsaccate grain. Whereas it is ellipsoidal in shape, the distal grooves represent a distinct geometric feature (Fig. 13.4). However, Monoletes was not tested with and without this feature to determine if the grooves might have a similar impact on settling speed as the geometric variations of Gothania had on that taxon’s settling speed. Overall, drag coefficient of the Monoletes grain type closely resembles that of a sphere, which would be expected given its principal axis ratios being closer to those of a sphere than the saccate models. The predicted settling speed of Monoletes was extremely large (Table 13.2); hence, the gravitational force due to its large mass would most likely dominate any aerodynamic effects on settling speed cause by variations in drag coefficient. As discussed in Schwendemann et al. (2007) and postulated by Niklas (1992), Monoletes was most likely gravity pollinated. Taylor and Millay (1979) also hypothesized that Monoletes could have been animal pollinated due to structural characteristics, which could have contained chemicals and thereby facilitate zoophily.

We are indebted to Thomas N. Taylor for his innovative and important work, his influential and leadership roles, his thoughtful mentorship, and his enduring friendship. He was passionate about paleobotany, creating new knowledge through research, and mentoring and training new generations of scientists. He frequently said that the best thing about paleobotany was the people. We feel privileged to have known him personally and worked closely with him for so many years or to be connected to him through his scholarly lineage. Tom continues to inspire us, and we miss him dearly. The authors also thank the Biology Department at The College of New Jersey (particularly Matthew Wund, Tracy Kress, Wendy Clement, and Keith Pecor) for use of their environmental chambers. This study was supported in part by the Council on Undergraduate Research Fellows Award to J.M.O and The College of New Jersey.

5. CONCLUSIONS This is the first study to experimentally demonstrate that grain geometry and the presence of sacci have an effect on the aerodynamics of fossil pollen. For all four saccate taxa studied, geometrical differences in overall pollen grain shape and differences in saccus size affected pollen drag. Modeling the fossil grains both with and without their sacci provided the opportunity to directly investigate the role of morphology, size, weight, and presence/absence of these structural bladders on aerodynamic efficiency. It is clear that having sacci yielded differences in the shape factor and drag coefficient, empirically demonstrating that sacci have an effect on the aerodynamics of pollen flight at the low Reynolds numbers associated with the fossil grains. Bisaccate grains of Pinus and Pteruchus had higher drag coefficients and remained airborne longer, and their sacci increased aerodynamic efficiency. In contrast, for the monosaccate grain of Gothania the saccus served to increase the grain’s settling speed due to subtle variations in geometric attributes. This increase was not predicted by the measured aerodynamic coefficients or by the published literature, demonstrating that low Reynolds number aerodynamics is still an evolving field of study. This study also provides further evidence that using a comprehensive, multidisciplinary approach is both valuable

REFERENCES Blackmore, S., Barnes, S.H., 1986. Harmomegathic mechanisms in pollen grains. In: Blackmore, S., Ferguson, I.K. (Eds.), Pollen and Spores: Form and Function. Academic Press, London, England, pp. 137e149. Clift, R., Grace, J.R., Weber, M.E., 1978. Bubbles, Drops, and Particles. Academic Press, New York. NY. Crane, P.R., 1986. Form and function in wind dispersed pollen. In: Blackmore, S., Ferguson, I.K. (Eds.), Pollen and Spores: Form and Function. Academic Press, London, England, pp. 179e202. Ehrlich, H.G., Hall, J.W., 1959. The ultrastructure of Eocene pollen. Grana Palynologica 2, 32e35. Fernández-Morán, H., Dahl, A.O., 1952. Electron microscopy of ultrathin frozen sections of pollen grains. Science 116, 465e467. Grega, L., Anderson, S., Cheetham, M., Clemente, M., Colletti, A., Moy, W., Talarico, D., Thatcher, S.L., Osborn, J.M., 2013. Aerodynamic characteristics of saccate pollen grains. International Journal of Plant Sciences 174, 499e510. Leslie, A.B., 2010. Flotation preferentially selects saccate pollen during conifer pollination. New Phytologist 188, 273e279. McNown, J.S., Malaika, J., 1950. Effects of particle shape on settling velocity at low Reynolds numbers. Transactions of the American Geophysical Union 31 (1), 74e82. Militzer, J., Kan, J.M., Hamdullahpur, F., Amyotte, P.R., Al Taweel, A.M., 1989. Drag coefficients for axisymmetric flow around individual spheroidal particles. Powder Technologies 57, 193e195. Niklas, K.J., 1981. Airflow patterns around some early seed plant ovules and cupules: Implications concerning efficiency in wind pollination. American Journal of Botany 68, 635e650. Niklas, K.J., 1983. The influence of Paleozoic ovule and cupule morphologies on wind pollination. Evolution 37, 968e986. Niklas, K.J., 1985. The aerodynamics of wind pollination. The Botanical Review 51, 328e386. Niklas, K.J., 1992. Plant Biomechanics: An Engineering Approach to Plant Form and Function. The University of Chicago Press, Chicago, IL. Osborn, J.M., 1994. The morphology and ultrastructure of Caytonanthus. Canadian Journal of Botany 72, 1519e1527.

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Osborn, J.M., 2007. Palynology In: McGraw-Hill Encyclopedia of Science and Technology, tenth ed., vol. 12. McGraw-Hill, New York, NY, pp. 762e766. Osborn, J.M., Taylor, M.L., 2010. Pollen and coprolite structure in Cycadeoidea (Bennettitales): Implications for understanding pollination and mating systems in Mesozoic cycadeoids. In: Gee, C.T. (Ed.), Plants in Deep Mesozoic Time: Morphological Innovations, Phylogeny, and Ecosystems. Indiana University Press, Bloomington, IN, pp. 34e49. Osborn, J.M., Taylor, T.N., 1993. Pollen morphology and ultrastructure of the Corystospermales: Permineralized in situ grains from the Triassic of Antarctica. Review of Palaeobotany and Palynology 79, 205e219. Osborn, J.M., Taylor, T.N., 1994. Comparative ultrastructure of fossil gymnosperm pollen and its phylogenetic implications. In: Kurmann, M.H., Doyle, J.A. (Eds.), Ultrastructure of Fossil Spores and Pollen. Royal Botanic Gardens, Kew, England, pp. 99e121. Phipps, C.J., Osborn, J.M., Stockey, R.A., 1995. Pinus pollen cones from the Middle Eocene Princeton Chert (Allenby formation) of British Columbia, Canada. International Journal of Plant Sciences 156, 117e124. Proctor, M., Yeo, P., Lack, A., 1996. The Natural History of Pollination. Timber Press, Portland, OR. Runions, C.J., Rensing, K.H., Takaso, T., Owens, J.N., 1999. Pollination of Picea orientalis (Pinaceae): Saccus morphology governs pollen buoyancy. American Journal of Botany 86, 190e197. Schwendemann, A.B., Wang, G., Mertz, M.L., McWilliams, R.T., Thatcher, S.L., Osborn, J.M., 2007. Aerodynamics of saccate pollen and its implications for wind pollination. American Journal of Botany 94, 1371e1381. Stokes, G.G., 1851. On the effect of the inertial friction of fluids on the motion of pendulums. Transactions of Cambridge Philosophical Society 9 (Part II), 8e106. Taylor, T.N., 1968. Application of the scanning electron microscope in paleobotany. Transactions of the American Microscopical Society 87, 510e515. Taylor, T.N., 1973. A consideration of the morphology, ultrastructure and multicellular microgametophytes of Cycadeoidea dacotensis pollen. Review of Palaeobotany and Palynology 16, 157e164. Taylor, T.N., 1976. The ultrastructure of Schopfipollenites: Orbicules and tapetal membranes. American Journal of Botany 63, 857e862. Taylor, T.N., 1978. The ultrastructure and reproductive significance of Monoletes (Pteridospermales) pollen. Canadian Journal of Botany 56, 3105e3118. Taylor, T.N., 1982. Ultrastructural studies of Paleozoic seed fern pollen: Sporoderm development. Review of Palaeobotany and Palynology 37, 29e53.

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Taylor, T.N., 1990. Microsporogenesis in fossil plants. In: Blackmore, S., Knox, R.B. (Eds.), Microspores: Evolution and Ontogeny. Academic Press, London, England, pp. 121e145. Taylor, T.N., Daghlian, C.P., 1980. The morphology and ultrastructure of Gothania (Cordaitales) pollen. Review of Palaeobotany and Palynology 29, 1e14. Taylor, T.N., Eggert, D.A., 1969. Studies of spores from Carboniferous fructifications. I. Introduction and preliminary survey utilizing the scanning electron microscope. Transactions of the American Microscopical Society 88, 431e444. Taylor, T.N., Millay, M.A., 1979. Pollination biology and reproduction in early seed plants. Review of Palaeobotany and Palynology 27, 329e355. Taylor, T.N., Rothwell, G.W., 1982. Studies of seed fern pollen: Development of the exine in Monoletes (Medullosales). American Journal of Botany 69, 570e578. Taylor, T.N., Osborn, J.M., Taylor, E.L., 1996. The importance of in situ pollen and spores in understanding the biology and evolution of fossil plants. In: Jansonius, J., McGregor, D.C. (Eds.), Palynology: Principles and Applications, vol. 1. American Association of Stratigraphic Palynologists Foundation, pp. 427e441. Taylor, T.N., Taylor, E.L., Krings, M., 2009. Paleobotany: The Biology and Evolution of Fossil Plants, second ed. Academic Press, Amsterdam. Thornhill, J.W., Matta, R.K., Wood, W.H., 1965. Examining threedimensional microstructures with the scanning electron microscope. Grana Palynologica 6, 3e6. Tomlinson, P.B., 1994. Functional morphology of saccate pollen in conifers with special reference to Podocarpaceae. International Journal of Plant Sciences 155, 699e715. Tomlinson, P.B., 2000. Structural features of saccate pollen types in relation to their function. In: Harley, M.M., Morton, C.M., Blackmore, S. (Eds.), Pollen and Spores: Morphology and Biology. England, Royal Botanical Gardens, Kew, pp. 147e162. Vogel, S., 1994. Life in Moving Fluids: The Physical Biology of Flow, second ed. Princeton University Press, Princeton, NJ. Wilson, L., Huang, T.C., 1979. The influence of shape on the atmospheric settling velocity of volcanic ash particles. Earth and Planetary Science Letters 44, 311e324. Wodehouse, R.P., 1935. Pollen Grains. Their Structure, Identification and Significance in Science and Medicine. McGraw-Hill Book Company, New York and London. Zavada, M.S., Taylor, T.N., 1986. The role of self-incompatibility as a mate choice mechanism in the gymnosperm-angiosperm transition: A hypothesis. American Naturalist 129, 538e550.

Chapter 14

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification, and the Environmental Distribution of Marattialean Ferns Through Time Gar W. Rothwell1, 2, Michael A. Millay3 and Ruth A. Stockey2 1

Ohio University, Athens, OH, United States; 2Oregon State University, Corvallis, OR, United States; 3Ohio University Southern, Ironton, OH,

United States

1. INTRODUCTION Marattialean ferns are homosporous pteridophytes distributed across tropical/subtropical wetlands worldwide (Campbell, 1911; Bower, 1926; Kramer and Green, 1990; Murdock, 2008a), with six genera and w60e110 species recognized in the most recent systematic treatment of the living taxa (Murdock, 2008a,b). Marattiales has one of the richest and best documented fossil records of all fern clades (Stewart and Rothwell, 1993; Millay, 1997; DiMichele and Phillips, 2002; Taylor et al., 2009), with Paleozoic taxa frequently assigned to the Psaroniaceae (Unger) sensu Herbst (1986) and crown group species comprising the Marattiaceae Kaulfuss (Seward, 1910; Hill and Camus, 1986; Murdock et al., 2006; Murdock, 2008a,b). Species of the Psaroniaceae were a major herbaceous element of the late Paleozoic, where they became the dominant canopy trees in many environments of the paleotropical wetlands during the Late Pennsylvanian and basal Permian (e.g., Corsin, 1951, 1960a,b; Dalinval, 1960; Millay, 1997; DiMichele and Phillips, 2002; Cleal, 2015). Unequivocal fossils of the Psaroniaceae appear first at about the MississippianePennsylvanian boundary (Williamson, 1876; Pfefferkorn, 1976; DiMichele and Phillips, 1977, 2002), are most common from the Middle Pennsylvanian through the basal Permian (i.e., Cleal, 2015), and are known to extend into the Triassic

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00014-0 Copyright © 2018 Elsevier Inc. All rights reserved.

(e.g., Delevoryas et al., 1992). Species of the Marattiaceae are recognized first in the Late Permian (e.g., Hill et al., 1985; Liu et al., 2001) and are a prominent vegetational component on several continents during the Triassic and Jurassic. Marattiaceous species become extremely rare by the Cretaceous and are virtually absent from the Cenozoic record of fossil plants (van Cittert, 1966; van Konijnenburg-van Cittert, 1975a,b; Hill and Camus, 1986; Hill, 1987; Millay, 1979; Collinson, 2001; Taylor et al., 2009). With the exception of the recently described Marattiopsis vodrazkae Kva
cek (2014) and unnamed linear synangia attached to thin laminar pinnules (Vera and Césari, 2016), all previous reports of marattialean species from post-Jurassic deposits are based on fossils of equivocal systematic affinities (e.g., Brown, 1934; MacGinitie, 1969; Palamarev et al., 1975; Hu et al., 2006) and have not been widely accepted by subsequent workers. Against this background, the recent discovery in Early Cretaceous deposits of radial to oval, anatomically preserved synangia with monolete spores, similar to those of the modern genus Christensenia Maxon (1905) emend. Rolleri (1993), initially led us to suspect that the Cretaceous fossils represent an extinct species of that marattiacean genus. However, serial sections of the fossil synangia reveal that the sporangia are longitudinally elongate and have free sporangial tips and a two-parted dehiscence

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mechanism that includes separation of the sporangial apices and longitudinal rupture of the sporangium. Such features are more characteristic of the Paleozoic Scolecopteris type of synangium (i.e., stem group Psaroniaceae) than of crown group Marattiaceae (Table 14.1; Millay, 1997; Murdock, 2008a,b). In the current contribution, we characterize and name the newly recognized Lower Cretaceous specimens as Escapia christensenioides Rothwell, Millay & Stockey gen. et sp. nov., define the families Psaroniaceae and Marattiaceae, and map their paleogeographic and paleoclimatic distributions through time to plot the evolutionary radiation of Marattiales. These Early Cretaceous fertile structures provide the first evidence that the family Psaroniaceae persisted into the Early Cretaceous. Geologically, E. christensenioides extends the stratigraphic range for the Psaroniaceae from the Triassic to the Cretaceous and represents the third youngest reliable record of Marattiales in the fossil record. Tabulation of paleontological occurrences for Marattiales through time reveals that species of the order have inhabited tropical and warm subtropical wetlands throughout the geological distribution of the clade. Species were most abundant on different continents during different segments of geological time, and the stem group Psaroniaceae coexisted with the crown group Marattiaceae into the Cretaceous.

2. MATERIAL AND METHODS Escapia christensenioides is represented by 10 synangia (Appendix 1), one of which is attached abaxially below a vein on a small pinnule fragment. Specimens are preserved by calcareous cellular permineralization in carbonate marine concretions derived from a carbonate-cemented graywacke matrix at the Apple Bay locality on northern Vancouver Island, British Columbia, Canada (Stockey et al., 2006). At this locality, the concretion-bearing sediments crop out on the beach along Quatsino Sound (50
360 2100 N, 127
390 2500 W; UTM 9U WG 951068) on northern Vancouver Island, British Columbia, Canada. Oxygen isotope analysis dates the sediments to c. 136 Ma (D. R. Gröcke, Durham University, UK, personal communication), which is in the Valanginian Stage of the Early Cretaceous (Cohen et al., 2013). Unexpectedly, the greatest similarities of the newly discovered Lower Cretaceous fossils are to Middle Pennsylvanian permineralized specimens of Scolecopteris alta Watson and S. altissima Mamay (Psaroniaceae), which are preserved in coal balls, including those from the Lewis Creek, KY, and Sahara No. 6 coal mine, IL, respectively (Millay, 1982). Therefore, the well-known cellulose acetate peel technique (Joy et al., 1956) was used to produce serial sections of both the Cretaceous and Pennsylvanian fossil

specimens. Microscope slides were prepared with Eukitt (O. Kindler GmbH, Freiburg, Germany) xylene-soluble mounting medium. Transmitted light images were captured using a Better Light digital scanning camera (Better Light Inc., Placerville, CA, USA). Scanning electron microscopy (SEM) of spores was imaged from peel sections coated with 100 Å Au on a JEOL 6301F SEM at 5 kV. All images were processed using Adobe Photoshop 7.0 (Adobe, San Jose, CA, USA). Specimens of Escapia christensenioides are deposited in the University of Alberta Paleobotanical Collections under their respective concretion numbers (viz., P13170; P13189; P13330C top; P13396; P13410; P13537; P13560A; P13732C top; P14628F top; P14693). Paleogeographic distributions of marattialean species were plotted on global paleoclimatic maps produced in the PALEOMAP Project (Scotese et al., 1999; Scotese, 2001, 2013; http://www.scotese.com/).

3. SYSTEMATIC PALEONTOLOGY 3.1 Systematics Order MARATTIALES Link, 1833 Family PSARONIACEAE Unger ex Endlicher (1842) emend. Herbst, 1986 (¼ Asterothecaceae Stur, 1883) Genus Escapia Rothwell, Millay & Stockey gen. nov.

3.1.1 Generic Diagnosis Pinnules with repeatedly dichotomizing veins, with round to oval, sessile synangia. Sporangia elongate, exannulate, surrounding a parenchymatous area in basal half; laterally confluent prior to dehiscence except at apex. Sporangial tips with small, solidly cellular extension. Sporangial cavities largest basally, tapering only slightly acropetally. Outer sporangial walls forming uniformly thick synangial wall; free portion of inner-facing sporangial walls thin, tapering to central midline. Dehiscence by sporangial separation in distal half of synangium and rupture of elongate cells occupying central midline of inner-facing sporangial walls. Spores bilateral, monolete, with thin, loose perispore.

3.1.2 Etymology The generic name Escapia is proposed to honor Dr. Ignacio Escapa, CONICET, Museo Paleontólogico Egidio Feruglio, Trelew, Argentina, for his reinterpretation of the extinct genus Marattiopsis, and his insights into marattialean evolution and phylogeny.

3.1.3 Type Species Escapia christensenioides Rothwell, Millay et Stockey, sp. nov.

TABLE 14.1 Diagnostic characters of the families Psaroniaceae and Marattiaceae Marattiaceaeb

Psaroniaceae and Marattiaceae

Stem

Upright, radial; polycyclic amphiphloic siphonostele with tabular (tangentially elongate) vascular strands or irregular and feebly polycyclic dictostele with irregular to rounded vascular strands; leaf traces monomeristelic or divide into polymeristelic; endodermis not evident

Creeping or upright, radial or bilateral; dictyostele of amphiphloic meristeles in one or more concentric rings; leaf traces polymeristelic; endodermis in stem and root of Marattia, Angiopteris, Christensenia, Danaea

Endarch metaxylem; endarch phloem

Roots

Naked (no root hairs known); root growth from stem outer vascular bundles, with cortical proliferation

Multicellular root hairs; root growth from stem inner vascular bundles, intrusive to stem cortex

Polyarch metaxylem; cortical parenchyma dense or aerenchymatous, peripheral or internal fiber cells

Histology

Sclerenchyma present in stem, leaf, and roots as a peripheral cortical boundary, interxylary bands or nests

Sclerenchyma absent from stem (Danaea may have sclereids in stem); opaline idioblasts

Tannin cells, mucilage cells, and lysigenous mucilage canals

Paraphyses uniseriate or branched; trichomes eglandular, glandular, capitate; tanniferous spines; scales basifixed, peltate, lobed, fimbriate; scales or trichomes may develop from basal hourglass cell

Trichomes/scales uni-bi-multiseriate; scales simple, basifixed or peltate; spines

Indument

Frond

Rachis/pinnae without stipules, stem buds or pulvini; frond division compound and pinnate, pinnule margins parallel and/or undulating, apices blunt; reticulate venation only at foliar margin if present; false veins absent

Rachis base with pair of thin or amylaceous stipules (modified pinna pair), lobed, fimbriate, with stem buds; rachis or pinnae with pulvini (node of modified pinna base or pinna pair) mechanical or not; pneumathodes, awls, lenticels; frond division simple, pedate or palmate; pinnule/blade margins entire, toothed, decurrent, tapering at base and apex; pinnae winged; reticulate venation; false veins; stomata anisocytic, cyclocytic, hexacytic, porocyclocytic

Fronds pinnate, veins simple, open dichotomous; hydathodes, pinnule/blade margins crisped; dichotomous foliar branching; stomata anomocytic

Sori and dehiscence

Sporangia elongate, tapering to pointed apex; sporangia crowded and fused to form functional synangium of radial or bilateral form; bilateral synangia not forming valves separating at maturity; sporangia separate on dehiscence causing rupture at thin area along inner midline

Sporangia squat with blunt apices; sporangia free, attached near base or completely fused; sporangia crowded or fused during development but dehisce independently; bilateral synangia may have valves that separate at maturity; sporangia rupture by local cell shrinkage along inner midline or at apex; sporangia may have functional annulus of thick-walled cells

Radial and bilateral synangia

Spores

100e9,000 spores per sporangium

1,450e7,500 spores per sporangium

Perispore present; perispore layer covers ornamentation or forms ornamentation

a

Characters modified from Mamay (1950), Morgan (1959), Ewart (1961), Stidd and Phillips (1968), Millay (1979, 1997), Millay and Taylor (1984), Mickle (1984), Herbst (1986), and Cleal (2015). Characters modified from Bower (1897), Farmer and Hill (1902), West (1915, 1917), Hill and Camus (1986), Mengascini and Rodriguez (2011), Rolleri et al. (1991, 2003, 2011), Murdock (2008b), and Christenhusz (2010).

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Psaroniaceaea

b

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3.1.4 Specific Diagnosis Pinnules are thin, with veins dichotomizing with helical and scalariform tracheids; transfusion tissue is between vein and sessile synangium. Synangia are round to oval in cross section, 0.9e1.0  0.9e1.8 mm in diameter w1.0 mm long. Synangia of seven to 12 sporangia are laterally attached except in the apical third; outer-facing sporangial wall is five or six cells thick, with some cells having frothy brown contents. Spores are reniform to ovoid, 16e23  13e15 mm; exine baculate with loose perispore; ornamentation units are 1.0 mm long and 0.5 mm wide.

3.1.5 Holotype Hic Designatus Synangium is oriented in cross section, with 11 sporangia containing spores, preserved in University of Alberta (UAPC-ALTA) concretion P13330C top (Figs. 14.1, 14.4, 14.14, 14.15, 14.18e22).

3.1.6 Paratypes Oval synangium is attached to a pinnule fragment in University of Alberta (UAPC-ALTA) concretion Pl3560A (Figs. 14.3, 14.7e12), and obliquely sectioned synangium has smooth-walled spores in University of Alberta (UAPCALTA) concretion P13396C top (Figs. 14.5, 14.13, 14.15).

3.1.7 Locality Coastal exposures in Quatsino Sound at Apple Bay on Vancouver Island, British Columbia, Canada (50
360 2100 N; 127
390 2500 W; UTM 9U WG 951068)

3.1.8 Stratigraphic Position and Age Longarm Formation Cretaceous.

equivalent,

Valanginian,

Early

3.1.9 Etymology The specific epithet christensenioides refers to the similarity of the synangia to those of extant Christensenia Maxon sensu Rolleri (2003).

3.2 Description Synangia range from circular (0.9e1.0 mm in cross section) to oval (0.9  1.8 mm in cross section), and consist of seven to 12 sporangia (Appendix 1; Figs. 14.1e4). No appropriate sections were available to accurately determine synangium length, but oblique sections reveal that component sporangia are at least 1.0 mm long. Synangia are sessile (Figs. 14.9e11) and broadly attached (Fig. 14.5, area between arrows), showing no evidence of indument at the base (Fig. 14.5). Oval synangia are oriented with their axes

parallel to the adjacent vein (Figs. 14.8e11). Sporangia are arranged around a parenchymatous core in the basal half of the synangium (Figs. 14.1 and 14), and surround a hollow central region distally (Figs. 14.4 and 14.6). Individual sporangia are elongate longitudinally (Fig. 14.5), are widest near the base, and taper above mid-level to a narrow tip extension (Figs. 14.4 and 14.6). For most of the length of the synangium, the outer wall is uniformly five to six cells thick (Figs. 14.1e5 and 14.13), consisting of parenchymatous cells that may have clear lumens or show internal contents of an amber-colored material and/or varying densities of black pyrite crystals (Figs. 14.1e5 and 14.13). The outer-facing wall thickness decreases to 3e4 cells near the level of foliar attachment (Fig. 14.5). Synangia have a surface layer of thin, uniformly-sized epidermal cells (Figs. 14.5 and 14.13). A small number of probable trichome bases also have been identified among epidermal cells of the outer synangial wall (Fig. 14.15, at arrow). Cells of the core of the synangium are polygonal and nearly isodiametric in cross sections. They measure 40e50 mm in diameter, with some appearing parenchymatous with uniformly thick walls (Figs. 14.2 and 14.3) and others having thicker walls only at the corners (Figs. 14.1 and 14.14). Cells toward the periphery of the core have prominent walls and become elongated radially as they extend between adjacent sporangial chambers as septa up to four cells thick (Figs. 14.1, 14.2, 14.5, and 14.14). The central parenchymatous area terminates at the midlevel of the synangium, above which sporangia surround a hollow center. Before dehiscence, sporangia maintain attachment until just proximal to their tips, which are free and curve inward (Figs. 14.4 and 14.6). Innerfacing sporangial walls are one cell thick (Fig. 14.4) and sometimes show remnants of a persistent tapetum. At maturity, sporangia separate laterally and dehisce via a longitudinal slit along the midline of the inner wall (Fig. 14.4). The opening extends from below the level of lateral separation (Fig. 14.4) to just below the solidly cellular sporangial tip (Fig. 14.6, at arrow). Proportions of a synangium with a parenchymatous core or hollow center, and with separate sporangial tips, have been interpreted from serial oblique sections of a specimen in which one sporangium is sectioned through the apex (Fig. 14.6). This sporangium is sectioned at the tip in peel #0 of the specimen (P14628F top). By peel #6 of the same series, the same sporangium (Fig. 14.6, at arrow) is sectioned at the base of the dehiscence slit. By peel #10, the central synangial area is almost all parenchyma, and by peel #30, the synangium base is evident. The open central area where sporangial dehiscence occurs is located in the distal third of the synangium. One specimen shows evidence of synangial attachment to the surface of a small pinnule fragment (Figs. 14.8e11). Cells of the pinnule lamina are incompletely preserved but

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FIGURES 14.1e7 Escapia christensenioides gen. et sp. nov. Fig. 1. Cross section of radially symmetrical synangium at midlevel. Note parenchymatous sporangial walls and central area of collenchyma-like tissue; epidermis compressed and abraded. Holotype P13330 C top #30 80. Scale bar ¼ 0.2 mm. Fig. 2. Cross section of bilaterally symmetrical synangium below midlevel. Thick-walled cells occupy center of synangium. Outer-facing walls compressed and abraded. P13560 A #16 70. Scale bar ¼ 0.2 mm. Fig. 3. Oblique cross section of synangium base just below sporangial cavities. Irregular surface contours appear to be natural. P13560 A #16 80. Scale bar ¼ 0.2 mm. Fig. 4. Oblique cross section of synangium near sporangial tips. Innerfacing sporangium walls opened along inner midline and sporangial tips separate (arrow). Holotype P13330 C top #1 90. Scale bar ¼ 0.2 mm. Fig. 5. Oblique longitudinal section of synangium parallel with long axis of oval synangium. Section passes through synangium center, at arrow. Sporangium bases in collenchyma-like tissue, with central zone of thick-walled cells. P13396 C top #2 53. Scale bar ¼ 0.2 mm. Fig. 6. Oblique section of synangium near apex showing three free sporangium tips (arrows) and spores. P14628 F top #2 105. Scale bar ¼ 0.2 mm. Fig. 7. Scalariform tracheids of vein in base of synangium. P13560 A #30 300. Scale bar ¼ 0.1 mm.

FIGURES 14.8e17 Escapia christensenioides gen. et sp. nov. Figs. 8e11, all 30. Scale bar ¼ 0.5 mm. Serial paradermal sections of pinnule lamina fragment in area of synangial attachment. All P15560 A. Fig. 8. Pinnule lamina (l) with branching veins. Note dark cell walls of bundle sheath cells. #30. Fig. 9. Slightly more abaxial level of pinnule lamina (l) with forking veins, and transfusion tissue (arrow) at base of synangium (at right). #27. Fig. 10. Still more abaxial level of pinnule fragment showing transfusion tissue (arrow) at level where margin of synangium base (red arrowheads) is visible. #21. Fig. 11. Most abaxial section of series, showing synangium base just distal to separation from pinnule lamina. #16. Fig. 12. Longitudinal section of small forking pinnule vein showing scalariform wall thickenings of tracheids, and dark walls of bundle sheath cells (bs). P15560 A #28 160. Scale bar ¼ 0.1 mm. Fig. 13. Oblique section of synangium wall in basal region, showing sporangial cavity with enclosed spores, two to three cell layers, and epidermis of small cells. Black cell contents consist of pyrite crystals. P13396 C top #15 135. Scale bar ¼ 0.1 mm. Fig. 14. Cross section of cellular central core near base of synangium, with multicellular septae between 11 sporangia. Note distinct cell walls near periphery of core, and cells with thickened corners at center. Holotype P13330 C top #15 180. Scale bar ¼ 0.1 mm. Fig. 15. Cross section at periphery of synangial wall showing internal cells, epidermis (at upper right), and possible trichome base (arrow). Holotype P13330 C top #3 240. Scale bar ¼ 0.1 mm. Fig. 16. Smoothwalled, bean-shaped spores from within sporangia. P13396 C top #14 700. Scale bar ¼ 20 mm. Fig. 17. Apparently more mature spores than those in Fig. 16, showing spiny exine and loose perispore. Several spores represented by perispore only. P14628 F top #2 700. Scale bar ¼ 20 mm.

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FIGURES 14.18e25 Spores. Figs. 18e22, SEM images of Escapia christensenioides gen. et sp. nov. Spores from Holotype P13330 C top #9. Fig. 18. Cluster of spores showing shape and sculpturing with perispore largely intact. 1,450. Scale bar ¼ 1 mm. Fig. 19. Spore with largely intact perispore and monolete suture at top. 3900. Scale bar ¼ 1 mm. Fig. 20. Spore with distal surface cut away, showing monolete suture from inside. 3200. Scale bar ¼ 1 mm. Fig. 21. Section view of spore wall showing exine with bacula (foreground) and perispore (background). 11,300. Scale bar ¼ 0.2 mm. Fig. 22. Surface of spore with intact perispore. 13,800. Scale bar ¼ 0.2 mm. Figs. 23e25. Light and SEM images of spores of Scolecopteris altissima from UICC 3552D. Fig. 23.Several reniform monolete spores. UICC #6677 1000. Scale bar ¼ 1 mm. Fig. 24. Single spore showing papillate ornamentation. UICC #6677 2600. Scale bar ¼ 1 mm. Fig. 25. SEM image of spore showing papillate surface somewhat obscured by perispore. UICC 3552D 3600. Scale bar ¼ 1 mm. SEM, scanning electron microscopy.

clearly show the thickness and extent of the tissue present (Figs. 14.8 and 14.9 at l). A series of successively more abaxial paradermal sections (Figs. 14.8e11) reveal a vein that dichotomizes three times at regular intervals, with a

synangium attached below one of the vein branches (Figs. 14.9e11). Each vein displays a narrow strand of tracheids with scalariform and reticulate secondary wall thickenings (Fig. 14.12). The strand is surrounded by a

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narrow zone of incompletely preserved cells and a prominent bundle sheath of elongated cells with dark walls (Figs. 14.8e10 and 14.12 at bs). This sequence of sections reveals that the synangium is sessile, relatively broadly attached, and vascularized by basal transfusion tracheids (Fig. 14.7) that underlie the vein (Figs. 14.9 and 14.10 at arrows and 14.11). Transfusion tracheids are short with fine scalariform secondary wall thickenings (Fig. 14.7). Six of the 10 available synangia have sporangia that contain spores (Appendix 1; Figs. 14.1e2 and 14.4e6). Some of the spore-containing sporangia have open dehiscence slits (e.g., Fig. 14.6, at left), and taken together, these sporangia suggest that the specimens have been preserved at varying stages of maturity. Spore morphology is reniform or ovate (Figs. 14.18 and 14.19) and monolete, and most spores have an exine ornamentation of papillae (Fig. 14.17) or bacula (Figs. 14.18e22). Ornamentation units measure 1.0 mm in height and 0.5 mm in diameter. Papillae observed with light microscopy resemble rounded mounds, while SEM observations reveal a more rod-like ornament of bacula with an uneven covering of perispore (Fig. 14.21). The perispore shows a microgranulate surface appearance at higher magnifications (Fig. 14.22). Spores from one specimen (P13396; Figs. 14.5 and 14.16) are in the same size range as other Escapia spores, but are psilate and appear to have thinner walls than the ornamented spores. These spores may be less mature than the highly ornamented specimens preserved in the other synangia.

3.3 Occurrences of Marattiales Through Time Possible Marattiales as ancient as the Lower Carboniferous have been described (Lesquereux, 1866; Crookall, 1955; Pfefferkorn, 1976). Surface impressions of tree trunks bearing large leaf scars in a helical or paired arrangement are suggestive of the psaroniaceous marattialean growth habit (Grand’Eury, 1877; Hirmer, 1927; Crookall, 1955; Morgan, 1959), but these fossils typically lack confirming evidence regarding sporangial characters, stem histology, root anatomy, and root mantle production (DiMichele and Phillips, 1977; Gerrienne et al., 1999). Therefore, with the exception of one Serpukhovian occurrence of the genus Megaphyton Artis from the Upper Mississippian of the Illinois Basin (Pfefferkorn, 1976), they are not represented by the occurrences of Marattiales that we include on paleogeographic/paleoclimatic maps through time (Figs. 14.32e37). Stronger diagnostic evidence for marattialean tree ferns from pre-Pennsylvanian age deposits consists of isolated radial synangia bearing spores with perispore (Burnitheca Meyer-Berthaud and Galtier, 1986) or the remains of a root mantle. However, considered separately, any of these fossils also could represent some

other clade such as a group of seed ferns, tree-sized ferns of other clades, or other tree fern-like plants (Galtier and Hueber, 2001; Soria and Meyer-Berthaud, 2004). The earliest confirmed occurrences of histologically preserved Marattiales are Psaronius simplicicaulis DiMichele and Phillips (1977) from the Lower Pennsylvanian of North America, Psaronius renaultii Williamson (1876) and Scolecopteris (Cyathotrachus) alta Watson (1906) from the Westphalian A of the United Kingdom. The description of Megaphyton in Upper Namurian deposits of Illinois (Pfefferkorn, 1976) may indicate the occurrence of marattialeans in the latest Mississippian, but that occurrence also is not confirmed by other marattiaceous fossils. Occurrences of these species and more recent fossil evidence for Marattiales (Appendix 2) have been plotted on global paleoclimatic maps developed in the PALEOMAP project (Scotese et al., 1999, 2013; Scotese, 2001) for the time interval of the Pennsylvanian through the Neogene (Figs. 14.32e37). These maps document the global distribution patterns and habitat tolerances of Marattiales through several time intervals and illustrate that marattialean taxa have inhabited tropical and wet subtropical environments throughout geological time. The most ancient distribution (Mississippian/Pennsylvanian) of the Marattiales clade lies within the equatorial tropics of western Pangaea (Fig. 14.32; i.e., the Euramerican region of the Equatorial Floristic Province sensu DiMichele et al., 2006). By the Late Pennsylvanian, marattialean species are dispersed across all of tropical Pangaea in both Euramerican and Cathaysian regions of the Equatorial Floristic Province. During most of the Permian (Figs. 14.33 and 14.34), marattialeans become more restricted but still thrive in the wet tropics of eastern Pangaea (i.e., Cathaysian region of the Equatorial Floristic Province). During the same time interval, the clade becomes dispersed throughout what appear to be subtropical, seasonally wet (DiMichele and Philips, 1996, 2002), and possibly even arid climates (i.e., river terrace floras?) throughout western Pangaea (Figs. 14.33 and 14.34). While most occurrences through time are within environments that are mapped as tropical and moist subtropical, some are plotted in more arid regions that are adjacent to the tropical or paratropical zones (Figs. 14.32e37). At the present time, we do not know if the occurrences of more arid environments represent wider tolerances of some marattialean species in the past (particularly during the mid- and Late Permian; Fig. 14.34), if those distributions represent local conditions that are modified by adjacent marine or fluvial influences (Escapa et al., 2014) and/or if further refinement of paleoclimatic maps will bring all of the distributions into the moist tropical and subtropical habitats that are populated by living species (Christenhusz, 2007; Murdock, 2008a).

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FIGURES 14.26e31 Paleozoic synangia of the Scolecopteris alta group. Fig. 26. Scolecopteris alta synangium in median longitudinal section (at right), and synangium in oblique transverse section through five sporangial tips (at left). Sporangial cavities end abruptly with outer wall extending into acute tips. OSU no.7952. 1564 H1top, No. 423 series 3 90. Scale bar ¼ 0.2 mm. Figs. 27e29 and 31. Scolecopteris altissima. Fig. 27. Decurrent pinnules and synangia in cross section. Note pinnule midveins (mv) and two lateral veins (l). UICC #6666. 3116B bot #70. 72. Scale bar ¼ 0.2 mm. Fig. 28. Oblique transverse section of synangial apex. Two sporangial tips at right show small sporangial cavity or solid tip distal to cavity. UICC 1111A bot. 150. Scale bar ¼ 0.1 mm. Fig. 29. Synangium in median longitudinal section. Note remains of pedicel, and solid sporangium tip, at arrow. UICC 3687A5 bot #48. 65. Scale bar ¼ 0.2 mm. Fig. 30. Scolecopteris alta. Synangium base in cross section showing central cellular area. OSU 1564 H1top #444 ser. 3 130. Scale bar ¼ 0.1 mm. Fig. 31. Scolecopteris altissima synangium midlevel in cross section, showing hollow central area surrounded by sporangia. WU no. 1692. 130. Scale bar ¼ 0.1 mm.

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FIGURE 14.32 Geological history of Marattialean ferns plotted on paleogeographic/paleoclimatic maps from the Paleomap Project (Scotese, 2001) showing distributions through time. Boundaries of tropical zones slightly modified and extrapolated at lateral margins. Tropical regions shaded in green. Occurrences of taxa plotted from literature cited for each time segment, and reflect wider geological time span than identified by each map. Some occurrences in warm temperate and arid regions may reflect oceanic influences that moderate climate (Escapa et al., 2014). Some occurrences omitted from dense clusters of localities for clarity. Environmental tolerances of living marattialean species suggest additional refinement of boundaries for climatic zones may be needed. Fig. 32. Oldest conclusive occurrences of Marattiales in Lower Pennsylvanian (Bashkirian; 323e315 Ma) on map modified from Scotese (2001) for BashkirianeMoscovian.

FIGURE 14.33 Middle PennsylvanianeEarly Permian Marattiales (MoscovianeSakmarian; 315e283 Ma) on map modified from Scotese (map 12_295; Scotese, 2001) for Gzelian.

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FIGURE 14.34 Mid PermianeEnd Permian Marattiales (ArtinskianeChanghsingian; 251e183 Ma) on map modified from Scotese (map 14_260; Scotese, 2001) for Lower Triassic.

During the Triassic and Jurassic periods, marattialeans continue to be well represented in the equatorial tropics of what had previously been eastern Pangaea (Figs. 14.35 and 14.36), but are distributed at lower frequencies in warm temperate climates of both the Northern and Southern Hemispheres (Figs. 14.35 and 14.36). The paucity of marattialean fossil remains from what is now North America originates in the Permian (Fig. 14.34) and continues throughout the rest of the Mesozoic and Cenozoic fossil record (Figs. 14.35e37). During the Cretaceous and Cenozoic, there are only three convincing occurrences of Marattiales (Fig. 14.37): one from an exotic terrain on the west coast of North America (this report) and two from the Antarctic Peninsula (Kva
cek, 2014; Vera and Césari, 2016). Interestingly, all three are from what appear to be marine-influenced habitats of warm temperate climates in the Western Hemisphere (Fig. 14.37).

4. DISCUSSION 4.1 Relationships of Escapia christensenioides Compared with extant genera of Marattiaceae, the synangia of E. christensenioides are most similar to those of Christensenia spp. Both have a relatively large number of sporangia (Escapia, 7e12; Christensenia, 8e12) arranged

in a cup-like structure (Rolleri, 1993) and a parenchymatous histology of the synangial walls (illustrated by Luerssen, 1875). Synangia in both genera have a developmental plasticity permitting radial forms to become oval and elongated parallel to the underlying vein. However, Christensenia synangia have a narrow dome-shaped attachment area with the pinna surface (“receptacle” of Rolleri, 1993) and can be shed from the plant, whereas Escapia synangia have a broad sessile attachment. In the extant Marattiaceae, a nest of thin-walled trichomes or paraphyses is usually produced around the base of superficial synangia (Campbell, 1911; Hill and Camus, 1986; Murdock, 2008b). Such paraphyses are present around the base of Christensenia synangia but are absent from the base of Escapia synangia, although a few trichomes appear to be present on the synangial surface. Most importantly, sporangia of Christensenia are completely fused, whereas Escapia sporangia have free tips that separate laterally during dehiscence. Due to the shallow contours of the synangial apex in Christensenia, sporangia have little space for internal vertical dehiscence, and the slits are horizontally oriented at the apices of sporangia. In contrast, the dehiscence slits of E. christensenioides are vertically oriented toward the interior of the synangium. The cause of the rupture of the sporangial tips is summarized by Bower (1897, p. 47) for Christensenia (¼Kaulfussia): “The outer wall of the sporangia retains its

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FIGURE 14.35 Triassic Marattiales (InduaneRhaetian; 252e201 Ma) on map modified from Scotese (map 17_210; Scotese, 2001) for Upper Triassic.

FIGURE 14.36 Jurassic Marattiales (HettanianeTithonian; 201e145 Ma) on map modified from Scotese (map Lower Jurassic-180; Scotese, 2001) for Lower Jurassic.

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FIGURE 14.37 Cretaceous e Pleistocene Marattiales (BerriasianeUpper Pleistocene; 145e0.2 Ma) on map modified from Scotese (map Lower Cretaceous-120; Scotese, 2001) for Lower Cretaceous.

bulky character up to the period of dehiscence, and there is no specially indurated superficial layer. The dehiscence is by a narrow slit, which opens by shrinking of the adjoining cells; there is no annulus.” More specifically, he writes, “Very shortly after the stage shown in Fig. 39, the growth of the tissue above the sterile septa becomes more active than that above the sporangia, and the result is the formation of a narrow slit-like depression (Fig. 40); but as is shown by Figs. 35, 36, and 41, this extends only for a short distance in a radial direction, while its position is upon the oblique inner rim of the sorus. It is upon the base of this slit that the rupture takes place at maturity, the cells adjoining it, both below and laterally, dry up, and the result is that the pore gapes open in much the same way as that described for Danaea” (Bower, 1897, p. 45). Among all genera of the Marattiales through time, Escapia is most similar to species in the Alta Group of Scolecopteris Zenker of the Psaroniaceae (Millay, 1982). Watson (1906) established Cyathotrachus altus for wellvascularized cup-shaped synangia with small ovoid spores, and Mamay (1950) distinguished his species C. altissimus based on its larger synangium size. Millay (1982) transferred Cyathotrachus to Scolecopteris based only on synangium morphology, which did not adequately consider all of the characters available. Additional species of the Alta Group also share with E. christensenioides distinctive foliar and spore characters (Millay, 1982;

Figs. 14.26e31 and 14.23e25; Jennings and Millay, 1978; Millay and Galtier, 1990). Important characters include thin, flat foliage bearing cup-like synangia (Fig. 14.27) that have a parenchymatous wall structure (Figs. 14.28 and 14.30) and small, monolete, oval to reniform spores (Figs. 14.23e25). In two species, S. alta (Watson) Millay and S. globiforma Millay & Galtier, the central void of the synangium is enclosed by extensions of the sporangial tips (Fig. 14.26), but other species (e.g., S. altissima [Mamay] Millay and S. unita [¼Ptychocarpus unita of Renault] Jennings & Millay) show small cellular extensions around an otherwise open cup (Fig. 14.29). The increased surface area available on the central cellular area in the synangial base makes possible the relatively large number of sporangia in S. altissima (5e9; Fig. 14.31) and Escapia (7e12; Figs. 14.18e19) and limits spore release to the distal third to half of each sporangium (Millay, 1982). A major difference between the Paleozoic and Cretaceous fossils is the vascularized pedicel (0.2e0.5 mm long) in S. altissima, which is absent from synangia of Escapia. Instead, Escapia synangia have transfusion tissue between the pinnule vein and the broad sessile attachment of the synangium (approximately four-fifths of synangium diameter). Walls of the synangium can be two or three cells thick in species of the Alta Group of Scolecopteris, whereas outer-facing sporangial walls in Escapia are five cells thick, about the same as most extant marattialean ferns with

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exposed superficial synangia (Luerssen, 1874, 1875; Hill and Camus, 1986). As currently understood, synangial structure clearly places the genus Escapia within the Psaroniaceae (Table 14.1), and spore morphology is consistent with the Alta Group of Scolecopteris.

4.2 Characterization of the Families Psaroniaceae and Marattiaceae The late Paleozoic has yielded abundant compressed and anatomically preserved specimens of all organs of the Marattiales (e.g., Grand’Eury, 1877; Kidston, 1923e1925; Corsin, 1951; Dalinval, 1960; Mickle, 1984; Morgan, 1959; Phillips, 1980; Li and Cui, 1995), and almost all of these fossils are easily assignable to the Psaroniaceae. Although very incompletely understood as individual species of whole plants, psaroniaceous fossils do provide a reliable sampling of character variation within the family (Table 14.1). Traits that we consider to be diagnostic for the Psaroniaceae are found in the stem, frond, root mantle, and synangium. These include (1) stem tissues externally limited by a cylinder of sclerenchyma dissected only by leaf trace departure, (2) highly dissected fronds with small pinnules and rachides that lack both stipules and pulvini, (3) root mantle production, and (4) synangia with exannulate sporangia that separate as a part of spore release (Table 14.1). This family concept rests partially on the conspecificity of disarticulated, anatomically preserved stems and fertile leaves found together in geological strata or the rock matrix (Barthel, 1976; Tavares et al., 2014) but is primarily supported by a comparison of cell types, tissue organization, and distinctive indument (Stidd, 1971; Millay, 1979). The most extensive examples of tissuee organ matching are the holomorph assemblages of Lesnikowska (1989) that connect Scolecopteris species with psaronii based on locality co-occurrence and tissue composition. There are rare examples of pecopterid foliage found attached to stems assignable to Caulopteris and Psaronius (e.g., Renault and Zeiller, 1888e1890; Stidd, 1967). This confirms that marattialean organs from Pennsylvanian and basal Permian strata (Phillips, 1980) represent dispersed parts of the same plant family (i.e., Psaroniaceae). Character variation present among extant genera of the Marattiaceae (Table 14.1) has been clarified by morphological studies of Angiopteris (Hill and Camus, 1986; Mengascini, 2002; Rolleri, 2002), Archangiopteris (Mengascini, 2002), Christensenia (Luerssen, 1875; Rolleri, 1993; Rolleri et al., 1996), Danaea (Christenhusz et al., 2008), Eupodium (Christenhusz, 2010), Marattia (Luerssen, 1874; Hill and Camus, 1986; Lavalle, 2003; Lavalle et al., 2011), and Ptisana (Murdock, 2008b), as well as by systematic studies of the family as a whole (Hill and Camus,

1986; Liu et al., 2000; Rolleri et al., 2003; Christenhusz et al., 2008; Murdock, 2008a,b; Senterre et al., 2014). Features that characterize extant Marattiaceae include both plesiomorphous characters, also present in fossil taxa, and derived characters that distinguish crown group taxa and the family itself (Stidd, 1974; Hill and Camus, 1986; Murdock, 2008a,b). The combination of our study of the anatomically preserved synangia of E. christensenioides and our characterization of the families Psaroniaceae and Marattiaceae prompted us to revisit questions about (1) which characters adequately define the Marattiaceae, (2) to which family the late Paleozoic and Mesozoic genera of Marattiales belong, and (3) from which stem group or stem groups the extant species originated. The last two questions are addressed in a comprehensive phylogenetic analysis of Marattiales, which will appear elsewhere. Relative to the relationships of Escapia, crown group species traditionally have been considered to be descended from at least two Paleozoic synangial morphologies: the elongate bilateral form of Eoangiopteris (Mamay, 1950; Millay, 1978) and Millaya (Mapes and Schabilion, 1979) and the more common radial types such as Scolecopteris Zenker (Millay, 1979) and Acitheca Schimper (Zodrow et al., 2006). Functional synangia of both forms are composed of sporangia that (1) laterally separate as part of dehiscence and then (2) rupture along the inner sporangium midline (Mamay, 1950; Millay, 1979). Cells of the inner sporangial walls are obliquely oriented to the line of dehiscence in Scolecopteris (Millay, 1979), which suggests to us the leveraged transfer of an oblique pull on the suture related to dorsal sporangial wall contraction by cell shrinkage. The two events almost certainly are mechanically related, although the outer sporangial wall structure does not reveal the causal mechanism (e.g., laminar collenchyma). In radial synangia, the inner sporangial walls are appressed or enclose a central hollow before dehiscence, and spore release cannot occur without sporangium disengagement. Observations have shown that appressed sporangia contain spores, whereas separated sporangia are partially or completely empty (Millay, 1979). This method of spore release is considered here to be one of the defining characters of the family Psaroniaceae. Synangia of Escapia have the two-parted spore release of the Psaroniaceae (Figs. 14.4, 14.6), demonstrating that in radial forms this dehiscence mechanism persisted into the Early Cretaceous. By contrast, in the extant genera of Marattiaceae, sporangia may be separate but crowded at maturity (i.e., Archangiopteris sensu Mengascini, 2002), may be not crowded and have dehiscence aided by an annulus-like structure (e.g., Angiopteris: Sporne, 1962; Hill and Camus, 1986), or may have complete sporangial fusion with dehiscence accomplished by local cell shrinkage (e.g., Christensenia and Danaea: Luerssen, 1875; Bower,

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1897; Campbell, 1911). In the bivalved synangia of Eupodium, Marattia, and Ptisana, sporangial dehiscence involves local cell shrinkage along the midline of the sporangium after the two valves separate (Luerssen, 1875; Hill and Camus, 1986; Murdock, 2008a). Cells of the inner sporangial wall are oriented parallel to the line of dehiscence (Hill and Camus, 1986), and this trait is correlated with the stationary sporangial position. Synangial structure has traditionally been the primary feature used to define genera or groups of genera at the family level (e.g., Angiopteridaceae, Christenseniaceae, Danaeaceae, Marattiaceae [Reimers, 1954; Ching, 1958, 1999; Devi, 1981; Doweld, 2001]). We suggest that whatever the degree of sporangial fusion, the dehiscence mechanism is essentially equivalent in all extant Marattiaceae: the synangium as an organ to effect dehiscence is vestigial because the sporangia open without having to separate from each other. We consider this to be one of the defining characters of the Marattiaceae. Another diagnostic feature of extant members of the Marattiaceae is a distinctive frond type with paired stipules at the base of the rachis and swollen collenchymatous pulvini on the rachis or pinnae. Both features are interpreted as having arisen by modifications of pinnae at a rachial node or from branching of the frond (Campbell, 1911; Hill and Camus, 1986). Stipules may be thin and papery or amylaceous in nature and function in protecting the emerging crozier (Hill and Camus, 1986). The pulvini may allow a frond segment to relax or orient to sunlight (Chang, 1975) or separate without damage to the stem (Holttum, 1978). Ptisana pinnule bases exhibit an abscission zone (a notch or suture) that facilitates pinnule separation (Murdock, 2008b). None of the more completely known psaroniaceous compression/impression foliage forms from the Paleozoic (i.e., Acitheca Schimper sensu Zodrow et al.; Asterotheca Presl in Corda emend. Cleal; Crenulopteris Bell sensu Wittry et al.; Cyathocarpus Weiss emend. Cleal; Diplazites Goppert emend. Cleal; Lobatopteris Wagner emend. Cleal; Polymorphopteris Wagner emend. Cleal; Remia Knight emend. Cleal) have been demonstrated to have sutures, pulvini, or stipules (Wagner, 1959; Knight, 1985; Zodrow et al., 2006; Wittry et al., 2014; Cleal, 2015). Otherwise, these marattialean foliage types bear synangia with the spore type and high spore number per sporangium that support their assignment to the Marattiales (Cleal, 2015).

4.3 Aphlebia, Stipules, and Pulvini in Eusporangiate Ferns and Fern-Like Plants Some early fern groups such as the Zygopteridales and Stauropteridales had paired laminar segments (aphlebia) at the base of rachides and pinnae (i.e., aphlebia: Dennis, 1974; Phillips and Galtier, 2005; Farahimanesh et al.,

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2014), but such structures appear to have multiple parallel origins and are nonhomologous with the stipules of marattialean ferns (Rothwell and Stockey, 2008). Stipules and pulvini are considered here to be a diagnostic feature of the Marattiaceae but are currently unknown from their fossil record. However, based on field experiments, Hill (1987) presents the possibility that the soft tissues of pulvini easily decomposed in most depositional environments, causing pinnae to become separated. Alternatively, Hill (1987) suggested that once separated from the stem, frond pulvini may have shrunken before fossilization and not be recognizable as such.

4.4 Stratigraphic Range of the Family Psaroniaceae Throughout the Pennsylvanian and much of the Permian, fossil remains of the Marattiales are all assignable to the Psaroniaceae, with the first well-documented occurrence of the Marattiaceae occurring in the Late Permian (e.g., Hill et al., 1985; Liu et al., 2001). The Psaroniaceae remain the most common representatives of the Marattiales until the Early Triassic, where more modern-appearing forms such as Danaeites and Danaeopsis begin to predominate (e.g., Herbst, 1977a,b; Tidwell and Ash, 1994; Liu et al., 2001; Kustatscher and van Konijnenburg-van Cittert, 2011; Pott, 2014). The occurrence of anatomically preserved fertile pinnules of Scolecopteris antarctica (Delevoryas et al., 1992) in the early Middle Triassic of Antarctica demonstrates that this psaroniaceous synangium type continued into the Mesozoic. The presence of wall thickenings termed “buttresses” on the inner surfaces of cells in the outer sporangial walls of S. antarctica suggests a possible role in aiding dehiscence. Buttresses are not currently known to be present in other psaroniaceous genera, but possibly similar wall thickenings are illustrated in the synangial wall of Marattia costulisoria Alston by Hill and Camus (1986, Fig. 14.17B). The morphology of S. antarctica pinnules is distinctive, with pinnule margins acutely reflexed abaxially toward the midrib and synangia held parallel to and enclosed between the two surfaces. The same foliar organization is present in Permian specimens of Dizeugotheca (Archangelsky and de la Sota, 1960) and Gemellitheca saudica (Wagner et al., 1985). An important part of the Late Permian and Triassic fossil record of marattialean ferns consists of compression fossils of unmodified foliage on which radial synangia appear as star-shaped sori after dehiscence. This compression/impression form was placed in the genus Asterotheca Presl in Corda (1845) of the family Psaroniaceae. Cleal (2015) has emended Asterotheca to include features of the frond architecture, pinnule venation, synangium form, and

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spore morphology, so the species attributed in the past to this morphotaxon form a more natural phylogenetic group. Fossils of the general Asterotheca type have been documented throughout the Triassic (Herbst, 1977a,b; Tidwell and Ash, 1994; Kustatscher and van Konijnenburg-van Cittert, 2011; Pott, 2014). However, Cleal (2015, p. 6) questions the assignment of these species to the Carboniferous form of Asterotheca because, although they have pecopterid pinnules and radially stellate sori, “they do not display the same type of large, bulbous sporangia as the type species of Asterotheca. Moreover, where in situ spores have been found in such sori, they are monolete or pseudomonolete, rather than trilete like many of the Paleozoic species of Asterotheca. The generic position of these Triassic species clearly needs to be revised,” but their assignment to the Psaroniaceae appears to be accurate.

4.5 Arrival of the Family Marattiaceae Throughout the Pennsylvanian and Permian periods, the vast majority of marattialean fossils are clearly assignable to the Psaroniaceae, but well-preserved compression fossils found in Late Permian sediments reveal that the Marattiaceae originated before the end of the Paleozoic (e.g., Hill et al., 1985; Liu et al., 2001). Generic delineation in fossil Marattiales relies heavily on synangial characters because of the plesiomorphous foliar morphology and homogeneous anatomy of the family in the Pennsylvanian. In the Permian, a different marattialean frond type appears; one that is fewer times pinnate and appears stout because the rachis and pinna midrib are broad, with elongate tapering pinnules. A significant example of this foliage type from the Late Permian of Saudi Arabia consists of both sterile and fertile specimens assignable to the Marattiaceae (Qasimia: Hill et al., 1985). Qasimia synangia are constructed of two parallel rows of laterally fused sporangia that extend laterally from the midvein to the pinnule margin. Individual sporangial tips are fused along a continuous curving suture line to form symmetrical, laterally elongate, bivalved synangia. Synangia are oriented perpendicular to the abaxial pinnule surface and, except for their lateral extent, resemble the deeply cut bivalved synangia of the extant marattialean genus Ptisana (Murdock, 2008b). The assignment of Qasimia to Marattiaceae by Hill et al. (1985) is based on both the synangial morphology and the resemblance of its foliage to Jurassic marattialeans such as Marattia asiatica Kawasaki and Marattia anglica (Thomas) Harris. There are currently no other examples of the bivalved Qasimia type of synangium known before these two Jurassic examples of Marattia. Permian specimens of Danaeites rigida Liu et al. (2001) approach this condition, but individual sporangial tips appear to separate in those synangia.

Marattialean stems are known from throughout the Permian, differing by variations in phyllotaxis, distribution of stem sclerenchyma, and the configuration of the foliar vascular strands in cross section (Corda, 1845; He et al., 2010, 2013; Herbst, 1985, 1986, 1987, 1992; Mickle, 1984; Ogura, 1972; Tavares et al., 2011; Tian et al., 1992). The Gondwana flora of the South American Craton includes three marattialean fern stems, Psaronius, Tietea SolmsLaubach sensu Herbst, and Tuvichapteris Herbst, which are similar in basic organization but show varying degrees of dissection of the internal cauline vascular strands and leaf traces (Herbst, 1986, 1987, 1992; Tavares et al., 2011). Pennsylvanian Psaronius stems usually have a regular organization of the internal vascular cycles, but some Permian examples (P. arrojadoi [Pelourde] Herbst, P. braziliensis Brongniart) have a central area of apparently disorganized vascular strands, including closed circles. In Tietea stems, most of the internal xylem strands show no organization into cycles or “polycyclic rings” except the outermost cycle. Leaf trace formation in the outer cycle is like that of Psaronius. In Tuvichapteris stems, there are no cycles apparent among the meristeles, and the emergent leaf trace is composed of several meristeles. These variations in vascular anatomy are illustrative of what might be expected during a transition from Psaroniaceae to Marattiaceae (Table 14.1). The cause of the increased vascular dissection exhibited by Tietea and Tuvichapteris stems is suggested to be related to water stress in a wetedry seasonal climate (Tavares et al., 2011) or an adaptation to the dryer climate that accompanies the long interglacial periods. Mettenius (1864) mentions an Angiopteris that exhibited decreased vascular dissection while in an unfavorable cultivation situation.

4.6 Floristic Turnover of Psaroniaceae to Marattiaceae There is no dramatic change in the marattialean flora at the CarboniferousePermian boundary. However, there is a significant shift from humid ever-wet to less humid and semiarid/arid floras at that time (DiMichele et al., 2005; DiMichele, 2006), such that the most common Pennsylvanian marattialeans were progressively replaced by other taxa in successively more recent Lower Permian assemblages. Psaroniaceous fossils become more common in apparently non-swamp deposits, suggesting a widening of ecological tolerances (Fig. 14.34; van Waveren et al., 2007). Compression/impression foliage of marattialean (i.e., Psaroniaceae) affinity is found throughout the Pennsylvanian and extends into the Lower Permian. These foliage forms have traditionally been assigned to the genus Pecopteris if vegetative, but the type species of that genus does not represent a marattialean fern. As a result, the

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recognized marattialean species of these foliage forms have been segregated into several distinct genera based on additional characters of the fertile pinnules (see Cleal, 2015, for a detailed explanation of this topic). Marattialean compression/impression “pecopterid” species represent the fossil plants Acitheca Schimper sensu Zodrow et al., Crenulopteris Wittry et al., Cyathocarpus Weiss emend. Cleal, Diplazites Göppert emend. Cleal, Lobatopteris Wagner emend. Cleal, Polymorphopteris Wagner emend. Cleal, and Remia Knight emend. Cleal. These plants become much less common after the Sakmarian Epoch of the Lower Permian, and new genera appear: Asterotheca non Cleal; Bifarusotheca Zhao, Zuangguan, Shanzhen & Zhahaogi; Convexocarpus Naugolnykh; Danaeites (Göppert) Stur; Dizeugotheca Archangelsky & la Sota; Fimbriotheca Zhu & Chen; Pectinangium Li, Deng, Zhou, Xu & Zhu sensu Wan and Basinger; Qasimia Hill, Wagner & El-Khayal; and Rajahia Kon’no. These genera are based on compression/impression specimens that have allowed for sufficiently detailed descriptions and illustrations of the fossil remains. At the beginning of the Triassic there is a dramatic reversal in familial affinities of marattialean fossils such that the majority of them conform to the Marattiaceae (Fig. 14.35; e.g., Kimura and Tsujii, 1980; Hill, 1987; Wang, 1999; Yang et al., 2008; Kustatscher and van Konijnenburg-van Cittert, 2011; Kustatscher et al., 2012; Escapa et al., 2014). In contrast to the frequent occurrence of both anatomically preserved and compression fossils of Marattiales from the late Paleozoic, Mesozoic species are represented primarily by compressed fragments of vegetative and fertile fronds. There are numerous reports and descriptions of such fossils from Triassic and Jurassic strata worldwide (e.g., Hill et al., 1985; Hill, 1987; Wang, 1999; Liu et al., 2001; Yang et al., 2008; Kustatscher et al., 2012; Escapa et al., 2014) revealing that marattialeans played an important role (or were at least present) in many plant communities. Because of the type of fossil record available, characterization of Mesozoic marattialeans has focused on the morphology of pinnules and synangia and, to a lesser extent, on cuticles and/or spores. Mesozoic marattiaceous species frequently have been assigned either to modern genera (e.g., Marattia asiatica [Kawasaki] Harris, 1961; Kimura and Tsujii, 1980; Wang, 1999; Angiopteris blackii [van Konijnenburg-van Cittert] Hill, 1987) or to extinct genera that may be morphologically similar to the modern genera (e.g., Marattiopsis sensu Bomfleur et al., 2013; Escapa et al., 2014; Kva
cek, 2014; Danaeopsis Heer ex Schimper, nom. conserv. Zijlstra, Kustatscher and van Konijnenburg-van Cittert, 2010). If the form of the fossil synangium is similar to Marattia,

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Danaea, or Angiopteris, the remains are most often compared only with members of the Marattiaceae. Our compilation of characters that typify the Marattiaceae (Table 14.1) expands on those identified by Herbst (1986) and includes stems with polycyclic dictyosteles composed of meristeles, fronds with stipules and pulvini, and sporangial dehiscence by local cell shrinkage or, in some taxa, with the aid of an annulus.

4.7 Paleoecology of the Psaroniaceae Marattialean ferns are a common component of the “everwet” Pangaean coal swamp floras of the Middle Pennsylvanian. In Euramerican peat swamps, they compose about 10%e20% of the peat biomass when averaged across the whole peat landscape (DiMichele and Phillips, 2002). The vegetative pinnules of many species possess hydathodes that make water loss possible in the high humidity of the everwet swamp environment (Scott and Holden, 1933; Lesnikowska and Galtier, 1992). Psaronius plants probably occupied both understory and forest canopy positions, because small trunks of several types have been discovered, including one that may lack a root mantle (Lesnikowska, 1989). Clear evidence of the presence of small marattialeans is the tiny fertile frond of Araiangium that bears naked superficial synangia on flat pinnules still in the crozier stage of development (Millay, 1977). Other examples are found in the Alta Group of Scolecopteris (i.e., S. alta Watson, S. altissima Mamay, S. globiforma Millay and Galtier, S. nigra Millay, S. unita Renault), which is characterized by delicate flat foliage carrying uniformly thin-walled synangia on the lower pinnule surface. This combination suggests both a sheltered growth habit (location) and a chemical form of herbivore repellant such as the mucilage and tannin cells they exhibit. Coprolites composed entirely of spores are common in coal balls (Labandeira, 2002), so protection from herbivory is a valid adaptational consideration. Both compression/impression and anatomically preserved marattialean fossil foliage are commonly dimorphic, with the fertile pinnules modified to protect the sori from moisture loss. Xeric foliar modifications have been discussed primarily for marattialean fossils found in sediments that suggest preservation in a dry tropical or seasonal dry climate (e.g., Tavares et al., 2014). For coal swamp marattialeans, Millay (1979) suggested that the abundant abaxial trichomes and fibrous, downturned, pinnule laminae in the Latifolia Group of Scolecopteris (S. calicifolia Millay, S. fragilis Millay, S. latifolia Graham, S. mamayi Millay, S. monothrix Ewart, S. parkerensis Lesnikowska and Willard, S. vallumii Millay) functioned to protect the synangia from dehydration during development or from animal predation. These features also suggest that

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Latifolia Group species occupied the wetland forest canopy, where their modified foliage may have addressed hydric stress from direct solar exposure. Other foliar traits exhibited by marattialeans that are associated with seasonal or dry environments are also present in some classic peat swamp species of Scolecopteris. The stout in-rolled fibrous pinnule margins of Scolecopteris calicifolia and S. mamayi resemble the pinnules of Buritranopteris costata Tavares et al. (2014), which is preserved in a seasonal dryland geological setting. The calcite mode of preservation in S. calicifolia and S. mamayi also allows a more natural sense of the morphology of this foliar modification. The downwardly extended pinnule margins of Scolecopteris latifolia is like the “skirt” of Acitheca polymorpha fertile pinnules (Zodrow et al., 2006), but in Acitheca the elongate sporangia are twice as long as in S. latifolia and extend beyond the hem. In the coal swamp plant Scolecopteris incisifolia Mamay, the acutely folded pinnule margins sandwich synangia between the upper and lower pinnule surfaces in the same way demonstrated for the Late Permian Gemellitheca saudica (Wagner et al., 1985). All scolecopterids with modified pinnule margins have the areas around the synangia filled with an abundance of trichomes or thin scales (e.g., Scolecopteris antarctica Delevoryas, T.N. Taylor & E.L. Taylor [1992]; S. monothrix Ewart [1961]). Detection of this feature is subject to variations of preservation for compression/impression specimens. To some extent, we have to consider that even in the Middle Pennsylvanian coal swamps some marattialean ferns had foliar adaptations suitable for exposure to dry periods and seasonality. In the Permian, the cauline adaptation to the warming climate is the further dissection of the stelar cycles exhibited by Psaronius arrojadoi (Pelourde) Herbst, Psaronius brasiliensis Brongniart, Tietea derbyi Herbst, and Tuvichapteris solmsi Herbst.

Late Pennsylvanian-Permian by spreading from the shrinking peat swamps to the floodplains and wet lowlands of the early Early Permian (DiMichele and Phillips, 2002). This observation supports the notion that Pennsylvanian marattialean ferns had acquired the ability to widen their ecological tolerances. During the Pennsylvanian-Permian transition, there was “a change from a cool to a much warmer and partly drier climate. That transition was characterized by a period of warming that started near the Moscovian-Kasimovian (Late Pennsylvanian) boundary, after which glacial conditions reappeared in last stage of the Pennsylvanian, the Gzhelian. Non-glacial conditions were only fully established at the end of the Early Permian (Artinskian)” (van Waveren et al., 2007, p. 1). For this reason, and the diminishing occurrences of the typical Pennsylvanian marattioid foliage associations, we have chosen the Sakmarian as the end of the dominance of the Paleozoic marattialean ferns in the Permian (Fig. 14.33). The fossil record of Marattiales provides evidence for major changes in distribution patterns through geological time. These include an abundance of both anatomically preserved and compressed species across the equatorial paleotropics from the Middle Pennsylvanian through the basal Permian (Fig. 14.33; DiMichele and Phillips, 2002), the appearance of species in Gondwana, and the absence of species from equatorial North America later in the Permian (Fig. 14.34). Other changes are the occurrence of anatomically preserved species in China during the Permian (Fig. 14.34), the prevalence of compression species and almost total absence of anatomically preserved species from Mesozoic strata, and a virtual absence of marattialean fossils from the post-Mesozoic fossil record (Appendix 2). Against this backdrop, it is curious that all three confirmed occurrences of Cretaceous marattialeans consist of anatomically preserved specimens (i.e., Kva
cek, 2014; Vera and Césari, 2016, this report).

4.8 Paleogeographic/Paleoclimatic Distribution of Marattiales

5. CONCLUSIONS

The lightweight and basally spreading adventitious root systems of the marattialean tree ferns afforded them a stable growth platform on moist soils and in areas of accumulated plant debris. Their preferred ecological niche was the peat swamp, where they constituted 60% to more than 80% of the peat biomass (Phillips et al., 1985). Many of the characteristic coal swamp species of lycopods and calamites became less abundant at the CarboniferousePermian boundary due to a warming trend that started in the Euramerican west and moved east toward northern Pangaea (DiMichele and Philips, 1996; Poulsen et al., 2007; van Waveren et al., 2007). A large portion of the wetlanddependent flora was to become extinct, but the marattialean ferns prospered, becoming more abundant in the

Discovery of superficially Christensenia-like, but more fundamentally Scolecopteris-like, synangia in Early Cretaceous deposits on Vancouver Island, western Canada, reveals that stem group Psaroniaceae persisted much longer into the Mesozoic than previously realized and prompts a more thorough characterization of the Marattiales stem group Psaroniaceae and crown group Marattiaceae. The two families are distinguished by features of plant architecture, root production, frond and pinnule characters, and structural features and dehiscence mechanisms of the synangia. A compilation of worldwide occurrences of fossil marattialeans through time reveals similarities to both the distribution and climatic tolerances of living species and apparently the existence of wider distributions and ecological

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tolerances in the past. Whereas modern marattialeans are a common component of many tropical wetland floras across both the Old World and the New World, extinct species inhabited a wide band of latitudes in both wetland and seasonally dry climates at different times in the past. The extensive fossil record of Marattiales extends from about the MississippianePennsylvanian boundary through the Jurassic, but fossils become extremely rare in Cretaceous deposits and are virtually absent from the Cenozoic fossil record. Marattialeans first appear in the ever-wet equatorial tropics at about the MississippianePennsylvanian boundary and are characterized by the stem group family Psaroniaceae throughout the Paleozoic. Psaroniaceous species extended into climates of seasonal wetness during the Permian. The first representatives of the crown group Marattiaceae appear during the Upper Permian in what is now northern Africa and China (Hill et al., 1985; Liu et al., 2000). Species of Marattiaceae diversify rapidly and spread throughout wetland and seasonal biomes in both the Northern and Southern Hemispheres, becoming the predominant representatives of Marattiales by the Early Triassic. Concurrently, there is a dramatic reduction in both the diversity and geographic distributions of Psaroniaceae, but Escapia christensenioides gen. et sp. nov. demonstrates that the family persisted until at least the Early Cretaceous in western North America. Although geographically widespread, marattiaceous species are reduced to minor components in an increasing percentage of floras during the Upper Jurassic and are nearly absent from younger paleontological records. The most recent fossil evidence for marattialean ferns and the only other confirmed postJurassic occurrences of Marattiaceae are the Early Cretaceous (Aptian) linear synangia from the Antarctic Peninsula (Vera and Césari, 2016) and the Late Cretaceous Marattiopsis vodrazkae, which is also from the Antarctic peninsula (Kva
cek, 2014). The virtual absence of Marattiales from the Cenozoic fossil record has yet to be reconciled with the widespread occurrence of the order in modern tropical wetlands.

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293

FURTHER READING DiMichele, W.A., Cecil, C.B., Chaney, D.S., Elrick, S.D., Lucas, S.G., Lupia, R., Nelson, W.J., Tabor, N.J., 2011. Pennsylvanian-Permian vegetational changes in tropical Euramerica. In: Harper, J.A. (Ed.), Geology of the Pennsylvanian-Permian in the Dunkard Basin. Guidebook for the 76th Annual Field Conference of Pennsylvania Geologists. Field Conference of Pennsylvania Geologists, Inc., pp. 60e102 Gastaldo, R.A., DiMichele, W.A., Pfefferkorn, H.W., 1996. Out of the icehouse into the greenhouse: a Late Paleozoic analog for modern global vegetational change. GSA Today 6, 1e7. Halle, T.G., 1937. The relation between the Late Paleozoic flora of eastern and northern Asia. In: 2-ième Congrès International de la Stratigraphie du Carbonifère, Heerlen, vol. 1, pp. 233e245. Odreman-Rivas, O., Wagner, R.H., 1979. Precisiones sobre algunas floras carboníferas pérmicas de los Andes venezolanos. Boletín de Geologia 13, 77e79. Rees, P.M., Ziegler, A.M., Gibbs, M., Kutzbach, J.E., Behling, P.J., Rowley, D.B., 2002. Permian phytogeographic patterns and climate data/models comparisons. Journal of Geology 110, 1e31. Wagner, R.H., 1993. Climatic significance of the major chronostratigraphic units of the Upper Palaeozoic. In: Comptes Rendus du 12è Congrès Carbonifère, Buenos Aires 1991, vol. 1, pp. 83e108. Wagner, R.H., 2004. Climatic changes as mirrored by Carboniferous and Permian floral distributions. Monografi ás Jardín Botánico Córdoba 11, 29e39. Ziegler, A.M., 1990. Phytogeographic patterns and continental configuration during the Permian period. In: McKerrow, W.S., Scotese, C.R. (Eds.), Palaeozoic Palaeogeography and Biogeography. Geological Society of London, pp. 363e379. Memoir 12.

APPENDIX 1: SYNANGIUM CHARACTERS OF ESCAPIA CHRISTENSENIOIDES SPECIMENS

Character Specimen No.

Diameter (L/W) in mm

No. of Sporangia

Shape

Spores

Exine

Perispore

13170 E bot

1.3/1.0

8?

Oval



e

e

13189 D top

0.8/?

?

?

þ

Baculate

Thin

13330 C top

1.0/1.0

11

Round

þ

Baculate

Thin

13396 C top

1.7/?

?

Oval

þ

Psilate

Thin

13410 B top

1.5/1.0

10?

Oval

þ

Baculate

Thin

13537 F top

1.0/1.2

10

Oval



e

e

13560 A

1.3/0.9

12

Oval

þ

Baculate

Thin

13732 B bot

0.9/0.9

8

Round



e

e

14628 F top

1.8/1.0

10

Oval

þ

Baculate

Thin

14693 A2 bot

>0.9/0.9

7

Round



e

Thin

APPENDIX 2: PALEONTOLOGICAL OCCURRENCES OF MARATTIALEAN FERNS 294

Pennsylvanian Occurrences Family

Stratigraphy/Geography

Age (Ma)

References

Acaulangium bulbaceum (Graham) Millay

Psaroniaceae

Mattoon Formation, Calhoun Coal; “Berryville,” and “Calhoun,” Richland County, IL, USA

Late Pennsylvanian

Graham (1934) and Millay (1977)

Acitheca adaensis Mapes et Schabilion

Psaroniaceae

Wewoka Formation; Ada, Pontotoc County, OK, USA

Upper Moscovian

Mapes and Schabilion (1979a)

Acitheca alii Zodrow,
Sim unek, Cleal, Bek, et P
seni
cka

Psaroniaceae

Sydney Coal Field, Lloyd Cove Seam; Cape Breton Island, Nova Scotia, Canada

Upper Moscovian

Zodrow et al. (2006)

Acitheca ambigua (Presl in Sternberg) N
emejc

Psaroniaceae

Bohemian Massif, Ny´
rany Member, Kladno Formation; Plze
n Basin, Plasy, Czech Republic.

Upper Moscovian, Asturian

N
emejc (1940) and emend Zodrow et al. (2006)

Acitheca (Pecopteris) ambigua (Sternberg) N
emejc

Psaroniaceae

Assise de la Houve, zone de Forbach, Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Acitheca (Pecopteris) polymorpha (Brongniart) Schimper

Psaroniaceae

Gerona, Spain

Stephanian

´ lvarez-Ramis et al. A (1971)

Acitheca (Pecopteris) polymorpha (Brongniart) Schimper

Psaroniaceae

Res‚it‚a Formation; South Carpathian Mountains, Res‚it‚a Basin, Lupac, Romania

Stephanian

Bitoianu (1973)

Acitheca polymorpha (Brongniart) Schimper

Psaroniaceae

Core of the Velebit Anticline, similar to Auernig Group in Austria; Velebit Mts. and Lika region, Croatia

Upper Kasimovian or lowermost Gzhelian

Cleal et al. (2015)

Acitheca polymorpha (Brongniart) Schimper

Psaroniaceae

Sydney Coal Field, Emery seam to top of Morien Series; Cape Breton Island, Nova Scotia, Canada

Late Pennsylvanian; Moscovian

Bell (1938)

Acitheca polymorpha (Brongniart) Schimper

Psaroniaceae

Bohemian Massif; Czech Republic

Upper MoscovianeKasimoviane lower Gzhelian

emend Zodrow et al. (2006)

Acitheca (Pecopteris) polymorpha (Brongniart) Schimper

Psaroniaceae

Bassin de Blanzy et du Creusot; mines de Blanzy, Longpendu, Montchanin, Perrecy, Saint-Be´rain, France

Stephanian

Zeiller (1906)

Acitheca (Pecopteris) polymorpha (Brongniart) Schimper

Psaroniaceae

Bassin de Blanzy et du Creusot; mines de Bert, Perrecy, France

Autunian

Zeiller (1906)

Acitheca polymorpha (Brongniart) Shimper

Psaroniaceae

Auernig Formation; Southern Karavanke Mountain, Jesenice, N.E. Slovenia

Gzhelian D

P
seni
cka et al. (2015)

Acitheca polymorpha (Scolecopteris verbeeki n. sp.) (Brongniart) Shimper

Psaroniaceae

Soengei Garing und Soengei Menkarang, Sumatra

Oberkarbons

Jongmans and Gothan (1925)

Acitheca polymorpha (Brongniart) Shimper

Psaroniaceae

Radstockian Series; Somerset and Bristol Coalfields, South Wales Coalfield, Warwickshire Coalfield. Staffordian Series, Forest of Dean Coalfield, Shrewsbury Coalfield, Somerset and Bristol Coalfield, UK

Westphalian D

Kidston (1923e1925)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Assise de la Houve, zone de St-Avold, Sarre Coalfields, Sie`ge Hostenbach, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Acitheca polymorpha (Brongniart) Shimper

Psaroniaceae

Assise de Sarrelouis, zone de Dilsburg; Sarre Coalfield, Dilsburg, Griesborn, France

Stephanian

Corsin (1951)

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Jangseong Formation, BeC horizons; Samcheong Coalfield, Korea

Asselian or Sakmarian

Chun (1985)

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

van Waveren et al. (2007)

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Taiyuan Formation; Inner Mongolia Autonomous Region, near Shanxi Province, China

Asselian

Li (1995)

Acitheca salviniaefolia Stockmans et Mathieu

Psaroniaceae

Taiyuan Formation; North China Floral Province; Tangshan Prefecture, Hebei Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Acitheca salviniaefolia Stockmans et Mathieu

Psaroniaceae

Taiyuan Formation; Northwest China Province; Longshou Mt., Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Araiangium pygmaeum (Graham) Millay

Psaroniaceae

Mattoon Formation McLeansboro Group, Calhoun Coal; “Berryville” and “Calhoun,” Richland County, IL, USA

Late Pennsylvanian

Millay (1982a)

Artisophyton goldenbergii (Weiss) Pfefferkorn

Psaroniaceae

Neunkirchen Formation; Heinitzgrube, Saarbru¨cken, State of Saarland, Germany

Asselian or Sakmarian

Weiss (1860) and Pfefferkorn (1976)

Artisophyton insignis (Lesquereux) Pfefferkorn

Psaroniaceae

Carbondale Formation, Energy Shale Member, above Herrin No. 6 Coal; Duquoin, IL, USA

Middle Pennsylvanian

Pfefferkorn (1976)

Artisophyton mclayi (Lesquereux) Pfefferkorn

Psaroniaceae

Carbondale Formation, Coal No. 3; St. John, Perry County, IL, USA

Middle Pennsylvanian

Pfefferkorn (1976)

Asterotheca daubreei Zeiller

Psaroniaceae

Radstockian Series; Radstock, Somerset, UK

Radstockian Stephanian

Kidston (1923e1925)

Asterotheca herdii Bell

Psaroniaceae

Sydney Coal Field, Morien series, Mullins seam to Lloyd Cove seam; Cape Breton Island, Nova Scotia, Canada

Late Pennsylvanian West. D

Bell (1938)

Asterotheca macromarginata Fang

Psaroniaceae

Taiyuan Formation; North China Floral Province; Huainan Huaibei Coal Field, Anhui Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Asterotheca piatnitzkyi (Frenguelli) Vieira, Iannuzzi et Guerra-Sommer

Psaroniaceae

Formac¸a˜o La Golondrina, La Golondrina Basin, Patagonia, Argentina

Asselian or Sakmarian

Vieira et al. (2007)

Asterotheca robbii Bell

Psaroniaceae

Sydney Coal Field, Morien series, Tracy seam to Point Aconi seam; Cape Breton Island, Nova Scotia, Canada

Late PennsylvanianWest. D

Bell (1938)

Asterotheca singeri Archangelsky

Psaroniaceae

Formac¸a˜o La Golondrina, La Golondrina Basin, Patagonia, Argentina

Asselian or Sakmarian

Archangelsky and Cu´neo (1984) Continued

295

Psaroniaceae

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Acitheca polymorpha (Brongniart) Shimper

296

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Asterotheca sternbergii (Go¨ppert) Stur

Psaroniaceae

Georgenthal Formation; Stollenwand bei Kleinschmalkalden, Stollenhalde am Regenberg bei Zella-Mehlis. Manebach Formation; Burgberg bei Breitenbach. Goldlauter Formation; Sperbersbach, Raubschloss bei Do¨rrberg, Pochwerksgrund, Mittelberg, Austria

Rotliegend

Barthel (2005)

Buritiranopteris costata Tavares, Rohn, Ro¨bler, et Noll

Psaroniaceae

Motuca Formation, Parnaı´ba Basin; State of Tocantins, Brazil

Early Permian?

Tavares et al. (2014)

Caulopteris sp. Lindley et Hutton

Psaroniaceae

Sydney Coalfield, Cape Breton, Nova Scotia, Canada

Asturian

Zodrow et al. (2006)

Caulopteris sp. Lindley et Hutton

Psaroniaceae

Saginaw Group, Michigan Coal Basin, Grand Ledge, Eaton County, MI, USA

Pennsylvanian

Arnold (1949)

Caulopteris anglica Kidston

Psaroniaceae

Radstock Group; Radstock, County Somerset, England, UK

Asturian

Kidston (1888)

Caulopteris arberi Crookall

Psaroniaceae

Radstock Group; Braysdown, Camerton, County Somerset, UK

Asturian

Crookall (1955)

Caulopteris cyclostigma Lesquereux

Psaroniaceae

Coal No.1; Oliphant, IL, USA. Radstock Group; Radstock, Braysdown, Camerton, County Somerset, UK

Asturian

Crookall (1955)

Caulopteris grandis Grand’Eury

Psaroniaceae

Bassin de houiller de Blanzy; mines de Blanzy, Sainte-Marie, France

Stephanian

Zeiller (1906)

Caulopteris lindleyi Brongniart

Psaroniaceae

Radstock Group; Radstock, Camerton, County Somerset, UK

Asturian

Crookall (1955)

Caulopteris macrodiscus Brongniart

Psaroniaceae

Farrington Group; Coalpitheath, near Bristol, Somerset and Bristol Coalfield, County Bristol, England, UK

Asturian (lower)

Crookall (1955)

Caulopteris peltigera Brongniart

Psaroniaceae

Coal Measures; Mines d’Alais, Department du Gard. Bassin de houiller de Blanzy; mines de Blanzy, Sainte-He´le`ne, France

Stephanian

Brongniart (1828), Grand’Eury (1877), and Zeiller (1906)

Caulopteris peltigera Brongniart

Psaroniaceae

Commentry Coal Field; department de Allier, France

Asturian

Brongniart (1828)

Caulopteris wortheni Lesquereux

Psaroniaceae

Bond or Mattoon Formation; near Carmi, White County, IL, USA

Late Pennsylvanian

Lesquereux (1866)

Crenulopteris acadica (Bell) Wittry et al. (¼Lobatopteris vestita [Lesquereux] Wagner)

Psaroniaceae

Ervedosa, Oporto region, Portugal

Upper Asturian

Wagner and Lemos de Sousa (1983) and Wittry et al. (2014)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Psaroniaceae

Post-Leonian basin, northern Palencia, Cantabrian Mts., NW Spain

Asturian

Wagner and Varker (1971) and Wagner and ´ lvarez-Va´zquez (2010) A

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Francis Creek Shale, Carbondale Formation; “Mazon Creek,” Will County, IL, USA

Lower Cantabrian

Langford (1958), Darrah (1970) and Janssen (1979)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Carbondale Formation, Kewanee Group; “Carterville,” Williamson County, IL, USA

Middle Pennsylvanian

Gastaldo (1977)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Northern Anthracite Coal Basin, upper Allegheny Formation; Wilkes Barre, PA, USA

Upper Pennsylvanian

Oleksyshyn (1982)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Northern Appalachian Coal Basin, upper Allegheny Formation, Wilkes Barre, PA, USA

Upper Pennsylvanian

Wagner and Lyons (1997) and Blake et al. (2002)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Canadian Maritimes: Pictou Formation, New Brunswick, Canada

Upper Moscovian

Bell (1962)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Upper Sydney Mines Formation, Sydney Coalfield, Cape Breton, NS

Middle Pennsylvanian

Bell (1938)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Grovesend Formation; Somerset Coalfield, UK

Asturian

Kidston (1924), Thomas and Cleal (1994), Cleal (1997), and Pendleton et al. (2012)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Staffordian Series; Forest of Dean and associated coalfields, UK

“Staffordian”

Arber (1912), Wagner and Spinner (1972), and Cleal (1986, 1987, 1997)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Upper Pennant Formation and Grovesend Formation; South Wales, UK

Asturian

Cleal (1978, 1997, 2007)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Halesowen Formation; Halesowen, England, UK

Asturian

Besly and Cleal (1997) and Cleal (2005, 2008)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Upper Silesian Coal Basin, Libia z-Member, Poland

Westphalian B

Kotasowa (1979) and Kotasowa and Migier (1995)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Dobrudzha Coal Basin, Gurkovo Formation, Bulgaria

Late Asturian

Cleal et al. (2004)

Crenulopteris acadica (Bell) Wittry et al.

Psaroniaceae

Zonguldak-Amasra Coal basin, Kizilli Formation, Turkey

Langsettian

Kerey et al. (1985) and Cleal and van Waveren (2012)

Crenulopteris (Asterotheca) lamuriana (Heer) Wittry et al.

Psaroniaceae

Radstockian Series: Radstock, Somerset, UK

Asturian

Kidston (1923e1925)

297

Continued

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Crenulopteris acadia (Bell) Wittry et al.

298

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Crenulopteris (Asterotheca) lamuriana (Heer) Wittry et al.

Psaroniaceae

Assise de la Houve, zone de St-Avold, Sarre Coalfield, Victoria, borehole at Dourdal, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Crenulopteris (Pecopteris) lamuriana (Heer) Wittry et al.

Psaroniaceae

Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed, Wanamie, near Wilkes-Barre, PA, USA

Westphalian B

Oleksyshyn (1982)

Crenulopteris lamuriana (Heer) Wittry et al.

Psaroniaceae

La Mure Coal Basin; Coˆte Belle, La Motte d’Aveillans, Ise`re, France

Barruelian

Wittry et al. (2014)

Crenulopteris (Asterotheca) lamuriana (Heer) Wittry et al.

Psaroniaceae

Assise de Sarrelouis, zone de Dilsburg, Sarre Coalfield, Griesborn, France

Stephanian

Corsin (1951)

Crenulopteris lamuriana (Heer) Wittry et al.

Psaroniaceae

Cantabrian Substage; Guardo Coalfield. Barruelian Substage; Sabero and BarrueloRedondo Coalfields. Saberian Substage; Sabero Coalfield, NW Spain

Stephanian

Wagner et al. (1983), Knight (1985), and ´ lvarezWagner and A Va´zquez (2010)

Crenulopteris lamuriana (Heer) Wittry et al.

Psaroniaceae

La Mure coal basin, French Alps, SE France

Barruelian

Heer (1872, 1877), Martin (1961) and Sarrot-Reynauld de Cresseneuil (1961)

Crenulopteris lamuriana (Heer) Wittry et al.

Psaroniaceae

Assise de Rive-de-Gier, Saint-E´tienne, Loire Coalfield, France

Barruelian

Doubinger et al. (1995)

Crenulopteris lamuriana (Heer) Wittry et al.

Psaroniaceae

Ce´vennes Coalfield, Ce´vennes, France

Barruelian

Remy and Remy (1966)

Crenulopteris lamuriana (Heer) Wittry et al.

Psaroniaceae

Dilsburger and basal Heusweiler Formations, Saar-Lorraine, France

Saberian

Corsin (1951), Gutho¨rl (1953), and Remy and Remy (1966)

Crenulopteris lamuriana (Heer) Wittry et al.

Psaroniaceae

Cote Belle, La Motte d’Aveillans, Isere, France

Barruelian

Wittry et al. (2014), Shen (1995) (Li, 1995), and Jongmans (1960)

Crenulopteris (Lobatopteris) lamuriana (Heer) Wittry et al.

Psaroniaceae

Puertollano Coal Basin, Province of Cuidad Real (La Mancha), Central Spain

Stephanian B

Wagner (1983b)

Crenulopteris (Lobatopteris) lamuriana (Heer) Wittry et al.

Psaroniaceae

Sabero Coalfield, Calero, Barruelo/Redondo Coalfields, Spain

Lower Barruelian

Wagner (1962) and Wittry et al. (2014)

Crenulopteris (Lobatopteris) lamuriana (Heer) Wittry et al.

Psaroniaceae

Santa Susana Basin, Spain

Upper Asturian

´ lvarezWagner and A Va´zquez (2010)

Crenulopteris (Lobatopteris) lamuriana (Heer) Wittry et al.

Psaroniaceae

Pen˜acorba coal group; Guardo Coalfield, Spain

Cantabrian

´ lvarezWagner and A Va´zquez (2010)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Psaroniaceae

Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Crenulopteris lamuriana (Heer) Wittry et al.

Psaroniaceae

Assise de Sarrelouis, zone de Dilsburg, Sarre Coalfield, Dilsburg, Griesborn, Ensdorf, France

Stephanian

Corsin (1951)

Crenulopteris lamuriana (Heer) Wittry et al.

Psaroniaceae

Stangalp, Styria, Austria

(?)Barruelian

Jongmans (1938) and Wittry et al. (2014)

Crenulopteris micromiltonii (Bertrand ex Corsin) Wittry et al.

Psaroniaceae

Heiligenwald Formation, Heinrich Coal; Victoria Mine, State of Saarland, Germany

Middle Asturian

Wittry et al. (2014)

Crenulopteris micromiltonii (Bertrand ex Corsin) Wittry et al.

Psaroniaceae

Morien Group, between Mullins and Lloyd Cove seams; Sydney Coalfield, Cape Breton, NS, Canada

Upper Moscovian ¼ Stephanian

Zodrow and Cleal (1985)

Crenulopteris micromiltonii (Bertrand ex Corsin) Wittry et al.

Psaroniaceae

Pennant Formation, Brithdir, Swansea and Rhondda Members); South Wales Coalfield, UK

Pennsylvanian

Cleal (1978, 1997, 2007)

Crenulopteris micromiltonii (Bertrand) Wittry et al.

Psaroniaceae

Assise de la Houve, zone de St-Avold, Faulquemont Coalfield, Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Crenulopteris micromiltonii (Bertrand ex Corsin) Wittry et al.

Psaroniaceae

Upper Geisheck Formation, Luisenthal Formation, Heiligenwald Formation; Saar-Lorraine, France

Asturian

Corsin (1951), Germer (1971), Cleal (1984), and Laveine (1989)

Crenulopteris (Lobatopteris) micromiltonii (Bertrand) Wittry et al.

Psaroniaceae

Ervedosa, Oporto region, Portugal

Upper Asturian

Wittry et al. (2014) and Wagner and Lemos de Sousa Sousa (1983)

Crenulopteris micromiltonii (Bertrand ex Corsin) Wittry et al., 2014

Psaroniaceae

Sabero Coalfield, N. Spain

Barruelian

Wagner and Lemos de Sousa (1983) and Wagner and A´lvarezVa´zquez (1991, 2010)

Crenulopteris (Lobatopteris) micromiltonii (Corsin) Wittry et al.

Psaroniaceae

Barruelo Formation, Carboneros Member, Barruelo/Redondo Coalfields, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus sp. (Weiss) Cleal

Psaroniaceae

Velebit Mts. and Lika region, Croatia

Upper Kasimovian or lowermost Gzhelian

Weiss (1869) and Cleal et al. (2015)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Taiyuan Formation; Northwest China Floral Province; N. Qilian Mts., Longshou Mts., Nagqu, Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Padochov Formation, Rosice-Oslavany 1st Coal Seam; Boskovice Basin, river Oslava, near Oslavany, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae


´
cany Horizon, NesloPadochov Formation, Rı vice Fish Rock locality, near Neslovice, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Crenulopteris (Lobatopteris) lamuriana (Heer) Wittry et al.

299

Continued

300

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Padochov Formation, Zbon
ek-Svita´vka Horizon; Boskovice Basin, Svita´vka locality, Hadisko Hill, near Boskovice, Czech Republic

Lower Sakmarian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Padochov Formation, Lub
e Horizon; Boskovice Basin, Kladoruby locality, near Letovice, Czech Republic

Sakmarian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Taiyuan Formation; North China Floral Province; Shanxi, W. Henan, S. Liaoning and W. Jilin Provinces; Tangshan, Hebei Province, China

Asselian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Uppermost Taiyuan Formation, Wuda Tuff; North China Block, Wuda, Inner Mongolia Autonomous Region, China

Gzhelian- Asselian

Wang and Pfefferkorn (2013)

Cyathocarpus (Scolecopteris) arborea (Schlotheim) Cleal

Psaroniaceae

Manebach Formation; Crock, Manebach, Burgberg bei breitenbach. Goldlauter Formation; Bahnhof Gehlberg, Raubschloss bei Do¨rrberg, Rodebach bei Benschausen, Sembach Winterstein. Oberhof Formation; Mo¨st. Germany

Rotliegend

Barthel (2005)

Cyathocarpus arborea (Sternberg) Weiss

Psaroniaceae

Southern Anthracite coal basin, Llewellyn Formation, Buck Mountain (No. 5) coal bed; St. Clair, near Pottsville, PA. Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA, USA

Asturian

Oleksyshyn (1982)

Cyathocarpus arborea (Sternberg) Weiss

Psaroniaceae

Tineo, Rengos, Tormaleo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus arborea (Sternberg) Weiss

Psaroniaceae

La Pernı´a Coalfield, NW Spain

Upper Asturian

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus arborea (Sternberg) Weiss

Psaroniaceae

Barruelo Formation, Carboneros Member, Barruelo/Redondo Coalfields, Sabero Coalfield, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus arborea (Sternberg) Weiss

Psaroniaceae

Carbondale Formation, Francis Creek Shale; “Mazon Creek,” Will County, IL, USA

Lower Cantabrian

Noe´ (1925)

Cyathocarpus (Pecopteris) arborea (Sternberg) Weiss

Psaroniaceae

Assise de Sarrelouis, zone de Dilsburg, Mines de la Houve, Sarre Coalfield, Ensdorf, France

Stephanian

Corsin (1951)

Cyathocarpus arborea (Sternberg) Weiss

Psaroniaceae

Grovesend Formation (Radstock Member); Kilmersdon, near Radstock, Somerset, UK

Upper Moscovian (Asturian)

Cleal (2015)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Chaumoune Canton, Switzerland

Kasimovian (Stephanian)

Cleal (2015)

Cyathocarpus arborea (Sternberg) Weiss

Psaroniaceae

La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus (Pecopteris) candolleanus (Brongniart) Weiss

Psaroniaceae

Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA, USA

Asturian

Oleksyshyn (1982)

Cyathocarpus (Pecopteris) candolleanus (Brongniart) Weiss

Psaroniaceae

Assise de la Houve, zone de St-Avold, Sarre Coalfield, Hostenbach, mines de la Houve, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Cyathocarpus candolleanus (Brongniart) Weiss

Psaroniaceae

Carrasconte subarea/Villablindo Coalfield, Cabrales cf., Pico Cordel, Puente Pumar cf., El Bierzo cf., Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus candolleanus (Brongniart) Weiss

Psaroniaceae

Douro Basin, Douro Coalfield; Oporto region, Portugal

Stephanian C

Wagner (1983a) and Wagner and Lemos de Sousa (1983)

Cyathocarpus candolleanus (Brongniart) Weiss

Psaroniaceae

Bassin de Blanzy et Creusot; mines de Blanzy, Creusot, Longpendu, Saint-Be´rain, France

Stephanian

Zeiller (1906)

Cyathocarpus candolleanus (Brongniart) Weiss

Psaroniaceae

Bassin de Blanzy et Creusot; mines de Bert, Perrecy, France

Autunian Saxonian infe´rieur

Zeiller (1906)

Cyathocarpus candolleanus (Brongniart) Weiss

Psaroniaceae

Barruelo Formation, Carboneros Member; Barruelo/Redondo, Valdeo´n, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus candolleanus (Brongniart) Weiss

Psaroniaceae

La Magdalena Coalfield, Canseco/Rucayo Coalfields, Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus candolleanus (Brongniart) Weiss

Psaroniaceae

El Bierzo, NW Leon Province, NW Spain

Lower Stephanian C

Wagner (1983b)

Cyathocarpus candolleanus (Brongniart) Cleal

Psaroniaceae

Taiyuan Formation; Northwest China Floral Province, N. Qilian Mts., Longshou Mts., Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Cyathocarpus candolleanus (Brongniart) Cleal

Psaroniaceae

Padochov Formation, Rosice-Oslavany 1st Coal Seam; Boskovice Basin, river Oslava, near Oslavany, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Cyathocarpus candolleanus (Brongniart) Cleal

Psaroniaceae

Uppermost Taiyuan Formation, Wuda Tuff; North China Block, Wuda, Inner Mongolia Autonomous Region, China

Gzhelian-Asselian

Wang and Pfefferkorn (2013)

Cyathocarpus candolleanus (Brongniart) Cleal

Psaroniaceae

Taiyuan Formation; North China Floral Province; Shanxi, Shandong, S. Liaoning and W. Jilin Provinces, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Cyathocarpus candolleanus (Brongniart) Cleal

Psaroniaceae

Jangseong Formation, BeC horizons; Samcheong Coalfield, Korea

Asselian or Sakmarian

Chun (1985)

301

Psaroniaceae

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Cyathocarpus arborea (Sternberg) Weiss

Continued

302

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Cyathocarpus (Pecopteris) candolleanus (Brongniart) Cleal

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

van Waveren et al. (2007)

Cyathocarpus (Scolecopteris) candolleanus (Brongniart) Cleal

Psaroniaceae

Weissig Basin, Elbe lineament, near Dresden, Saxony, Germany

Asselian

Barthel et al. (2010)

Cyathocarpus (Scolecopteris) candolleanus (Brongniart) Cleal

Psaroniaceae

¨ hrenkammer, Alltal Georgenthal Formation; O und Stollenwand, Stollenhalde am Regenberg, Gr. Spanntiegel. Manebach Formation; Pfannthal, Seitental des Gabelbaches, Manebach, Burgberg bei Breitenbach. Goldlauter Formation; Fundorte. Oberhof Formation; Schweizerhu¨tte, Bhf. Oberhof. Germany

Rotliegend

Barthel (2005)

Cyathocarpus (Pecopteris) candolleanus (Brongniart) Cleal

Psaroniaceae

Padochov Formation, Rosice-Oslavany 1st Coal Seam; Boskovice Basin, river Oslava, near Oslavany, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Cyathocarpus cyatheus (Brongniart) Mosbrugger Cleal

Psaroniaceae

Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA, USA

Asturian

Oleksyshyn (1982)

Cyathocarpus cyatheus (Brongniart) Mosbrugger Cleal

Psaroniaceae

Amao, Carrasconte subarea/Villablino Coalfield, Henarejos cf., Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus cyatheus Brongniart auctorum

Psaroniaceae

Rangos, Carrasconte subarea/Villablino Coalfield, cf. Pen˜a Cilda´ Formation, Pico Cordel cf., Puente Pumar, Henarejos, El Bierzo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus cyatheus (Brongniart) Mosbrugger Cleal

Psaroniaceae

Douro Basin, Douro Coalfield; Oporto region, Portugal

Stephanian C

Wagner (1983a) and Wagner and Lemos de Sousa (1983)

Cyathocarpus (Eupecopteris) cyatheus (Brongniart) Mosbrugger Cleal

Psaroniaceae

Sydney Coal Field, Morien series, Carr seam; Cape Breton Island, Nova Scotia, Canada

Late Pennsylvanian upperMoscovian ¼ Stephanian

Bell (1938)

Cyathocarpus cyatheus (Brongniart) Mosbrugger

Psaroniaceae

La Magdalena Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus (Pecopteris) cyatheus (Brongniart) Mosbrugger Cleal

Psaroniaceae

Assise de Sarrelouis, Dilsburg, Mines de la Houve, Sarre Coalfield, near Ensdorf, Germany

Stephanian

Corsin (1951)

Cyathocarpus (Pecopteris) cyatheus (Brongniart) Mosbrugger Cleal

Psaroniaceae

Assise de la Houve, zone de St-Avold, Sarre Coalfield, Victoria (Pu¨ttlingen), France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Cyathocarpus cyatheus (Brongniart) Mosbrugger Cleal

Psaroniaceae

Bassin de Blanzy et Creusot; mines de Blanzy, Creusot, Longpendu, Montchanin, Saint-Be´rain, France

Stephanian

Zeiller (1906)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Bassin de Blanzy et Creusot; mines de Bert et Perrecy, France

Autunian Saxonian infe´rieur

Zeiller (1906)

Cyathocarpus (Pecopteris) cyatheus Schlotheim Cleal

Psaroniaceae


´
cany Horizon, NesloPadochov Formation, Rı vice Fish Rock locality, near Neslovice, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) cyatheus Schlotheim Cleal

Psaroniaceae

Padochov Formation, Zbon
ek-Svita´vka Horizon; Svita´vka locality, Hadisko Hill, near Boskovice, Czech Republic

Lower Sakmarian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) cyatheus Schlotheim Cleal

Psaroniaceae

Padochov Formation, Lub
e Horizon; Boskovice Basin, Kladoruby locality, near Letovice, Czech Republic

Sakmarian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) cyatheus Schlotheim Cleal

Psaroniaceae

Taiyuan Formation; Northwest China Province; N. Qilian Mts., Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Taiyuan Formation; Northwest China Floral Province; Longshou Mt., Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) cyatheus Schlotheim Cleal

Psaroniaceae

Taiyuan Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province; Shandong, Shanxi, S. Liaoning and W. Jilin Provinces, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Mosbrugger Cleal

Psaroniaceae

Assise de la Houve, zone de St-Avold, Sarre Coalfield, mines de la Houve, Faulquemont Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Mosbrugger Cleal

Psaroniaceae

Southern Anthracite coal basin, Llewellyn Formation, Buck Mountain (No. 5) coal bed; St. Clair, near Pottsville, PA, USA

Asturian

Oleksyshyn (1982)

Cyathocarpus hemitelioides (Brongniart) Mosbrugger Cleal

Psaroniaceae

Bassin de Blanzy et Creusot; mines de Blanzy, Creusot, mines de Longpendu, Montchanin, Perrecy, France

Stephanian

Zeiller (1906)

Cyathocarpus hemitelioides (Brongniart) Mosbrugger Cleal

Psaroniaceae

Asturias Province, Tineo, Spain

Stephanian B

Wagner and ´ lvarez-Va´zquez (2010) A

Cyathocarpus hemitelioides (Brongniart) Mosbrugger Cleal

Psaroniaceae

El Bierzo, NW Leo´n Province, NW Spain

Lower Stephanian C

Wagner (1983b)

Cyathocarpus hemitelioides (Brongniart) Mosbrugger Cleal

Psaroniaceae

Bassin de Blanzy et Creusot; mine de Bert, France

Autunian Saxonian infe´rieur

Zeiller (1906)

Cyathocarpus hemitelioides (Brongniart) Mosbrugger Cleal

Psaroniaceae

Pen˜acorba coal group; Tejerina/Ocejo de la Pen˜a, Spain

Cantabrian

Wagner and ´ lvarez-Va´zquez (2010) A

Cyathocarpus hemitelioides (Brongniart) Mosbrugger Cleal

Psaroniaceae

Barruelo Formation, Carboneros Member; Sabero Coalfield, Barruelo/Redondo Coalfield, Spain

Barruelian

Wagner and ´ lvarez-Va´zquez (2010) A

303

Psaroniaceae

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Cyathocarpus cyatheus (Brongniart) Mosbrugger Cleal

Continued

304

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Cyathocarpus hemitelioides (Brongniart) Mosbrugger Cleal

Psaroniaceae

Puerto Ventana, La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Canseco/Rucayo Coalfields, Spain

Saberian

Wagner and ´ lvarez-Va´zquez (2010) A

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Jangseong Formation, BeC horizons; Samcheong Coalfield, Korea

Asselian or Sakmarian

Chun (1985)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Manebach Formation; Manebach, Germany

Rotliegend

Barthel (2005)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Taiyuan Formation; Northwest China Floral Province; Longshou Mt., Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Cyathocarpus hemitelioides (Brongniart) Cleal

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

van Waveren et al. (2007) and Jongmans and Gothan (1935)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Shanxi Formation; Wuda District, Inner Mongolia Autonomous Region, China

Asselian or Sakmarian

Pfefferkorn and Wang (2007)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Taiyuan Formation; North China Floral Province; Tangshan Prefecture, Hebei Province, and W. Jilin Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Padochov Formation, Rosice-Oslavany 1st Coal Seam; Boskovice Basin, river Oslava, near Oslavany, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

van Waveren et al. (2007)

Cyathocarpus (Pecopteris) lepidorachis (Brongniart) Cleal

Psaroniaceae

Taiyuan Formation; North China Floral Province; Tangshan Prefecture, W. Henan Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Cyathocarpus (Pecopteris) lepidorachis (Brongniart) Cleal

Psaroniaceae

Padochov Formation, Rosice-Oslavany 1st Coal Seam; Boskovice Basin, river Oslava, near Oslavany, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) lepidorachis (Brongniart) Cleal

Psaroniaceae

Shansi Formation; North China Floral Province; Inner Mongolia Autonomous Region, Jungar County, Huainan Huaibei Coal Field, Anhui Province; N. Weihe graben, Shanxi Province; Fengfeng mining district, Tangshan Prefecture, Hebei Province, China

Sakmarian

Shen (1995) (Li, 1995) (Li, 1995)

Cyathocarpus (Pecopteris) lepidorachis (Brongniart) Cleal

Psaroniaceae

Shansi Formation; Northwest China Floral Province; N. Qilian Mt., Xizang Autonomous Region, China

Sakmarian

Shen (1995) (Li, 1995) (Li, 1995)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Psaroniaceae

Assise de la Houve, zone de St-Avold, Sarre Coalfield, Bremsberg, Hostenbach, Victoria (Pu¨ttlingen), France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Cyathocarpus (Asterotheca) lepidorachis (Brongniart) Mosbrugger Cleal

Psaroniaceae

Radstockian Series; Somerset and Bristol Coalfield. Staffordian Series; Shrewsbury Coalfield, South Wales Coalfield. UK

Asturian

Kidston (1923e1925)

Cyathocarpus (Pecopteris) lepidorachis (Brongniart) Mosbrugger Cleal

Psaroniaceae

Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA

Asturian

Oleksyshyn (1982)

Cyathocarpus cf. lepidorachis (Brongniart) Mosbrugger Cleal

Psaroniaceae

Pen˜acorba coal group; Gamonedo/Inguanzo, east Asturias, Spain

Cantabrian

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus lepidorachis (Brongniart) Mosbrugger Cleal

Psaroniaceae

El Bierzo, NW Leon Province, NW Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Cyathocarpus cf. lepidorachis (Brongniart) Mosbrugger Cleal

Psaroniaceae

El Bierzo, NW Leon Province, NW Spain

Lower Stephanian C

Wagner (1983b)

Cyathocarpus (Pecopteris) lepidorachis (Brongniart) Cleal

Psaroniaceae

Padochov Formation, Rosice-Oslavany 1st Coal Seam; Boskovice Basin, river Oslava, near Oslavany, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Danaeites (Goeppert) Stur sp.

Psaroniaceae

Lower part, Kaipaizileike Formation; northwest Tarim Basin, southern Xinjiang Autonomous Region, China

Sakmarian

Shen (1995) (Li, 1995)

Danaeites emersonii Lesquereux

Psaroniaceae

La Magdalena Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Danaeites emersonii Lesquereux

Psaroniaceae

Carrasconte subarea, Villablino Coalfield, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Diplazites emarginatus (Go¨ppert) Cleal

Psaroniaceae

Wettin, State of Sachen, Germany

Late Moscovian

Go¨ppert (1836)

Diplazites emarginatus (Go¨ppert) Cleal

Psaroniaceae

La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Canseco/Rucayo Coalfields, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Diplazites emarginatus (Go¨ppert) Cleal

Psaroniaceae

Amao, Tineo, Rengos, Carrasconte subarea, Villablino Coalfield, Cabrales district, Pen˜a Cilda´, Henarejos, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Danaeites (Pecopteris) mengkarangensis Jongmans et Gothan

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

van Waveren et al. (2007) and Rigby (1998)

Danaeites (Pecopteris) mengkarangensis Jongmans et Gothan

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Asselian or Sakmarian

Jongmans and Gothan (1935) and Rigby (1998)

305

Continued

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Cyathocarpus (Pecopteris) lepidorachis (Brongniart) Mosbrugger Cleal

306

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Danaeites (Pecopteris) rigida Yabe et Oishi

Psaroniaceae

Taiyuan Formation; Northwest China Floral Province; Longshou Mt., Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Danaeites saraepontanus Stur

Psaroniaceae

Taiyuan Formation; Northwest China Floral Province; Longshou Mt., Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) hallei Kawasaki

Psaroniaceae

Taiyuan Formation; North China Floral Province; Inner Mongolia Autonomous Region; Anhui Province, Jungar County, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Diplazites longifolius Brongniart

Psaroniaceae

Carrasconte subarea, Villablino Coalfield, Pen˜a Cilda´ Formation, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Diplazites (Pecopteris) unitus (Brongniart) Cleal

Psaroniaceae

Southern Anthracite coal basin, Llewellyn Formation, Buck Mountain (No. 5) coal bed; St. Clair, near Pottsville, PA. Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA, USA

Asturian

Oleksyshyn (1982)

Diplazites (Pecopteris) unitus (Brongniart) Cleal

Psaroniaceae

Carbondale Formation, Francis Creek Shale; “Mazon Creek,” Will County, IL, USA

Lower Cantabrian

Noe´ (1925)

Diplazites (Ptychocarpus) unitus (Brongniart) Cleal

Psaroniaceae

Sydney Coal Field, Emery seam to top of Morien series; Cape Breton Island, Nova Scotia, Canada

Asturian Upper Moscovian

Bell (1938)

Diplazites (Ptychocarpus) unitus (Brongniart) Cleal

Psaroniaceae

Radstockian Series; Somerset and Bristol Coalfields, South Wales Coalfield, South Staffordshire Coalfield, North Wales Coalfield. Staffordian Series; Forest of Wyre Coalfield, Somerset and Bristol Coalfield. UK

Asturian

Kidston (1923e1925)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Ablanedo Formation, Ablanedo, area of Riosa, NW Central Asturian Coalfield, Cantabrian Mts., NW Spain

Asturian

Jongmans and Wagner (1957)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Bassin de Blanzy et Creusot; mines de Blanzy (Saint-Franc¸ois, Maugrand, Sainte-He´le`ne, Magny), mines de Longpendu, Montchanin, Perrecy, Saint-Be´rain, France

Stephanian

Zeiller (1906)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Lorraine Coal Basin, France

Westphalian/Stephanian boundary

Laveine (1973)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Sydney mines Formation, Stubbard Seam; Sydney Coalfield, Cape Breton, Canada

Upper Moscovian (Asturian)

Cleal (2015)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Carbondale Formation, Francis Creek Shale; “Mazon Creek,” Will County, IL, USA

Lower Cantabrian

Jennings and Millay (1979)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Grovesend Formation; Severn Coalfield, South Wales, UK

Upper Moscovian (Asturian)

Cleal (2015)

Diplazites (Pecopteris) unitus (Brongniart) Cleal

Psaroniaceae

Assise de Sarrelouis, zone de Dilsburg, Sarre Coalfield, Griesborn, Ensdorf, mines de la Houve, France

Stephanian

Corsin (1951)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Puertollano Coal Basin, Province of Cuidad Real (La Mancha), Central Spain

Stephanian B

Wagner (1983b)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Oporto region, Douro Basin, Douro Coalfield, Portugal

Stephanian C

Wagner and Lemos de Sousa (1983)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Post-Leonian basin, northern Palencia, Cantabrian Mts., NW Spain

Asturian

Wagner and Varker (1971)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Ervedosa; Sierra de la Demanda (Burgos); Riosa/Olloniego and Aller/Nalo´n areas of the Central Asturian Coalfield, Spain

Lower Asturian

´ lvarezWagner and A Va´zquez (2010)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Santa Susana Basin, Guardo Coalfield, La Pernia, Aguiro´, Spain

Upper Asturian

´ lvarezWagner and A Va´zquez (2010)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Pen˜acorba coal group; Barruelo/Redondo Coalfields, Guardo Coalfield, Tejerina/Ocejo de la Pen˜a, Spain

Cantabrian

´ lvarezWagner and A Va´zquez (2010)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Barruelo Formation, Carboneros Member, Barruelo/Redondo Coalfields, Sabero Coalfield, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Asturias, Spain

Stephanian

Wagner (1971)

Diplazites unitus (Brongniart) Cleal

Psaroniaceae

Olloniego Formation, NW. border Central Asturian Coalfield, Spain

Asturian

Wagner (1971)

Diplazites (Pecopteris) cf. unita (Brongniart) Cleal

Psaroniaceae

India-Himalaya Block; Qubu of Tingri County, Xizang Autonomous Region, China

Early Permian

Shen (1995) (Li, 1995)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Uppermost Taiyuan Formation, Wuda Tuff; North China Block, Wuda, Inner Mongolia Autonomous Region, China

Gzhelian Asselian

Wang and Pfefferkorn (2013)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Henryetta Coal (Croweburg Coal equivalent); Okmulgee County, between Okmulgee and Morris, OK, USA

Middle Pennsylvanian

Moore et al. (2013)

Diplazites (Scolecopteris) unita (Brongniart) Cleal

Psaroniaceae

Georgenthal Formation; Stollenwand und Alltel Kleinschmalkalden, Stollenhalde am Regenberg Ka¨lberza¨hltunnel. Schnepfkopfgraben, Lo¨hme. Manebach Formation; Manebach, Mordflek, Pfannthal, Sachsendelle. Goldlauter Formation; Sperbersbach. Oberhof Formation; Bhf. Oberhof. Germany

Rotliegend

Barthel (2005)

307

Psaroniaceae

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Diplazites (Pecopteris) unitus (Brongniart) Cleal

Continued

308

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

van Waveren et al. (2007) and Rigby (1998)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Irian Jaya, Locality B, West New Guinea

Early Permian

Jongmans (1940), Visser and Hermes (1962), and Rigby (1998)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Taiyuan Formation; Northwest China Province; N. Qilian Mts., Longshou Mt., Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Eoangiopteris andrewsii Mamay

Psaroniaceae

Lower to Middle Cherokee Group, Des Moines Series; Urbandale Mine, Polk County, IA, USA

Middle Pennsylvanian

Mamay (1950)

Eoangiopteris goodii Millay

Psaroniaceae

Coals of the Monongahela Series; Shade, Athens County, OH, USA

Late Pennsylvanian

Millay (1978)

Grandeuryella renaultii (Stur) Weiss

Psaroniaceae

Poudingue Mosaı¨que; Grand Croix, near St.E´tienne, department de Loire, France

Stephanian

Weiss (1885) and Lesnikowska and Galtier (1992)

Lobatopteris ambigua (Presl in Sternberg) N
emejc

Psaroniaceae

Barruelo Formation, Carboneros Member; Barruelo/Redondo Coalfields, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris corsinii Wagner

Psaroniaceae

Tineo, Carrasconte subarea, Villablino Coalfield, Henarejoas, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris corsinii Wagner

Psaroniaceae

Puertollano Coal Basin, Province of Cuidad Real (La Mancha), Central Spain

Stephanian C

Wagner (1983b) and ´ lvarezWagner and A Va´zquez (2010)

Lobatopteris corsinii Wagner

Psaroniaceae

El Bierzo, NW Leon Province, NW Spain

Stephanian B

Wagner (1983b) and ´ lvarezWagner and A Va´zquez (2010)

Lobatopteris corsinii Wagner

Psaroniaceae

Puerto Ventana, La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris cf. corsinii Wagner

Psaroniaceae

Velebit Mts. and Lika region, Croatia

Upper Kasimovian or lowermost Gzhelian

Cleal et al. (2015)

Lobatopteris geinitzii (von Gutbier) Wagner

Psaroniaceae

Mauchline Volcanic Group; Mauchline Basin, Stair, on River Ayr, Scotland

Lower Rotliegend

Wagner (1966)

Lobatopteris geinitzii (Gutbier) Wagner

Psaroniaceae

Georgenthal Formation; Ka¨lberzha¨l Tunnel Mehlis. Manebach Formation; Ochsenwiese, Crock, Grube Fu¨rchtegott im Pfannthal, Manebach, Blauer Stein am Mordfleck, Germany

Rotliegend

Barthel (2005)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Pen˜arroya-Belmez Coalfield; Guadiato region, Province of Co´rdoba, Spain

Westphalian B

Wagner (1983b)

Lobatopteris (Pecopteris) miltonii (Artis) Wagner

Psaroniaceae

South Staffordshire Coalfield; Red Clay Series, Granville Clay Pit, Old Hill, UK

Middle Coal Measures

Arber (1916) and P
seni
cka (2006)

Lobatopteris (Pecopteris) miltonii (Artis) Wagner

Psaroniaceae

Carbondale Formation, Francis Creek Shale; “Mazon Creek,” Will County, IL, USA

Lower Cantabrian

Noe´ (1925)

Lobatopteris (Pecopteris) miltonii (Artis) Wagner

Psaroniaceae

Southern Anthracite coal basin, Llewellyn Formation, Buck Mountain (No. 5) coal bed; St. Clair, near Pottsville, PA, USA

Asturian

Oleksyshyn (1982)

Lobatopteris (Pecopteris) miltonii (Artis) Wagner

Psaroniaceae

South Staffordshire Coalfield; Red Clay Series, Granville Clay Pit, Old Hill, UK

Middle Coal Measures

Arber (1916)

Lobatopteris (Pecopteris) miltonii (Artis) Wagner

Psaroniaceae

Saginaw Group, Michigan Coal Basin, Grand Ledge, Eaton County, MI, USA

Pennsylvanian

Arnold (1949)

Lobatopteris miltonii (Artis) Wagner

Psaroniaceae

Middle Coal Measures Formation (Barnsley Main Seam); Barnsley, County Yorkshire, UK

Upper Bashkirian (Duckmantian)

Cleal (2015)

Lobatopteris (Asterotheca) miltonii (Artis) Wagner

Psaroniaceae

Sydney Coal Field, Morien series; Cape Breton Island, Nova Scotia, Canada

Late Penn. Westphalian C-D

Bell (1938)

Lobatopteris miltonii (Artis) Wagner

Psaroniaceae

Olloniego Formation, Central Asturian Coalfield, Malpica, Spain

Lower to middle Asturian

Wagner (1971)

Lobatopteris miltonii (Artis) Wagner

Psaroniaceae

Assise de Sulzbach, Neunkirchen, Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Lobatopteris (Asterotheca) miltonii (Artis) Wagner

Psaroniaceae

Assise de Sulzbach, Neunkirchen, Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Lobatopteris obtusa Yang

Psaroniaceae

Taiyuan Formation; North China Floral Province, W. Henan Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Lobatopteris orienervosa (Corsin) Cleal

Psaroniaceae

Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA, USA

Asturian

Oleksyshyn (1982)

Lobatopteris orienervosa (Corsin) Cleal

Psaroniaceae

Assise de la Houve, zone de Forbach; Merlebach, Sarre and Moselle Coalfields, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Lobatopteris (Asterotheca) orienervosa (Corsin) Cleal

Psaroniaceae

Assise de la Houve, zone de Forbach; Merlebach Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Lobatopteris cf. polypodioides Brongniart ?

Psaroniaceae

Barruelo Formation, Carboneros Member, Sabero Coalfield, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris (Pecopteris) polypodioides Knight

Psaroniaceae


´
cany Horizon, NesloPadochov Formation, Rı vice Fish Rock locality, near Neslovice, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Lobatopteris (Pecopteris) precursor Stockmans et Willie`re

Psaroniaceae

Pen˜arroya-Belmez Coalfield; Guadiato region, Province of Co´rdoba, Spain

Westphalian B Duckmantian

Wagner (1983b)

309

Psaroniaceae

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Lobatopteris (Pecopteris) lignyi Stockmans et Willie`re

Continued

310

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Lobatopteris cf. pseudovestita White

Psaroniaceae

Barruelo Formation, Carboneros Member, Sabero Coalfield, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris cf. pseudovestita White

Psaroniaceae

Barruelo Formation, Carboneros Member, Sabero Coalfield, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris serpentigera Wagner

Psaroniaceae

RiosaeOlloniego area, Central Asturian Coalfield, Spain

Lower Asturian

Wagner and Lemos de Sousa (1983)

Lobatopteris serpentigera Wagner

Psaroniaceae

Barruelo Formation, Carboneros Member, Barruelo/Redondo, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris serpentigera Wagner

Psaroniaceae

Olloniego Formation, NW. border Central Asturian Coalfield, La Pereda, Spain

Asturian

Wagner (1971)

Lobatopteris tongshanensis Stockmans et Mathieu

Psaroniaceae

Taiyuan Formation; North China Floral Province; Tangshan Prefecture, Hebei Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Lobatopteris vestita (Lesquereux) Wagner

Psaroniaceae

Henryetta Coal (Croweburg Coal equivalent); Okmulgee County, between Okmulgee and Morris, OK, USA

Middle Pennsylvanian

Moore et al. (2013)

Lobatopteris vestita auct Wagner

Psaroniaceae

Grovesend Formation (Radstock Member), Radstock, County Somerset, UK

Upper Moscovian (Asturian)

Cleal (2015)

Lobatopteris vestita sensu Wagner

Psaroniaceae

Santa Susana Basin, Guardo Coalfield, Aguiro´, La Pernı´a Coalfield, Spain

Upper Asturian

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris vestita sensu Wagner

Psaroniaceae

Pen˜acorba coal group; Guardo Coalfield, Spain

Cantabrian

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris viannae (Teixeira) Wagner

Psaroniaceae

Asturias Province, Tineo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris viannae (Teixeira) Wagner

Psaroniaceae

Douro Basin, Douro Coalfield; Oporto region, Portugal

Stephanian C

Wagner and Lemos de Sousa (1983)

Lobatopteris viannae (Teixeira) Wagner

Psaroniaceae

Pen˜acorba coal group; Guardo Coalfield, Spain

Cantabrian

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris viannae (Teixeira) Wagner

Psaroniaceae

Barruelo Formation, Carboneros Member, Barruelo/Redondo Coalfields, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Lobatopteris viannae (Teixeira) Wagner

Psaroniaceae

Puerto Ventana, La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Canseco/Rucayo Coalfields, Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Megaphyton circulare Crookall

Psaroniaceae

Above Steam Coal (Edge Coal Group), Carboniferous Limestone Series; Herbershire Colliery, near Denny, County Stirlingshire, UK

Lower Carboniferous

Crookall (1955)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Psaroniaceae

Above Steam Coal (Edge Coal Group), Carboniferous Limestone Series; Stripeside Pit, Herbershire Colliery, near Denny, County Stirlingshire, UK

Lower Carboniferous

Crookall (1955)

Megaphyton approximatum Lindley and Hutton

Psaroniaceae

Roof of High Main Coal; Jarrow Colliery, County Durham, England, UK

Westphalian B

Crookall (1955)

Megaphyton frondosum Artis

Psaroniaceae

Shale above the Low Main Seam; Felling Colliery, County Durham, England, UK

Westphalian B

Crookall (1955)

Megaphyton goldenbergii Weiss

Psaroniaceae

Barnsley Thick Coal; Monckton Main Colliery, Barnsley, County Yorkshire, UK

Westphalian B

Crookall (1955)

Megaphyton gwynne-vaughanii Crookall

Psaroniaceae

Barnsley Thick Coal; Darton near Barnsley, Yorkshire, England, UK

Westphalian B

Crookall (1955)

Megaphyton elongatum Kidston

Psaroniaceae

Radstock Group; Radstock, Tyning Pit, Ludlow’s Pit, Middle Pit, County Somerset, UK

Asturian

Crookall (1955)

Millaya tularosana Mapes et Schabilion

Psaroniaceae

Bursum Formation; Tularosa, NM, USA

Wolfcampian; Lower Permian

Mapes and Schabilion (1979b)

Pecopteris sp.

Psaroniaceae

Pyre´ne´es Be´arnaises, rive gauche de la Valle´e du Gave d’Aspe, au Sud d’Urdos (outcrop AS75)

Namurian AeWestphalian B

Del Volve´ and Laveine (1985)

Pecopteris sp.

Psaroniaceae

Paradox Basin, Cutler Group; San Juan County, “Indian Creek,” Utah, USA

Pennsylvanian-Permian

DiMichele et al. (2014)

Pecopteris sp.

Psaroniaceae

Mengkarang Formation; Karing river, Bangko, Jambi, Sumatra, Indonesia

Asselian or Sakmarian

Waveren et al. (2005); Rigby (1998)

Pecopteris affinis Brongniart

Psaroniaceae

Assise de la Houve, zone de St-Avold, Sarre Coalfield, Victoria (Pu¨ttlingen), France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris affinis

Psaroniaceae

La Magdalena Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris affinis (Schlotheim) Brongniart

Psaroniaceae

Taiyuan Formation; Northwest China Floral Province; Longshou Mt., Nagyu, Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Pecopteris ameromii Stockmans et Willie`re

Psaroniaceae

Puertollano Coal Basin, Province of Cuidad Real (La Mancha), Central Spain

Stephanian B

Wagner (1983b)

Pecopteris ameromii Stockmans et Willie`re

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C

Wagner (1983b)

Pecopteris ameromii Stockmans et Willie`re

Psaroniaceae

Barruelo Formation, Carboneros Member, Sabero Coalfield, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris ameromii Stockmans et Willie`re

Psaroniaceae

Fonfrı´a, Villablino Coalfield, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Megaphyton obscurum Crookall

311

Continued

312

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris ameromii Stockmans et Willie`re

Psaroniaceae

Carrasconte subarea, Villablino Coalfield, Cabrales, Pico Cordel, Henarejos, El Bierzo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris ameromii Stockmans et Willie`re

Psaroniaceae

La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris cf. ameromii Stockmans et Willie`re

Psaroniaceae

Oporto region, Douro Basin, Douro Coalfield, Portugal

Stephanian C

Wagner (1983a) and Wagner and Lemos de Sousa (1983)

Pecopteris apicalis Knight

Psaroniaceae

Pen˜a Cilda´ Formation, Henarejos, El Bierzo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris apicalis Knight

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C

Wagner (1983b)

Pecopteris apicalis Knight

Psaroniaceae

Barruelo Formation, Carboneros Member, Barruelo/Redondo Coalfields, Sabero Coalfield, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris apicalis Knight

Psaroniaceae

La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris arcuata Halle

Psaroniaceae

Taiyuan Formation; Northwest China Floral Province; N. Qilian Mts., Longshou Mts., Qinghai Plateau, Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Pecopteris arcuata Halle

Psaroniaceae

Taiyuan Formation; North China Floral Province; Weihe River, W. Henan Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Pecopteris arcuata Halle

Psaroniaceae

Irian Jaya, Locality A, along Otakwa river, West New Guinea

Early Permian

Jongmans (1940)

Pecopteris arcuata Halle

Psaroniaceae

Gangdise-Nyainqentanglha Block; Xizang Autonomous Region, Xiagangjiang, Geˆrzeˆ County, China

Early Permian

Li (1995)

Pecopteris arcuata Halle, 1927

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Asselian or Sakmarian

Jongmans and Gothan (1935), Rigby (1998), and van Waveren et al. (2007)

Pecopteris armasii Zeiller

Psaroniaceae

Radstockian Series; Somerset and Bristol Coalfield, UK

Asturian

Kidston (1923e1925)

Pecopteris aspidioides Sternberg

Psaroniaceae

Pilzen Basin, Whetstone Horizon, Lower Radnice Coal; Pilzen Basin, Nyrany Coalfield, Uxa Mine, Czech Republic

Lower Bolsovian

Oplu
stil et al. (2007)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species


a´rky Intra-Sudetic Basin, Prkenny´ d ul Zd’
a´rky Coal; Zden
ek Nejedly´Member, 3rd Zd’ mire, Male´ Svato
novice, Czech Republic

Duckmantian

Oplu
stil et al. (2007)

Pecopteris aspidioides Sternberg

Psaroniaceae

S. Radnice Basin, Radnice Member, Ov
c´ın coal deposit, western Bohemia, Czech Republic

Early Moscovian (Bolsovian)

Oplu
stil et al. (2014)

Pecopteris aspidioides Sternberg

Psaroniaceae

Assise de la Houve, zone de St-Avold, Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris bourozi Dalinval

Psaroniaceae

Bassin Houiller du Nord; Faisceau de Pouilleuse, Assise d’Anzin et sommet du faiseau de Six-Sillons de l’Assise Bruay, France

Westphalian B and C

Dalinval (1960)

Pecopteris bucklandii Brongniart

Psaroniaceae

Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA, USA

Alleghenian, Conemaughian, and lower Monongahelan Asturian

Oleksyshyn (1982)

Pecopteris bucklandii Brongniart

Psaroniaceae

Assise de la Houve, zone de St-Avold, mines de la Houve

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris (Eupecopteris) bucklandii Brongniart

Psaroniaceae

Radstockian Series; Somerset and Bristol Coalfields, South Wales Coalfield. Staffordian Series; Somerset and Bristol Coalfields, Kent Coalfield, UK

Asturian

Kidston (1923e1925)

Pecopteris (Eupecopteris) camertonensis Kidston

Psaroniaceae

Radstockian Series; Somerset and Bristol Coalfields, South Wales Coalfield, UK

Asturian

Kidston (1923e1925)

Pecopteris camertonensis Kidston

Psaroniaceae

Pen˜acorba coal group; Barruelo/Redondo Coalfields, Spain

Upper Cantabrian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris camertonensis Kidston

Psaroniaceae

Barruelo Formation, Carboneros Member, Barruelo/Redondo Coalfields, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris camertonensis Kidston

Psaroniaceae

La Magdalena Coalfield, Sabero Coalfield, Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris cf. camertonensis Kidston

Psaroniaceae

Tormaleo, Cangas del Narcea, Spain

Westphalian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris chihliensis Stockmans et Mathieu

Psaroniaceae

Taiyuan Formation; North China Floral Province; Jungar Banner, Inner Mongolia Autonomous Region, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Pecopteris (Eupecopteris) cisti Brongniart

Psaroniaceae

Radstockian Series; Somerset and Bristol Coalfields. Staffordian Series; Somerset and Bristol Coalfields. UK

Asturian

Kidston (1923e1925)

Pecopteris cistii Brongniart

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Asselian or Sakmarian

Jongmans and Gothan (1935), Rigby (1998), and van Waveren et al. (2007)

Pecopteris clintonii Lesquereux

Psaroniaceae

Assise de la Houve, zone de St-Avold, Petit Roselle, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

313

Psaroniaceae

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Pecopteris aspidioides Sternberg

Continued

314

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris clintonii Lesquereux

Psaroniaceae

Drywood Formation; Missouri Coal Basin, Clary Pit, Henry County, MO, USA

Pennsylvanian

Basson (1968)

Pecopteris daubreei Zeiller

Psaroniaceae

Santa Susana Basin, Spain

Upper Asturian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris daubreei Zeiller

Psaroniaceae

Tineo, Carrasconte (Villablino), cf. Pen˜a Cilda´ Formation, Henarejos, El Bierzo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris daubreei Zeiller

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C

Wagner (1983b)

Pecopteris daubreei Zeiller

Psaroniaceae

Oporto region, Douro Basin, Douro Coalfield, Portugal

Stephanian C

Wagner and Lemos de Sousa (1983)

Pecopteris daubreei Zeiller

Psaroniaceae

Barruelo Formation, Carboneros Member; Sabero Coalfield, Barruelo/Redondo Coalfields, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris daubreei Zeiller

Psaroniaceae

Puerto Ventana, La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris (Asterotheca) daubreei Zeiller

Psaroniaceae

Bassin de houiller de Blanzy et du Creusot; mines de Blanzy, Creusot, Montchanin, France

Stephanien

Zeiller (1906)

Pecopteris daubreei Zeiller

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Asselian or Sakmarian

Jongmans and Gothan (1935), Rigby (1998), and van Waveren et al. (2007)

Pecopteris (Scolecopteris) daubreei Zeiller

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

Waveren et al. (2005, 2007)

Pecopteris deltoidea Wagner

Psaroniaceae

Barruelo Formation, Carboneros Member; Barruelo/Redondo, Valdeo´n, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris densifolia Go¨ppert

Psaroniaceae

Assise de la Houve, zone de St-Avold, Hostenbach, Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris cf. densifolia Go¨ppert

Psaroniaceae

Puertollano Coal Basin, Province of Cuidad Real (La Mancha), Central Spain

Stephanian B

Wagner (1983b)

Pecopteris densifolia Go¨ppert

Psaroniaceae

Tineo, Rengos, Tormaleo, Pen˜a Cilda´ Formation, El Bierzo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris densifolia Go¨ppert

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C

Wagner (1983b)

Pecopteris densifolia Go¨ppert

Psaroniaceae

Douro Basin, Douro Coalfield; Oporto region, Portugal

Stephanian C

Wagner (1983a) and Wagner and Lemos de Sousa (1983)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Barruelo Formation, Carboneros Member; Sabero Coalfield, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris densifolia Go¨ppert

Psaroniaceae

Padochov Formation, Rosice-Oslavany 1st Coal Seam; Boskovice Basin, river Oslava, near Oslavany, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Pecopteris densifolia Go¨ppert

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

van Waveren et al. (2007)

Pecopteris densifolia Go¨ppert

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Asselian or Sakmarian

Jongmans and Gothan (1935), Rigby (1998), and van Waveren et al. (2007)

Pecopteris (Scolecopteris) densifolia Go¨ppert

Psaroniaceae

Manebach Formation; Manebach, Germany

Rotliegend

Barthel (2005)

Pecopteris dentata Brongniart

Psaroniaceae

Drywood Formation; Missouri Coal Basin, Gilkerson’s Ford, Henry County, MO, USA

Pennsylvanian

Basson (1968)

Pecopteris (Asterotheca?) densifolia Go¨ppert

Psaroniaceae

Bassin de houiller de Blanzy; mines de Blanzy (Sainte- He´le`ne), France

Stephanien

Zeiller (1906)

Pecopteris (Asterotheca?) densifolia Go¨ppert

Psaroniaceae

Bassin de houiller de Blanzy; mines de Bert, France

Autunien

Zeiller (1906)

Pecopteris cf. densifolia Go¨ppert

Psaroniaceae

Puerto Ventana, La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Canseco/Rucayo, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris djambiensis Jongmans et Gothan

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Asselian or Sakmarian

Jongmans and Gothan (1935), Rigby (1998), and van Waveren et al. (2007)

Pecopteris fletti Kidston

Psaroniaceae

Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA, USA

Asturian

Oleksyshyn (1982)

Pecopteris (Eupecopteris) fletti Kidston

Psaroniaceae

Radstockian Series; Radstock, Somerset, UK

Asturian

Kidston (1923e1925)

Pecopteris folchwillerensis Corsin

Psaroniaceae

Assise de la Houve, zone de St-Avold, Mines de St Avolde, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris hispanica Wagner

Psaroniaceae

Cin˜era-Matallana Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris huichensis Hsu¨

Psaroniaceae

Taiyuan Formation, North China Floral Province; Huainan Huaibei Coalfield, Anhui Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Pecopteris cf. hutchetii Corsin

Psaroniaceae

Ervedosa, Oporto region, Portugal

Gzhelian; upper Asturian

Wagner and Lemos de Sousa (1983)

Pecopteris hutchetii Corsin

Psaroniaceae

Assise de Sulzbach, Neunkirchen Group, Petit Rosselle, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

315

Psaroniaceae

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Pecopteris cf. densifolia Go¨ppert

Continued

316

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris incerta Corsin

Psaroniaceae

Assise de la Houve, zone de St-Avold, Mines de St Avolde, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris integra Andrae in Germar

Psaroniaceae

Radstockian Series, Farrington Group: Glamorganshire, UK

Asturian

Kidston (1923e1925)

Pecopteris integra Andrae in Germar

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C

Wagner (1983b)

Pecopteris integra (Andrae) Schimper

Psaroniaceae

Jangseong Formation, BeC horizons; Samcheong Coalfield, Korea

Asselian

Chun (1985)

Pecopteris jongmansii Wagner

Psaroniaceae

Puertollano Coal Basin, Province of Cuidad Real (La Mancha), Central Spain

Stephanian B

Wagner (1983b)

Pecopteris jongmansii Wagner

Psaroniaceae

Tineo, Rengos, Tormaleo, Henarejos, El Bierzo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris jongmansii Wagner

Psaroniaceae

Puerto Ventana, La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris jongmansii Wagner

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C

Wagner (1983b)

Pecopteris lativenosa Halle

Psaroniaceae

Uppermost Taiyuan Formation, Wuda Tuff; North China Block, Wuda, Inner Mongolia Autonomous Region, China

Gzhelian Asselian

Wang and Pfefferkorn (2013)

Pecopteris laxenervosa Wagner et Lemos de Sousa

Psaroniaceae

Santa Susana Basin, Spain

Upper Asturian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris laxenervosa Wagner et Lemos de Sousa

Psaroniaceae

Carrasconte subarea, Villablino Coalfield, Pen˜a Cilda´ Formation, El Bierzo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris laxenervosa Wagner et Lemos de Sousa

Psaroniaceae

La Magdalena Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris (Lobatopteris) lignyi Stockmans et Willie`re

Psaroniaceae

Pen˜arroya-Belmez Coalfield; Guadiato region, Province of Co´rdoba, Spain

Westphalian B

Wagner (1983b)

Pecopteris limae Teixeira

Psaroniaceae

Oporto region, Douro Basin, Douro Coalfield, Portugal

Stephanian C

Wagner (1983a), Wagner and Lemos de Sousa (1983)

Pecopteris linsiana Stockmans et Mathieu

Psaroniaceae

Taiyuan Formation; North China Floral Province, Tangshan Prefecture, Hebei Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Pecopteris liuiana Lee

Psaroniaceae

Taiyuan Formation; Northwest China Floral Province; N. Qilian Mt., Xizang Autonomous Region, China

Asselian

Shen (1995) (Li, 1995)

Pecopteris lobulata Dalinval

Psaroniaceae

Sierra de la Demanda, Spain

Lower Asturian

´ lvarezWagner and A Va´zquez (2010)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

La Magdalena Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris (Acitheca) longifolia Brongniart

Psaroniaceae

Assise de la Houve, zone de St-Avold, Sarrebruck Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris longiphylla Corsin

Psaroniaceae

Assise de la Houve, zone de St-Avold, Victoria (Pu¨ttlingen), Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris macronervosa Corsin

Psaroniaceae

Assise de Sarrelouis, zone de Dilsburg, Sarre Coalfield, Griesborn, France

Stephanian

Corsin (1951)

Pecopteris melendezii Wagner

Psaroniaceae

Tineo, Rengos, Tormaleo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris melendezii Wagner

Psaroniaceae

Douro Basin, Douro Coalfield; Opporto region, Portugal

Stephanian C

Wagner and Lemos de Sousa (1983)

Pecopteris melendezii Wagner

Psaroniaceae

La Pernia Coalfield, Spain

Upper Asturian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris melendezii Wagner

Psaroniaceae

Pen˜acorba coal group; Guardo Coalfield, Spain

Upper Cantabrian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris melendezii Wagner

Psaroniaceae

Barruelo Formation, Carboneros Member; Sabero Coalfield, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris melendezii Wagner

Psaroniaceae

Puerto Ventana, La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Canseco/Rucayo, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris mengkarangensis Jongmans et Gothan

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Asselian or Sakmarian

Jongmans and Gothan (1935) and van Waveren et al. (2007)

Pecopteris microphylla Corsin

Psaroniaceae

Assise de la Houve, zone de St-Avold, Victoria (Pu¨ttlingen), Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris (Eupecopteris) minor Kidston

Psaroniaceae

Lanarkian Series; Ayrshire and Lanarkshire Coalfields, UK

Duckmantian

Kidston (1923e1925)

Pecopteris monyi Zeiller

Psaroniaceae

Puertollano Coal Basin, Province of Cuidad Real (La Mancha), Central Spain

Stephanian B

Wagner (1983b)

Pecopteris monyi Zeiller

Psaroniaceae

Amao Coalfield, Carrasconte subarea, Villablino Coalfield, Pen˜a Cilda´ Formation, Henarejos, El Bierzo, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris monyi Zeiller

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C

Wagner (1983b)

Pecopteris monyi Zeiller

Psaroniaceae

Douro Basin, Douro Coalfield; Oporto region, Portugal

Stephanian C

Wagner (1983a) and Wagner and Lemos de Sousa (1983)

Pecopteris monyi Zeiller

Psaroniaceae

Post-Leonian basin, northern Palencia, Cantabrian Mts., NW Spain

Asturian

Wagner and Varker (1971) Continued

317

Psaroniaceae

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Pecopteris longifolia Brongniart

318

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris monyi Zeiller

Psaroniaceae

Santa Susana Basin, Guardo Coalfield, La Pernia, Spain

Upper Asturian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris monyi Zeiller

Psaroniaceae

Pen˜acorba coal group; Barruelo/Redondo, Tejerina/Ocejo de la Pen˜a, Spain

Cantabrian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris monyi Zeiller

Psaroniaceae

Barruelo Formation, Carboneros Member; Sabero Coalfield, Valdeo´n, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris monyi Zeiller

Psaroniaceae

La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris monyi Zeiller

Psaroniaceae

Taiyuan Formation; North China Floral Province; Tangshan City, Hebei Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Pecopteris monyi Zeiller

Psaroniaceae

Manebach Formation; Manebach, Kammerberg, Germany

Rotliegend

Barthel (2005)

Pecopteris monyi Zeiller

Psaroniaceae

Irian Jaya, Locality B, West New Guinea

Early Permian

Asama et al. (1975), Visser and Hermes (1962) and Rigby (1998)

Pecopteris monyi Zeiller

Psaroniaceae

Jangseong Formation, BeC horizons; Samcheong Coalfield, Korea

Asselian

Chun (1985)

Pecopteris nyranensis N
emejc

Psaroniaceae

Ervedosa, Oporto region, Portugal

Upper Asturian

Wagner and Lemos de Sousa (1983)

Pecopteris obliquenervis Corsin

Psaroniaceae

Riosa/Olloniego and Aller/Nalo´n areas of the Central Asturian Coalfield, Spain

Lower Asturian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris cf. obliquenervis Corsin

Psaroniaceae

Santa Susana Basin, Spain

Upper Asturian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris cf. obliquenervis Corsin

Psaroniaceae

Olloniego Formation; Central Asturian Coalfield, Locality 14, Malpica, Spain

Lower to middle Asturian

Wagner (1971)

Pecopteris obliquenervis Corsin

Psaroniaceae

Assise de la Houve, zone de Forbach, Sarre and Moselle Coalfields, Merlebach, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris ocejensis Wagner

Psaroniaceae

Post-Leonian basin, northern Palencia, Cantabrian Mts., NW Spain

Asturian

Wagner and Varker (1971)

Pecopteris opulenta Corsin

Psaroniaceae

Assise de la Houve, zone de Faulquemont, mines de Hautes-Vigneulles, and zone de StAvold, Faulquemont Coalfields, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris oreopteridia Schlotheim

Psaroniaceae

Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA, USA

Westphalian B

Oleksyshyn (1982)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Bassin de houiller de Blanzy et du Creusot; mines de Blanzy, Longpendu, Montchanin, France

Stephanian

Zeiller (1906)

Pecopteris oreopteridia Schlotheim

Psaroniaceae

Bassin de houiller de Blanzy et du Creusot; Charmoy, France

Autunien

Zeiller (1906)

Pecopteris oreopteridia Schlotheim

Psaroniaceae

South Staffordshire Coalfield; Red Clay Series, Granville Clay Pit, Old Hill, UK

Staffordian Series Middle Coal Measures

Arber (1916)

Pecopteris (Scolecopteris) oreopteridia Schlotheim ex Sternberg

Psaroniaceae

Weissig Basin, Elbe lineament, near Dresden, Saxony, Germany

Asselian

Barthel et al. (2010)

Pecopteris oreopteridia Schlotheim

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Asselian or Sakmarian

Jongmans and Gothan (1935) and van Waveren et al. (2007)

Pecopteris (Scolecopteris) oreopteridia Schlotheim

Psaroniaceae

¨ hrenkammer, Alltel Georgenthal Formation; O und Stollenwand, Stollenhalde am Regenberg. Manebach Formation; Pfannthal, Seitental des Gabelbaches, Burgberg bei Breitenbach, Manebach. Goldlauter Formation; Mittelberg, Sperbersbach, La¨ndergraben. Oberhof Formation; Schweizerhu¨tt Rd, Lochbrunnen excavation, Germany

Rotliegend

Barthel (2005)

Pecopteris orientalis (Shenk) Potonie´

Psaroniaceae

Mengkarang Formation; Merangin river locality13,14,16, Bangko of Jambi Province, Sumatra, Indonesia

Asselian

Waveren et al. (2005)

Pecopteris orientalis (Schenk) Potonie´

Psaroniaceae

Jangseong Formation, BeC horizons; Samcheong Coalfield, Korea

Asselian

Chun (1985)

Pecopteris orientalis (Schenk) Potonie´

Psaroniaceae

Taiyuan Formation; Northwest China Floral Province; Huainan Huaibei Coalfield, Anhui Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

Pecopteris orientalis (Schenk) Potonie´

Psaroniaceae

Irian Jaya, Locality A, along Otakwa River, West New Guinea

Early Permian

Jongmans (1940) and Asama et al. (1975)

Pecopteris orientalis (Shenk) Potonie´

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

van Waveren et al. (2007)

Pecopteris cf. paleacea Zeiller

Psaroniaceae

Puertollano Coal Basin, Province of Cuidad Real (La Mancha), Central Spain

Stephanian B

Wagner (1983b)

Pecopteris paleacea Zeiller

Psaroniaceae

Tineo, Carrasconte subarea, Villablino Coalfield, Cabrales Coalfield, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris paleacea Zeiller

Psaroniaceae

Barruelo Formation, Carboneros Member; Barruelo/Redondo Coalfields, Sabero Coalfield, Valdeo´n, Spain

Barruelian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris paleacea Zeiller

Psaroniaceae

Puerto Ventana, La Magdalena, Cin˜eraMatallana Coalfield, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Continued

319

Psaroniaceae

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Pecopteris oreopteridia Schlotheim

320

Species

Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris paleacea Zeiller

Psaroniaceae

Assise de Sarrelouis, Dilsburg, Mines de la Houve, Sarre Coalfield, Ensdorf, France

Stephanian

Corsin (1951)

Pecopteris parvula Vetter

Psaroniaceae

Carrasconte subarea, Villablino Coalfield, Spain

Stephanian B

´ lvarezWagner and A Va´zquez (2010)

Pecopteris paucinervis

Psaroniaceae

Irian Jaya, Locality A, along Otakwa River, West New Guinea

Early Permian

Jongmans (1940) and Asama et al. (1975)

Pecopteris cf. pectinata Corsin

Psaroniaceae

La Magdalena Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris pectinata P. Bertrand

Psaroniaceae

Assise de la Houve, zone de St-Avold, mines de la Houve, Sarre Coalfield, Victoria (Pu¨ttlingen), France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris pilosa Dawson

Psaroniaceae?

Cumberland Group; Greville Bay, Cumberland County, Nova Scotia, Canada

Westphalian B

Bell (1944)

Pecopteris pilosa Dawson

Psaroniaceae?

Assise de la Houve, zone de St-Avold, mines de la Houve, Sarre Coalfield, Victoria, (Pu¨ttlingen), France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris platonii Grand’Eury

Psaroniaceae

Assise de la Houve, zone de Forbach, Ja¨gersfreude, Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris polita Corsin

Psaroniaceae

Assise de la Houve, zone de St-Avold, Hostenbach, Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris cf. polita Corsin

Psaroniaceae

La Magdalena Coalfield, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

´ lvarezWagner and A Va´zquez (2010)

Pecopteris polypodioides Knight

Psaroniaceae


´
cany Horizon, NesloPadochov Formation, Rı vice Fish Rock locality, near Neslovice, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Pecopteris pseudo-bucklandii Andrae

Psaroniaceae

Bassin de houiller de Blanzy et du Creusot; mines de Bert, France

Autunien

Zeiller (1906)

Pecopteris pseudobucklandii (Andrae in Germar) Stur

Psaroniaceae

Weissig Basin, Elbe lineament, near Dresden, Saxony, Germany

Asselian

Barthel et al. (2010)

Pecopteris cf. pseudobucklandii (Andrae in Germar) Stur

Psaroniaceae

Padochov Formation, Rosice-Oslavany 1st Coal Seam; Boskovice Basin, river Oslava, near Oslavany, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Pennsylvanian Occurrencesdcont’d

Pecopteris (Scolecopteris) pseudobucklandii (Andrae in Germar) Stur

Rotliegend

Barthel (2005)

Psaroniaceae

Drywood Formation; Missouri Coal Basin, Clary Pit, Henry County, MO, USA

Pennsylvanian

Basson (1968)

Pecopteris pseudovestita White

Psaroniaceae

Carbondale Formation, Francis Creek Shale; “Mazon Creek,” Will County, IL, USA

Lower Cantabrian

Noe´ (1925)

Pecopteris (Eupecopteris) pteroides Brongniart

Psaroniaceae

Radstockian Series; Somerset and Bristol Coalfield, UK

Asturian

Kidston (1923e1925)

Pecopteris (Asterotheca) punctata Corsin

Psaroniaceae

Olloniego Formation; NW. border Central Asturian Coalfield, Locality 15, Spain

Asturian

Wagner (1971)

Pecopteris punctata Corsin

Psaroniaceae

Assise de la Houve, zone de St-Avold, Petit Rosselle, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris raconensis N
emejc

Psaroniaceae

Post-Leonian basin, northern Palencia, Cantabrian Mts., NW Spain

Asturian

Wagner and Varker (1971)

Pecopteris raconensis N
emejc

Psaroniaceae

Pen˜acorba coal group; Guardo Coalfield, Tejerina/Ocejo de la Pen˜a, Spain

Cantabrian

Wagner and A´lvarezVa´zquez (2010)

Pecopteris raconensis N
emejc

Psaroniaceae

Santa Susana Formation, Guardo Coalfield, La Pernia, Spain

Upper Asturian

Wagner and A´lvarezVa´zquez (2010)

Pecopteris rarinervosa Corsin

Psaroniaceae

Assise de Potzberg, Sarre Coalfield, Reisweiler; Assise de Sarrelouis, zone de Dilsburg, Sarre Coal field, Griesborn, France

M. Stephanian

Corsin (1951)

Pecopteris robustissima Wagner

Psaroniaceae

Tineo, Rengos, Tormaleo, Carrasconte subarea, Villablino Coalfield, El Bierzo, Spain

Stephanian B

Wagner and A´lvarezVa´zquez (2010)

Pecopteris robustissima Wagner

Psaroniaceae

Puerto Ventana, La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Leo´n Province, NW Spain

Saberian

Wagner and A´lvarezVa´zquez (2010)

Pecopteris robustissima Wagner

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C

Wagner (1983b)

Pecopteris rotundifolia Corsin

Psaroniaceae

Assise de Sarrelouis, zone de Dilsburg, Sarre Coalfield, Ensdorf, Griesborn, France

Stephanian

Corsin (1951)

Pecopteris sahnii Hsu¨

Psaroniaceae

Taiyuan Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province, China

Asselian

Shen (1995) (Li, 1995) (Li, 1995)

321

Pecopteris pseudovestita White

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

¨ hrenkammer, Alltel Georgenthal Formation; O und Stollenwand bei Kleinschmalkalden, Stollenhalde am Regenberg in Zella-Mehlis. Manebach Formation; Crock, Grube Furchtegott im Pfannthal, Sachsendelle unter der Schmu¨cke, Manebach, Burgberg und Homigtal bei Breitenbach. Goldlauter Formation; Pochwerksgrund, Tambacher Tal, Mittelberg, Sperbersbach, Langerainspitze am Bhf. Gehlberg. Oberhof Formation; Langes Tal zwischen Mo¨st und Rennsteig, Germany

Continued

322

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris saraefolia P. Bertrand

Psaroniaceae

Assise de la Houve, zone de Forbach, Merlebach, Faulquemont Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris saraei Corsin

Psaroniaceae

Assise de Sulzbach, Neunkirchen, Mines de la Sarre, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris saraepontana Stur

Psaroniaceae

Assise de la Houve, zone de St-Avold, Victoria (Beust-Heinrich), France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris squamosa Lesquereux

Psaroniaceae?

Carbondale Formation, Francis Creek Shale; “Mazon Creek,” Will County, IL, USA

Lower Cantabrian

Noe´ (1925)

Pecopteris cf. subcrenulata Lesquereux

Psaroniaceae

Pen˜a Cilda´ Formation; E. Cordillera Canta´brica, Spain

Stephanian B

Wagner and A´lvarezVa´zquez (2010)

Pecopteris subcrenulata (Lesquereux) Wittry

Psaroniaceae

Henryetta Coal (Croweburg Coal equivalent); Okmulgee County, between Okmulgee and Morris, OK, USA

Middle Pennsylvanian

Moore et al. (2013)

Pecopteris tenuinervosa Corsin

Psaroniaceae

Assise de la Houve, Mines de Petit- Roselle, Sarre and Moselle Coalfields, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris ticleanui Popa et P
seni
cka

Psaroniaceae

Res‚it‚a Formation; South Carpathian Mountains, Res‚it‚a Basin, Secu, Romania

Asturian-Stephanian

Popa and P
seni
cka (2010)

Pecopteris trevirani (Go¨ppert) Presl in Sternberg

Psaroniaceae

Barruelo Formation, Carboneros Member; Sabero Coalfield, Spain

Barruelian

Wagner and A´lvarezVa´zquez (2010)

Pecopteris (Orthotheca) treviranii Goeppert

Psaroniaceae

Assise de la Houve, zone de St-Avold, Victoria (Pu¨ttlingen), France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris truncata Rost

Psaroniaceae

Pen˜acorba coal group; Gamonedo/Inguanzo, Spain

Cantabrian

Wagner and A´lvarezVa´zquez (2010)

Pecopteris (Asterotheca) truncata Rost

Psaroniaceae

Bassin de houiller de Blanzy et du Creusot; mines de Blanzy, Sainte-He´le`ne, France

Stephanian

Zeiller (1906)

Pecopteris unitaeformis Jongmans et Gothan

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Asselian or Sakmarian

Jongmans and Gothan (1935) and van Waveren et al. (2007)

Pecopteris cf. vera Gastaldo et Matten

Psaroniaceae

La Magdalena Coalfield, Leo´n Province, NW Spain

Saberian

Wagner and A´lvarezVa´zquez (2010)

Pecopteris (Scolecopteris) verbeekii Jongmans et Gothan

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

Jongmans and Gotha (1935) and van Waveren et al. (2007)

Pecopteris verbeekii Jongmans et Gothan

Psaroniaceae

Mengkarang Formation; Merangin river locality16, Bangko of Jambi Province, Sumatra, Indonesia

Asselian

Waveren et al. (2005)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Pecopteris vestita Lesquereux

Psaroniaceae

Carbondale Formation, Francis Creek Shale; “Mazon Creek,” Will County, IL, USA

Lower Cantabrian

Noe´ (1925)

Pecopteris victoriae Corsin

Psaroniaceae

Assise de la Houve, zone de St. Avold, Hostenbach, Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris villosa Brongniart

Psaroniaceae

Assise de la Houve, zone de St-Avold, Victoria (Pu¨ttlingen) and Ja¨gersfreude, Sarre Coalfield, France

Westphalian E´tage de Sarrebru¨ck

Corsin (1951)

Pecopteris (Eupecopteris) villosa Brongniart

Psaroniaceae

Radstockian Series; Somerset and Bristol Coalfield, UK

Asturian

Kidston (1923e1925)

Pecopteris waltonii Corsin

Psaroniaceae

Assise de Sarrelouis, zone de Go¨ttelborn; Assise de la Houve, Petite Rosselle, France

Stephanian

Corsin (1951)

Pecopteris wongi Corsin (non Halle)

Psaroniaceae

Assise de Sarrelouis, zone de Dilsburg, Sarre Coalfield, Griesborn, France

Stephanian

Corsin (1951)

Polymorphopteris cistii (Brongniart) Wagner

Psaroniaceae

Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA, USA

Westphalian B

Oleksyshyn (1982)

Polymorphopteris folchwillerensis (Corsin) Knight

Psaroniaceae

Barruelo Formation, Carboneros Member, Sabero Coalfield, Spain

Barruelian

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris folchwillerensis (Corsin) Knight

Psaroniaceae

La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Leo´n Province, NW Spain

Saberian

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris integra (Andrae) Wagner

Psaroniaceae

La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Leo´n Province, NW Spain

Saberian

Wagner (1999) and Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris integra (Andrae) Wagner

Psaroniaceae

Carrasconte and Villablindo subarea, El Bierzo, Leo´n Province, Spain

Stephanian B

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris cf. magdalenae Wagner

Psaroniaceae

Barruelo Formation, Carboneros Member, Sabero Coalfield, Spain

Barruelian

Wagner (1964) and Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris magdalenae Wagner

Psaroniaceae

La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Leo´n Province, NW Spain

Saberian

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris magdalenae Wagner

Psaroniaceae

Pen˜a Cilda´ Formation, Pen˜a Cilda´, Spain

Stephanian B

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris multifurcata Wagner

Psaroniaceae

Pen˜acorba coal group; Guardo Coalfield, Spain

Cantabrian

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris multifurcata Wagner

Psaroniaceae

Barruelo Formation, Carboneros Member, Sabero Coalfield, Spain

Barruelian

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris multifurcata Wagner

Psaroniaceae

Sabero Coalfield, Leo´n Province, NW Spain

Saberian

Wagner and A´lvarezVa´zquez (2010)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

cf. Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

Ervedosa, Oporto region, Portugal

Upper Asturian

Wagner and Lemos de Sousa (1983)

323

Continued

324

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

Northern Anthracite coal basin, Llewellyn Formation, Baltimore coal bed; Wanamie, near Wilkes-Barre, PA, USA

Asturian

Oleksyshyn (1982)

Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

Puertollano Coal Basin, Province of Cuidad Real (La Mancha), Central Spain

Stephanian B

Wagner (1983b)

Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

Tineo, Rengoes, Tormaleo, Puente Pumar, Henarejos, El Bierzo, Spain

Stephanian B

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C

Wagner (1983b)

Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

Douro Basin, Douro Coalfield; Oporto region, Portugal

Stephanian C

Wagner et Lemos de Sousa (1983)

Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

Post-Leonian basin, northern Palencia, Cantabrian Mts., NW Spain

Asturian

Wagner and Varker (1971)

Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

Barruelo Formation, Carboneros Member, Sabero Coalfield, Spain

Barruelian

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

Pen˜acorba coal group; Barruelo/Redondo, Guardo Coalfield, Tejerina/Ocejo de la Pen˜a, Spain

Cantabrian

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

Guardo Coalfield, La Pernı´a, Spain

Upper Asturian

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris polymorpha (Brongniart) Wagner

Psaroniaceae

Puerto Ventana, La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Canseco/Rucayo, Sabero Coalfield, Leo´n Province, NW Spain

Saberian

Wagner (1959) and Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris (Pecopteris) polymorpha (Brongniart) Wagner

Psaroniaceae


´
cany Horizon, NesloPadochov Formation, Rı vice Fish Rock locality, near Neslovice, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Polymorphopteris pseudobucklandii (Andrae) Wagner

Psaroniaceae

Tineo, Rengos, Tormaleo, Spain

Stephanian B

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris sotillosensis Stockmans & Willie`re

Psaroniaceae

Sabero Coalfield, Leo´n Province, NW Spain

Saberian

Wagner and A´lvarezVa´zquez (2010) and Stockmans and Willie`re (1965)

Polymorphopteris subelegans (Potonie´) sensu Wagner

Psaroniaceae

Tineo, Rengos, Tormaleo, Carrasconte and Villableno subarea, Pen˜a Cilda´, El Bierzo, Spain

Stephanian B

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris subelegans (Potonie´) sensu Wagner

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C

Wagner (1983b)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Psaroniaceae

Puerto Ventana, La Magdalena Coalfield, Cin˜era-Matallana Coalfield, Leo´n Province, NW Spain

Saberian

Wagner and A´lvarezVa´zquez (2010)

Polymorphopteris villablinensis Wagner

Psaroniaceae

Puertollano Coal Basin, Province of Cuidad Real (La Mancha), Central Spain

Stephanian B

Wagner (1983b)

Polymorphopteris villablinensis Wagner

Psaroniaceae

El Bierzo, NW Leo´n, NW Spain

Lower Stephanian C, Saberian

Wagner (1983b)

Psaronius Cotta sp.

Psaroniaceae

coal seam m3, Donetsk Basin; Donetsk, Ukraine

Westfalian D, Moscovian

Snigirevskaya (1972)

Psaronius Cotta sp.

Psaroniaceae

Manebach Formation; Manebach, Oberflo¨z, Germany

Rotliegend

Barthel (2005)

Psaronius blicklei Morgan

Psaroniaceae

Mattoon Formation, McLeansboro Group; “Berryville,” Sumner, Lawrence County, IL, USA

Late Pennsylvanian

Morgan (1959)

Psaronius chasei (Morgan) Mickle

Psaroniaceae

Mattoon Formation, McLeansboro Group; “Berryville,” Sumner, Lawrence County, IL, USA

Late Pennsylvanian

Morgan (1959) and Mickle (1984)

Psaronius hexagonus “Gu et Zhi”

Psaroniaceae

Emeishan Formation; Sichuan Province, China

Early Permian

Li and Cui (1995)

Psaronius magnificus Rothwell et Blickle

Psaroniaceae

Upper Conemaugh-lower Monongahela Group; Lodi Township, Athens County, OH, USA

Late Pennsylvanian

Rothwell and Blickle (1982)

Psaronius melanedrus Morgan

Psaroniaceae

Cherokee Group, Des Moines Series; West Mineral, Cherokee County, KS, USA

Middle Pennsylvanian

Morgan (1959)

Psaronius musaeformis Corda

Psaroniaceae

Leukersdorf Formation, Erzgebirge Basin, Zeisigwald Tuff Horizon; Chemnitz, Saxony, Germany

Early Permian

Corda (1845)

Psaronius paucivasculosis (Blickle) Mickle

Psaroniaceae

Under Connellsville Sandstone, Upper Conemaugh Group; Shade, Lodi Township, Athens County, OH, USA

Late Pennsylvanian

Mickle (1984)

Psaronius renaultii Williamson

Psaroniaceae

Scottish Lower Coal Measures; County Ayrshire, Scotland, UK

Low in Westphalian A

Williamson (1876)

Psaronius schopfii Mickle

Psaroniaceae

Upper Conemaugh-lower Monongahela Group; Shade, Lodi Township, Athens County, OH. USA

Late Pennsylvanian

Mickle (1984)

Psaronius simplex Unger

Psaroniaceae

Chemnitz, Germany; Autun, France

Middle Rotliegendes

Zeiller (1890)

Psaronius simplex Unger

Psaroniaceae

Assise de Millery; Autun Basin, Autun, Central France

Upper Autunian

Stenzel (1854, 1906)

nius Psaronius simplicicaulis DiMichele et Phillips

Psaroniaceae

Illinois Coal Basin; Vandruff Island, Milan, Rock Island County, IL, USA

Morrowan (Leary, 1974)

DiMichele and Phillips (1977)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Polymorphopteris subelegans (Potonie´) sensu Wagner

325

Continued

326

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Radstockia kidstonii Taylor

Seed fern?

Carbondale Formation, Francis Creek Shale; “Mazon Creek,” Will County, IL, USA

Lower Cantabrian

Taylor (1967)

Rajahia (Pecopteris) pseudohemitelioides Kon’no

Psaroniaceae

Mengkarang Formation; Bangko of Jambi Province, Sumatra, Indonesia

Asselian or Sakmarian

van Waveren et al. (2007)

Remia pinnatifida (Gutbier) Knight, emend Cleal

Psaroniaceae

Sabero Coalfield, Leo´n, NW. Spain

Stephanian Barruelian

Knight (1985) and emend Cleal (2015)

Remia pinnatifida (Gutbier) Knight, emend Cleal

Psaroniaceae

Sabero Coalfield, Leo´n, NW. Spain

Barruelian

Wagner and A´lvarezVa´zquez (2010)

Remia pinnatifida (Gutbier) Knight, emend Cleal

Psaroniaceae

Cin˜era-Matallana Coalfield, Leo´n Province, NW Spain

Saberian

Wagner and A´lvarezVa´zquez (2010)

Remia (Pecopteris) pinnatifida (Gutbier) Knight

Psaroniaceae

Mauchline Volcanic Group; Mauchline Basin, Mauchline Parrish, on River Ayr, Scotland

Lower Rotliegend

Wagner (1966)

Remia pinnatifida (Gutbier) Knight

Psaroniaceae

Weissig Basin, Elbe lineament, near Dresden, Saxony, Germany

Asselian

Barthel et al. (2010)

Remia pinnatifida (Gutbier) Knight

Psaroniaceae


´
cany Horizon, NesloPadochov Formation, Rı vice Fish Rock locality, near Neslovice, Czech Republic

Asselian


Sim unek and Martı´nek (2009)

Remia pinnatifida (Gutbier) Knight

Psaroniaceae

Padochov Formation, Zbon
ek-Svita´vka Horizon; Svita´vka locality, Hadisko Hill, near Boskovice, Czech Republic

Lower Sakmarian


Sim unek and Martı´nek (2009)

Remia pinnatifida (Gutbier) Knight

Psaroniaceae

Manebach Formation; Crock, Manebach, Mordflek. Goldlauter Formation; Arnsburg, Mittelberg, Benshausen, Sperberbach, Weinstrasse. Rotterode Formation: Gasberg bei Rotterode. Oberhof Formation; Schuchardstkopf, Donaurasen, Mo¨st, Mo¨sewegwiese bei Tambach, Lochbrunnen und Bahnhof Oberhof. Germany

Rotliegend

Barthel (2005)

Scolecopteris (Cyathotrachus) alta Watson

Psaroniaceae

Lanarkian Series; Shore, Lancashire, England, UK

Westphalian A

Watson (1906)

Scolecopteris (Cyathotrachus) alta (Watson) Millay

Psaroniaceae

Breathitt Formation; “Lewis Creek,” Leslie County, KY, USA

Lower Middle Penn.

Millay (1982b)

Scolecopteris (Cyathotrachus) altissima (Mamay) Millay

Psaroniaceae

Cherokee Group, Des Moines Series; Urbandale Mine, Polk County, IA, USA

Middle Pennsylvanian

Mamay (1950) and Millay (1982b)

Scolecopteris calicifolia Millay

Psaroniaceae

Cherokee Group, Des Moines Series; West Mineral, Cherokee County, KS, USA

Middle Pennsylvanian

Millay (1979)

Scolecopteris charma Lesnikowska et Millay

Psaroniaceae

Conemaugh Group, Duquesne Coal; Steubenville, Jefferson County, OH, USA

Late Pennsylvanian

Lesnikowska and Millay (1985)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Breathitt Formation; “Lewis Creek,” Leslie County, KY, USA

Middle Pennsylvanian

Millay (1982c)

Scolecopteris dispora Lesnikowska et Willard

Psaroniaceae

Cliffland Coal Member; Schuler Mine, Polk County, IA, USA

Early or late Bolsovian

Lesnikowska and Willard (1997)

Scolecopteris elegans (Zenker) Barthel

Psaroniaceae

Bannewitz Formation, Do¨hlener Basin; Kleinnaundorf, Germany

Rotliegend

Zenker (1837), Strasburger (1874), and Barthel (1976)

Scolecopteris fragilis Millay

Psaroniaceae

Cherokee Group, Des Moines Series; “What Cheer,” Keokuk County, IA, USA

Middle Pennsylvanian

Millay (1979)

Scolecopteris globiforma Millay et Galtier

Psaroniaceae

Poudingue Mosaı¨que; Grand Croix, near St. E´tienne, department Loire, France

Stephanian

Millay and Galtier (1990)

Scolecopteris gnoma Lesnikowska and Millay

Psaroniaceae

Sturgis Formation, Baker Coal; Providence, Webster County, KY, USA

Middle Pennsylvanian

Lesnikowska and Millay (1985)

Scolecopteris illinoensis Ewart

Psaroniaceae

Mattoon Formation, McLeansboro Group; “Berryville,” Sumner, Lawrence County, IL, USA

Late Pennsylvanian

Ewart (1961) and Millay (1979)

Scolecopteris incisifolia Mamay

Psaroniaceae

Lower to middle Cherokee Group, Des Moines Series; Urbandale Mine, Polk County, IA, USA

Middle Pennsylvanian

Mamay (1950)

Scolecopteris iowensis (Mamay) Millay

Psaroniaceae

Lower to middle Cherokee Group, Des Moines Series; Urbandale Mine, Polk County, IA, USA

Middle Pennsylvanian

Mamay (1950) and Millay (1979)

Scolecopteris latifolia (Graham) Mamay

Psaroniaceae

Mattoon Formation, McLeansboro Group, Calhoun Coal; Calhoun coal mine, Richland County, IL, USA

Late Pennsylvanian

Graham (1934) and Mamay (1950)

Scolecopteris latifolia (Graham) Mamay

Psaroniaceae

Carbondale Formation, Kewanee Group; Sahara Mine, Carrier Mills, Saline County, IL. Lisman Formation, Allegheny Series; Providence, Webster County, KY. Cabanis Formation, Cherokee Group, Des Moines Series, P & M Mine, West Mineral, Cherokee County, KS, USA

Middle Pennsylvanian

Millay (1979)

Scolecopteris macrospora Jennings and Millay

Psaroniaceae

Carbondale Formation, Kewanee Group; Carterville, Williamson County, IL, USA

Middle Pennsylvanian

Jennings and Millay (1978)

Scolecopteris majopsis Millay

Psaroniaceae

Carbondale Formation, Kewanee Group; Sahara Mine, Carrier Mills, Saline County, IL, USA

Middle Pennsylvanian

Millay (1979)

Scolecopteris major Mamay

Psaroniaceae

Lower to middle Cherokee Group, Des Moines Series; Urbandale Mine, Polk County, IA, USA

Middle Pennsylvanian

Mamay (1950)

Scolecopteris mamayi Millay

Psaroniaceae

Lisman Formation, Allegheny Series; Providence, Webster County, KY, USA

Middle Pennsylvanian

Millay (1979)

327

Psaroniaceae

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Scolecopteris conicaulis Millay

Continued

328

Pennsylvanian Occurrencesdcont’d Family

Stratigraphy/Geography

Age (Ma)

References

Scolecopteris minor Hoskins

Psaroniaceae

McLeansboro Group; Danville #7 coal, Hegler mine, Danville, Vermilion County, IL, USA

Late Pennsylvanian

Hoskins (1926)

Scolecopteris minor (Hoskins) var. parvifolia (Graham) Mamay

Psaroniaceae

Lower to Middle Cherokee Group, Des Moines Series; Urbandale Mine, Polk County, IA, USA

Middle Pennsylvanian

Graham (1934) and Mamay (1950)

Scolecopteris monothrix Ewart

Psaroniaceae

Mattoon Formation, McLeansboro Group; “Berryville,” Sumner, Lawrence County, IL, USA

Late Pennsylvanian

Ewart (1961)

Scolecopteris nigra Millay

Psaroniaceae

Carbondale Formation, Kewanee Group; Sahara Mine, Carrier Mills, Saline County, IL, USA

Middle Pennsylvanian

Millay (1982b)

Scolecopteris oliverii Scott

Psaroniaceae

Assise de Millery; Autun Basin, Autun, Central France

Upper Autunian

Scott (1932)

Scolecopteris parkerensis Lesnikowska et Willard

Psaroniaceae

Patoka Formation, Missourian Provincial Series; “St. Wendel,” Posey County, IN, USA

Late Pennsylvanian

Lesnikowska and Willard (1997)

Scolecopteris parvifolia (Mamay) Millay

Psaroniaceae

Mattoon Formation, McLeansboro Group; “Berryville,” Sumner, Lawrence County, IL, USA

Late Pennsylvanian

Millay (1979)

Scolecopteris revoluta (Baxter) Millay

Psaroniaceae

Cabanis Formation, Cherokee Group, Des Moines Series; P & M Mine #19, Hallowell, Cherokee County, KS, USA

Middle Pennsylvanian

Baxter (1975) and Millay (1979)

Scolecopteris saharaensis Millay

Psaroniaceae

Carbondale Formation, Kewanee Group; Sahara Mine, Carrier Mills, Saline County, IL, USA

Middle Pennsylvanian

Millay (1979)

Scolecopteris shadensis Stubblefield

Psaroniaceae

Above Connellsville Sandstone; Shade, Athens County, OH, USA

Late Pennsylvanian

Stubblefield (1984)

Scolecopteris shanxiensis Wang et al.

Psaroniaceae

Taiyuan Formation; Taiyuan City, Shanxi Province, China

Early Early Permian

Wang et al. (1999)

Scolecopteris sinensis Zhao

Psaroniaceae

Taiyuan Formation; Shanxi Province, China

Upper Carboniferous

Zhao (1991)

Scolecopteris (Ptychocarpus) unita (Renault) Millay et Galtier

Psaroniaceae

Assise de Millery; Autun Basin, Autun, Central France

Upper Autunian

Renault (1883) and Millay and Galtier (1990)

Scolecopteris vallumii Millay

Psaroniaceae

Carbondale Formation, Kewanee Group; Sahara Mine, Carrier Mills, Saline County, IL, USA

Middle Pennsylvanian

Millay (1979)

Stipitopteris shanxiensis Xiang et al.

Psaroniaceae

Taiyuan Formation; Xisuan Coalfield, Xindao Village, Shanxi Province, China

Sakmarian

Xiang et al. (2008)

Sturiella (Scolecopteris) intermedia (Renault) Weiss

Psaroniaceae

Poudingue Mosaı¨que; Grand Croix, near St. E´tienne, department Loire, France

Stephanian B

Renault (1883) and Lesnikowska and Galtier (1991)

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Species

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

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Permian Occurrences Species

Family

Stratigraphy/Geography

Age (Ma)

References

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Shanxi Formation; Northwest China Floral Province; N. Qilian Mt., Qinghai Province, China

Artinskian

emend Zodrow et al. (2006) and Shen (1995) (Li, 1995)

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Dahuanggou Formation; Northwest China Floral Province; N. Qilian Mt., Hexi Corridor, Qinghai Province, China

Kungurian

Shen (1995) (Li, 1995)

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Shanxi Formation; Inner Mongolia Autonomous Region, Jungar County, Anhui Province, China

Artinskian

Shen (1995) (Li, 1995)

Acitheca (Scolecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Manebach Formation; Manebach, Germany

Rotliegend

Barthel (2005)

Acitheca (Pecopteris?) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Artinskian

Jongmans and Gothan (1925)

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow

Psaroniaceae

Lower Shihhotse Formation; Inner Mongolia Autonomous Region, Jungar County, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar County, Shanxi Province, Inner Mongolia Autonomous Region; W. Henan Province, Tangshan Prefecture, Hebei Province, China

Artinskian

Shen (1995) (Li, 1995)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

335

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Jungar County, Shanxi, Inner Mongolia Autonomous Region; Fengfeng, Shandong Province, China

Kungurian

Shen (1995) (Li, 1995)

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; Tangshan Prefecture, Hebei Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Acitheca (Pecopteris) polymorpha (Brongniart) Zodrow et al.

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Artinskian or Sakmarian

Jongmans and Gothan (1935)

Acitheca salviniaefolia Stockmans et Mathieu

Psaroniaceae

Shansi Formation; North China Floral Province; Shanxi Province, W. Henan Province, and Tangshan Prefecture, Hebei Province, China

Artinskian

Zodrow et al. (2006) (¼Acitheca polymorpha?) and Shen (1995) (Li, 1995)

Acitheca salviniaefolia Stockmans et Mathieu

Psaroniaceae

Shanxi Formation; Northwest China Province N. Qilian Mt., Longshou Mt., Xizang Autonomous Region, China

Artinskian

Shen (1995) (Li, 1995)

Acrogenotheca ramificata Naugolnykn

Psaroniaceae

Middle Fore Urals, Perm Region, Chekarda Locality 1, lower Cisalurian series, Russia

Kungurian

Naugolnykn (2013)

Asterotheca sp. Presl in Corda

Psaroniaceae

Halgaito Formation; Paradox Basin, “Indian Creek,” San Juan County, Utah, USA

Wolfcampian, Lower Permian

DiMichele et al. (2014)

Asterotheca macromarginata Fang

Psaroniaceae

Shansi Formation; North China Floral Province; Huainan Huaibei Coal Field, Anhui Province, China

Artinskian

Shen (1995) (Li, 1995)

Asterotheca orientalis (Schenk) Potonie´

Psaroniaceae

Tafengkou Formation; Pingdingshen Coalfield, District Yehsien, central Henan Province, China

Late Permian

Sze (1954)

Bifariusotheca qinqlongensis Zhao et al.

Psaroniaceae

Quinglong Coalfield, Qinglong County, Guizhou Province, China

Late Permian

Zhao et al. (1980)

Bifariusotheca tetralinea Zhao et al.

Psaroniaceae

Qinglong Coalfield, Quinglong County, Guizhou Province, China

Late Permian

Zhao et al. (1980)

Caulopteris sp. Lindley et Hutton

Psaroniaceae

Manebach Formation; Manebach, Germany

Rotliegend

Barthel (2005)

Caulopteris sp. Lindley et Hutton

Psaroniaceae

Cutler Group, Halgaito Formation; Paradox Basin, Valley of the Gods, Utah, USA

Wolfcampian, Lower Permian

DiMichele et al. (2014)

Cohaerensitheca sahnii (Hsu¨) Liu et Yao

Psaroniaceae

Lungtan Formation, Bed 8; Funiushan Coal Mine, Zhenjiang, Jiangsu Province, China

Lengwuan Stage of Guadalupian

Liu and Yao (2006)

Convexocarpus distichus Naugolnykh

Psaroniaceae

Lower Cisalurian series; Middle ForeUrals, Perm Region, Krutaya Katushka 1,2 and Rakhmangulovo 1,2 localities, Komi Autonomous Republic, Russia

Kungurian

Naugolnykh (2013)

Corsinopteris dicranophora (Naugolnykh) Naugolnykh

Psaroniaceae

Lower Cisalurian series; Middle ForeUrals, Perm Region, Checkarda 1 locality, Komi Autonomous Republic, Russia

Kungurian

Naugolnykh (2013)

Continued

336

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Corsinopteris petschorica (Fefilova) Doweld

Psaroniaceae

Lower Cisalurian series; Middle ForeUrals, near Pechora River, Borehole IK-657 (765 m), Komi Autonomous Republic, Russia

Kazanian, middle Permian

Naugolnykh (2013) and Doweld (2001)

Corsinopteris semiliberia (Naugolnykh) Doweld

Psaroniaceae

Inta Formation; Kozhim River bank, Kozhim 5 locality, Komi Autonomous Republic, Russia

Ufimian

Naugolnykh (2013)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Shanxi Formation; Northwest China Province; N. Qilian Mts., Longshou Mts., Xizang Autonomous Region, China

Artinskian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) cf. arborea (Brongniart) Cleal

Psaroniaceae

Padochov Formation, Ba
cov Horizon; Boskovice Basin, Ba
cov locality, Quarry 3, near Boskovice, Czech Republic

Artinskian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Dahuanggou Formation; Northwest China Floral Province; Longshou Mts., Xizang Autonomous Region, China

Artinskian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Shansi Formation; North China Floral Province; Jungar, Huainan Huaibei Coalfield; Shanxi, W. Henan, S. Liaoning, and W. Jilin Provinces, China

Artinskian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Lower Shiihhotse Formation; North China Floral Province; N. Weihe Basin, Hebei Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) arborea (Brongniart) Cleal

Psaroniaceae

Qiangtang-Yushu Block; Wuli Basin, Golmud City, Qinghai Provence, China

Early Late Permian

Shen (1995) (Li, 1995)

Cyathocarpus arborea (Schlotheim) Cleal

Psaroniaceae

Hambaegsan Formation; Samcheong Coalfield, Korea

Changhsingian

Chun (1985) and Cleal (2015)

Cyathocarpus (Pecopteris) arborea (Schlotheim) Cleal

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Artinskian

Jongmans and Gothan (1935) and Asama et al. (1975)

Cyathocarpus (Pecopteris) arborea (Schlotheim) Cleal

Psaroniaceae

Jangseong Formation, BeC horizons; Samcheong Coalfield, Korea

Asselian or Sakmarian

Chun (1985)

Cyathocarpus badoensis Fang

Psaroniaceae

Lower Shihhotese Formation; North China Floral Province; Huainen Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Cyathocarpus candolleanus (Brongniart) Cleal

Psaroniaceae

Shanxi Formation; Northwest China Floral Province, N. Qilian Mts., Longshou Mts., Xizang Autonomous Region, China

Artinskian

Shen (1995) (Li, 1995)

Cyathocarpus candolleanus (Brongniart) Cleal

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar Banner, Xinjiang; Shanxi Province, W. Henan Province; Fengfeng, Shandong Province, China

Artinskian

Shen (1995) (Li, 1995)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

337

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Cyathocarpus candolleanus (Brongniart) Cleal

Psaroniaceae

Lower Shihhotese Formation; North China Floral Province; Shanxi Province; Huainen Huaibei Coalfield, Anhui Province; Fengfeng, Shandong Province; S. Liaoning and W. Jilin Provinces, China

Kungurian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) candolleanus (Brongniart) Cleal

Psaroniaceae

Residentie Djambi, Sumatra, Indonesia

Artinskian

Jongmans and Gothan (1935)

Cyathocarpus (Pecopteris) cyatheus Schlotheim

Psaroniaceae

Padochov Formation, Mı´chov Horizon; Boskovice Basin, Mı´chov Hill locality, near Letovice, Czech Republic

Artinskian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) cyatheus Schlotheim

Psaroniaceae

Padochov Formation, Ba
cov Horizon; Boskovice Basin, Ba
cov locality, Quarry 3, near Boskovice, Czech Republic

Artinskian


Sim unek and Martı´nek (2009)

Cyathocarpus (Pecopteris) cyatheus Schlotheim

Psaroniaceae

Shanxi Formation; Northwest China Province; Longshou Mts., Xizang Autonomous Region, China

Artinskian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) cyatheus Schlotheim

Psaroniaceae

Dahuanggou Formation; Northwest China Province; Longshou Mt., Xizang Autonomous Region, China

Kungurian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) cyatheus Schlotheim

Psaroniaceae

Lower part, Kaipaizileike Formation; northwest Tarim Basin, Xinjiang, China

Artinskian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) cyatheus Schlotheim

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar Basin; Tangshan Prefecture, N. Weihe Basin, Hebei Province; Shanxi Province; Huainan Huaibei Coalfield, Anhui Province; Shandong Province, China

Artinskian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) cyatheus Schlotheim

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province, Tangshan, Hebei province; S. Liaoning and W. Jilin Provinces, China

Kungurian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) cyatheus Schlotheim

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; Tangshan, Hebei Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Kupukuziman Formation; northwest Tarim Basin, southern Xinjiang, China

Artinskian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Shanxi Formation; Northwest China Province; N. Qilian Mt., Longshou Mt., Xizang Autonomous Region, China

Artinskian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Dahuanggou Formation; Northwest China Floral Province; Longshou Mt., Xizang Autonomous Region, China

Kungurian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Loei-Dan Sai Highway, Changwat Loei, Thailand

Early Late Permian

Asama et al. (1968)

Continued

338

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Cyathocarpus hemitelioides (Brongniart) Cleal

Psaroniaceae

Hambaegsan Formation; Samcheong Coalfield, Korea

Changhsingian

Chun (1985) and Cleal (2015)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Shansi Formation; North China Floral Province; Jungar County, Huainan Huaibei Coalfield, Anhui Province; Fengfeng mining district, Hebei Province, China

Artinskian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; N. Weihe graben, Shanxi Province; Huainan Huaibei Coalfield, Anhui Province; Tangshan Prefecture, Hebei Province; and Jilin Province, China

Kungurian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) hemitelioides (Brongniart) Cleal

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; N. Weihe graben, Hebei Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Cyathocarpus (Pecopteris) lepidorachis (Brongniart) Cleal

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Jungar County, Tangshan Prefecture, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Danaeites guangxingensis Huang

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; S. Liaoning and W. Jilin Provinces, China

Early Late Perman

Shen (1995) (Li, 1995)

Danaeites mirabilis “Gu et Zhi” 1974

Psaroniaceae

Shansi Formation; North China Floral Province; Jungar County, Anhui Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Danaeites (Pecopteris) rigida Yabe et Oishi

Psaroniaceae

Xuanwei Formation; Yunnan Province, Xuanwei City, south China

Late Permian

Liu et al. (2001)

Danaeites (Pecopteris) rigida Yabe et Oishi

Psaroniaceae

Shanxi Formation; Northwest China Floral Province; Longshou Mt., Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) sp.

Psaroniaceae

Loei-Dan Sai Highway, Changwat Loei, Thailand

Kungurian

Asama et al. (1968) and Rigby (1998)

Diplazites (Fascipteris) densata “Gu et Zhi”

Psaroniaceae

Qiangtang-Yushu Block; Xizang Autonomous Region, Qamdo Prefecture, Toba, China

Early Late Permian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) hallei Kawasaki

Psaroniaceae

Shansi Formation; North China Floral Province; Inner Mongolia Autonomous Region, Jungar County; Huainan Huaibei Coal Field, Anhui Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) hallei Kawasaki

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Inner Mongolia Autonomous Region; Jungar County, Huainan Huaibei Coal Field, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) hallei Kawasaki

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; N. Weihe Graben, Shanxi Province; Huainan Huaibei Coal Field, Anhui Province; Tangshan Prefecture, Hebei Province; W. Jilin Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

339

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Diplazites (Ptychocarpus) malaianus Kon’no, Asama, Rajah

Psaroniaceae

Linggiu Formation; Gunong Blumut area, Central Johore, West Malaysia, Indonesia

Early Late Permian

Kon’no et al. (1970)

Diplazites (Fascipteris) stena Gu et Zhi

Psaroniaceae

Qiangtang-Yushu Block; Xizang Province, Qamdo Prefecture, Toba, China

Early Late Permian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) subantiqua Kon’no

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; S. Liaoning and W. Jilin Provinces, China

Early Late Permian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) kaishanensis Kon’no

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; S. Liaoning and W. Jilin Provinces, China

Early Late Permian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) tibeticus Li et Yao

Psaroniaceae

Qiangtang-Yushu Block, Rejuechaka Formation; Xizang Autonomous Region and Qinghai Province, Shuanhu, China

Late Permian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) tibeticus Li et Yao, 1981

Psaroniaceae

Quiangtang-Yushu Block, Rejuechaka Formation; Shuanghui, north Xizang Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) tingii Halle

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; Anhui Province, Huainan-Huaibei Coalfield, China

Early Late Permian

Shen (1995) (Li, 1995)

Diplazites (Ptychocarpus) tongtianheensis He et Zhang

Psaroniaceae

Quiangtang-Yushu Block; Laxiu Township, Yushu County, Qinghai Province, China

Early Late Permian

He and Zhang (1984)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Padochov Formation, Mı´chov Horizon; Boskovice Basin, Mı´chov Hill locality, near Letovice, Czech Republic

Artinskian


Sim unek and Martı´nek (2009)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Shanxi Formation; North China Floral Province, Jungar, N. Weihe, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; N. Weihe Basin, Hebei Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; N. Weihe, Hebei Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Hambaegsan Formation; Samcheong Coalfield, Korea

Changhsingian

Chun (1985) and Cleal (2015)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Shanxi Formation; Northwest China Province; N. Qilian Mts., Hexi Corridor, Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Diplazites (Pecopteris) unita (Brongniart) Cleal

Psaroniaceae

Yaogou Formation; Northwest China Province; N. Qilian Mts., Xizang Autonomous Region, China

Early Late Permian

Shen (1995) (Li, 1995)

Dizeugotheca waltonii Archangelsky et de la Sota

Psaroniaceae

Patagonia, Argentina

Permian

Archangelsky and Cu´neo (1984)

Eoangiopteris Mamay sp.

Psaroniaceae

Xuanwei Formation; Guizhou Province, Shanjiaoshu mine, China

Late Permian

Hilton et al. (2004)

Continued

340

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Fimbriotheca tomentosa Zhu et Chen

Psaroniaceae

Tanshanwan Formation; Yangxin District, Hubei Province, China

Early Late Permian

Zhu and Chen (1981)

Gemellitheca saudica Wagner, Hill et ElKhayal

Psaroniaceae

Late Unayzah Plant Beds of central Saudi Arabia; Gomaniimbrick Formation; southeast Anatolia, Hazro, Turkey

Late Permian

Wagner et al. (1985)

Lobatopteris ensifolia Halle

Psaroniaceae

Shansi Formation; North China Floral Province; Jungar County and Huainan-Huaibei Coalfield, Anhui Province; and Tangshan Prefecture, Hebei Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Lobatopteris ensifolia Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Shanxi Province; Huainan-Huaibei Coalfield, Anhui Province; N. Weihe Graben, Tangshan Prefecture, Hebei Province, China

Kungurian

Shen (1995) (Li, 1995)

Lobatopteris ensifolia Halle

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; Shanxi Province; Tangshan Prefecture, N. Weihe graben, Hebei Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Lobatopteris lingulata Halle

Psaroniaceae

Shansi Formation; North China Floral Province; Inner Mongolia Autonomous Region, Jungar County; Anhui Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Lobatopteris lingulata Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Shanxi Province; N. Weihe graben, Hebei Province, China

Kungurian

Shen (1995) (Li, 1995)

Lobatopteris lingulata Halle

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; Shanxi Province, N. Weihe graben, Hebei Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Lobatopteris multifolia Kon’no et Asama

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; W. Henan Province, and Huainan-Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Lobatopteris obtusa Yang

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Huainan Prefecture, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Lobatopteris obtusa Yang

Psaroniaceae

Shihchienfeng Formation; North China Floral Province; W. Henan Province, China

Changhsingian

Shen (1995) (Li, 1995)

Lobatopteris sinensis Halle

Psaroniaceae

Shansi Formation; North China Floral Province; Shanxi Province, Jungar County, and Tangshan Prefecture in Hebei Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Lobatopteris sinensis Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Shanxi Province; Jungar County, Tangshan Prefecture, Hebei Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris sp.

Psaroniaceae

Loei and Phetchabun, Thailand

Kungurian

Rigby (1998)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

341

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris sp.

Psaroniaceae

Shuangtsu¨an Formation: Badachu Park, western Beijing, China

Late Permian

Zhang et al. (1992)

Pecopteris sp.

Psaroniaceae

Halgaito Formation; Paradox Basin, “Valley of the Gods,” San Juan County, Utah, USA

Wolfcampian; Lower Permian

DiMichele et al. (2014)

Pecopteris sp.

Psaroniaceae

Halgaito Formation; Paradox Basin, “Indian Creek,” San Juan County, Utah, USA

Wolfcampian; Lower Permian

DiMichele et al. (2014)

Pecopteris affinis (Schlotheim) Brongniart

Psaroniaceae

Shanxi Formation; Northwest China Province, Longshou Mt., Nagyu Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris affinis (Schlotheim) Brongniart

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar Basin.Xinjiang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris anderssonii Halle

Psaroniaceae

Qiangtang-Yushu Block, Toba, Quamdo Prefecture, Xizang Autonomous Region, Qinghai Province,China

Late Permian

Shen (1995) (Li, 1995)

Pecopteris anderssonii Halle

Psaroniaceae

Dahuanggou Formation; Northwest China Floral Province; N. Qilian Mt., Xizang Autonomous Region, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris anderssonii Halle

Psaroniaceae

Sunan Formation; Northwest China Floral Province; N. Qilian Mt., Xizang Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Pecopteris anderssonii Halle

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar Banner, Inner Mongolia Autonomous Region, Huainan-Huaibei Coalfield, Anhui Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris anderssonii Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; N. Weihe, Hebei Province; Shanxi Province, W. Henan Province; Huainan-Huaibei Coalfield, Anhui Province; Shandong Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris anderssonii Halle

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; N. Weihe, Tangshan, Hebei Province; W. Henan Province; , Huainan-Huaibei Coalfield, Anhui Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris angustilingulata Li, Yao, et Deng

Psaroniaceae

Qiangtang-Yushu Block; Toba, Quamdo Prefecture, Xizang Autonomous Region, Qinghai Province,China

Late Permian

Shen (1995) (Li, 1995)

Pecopteris anthriscifolia Go¨ppert

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Jungar Banner, Inner Mongolia Autonomous Region, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris anthriscifolia Go¨ppert

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; S. Liaoning Province, W. Jilin Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris anthriscifolia Go¨ppert

Psaroniaceae

Sunan Formation; Northwest China Floral Province; N. Qilian Mt., Xizang Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Continued

342

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris arcuata Halle

Psaroniaceae

Shanxi Formation; Northwest China Floral Province; Longshou Mts., Hexi Corridor, Qinghai Plateau, Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris arcuata Halle

Psaroniaceae

Dahuanggou Formation; Northwest China Floral Province, Hexi Corridor, Qinghai Plateau, Xizang Autonomous Region, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris arcuata Halle

Psaroniaceae

Shanxi Formation; North China Floral Province; Shaanxi; Jungar Basin, N. Weihe Plain, W. Henan; Huainan Huaibei Coalfield, Anhui Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris arcuata Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; N. Weihe Basin, Shaanxi Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris arcuata Halle

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; N. Weihe Basin, Hebei Province; Huainan Huaibei Coalfield, Anhui Province; S. Liaoning Province, W. Jilin Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris arcuata Halle, 1927

Psaroniaceae

Qiangtang-Yushu Block; Wuli Basin, Golmud City, Qinghai Provence, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris arcuata Halle, 1927

Psaroniaceae

Linggiu Formation; Gunong Blumut area, Central Johore, West Malaysia

Early Late Permian

Kon’no et al. (1970)

Pecopteris arcuata Halle

Psaroniaceae

Jengka Pass, Pahang, Malaysia, Indonesia

Late Permian

Kon’no and Asama (1970) and Rigby (1998)

Pecopteris bobrovi Neuberg

Psaroniaceae

Sunan Formation; Northwest China Floral Province, N. Qilian Mt., Xizang Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Pecopteris cf. cadeadensis Rohn et Ro¨sler

Psaroniaceae

Titicaca Group, Chutani Formation; San Pablo de Tiquina, Antiplano of Bolivia

Permian

Iannuzzi et al. (2004)

Pecopteris chihliensis Stockmans et Mathieu

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar Banner, Inner Mongolia Autonomous Region

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris chihliensis Stockmans et Mathieu

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Shandong Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris chihliensis Stockmans et Mathieu

Psaroniaceae

Upper Shihhotse Formation North China Floral Province; Beijing, Tangshan, Hebei Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris crassinervis Yang

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; Henan Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris densifolia Go¨ppert

Psaroniaceae

Shanxi Formation; Northwest China Province, N. Qilian Mt., Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

343

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris densifolia Go¨ppert

Psaroniaceae

Shanxi Formation; North China Floral Province; Henan Province, Tangshan Prefecture, Hebei Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris densifolia Go¨ppert

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; W. Henan, W. Liaoning and W. Jilin Provinces, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris densifolia Go¨ppert

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; Tangshan Prefecture, Hebei Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris dolianitii Rohn et Ro¨ßler

Psaroniaceae

Titicaca Group, Chutani Formation; San Pablo de Tiquina, Antiplano of Bolivia

Permian

Iannuzzi et al. (2004)

Pecopteris echinata “Gu et Zhi”

Psaroniaceae

Qiangtang-Yushu Block, XizangQinghai Provinces, Toba, Quamdo Prefecture, China

Late Permian

Shen (1995) (Li, 1995)

Pecopteris flexa Yang

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Henan, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris fleusuosus Yang

Psaroniaceae

Shanxi Formation; North China Floral Province; Henan Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris fungfungensis Lee

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris fungfungensis Lee

Psaroniaceae

Shanxi Formation; North China Floral Province; Fengfeng, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris fuyuanensis Zhang

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris gracifolia Fang

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris gracilenta “Gu et Zhi”

Psaroniaceae

Sunan Formation; Northwest China Province; N. Qilian Mt., Inner Mongolia, Xizang Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Pecopteris gracilenta “Gu et Zhi”

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris guizhouensis “Gu et Zhi”

Psaroniaceae

Qiangtang-Yushu Block; Wuli Basin, Golmud City, Qinghai Provence, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris guizhouensis “Gu et Zhi”

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris helenaeana Zalessky

Psaroniaceae

North Greenland fold belt; Johannes V. Jensen Land, Midtkap, eastern North Greenland

Late Permian

Wagner et al. (1982)

Continued

344

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris heteropinna Yabe et Oishi

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris hirta Halle

Psaroniaceae

Sunan Formation; Northwest China Province, N. Qilian Mt., Xizang Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Pecopteris hirta Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Jungar Basin, N. Weihe Basin, Shaanxi Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris huichensis Hsu¨

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar Coal Field, Inner Mongolia Autonomous Region; Huainan Huaibei Coalfield, Anhui Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris imbricata Stockmans et Mathieu

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; Tangshan Prefecture, Hebei Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris integra (Andrae) Schimper

Psaroniaceae

Hambaegsan Formation; Samcheong Coalfield, Korea

Changhsingian

Chun (1985)

Pecopteris jongmansii Wagner

Psaroniaceae

Village of Dadas, Hazro region, S.E. Anatolia, Turkey

Middle Late Permian

Wagner (1962)

Pecopteris karporii Radcz.

Psaroniaceae

Fangshankou Group; Northwest China Floral Province; Beishan Town, Hunan Province, China

Changhsingian

Shen (1995) (Li, 1995)

Pecopteris lativenosa Halle

Psaroniaceae

Loei-Dan Sai Highway, Changwat Loei, Thailand

Kungurian

Asama et al. (1968) and Rigby (1998)

Pecopteris lativenosa Halle

Psaroniaceae

Shanxi Formation; Wuda District, Inner Mongolia Autonomous Region, China

Early Permian

Pfefferkorn and Wang (2007)

Pecopteris lativenosa Halle

Psaroniaceae

Shanxi Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province; Shandong Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris lativenosa Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province Jungar Basin, Inner Mongolia Autonomous Region; N. Weihe Basin, W. Henan; Huainan Huaibei Coalfield, Anhui Province; Shandong Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris lativenosa Halle

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; Huainan Huaibei Coalfield, Beijing, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris lativenosa Halle

Psaroniaceae

Shanxi Formation; Northwest China Floral Province, Qilian Mt., Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris lativenosa Halle

Psaroniaceae

Dahuanggou Formation; Northwest China Floral Province, N. Qilian Mt., Longshou Mt., Xizang Autonomous Region, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris lativenosa Halle

Psaroniaceae

Yaogou Formation; Northwest China Floral Province; N. Qilian Mt., Xizang Autonomous Region, China

Early Late Permian

Shen (1995) (Li, 1995)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

345

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris lativenosa Halle

Psaroniaceae

Sunan Formation; Northwest China Floral Province; N. Qilian Mt., Xizang Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Pecopteris lativenosa Halle

Psaroniaceae

Hongquan Formation; Northwest China Floral Province; Longshou Mt., Xizang Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Pecopteris lingulata Liu

Psaroniaceae

Shanxi Formation; North China Floral Province; Shanxi Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris linsiana Stockmans et Mathieu

Psaroniaceae

Shanxi Formation; North China Floral Province; Tangshan Prefecture, Hebei Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris liuiana Lee

Psaroniaceae

Shanxi Formation; Northwest China Floral Province; Longshou Mt., Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris liuiana Lee

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar Banner, Inner Mongolia Autonomous Region, Shanxi Province; Huainan Huaibei Coalfield, Anhui Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris liuiana Lee

Psaroniaceae

Lower Shihhotse Formation; Huainan Huaibei Coalfield, Hebei Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris marginata “Gu et Zhi”

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar Banner, Inner Mongolia Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris marginata “Gu et Zhi”

Psaroniaceae

Lower Shihhotse Formation; Huainan Huaibei Coalfield, Hebei Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris marginata “Gu et Zhi”

Psaroniaceae

Upper Shihhotse Formation; N. Weihe River Basin, Inner Mongolia Autonomous Region, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris marginata “Gu et Zhi”

Psaroniaceae

Sunan Formation; Northwest China Floral Province, N. Qilian Mt., Xizang Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Pecopteris monyi Zeiller

Psaroniaceae

Mauchline Volcanic Group; Mauchline Basin, Mauchline Parrish, on River Ayr, Scotland

Lower Rotliegend

Wagner (1983)

Pecopteris monyi Zeiller

Psaroniaceae

Shanxi Formation; Northwest China Floral Province, N. Qilian Mt., Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris monyi Zeiller

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar Basin, Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris muchangensis Huang

Psaroniaceae

Shanxi Formation; North China Floral Province; Jungar Basin, Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris nervosa Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; W. Henan Province, Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris nervosa Halle

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; W. Henan Province, Huainan Huaibei Coalfield, Anhui Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Continued

346

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris nitida Wagner

Psaroniaceae

Village of Dadas, Hazro region, S.E. Anatolia, Diyarbakir Province, Turkey

Middle Late Permian

Wagner (1962)

Pecopteris norinii Halle

Psaroniaceae

Hambaegsan Formation; Samcheong Coalfield, Korea

Changhsingian

Chun (1985)

Pecopteris norinii Halle

Psaroniaceae

Shanxi Formation; North China Floral Province; Shandong Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris norinii Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; W. Henan Province, Shanxi Province, China

Late Early Permian, Kungurian

Shen (1995) (Li, 1995)

Pecopteris norinii Halle

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; N. Weihe Graben, Tangshan City, Hebei Province; Huainan Huaibei Coalfield, Anhui Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris obliquenervis Yang

Psaroniaceae

Lower Shihhotse Formation; Northwest China Floral Province; W. Henan Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris (Scolecopteris) oreopteridia Schlotheim

Psaroniaceae

Leukersdorf Formation, Altendorf chert Horizon; Chemnitz basin, Chemnitz-Altendorf, Germany

Rotliegend

Schneider et al. (2012)

Pecopteris orientalis (Shenk) Potonie´

Psaroniaceae

Hambaegsan Formation; Samcheong Coalfield, Korea

Changhsingian

Chun (1985)

Pecopteris orientalis (Shenk) Potonie´

Psaroniaceae

Kupukuziman Formation; northwestern Tarim Basin, southern Xinjiang Autonomous Region, China

Artinskian or Sakmarian

Shen et al. (1991)

Pecopteris orientalis (Shenk) Potonie´

Psaroniaceae

Lower part, Kaipaizileike Formation; northwest Tarim Basin, southern Xinjiang Autonomous Region, China

Kungurian

Wu (1993) and Shen (1995) (Li, 1995)

Pecopteris orientalis (Shenk) Potonie´

Psaroniaceae

Shanxi Formation; Northwest China Province, N. Qilian Mt., Hexi Corridor, Longshou Mt., Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris orientalis (Shenk) Potonie´

Psaroniaceae

Dahuanggou Formation; Northwest China Province, N. Qilian Mt., Hexi Corridor, Inner Mongolia Autonomous Region, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris orientalis (Shenk) Potonie´

Psaroniaceae

Yaogou Formation; Northwest China Province, N. Qilian Mt., Inner Mongolia Autonomous Region, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris orientalis (Schenk) Potonie´

Psaroniaceae

Shanxi Formation; Northwest China Floral Province; Jungar, N. Weihe River Basin, Shaanxi Province; W. Henan Province, Huainan Huaibei Coalfield, Anhui Province; Fengfeng Mining District, Inner Mongolia Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris orientalis (Schenk) Potonie´

Psaroniaceae

Lower Shihhotse Formation; Northwest China Floral Province; Jungar Banner, Xizang Autonomous Region, N. Weihe River Basin, Shaanxi; W. Henan Province, Huainan Huaibei Coalfield, Anhui Province, Shandong Province, China

Kungurian

Shen (1995) (Li, 1995)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

347

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris orientalis (Schenk) Potonie´

Psaroniaceae

Upper Shihhotse Formation; Northwest China Floral Province; Jungar Banner, Xizang Autonomous Region, N. Weihe, Hebei Province; Beijing, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris cf. pedrasica Read

Psaroniaceae

Titicaca Group, Chutani Formation; San Pablo de Tiquina, Antiplano of Bolivia

Permian

Iannuzzi et al. (2004)

Pecopteris cf. phegopteroides Feistmantel

Psaroniaceae

Village of Dadas, Hazro region, S.E. Anatolia, Turkey

Artinskian or Sakmarian

Wagner (1962)

Pecopteris pirae Wagner

Psaroniaceae

Village of Dadas, Hazro region, S.E. Anatolia, Turkey

Artinskian or Sakmarian

Wagner (1962)

Pecopteris polypodioides Knight

Psaroniaceae

Padochov Formation, Mı´chov Horizon; Boskovice Basin, Mı´chov Hill locality, near Letovice, Czech Republic

Artinskian


Sim unek and Martı´nek (2009)

Pecopteris potoniei N
emejc

Psaroniaceae

Manebach Formation; Manebach, Germany

Rotliegend

Barthel (2005)

Pecopteris sahnii Hsu¨

Psaroniaceae

Shanxi Formation; North China Floral Province; N. Weihe, Hebei Province; Huainan Huaibei Coalfield, Anhui Province,China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris sahnii Hsu¨

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; N. Weihe River Valley, Shaanxi Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris sahnii Hsu¨

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; N. Weihe Plain, Inner Mongolia Autonomous Region, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris sinobuntonneti Stockmans et Mathieu

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; Tangshan, Hebei Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris shanxiensis Liu

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; N. Weihe Plain, Inner Mongolia Autonomous Region, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris shenhouensis Yang

Psaroniaceae

Shanxi Formation, North China Floral Province; W. Henan Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris shuanghuensis Li et Yao

Psaroniaceae

Qiangtang-Yushu Block, Rejuechaka Formation; Xizang-Qinghai Provinces, Shuanghu, China

Late Permian

Shen (1995) (Li, 1995)

Pecopteris taiyuanensis Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Jungar Banner, Xinjiang Autonomous Region, N. Weihe River Basin, Shanxi; W. Henan Province; Huainan Huaibei Coalfield, Anhui Province; Shandong Province; Fengfeng, Inner Mongolia Autonomous Region, China

Kungurian

Shen (1995) (Li, 1995)

Continued

348

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris taiyuanensis Halle

Psaroniaceae

Dahuanggou Formation; Northwest China Province, Hexi Corridor, Qinghai Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris tenuidermis Wagner

Psaroniaceae

Village of Dadas, Hazro region, S.E. Anatolia, Turkey

Middle Late Permian

Wagner (1962)

Pecopteris tenuicostata Halle

Psaroniaceae

Shanxi Formation; North China Floral Province; N. Huainan Huaibei Coalfield, Anhui Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris tenuicostata Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Jungar Basin, Xinjiang Autonomous Region; N. Weihe River Basin, Shaanxi; W. Henan Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris tenuicostata Halle

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province N. Weihe River, W. Henan Province; Huainan Huaibei Coalfield, Anhui Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris tenuicostata Halle

Psaroniaceae

Daquan Formation; Northwest China Floral Province, Longshou Mt., Inner Mongolia Autonomous Region, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris tenuicostata Halle

Psaroniaceae

Sunan Formation; Northwest China Floral Province, N. Qilian Mt., Hexi Corridor, Inner Mongolia Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Pecopteris tenuicostata Halle

Psaroniaceae

Hongquan Formation; Northwest China Floral Province; Longshou Mt., Inner Mongolia Autonomous Region, China

Changhsingian

Shen (1995) (Li, 1995)

Pecopteris trachyrachis Xiao

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; W. Henan Province; Shanxi Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris tuberculata Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Jungar, Banner, Inner Mongolia Autonomous Region; Shanxi Province, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris tuberculata Halle

Psaroniaceae

Shanxi Formation; North China Floral Province; Tangshan Prefecture, Hebei Province, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris cf. wongii Halle pars.

Psaroniaceae

Village of Dadas, Hazro region, S.E. Anatolia, Turkey

Middle Late Permian

Wagner (1962)

Pecopteris cf. wongii Halle

Psaroniaceae

Shanxi Formation; North China Floral Province; N. Weihe Basin, Hebei Province; Huainan Huaibei Coalfield, Anhui Province; Shandong, S. Liaoning and W. Jilin Provinces, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris cf. wongii Halle

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; N. Weihe Basin, Hebei Province; Huainan Huaibei Coalfield, Anhui Province; S. Liaoning and W. Jilin Provinces, China

Kungurian

Shen (1995) (Li, 1995)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

349

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Pecopteris cf. wongii Halle

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; N. Weihe Basin, Hebei Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris wongii Halle

Psaroniaceae

Shanxi Formation; Northwest Floral Province; Longshou Mt., Hexi Corridor, Xizang Autonomous Region, China

Artinskian or Sakmarian

Shen (1995) (Li, 1995)

Pecopteris wongii Halle

Psaroniaceae

Dahuanggou Formation; Northwest Floral Province; Hexi Corridor, Xizang Autonomous Region, China

Kungurian

Shen (1995) (Li, 1995)

Pecopteris yabei Kawasaki

Psaroniaceae

Upper Shihhotse Formation; North China Floral Province; S. Liaoning Province, W. Jilin Province, China

Early Late Permian

Shen (1995) (Li, 1995)

Pecopteris yinii Kon’no, Asama et Rajha

Psaroniaceae

Linggiu Formation; Gunong Blumut area, Central Johore, West Malaysia, Indonesia

Late Permian

Kon’no et al. (1970) and Rigby (1998)

Pecopteris zhangzhuangensis Fang

Psaroniaceae

Lower Shihhotse Formation; North China Floral Province; Huainan Huaibei Coalfield, Anhui Province, China

Kungurian

Shen (1995) (Li, 1995)

Pectinangium lanceolatum (Li et al.) Wan et Basinger

Psaroniaceae

Longtan Formation; Jiangsu, Jiangxi and Guangdong Provinces, China

Late Permian, P12

Li et al. (1974) and Wan and Basinger (1992)

Pectinangium unifurcata (Li et al.) Wan et Basinger

Psaroniaceae

Longtan Formation; Jiangxi and Guangdong Provinces, China

Late Permian

Yang and Chen (1979) and Wan and Basinger (1992)

Psaronius Cotta sp.

Psaroniaceae

Xuanwei Formation; Shanjiaoshu mine, Guizhou Province, China

Late Permian

Hilton et al. (2004)

Psaronius arrojadoi (Pelourde) Herbst

Psaroniaceae

Corumbataı´ Formation, Parana´ Basin, Passa Dois Group; Sa˜o Paulo and Casa Branca, Brazil

Guadalupian

Tavares et al. (2011) and Herbst (1985)

Psaronius brasiliensis (Unger) Brongniart

Psaroniaceae

Locality between Oeiras and Sa˜o Gonc¸ala d’Amarante, Province of Piauhy, Brazil

Permian

Brongniart, 1872

Psaronius housuoensis D’Rozario et al.

Psaroniaceae

Xuanwei Formation, Lopingian Series; Fuyuan County, Housuo Coal Mine, Yunnan Province, China

Late Permian

D’Rozario et al., 2011

Psaronius infarctus Unger

Psaroniaceae

Leukersdorf Formation, Zeisigwald Tuff; Chemnitz Basin, Chemnitz, Germany

Rotliegend

Schneider et al. (2012)

Psaronius jiangsuensis Yao.et al.

Psaroniaceae

Jiangsu Province, China

Kungurian

Yao et al. (1994)

Psaronius johorensis Ogura

Psaroniaceae

Linggiu Formation; Gunong Blumut area, Central Johore, West Malaysia, Indonesia

Late Permian P12

Kon’no and Asama (1970) and Ogura (1972)

Psaronius laowujiensis He et al.

Psaroniaceae

Xuanwei Formation; Panxian County, Laowuji Mine, Guizhou Province, China

Late Permian

He et al. (2010)

Psaronius panxianensis He et al.

Psaroniaceae

Xuanwei Formation; Panxian County, Guizhou Province, China

Late Permian

He et al. (2008)

Psaronius simplex Unger

Psaroniaceae

Leukersdorf Formation, Erzgebirge Basin, Zeisigwald Tuff Horizon; Chemnitz, Saxony, Germany.

Middle Rotliegend

Stenzel (1854, 1906)

Continued

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SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Psaronius sinensis Sze

Psaroniaceae

Omeishan Basalt; Omei Mountain, western Kweichow, district of Weining, W. Szechuan Province, China

Middle Rotliegend

Sze (1942, 1947)

Psaronius wangii Tian, Li et Guo

Psaroniaceae

Hsuanwei Formation; Panxian County, Guizhou Province, China

Late Permian

Tian et al. (1992)

Psaronius xuii He et al.

Psaroniaceae

Xuanwei Formation; Panxian County, Guizhou Province, China

Lopingian

He et al. (2013)

Qasimia schyfsmae Hill, Wagner et ElKhayal

Marattiaceae?

Khuff Formation; Unayzah, central Saudi Arabia

Lopingian

Hill et al. (1985)

Qasimia (Taeniopteris) tobaensis Li, Yao et Deng

(fertile?) Marattiaceae?

Qiangtang-Yushu Block; Toba, Qamdo Prefecture, Xizang Autonomous Region,China

Late Permian P1:2

Shen (1995) (Li, 1995) and Li et al. (1982)

Rajahia (Pecopteris) bifurcata Kon’no

Psaroniaceae

Linggiu Formation; Gunong Blumut area, Central Johore, West Malaysia, Indonesia

Late Permian P12

Kon’no et al. (1970) and Rigby (1998)

Rajahia (Pecopteris) bifurcata Kon’no

Psaroniaceae

Qiangtan-Yushu Block, Toba Formation, Qamdo Prefecture, Xizang Autonomous Region-Qinghai Province, China

Late Permian

Shen (1995) (Li, 1995)

Rajahia (Pecopteris) calceiformis Li et Yao

Psaroniaceae

Qiangtan-Yushu Block, Rejuechaka Formation; Shuanghu, Toba Formation, Quamdo Prefecture; Laxiu, Yushu Prefecture; Xizang-Qinghai Provinces, China

Late Permian

Shen (1995) (Li, 1995)

Rajahia (Pecopteris) linggiuensis Kon’no

Psaroniaceae

Linggiu Formation; Gunong Blumut area, Central Johore, West Malaysia, Indonesia

Late Permian

Kon’no et al. (1970) and Rigby (1998)

Rajahia minor Zhang

Psaroniaceae

Sunan Formation; Northwest China Floral Province, N. Qilian Mt., Xijiang Province, China

Changhsingian

Shen (1995) (Li, 1995)

Rajahia (Pecopteris) mirabilis “Gu et Zhi”

Psaroniaceae

Qiangtan-Yushu Block, Toba, Quamdo Prefecture, Xizang-Qinghai Provinces, China

Late Permian

Shen (1995) (Li, 1995)

Rajahia (Pecopteris) pseudohemitelioides Kon’no, Asama et Rajah

Psaroniaceae

Qiangtang-Yushu Block, Toba, Quamdo Prefecture, Xizang-Qinghai Provinces, China

Late Permian

Shen (1995) (Li, 1995)

Rajahia (Pecopteris) pseudohemitelioides Kon’no, Asama et Rajah

Psaroniaceae

Linggiu Formation; Gunong Blumut area, Central Johore, West Malaysia, Indonesia

Late Permian

Kon’no et al. (1970) and Rigby (1998)

Rajahia (Pecopteris) quamdoensis Li, Yao et Deng

Psaroniaceae

Qiangtang-Yushu Block, Toba, Quamdo Prefecture, Xizang-Qinghai Provinces, China

Late Permian

Shen (1995) (Li, 1995)

Rajahia (Pecopteris) rajahii Kon’no, Asama et Rajah

Psaroniaceae

Linggiu Formation; Gunong Blumut area, Central Johore, West Malaysia, Indonesia

Late Permian

Kon’no et al. (1970) and Rigby (1998)

Rajahia (Pecopteris) sengensis Kon’no, Asama et Rajah

Psaroniaceae

Linggiu Formation; Gunong Blumut area, Central Johore, West Malaysia, Indonesia

Late Permian

Kon’no et al. (1970) and Rigby (1998)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

351

Permian Occurrencesdcont’d Species

Family

Stratigraphy/Geography

Age (Ma)

References

Scolecopteris sp.

Psaroniaceae

Xuanwei Formation; Shanjiaoshu mine, Guizhou Province, China

Late Permian

Hilton et al. (2004)

Scolecopteris guizhouensis He et al.

Psaroniaceae

Wangjiazhai Formation; Shuicheng County, western Guizhou Province, China

Changhsingian

He et al. (2006)

Taiyuanitheca tetralinea Gao et Thomas

Psaroniaceae

Lower Shihhotese Formation; Taiyuan City, Simugedong, Dongshan, Shanxi Province, north China

Early Permian

Gao and Thomas (1993)

Tietea singularis (Solms-Laubach) Herbst

Psaroniaceae

Corumbataı´ Formation, Parana´ Basin, Passa Dois Group; Sa˜o Paulo, Brazil

Permian

Tavares et al. (2011) and Herbst (1986)

Tietea derbyi Herbst

Psaroniaceae

Zona de Carolina, Estado de Maranhao, northern Brasil

Permian?

Herbst (1992)

Tuvichapteris solmsi Herbst

Marattiaceae ?

Independence Formation; Zona Cantera Cachimbo, Departamento Caaguazu´, Paraguay

Late Permian

Herbst (1987)

Zhutheca densata (Gu et Zhi) Liu, Li et Hilton

Psaroniaceae

Xuanwei Formation; Xuanwei City, Yunnan Province, China

Late Permian

Liu et al. (2000)

References Archangelsky, S., and R. Cúneo. 1984. Zonacíon del Pérmico continental Argentino sobre la base de sus plantas fósiles. In: Carmen Perrillat, M., (Ed.). Memorias, third Congreso Latinoamericano de Paleontologia, pp. 143e153. Asama, A., J. Hongnusonthi, J. Iwai, E. Kon’no, S.S. Rajah and M. Veeraburas. 1975. Summary of the Carboniferous and Permian plants from Thailand, Malaysia and adjacent areas. Geology and Palaeontology of Southeast Asia 15: 77e101. Asama, A., J. Iwaii, M. Veeraburas and A. Hongnusonthi. 1968. Permian plants from Loei. Geology and Paleontology of Southeast Asia 4: 82e99, 5 pls. Barthel, M. 2005. Die Rotliegendflora des Thüringer Waldes. Teil 3: Farne. Veröffentlichungen Naturhistorisches Museum Schleusingen 20: 27e56. Brongniart, A. 1872. Notice sur le Psaronius brasiliensis. Bulletin of the Botanical Society of France 19: 3e10. Chun, H-Y. 1985. Upper Carboniferous floral assemblages and their stratigraphyc significances in Korea. Dixième Congrès International de Stratigraphie et de Géologie du Carbonifère. Madrid. 1: 59e70. Cleal, C.J. 2015. The generic taxonomy of Pennsylvanian age marattialean fern frond adpressions. Palaeontographica 292B: 1e21.

D’Rozario, A., B. Sun, J. Galtier, S-J. Wang, W-Y. Guo, Y-F. Yao and C-S. Li. 2011. Studies of the Late Permian permineralized tree fern Psaronius housuoensis sp. nov. from Yunnan Province, southwest China. Review of Palaeobotany and Palynology 163: 247e263. DiMichele, W.A., C.B. Cecil, D.S. Chaney, S.D. Elrick and W.J. Nelson. 2014. Fossil floras from the Pennsylvanian-Permian Cutler Group of Southeastern Utah. In: MacLean, J.S., R.F. Biek and J.E. Huntoon, (Eds.). Geology of Utah’s Far South: Utah Geological Association Publication 43: 491e504. Doweld, A.B. 2001. Corsinopteris, A new substitute name for Orthotheca (Marattiales Marattiopsida). Taxon 50: 1097e1099. Gao, Z., and B.A. Thomas. 1993. A new fern from the Lower Permian of China and its bearing on the evolution of the marattialeans. Palaeontology 36: 81e89. He, X., J. Jin, S. Wang, X. Fu, N. Li, and Y. Li. 2010. Anatomically preserved marattialean plants from the Upper Permian of Southwestern China: the trunk of Psaronius laowujiensis sp. nov. International Journal of Plant Science 171: 662e678. He, X-Y., S-J. Wang, J. Hilton and Y-L. Zhou. 2006. A new species of the marattialean fern Scolecopteris (Zenker) Millay from the uppermost Permian of Guizhou Province,

352

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south-western China. Botanical Journal of the Linnaean Society 151: 279e288. He, X-Y., S-J. Wang, J. Hilton, B.L. Tian and Y-L. Zhou. 2008. Anatomically preserved marattialean plants from the Upper Permian of southwestern China: the trunk of Psaronius panxianensis sp. nov. Plant Systematics and Evolution 272: 155e180. He, X-Y., S-J. Wang, J. Hilton, J. Galtier, Y-J. Li and L. Shao. 2013. A unique trunk of Psaroniaceae (Marattiales)e Psaronius xuii sp. nov., and subdivision of the genus Psaronius Cotta. Review of Palaeobotany and Palynology 197: 1e14. He, Y. and S. Zhang. 1984. Late Permian fossil plants around Shanglaxiu district of Yushu County, Qinghai Province and their geological significance. Contributions to Geology of Qinghai-Xizang (Tibet) Plateau 14: 115e124, 1e2 pls. Herbst, R. 1985. Nueva descripcion de Psaronius arrojadoi (Pelourde) (Marattiales), del permico de Brasil. Ameghiniana 21: 243e258. Herbst, R. 1986. Studies on Psaroniaceae. I. The family Psaroniaceae (Marattiales) and a redescription of Tietea singularis Solms-Laubach; from the Permian of Brazil. In: Congreso Argentino Paleontologia Y Bioestratigrafia, 4. Mendoza. Actas Mendoza 1: 163e171. Herbst, R. 1987. Studies on Psaroniaceae. II. Tuvichapteris solmsi nov. gen. et sp. from the Permian of Paraguay and Uraguay. In: Congreso Latinoamericano de Paleontologia, 4. Santa Cruz de la Sierra. Anais Bolívia 1: 267e282. Herbst, R. 1992. Studies on Psaroniaceae. III. Tietea derbyi n. sp., from the Permian of Brazil. Courier Forschungsinstitut Senckenberg 147: 155e161. Hill, C. R., R.H. Wagner and A.A. El-Khayal. 1985. Qasimia gen. nov., an early Marattia-like fern from the Permian of Saudi Arabia. Scripta Geologica 79: 1e50. Hilton, J., S-J. Wang, J. Galtier, I. Glasspool and L. Stevens. 2004. An Upper Permian permineralized plant assemblage in volcaniclastic tuff from the Xuanwei Formation, Guizhou Province, southern China, and its palaeofloristic significance. Geological Magazine 141: 661e674. Iannuzzi, R., C.E.L. Vieira, M. Guerra-Sommer, E. Díaz-Martínez and G.W. Grader. 2004. Permian plants from the Chutani Formation (Titicaca Group, northern Altiplano of Bolivia): II. The morphogenus Glossopteris. Anais da Academia Brasileira de Ciências 76: 129e138. Jongmans, W.J., and W. Gothan. 1935. Die paläobotanischen Ergebnisse der Djambi-Expedition 1925. 2. Die

paläobotanische Ergebnisse. Jaarboek van het Mijnwezen in Nederlandsch Indië. Verhandelingen 59: 71e121. Jongmans, W.J., and W. Gothan. 1925. Beiträge zur Kenntnis der Flora des Oberkarbons von Sumatra. Verhandelingen Geologische Mijnbouwkundig Genootschap Nederlandschen Koloniën 8: 279e303. Kon’no, E., and K. Asama. 1970. Some Permian plants from the Jengka Pass, Pahang, West Malaysia. Geology and Palaeontology of Southeast Asia VIII: 97e132, pls. 17e24. Kon’no, E., K., Asama and S.S. Rajah. 1970. The late Permian Linggiu flora from the Gunong Blumut area, Johore, Malaysia. Bulletin of the Natural Science Museum, Tokyo. 13: 491e575, 17 pls. Li, X., (Ed.). 1995. Fossil Floras of China through the Geological Ages. pp. 695, 144 pls. Guangdong Science and Technology Press. Guangzhou, China (English Edition). Li, X., L. Deng, Z. Zhou, R. Xu and J. Zhu. 1974. Fossil Plants of China, I. Paleozoic Plants of China. Pectinangium gen. nov. In: Institute of Geology and Palaeontology and Institute of Botanical Academia Sinica (“Gu and Zhi,” Editorial Committee). Science Publishing House, Beijing. pp. 166e167. Li, X., Z. Yao and L. Deng. 1982. An early Late Permian flora from Toba, Quamdo District, Eastern Xizang. Palaeontolgy of Xizang V: 17e44, 13 pls. Liu, H.L., C-S. Li and J. Hilton. 2000. Zhutheca Liu, Li et Hilton gen. nov., the fertile pinnules of Fascipteris densata Gu et Zhi and their significance in marattialean evolution. Review of Palaeobotany and Palynology 109: 149e160. Liu, H.L., C-S. Li and J. Hilton. 2001. Fertile pinnules of Danaeites rigida Gu and Zhi (Marattiales) from the Upper Permian of south China. Botanical Journal of the Linnean Society 136: 107e117. Liu, L-J., and Z-Q. Yao. 2006. Cohaerensitheca: a new Paleozoic marattialean genus for compression-impression plant fossils from China. Paleoworld 15: 68e76. Naugolnykh, S.V. 2013. Permian ferns of western Angaraland. Paleontological Journal 47: 1379e1462. Ogura, Y. 1972. Psaronius from Linggiu, Johore, Malaya. Geology and Paleontology of Southeast Asia 10: 604-619. Pfefferkorn, H.W. and J. Wang. 2007. Early Permian coal-forming floras preserved as compressions from the Wuda District (Inner Mongolia, China). International Journal of Coal Geology 69: 90e102. Rigby, J.F. 1998. Upper Paleozoic floras of SE Asia. In: Hall, E.R., and J.D. Holloway, (Eds.). Biogeography and

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Geological Evolution of SE Asia. Backhuys Publishing, Leiden. Schneider, J.W., R. Rößler and F. Fischer. 2012. Rotliegend des Chemnitz-Beckens (syn. Erzgebirge-Becken). Schriftenreihe der Deutschen Gesellschaft für Geowissenschaften 61: 530e588; Hannover. Shen, G., B. Sun and Y. Wang. 1991. On Permian tropical islands phytocommunity. Abstracts of 29th Geologic Congress 1: 104. Shen, G.L. 1995. Fossil floras of China through the geological ages. 4. Permian Floras. p. 127e223. In: Li, X., (Ed.). Fossil Floras of China through the Geological Ages. English Edition. Guangdong Science and Technology Press. Guangzhou, China.
unek, Z., and Karel Martínek. 2009. A study of Late Sim Carboniferous and Early Permian plant assemblages from the Boskovice Basin, Czech Republic. Review of Palaeobotany and Palynology 155: 275e307. Stenzel, G. 1854. Über die Starsteine. Nova Acta Academia Caesarea Leopoldino-Carolinae Naturae Curiosorum 24(2). Breslau und Bonn. Stenzel, G. 1906. Die Psaronien, Beobachtungen und Betrachtungen. Beiträge zur Paläontologie und Geologie Öesterreich-Ungarns und des Orients 19: 85e123, pls. 1e7. Sze, H.C. 1942. Über ein neues Exemplar von Psaronius aus dem Omeishan Basalt in Weining (Kueichou) mit besonderer Berücksichtigung des Alters des Basaltes in Südwestchina. Bulletin of the Geology Society of China 22: 105e131. Sze, H.C. 1947. On the structure of Psaronius sinensis from the Omeishan Basalt Series in southwestern China. The Journal of Geology 55: 160e167. Sze, H.C. 1954. A preliminary study of the fossil flora of the Pingtingshan coal field in central Honan. Scientia Sinica 3: 323e334, pls.1e4. Tavares, T.V., R. Rohn, and S. Merlotti. 2011. Caules permineralizados de Tietea e Psaronius na bacia do Paraná (Formação Corumbataí, Permiano). Pesquisas em Geociências 38: 114e131. Tian, B.L., Y.J. Li, and Y.T. Guo. 1992. On the study of Psaronius wangii (sp. nov.) from Xuanwei Formation of Pan Xian, Guizhou. In: Li, Z.L., (Ed.). Collected Works for Memory of the 100 Anniversary of the Birthday of Dr. Wang Zhu-Quan. Coal Industry Press, Beijing (in Chinese). Vieira, C.E.L., R. Iannuzzi, and M. Guerra-Sommer. 2007. Revisão de pecopterídeas polimórficas do neopaleozóico da América do Sul. Revista Brasileira de Paleontologia 10: 107e116.

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Wagner, R.H. 1962. On a mixed Cathaysia and Gondwana flora from SE. Anatolia (Turkey). Compte Rendu du Quatrième Congrès pour l’avancement des études de stratigraphie et de géologie du Carbonifére (Heerlen septembre 15e20, 1958) Tome III 1962. Wagner, R.H. 1983. A lower Rotliegend flora from Ayrshire. Scottish Journal of Geology 19: 135e155. Wagner, R.H., C.R. Hill and A.A. El-Khayal. 1985. Gemellitheca gen. nov., a fertile pecopterid fern from the upper Permian of the Middle East. Scripta Geologica 79: 51e74. Wagner, R.H., N.J. Soper and A.K. Higgins. 1982. A Late Permian flora of Pechora affinity in North Greenland. Grønlands Geologiske Undersøgelse 108: 5e13. Wan, Z., and J.F. Basinger. 1992. On the fern Pectinangium Li et al., emend (Marattiales), with spores in situ from the Permian of southern China. Review of Palaeobotany and Palynolology 75: 219e238. Wu, S. 1993. Formation and evolution of floristic provinces of Carboniferous-Permian in Xinjiang. Xinjiang Geology 11: 17e22 (in Chinese with English abstract). Yang, G., and F. Chen. 1979. Palaeobotany. In: Hou, Hongfei, et al., (Eds.). Late Permian Coal-Bearing Strata and Fossils in Guangdong. Geology Publishing House, Beijing. pp. 104e139 (in Chinese). Yao, Z-Q., L-J. Liu and C-D. Li, 1994. Psaronii of Gigantopteris-flora from Jiangsu, China. Acta Palaeontology Sinica 33: 604e619. Zhang, S., Q. Wang, Z. Xiao, J-P. Laveine and Y. Lemoigne. 1992. The Permian flora from the Shuangtsüan Formation of the Western Hills of Beijing, North China. Annales de la Société Géologique du Nord 1: 179e187. Zhao, X., M. Zuangguan, Z. Shanzhen and Y. Zhahaogi. 1980. Late Permian flora from W. Guizhou and E. Yunnan. pp. 70e99. In: Nanjing Institute of Geology and Palaeontology, Academia Sinica, (Ed.). Stratigraphy and Palaeontology of the Upper Permian Coal Measures of W. Guizhou and E. Yunnan. Science Press, Beijing (in Chinese). Zhu, J., and G-X. Chen. 1981. Fimbriotheca tomentosa Zhu et Chenea new genus and species from Permian of China and its systematic position. Acta Botanica Sinica 23: 487e491. pl. 1.
unek, C.J. Cleal, J. Bek, and J. Zodrow, E.L., Z. Sim P
seni
cka. 2006. Taxonomic revision of the Palaeozoic marattialean fern Acitheca Schimper. Review of Palaeobotany and Palynology 138: 239e280.

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Triassic Occurrences of Marattialean Fernsa Species

Family

Geography

Age (Ma)

References

Angiopteris antiqua Xu et Chen

Marattiaceae

China

Upper Triassic

Xu et al. (1974)

Angiopteris hongniensis Chen & Duan

Marattiaceae

China

Upper Triassic

Chen et al. (1979)

Angiopteris taeniopteroides Yang

Marattiaceae

China

Upper Triassic

Yang (1978)

Angiopteris yungjenensis Xu et Chen

Marattiaceae

China

Upper Triassic

Xu et al. (1979)

Angiopteris spp.

Marattiaceae

China

Upper Triassic

Yang (1978) Xu et al. (1974) Xu et al. (1979) Chen et al. (1979)

Asterotheca spp.

?

Triassic

Krasser (1909) Van Konijnenburg-van Cittert (2002) Tidwell and Ash (1994)

Bernouillia spp. Heer

Marattiaceae

Triassic

Krasser (1909)

Boreopteris erenkensis Moguchevia

Marattiaceae

Danaeopsis spp.

Marattiaceae

Lower & Middle Triassic, Europe

Danaeopsis hughesi Feistmantel

Marattiaceae

India

Middle Gondwana

South Africa

Rhaetic

China

Rhaetic

Tonkin

Rhaetic

Krasser (1900)

Eastern U.S. Sweden

Late Triassic

Ward (1900a,b) Halle (1921)

Triassic

van Konijnenburg-van Cittert (2002) Tidwell and Ash (1994) Arnold (1964) Li et al. (1995)

Daeniopteris

Lunz, Germany

Moguchevia (1973)

Daeniopteris spp.

Kustatscher et al. (2012) Feistmantel (1882) Seward (1908)

Marattia aganzhenensis Yang, Wang et Pfefferkorn

Marattiaceae

Gansu, China

Liassic; Lower Jurassic

Yang et al. (2008)

Marattia asiatica Kawasaki

Marattiaceae

China, East Asia, Middle East

Upper Triassic

Chen, and Duan (1981) Wang (1999) Van Konijnenburg-van Cittert (2002)

Marattia crenulata

Marattiaceae

Sweden

Upper Triassic

Lundblad (1950)

Marattia litangensis

Marattiaceae

Sichuan, China

Upper Triassic

Yang (1978)

Marattia orientalis

Marattiaceae

Yunan China, Vietnam, Korea, Japan

Upper Triassic

Sze et al. (1963)

Marattia paucicostata

Marattiaceae

Yunan, China

Upper Triassic

Li et al. (1976)

Marattia spp.

Marattiaceae

Northern Hemisphere

Triassic

Wang (1999)

Marattiopsis sp.

Marattiaceae

Italy

Middle Triassic (Anisian)

Van Konijenburg-van Cittert et al. (2006)

Marattiopsis spp.

Marattiaceae

Arctic Canada

Upper Triassic

Ash and Bassinger (1991)

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355

Triassic Occurrences of Marattialean Fernsadcont’d Species

Family

Geography

Age (Ma)

References

Marattiopsis sp.

Marattiaceae

Italy

Middle Triassic (Anisian)

Van Konijenburg-van Cittert et al. (2006)

Marattiopsis marantacea Presl.

Lunz, Germany

Triassic

Krasser (1909)

Rhaetic

Go¨eppert, 1836e32 Schimper (1869) Schenk (1883)

Scania, Franconia & Tonkin

Rhatic

Fontaine, in Ward (1900) Ward (1900a,b) Mo¨ller (1902) Zeiller (1903)

Marattiaceae

Eastern Australia

Early Triassic

Webb (1983)

Rhinipteris

Marattiaceae

Greenland

Late Triassic

Harris (1926)

Rinitsia arrondiana Herbst

Marattiaceae

Patigonia

Formacio´n Can˜ado´n Largo, Jurassic

Herbst (1988)

Scolecopteris spp.

Psaroniaceae?

Antarctica

Middle Triassic

Tidwell and Ash (1994)

Scolecopteris antarctica

Marattiaceae

Antarctica

Middle Triassic

Delevoryas et al. (1992)

Marattiopsis sp.

Marattiaceae

Italy

Middle Triassic (Anisian)

Van Konijenburg-van Cittert et al. (2006)

Marattiopsis marantacea

Marattiaceae

Marattiopsis muensteri (Goeppert) Schimper

Marattiaceae

Ogmos sp.

a Sources providing information about numerous occurrences and additional references include Li et al. (1995), Wang (1999), Escapa et al. (2014), and the Paleobiology Database (current version: http://fossilworks.org/cgi-bin/bridge.pl). Information about Romanian occurrances was provided by Dr. M. Popa (Bucharest), and about Hungarian occurrances was provided by Dr. M. Barbacka (Budapest).

References Arnold, C. A. 1964. Mesozoic and Tertiary fern evolution and distribution. Memoirs of the Torrey Botanical Club 21: 58e66. Ash, S. R. and J. F. Bassinger. 1991. A high latitude Upper Triassic flora from the Heiberg Formation, Sverdrup Basin, Arctic Archipelago. Geological Survey of Canada Bulletin 412: 101e131. Chen, Y. and S. Duan. 1981. Late Triassic flora of Hongni Yanbian District of Sichuan. In: 12th Annual Conference of the Palaeontological Society of China. pp. 153e157. Chen, Y., S. Duan and Y. Zhang. 1979. New species of late Triassic plants from Yanbian, Sichuan, I. Acta Botainca Sinica 21: 57e63. Delevoryas, T., T. N. Taylor and E. L. Taylor. 1992. A marattialean fern from the Triassic of Antarctica. American Journal of Botany 74: 101e107. Escapa, I.H., B. Bomfleur, N.R. Cuneo and R. Scasso. 2014. A new marattiaceous fern from the Lower Jurassic of Patagonia (Argentina): the renaissance of Marattiopsis. Journal of Systematic Palaeontology 13: 677e689. DOI: 10.1080/14772019.2014.936974.

Feistmantel, O. 1882. The fossil Flora of the South Rewah Gondwana Basin. Mem. Geol. Surv. India. Fossl Flor. Lower Gondwana, I. Fontaine, W.M. In: Ward, L.F. 1900. Status of the Mesozoic Floras of the United States, I. U.S. Geological Survey, 20th Annual Report, Washington, DC, USA. Göeppert, H.E. 1836. Die Fossilen Farnkrä Nova acta Leop. Car. vol. XVII, (Supplement). Halle, T. G. 1921. On the sporangia of some Mesozoic ferns. Arkiv for Botanik; Kungliga Svenska VetenskapsAkademiens Handlingar 17: 1e28. Harris, T M 1926. The Rhaetic flora of Scoresby Sound, East Greenland. Medd. Gronland, Kjobenhavin 68: 45e148. Herbst, R. 1988. La flora Triasica del Grupo el Tranquilo, Provincia de Santa Cruiz (Patagonia). Parte II. Filicopsida Ameghiniana 25: 365e379. Krasser, F. 1900. Die von W.A. Obrutschew in China and Centralasien 1893e94 gesammelten fossilen Pflanzen. Denkschriften Akademie der Wissenschaften in Wien LXX, pl. II. Krasser, F.1909. Die Diagnosen der von D. Stur in der obertriadischen Flora der Lunzerschichten als

356

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Marattiaceenarten unterschiedenen Farne. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften in Wien CXVIII. Abt. I. Kustatscher, E., K.-P. Kelber, and J. H. A. Van Konijnenburg-van Cittert. 2012. Danaeopsis Heer ex Schimper 1869 and its European Triassic species. Review of Palaeobotany and Palynology 183:32e49. Li P.J., Z.Y. Caoand S.Q. Wu. 1976. Mesozoic plants of Yunnan. pp. 87e160. In: Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, (Ed.). Mesozoic Fossils of Yunnan. I. Science Press, Beijing (in Chinese). Li, X., Z. Zhou, C. Cai, G. Sun, S. Ouyang, and L. Deng, (Eds.). 1995. Fossil Floras of China through the Geological Ages. Guangdong Science and Technology Press, Guangzhou, China. Lundblad, A. B. 1950. Studies in the Rhaeto-Liassic Floras of Sweden I (Pteridophyta, Pteridospermae, and Cycadophyta from the mining district of NW Scania). Kungliga Svenska Vetenskaps-Akademiens Handlingar 1: 1e82. Mogucheva, N.K. 1973. Early Triassic flora of the Tunguska basin. Nedra 154: 1e112. Möller, H. 1902. Bidrag till Barnholms Fossila Flora. Pteridofyter. Lunds Universitets Årsskrift XXXVIII(5). Schenk, A. 1883. Pflanzliche Versteinerungen. Richthofen’s “China”, vol. IV, Berlin, Germany. Schimper, W.P. 1869. Traité de Paléontologie végétale. vol. I, Paris, France. Seward, A.C. 1908. On a collection of fossil plants from South Africa. Quarterly Journal of the Geological Society LXIV(Pt. I): 95. Sze, H.C., Li, X.X., Zhou, Z.Y., Li, P.J., Wu, S.Q., Ye, M.N. and Shen., G.L. 1963. Mesozoic plants of China. vol. 2 of Fossil plants of China. Science Press, Beijing. 429 pp. (in Chinese). Tidwell, W. D. and S. R. Ash. 1994. A review of selected Triassic to Early Ceretaceous ferns. Journal of Plant Research 107: 417e442.

Van Konijenburg-van Cittert, J.H.A., E. Kustatscher and M. Wachtler. 2006. Middle Triassic (Anisian) ferns from Kühwiesenkopf (Monte Prá Della Vacco), Dolomites, Northern Italy. Palaeontology 49: 943e968. van Konijnenburg-van Cittert, J.H.A. 2002. Ecology of some Late Triassic to Early Cretaceous ferns in Euyrasia. Review of Palaeobotany and Palynology 119: 113e124. Wang, Y.D. 1999. Fertile organs and in situ spores of Marattia asiatica (Kawasaki) Harris (Marattiales) from the Lower Jurassic Hsiangchi Formation in Hubei, China. Review of Palaeobotany and Palynology 107:125e144. Ward, L. F. 1900a. Status of the Mesozoic floras of the United States. 1. The older Mesozoic. Twentieth Annual Report of the U.S Geological Survey. Part II: 211e748. Ward, L.F. 1900b. Status of the Mesozoic Floras of the United States, I. U.S. Geological Survey, 20th Anniversary Report, Washington, DC, USA. Webb, J. A. 1983. A new plant genus, possibly a marattialean fern from the Middle Triassic of eastern Australia. Memoirs of the Association of Australasian Palaeontologists 363e371. Xu, R. (Hsu, J.), J. Zhu, Y. Chen, S. Duan, Y. Hu and W. Zhu. 1974. New genera and species of Late Triassic plants from Yungjen, Yunnan, I. Acta Botanica Sinica 6: 266e278. Xu, R., J. Zhu, Y. Chen, S. Duan, Y. Hu and W. Zhu. 1979. Chinese Late Triassic Plants from Baoding. Science Press, Peking. 130 pp. Yang, X.H. 1978. Mesozoic plants. pp. 469e536. In: Chengdu Institute of Geology and Mineral Resources (Southwest China Institute of Geological Science), (Ed.). Palaeontological Atlas of Southwestern China: Sichuan. Pt 2. Geological Publishing House, Beijing (in Chinese). Zeiller, 1903. Pl. IX. Flore fossile des Gites de Carbon du Tonkin. Études des Gites Min. France. Paris. Pl. IX. (Rhaetic beds of Scania, Franconia and Tonkin).

Jurassic Occurrences of Marattialean Fernsa Species

Family

Stratigraphy/ Geography

Age (Ma)

References

Angiopteris blackii van Cittert

Marattiaceae

Yorkshire, UK

Aalenian? Middle Jurassic

van Konkjenburg-van Cittert (1975) Hill (1987)

Angiopteris richthofeni Schenk (M. muensteri?)

Marattiaceae

China

Jurassic

Schenk (1885)

Asterotheca fecunda sensu Sota and Archangelsky

?

Patignia

Formacio´n Can˜ado´n Largo, Jurassic

Herbst (1988)

Asterotheca fuchsii (Zeiller) Kurtz

?

Queensland

Ipswith Series, Jurassic

Townrow (1957)

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

Jurassic Occurrences of Marattialean Fernsadcont’d Species

Family

Stratigraphy/ Geography

Age (Ma)

References

Asterotheca menendezii sensu Sota and Archangelsky

?

Patigonia

Formacio´n Can˜ado´n Largo, Jurassic

Herbst (1988)

Asterotheca rigybana Herbst

?

Patigonia

Formacio´n Can˜ado´n Largo, Jurassic

Herbst (1988)

Daniopsis fecunda

Marattiaceae

Patigonia

Formacio´n Can˜ado´n Largo, Jurassic

Herbst (1988)

Marattia aganzhenensis Yang, Wang et Pfefferkorn

Marattiaceae

Gansu, China

Liassic; Lower Jurassic

Yang et al. (2008)

Marattia anglica (Thomas) Harris

Marattiaceae

England (Yorkshire)

Eustarine Series

Harris (1961)

Marattia asiatica Kawasaki

Marattiaceae

World wide

Lower Jurassic

Wang et al. (1999)

Marattia barnardii

Marattiaceae

Iran and Afghanistan

Lower Jurassic

Schweitzer et al. (1997)

Marattia hoerensis

Marattiaceae

Marattia intermedia

Marattiaceae

Iran

Lower Jurassic

Wang (1999) and van Konkjenburg-van Cittert (2002)

Marattia muensteri

Marattiaceae

France and Germany

Lower Jurassic

Schenk (1867) and Schimper (1869)

Marattia orientalis

Marattiaceae

Yunan, China, Vietnam, Korea, Japan

Lower Jurassic

Sze et al. (1963)

Marattiopsis spp.

Marattiaceae

China

Lower and Middle Jurassic

Li et al. (1995) Zhou (1983)

Arctic, Canada

Lower Jurassic

Ash and Basinger (1991)

Worldwide

Jurassic

Escapa et al. (2014)

Worldwide

Jurassic

Wang et al. (1999)

Southern China

Early-mid Jurassic

Li et al. (1995)

Hubei, China, East Asia, Middle East

Lower Jurassic

Yang (1978)

Marattiopsis asiatica

Marattiaceae

Marattiopteris boweri Seward ¼Angiopteris sensu Hill, 1987

Marattiaceae

Southerland, Scotland

Jurassic

Seward (1911) and van Konkjenburg-van Cittert and Van der Burgh (1989) Hill (1987)

Marattiopsis macrocarpa

Marattiaceae

India

Jurassic

Seward and Sahni (1920)

Marattiopsis muensteri Goeppert

Marattiaceae

Bornholm

Jurassic

Bartholin (1982)

California

Fontaine in Ward (1900)

Cauceasia & Turkestan, Egypt

Mo¨ller (1902); Seward (1907)

Rinitsia colliveri Herbst

Marattiaceae

Patigonia

Formacio´n Can˜ado´n Largo, Jurassic

Herbst (1988)

Tranquilia jalfinii Herbst

Marattiaceae

Patigonia

Formacio´n Can˜ado´n Largo, Jurassic

Herbst (1988)

Tranquilia whitneyi (Newberry) Herbst

Marattiaceae

Patigonia

Formacio´n Can˜ado´n Largo, Jurassic

Herbst (1988)

a Sources providing information about numerous occurrences and additional references include Li et al. (1995), Wang (1999), Escapa et al. (2014), and the Paleobiology Database (current version: http://fossilworks.org/cgi-bin/bridge.pl). Information about Romanian occurrances was provided by Dr. M. Popa (Bucharest), and about Hungarian occurrances was provided by Dr. M. Barbacka (Budapest).

357

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SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

References Ash, S. R. and J. F. Bassinger. 1991. A high latitude Upper Triassic flora from the Heiberg Formation, Sverdrup Basin, Arctic Archipelago. Geological Survey of Canada Bulletin 412: 101e131. Bartholin, C.T. 1892. pl. IX. Nogle I den bornholmske Jurasformation furkommmende Plantefursteninger. Botanisk Tidskrift Kjövenhaven XVIII(1). Escapa, I.H., B Bomfleur, N.R. Cuneo and R. Scasso. 2014. A new marattiaceous fern from the Lower Jurassic of Pataghonia (Argentina): the renaissance of Marattiopsis. Journal of Systematic Palaeontology 13: 677e689. DOI: 10.1080/14772019.2014.936974. Fontaine, In: Ward. 1900. pl. LV, Figs. 305. Harris, T.M. 1961. The Yorkshire Jurassic Flora, I: thallophyta-Pteridophyta. British Museum (Natural History), London, UK. Herbst, R. 1988. La flora Triasica del Grupo el Tranquilo, Provincia de Santa Cruiz (Patagonia). Parte II. Filicopsida Ameghiniana 25: 365e379. Hill, C.R. 1987. Jurassic Angiopteris (Marattiales) from North Yourkshire. Review of Palaeobotany and Palynology 51: 65e93. Li, X., Z. Zhou, C. Cai, G. Sun, S. Ouyang, and L. Deng, (Eds.). 1995. Fossil Floras of China through the Geological Ages. Guangdong Science and Technology Press, Guangzhou, China. Möller, H. 1902. Bidrag till Barnholms Fossila Flora. Pteridofyter. Lunds Universitets Årsskrift XXXVIII(5). Schenk, A. 1885. Die während der Reise des Grafen Bela Széchenyi in China gesammelten fossilen Planzen. Palaeontographica XXXI: 165. Schimper, W.P. 1869. Traité de paléontologie végétale. 1. Bailliére, Paris. Schweitzer, H.J., J.H.A.Van Konijnenburg-van Cittert and Van der Burgh, J. 1997. The Rhaeto-Jurassic flora of Iran and Afghanistan. 10. Bryophyta, Lycophyta, Sphenophyta, PteridophytadEusporangiatae and Protoleptosporangiatae. Palaeontographica 243B: 103e192. Sehenk, A. 1867. Die fossile Flora der Grenzschichten des Keupers und Lias Frankens. Kreidel, Wiesbaden. Seward, A.C. 1907. Jurassic plants from Caucasia and Turkestan. Mém. Com. Géol. St. Pétersbourg, Livr vol. 38, pl. II, Figs. 16e18.

Seward, A.C. 1911. The Jurassic flora of Southerland, Transactions of the Royal Society of Edinburgh 47: 643e709. Seward, A.C. and B. Sahni. 1920. Indian Gondwana Plants: A Revision. Palaeontographica India, Geological Survey of India Memiors n.s., vol. 7, no. 1. Government of India Central Publication Branch, Calcutta, India. Sze, H.C., Li, X.X., Zhou, Z.Y., Li, P.J., Wu, S.Q., Ye, M.N. and Shen., G.L. 1963. Mesozoic plants of China. Volume 2 of Fossil Plants of China. Science Press, Beijing. 429 pp. (in Chinese). Townrow, J.A. 1957. On Dicroidium, probably a pteridospermous leaf, and other leaves now removed from this genus. South African Journal of Geology 60: 1e36. Van Konijnenburg-van Cittert, J.H.A. 2002. Ecology of some Late Triassic to Early Cretaceous ferns in Eurasia. Review of Palaeobotany and Palynology 119: 113e124. Van Konijnenburg-van Cittert, J.H.A. and Van der Burgh, J. 1989. The flora from the Kimmeridgian (Upper Jurassic) of Culgower, Sutherland, Scotland. Review of Palaeobotany and Palynology 61: 1e51. Van Konkjenburg-van Cittert, J.H.A. 1975. Some notes on Marattia anglica from the Jurassic of Yorkshire. Review of Palaeobotany and Palynology 20: 205e214. Wang, Y.D. 1999. Fertile organs and in situ spores of Marattia asiatica (Kawasaki) Harris (Marattiales) from the Lower Jurassic Hsiangchi Formation in Hubei, China. Review of Palaeobotany and Palynology 107: 125e144. Wang, S-J., C.S. Li and B.L. Tian. 1999. Anatomy of a new species of Scolecopteris (Marattiales) from early stage of early Permian in China. Acta Botanica Sinica 41: 433e438. Yang, S., Wang, J. and Pfefferkorn, H.W. 2008. Marattia aganzhensis sp. nov., from the Lower Jurassic Daxigou Formation of Lanzhou, Gansu, China. International Journal of Plant Sciences 169: 473e482. Yang, X.H. 1978. Mesozoic plants. pp. 469e536. In: Chengdu Institute of Geology and Mineral Resources (Southwest China Institute of Geological Science), (Ed.). Palaeontological Atlas of Southwestern China: Sichuan. Pt 2. Geological Publishing House, Beijing (in Chinese). Zhou, Z. 1983. Late Triassic plants from Shaqiao, Hengyang, Hunan Province. Palaeontologica Cathaya 4: 131e197.

Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification Chapter j 14

359

Cretaceous Occurrences (and Unconfirmed Reports) Species

Nature of Fossils

Family

Stratigraphy/ Geography

Escapia christensenioides

Synangia/pinule fragment

Psaroniaceae

Valangenian

Rothwell et al. (2016, this report)

Marattiopsis vodrazke

Pinnules/synangia

Marattiaceae

Campanian

Kva
cek (2014)

Gosauopteris danaeoides

Vegetative simple leaves

Toothed, entire vegetative leaves; possible Maratiaceae

Campanian

Herman and Kva
cek (2010)

Nathorstia agustifolia Heer

Pinnules/sporangia

Matoniaceae

L. Cretaceous/ Greenland

Heer (1880)

?

L. Cretaceous/ Bohmea

Bayer (1899) Nathorst (1908) Krassilov (1964) Van Konijnenburgvan Cittert (1993)

References

Uncomfirmed Reports

Drymaria fascia Bayer (¼Nathorstia?)

Danaea firmis Heer

Pinnules and “synangia”

?

Cretaceous/Greenland

Heer (1868e1883)

Goolangia minnesotensis Hu, Dilcher, H. Schneid., & Jarzen

Coalified sporangium with spores

?, coalified sporangia of uncertain affinities

Dakota Formation, Latest Albian to earliest Cenomanian/ Minnesota

Hu et al. (2006)

Mesozoisynangia trilobus Hu, Dilcher, H. Schneid., et Jarzen

Coalified sporangia with spores

?, coalified sporangia of uncertain affinities

Dakota Formation, Latest Albian to earliest Cenomanian/ Minnesota

Hu et al. (2006)

References Bayer, G. 1899. Einige neue Pflanzen der Perucer Kreideschichten in Böhemen. Sitzungsberichte der KöniglichBöhmischen Gesellschaft der Wissenschaften in Prag. Heer, O. 1868e1883. Flora Fossilis Arctica. Zurich, Switzerland. Heer, O. 1880. Nachträge zur Fossilen Flora Grönlands. Kungliga Svenska Vetenskaps-Akademiens Handlingar XII. (Flore Fossile Arctic vol. VI. 1882). Herman, A.B. and J. Kva
cek. 2010. Late Cretaceous Grünbach Flora of Austria. Naturhistorisches Museum Wien. Österreich, Austria. Hu, S., D. L. Dilcher, H. Schneider and D. M. Jarzen. May 2006. Eusporangiate Ferns from the Dakota Formation, Minnesota, U.S.A. International Journal of Plant Sciences 167(3): 579e589.

Krassilov, V.A., 1964. On the genus Nathorstia (ferns). Paleontology Zh. 2: 115e120. Kva
cek, J. 2014. Marattiopsis vodrazkae sp. nov. (Marattiaceae) from the Campanian of the Hidden Lake Formation, James Ross Island, Antarctica. Acta Musei Nationalis Pragae Series BeHistoria Naturalis 70: 211e218. Nathorst, A.G. 1908. Paläbotanisch. Mitteilungen, III. Vetenskaps-Akademiens Handlingar XLIII(3). Rothwell, G.W., M.A. Millay and R.A. Stockey. 2016. Escapia gen. nov.: morphological evolution, environmental distribution, and the evolutionary/paleophytographic diversification of marattialean ferns (this report). van Konijnenburg-van Cittert, J.H.A. 1993. A review of the Matoniaceae based on in situ spores. Review of Palaeobotany and Palynology 78: 235e267.

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SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Post-Cretaceous Reported Occurrences of Uncertain Affinities Nature and Affinities of Fossils

Species

Family

Geography

Age

References

Angiopteris ruzinciniana Palamarev, Petkova & Usunova

?

Vegetative leaf fragments; uncertain affinities, probably angiosperm

Bulgaria

Upper Miocene

Palamarev et al. (1975) and Hill (1987)

Danaea coloradensis Knowlton

?

Pinnule; unidentifiable

Colorado, USA

Eocene

Knowlton (1922, 1930) and MacGinitie (1969)

Danaea borealis Pabst

?

Vegetative pinnules; uncertain affinities

Washington State, USA

Eocene

Pabst (1968)

Marattia hookeri Gardner & Ettingshausen

?

Vegetative pinnules; uncertain affinities

Isle of White

Eocene

Gardnerand von Ettingshausen (1882)

References Gardner, J.S. and C. von Ettingshausen. 1882. A monograph of the British Eocene Flora. vol. I. Filices. Palaeont. Soc. London. pl. XII. Figs. 1e7. Hill, C.R. 1987. Jurassic Angiopteris (Marattiales) from North Yourkshire. Review of Palaeobotany and Palynology 51: 65e93. Knowlton, F.H. 1922. Revision of the flora of the Green River Formation, with description of new species. U.S. Geological Survey Professional Paper F131: 133e182. Knowlton, F.H. 1930. The flora of the Denver and associated Formations of Colorado. Professional Papers U.S. Geological Survey 155: 1e142, 59 pls.

MacGinitie, H.D. 1969. The Eocene Green River flora of northwestern Colorado and northeastern Utah. University of California Publications in Geological Sciences 83: 1e203. Pabst, M.B. 1968. The flora of the Chuckanut Formation of northwestern Washington; The Equisetales, Filicales, and Coniferales. University of California Publications in Geological Sciences 76: 1e61. Palamarev, E., Petkova, A. and Usunova, K. 1975. Fossil fern fronds from the Miocene of Bulgaria. Fitologiya 2: 25e33.

Chapter 15

Heterosporous Ferns From Patagonia: The Case of Azolla Facundo De Benedetti1, Marı´a del C. Zamaloa2, Marı´a A. Gandolfo3 and Ne´stor Rube´n Cu´neo1 1

Museo Paleontológico Egidio Feruglio, CONICET, Trelew, Argentina; 2Universidad de Buenos Aires, Buenos Aires, Argentina; 3Cornell University,

Ithaca, NY, United States

1. INTRODUCTION Azolla Lamarck is a genus of aquatic ferns characterized by its small floating sporophyte, which consists of a profusely branched stem bearing alternately arranged imbricate leaves and pendulous roots (Saunders and Fowler, 1993). The leaves are two-lobed: one floating dorsal lobe and one submerged ventral lobe. Azolla is heterosporous and carries indusiate sori on short stalks surrounded by a parenchymatous layer known as the sorophore envelope (Nagalingum et al., 2006). The megasporangiate sorus bears a single megasporangium, which in turn produces a solitary viable megaspore, whereas the microsporangiate sorus produces 8e130 pedunculated microsporangia, each one containing approximately 3e10 pseudocellular structures called massulae, and each in turn containing 32e64 microspores (Lumpkin and Plucknett, 1980). Nagalingum et al. (2006) restricted the term “sporocarp” to a sorophore envelope and all it contains. About seven extant species are attributed to Azolla, with tropical and temperate worldwide distribution (Pereira et al., 2011); they are found freely floating and forming extensive communities due to their active vegetative multiplication in low-energy freshwater environments such as swamps and ponds (Carrapiço, 2010). The genus has a worldwide fossil record that extends back to the Late Cretaceous, but the stratigraphic range of individual species is relatively short (Fowler, 1975; Collinson, 1980; Kovach and Batten, 1989; Batten and Kovach, 1990). Most fossil species are known only from dispersed megaspores and massulae because these structures are impregnated with sporopollenin that gives them high resistance to decay (Hall, 1968; Lucas and Duckett, 1980). The fragile sporophyte is rarely preserved (Sahni and

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00015-2 Copyright © 2018 Elsevier Inc. All rights reserved.

Rao, 1934; Sahni, 1942; Sweet and Chandrasekharam, 1973; Melchior and Hall, 1983; Nambudiri and Chitaley, 1991; McIver and Basinger, 1993; Hoffman and Stockey, 1994; Gandolfo et al., 2014). In Argentina, the Late Cretaceous record is abundant although it is based principally on microspore massulae, which have little or no systematic value (Palamarczuk and Gamerro, 1988; Papú, 1988, 1990, 2002; Papú et al., 1988; Puebla et al., 2014; Quattrocchio et al., 2005; Vallati, 2010). In contrast, megaspores, which have a high taxonomic value, are scarcely recorded and only one species has been formally described from the Late Cretaceous of Patagonia (Vallati et al., 2017). Cúneo et al. (2014) and Gandolfo et al. (2014) reported, without describing, the presence of Azolla-like megaspores and microspore massulae, and sporophytes, from sediments of the Upper Cretaceous La Colonia Formation. In this contribution, we describe in detail a new species of Azolla based on megaspores attached to microspore massulae from the Upper Cretaceous La Colonia Formation, Chubut Province, Patagonia, Argentina (Fig. 15.1AeC). We compare the new species with extant and fossil species and discuss its paleogeographical and paleoenvironmental implications. In addition, we briefly discuss the value of fossil Azolla spores for understanding the phylogeny of the genus.

2. MATERIAL AND METHODS 2.1 Stratigraphy The La Colonia Formation outcrops on the southeast slope of the Somuncurá Massif, which is exposed between Telsen and Gan Gan, Chubut Province, Patagonia, Argentina (Fig. 15.1A,B). The unit is considered to have been deposited during the Late Cretaceous (Campanian-Maastrichtian), 361

362

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

(A)

(B)

(C)

FIGURE 15.1 Map showing the location of the outcrops of La Colonia Formation in Chubut Province, Argentina. The studied samples come from the mid-levels of the Cañadón del Irupé and Quebrada del Helecho localities (red dots).

although its upper levels could be earliest Paleocene in age, as indicated by several chronostratigraphic markers including marine invertebrates, dinoflagellates, mammals, dinosaurs, and plant macrofossils (Bonaparte, 1985; Gasparini and Spalletti, 1990; Pascual et al., 2000; Gandolfo and Cúneo, 2005; Navarro et al., 2012; Cúneo et al., 2014; Gandolfo et al., 2014; Guler et al., 2014; Gasparini et al., 2015; Borel et al., 2016). The La Colonia Formation consists of thick, mostly clayey or silty beds that are massive, laminated, or heterolithic. The samples examined in this report come from the mid-levels exposed at the Cañadón del Irupé and Quebrada del Helecho localities (Fig. 15.1C). These sediments were deposited in freshwater coastal environments (lagoons or similar), with sporadic fine-grained sand beds associated with coastal sand bars (Cúneo et al., 2013, 2014).

light microscopy (LM) and directly on stubs using doublesided tape for SEM. LM observations were made with a Leitz Dialux 20 microscope coupled with a Leica EC3 camera at the Facultad de Ciencias Exactas y Naturales of the Universidad de Buenos Aires (FCEN, UBA). SEM observations were made with a Philips XL30 TMP microscope at the Museo Argentino de Ciencias Naturales Bernardino Rivadavia (MACN), Buenos Aires, Argentina. For transmission electron microscopy (TEM), megaspores were treated following standard techniques (Baldoni and Taylor, 1985) and observed with a Zeiss-EM109T microscope at the Facultad de Medicina of the Universidad de Buenos Aires (FMED, UBA), Buenos Aires, Argentina. All specimens are deposited in the palynological collection of the Museo Paleontológico Egidio Feruglio (MEF), Trelew, Chubut, Argentina, under the numbers MPEF-PA 80 to 99.

2.2 Palynological Techniques

2.3 Terminology and Classification

Sedimentary samples were mechanically disaggregated and treated with hydrofluoric acid (70%) and hydrochloric acid (30%). The residues were decanted and washed several times; as a result, several hundred specimens were recovered. Megaspores and massulae were picked and cleared with 10% sodium hypochlorite solution for 5e20 min. Longitudinal sections of megaspores for scanning electron microscopy (SEM) were made by using a razor blade. Specimens were mounted on slides with glycerin jelly for

The megaspore apparatus of the heterosporous fern Azolla is the most complex reproductive structure among extant pteridophytes (Tryon and Lugardon, 1991), and the terminology used to describe the megaspore apparatus and its associated massulae varies considerably (see Kempf, 1969; Sweet and Hills, 1976; Fowler, 1975; among others). Here, we follow the terminology of Fowler and Stennett-Willson (1978) as used by Collinson (1980, 1991), Batten and Collinson (2001), Collinson et al. (2009, 2010, 2013), and

Upper Cretaceous Azolla From Patagonia, Argentina Chapter j 15

Van der Burgh et al. (2013) among others. The basic megaspore apparatus of Azolla consists of the megaspore body and the floating or “swimming” apparatus situated on the proximal pole. The megaspore is nearly spherical and has a trilete mark. The floating apparatus consists of pseudocellular structures, or floats, that are attached to the megaspore either directly or by a columella (an extension of the perine located above the trilete laesurae from which hairs arise to enmesh the floats), and sometimes a collar (a structure that delimits the periphery of the proximal surface of the megaspore). The term “float” is a misnomer, because it has been demonstrated conclusively that the floats do not render the megaspores more buoyant (Fowler, 1975). The sporoderm consists of three layers: the intine (thin inner layer, not preserved in fossils), the exine (megaspore wall proper), and the perine (additional external layer). The perine is formed by an inner, commonly “granular” endoperine and an outer, “columnar” exoperine, which in the surface view has a baculate, regulate, to tuberculate and/or reticulate appearance. Hairs may extend from this surface and cover much or all of the megaspore apparatus to form the filosum. If they originate below the collar region (over the megaspore itself), they are termed infrafilosum; if they originate from the collar region, the columella, or from the floats, they represent the suprafilosum (Batten and Collinson, 2001). The microspores are spherical with trilete laesurae, variable in number and embedded in a pseudocellular matrix termed massulae (Lumpkin and Plucknett, 1980; Saunders and Fowler, 1993). In most species, the massulae develop external projections called glochidia, whose function is to attach the massulae to the megaspores by becoming entangled with the filaments of the filosum (Hoffman and Stockey, 1994). Glochidia can be filamentous or can have circinate, globular, or anchor-shaped tip terminations (Hall, 1969). Spore terminology follows Punt et al. (2007). Suprageneric classification follows Smith et al. (2006). Numbers between brackets represent the arithmetic average of the range of measurements.

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Additional material: MPEF-PA 87e91, 96e99 Repository: Palynology Collection, MEF Type locality: Cañadón del Irupé, NE Chubut Province Stratigraphic horizon: La Colonia Formation, Upper Cretaceous

3.2 Specific Diagnosis Megaspore apparatus is ovoid, c. 360 (400) 520 mm long and c. 260 (270) 360 mm wide, partially covered by a thick mat of intertwined hairs. Megaspore trilete, spherical to sub-spherical, c. 250e320 mm in diameter. Megaspore wall is formed by exine and a much thicker two-layered perine. In LM, exine and endoperine appear homogeneous, whereas exoperine is columellate and has a reticulate surface. In thin section under TEM, exine is relatively homogeneous with dispersed small irregular cavities; endoperine is of granular appearance and spongy structure; exoperine consists of contorted nodular or clavate to tabular partially fused masses. Under SEM, exoperine surface consists of muri linked to form a reticulum with rounded lumina. Hairs emerge from the exoperine surface and cover completely the megaspore forming the infrafilosum. Float system is thimble shaped, occupying at least the upper twofifths of the megaspore apparatus. Floats spongy pseudovacuolate, 18e21 or more, arranged in three (exceptionally four) tiers. Lower level with 9e12 small spherical, elliptical, or rhomboidal floats that extend over the proximal surface of the megaspore. Middle level with 6 or more larger floats, rhombic-shaped or irregular, often with a large invagination. Upper level with three large rhombic floats with deep invaginations. Modified perine forms a proximal dome-shaped columella. Hairs arise from the reticulate surface of the floats and from the columella. Microspore massulae are irregular, elliptical or triangular in shape, with a granular appearance and spongy vacuolated structure. Microspores trilete, psilate, c. 14e30 mm in equatorial diameter. Surface of the microspore massulae with numerous aseptate glochidia of up to 35 mm long, with a stalk of uniform width and distally broadening and then constricted below an anchor-shaped tip. Flukes narrow gradually and with recurved hooks.

3.1 Systematic Palaebotany

3.3 Description

Order Salviniales Britton, 1901 Family Salviniaceae Martinov, 1820 Genus Azolla Lamarck, 1783 Type species Azolla filiculoides Lamarck, 1783 Azolla coloniensis De Benedetti and Zamaloa, sp. nov. Derivation of name: from the stratigraphic unit La Colonia Formation Holotype: MPEF-PA 80 Paratypes: MPEF-PA 80e86, 92e95

MegasporesdThe megaspore apparatus is oval to elliptical in outline (Plate I, 1e4), sometimes distorted by compaction (Plate II, 2). Many specimens were found with stalk remains (Plate I, 5). The megaspore apparatus is composed of a spherical to sub-spherical megaspore (Plate I, 3 and 4) and a float apparatus (Plate I, 1e8). The rays of the trilete laesurae extend up to half of the spore radius (Plate I, 12). The megaspore apparatus is partially covered by a thick mat of intertwined hairs. The megaspore surface is

PLATE I Megaspore apparatuses and megaspore of Azolla coloniensis sp. nov. (1e3, 5e7, 9e11, and 13e21: SEM; 4, 8, and 12: LM). Scale bars: (1e8, 15, and 19) ¼ 100 mm; (9e11, 13, 16, 17, 20, and 21) ¼ 20 mm; (14) ¼ 10 mm; (18) ¼ 5 mm; (12) ¼ 40 mm. (1) Megaspore apparatus with three levels of rhomboidal floats. MPEF-PA 80. (2) Megaspore apparatus with four levels of floats well defined. MPEF-PA 81. (3) Megaspore apparatus uncompressed, showing the spherical megaspore. MPEF-PA 80. (4) Megaspore apparatus showing the spherical megaspore and the float apparatus located on the proximal region. Note the thick perine. MPEF-PA 92. (5) Megaspore apparatus revealing the columella (c). Note perinal hairs (h) that enmeshed the floats, stalk remains (st), and two microspore massulae attached near center of megaspore apparatus (arrows). MPEF-PA 81. (6) Megaspore apparatus. A megaspore fragment is displaced towards the apex, on the right side. Numerous microspore massulae are entangled among the perinal hairs of the columella that still holds together most of the floats. MPEF-PA 81. (7) Megaspore apparatus in polar view showing the three invaginated floats of the upper level. MPEF-PA 81. (8) Megaspore apparatus showing floats with deep invaginations and reticulate surface. MPEF-PA 92. (9) Detail from (5). Columella extending proximally through the float system. MPEF-PA 81. (10) Detail from (7). Megaspore surface completely covered by a thick mat of intertwined hairs (infrafilosum). MPEF-PA 81. (11) Detail from (7). Float surface partly visible beneath the covering of hairs (suprafilosum). Note the reticulate surface and the isolated glochidia. MPEF-PA 81. (12) Trilete laesurae. MPEF-PA 93. (13) Detail from (6). Float with reticulate surface from the middle level. Note the isolated glochidia (arrow). MPEF-PA 81. (14) Detail from (6). Megaspore fragment. Note the reticulate surface of the exoperine. MPEF-PA 81. (15 and 19) Longitudinal sections of megaspore apparatus. (15) MPEF-PA 81; (19) MPEF-PA 82. (16) Detail from (15). Spongy structure of the floats. MPEF-PA 81. (17) Detail from (15). Megaspore wall showing foveas in inner and outer sides of the exine (ex). MPEF-PA 81. (18) Detail from (15). Close up of the megaspore wall showing exine (ex), endoperine (enp) and exoperine (exp). MPEF-PA 81. (20) Detail from (19). Foveas in the inner side of the exine. MPEF-PA 82. (21) Detail from (19). Megaspore wall showing the strongly vacuolated structure of the perine. MPEF-PA 82.

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PLATE II Megaspore apparatuses and microspore massulae of Azolla coloniensis sp. nov. (1e8, 10 and 11: SEM; 9 and 12: LM; 13 and 14: TEM). Scale bars: (1 and 2) ¼ 100 mm; (3) ¼ 200 mm; (4 and 5) ¼ 50 mm; (6e9) ¼ 20 mm; (10 and 11) ¼ 5 mm; (12) ¼ 15 mm; (13) ¼ 10 mm; (14) ¼ 4 mm. (1) Megaspore apparatus with two clusters of microspore massulae attached (arrows). MPEF-PA 83. (2) Megaspore apparatus compressed from the apex to the base, with attached microspore massulae (arrow). MPEF-PA 83. (3) Cluster of microspore massulae inferred to represent the partial content of a microsporangiate sorus, and each spherical to ovoid compact subunit inferred to represent the content of one microsporangium. Note the cluster at the base slightly separated into component massulae (arrow). MPEF-PA 83. (4 and 5) Typical ovoid clusters of microspore massulae. One of these with peduncle remains (arrow in 5). (4 and 5) MPEF-PA 83. (6 and 7) Microspore massulae with numerous anchor-shaped tips glochidia, some with broad basal attachment (arrow in 7). (6) MPEF-PA 85; (7) MPEF-PA 84. (8) Cluster of massulae exposing the inner microspores. MPEF-PA 83. (9) Microspore massulae with four trilete microspores (arrows). MPEF-PA 94. (10) Detail of glochidia. Note the recurved hooks (arrows). MPEF-PA 84. (11) Glochidia entwined in the perinal hairs of the megaspore apparatus (arrow). MPEF-PA 86. (12) Microspore massulae showing microspore contents and aseptate glochidia. Note the trilete mark (arrow). MPEF-PA 94. (13) Thin-section through whole compressed specimen showing megaspore wall layers. MPEF-PA 95. (14) Detail from (13). Megaspore wall showing the homogeneous exine (ex), the spongy endoperine (enp) and the dense elements of the exoperine (exp). MPEF-PA 95.

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completely covered by the infrafilosum, with hairs c. 0.4e1.0 mm in diameter (Plate I, 10); however, the floats surface is usually partly visible beneath the suprafilosum (Plate I, 11 and 13). In LM, exine and endoperine appear homogeneous, whereas exoperine is columellate (Plate I, 4). Under LM and SEM, the exoperine surface is clearly reticulate (Plate I, 4 and 14) with muri of about 1.0e2.5 mm in width and rounded lumina of up to 5.5 mm in diameter (Plate I, 14). SEM and TEM analyses shows that the wall consists of an exine, c. 3e4 mm thick, and a vacuolated two-layered perine, c. 12e20 mm thick (Plates I, 15,18,19,21 and II, 13,14). Under TEM, the exine has dispersed small irregular cavities (Plate II, 13 and 14). The endoperine is c. 4e8 mm thick and has a granular appearance and a spongy structure (Plate II, 14). The exoperine is c. 6e12 mm thick and consists of contorted nodular or clavate masses, sometimes elongated parallel to the megaspore surface, and covering internal cavities (Plate II, 14). In most of the SEM sections, the inner and outer surfaces of the exine show foveas (of up to 6 mm in diameter) that are irregularly arranged (Plate I, 17 and 20). Float system extends over the proximal surface of the megaspore and consists of 18e21 or more floats arranged in three tiers (only one specimen was found with four tiers, see Plate I, 2). The floats are spongy (Plate I, 8, 16 and 19) and variable in shape and size (c. 50e150 mm). The lower level of floats covers part of the megaspore body and is the most numerous, consisting of 9e12 small spherical, elliptical, rhombic, or irregular floats (Plate I, 1 and 6). The floats of the middle level are larger and lesser in number than those of the lower level (6 or more), and they often have a large central invagination and are irregular to rhombic shaped (Plate I, 1, 2 and 6). Floats of the middle level sometimes overlap the floats of the lower level (Plate I, 6). At the upper level, there are three rhombic shaped floats with deep invaginations (Plate I, 1, 6 and 7). If there is a fourth level, the floats are like those of the lower level (Plate I, 2). The float surface is reticulate and hairs emerge from it (Plate I, 8, 11, and 13). The perine forms a cone-shaped columella that extends proximally through the float system and covers the trilete laesurae of the megaspore (Plate I, 5). The columella surface is scabrate, and hairs arise from this to enmesh the floats (Plate I, 9). The perinal hairs that arise from both the columella, and the floats constitute the suprafilosum (reconstruction in Fig. 15.2). MicrosporesdThe microspore massulae were found attached to the megaspore apparatus in groups (Plates I, 5, 6, and II, 1) or alone (Plate II, 2) and isolated as single massulae (Plate II, 6, 7 and 9) or grouped in clusters (Plate II, 3e5). Some of these groups appear to represent the partial content of a microsporangiate sorus (Plate II, 3), and some spherical to ovoid clusters are interpreted as the content of the entire microsporangia (c. 195 mm in

FIGURE 15.2 Reconstruction of sectional view of A. coloniensis; c, columella; enp, endoperine; ex, exine; exp, exoperine; inf, infrafilosum; sf, suprafilosum. Scale bar ¼ 100 mm.

maximum dimension) due to the arrangement of strongly appressed massulae (Plate II, 4 and 5). One of these clusters seems to preserve the remains of the microsporangial wall and the base of the stalk (Plate II, 5). The number of massulae per microsporangia is difficult to determine but appears to be 16 of them (Plate II, 1, 4, and 5) and probably 4 microspores per massulae (Plate II, 9). The microspore massulae are variable in size [c. 55 (75) 140 mm in diameter] and shape; they can be rounded, elliptical, or triangular and have a granular appearance (Plates I, 5, 6 and II, 6, 7). They are spongy with a vacuolated structure (Plate II, 9 and 12). The microspores are trilete, psilate (Plate II, 8, 9 and 12), with rays of the laesurae extending about one third of the spore radius (Plate II, 12). The surface of the microspore massulae has numerous aseptate glochidia up to 30 mm long, with relatively uniform stalk (1.2e1.7 mm wide) and sometimes with broad (up to 7 mm wide) basal attachment, but always with a distal dilation and a distinct constriction below an anchorshaped tip (4e6 mm wide) (Plate II, 6, 7, and 10e12). The total fluke length is up to 6 mm long. The flukes narrow gradually and have recurved hooks (Plate II, 10). The anchor-shaped tips of the glochidia serve to attach the massulae to the perinal hairs of the megaspore apparatus (Plate II, 11).

4. DISCUSSION Fossil and extant Azolla megaspores are characterized by the spore body shape, the presence of floats on the proximal pole, and the spore wall consisting of an exine and a twolayered perine, while the microspores are spherical and embedded in massulae. All these diagnostic features are observed in the Patagonian spores; therefore, there is no doubt that the spores recovered from the La Colonia Formation belong to the genus Azolla.

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4.1 Comparison With Modern Azolla Species

4.2 Comparison With Other Fossil Azolla Species

The taxonomy of Azolla is controversial; six or seven extant species have been proposed. The species identification relies on vegetative and reproductive characters, but some of them are highly variable leading to misinterpretations and, as a result, several classifications have been proposed (i.e., Svenson, 1944; Saunders and Fowler, 1993; Evrard and van Hove, 2004). Molecular data did not provide a conclusive Azolla taxonomy (Reid et al., 2006; Metzgar et al., 2007; Pereira et al., 2011). Currently, most authors accept seven species placed in two sections differentiated by reproductive characters: section Azolla (A. caroliniana Willd., A. mexicana Presl., A. microphylla Kaulf., A. filiculoides Lam., and A. rubra R.Br.) and section Rhizosperma (A. nilotica Decne. ex Mett. and A. pinnata R.Br.). The sections can be distinguished by the number of floats that are present in the megaspore apparatus; while in section Azolla there are three floats in one tier, section Rhizosperma presents nine floats arranged in two tiers (six in the lower and three at the top). As mentioned, Azolla coloniensis is characterized for having 18e21 or more floats; consequently, it does not belong to either section. Clearly, Azolla coloniensis differs from all modern species because of the features of its floating apparatus. Furthermore, extant species have rounded to subtriangular floats with few perinal hairs, whereas in A. coloniensis, the floats are variable in size and shape and are covered with a dense mat of hairs. In addition, the float zone of extant species is divided into three compartments that originate from the suprafilosum and, together with the apical cap (part of the original megasporangial wall) and the basal collar, constitute the retention mechanism (Collinson, 1980; Saunders and Fowler, 1993). A. coloniensis lacks an apical cap and collar, and the float zone is not divided into compartments. Differences are also conspicuous when comparing extant and the Patagonian fossil microsporangia. Microsporangia of modern species contain 32e64 microspores arranged in 3e10 massulae (Lumpkin and Plucknett, 1980 Nagalingum et al., 2006), while in A. coloniensis there are probably 64 microspores but arranged in 16 massulae (w four per massulae). Members of section Azolla produce microspore massulae that have glochidia with anchorshaped tips, while in section Rhizosperma, the glochidia are hair shaped (A. pinnata) or they are absent (A. nilotica) (Guo-Fan and Yue-Chan, 1987). Remarkably, A. coloniensis have aseptate glochidia with anchor-shaped tips similar to those present in section Azolla; however, extant species usually have septate glochidia, although both septate and nonseptate glochidia may be found in the same massulae (Pereira et al., 2001).

Fossil species delimitation in Azolla is based primarily on the anatomy and morphology of the reproductive structures and the ultrastructure of the megaspore wall (Kempf, 1969; Snead, 1969; Fowler and Stennett-Willson, 1978); based on these characters, approximately 70 Azolla sp. are currently recognized in the fossil record that extends back into the Upper Cretaceous (complete lists can be found in Sweet and Hills, 1976; Collinson, 1980; Batten and Kovach, 1990; Vajda and McLoughlin, 2005). The majority of Azolla fossil sp. differ from A. coloniensis in that all of them have nine or fewer floats and all lack glochidia or glochidia with anchor-shaped tips. Therefore, we discarded the placement of the Patagonian fossils in any of them. It is important to mention that Vallati et al. (2017) recently described a new fossil species of Azolla, A. colhuehuapensis, based on megaspores and massulae from the Maastrichtian Lago Colhué Huapi Formation, Golfo San Jorge Basin, Chubut, Patagonia, Argentina. A distinctive feature of this species is that the floats are located in compartments of prismatic geometry separated by a dense hairy wall. These compartments are very similar to the invaginations observed in the floats of A. coloniensis and, like those, may represent the entire floats. However, A. colhuehuapensis belongs to section Rhizosperma, precisely, because of the number and position of the floats and the lack of glochidia (Vallati et al., 2017). Interestingly, only 13 fossil species previously described are characterized by multifloated megaspores and microspore massulae with anchor-shaped glochidia (Table 15.1). All these species come from Northern Hemisphere areas except for A. boliviensis Vajda and McLoughlin reported from Bolivia. Azolla teschiana Florschütz emend. Batten and Collinson and Azolla bulbosa Snead emend. Sweet and Hills can be easily distinguished from A. coloniensis by the presence of protuberances on the exoperine surface, a feature absent in the Patagonian material (Batten and Collinson, 2001; Sweet and Hills, 1976). Azolla anglica Martin has a lessdeveloped filosum and up to 24 floats arranged in three tiers, but the floats do not have invaginations (Martin, 1976). Furthermore, its exoperine surface is regularly foveolate, with lumina c. 1.0e2.5 mm in diameter and of muri c. 3.0e5.0 mm in width, and has septate glochidia. Azolla velus (Dijkstra) Jain and Hall emend. Batten and Collinson differs from A. coloniensis by the development of a cone-shaped apex derived from the suprafilosum that obscures the floats (Batten and Collinson, 2001). The species Azolla stanleyi Jain and Hall and Azolla areolata Sweet and Hills have filaments on the columella that extend over the megaspore apparatus forming a dense apical mat, and both have more than 15 sub-rectangular,

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Azolla Species

Age

Locality

Filosum

Exoperine Surface

Number of Floats

A. anglica

Paleocene

England

Dense on floats, scarce over the megaspore

Foveolate

24

Septate, anchor-shaped tip with, recurved hooks

A. arctica

Eocene

Arctic Ocean

Dense over the entire megaspore

Rugulate, varying from punctate to fossulate

15e18

Aseptate, anchor-shaped tip without recurved flukes. Long and short

A. areolata

Paleocene-?Eocene

Canada

Dense on floats, scarce over the megaspore

Foveolate

18 (usually 24) to 27

Aseptate, anchor-shaped tip with recurved hooks

A. boliviensis

Maastrichtian-Paleocene

Bolivia

Scarce to moderate

Reticulate

30

Aseptate, anchor-shaped tip with recurved flukes

A. bulbosa

Paleocene

Canada

Dense on floats, absent over the megaspore

Rugulate to reticulate

21 (usually 24) to 27

Aseptate, anchor-shaped tip with recurved hooks

A. coloniensis

Late Cretaceous

Argentina

Scarce to moderate on floats, dense over the megaspore

Reticulate

18e21 (usually) or more

Aseptate, anchor-shaped tip with recurved hooks

A. colwellensis

Late Eocene

England

Scarce on floats, dense over the megaspore

Columnar-rugulate

18 (up to 24)

Septate, anchor-shaped tip with recurved hooks

A. distincta

Late Cretaceous and Paleocene

North America

Absent on floats, dense over the megaspore

Reticulate

>9

Aseptate, with anchor-shaped tip. Flukes with recurved hooks

A. montana

Late Cretaceous, Paleocene and Early Eocene

North America

Dense over the entire megaspore

Ruguloreticulate

15e20

Aseptate, with anchor-shaped tip. Flukes with recurved hooks

A. nuda

Eocene

Arctic Ocean

Dense over the entire megaspore

Rugulate

>9

Aseptate, anchor-shaped tip without recurved flukes

A. schopfii

Late Cretaceous and Paleocene

North America

Absent on floats, scarce over the megaspore

Reticulate

15e22

Aseptate, usually simple, spinose processes, seldom hooked

A. stanleyi

Paleocene

North America

Dense over the entire megaspore

Ruguloreticulate

18e24

Aseptate, anchor-shaped tip with recurved hooks

A. teschiana

Paleocene

Europe

Dense on floats, scarce over the megaspore

Rugulate-tuberculatefoveolate

24

Aseptate, anchor-shaped tip with recurved hooks

A. velus

Paleocene

North America

Dense over the entire megaspore

Reticulate

>9

Aseptate, with anchor-shaped tip. Flukes with recurved hooks

Glochidia

SECTION j III Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

TABLE 15.1 Azolla Fossil Species Characterized by Multifloated Megaspores and Microspore Massulae With Anchor-Shaped Glochidia Including A. coloniensis sp. nov.

Upper Cretaceous Azolla From Patagonia, Argentina Chapter j 15

rhombic, or spherical floats roughly organized in three tiers but lack deep invaginations, an obvious character of A. coloniensis (Jain and Hall, 1969; Sweet and Hills, 1976). Azolla schopfii Dijkstra emend. Batten and Collinson has a scarce filosum, so the megaspore surface is always visible (Batten and Collinson, 2001). Azolla distincta Snead resembles A. coloniensis in the dense filosum, but its floats are discoidal in all levels and the glochidia lack the distal dilation (Snead, 1969; Jain, 1971). Azolla colwellensis Collinson megaspores have a welldeveloped collar and massulae with hairs along with septate glochidia, which are completely different from the Patagonian species (Collinson, 1980). Azolla montana Hall and Swanson emend. Jain and Hall is characterized by a hollow columella, with an open pore in the top and 10e20 slightly spherical floats arranged in two or three levels, and it has four microspores massulae per microsporangia (Jain and Hall, 1969). Azolla arctica Collinson et al. and Azolla nuda Van der Burgh et al. have the megaspore apparatus completely covered by a thick mat of intertwined hairs like Azolla coloniensis, but the float system is compact and dome shaped, with discoid to spherical floats on two or three tiers (Collinson et al., 2009; Van der Burgh et al., 2013). Moreover, in A. arctica, the surface of the microspore massulae has small hairs and glochidia in two size classes (long and shorter glochidia), and like A. nuda, the flukes of the glochidia are not recurved. Azolla boliviensis has up to 30 little disc-shaped floats arranged in three tiers that are completely different from the ones so characteristic of A. coloniensis (Vajda and McLoughlin, 2005).

4.3 Taxonomy, Systematics, and Divergence Time Estimates As previously discussed, the systematics and taxonomy of Azolla are complicated and, so far, there is no consensus among researchers. Nonetheless, the two sections are well defined based on the morphology of the reproductive organs as section Azolla is characterized by megaspores with three floats and massulae with glochidia barbed at the tips and section Rhizosperma produces megaspores with nine floats and massulae without glochidia or with a few unbarbed ones (Tryon and Tryon, 1982). However, this classification allows the placement only of extant Azolla and only some of the fossil species within the two sections. Jain and Hall (1969, p. 538) erected the section Kremastospora to include species featuring “Megaspore apparatus with more than nine floats in the swimming apparatus; massulae with anchor-shape or hooked glochidia” and considered members of this section to include the fossil species Azolla teschiana, A. schopfii, A. montana, A. stanleyi, A. fragilis, A. velus, and probably A. elegans. Later, Sweet and Hills (1976) amended the original description for the section and excluded all the species

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except for A. teschiana and A. stanleyi, and the they added A. bulbosa, and A. areolata. Considering the characters observed at the new Patagonian fossil species, it is highly plausible that it could easily be placed within section Kremastospora. Regrettably, after Sweet and Hills (1976), very few researchers placed fossil Azolla spores within any section, and over the years, the use of the section Kremastospora has been abandoned in the literature. Reid et al. (2006) explored the relationships of Azolla using DNA sequence data from three noncoding regions, and Metzgar et al. (2007) analyzed molecular data from six plastid loci using penalized likelihood-Bayesian approaches. The results of both studies support the monophyly of the sections. Also, Metzgar et al. (2007) estimated a divergence time of 50.7 Ma (Early Eocene) for the split between the two sections. For calibrating their trees, they use the Santonian Azolla montana (w89 Ma; Collinson, 1991) as the fixed calibration point for constraining the Salvinia/Azolla node and A. filiculoides megaspores of Middle Miocene age (13.65 Ma; Mai, 2001) as minimum age for section Azolla. Based on this results, they concluded that diversification within Azolla began at 50.7 Ma. These results are not congruent with the fossil record. Azolla colhuehuapensis, a species that undoubtedly belongs to section Rhizosperma suggests that it was already present during the Maastrichtian; therefore, it is possible an earlier split between the two sections. The coexistence of A. coloniensis and A. boliviensis (two species with a floating apparatus with more than nine floats that cannot be placed within any formal section) and A. colhuehuapensis in South America indicates that the genus was already diverse during the Maastrichtian in the Southern Hemisphere. As previously mentioned, there are more than 70 fossil species that belong within Azolla; the majority of them are of Late Cretaceous/Paleogene in age, indicating that the genus was already highly diverse during the Early Eocene. Remarkably, it is after the Eocene that the diversity of the genus became reduced, as so many species disappeared from the record and only a few species reached Modern times. This phenomenon is observed in both hemispheres.

4.4 Paleogeographical Remarks The evolution of Salviniaceae is characterized by its sudden appearance and diversification, recognized by the record of a large variety of extinct aquatic fern genera during the Late Cretaceous (Hall, 1974; Collinson et al., 2013). In Argentina, the fossil record of megaspores related to Salviniaceae from the Upper Cretaceous include Paleoazolla patagonica Archangelsky et al., Azolla colhuehuapensis and Azolla coloniensis. In addition, dispersed microspores of Salviniaceae have a widespread distribution, including Paleoazolla patagonica, Parazolla Hall, Ariadnaesporites micromedusus Stough, Azollopsis polyancyra (Stough)

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FIGURE 15.3 Map showing the Upper Cretaceous fossil record of Salviniaceae in Argentina. Numbers: megaspores. (1) Azolla coloniensis (this report); (2) Paleoazolla patagonica (Archangelsky et al., 1999); (3) Azolla colhuehuapensis (Vallati et al., 2017). Letters: microspores. (a) Ariadnaesporites micromedusus (Vallati et al., 2016); (b) Azollopsis polyancyra (Stough, 1968; Papú, 2002; Marenssi et al., 2004); (c) Azollopsis cf. coccoides (Papú et al., 1988); (d) Paleoazolla patagonica (Puebla et al., 2014); (e) Parazolla sp. (Papú et al., 1988); (f) Azolla circinata (Puebla et al., 2014); (g) Azolla cretacea (Papú, 2002); (h) Azolla sp. (Palamarczuk and Gamerro, 1988; Papú, 1988, 1990, 2002; Papú et al., 1988; Quattrocchio et al., 2005; Vallati et al., 2017).

Sweet and Hills, Azollopsis cf. coccoides Hall emend. Sweet and Hills, Azolla circinata Oltz and Hall, Azolla cretacea Stanley, and numerous reports of Azolla sp. (Fig. 15.3). The new species is additional evidence of the widespread distribution of these aquatic ferns during the Late Cretaceous and strongly supports the hypotheses of major turnovers in water ferns across the CretaceousPaleogene transition (Hall, 1974; Collinson et al., 2013; and others). Although these hypotheses are based mainly on Northern Hemisphere records, new data from the Southern Hemisphere show that such evolutionary trends occurred simultaneously on a global scale.

4.5 Paleoenvironmental Remarks The La Colonia Formation is a geological unit deposited during the Late Cretaceous Atlantic transgression, where sedimentary deposits of coastal plains represented by estuaries, deltas, and barrier/lagoon complexes were accumulated (Malumián and Náñez, 2011). The samples studied here come from the middle levels of the unit, represented by massive (clays and silts) to finely laminated strata, probably deposited via suspension in stagnant freshwater bodies (Cúneo et al., 2014). The megaspores found in these rocks are interpreted as being preserved in situ or after minimal transport due to their excellent preservation and by

the microspore massulae frequently attached to megaspores. In addition, the presence of microspore clusters, which probably represent the whole content of one microsporangia, is another indicator of the proximity between the producing source and the deposition site, which allow estimation of the paleoenvironmental characteristics with a high degree of confidence. Modern Azolla sp. are considered to be an excellent indicator of freshwater and low-movement environments; they are frequently found in abundance floating on the surface of ponds, lakes, marshes, and slow-moving streams and less frequently in brackish water because they do not tolerate high salinity (Tryon and Tryon, 1982). Assuming that ecological requirements of the genus have changed little over time, the numerous specimens of A. coloniensis recovered from the La Colonia Formation suggest massive growth of these small floating plants in a favorable environment of calm waters. This interpretation is in agreement with previous sedimentary and paleobotanical studies from La Colonia Formation that assessed the presence of a diverse freshwater plant community. This community can be broadly divided into three groups: free-floating aquatic macrophytes that include Paleoazolla (Archangelsky et al., 1999), Azolla (this contribution), and a monocot of the family Araceae (Gallego et al., 2014); rooted macrophytes that include water ferns of the family Marsileaceae (Cúneo et al., 2013; Hermsen et al., 2013) and an eudicot of the family Nelumbonaceae (Gandolfo and Cúneo, 2005); and floating microphytes that include Botryoccoccus, Pediastrum, and Zignemataceae (Cúneo et al., 2014). Modern wetlands are characterized by water at or near the soil surface for some part of the year and plants that are adapted to living in conditions of water saturation all or part of the year (Keddy, 2010). Wetlands occupy lowlands and natural depressions, so they have a relatively high preservational potential and provide windows into ancient biodiversity (Greb et al., 2006). Based on the fossil record of La Colonia Formation, it is clear that by the Late Cretaceous there was a suite of lagoonal coastal wetlands in Patagonia that promoted the proliferation and, later, the preservation of freshwater plant communities. This type of environment is abundant in the Upper Cretaceous of the North Hemisphere, but little is known of what happened in Gondwana (see Cúneo et al., 2014; Gandolfo et al., 2014; Vallati et al., 2017). We are discovering that although the two hemispheres are well defined biogeographically, evolutionary processes occurred simultaneously on both of them. Xing et al. (2016) demonstrate that the Angiosperm Cenozoic fossil record, although extremely rich, is temporally, spatially, and phylogenetically biased. Furthermore, they proved that Northern Hemisphere is better sampled than the Southern Hemisphere. There are no doubts that these biases are extremely relevant when addressing studies focused on Cretaceous material; consequently, new collections and

Upper Cretaceous Azolla From Patagonia, Argentina Chapter j 15

studies are critical for evaluating evolutionary processes as well as the paleoenvironaments and paleocosystems in which these plants grew, diversified, and became extinct in Patagonia and the Southern Hemisphere in general.

5. CONCLUSIONS We describe a new fossil species of the heterosporous aquatic fern Azolla, A. coloniensis, from the Upper Cretaceous of the La Colonia Formation, Patagonia, Argentina. This new species is characterized by floating apparatuses that consist of more than nine floats placed in three tiers and glochidia with anchor-shaped tips. The new species is a contribution to the scarcely known record of Salviniaceae megaspores in Argentina and is further evidence of the rapid geographic dispersal and diversification of the genus during the Late Cretaceous. The extended record of microspore massulae of Salviniaceae from Argentina is indicative that wetlands environments were widely dispersed in southern regions and probably had a cosmopolitan distribution during the Late Cretaceous, when climatic conditions were propitious to the proliferation and diversification of the heterosporous water ferns. Based on this new evidence, it is clear that the relationships of extant and fossil Azolla members are in need of critical study; perhaps the evaluation of the fossil megaspores and microspores within a phylogenetic context (using a total evidence approach) will shed light on the systematics of Azolla and specially will help with the taxonomic placement of the fossil species. Although in discordance with molecular evidence, based on the fossil record it is evident that the genus Azolla was highly diverse during the Cretaceous-Eocene.

ACKNOWLEDGMENTS The authors thank the Museo Paleontológico Egidio Feruglio (MEF), and E. Ruigómez and other MEF staff for access to the fossil plant collections, P. Puerta, M. Caffa, J. Carballido, M. Delloca and C. González for fieldwork. We express our gratitude to the Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, for processing and observational facilities. To F. Tricárico, Museo Argentino de Ciencias Naturales B. Rivadavia, for technical assistance with the SEM. This work was supported by the Agencia Nacional de Promoción Científica y Tecnológica PICT 2433 to NCR, MCZ and MAG, and the National Science Foundation DEB-0345750, DEB-0918932, DEB0919071, DEB-1556136, DEB-1556666 to MAG, NRC and PW, as well as a Fulbright Fellowship to M.A.G.

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Chapter 20

Looking for Arbuscular Mycorrhizal Fungi in the Fossil Record: An Illustrated Guide Christopher Walker1, 2, Carla J. Harper4, 5, Mark C. Brundrett2, 6 and Michael Krings3, 4, 5 1

Royal Botanic Garden Edinburgh, Edinburgh, United Kingdom; 2University of Western Australia, Crawley, WA, Australia; 3Ludwig-Maximilians-

Universität München, Munich, Germany; 4SNSB-Bavarian State Collection for Palaeontology and Geology, Munich, Germany; 5University of Kansas, Lawrence, KS, United States; 6Department of Biodiversity, Conservation and Attractions, Swan Region, WA, Australia

1. INTRODUCTION It is widely accepted today that the establishment of plant life on land occurred concurrently with, and was profoundly influenced by, the evolution of mutually beneficial symbioses between the earliest plants and certain fungi (Pirozynski and Malloch, 1975; Selosse and Tacon, 1998; Brundrett, 2002; Humphreys et al., 2010; Bidartondo et al., 2011; Delaux et al., 2015). The scientifically most relevant fossil supporting this hypothesis is the arbuscular mycorrhiza (AM) occurring in the sporophytes and gametophytes of the early land plant Aglaophyton majus from the Lower Devonian Rhynie chert in northeastern Scotland (Remy et al., 1994; Taylor et al., 1995, 2005). The fungal partner (or partners), morphologically identical to some present-day members of the Glomeromycota (see Section 4.3.1), occurs in the form of extramatrical mycelium composed of mycelial bundles and hyphae. Individual hyphae enter the prostrate axes of the plant and subsequently spread out in the outer cortex. Arbuscules occur within a narrow zone of tissue between the outer and middle cortex (Taylor et al., 1995). Structures suggestive of similar associations in other Rhynie chert plants, including Rhynia gwynne-vaughanii and Nothia aphylla, have also been reported (Boullard and Lemoigne, 1971; Krings et al., 2007a,b). The morphology of the fungi involved in these fossil associations and the spatial distribution within the host plants are strikingly similar to present-day arbuscular mycorrhizal fungi (AMF). Extant AMF have been included in a single phylum, the Glomeromycota (e.g., Schüßler et al., 2001; Schüßler and Walker, 2010; Błaszkowski, 2012; Redecker et al., 2013).

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00020-6 Copyright © 2018 Elsevier Inc. All rights reserved.

However, recently it has been proposed that AMF, although having an immediate (presumably symbiotic) common ancestor, belong in two major high-level taxonomic groups, the Mucoromycotina and Glomeromycotina (Spatafora et al., 2016). The Glomeromycota contains almost all of the fungi that have been traditionally known as AMF, but one species (probably a species complex), informally known as the fine root endophyte (FRE), was placed, as Glomus tenue (formerly Rhizophagus tenuis), within this phylum. This species has now been shown, along with Endogone spp. and related organisms, to belong within the Mucoromycotina in the Mucorales and has been moved to a new genus as Planticonsortium tenue (Walker et al., 2018). As discussed in Chapter 19 in this volume, the fossil record of the glomeromycotan fungi goes back to the Early Devonian (e.g., Dotzler et al., 2006, 2009) and perhaps even earlier (Redecker et al., 2000, 2002). Molecular clock estimates, however, place the origin of the Glomeromycota perhaps in the Ediacaran or Cryogenian (600e720 Ma) (Lücking et al., 2009) or, in one estimate, as far back as the Tonian period of the Neoproterozoic (w980 Ma, see Fig. 2 in Blair, 2009; Fig. 3.1 in Taylor et al., 2015). This huge variation in estimates shows that there is still much work to be done before the evolutionary history of AMF is unraveled with confidence. The formation of mycorrhizal associations closely resembling present-day AM has variously been documented and illustrated throughout the late Palaeozoic to Cenozoic (e.g., Harper et al., 2013; Krings et al., 2011; Stockey et al., 2001; Taylor et al., 1995). Conversely, fossils of FRE are exceedingly rare (e.g., Krings et al., 2017a).

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Fossil AM and AMF have mostly been discovered by chance while examining plant morphology and internal organization. As a result, the record in general remains scanty. However, we believe that more compelling evidence of AM and AMF in fossil plants can be gathered if the paleobotanists studying structurally preserved plant remains are equipped with an accurate search image for mycorrhizal fungi and the core structural components of their associations with plants. The illustrated guide presented here provides researchers with a synopsis of important (i.e., recognizable in transmitted light) structural features of modern AMF and FRE. This is intended to facilitate the accurate identification of fossil members of this group of fungi and their discrimination from other, nonmycorrhizal fungi when examining structurally preserved plant fossils, but will also be of value for studies of modern AMF. Where available, fossil mycorrhizal fungi displaying the features included in this guide are also documented. Names of fungi follow Index Fungorum (indexfungorum.org).

2. MATERIALS USED TO ILLUSTRATE THE GUIDE There is considerable structural variability among and within mycorrhizal fungal species. All images used in this chapter to illustrate the structural characteristics show particular manifestations of these features in one species in a particular environment and host but do not necessarily reflect consistent traits that can be used to identify species with certainty. Even spore morphology and wall architecture can no longer be relied on for the identification of many extant species because organisms with very similar features may nowadays be placed in different taxa based on molecular analysis. All images of Rhynie chert fossils used in this chapter are based on material deposited in the Bayerische Staatssammlung für Paläontologie und Geologie at Munich, Germany (numbers preceded by “SNSB-BSPG”), and the Forschungsstelle für Paläobotanik am Geologisch Paläontologischen Institut, Westfälische Wilhelms-Universität, Münster, Germany (numbers preceded by “P”), except the material from Antarctica, which is deposited in the Division of Palaeobotany, University of Kansas, Lawrence, Kansas, USA (numbers preceded by “KUPB”). The images of extant fungal structures stem from the holdings of one of us (C.W.) that are now deposited at the Herbarium of the Royal Botanic Garden Edinburgh (Herbarium acronym “E”) unless otherwise noted (numbers preceded by “W”). Acquisition numbers and repository information for all figured fossils and images of extant fungi are given in Appendix I available at https://www.elsevier.com/booksand-journals/book-companion/9780128130124.

3. LIFE CYCLE OF EXTANT AMF The mycorrhiza (Fig. 20.1) develops initially from a propagule in the substrate, usually a germinating spore, but also from fragments of mycelium, or from hyphae growing from an existing mycorrhiza. As the germ tube or adventitious hypha contacts a suitable plant root, it may enter directly through a root hair, or by way of a distinct appressorium (sometimes known as a hyphopodium) (Fig. 20.2AeD [black arrows]) from which the fungus penetrates the plant surface (epidermis), often forming a distinct coil (Fig. 20.2C [white arrows]) before continuing growth through the cortical cells. Penetration of the cell walls is followed by hyphal growth within (intracellular) or between (intercellular) the cells of the root cortex, with the generation of repeatedly fine tree-like branching to form intracellular arbuscules, which invaginate the plasmalemma and provide a large surface area of contact between host and fungus where nutrient exchange takes place (e.g., Peterson and Massicotte, 2004; Parniske, 2008). Arbuscules, which are short-lived (i.e., 2e3 days, up to 1 week; see Tinker, 1975; Cox and Tinker, 1976), degrade and thus can be found in various stages of development and senescence within a single root (see also Chapter 19). The life cycle continues with the production of spores (Fig. 20.1). Depending on species, these spores may be entirely extraradical (outside the root) or both intraradical (i.e., within the root) and extraradical (Fig. 20.3E). For plants lacking roots (e.g., the Early Devonian Rhynie chert plants; see later), the terms “intramatrical” and “extramatrical” should be used instead. The spores are predominantly hypogeous and may be produced singly, or loosely associated in clusters, or in dense clusters or sporocarps containing many hundreds of spores. Some sporocarps or spore masses may be produced epigeously on the substrate surface or attached to above ground organic debris or plant stems. Whereas the arbuscules and hyphal coils are produced entirely within the host, the spores, therefore, must be sought in both the host and the surrounding substrate. Mycorrhizas of this sort can be visualized by clearing the fine roots with hot KOH followed by acidification and staining with an appropriate dye (often trypan blue or methyl blue; see Brundrett et al., 1984, 1996). The colonization density can be very variable, from almost every cortical cell containing fungus to occasional small colonies of fungus occupying just a few cells (Fig. 20.3).

4. STRUCTURAL CHARACTERISTICS OF AMF AMF have traditionally been defined and distinguished from one another based on features of the spore wall and mode of spore formation (Walker, 1983; Morton, 1988).

extraradical mycelium

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pericycle FIGURE 20.1 Overview of structural features and spatial distribution of arbuscular mycorrhiza within a plant rootlet. Note that not all fungal features compiled in this chart necessarily occur within a single rootlet. Modified from Walker (2013). Image © Christopher Walker.

FIGURE 20.2 Appressoria. (A) Longitudinal view of appressorium (black arrow). (B) Appressorium (black arrow) produced from extraradical hypha (white arrow). (C) Appressorium (black arrow) forming coiled hyphae (white arrows) in root cortex. (D) Planar view of appressorium (black arrow). Images © Christopher Walker.

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FIGURE 20.3 Root colonization of arbuscular mycorrhizal fungi in. (A) Uncolonized root (white arrow) and colonized root (black arrow). (B) Isolated colony in root (arrow). (C) Heavily colonized root with extramatrical hyphae. (D) Multiple arbuscules in colonized infected root. (E) Intraradical and extraradical spore formation. Images © Christopher Walker.

More recently, however, the use of molecular markers has become increasingly important in the characterization of AMF (Krüger et al., 2012). AMF are morphologically characterized by coenocytic (aseptate) mycelia, the production of specialized coils or arbuscules that represent the plantefungus interfaces and are highly effective in nutrient exchange, and asexual reproduction through mycelium fragmentation and chlamydospore production (Redecker and Raab, 2006; Schüßler and Walker, 2011). An additional distinctive morphological feature seen in some AMF is the production of thin-walled, sac-like vesicles, which are storage organs produced by the fungus within the host roots.

4.1 Arbuscules and Hyphal Coils The defining structure of AMF, the arbuscule (Figs. 20.4, 20.5, and 20.6AeB), seems to be unique to mycorrhizal fungi. Although some efforts have been made to distinguish different groupings of arbuscular morphology (Abbott, 1982; Daft and Nicolson, 1974; Thippayarugs et al., 1999), there is as yet no clear evidence that even the glomeromycotan (Fig. 20.5) and mucoromycotan (Fig. 20.6A and B) groups can be separated with much certainty by arbuscules alone. Within the Glomeromycota, early descriptive studies on mycorrhizas placed them into two broad morphological categories: Arum-type (finely branched arbuscules) and

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FIGURE 20.4 Inverted transmitted light image of Acaulospora sp. branching arbuscules within cells of the host plant (Mirbelia dilatata). Image © Christopher Walker.

Paris-type (coarse coil arbuscules) (Gallaud, 1904, 1905; Dickson, 2004). Today we know that there is an entire continuum of morphologies between these two extremes (see Fig. 1 in Dickson, 2004); moreover, an individual fungus can produce both morphologies (Kubota et al., 2005), depending on the environment or the host, or both (Dickson et al., 2007, Fig. 2). While the presence of arbuscules is usually a reliable indicator of mycorrhiza, arbuscule morphology cannot be used to assess systematic affinities. There is a major difference in arbuscule morphology between some AM genera, but is beyond scope of this chapter since they will likely not be well enough preserved. Nevertheless, some arbuscules, for example, are much coarser than others. On entry to the root, glomeromycotan fungi usually produce a hyphal coil (Fig. 20.7) before further ramifying through the cortex and forming arbuscules either in an adjacent cell (Fig. 20.4) or directly from the ramifying intercellular hyphae (Fig. 20.5A). Coarse hyphal coils (Fig. 20.7) and arbuscules together (Fig. 20.4) would be confirmational for a glomeromycotan fungus, whereas the very fine arbuscules found in many mycorrhizas are presently indistinguishable and thus cannot be used to separate different phylogenetic groups, even at the level of species. Hyphal coils can also be found among FRE, but they are finer and more angular than the coarse AMF and often have intercalary or branching swellings (Fig. 20.6C and D). Permineralized fossil arbuscules and arbuscule-like structures have been described, among others, from the Lower Devonian Rhynie chert (Taylor et al., 1995, 2005), the Carboniferous of Great

Britain (Strullu-Derrien et al., 2009; Krings et al., 2011), the Permian and Triassic of Antarctica (Stubblefield et al., 1987a,b; Phipps and Taylor, 1996; Schwendemann et al., 2011; Harper et al., 2013, 2015), and the Eocene Princeton chert from Canada (Stockey et al., 2001) (see also Chapter 19). To date, compelling fossils of hyphal coils (Fig. 20.7A and B) are known mainly from the Permian (Harper et al., 2013) and Triassic (Phipps and Taylor, 1996) but have not yet been conclusively demonstrated in geologically older fossils, with one possible exception from the Rhynie chert (Kidston and Lang, 1921, Plate 3, Fig. 28) (Fig. 20.8). The intracellular, coil-like structures mentioned in StrulluDerrien et al. (2014, see double arrowhead in Fig. 1F) remain inconclusive.

4.2 Vesicles Some AMF form thin-walled, sac-like structures in the host roots (Fig. 20.9AeD). These are considered to act as temporary storage organs, mainly for polyphosphates (Gerdemann, 1968). There is, however, a great deal of confusion in the matter of distinguishing vesicles from intraradical spores (Gerdemann, 1968). Some glomeromycotan groups (e.g., Gigasporaceae) do not form vesicles at all (at least none has ever been described). Others such as Acaulospora spp. do not form spores in roots, and therefore any intraradical sac-like structures formed by these organisms can be considered to be vesicles (Fig. 20.9C and D). On the other hand, many species with

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FIGURE 20.5 Diversity in arbuscule morphology of glomeromycotan fungi (black arrows ¼ attachment to trunk hypha). (A) Multiple arbuscules attached to trunk hypha. (B and C) Arbuscule of Glomus sp. (D) Rhizophagus sp. arbuscule in Plantago lanceolata. (E) Sclerocystis pubescens arbuscule. (F) Degraded arbuscules. Images © Christopher Walker.

glomoid spores apparently can form both vesicles and intraradical spores, but, in such organisms, it is difficult or impossible to know if the structures considered as vesicles are indeed anything other than the early stages of spore formation (see later) and therefore of a quite different function from true vesicles. Vesicles are thin-walled and balloon-like (Fig. 20.9A, C, and D) and lack occlusion, so any such structures with wall thickening or occlusion of the subtending hypha should probably be considered to be spores (Fig. 20.9B).

4.3 Spore Morphology, Development, and Germination The members of the Glomeromycota produce large, often thick-walled spores (Figs. 20.10 and 20.11), usually in the soil, but also sometimes in the host roots or even in rhizomes. Although some species have spores as small as 20e50 mm, most are much bigger (normally 100e300 mm), but up to about 1 mm in diameter (INVAM, 2018). Although many spores are of a relatively smooth outline (globose,

FIGURE 20.6 Arbuscules and hyphal coils of Planticonsortium tenue (Mucoromycota). (A and B) Finely branched arbuscules. (C) Tightly looped hyphal coil (arrows); note intercalary hyphal swellings. Vesicles (V). (D) Loose hyphal coil (arrows). Images © Christopher Walker.

FIGURE 20.7 Fossil and extant hyphal coils. (A) Permian coiled mycorrhiza from Antarctica. (B) Single coil from the Triassic of Antarctica. (CeE) Coils of extant fungi. (C) Glomus cf. majewskii. (D) Diversispora sp. (E) Cetraspora gilmorei. Figs. 20.7CeE images © Christopher Walker.

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FIGURE 20.8 Hyphal coil (arrows) with intracellular spore (originally marked vesicle [V]) from the Rhynie chert. Modified from Kidston and Lang (1921, Plate 3, Fig. 28).

FIGURE 20.9 Vesicles and intraradical spores. (A) Thin walled vesicle or immature spore (V) of Rhizophagus intraradices. (B) Thick walled intraradical spores (S) of Rhizophagus intraradices. (C) Intraradical sac-like structure or vesicle (V) of Acaulospora longula. (D) Vesicle (V) of Ambispora fennica. Images © Christopher Walker.

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FIGURE 20.10 Some of the diversity of glomeromycotan spores. (AeC) Diversipora sp. (D) Septoglomus sp. (E and F) Glomus mortonii. (G and H) Rhizophagus intraradices. (I and J) Claroideoglomus etunicatum. (K) Glomus macrocarpum. (L and M) Rhizophagus sp. (N and O) Sclerocystis pubescens. (P) Scutellospora calospora. (Q and R) Septoglomus constrictum. (S and T) Paraglomus occultum. (U) Scutellospora sp. (V) Dentiscutata erythropus. (W) Rhizophagus cf. aggregatus. (X) Rhizophagus intraradices. (Y) Redeckera pulvinatum. (Z) Glomus botryoides. (AA) Claroideoglomus claroideum. (AB) Funneliformis coronatum. (AC) Dentiscutata cerradensis. (AD) Acaulospora laevis. (AE) Acaulospora foveata. (AF) Acaulospora delicata. (AG) Dentiscutata erythropus. (AH) Dentiscutata heterogama. (AI) Scutellospora weresubiae. (AJ) Dentiscutata nigra. Images © Christopher Walker.

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FIGURE 20.11 Spore shapes of Rhizophagus cf. aggregatus. (A) Smooth subglobose spore. (B) An obovoid spore with several irregularly shaped spores. Images © Christopher Walker.

FIGURE 20.12 Typical glomoid spores (A) Pigmented spore of Funneliformis geosporum. (B) Colorless spore of Paraglomus brasilianum. Images © Christopher Walker.

sub-globose, ellipsoid, ovoid, obovoid) (Fig. 20.11A), they can develop remarkable shapes (Figs. 20.10L,M,W,X and 20.11B). This, however, is not a characteristic of any particular species or genus, despite one species (Rhizophagus irregularis) being named because of this feature. Irregularly shaped spores can be found in Archaeospora, Glomus, Rhizophagus, Dentiscutata, among other taxa, and probably in just about any AMF species. It is not known what stimulates spores to become misshapen. Even in a single-spore isolate both smooth and irregular spores can be produced within a root or in a pot culture with a single host plant (Fig. 20.11).

4.3.1 Glomoid Spores The name of this kind of spore (Fig. 20.12) comes from the defining genus of the Glomeromycota, Glomus. The spore type is basically a chlamydospore formed by terminal (often described as blastic) or intercalary inflation of a

hypha, which is followed by wall thickening. Such spores may be with or without some kind of occlusion by thickening of the subtending hypha, septum formation or some kind of plug. Glomoid spores are often large (100e>500 mm in diameter; see INVAM, 2018) and may possess persistent, colored walls. Some of the large, darkly colored spores (Fig. 20.12A) can persist in the soil after death for many years. Most large, spheroidal or ovoid fungal spores subtended by a hypha that are encountered in the fossil record (e.g., Kidston and Lang, 1921; Stubblefield and Banks, 1983; Stubblefield et al., 1985; Krings et al., 2009; Harper et al., 2015; Slater et al., 2015) are likely to represent glomoid spores produced by some member in the Glomeromycota (or at least, their progenitors). The structure marked (V) as a vesicle in Fig. 20.8 is thus probably an intracellular spore. Relatively small glomoid spores, which may lack pigmentation (Fig. 20.12B), characterize other species in the Glomeromycota, and these are more difficult to detect

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FIGURE 20.13 Comparison of a fossil spore with an extant Rhizophagus intraradices spore. (A) Elongate fossil spore from Rhynie chert (From Taylor et al., 1995, Fig. 16). (B) Corresponding line drawing for Fig. 13A; light blue ¼ lumen of spore and hypha, dark blue ¼ thick outer spore wall continuous with hyphal wall. (C) Rhizophagus intraradices elongated spore. (D) Corresponding line drawing for Fig. 20.13C; light blue ¼ lumen of spore and hypha, dark blue ¼ thick outer spore wall continuous with hyphal wall. Fig. 20.13C image © Christopher Walker.

in substrates. Such colorless spores seem to decay more quickly than the pigmented species (Fig. 20.12A). While glomoid spores usually are spheroidal or ovoid, unusually shaped spores also occur in many extant species. Similar unusually shaped spores have also been documented from the fossil record. For example, certain spores from the Rhynie chert are remarkably similar to those found in the present-day genera Glomus and Rhizophagus. Comparative images along with outline cartoons show two of these striking morphological similarities in shape and wall structure in Rhizophagus intraradices (Fig. 20.13AeD) and Glomus macrocarpum (Fig. 20.14AeD). Glomoid spores can be found singly (Fig. 20.12A and B), in clusters ranging from a few spores in loose clusters (Fig. 20.15A and B) to many spores in dense clusters that often are called sporocarps (Fig. 20.15C and D). These sporocarps may be naked or may be sheathed in a peridium that can vary from vestigial to complete. Some species, such as Funneliformis mosseae (Fig. 20.15E) form their spores both singly and in small sporocarps. In some genera (particularly Rhizophagus), spores may be formed within the root tissue (Figs. 20.3E and 20.15F), probably maturing as the roots senesce and being released into the substrate as the cortical cells decay. The genus Sclerocystis (Figs. 20.16 and 20.17) contains species that produce a particular type of sporocarp in which glomoid spores are arranged concentrically around a sterile central plexus. Some of these, such as Sclerocystis

rubiformis, lack any outer covering (peridium) and are little more than globose clusters of radiating spores (Fig. 20.16A and B) that appear more or less the same whichever way they are sectioned, but others may have a completely differentiated peridium (Figs. 20.16C and 20.17). Sclerocystis sinuosa (Fig. 20.16C) and S. dussii, the type species of the genus (Fig. 20.17), are good examples of the latter. In S. dussii, the sporocarps have a bilateral symmetry and because of this, horizontal and vertical sections have different appearances (Fig. 20.17). It is thus important, when examining fossilized specimens, that their orientation is known (Fig. 20.18). Moreover, glomoid spores are a common feature in the Rhynie cherts either as isolated structure within the matrix or in intact or degraded plant tissue; however, evidence of attachment to a central plexus is rare (Fig. 20.19). Even for those with experience, it is very difficult to identify, even to genus, large glomoid spores, due to the fact that such large spores are commonly found not only in the Glomerales and Diversisporales but also in the Archaeosporales This last order contains two genera with glomoid spores, one of which, Geosiphon (Fig. 20.20A), is not known to be mycorrhizal but is symbiotic in an endocytobiotic association with a cyanobacterium (Schüßler et al., 1994; Gehrig et al., 1996; Schüßler, 2002). In addition, at least one species of non-AMF, Mortierella ambigua in the Mucorales (Fig. 20.20B), produces glomoid spores similar to those seen in certain species in the

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FIGURE 20.14 Comparison of a fossil spore with an extant Glomus macrocarpum spore. (A) Irregularly shaped spore from Rhynie chert (From Taylor et al., 1995, Fig. 17) and (B) Corresponding line drawing. (C) Irregularly shaped Glomus macrocarpum spore and (D) Corresponding line drawing. Fig. 20.14B image © Christopher Walker.

Glomeraceae (Ansell, 1983), and an ascomycete chlamydospore (Complexipes moniliformis) was erroneously described as a highly ornamented likely member of the then Endogonaceae because of its glomoid “characteristic” form (Walker, 1979).

4.3.2 Gigasporoid Spores Two other kinds of spore (Fig. 20.21), represented by Gigaspora (gigasporoid) (Fig. 20.21A) and Scutellospora (scutellosporoid) (Fig. 20.21B), are formed initially from a small bulb from which it expands to form a large propagule. Spores with small bulbs on the subtending hyphae can also be seen in the Rhynie chert (Fig. 20.22A and B). In modern fungi, these can be recognized easily most of the time but can be less than “textbook” examples, and in some cases, the bulbous base can fail to complete, in which case the spores appear to be glomoid. The gigasporoid spore has a single structural wall, through which it germinates directly (Sward, 1981) On the other hand, the

scutellosporoid spore (possibly a highly modified sporangium) is initially similarly simple, but subsequently develops flexible inner wall components and germinates through a complex structure known as a germination shield (Walker and Sanders, 1986; see Section 4.3.4 later). These spore types are not normally found in clusters, though several may occupy empty nematode cysts, exuvia, or dead bodies of soil arthropods such as mites (e.g., Benny et al., 2016).

4.3.3 Acaulosporoid Spores A third major morphological grouping of spores form in quite a different way (Fig. 20.23). At first, a blastic saccule forms at the end of a hypha (Fig. 20.23AeE). Within this saccule, a robust, thick-walled propagule is formed either laterally (Fig. 20.23A) or terminally (Fig. 20.23B). Eventually, the propagule becomes detached (Fig. 20.23FeI) and more often than not, because they are quite delicate, little or no trace of the saccule remains except often as an

FIGURE 20.15 Arrangement of glomoid spores. (A) Glomus deserticola loose cluster of two spores. (B) Loose spore cluster of Rhizophagus cf. aggregatus spores. (C) Sporocarpic spores of Glomus macrocarpum. (D) Dense spore cluster of Diversispora epigaea lacking a peridium. (E) Funneliformis mossaea spores produced ectocarpically and in sporocarps with one to a few spores. (F) Intraradical spores of Rhizophagus intraradices. Images © Christopher Walker.

FIGURE 20.16 Sporocarps of Sclerocystis sp. (A) Sclerocystis rubiformis and (B) Sclerocystis sp. with no peridium but with a cluster of radiating spores around central plexus. (C) Sclerocystis sinuosa with a thin, differentiated peridium of sinuous hyphae. Images © Christopher Walker.

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FIGURE 20.17 Sclerocystis dussii sporocarps in different planes. (A) Longitudinal section. (B) Surface view (left) and transverse section (right). (C) Tangential section showing peridial hyphae. Images © Christopher Walker.

FIGURE 20.18 (AeF) Different focal planes of unnamed Rhynie chert sporocarpic fungus similar to a Sclerocystis sp.

apparent wall component surrounding the spore (Dalpé and Declerck, 2002). As with the scutellosporoid and gigasporoid spores, acaulosporoid spores do not normally form in clusters. There are currently six named genera (Acaulospora, Ambispora, Archaeospora, Entrophospora, Sacculospora and Otospora) that produce spores of this type, though perhaps some of these will be combined eventually. As with the glomoid spore-forming groups, although they all develop similarly, acaulosporoid spore-forming taxa are found among widely separated phylogenetic clades (Redecker and Raab, 2006; Krüger et al., 2011). One additional organism, named Sacculospora baltica, apparently also forms spores in a saccule (Fig. 20.23J), and thus

was originally placed in Entrophospora. It seems also to have been named Peridiospora tatachia in the Endogonales (Wu and Lin, 1997), indicating an element of confusion brought about by purely morphological taxonomic study. However, from the protologues of these two taxon names, the development from a saccule is not clearly evident. Some of these differently named genera are difficult or impossible to distinguish based on morphological evidence alone. Acaulosporoid spores have been found in the Rhynie chert (Figs. 20.24A,B and 20.25), including superbly preserved examples still attached to their saccules (Fig. 20.24A) (Dotzler et al., 2009). At the time of that publication, the

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FIGURE 20.19 Fossil glomoid spores surrounding a central plexus corresponding with a present day Sclerocystis sp. (A) Globose cluster of radiating spores around a central plexus (P). (B) Irregularly shaped spores surrounding a central plexus (P). (C) Higher magnification of plexus (black arrow) attached to globose spores (white arrows). (D) Four spores attached (white arrows) to a central plexus (black arrow).

FIGURE 20.20 Non-arbuscular fungi that form spores similar to those of some arbuscular mycorrhizal fungi. (A) Geosiphon pyriforme. (B) Mortierella ambigua. Images © Christopher Walker.

authors were unable to be sure about the relationship of these fossils with present-day species, but now it can be said that they fit well with the genus Ambispora. One characteristic of the genus Ambispora is the production of acaulosporoid spores and large glomoid spores, often 100 mm or larger (Walker et al., 2007), that resemble species

from the Glomeraceae (Figs. 20.24C,F and 20.25B,E). At least one species of Acaulospora also produces glomoid spores (Taylor et al., 2014), though these are very small (4e5 mm). The methods currently used for spore extraction from soils or similar substrates usually cause the two different kinds of spores to separate, but occasionally

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FIGURE 20.21 Gigasporoid spores. (A) Gigaspora candida with bulbous base (arrow) and simple wall structure. (B) Scutellospora calospora with bulbous base (arrow), complex wall structure and germination shield (upper left). Images © Christopher Walker.

they can be found still attached to each other. One prepared thin section of Rhynie chert shows spores that can be attributed to Ambispora, with glomoid spores in close proximity (Fig. 20.25AeE). Although it seems likely that these two types of spore belong to the same organism, it is impossible to be certain because they are not attached by shared hyphae.

4.3.4 Spore Germination

FIGURE 20.22 Rhynie chert spores with bulbous bases (arrows). (A) Tiny spore with bulbous base. (B) Tangential-planar view of bulbous base.

Many of the glomoid spores germinate simply by regrowth through the original subtending hypha (Fig. 20.26A and B), although at least one species, Claroideoglomus claroideum, may also germinate, after forming a thin-walled “endospore” (Walker and Vertberg, 1998), via direct regrowth of several germ tubes directly through the spore wall (Fig. 20.26E). In contrast, germination in many members of the Diversisporales is preceded by the production of a varyingly complex structure known as a germination shield (Walker and Sanders, 1986). Such structures are particularly evident in members of the Gigasporaceae (Fig. 20.27), although members of one genus therein, Gigaspora, lack complex inner wall components and germinate directly through the spore wall (Fig. 20.26C). The simple, coiled germination shield of the Rhynie chert fossil Scutellosporites devonicus shown in lateral view in Fig. 20.28A is probably similar to those found in present-day Acaulospora longula (Fig. 20.28B) and Scutellospora projecturata (Kramadibrata, 2000). This corresponds with the least complex morphology in the increasing complexity of such pregermination structures, culminating in very complex, much invaginated forms (Fig. 20.27D) (e.g., those of Dentiscutata spp.; see Oehl

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FIGURE 20.23 Acaulosporoid spores showing diversity of saccules and spores. See text for details. (A) Archaeospora trappei. (B) Entrophospora sp. (C) Acaulospora brasiliensis. (D) Ambispora fennica. (E) Otospora bareae. (F) Archaeospora trappei. (G) Entrophospora sp. (H) Acaulospora sp. (I) Ambispora leptoticha. (J) Peridiospora tatachia/Sacculospora baltica (?). Images © Christopher Walker.

et al., 2009, Figs. 38e44). The germination shields of the Ambispora-like Rhynie chert fossils (Fig. 20.28C and D) described by Dotzler et al. (2009) are remarkably similar to those of present-day Ambispora appendicula (Fig. 20.28E; see Spain et al., 2006).

4.4 Auxiliary Cells Accompanying the gigasporoid and scutellosporoid spores are so-called auxiliary cells (Fig. 20.29). These are usually clusters of small (w10e20 mm), spiny (Fig. 20.29A), knobbed (Fig. 20.29B) or smooth (Fig. 20.29C and D) structures of unknown function. Both gigasporoid and scutellosporoid spores can be associated with smooth auxiliary cells, which, when found singly, rather than in clusters, can be confused for small glomoid spores (Fig. 20.29C), and, when in clusters around a central “core” of mycelium (Fig. 20.29D), can superficially appear to be sporocarps of the glomoid spore-forming members attributed to Sclerocystis (see earlier).

4.5 Spore Wall The wall structure of spores is used widely as a diagnostic feature in the morphological taxonomy of the Glomeromycota

(e.g., Walker, 1983). Although it is also possible to compare the structure of fossil spores with recent species descriptions, it must be borne in mind that most current work on extant taxa is carried out with unfixed spores mounted on microscope slides in polyvinyl-alcohol-lactoglycerol (PVLG), which in itself can modify characters of the spore. Wall structures that vary from very simple, with a structure reflecting that of the spore-bearing hyphae, to highly complex with many components in several groups have taxonomic value, depending on the taxon (Fig. 20.30). Variation in the complexity and structure of spore wall can also be seen in Rhynie chert fossil (Fig. 20.31). However, some of the characters used for morphological comparisons are actually artifacts of this mounting method. One such feature, the so-called amorphous wall component (Morton, 1986), is in nature thin and flexible, usually 100 individuals of an unusual, long-stalked microorganism. The slide belongs to a series of 50 thin sections prepared of an aquatic facies of the Windyfield chert that is dominated by Croftalania venusta-dominated microbial mats. It was analyzed by using normal transmitted light microscopy; digital images were captured with a Leica DFC-480 camera and processed in Adobe Photoshop.

3. RESULTS The charophyte branch portion (likely of Palaeonitella cranii [Kidston et W.H. Lang] J. Pia; see Kelman et al., 2004) carrying the microorganisms is c. 550 mm long and up to w50 mm wide (denoted “ch” in Fig. 21.1A). It is located within a well-preserved microbial mat dominated by interlaced filaments of the cyanobacterium Croftalania venusta Krings et al. (2007). Within the mat framework, the host branch co-occurs with numerous other charophyte branches and branch portions, fungal hyphae and reproductive units, peronosporomycetes, other cyanobacteria and microscopic eukaryotic algae, as well as scattered land plant spores. The microbial overgrowth consists of a stand of >100 intact individuals, occupying an area of 150  w80 mm of the branch surface (Figs. 21.1A and 21.3). Microorganisms are densely spaced (with, on average, 1 mm long (Curds et al., 1983; Warren, 1986, 1987). Zooids vary in size (up to 160 mm long) and shape from spherical, cylindrical or cone shaped to inverted bell shaped, with a peristome (feeding apparatus) bearing oral cilia. Unfortunately, the fossils do not reveal any identifiable details of the internal organization. However, what appears to be an apical opening in several specimens might represent the epistomial disc surrounded by the retracted peristome. Moreover, several Vorticella and Pseudovorticella spp. are characterized by zooids covered in small

granules (e.g., Ji et al., 2005, 2006), and small granules occur also in many of the fossils; however, the occurrence of granules in the latter appears to be restricted to the apical rim of the cell. The stalks of Vorticella and Pseudovorticella contain a contractile myoneme (spasmoneme) that causes spiral contraction (Misra et al., 2010). The fossil stalks do not provide evidence of contraction in a spiral fashion. Rather, several specimens are bent or irregularly curved, which might be a preservation artefact but could as well be suggestive of stalk contraction in a zigzag fashion. The latter is known to occur in the extant ciliophore family Zoothamniidae (Lynn, 2010). For example, members in the genus Haplocaulus Precht are characterized by solitary, oval, cylindrical, or inverted bell-shaped zooids borne on stalks that may be as long as the zooid and, when contracted, are thrown into a zigzag fashion (Warren, 1988; Foissner and Brozek, 1996). Arguing against affinities to the Vorticellidae or Zoothamniidae is perhaps the diminutive size of the fossils (total length up to 30 mm), together with the presence of a prominent, gradually tapering neck region in many specimens. This feature is reminiscent of morphologies seen in Stentoridae (Heterotrichida) (Fig. 21.2F), rather than Vorticellidae and Zoothamniidae. However, members in the Stentoridae are distinctly larger (up to 4 mm) than the fossils (Johnson, 1893; Thamm et al., 2010).

4.2 Preservation in a Conservation Trap Long-stalked microorganisms attached to a substrate are virtually absent from the fossil record, with one or two notable exceptions. One of these exceptions is a single, Vorticella-like fossil that occurs as an inclusion within the wall of a Triassic leech cocoon from Antarctica (Bomfleur et al., 2012). Because other microinclusions (e.g., bacteria,

Exceptional Preservation of Sessile, Long-Stalked Microorganisms Chapter j 21

FIGURE 21.3 Long-stalked microorganisms from the Lower Devonian Windyfield chert. Graphic depiction of portion of host with overgrowth, slightly simplified to emphasize morphological variability of microorganism cell size and shape.

nematodes, spermatozoa) have also been found within the walls of fossil leech and clittelate cocoons (Manum et al., 1994; Bomfleur et al., 2012, 2015; McLoughlin et al., 2016), Bomfleur et al. (2012) have referred to these structures as microscopic conservation traps and inferred that such traps represent important sources of new information on the evolutionary history of lineages of organisms that do not normally lend themselves to preservation (in recognizable form). Another type of microscopic conservation trap yielding exceptional insights into ancient microbial life is amber (e.g., Schönborn et al., 1999; Martín-González et al., 2009; Girard et al., 2008; but see also Girard et al., 2011; Thiel et al., 2016). Preservation in amber and cocoon walls requires rapid inclusion in, and subsequent hardening of, a surrounding matrix (“embedding medium”); it typically yields single specimens or small numbers of individuals, while large sample sets are exceedingly rare. The fossil overgrowth on a charophyte branch from the Windyfield chert described in this study is remarkable because it consists of >100 intact individuals of a longstalked microorganism (Fig. 21.3). We have not previously discovered specimens of this microorganism during our longstanding, intensive work with several thousand thin sections representing a wide range of different (micro-) facies of the Rhynie and Windyfield cherts. We rule out the possibility that they have simply been overlooked because we always screen our slides carefully and at high magnification. The most plausible explanation for this scarcity of evidence is therefore that a very special microenvironmental setting was imperative for the delicate organisms to become preserved intact. The stalk is the most important feature through which this microorganism in fossil state becomes recognizable as a distinctive life form. If the cell were broken off and dislodged from the stalk, there would be no way to realize the true nature of the organism, even if both stalk and cell were preserved in pristine conditions. However, the stalk most certainly was susceptible to destructive mechanical forces such as water movement and

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thus rendered intact preservation of the organism unlikely. This raises the question, what made it possible that so many individuals became preserved in near-perfect condition in the Windyfield chert? The host charophyte branch occurs within a microbial mat framework constructed of tightly interlaced, long filaments of the cyanobacterium Croftalania venusta (Krings et al., 2007). However, C. venusta microbial mats are not monotypic, but rather represent assemblages comprised of different filamentous and coccoid cyanobacteria, fungi, algae, and peronosporomycetes (Krings et al., 2007, 2012, 2013; Krings and Taylor, 2015; Taylor and Krings, 2015); they also appear to have played an important role in land plant spore germination and gametophyte development (Taylor et al., 2005). We are unable to determine how the numerous charophyte branches and branch fragments, including the one colonized by the microorganisms, became entangled in the meshwork of cyanobacterial filaments, but suggest they might have been washed onto the mat surface and subsequently became engulfed by the filaments. Alternatively, they might represent parts of charophyte plants that became suffused in vivo by the microbial mat and subsequently disarticulated. Irrespective of how the branch portion carrying the microorganisms became embedded in the microbial mat, we hypothesize that, once surrounded by the mat framework, the interlaced cyanobacterial filaments, perhaps along with cyanobacterial extracellular polymeric substances forming a confluent, stabilizing matrix throughout the mat (e.g., Flemming and Wingender, 2001, 2010; Rossi and De Philippis, 2015), had a cushioning effect on destructive mechanical forces, and hence provided ideal conditions for the fragile microbial overgrowth to become preserved intact. Moreover, the cyanobacteria might also have excreted substances with biocidal properties that slowed down biological decomposition (e.g., Carmichael, 1992; Volk and Furkert, 2006). If these hypotheses are correct, then microbial mat frameworks in the Rhynie and Windyfield settings were effective as microscopic conservation traps but in a different way than amber and annelid cocoon wallsdnamely by prolonging the time for the microorganisms to become silicified intact, rather than by providing a special “embedding medium” that entraps and subsequently preserves the organisms.

5. CONCLUSIONS Discovery of a stand of long-stalked microorganisms on a charophyte branch from the Windyfield chert offers insights into the morphological diversity of Early Devonian soft-bodied microorganisms, and indicates that microbial mat frameworks can function as microscopic conservation traps in settings such as the Rhynie and Windyfield paleoenvironments. Although we are unable to determine

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the systematic affinities of the microorganisms, we believe it is worthwhile to document them because they can be used to measure past microbial biodiversity based on morphological distinctiveness. The inventory of distinctive morphologies provides the only access and thus is critical to subsequent studies assessing the function(s) of these organisms as integral parts of ancient ecosystems. We anticipate that, as research with the Rhynie and Windyfield cherts continues and increased attention is directed at microbial remains embedded within microbial mat frameworks, additional delicate fossils will be discovered that offer glimpses of a segment of ancient life with next to no fossil record from elsewhere.

ACKNOWLEDGMENTS Funds were provided by the National Science Foundation (EAR0949947), the Deutsche Forschungsgemeinschaft (KE 584/13-2), and the Alexander von Humboldt-Foundation (3.1-USA/1160852 STP). We are indebted to Nora Dotzler, Helmut Martin, and Stefan Sónyi (all Munich, Germany) for technical assistance and insightful comments on the manuscript.

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Chapter 22

Morphological Convergence in Forest Microfungi Provides a Proxy for Paleogene Forest Structure Jouko Rikkinen1 and Alexander R. Schmidt2 1

Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland; 2Geoscience Centre, University of Göttingen, Göttingen, Germany

1. INTRODUCTION Amber, fossilized plant resin from gymnosperms and angiosperms, is renowned for preserving a wide range of organisms in microscopic fidelity. These so-called amber inclusions comprise many groups of organisms, ranging from bacteria to arthropods and vertebrates (Penney, 2010; Ragazzi and Schmidt, 2011; Grimaldi and Ross, 2017). Organisms trapped in amber typically derive from forest ecosystems where they became stuck to resin outpourings in their habitats (Seyfullah and Schmidt, 2015). In addition, ambers are prime examples of chemical fossils that are relatively resistant to diagenesis and can retain their original chemical and isotopic compositions. Therefore, chemical profiles of ambers may support the detection of the resin-bearing plants and the reconstruction of the paleoenvironment and paleoclimate (Langenheim, 2003; Dal Corso et al., 2017). The study of amber and its inclusions should consequently enable the reconstruction of past forest ecosystems and even prevailing climatic conditions. However, several constraints exist for this approach. Much amber from the hundreds of worldwide localities does not contain notable inclusions or predominantly preserved arthropods, prokaryotes, and fungal mycelia (Martınez-Delclòs et al., 2004; Labandeira, 2014). Arthropods are indeed the most commonly studied amber inclusions, whereas fossil plant remains and palynomorphs, on which reconstructions of Cenozoic forests and derived climate estimates are typically based on (Ferguson et al., 1998; Bruch and Mosbrugger, 2002; Kunzmann and Walther, 2012), are relatively rare in amber. Only six worldwide amber deposits harbor plenty of plant inclusions, so far: Miocene Dominican and Mexican ambers,

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00022-X Copyright © 2018 Elsevier Inc. All rights reserved.

Paleogene Baltic, Bitterfeld, and Rovno ambers, and mid-Cretaceous Burmese amber (Penney, 2010). Further hurdles are linked to the physical properties of amber. Once reworked from the original sediment, amber may float or drift in sea water, and the notion exists that even amber specimens forming large deposits may have been reworked and transported, originally belonging to older and possibly geographically distinct sediments (Weitschat and Wichard, 2010). Baltic and Bitterfeld ambers constitute the largest Paleogene amber deposits worldwide, with estimated 640,000 tons of fossil resin for the Baltic deposit (Weitschat and Wichard, 2010) and approximately 3000 tons for the central German Bitterfeld locality (Liehmann, 2013). Hundreds of thousands of inclusions were found in Baltic amber, with >3000 species described from Baltic amber (Weitschat and Wichard, 2010) and >700 species reported from Bitterfeld amber (Rappsilber, 2016). Uncertainties regarding botanical provenance, age, and geographical origin are particularly associated with these two amber deposits. Langenheim (2003) introduced the term “Tertiary Baltic Amber Mystery” to refer to the conflicting evidence about the botanical source of succinite, which is the main resin variety of Baltic and Bitterfeld amber. Suggested source plants of succinite include representatives of the Araucariaceae, Cupressaceae, Pinaceae, and Sciadopityaceae (Langenheim, 2003; Yamamoto et al., 2006; Wolfe et al., 2009; Seyfullah et al., 2018). Baltic amber primarily derives from the marine Blue Earth layer that is predominantly exposed on the Samland Peninsula northwest of Kaliningrad (Russia) and contiguous areas. Baltic amber eroded from sediments is also

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frequently found washed ashore along the coast of the Baltic Sea, particularly on the Samland Peninsula and in the Baltic States, Poland, Denmark, Germany, and southern Sweden (Standke, 2008; Weitschat and Wichard, 2010). The absolute age of Baltic amber is still under debate. Palynological data suggest an upper Eocene (Priabonian) age (c. 38e34 million years) of the Blue Earth (Kosmowska-Ceranowicz et al., 1997; Standke, 1998, 2008). Fewer amounts of amber also occur in Lutetian (middle Eocene) sediments including the Lower Blue Earth and even in the upper Oligocene Lower Gestreifter Sand, leading to a possible age range of approximately 47e 24 million years before present for all Baltic amber-bearing strata (Kosmowska-Ceranowicz et al., 1997; Standke, 1998, 2008; Kasi nski and Kramarska, 2008). The frequently cited Lutetian age of the Blue Earth was originally suggested by Ritzkowski (1997), who dated glauconites from the amber-bearing layer. However, Clauer et al. (2005) showed that the applied dating methods can lead to older age estimates if the glauconites have been reworked or if nonglauconized detrital mica contaminated the glauconite splits. Redeposition of the Baltic amber into the Blue Earth layer has also been suggested (Weitschat and Wichard, 2010). However, typical signs of erosion which normally occur if amber has been reworked, such as “pebble-shaped” amber pieces or a dark oxidized crust, are absent in the material from the Blue Earth layer. The majority of amber from the Blue Earth is rather of a fresh lemon yellow color and unoxidized (Grimaldi and Ross, 2017). Bitterfeld amber derives from the Goitzsche open cast mine near the city of Bitterfeld in central Germany where it was mined from the 1970s to the 1990s (Liehmann, 2013). The amber-bearing sediment of this locality is the Bernsteinschluff Horizon, located in the upper part of the Cottbus Formation, and it has been dated as upper Oligocene with an absolute age of 25.3e23.8 million years (Knuth et al., 2002; Blumenstengel, 2004). A notion that Bitterfeld amber represents redeposited Eocene Baltic amber is based on the significant proportion of identical arthropod morphologies in amber from both localities (Weitschat, 1997). However, redeposition of Baltic amber is unlikely based on the reconstruction of the sedimentary environment of this amber deposit (Standke, 2008). In addition, chemical differences have been detected between Baltic and Bitterfeld succinite (Yamamoto et al., 2006; Vávra, 2008), and more additional resin types occur in the Bitterfeld area, compared with the Baltic region (Kosmowska-Ceranowicz and Vávra, 2015), which makes an identical provenance unlikely. A local reworking of preChattian amber, however, has not been dispelled so far (see Dunlop, 2010 and Wolfe et al., 2016, for discussion). In any case, Bitterfeld amber is Paleogene in age and its minimum age is approximately 24 million years.

Given these uncertainties, assumptions about forest composition, forest structure and climate of the source area of these ambers vary considerably, depending on the assumed age, origin and source plants (Sadowski et al., 2017). The search for amber inclusions that are indicative for certain forest types and forest structures is a logical consequence (Kaasalainen et al., 2017; Sadowski et al., 2017). Inclusions of filamentous fungi are common in amber from many deposits around the world (Beimforde and Schmidt, 2011). However, in most cases, only vegetative mycelia are preserved without any reproductive structures. As the accurate taxonomic assignment of such specimens is usually impossible, relatively few amber-preserved fungal fossils have so far been assigned to extant lineages (Beimforde et al., 2014; Kettunen et al., 2015, 2018). However, recent studies have demonstrated that European Paleogene amber is a valuable source of fossils in some taxonomic and ecological groups within the Ascomycota. Such findings have already provided valuable new insights into the diversity and evolutionary history of sooty molds (Schmidt et al., 2014), lichen-symbiotic and lichenassociated fungi (Hartl et al., 2015; Kaasalainen et al., 2015, 2017; Kettunen et al., 2016, 2017), and calicioid lichens and fungi (Rikkinen and Poinar, 2000; Rikkinen, 2003b; Tuovila et al., 2013; Rikkinen et al., 2018). Calicioid lichens and fungi, which are from now on referred to as “calicioids,” constitute a diverse group of tiny ascomycetes with superficially similar, usually well-stalked ascomata and which often accumulate mature ascospores on top of the apothecial disk to form a true mazaedium (Plates I, II, and III). Because the ascospores of most calicioids are dark, the mazaedium stains the finger if touched. The Finnish term for calicioids (nokinuppinen) is a diminutive of “smut-knob,” which accurately describes the smearing property of the persisting spore mass. Calicioids include both lichen-symbiotic, parasitic and saprotrophic species and include genera from several classes of Ascomycota. The polyphyletic nature of the group was first demonstrated by Tibell (1984) on morphological grounds and has since been confirmed in many molecular studies (Wedin and Tibell, 1997; Tibell and Wedin, 2000; Wedin et al., 2000, 2002; Tibell, 2003; Hibbett et al., 2007; Prieto et al., 2013; Prieto and Wedin, 2013, 2017; Beimforde et al., 2014; van den Broeck et al., 2017). Traditionally, Sphaerophorus Pers. and some other genera of fruticose macrolichens with mazaediate apothecia also were included in “calicioid lichens.” However, as their morphology, size, and ecology differ drastically from those of crustose species, they are not discussed further here. The aim of this study is to use all available information on the morphology and ecology of extant calicioids to reconstruct the substrate and habitat ecology of known fossil calicioids and then to use this information to open

Calicioids and Paleogene Forest Structure Chapter j 22

529

PLATE I Morphology of extant calicioid lichens of the genus Chaenotheca. (1) Chaenotheca trichialis (Ach.) Hellb. with minutely squamulose thallus. (2) Chaenotheca stemonea (Ach.) Müll. Arg. with farinaceous thallus. (3) Chaenotheca brunneola (Ach.) Müll. Arg. with immersed, endosubstratic thallus. All lichens were photographed in the field in central Finland. Scale bars ¼ 2 mm.

new insights into the stand structure and ecological conditions of European Paleogene amber forests. First, we introduce the morphology of extant calicioids and demonstrate that their structural features are intimately linked to habitat ecology and are instrumental for successful dispersal; we also explain the conspicuous morphological convergence between phylogenetically distant calicioid fungi. Then, we show that the adaptive traits of calicioids have not changed since at least the Eocene, and argue that their fundamental niches also have remained unchanged. Finally, we summarize what the diversity and relative abundance of fossil calicioids in amber tells us about the ecological conditions that once prevailed in European amber forests.

2. MORPHOLOGY, DISTRIBUTION, AND ECOLOGY OF EXTANT CALICIOIDS 2.1 Morphology and Anatomy Most nonlichenized calicioids have immersed mycelia and produce ascomata only on the surface of their substrate. While the vegetative thalli of some calicioid lichens also

are endosubstratic, most of them produce episubstratic crustose thalli (Plate I). Depending on the species, the thallus can be smooth, squamulose, verrucose, granular, or farinaceous, and in some species, the structure of the thallus is partly determined by growth conditions. The most conspicuous features of calicioids are the upright ascomata, which are invariably produced on the substrate surface (Plates I, II, and III). The size and shape of ascomata vary between different genera and species as can be expected in light of the highly polyphyletic nature of the group. In several genera, the ascomata are always stalked, while in others, they can be either stalked or sessile or always sessile. Even when mature, the ascomata are small, typically .05).

TABLE 25.7 Leaf Venation Density (Dv), Leaf Hydraulic Conductance (Kleaf), and Maximum Photosynthetic Capacity (Pc) for Glossopteris Leaves Grouped Into Six Bins by Paleolatitude Grouping

Dva

Kleafb

Pcc

S1

1.78

3.64

4.25

S2

1.80

3.70

4.31

S3

1.51

3.02

3.52

S4

2.05

4.24

4.93

S5

1.75

3.58

4.18

S6

2.20

4.58

5.32

a

mm/mm2. mmol/m2 s MPa. c mmol CO2/m2 s. b

suggest that atmospheric CO2 has little influence over leaf venation density and photosynthetic capacity. These authors studied leaf venation density of fossil leaves from a variety of taxa from different times and atmospheric CO2 concentrations and found significant changes to Dv through time. This study follows leaf venation density of

Glossopteris leaves through time and found no substantial difference despite examining leaves that occur over a wide range of CO2 concentrations.

4.3 Glossopteris Leaf Venation Density Across High Paleolatitude Environments It has been shown that diffuse light can lower the maximum amount of photosynthesis that a plant is capable of undergoing (Brodersen et al., 2008). Due to the diffuse nature of light at high latitudes, it can be assumed that photosynthetic rate and leaf venation density are likely lower as latitudes increase to the extreme; however, the results of this study suggest that there is no relation between leaf venation density and paleolatitude in Permian Glossopteris leaves (Figs. 25.4e25.6, Tables 25.5e25.7). The effects of paleolatitude on leaf venation density were studied with three different groupings of paleolatitudes. Since the paleolatitudes (Tables 25.1 and 25.2) of each locality represent a range of possibilities based on the possible time in which fossilization occurred and the limits of the reconstruction model, many of the localities occur in overlapping ranges. These overlapping localities were collapsed into bins for the statistical analysis. As the groupings are somewhat

Leaf Venation Density of Permian Leaf Morphotypes Chapter j 25

arbitrary, localities were grouped in three different ways in an attempt to remove experimenter bias from the analysis. In the case where the localities were lumped into two bins (L1, L2), statistical analysis could not reject the null hypothesis that Dv would be the same for Glossopteris leaves from the different paleolatitudes; however, the Pvalue (.056) for this analysis is fairly close to the traditional cut-off for significance. The unbalanced nature of this the Glossopteris Dv dataset does limit the statistical power of the test. When the results of this grouping are considered in conjunction with the other groupings, it does lend support to the idea that there is no real difference between the leaf venation density of the two groups. The Dv for Glossopteris leaves from a lower paleolatitude was 1.73 mm/mm2 and 1.79 for a Glossopteris leaf from a higher paleolatitude. This is the opposite of what was hypothesized earlier for leaves living under very diffuse light. In another grouping, localities were lumped into three separate bins (M1, M2, M3). A statistical analysis of Glossopteris Dv could not reject the null hypothesis that Dv would be the same for Glossopteris leaves from the different paleolatitudes. In this case, the P-value (.16) was not close to indicating significance. This adds more weight to the conclusion that paleolatitude has no observable effect of Glossopteris leaf venation density (Fig. 25.5, Table 25.6). The final grouping split the localities into six separate groups (S1, S2, S3, S4, S5, S6). Statistical analysis did show that there were statistically significant differences between the Dv grouped by different latitudes (Fig. 25.6, Table 25.7). The pattern of Dv and the groupings of similar Dv at a variety of latitudes suggest that paleolatitude was not the driver of these differences, but rather some random or unknown factor, or through uneven sampling. If paleolatitudes were driving the differences in Dv, we would expect to see a trend (increasing or decreasing) in Dv as the paleolatitude increases. Instead, the distribution of Dv varies and some low paleolatitude groups have distributions statistically indistinguishable from Dv at higher paleolatitude groups (Fig. 25.6). For example, S1 is statistically indistinguishable from S6. The conclusion drawn from these three analyses is that the leaf venation density of Glossopteris leaves did not change in an observable way in response to paleolatitude. This fits with the work of Chabot et al. (1979) that demonstrated that changes in angiosperm leaf morphology only occurred in response to integrated light flux and not instantaneous light flux.

5. CONCLUSIONS It can be difficult to detect changes in leaf venation density caused by changes in CO2 concentration or paleolatitude because of the many other environmental factors that are known to influence leaf venation density. The height of a

625

developing leaf is known to affect the leaf venation density of some plants by increasing Dv with increasing height (Roth-Nebelsick et al., 2001 and references therein) or by decreasing Dv with increasing height (Critchfield, 1960; Uhl and Mosbrugger, 1999). For some plants, leaf venation density is a function of leaf size (Gupta, 1961). Leaf venation density is also known to be affected by temperature, soil moisture, humidity, and nutrient deficiency (Uhl and Mosbrugger, 1999). Despite the potential noise involved in an analysis of leaf venation density, a statistically relevant signal was found in some of the areas of interest. Our knowledge of the high photosynthetic productivity in glossopterids has been based on wood production (Taylor and Ryberg, 2007; Miller et al., 2016). While this has provided information on high paleolatitude ecosystems, it has not been able to supply a comparison to nonglossopterids nor has it been able to look at variation in glossopterid wood based on leaf type. We currently lack cordaite wood at these localities as well as a way to determine the leaf morphotypes attached to the glossopterid wood. Analysis of leaf venation density has demonstrated that the Glossopteris leaf morphotype is more productive than the cooccurring Gangamopteris and Noeggerathiopsis leaf morphotypes. It is interesting that Glossopteris leaves, the most common, demonstrate a higher calculated maximum photosynthetic rate than Gangamopteris, the second most common glossopterid leaf morphotype. Statistical analysis of Glossopteris leaves from early and late Permian sediments has shown a significant difference in venation density. It appears that the highest density reticulate patterns were most common during the low atmospheric CO2 levels of the early Permian. Taylor and Ryberg (2007) noted that the early Permian woods studied in their analysis produced more cells per growth ring than those from the late Permian. It is possible that this could be related to the higher leaf venation density found in Glossopteris leaves growing during this time period. In general, a higher Dv leads to a higher calculated maximum photosynthetic rate; this could be the cause of the larger amount of cells in the early Permian wood. It can be difficult to directly compare these physiological values, as they are produced from a regression equation developed with plants growing in modern conditions (Boyce et al., 2017). Additionally, the changes in leaf venation density that occurred were small and unlikely to have represented a major change in photosynthetic capacity. There was no discernible difference in leaf venation density in Glossopteris leaves from different paleolatitudes. It is possible that effects of paleolatitude on Dv are masked by many of the preceding factors or that diffuse light or continuous light regimes caused by high paleolatitudes do not affect the anatomy of Glossopteris leaves. Jagels and Day (2004) showed that M. glypostroboides was able to

626

SECTION j V Antarctic Paleobotany

avoid downregulation of photosynthesis when grown under continuous light conditions. Other gymnosperms had lowered rates of photosynthesis as a result of foliar starch buildup (Equiza et al., 2006a). Investing photosynthates in new biomass allowed M. glyptostoboides to avoid photosynthetic downregulation. One tool at its disposal was epicormic shoots, a feature found in the glossopterids (Decombeix et al., 2010). It seems likely that growing at high paleolatitudes would require some physiological adaptations in order for plants to flourish. It does not appear that the leaf venation of Glossopteris contained any such adaptations, but there is potential in seeking out adaptations in other glossopterid features.

ACKNOWLEDGMENTS I am deeply indebted to Dr. Thomas N. Taylor, whose mentorship, lessons, stories, and friendship will not be forgotten. I am grateful for the help of Dr. Edith L. Taylor, who reviewed an early version of this manuscript, which was much improved by her valuable feedback. I also thank Dr. Rudy Serbet and Dr. Kevin Boyce for providing essential feedback on this manuscript.

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Ryberg, P.E., Taylor, E.L., Taylor, T.N., 2012. Antarctic glossopterid diversity on a local scale: the presence of multiple megasporophyll genera, Upper Permian, Mt. Achernar, Transantarctic Mountains, Antarctica. American Journal of Botany 99, 1531e1540. Sack, L., Scoffoni, C., 2013. Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist 198, 983e1000. Sack, L., Tyree, M.T., 2005. Leaf hydraulics and its implications in plant structure and function. In: Holbrook, N.M., Zwieniecki, M.A. (Eds.), Vascular Transport in Plants. Academic Press, Boston, MA, pp. 93e114. Scoffoni, C., Kunkle, J., Pasquet-Kok, J., Vuong, C., Patel, A.J., Montgomery, R.A., Givnish, T.J., Sack, L., 2015. Light-induced plasticity in leaf hydraulics, venation, anatomy, and gas exchange in ecologically diverse Hawaiian lobeliads. New Phytologist 207, 43e58. Slater, B.J., McLoughlin, S., Hilton, J., 2015. A high-latitude Gondwanan lagerstätte: the Permian permineralised peat biota of the Prince Charles Mountains, Antarctica. Gondwana Research 27, 1446e1473. Smith, T.M., Shugart, H.H., Woodward, F.I., 1997. Plant Functional Types: Their Relevance to Ecosystem Properties and Global Change. Cambridge University Press, Cambridge, United Kingdom, p. 388. Sokal, R.R., Rohlf, F.J., 1995. Biometry: The Principles and Practice of Statistics in Biological Research. W.H. Freeman, New York, NY, USA, p. 918. Taylor, E.L., Ryberg, P.E., 2007. Tree growth at polar latitudes based on fossil tree ring analysis. Palaeogeography, Palaeoclimatology, Palaeoecology 225, 246e264. Taylor, E.L., Taylor, T.N., Cúneo, N.R., 1992. The present is not the key to the past: a polar forest from the Permian of Antarctica. Science 257, 1675e1677. Taylor, T.N., Taylor, E.L., Krings, M., 2009. Paleobotany: The Biology and Evolution of Fossil Plants. Academic Press, New York, NY, p. 1254. Tewari, R., Chatterjee, S., Agnihotri, D., Pandita, S.K., 2015. Glossopteris flora in the Permian Weller Formation of Allan Hills, South Victoria Land, Antarctica: implications for paleogeography, paleoclimatology, and biostratigraphic correlation. Gondwana Research 28, 905e932. Tomezzoli, R.N., Vilas, J.F., 1999. Palaeomagnetic constraints on the age of deformation of the Sierras Australes thrust and fold belt, Argentina. Geophysical Journal International 138, 857e870.

Torsvik, T.H., Van der Voo, R., Preeden, U., Mac Niocaill, C., Steinberger, B., Doubrovine, P.V., van Hinsbergen, D.J.J., Domeier, M., Gaina, C., Tohver, E., Meert, J.G., McCausland, P.J.A., Cocks, L.R.M., 2012. Phanerozoic polar wander, palaeogeography and dynamics. Earth-Science Reviews 114, 325e368. Trivett, M.L., Pigg, K.B., 1996. A survey of reticulate venation among fossil and living land plants. In: Taylor, D.W., Hickey, L.J. (Eds.), Flowering Plant Origin, Evolution & Phylogeny. Springer US, Boston, MA, pp. 8e31. Uhl, D., Mosbrugger, V., 1999. Leaf venation density as a climate and environmental proxy: a critical review and new data. Palaeogeography, Palaeoclimatology, Palaeoecology 149, 15e26. Whittaker, R.H., 1965. Dominance and diversity in land plant communities. Science 147, 250e260. Williams, P.L., 1969. Petrology of upper Precambrian and Paleozoic sandstones in the Pensacola mountains, Antarctica. Journal of Sedimentary Research 39, 1455e1465. Wilson, J.P., 2016. Hydraulics of Psilophyton and evolutionary trends in plant water transport after terrestrialization. Review of Palaeobotany and Palynology 227, 65e76. Wilson, J.P., Fischer, W.W., 2011. Hydraulics of Asteroxylon mackei, an early Devonian vascular plant, and the early evolution of water transport tissue in terrestrial plants. Geobiology 9, 121e130. Wilson, J.P., Knoll, A.H., 2010. A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants. Paleobiology 36, 335e355. Wilson, J.P., Knoll, A.H., Holbrook, N.M., Marshall, C.R., 2008. Modeling fluid flow in Medullosa, an anatomically unusual Carboniferous seed plant. Paleobiology 34, 472e493. Xiong, D., Flexas, J., Yu, T., Peng, S., Huang, J., 2017. Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO2 in Oryza. New Phytologist 213, 572e583. Young, D.J., Ryburn, R.J., 1968. The geology of Buckley and Darwin Nunataks, Beardmore Glacier, Ross dependency, Antarctica. New Zealand Journal of Geology and Geophysics 11, 922e939. Zwieniecki, M.A., Stone, H.A., Leigh, A., Boyce, C.K., Holbrook, N.M., 2006. Hydraulic design of pine needles: one-dimensional optimization for single-vein leaves. Plant, Cell & Environment 29, 803e809.

Chapter 27

Cretaceous to Paleogene Vegetation Transition in Antarctica David J. Cantrill1, 2 1

Royal Botanic Gardens Victoria, Melbourne, VIC, Australia; 2The University of Melbourne, Parkville, VIC, Australia

1. INTRODUCTION The observations by J.D. Hooker on the floras of southern South America, Australia, and New Zealand lead to the conclusion that the floristic similarities were evidence of a “once more extensive flora, which has been broken up by geological and climatic causes” (Hooker, 1853). These circum-Antarctic patterns have fascinated biogeographers ever since. Congruence between phylogenetic patterns and patterns of Gondwana breakup have been used to support a vicariant origin for this distinctive southern biota (Brundin, 1966). However, patterns of relationships between taxa dispersed across the Southern Hemisphere are not always congruent with our understanding of the pattern of Gondwana fragmentation (Sanmartin and Ronquist, 2004), suggesting other processes such as West Wind Drift might be driving some of these distributions (Sanmartin et al., 2007; Winkworth et al., 2015). The development of divergence dating has further raised questions about vicariant scenarios based on Gondwana fragmentation as inferred clade divergence dates are often too young to be consistent with vicariance. In part this may be due to the calibration strategies employed (Sauquet et al., 2012) but also that fossil calibration points are transmogrified from minimum ages to absolute ages in the analysis phase (Sauquet et al., 2012), resulting in biases toward younger ages (Wilf and Escapa, 2015). As our knowledge of fossil floras of the Southern Hemisphere improves, the ages of clades are indeed being pushed backward (e.g., Eucalyptus subgenus Symphomyrtus; Gandolfo et al., 2011; Hermsen et al., 2012; Physalis Wilf et al., 2017), shifting dispersal scenarios toward ones consistent with vicariance across a number of lineages (Wilf and Escapa, 2015). A significant challenge in resolving what components of the extant vegetation are likely to be a result of vicariance

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00027-9 Copyright © 2018 Elsevier Inc. All rights reserved.

versus those components that are likely to be dispersed is the lack of extant biota on the Antarctic continent that prevents this landmass from being included in phylogenetic studies of extant organisms. This has resulted in an inferred role for the region and an assumption that it can be regarded as a single biogeographic unit. However, as pointed out by McLoughlin (2001), the Antarctic region can be broken into East Antarctica and West Antarctica, with both regions interacting separately with other Gondwana fragments. The Late Cretaceous through Paleogene is a critical period in shaping circum-Antarctic distribution patterns as this coincides with severing of connections between the present day continents that made up Gondwana, and the origin and radiation of key plant groups (Fig. 27.1). In this context I review the current state of knowledge of Antarctic vegetation through the critical Late Cretaceous to Paleogene and implications for biogeography across the Southern Hemisphere.

1.1 Geological and Geographic Framework Interpretation of phylogenies as supporting a vicariant origin of lineages relies on a robust understanding of the geological history of continental fragmentation. The pattern of Gondwana fragmentation is relatively well understood for the major continental masses (McLoughlin, 2001) but the role of smaller crustal blocks is less well established. The main continental landmass of East Antarctica can be regarded as a single biogeographic unit. However, it should be noted that our understanding of the paleogeography through the Cretaceous and Cenozoic is still rudimentary, and the presence of internal seaways that divided the continent into smaller regions (e.g., Wilkes Land; Aitken et al., 2014) and formation of mountain ranges that acted as 645

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FIGURE 27.1 Polar reconstruction of Gondwana at 84 Ma.

barriers (e.g., Gamburtsev Mountains, Bo et al., 2009; Ferraccioli et al., 2011) still remain to be resolved (Fig. 27.2). West Antarctica by comparison is composed of several crustal blocks (Antarctic Peninsula, Marie Byrd Land, Ellsworth-Whitmore Mountains, Thurston Island, and Haag Nunataks) (Dalziel and Elliot, 1982), each with independent histories, and they should be considered separately when developing a biogeographic framework based on geology (Fig. 27.2). West Antarctica is separated from East Antarctica by the Weddell Sea and the West Antarctic Rift System, the latter which formed a seaway between the two regions at times of global warmth.

1.1.1 West Antarctica Crustal Blocks The initiation of rifting between Antarctica and Africa in the Jurassic marked the breakup of Gondwana (Storey, 1995). The development of the incipient Weddell Sea began the isolation of Antarctica from other fragments of the supercontinent. Initial continental extension formed a

rift system, beginning the process of isolating some of the crustal blocks that make up West Antarctica today (Antarctic Peninsula, Haag Nunataks, Ellsworth-Whitmore Mountains). However, while the Weddell Sea Rift System underwent sea floor spreading in the north, the southern part of this system failed to form oceanic crust and today is underlain by continental crust (Hübscher et al., 1996; Hunter et al., 1996). The lack of outcrops and access to the southern Weddell Sea has made it difficult to study this region where the geology is complex (see Jordan et al., 2013, 2017 for a recent summary) and there are currently several competing hypotheses about the location and movement of various crustal fragments. The EllsworthWhitmore Mountains are variously thought to originate in a position near East Africa in the Natal Embayment (Randall and MacNiocaill, 2004; Dalziel, 2013) and were translated 1500 km southward and rotated by 90 degrees to their present position. More recently, based on geophysical evidence, they have been placed 1000 km southward (north of the Pensacola Mountains) and are considered to have been translated only 500 km and rotated by 30 degrees

Antarctic Cretaceous Paleogene Vegetation Chapter j 27

Sc

a oti

Se

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a

South Shetland Islands James Ross Island Seymour Island

Weddell Sea

AP HN

PM

S

sI

an

Ev

d for

Gamburtsev Mountains

IS

t

Ru

EWM Transantarctic Mountains

TI

We s

East Antarctica

tA

nta

rct

and

Ross Sea

es L

West Antarctica

ift

McMurdo Sound

Wilk

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FIGURE 27.2 Map of the Antarctic region. Dashed areas approximate boundaries of West Antarctic crustal blocks. AP, Antarctic Peninsula; EWM, Ellsworth-Whitmore Mountains; HN, Haag Nuanataks; PM, Pensacola Mountains; TI, Thurston Island.

(Jordan et al., 2017). Haag Nunataks have been treated as either a separate crustal block (Maslanj and Storey, 1990; Storey, 1991) or more recently as part of a contiguous Haag and Ellsworth-Whitmore Block (Jordan et al., 2013, 2017). The original position of the Antarctic Peninsula is also problematic as early rigid continent reconstructions with the Antarctic Peninsula fixed to East Antarctica result in the Antarctic Peninsula overlapping with the Falklands Plateau (e.g., Norton and Sclater, 1979), which is geologically and physically untenable (Dalziel and Elliot, 1982) and implies relative movement between the Antarctic Peninsula and East Antarctica during these time intervals. A better understanding of sea floor spreading patterns together with incorporating geological information has improved the reconstructions, and solutions to the Antarctic Peninsula issues have included treating South America as series of independent but juxtaposed crustal blocks (e.g., Konig and Jokat, 2006).

Critical to a discussion of Late Cretaceous and Paleogene biogeography the Ellsworth-Whitmore Mountains (and Haag Nunataks) were fixed relative to the Antarctic Peninsula by 175 Ma (Grunow et al., 1987). The oldest sea floor anomaly that can be confidently identified in the Weddell Sea is 147 Ma (Konig and Jokat, 2006), and by Early Cretaceous times the Antarctic Peninsula, Haag Nunataks, and the Ellsworth Whitmore Mountains were adjacent to East Antarctica. Whether this was continuous land or the blocks were separated by narrow straits is still an open question. The region between the Antarctic Peninsula, Haag Nunataks, and the Ellsworth Whitmore Mountains consists of a series of fault blocks (Maslanj and Storey, 1990; Jones et al., 2002) that are now occupied by deep valleys interpreted as rift grabens that constrain the position of present day ice streams (Evans and Rutford). For any discussion of Late Cretaceous and Paleogene biogeography the geographic relationship between the

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Antarctic Peninsula, Haag Nunataks, Ellsworth-Whitmore Mountains, and East Antarctica can be regarded as fixed but the timing of uplift and formation of the rifts between the fragments is critical. It has been suggested that parts of the Ellsworth-Whitmore Mountains uplifted in the Cretaceous (Fitzgerald and Stump, 1991). The geology of the Scotia Sea region is complex, making reconstruction of the separation of South America from the Antarctic Peninsula challenging (Dalziel et al., 2013). In Cretaceous times this region formed part of a continuous Pacific margin. Independent movement between Antarctic Peninsula and South America has been implied from the Late Cretaceous (Cunningham et al., 1995), and this compressional regime resulted in the partial closure of Rocas Verdes Basin (Dalziel et al., 2013) ensuring continuous land was present through this period of time. A change in tectonic regime that occurred in the Late Paleocene with the onset of rifting marked the start of separation between these two regions. Interpretations of the timing of separation of South America from the Antarctic Peninsula, and the formation of Drake Passage, ranges from 50 Ma (e.g., Livermore et al., 2005, 2007; Eagles et al., 2006; Ghiglione et al., 2008), 41 Ma (Scher and Martin, 2006), Oligocene (Lavwer and Gahagan, 2003) to 27 Ma (Barker, 2001; Barker and Burrell, 1977). It is envisaged that shallow seaways developed in the Paleogene (Livermore et al., 2005, 2007) with the critical question being when Drake Passage became an effective barrier for terrestrial exchange. Based on the unique nature of the Eocene mammal faunas from Seymour Island and the lack of certain South America groups it has been suggested that biotic separation occurred by 55 Ma (Reguero et al., 2014). The West Antarctic Rift separates Marie Byrd Land and Thurston Island from East Antarctica, and in this sector of Antarctica subduction ceased as a result of collision between the Hikurangi Plateau and the paleo-Pacific between 100 and 94 Ma (Mukasa and Dalziel, 2000). This resulted in extension along the Gondwana margin and ultimately the rifting of Zealandia (Chatham Rise, Campbell Plateau) by 84 Ma (Gaina et al., 1998). The response to this event in the Antarctic was initial uplift of the Transantarctic Mountains (southern rift flank) and formation of the West Antarctic Rift between 100 and 85 Ma (Fitzgerald, 2002) with an estimated 400 km of extension. This was followed by a second phase of extension in the Cenozoic between 43 and 26 Ma (Garnot et al., 2013). The second phase of extension was oblique north to south (Zattin et al., 2014) and the West Antarctic Rift may have extended as far as the southern Antarctic Peninsula (Eagles et al., 2009). Marie Byrd Land and Thurston Island form the other side of the present-day West Antarctic Rift System and represent the eroded roots of the Mesozoic pacific margin arc batholith. A similar chronology of denudation with

major periods of erosion forming a low-lying land surface in the Late Cretaceous (Spiegel et al., 2016) was followed by renewed uplift of the Marie Byrd Land Dome in the Cenozoic. The oldest volcanoes in this region are 30 Ma; this has been taken as timing of uplift but Spiegel et al. (2016) thought it was more recent (20 Ma). The interpretation that Marie Byrd Land was largely low lying in the Late Cretaceous and only uplifted more recently could lead to the interpretation that the Cretaceous rift system was bounded on this side by Zealandia (Chatham Rise, Campbell Plateau) and that Marie Byrd Land is a rift dome rather than the flank of the rift system.

1.1.2 East Antarctica In contrast to West Antarctica the isolation of East Antarctica from other Gondwana fragments is relatively well constrained. Australia-India-Antarctica started separating in the Late Jurassic with a seaway opening between Australia and Antarctic, first in the west but propagating eastward as the Australian Bight opened. Although a seaway was present between Australia and Antarctica (94 Ma), Australia remained connected to Antarctica via Tasmania and the South Tasman Rise, the latter only separating from Antarctica around 34 Ma (Royer and Rollet, 1997). However, a narrow seaway and shallow circulation is implied in the Eocene (Bijl et al., 2013). Africa separated in the Jurassic as part of the initial breakup of Gondwana, initial continental stretching between 184 and 171 Ma created a rift valley up to 300 km wide prior to oceanic spreading at 171 Ma (Nguyen et al., 2016). Adjacent to this region Madagascar/India and Sri Lanka were also rifting from Antarctica with separation at about 132 Ma. India rotated counterclockwise from Antarctica with the present day southern tip of India separating last (Gaina et al., 2007). The only complicating factor, and one that has been discussed as providing a potential terrestrial connection after separation (e.g., Hay et al., 1999), was the eruption and formation of the Kerguelen Plateau. This region is underlain by thinned continental crust upon which a voluminous large igneous province formed between 136 and 112 Ma (Direen et al., 2017). Peak volcanism occurred between 112 and 119 Ma and drilling on the Kerguelen Plateau recovered terrestrial sediments of late Albian to early Cenomanian age (Mohr and Gee, 1992a; Mohr et al., 2002); younger marine deposits (Coniacian) also contain a significant terrestrial component (Mohr and Gee, 1992b). Today a few scattered islands remain emergent so land has been present on this area since at least Late Cretaceous times. Extensive reduction in land area occurred in the Late Cretaceous as indicated by marine sediments across much of the Kerguelen Plateau. How long this region might have acted as a terrestrial connection between Antarctica and India is still

Antarctic Cretaceous Paleogene Vegetation Chapter j 27

an open question but it is unlikely to have been more recent than the mid- Cretaceous (Ali and Krause, 2011).

1.2 Paleogeography Although a robust understanding of relationships between the various crustal fragments that once made up Gondwana is necessary for terrestrial biogeographic studies this is only part of the equation. Continental crust, particularly crust thinned during continental extension, may sink below sea level, isolating biotas and severing terrestrial land connections. There are numerous low-temperature thermochronological studies that document phases of uplift and denudation across the Antarctic region including for the Transantarctic Mountains (Fitzgerald, 2002), Marie Byrd Land (Lindow et al., 2016; Spiegel et al., 2016), and Ellsworth Mountains (Fitzgerald and Stump, 1991) but they have yet to be integrated into a model of paleogeography through time. The most recent comprehensive attempt to model paleogeography has predicted the extent of land at the Eocene/Oligocene boundary based on removal of the ice sheet, isostatic unloading, thermal subsidence, global sea level curves, and plate tectonic movements (Wilson et al., 2012). This model predicts continuous land from the tip of the Antarctic Peninsula through West Antarctica to Australia. However, several of the model assumptions need further testing, especially in light of recent studies on the timing of uplift in Marie Byrd land (Lindow et al., 2016; Spiegel et al., 2016).

1.3 Climate Framework The Late Cretaceous through Paleogene is a period of globally warm climates with some of the warmest periods (e.g., mid-Cretaceous Climate Optimum [early Turonian]; Late Paleocene Thermal Maximum [LPTM]; Early Eocene Climatic Optimum [EECO]; Mid-Eocene Climatic Optimum [MECO]) in the last 90 Ma of Earth history. From the peak in global warmth in the early Turonian (Barral et al., 2017, and references therein) global climates cooled through the Late Cretaceous with peak cooler phases in the early Campanian and early Maastrichtian (Barral et al., 2017). Warming through the Maastrichtian was interrupted by events at the Cretaceous-Paleogene boundary with a short period of cooler conditions followed by continued warming through the Paleocene and Eocene to EECO. It should be noted that short warm intervals such as the LPTM occurred within this background of overall warming and represent a short-lived perturbation to climate. In the high southern latitudes the cooler Maastrichtian conditions have some evidence of sea ice (Bowman et al., 2013), and short-lived fluctuations in sea level have been suggested due to ice sheet formation (Miller et al., 2005). The lack of marine record of ice-rafted debris suggests that these ice

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sheets were on the interior of the continent rather than coastal. From the peak of warmth in the Eocene, global climate cooled with a sharp drop in temperatures at the Eocene-Oligocene boundary (Zachos et al., 2001). The exact timing of glaciation on Antarctica has been debated but new evidence suggests ice in the late Eocene (Carter et al., 2017) prior to the sharp cooling at the EoceneOligocene boundary (Zachos et al., 2001). These fluctuations had a profound effect on the vegetation across the southern high latitudes. During periods of warming tropical floras were pushed into higher latitudes (e.g., presence of Bombacaceae in Wilkes Land, East Antarctic margin; see Pross et al., 2012; Contreras et al., 2013) and are most noticeable in the Eocene. As a result the biogeographic patterns seen in the southern hemisphere should not be seen as being largely influenced by continental fragmentation but also in response to shifting climate and the availability of land for expansion of warmer biotas southward during periods of global warmth and the expansion of cool biotas northward during periods of climate cooling.

2. LATE CRETACEOUS VEGETATION Our window into Late Cretaceous Antarctic vegetation is limited to floras from West Antarctica and in particular the Antarctic Peninsula where material occurs in the James Ross Basin and the South Shetland Islands. In the James Ross Basin leaf-, wood-, and palynofloras are known from the Coniacian Hidden Lake Formation (Barreda et al., 1999; Cantrill and Poole, 2002, 2005; Hayes et al., 2006; Skala and Vodrázka, 2014; Kvacek, 2014; Kvacek and Vodrázka, 2016), Santonian to Campanian Santa Marta Formation (Cantrill and Poole, 2002, 2005; Hayes et al., 2006), late Campanian to early Maastrichtian Snow Hill Island Formation (Cantrill and Poole, 2002, 2005), and the early Maastrichtian to Danian Lopez de Bertodano Formation (Cantrill and Poole, 2005; Bowman et al., 2014). In the South Shetland Islands Late Cretaceous floras have been reported from Livingston Island at Williams Point (Rees and Smellie, 1989; Torres and Lemoigne, 1989; Chapman and Smellie, 1992; Philippe et al., 1999, Poole and Cantrill, 2001) and from King George Island (Dutra and Batten, 2000, and references therein). The flora of Williams Point was originally regarded as Triassic (Orlando, 1968) but based on plant fossil content is now regarded as Late Cretaceous and most likely Santonian to Campanian based on unpublished radiometric dates of ash horizons (Cantrill and Poole, 2012). The majority of plant fossil records come from King George Island where challenges with correlation of discontinuous outcrop, rapid facies variation, and issues with radiometric dating have created controversy over the age of the deposits. The Paradise Cove and Baranowski Glacier groups have been regarded as Late Cretaceous, largely based on whole-rock

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dating. Recent dating using single grain U/Pb series dating combined with magnetostratigraphy have indicated that the Paradise Cove Group is Late Cretaceous to early Paleocene and the Baranowski Glacier Group is early to middle Eocene (Nawrocki et al., 2010, 2011). This means the wellknown Zamek Formation flora previously regarded as Late Cretaceous (e.g., Zastawniak, 1994) should be considered early to middle Eocene (Mozer, 2012, 2013; Mozer et al., 2015). Importantly, it also raises questions about other sequences dated using whole-rock methods (e.g., Dutra and Batten, 2000) and whether these are also Eocene in age. Elsewhere Late Cretaceous palynomorphs have been recycled into Neogene sediments around the East Antarctic Margin (e.g., MacPhail and Truswell, 2004) but only provide limited insights into the vegetation.

2.1 Coniacian to Santonian (89.8e83.6 Ma) In the James Ross Basin the Coniacian Hidden Lake Formation contains abundant leaf material at several intervals (Hayes et al., 2006; Kvacek, 2014; Kvacek and Vodrázka, 2016) and wood (Cantrill and Poole, 2005; Skala and Vodrázka, 2014) throughout the section. Hayes et al. (2006) reported 30 leaf morphotypes including forms allied to the Sterculiaceae, Winteraceae, Eleaocarpaceae, Myrtaceae, and Nothofagaceae. The latter predates the appearance of Nothofagus pollen, which appears in the early Campanian (Keating, 1992; Dettmann et al., 1990). Kvacek and Vodrázka (2016) recorded the presence of Lauraceae, Nothofagaceae, Sterculiaceae, and Atherospermataceae, with the leaves of the latter being compared to extant Australian Daphandra and Doryphora. The wood flora reveals a high diversity of angiosperm types (Cantrill and Poole, 2005; Skala and Vodrázka, 2014) with none being particularly dominant and a number that could not be allied to extant families. Conifers still make up 50% of wood assemblage and are dominated by Podocarpoxylon with minor araucarian and cupressaceous wood (Cantrill and Poole, 2005). The pollen record yields a diversity of grains including Phyllocladites mawsonii (Lagarostrobus type) and other Podocarpaceae (Barreda et al., 1999). Among the angiosperm flora are Nyssapollenites (Euphorbiaceae), Clavatipollenites (Chloranthaceae), several proteaceous taxa, and the earliest record of Brenneripollis (monocotyledon) along with grains thought to represent thermophilic elements (e.g., Rhoipites) (Barreda et al., 1999). To date no quantitative counts of the palynoflora have been published and so information about the relative dominance of various elements and changes to the palynoflora composition are lacking. Nevertheless the combined palynology, leaf macrofloras, and wood suggest a mixed angiosperm podocarp conifer forest community. Significantly Nothofagidites is not recorded in this part of the succession.

Santonian floras occur in the lower part of the Santa Marta Formation (Lachman Crags Member) and include leaves (Hayes et al., 2006) and wood (Cantrill and Poole, 2005). Elsewhere in the Larsen Basin late Santonian floras include Table Nunatak where 11 types of angiosperm flowers have been recorded (Eklund, 2003; Eklund et al., 2004) together with mesofossils of ferns and conifers (Eklund et al., 2004). Although abraded, three of the flowers could be placed within Siparunaceae (close to Monimiaceae or Atherospermataceae), Winteraceae and Myrtaceae. In the South Shetland Islands the poorly age constrained flora from Williams Point (Cantrill and Poole, 2012 and references therein) contains a mixed conifer angiosperm assemblage with Monimiaceae and Cunoniaceae being present together with a diversity of angiosperm wood that could not be assigned to extant families (Poole and Cantrill, 2001). Leaf floras from these beds contain at least eight angiosperms including Lauraceae (Cinnamomoides) and a trilobed form (?Sterculiaceae) (Rees and Smellie, 1989). The Coniacian to Santonian floras document a mixed conifer angiosperm forest with high tree diversity compared to later times. The appearance of P. mawsonii marks the start of modernization of the coniferous element, and this taxon becomes a dominant component of the vegetation later in the Cretaceous. Quantitative studies of the palynoflora are needed to better understand changes in the vegetation through this interval of time.

2.2 Campanian to Early Maastrichtian (83e71.1 Ma) The Larsen Basin (Hathway, 2000; Olivero, 2012) sequence contains the best record of Antarctic vegetation from this time interval. Palynofloras, wood, and leaves have been recorded from the Santa Marta Formation (Hayes et al., 2006; Iglesias, 2016; Pujana et al., 2017), overlying Snow Hill Island and Lopez de Bertodano formations (Cantrill and Poole, 2005; Poole and Cantrill, 2006). These formations, which span the Campanian to Maastrichtian extend through the Cretaceous Paleogene boundary and into the Paleocene (Crame et al., 2004), record more fully marine conditions (Olivero, 2012). Leaf macrofossils are rare (except in the lower parts of the Santa Marta Formation) but wood (e.g., Poole and Francis, 2000; Poole et al., 2000a, 2000b, 2000c) and pollen (e.g., Askin, 1992) floras are better represented. Late Cretaceous (Campanian to Maastrichtian) floras have also been recorded from King George Island (Dutra and Batten, 2000) but the dates of some of these have been revised to Eocene (Nawrocki et al., 2010, 2011). The Campanian marks a period of change in the vegetation with the appearance, diversification, and rise to dominance of Nothofagaceae in both the pollen

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(Dettmann et al., 1990) and wood (Poole and Cantrill, 2006) records. By the end of the Campanian all four modern sections of Nothofagus are present. The wood flora also shows changes to the forest composition. A number of taxa present in the Conianacian and Santonian including Winteroxylon, Hedycaryoxylon tambourissioides, Sasafrasoxylon, and Illiciooxylon antarcticum together with Antarctoxylon species disappear within this interval (Cantrill and Poole, 2005) and are replaced by several species of Nothofagoxylon together with Myrceugenelloxylon and new species of Antarctoxylon (Cantrill and Poole, 2005). Conifers also show dramatic changes in this interval with the appearance of Phyllocladoxylon at the expense of other podocarp wood types. This genus increases dramatically in abundance into the Maastrichtian, all pointing to a decrease in diversity in the canopy species and a shift to a mixed Nothofagaceae/ conifer community. These forests show close affinities with the cool temperate rainforests of Valdivia where several different communities occur including (1) Lauraceae and Cunoniaceae (Eucryphia, Weinmannia, and others) with an understorey of Myrtaceae; (2) mixed Nothofagus/ Winteraceae/Podocarpaceae; and (3) higher altitude conifer (Araucariaaceae, Curpessaceae) and Nothofagus forests.

3. LATE MAASTRICHTIAN TO PALEOGENE The James Ross Basin contains a highly expanded Late Maastrichtian through Paleogene sequence exposed largely on Seymour Island where more than 1000 m of marine sediments accumulated (Crame et al., 2004; Bowman et al., 2012; Olivero, 2012). Although largely monotonous the sequence records subtle changes in sediment influx related to small scale transgressive/regressive cycles as evidenced by glauconitic horizons and hardgrounds (Crame et al., 2004). Earlier studies (e.g., Zinsmeister et al., 1989; Zinsmeister, 1998) on the marine fauna suggested turnover but no marked extinction at the Cretaceous-Paleogene boundary, but based on increased sampling and more detailed stratigraphy a marked extinction event is present with up to 61% of marine taxa disappearing at the Cretaceous-Paleogene (Witts et al., 2016). Evidence of terrestrial vegetation from the volcanic arc to the west includes spore/pollen (Dettmann and Thomson, 1987; Askin, 1988, 1990a,b, 1994; Bowman et al., 2014) and wood (Poole et al., 2000; Poole, 2002; Cantrill and Poole, 2005) floras with only sparse macrofossils (e.g., Cesari et al., 2001). Quantitative palynological analysis elucidated four climatic phases in the late Maastrichtian from cool and relatively humid with gradually increasing temperature and humidity followed by a sudden and short-lived humid event before returning to warm humid conditions just prior to the Cretaceous-Paleogene event (Bowman et al., 2014).

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Following the Cretaceous-Paleogene was a short-lived recovery phase and a return to cool and less humid conditions (Bowman et al., 2014). Bowman et al. (2014) described changes in terrestrial palynomorph abundance that document changes in vegetation leading up to and through the Cretaceous-Paleogene boundary. The three main components are P. mawsonii (Lagarostrobus), Podocarpidites (other Podocarapceae), and Nothofagidiites (Nothofagaceae). From the early Maastrichtian Nothofagaceae shows a slow decline from 20% to 30% of the flora to 10%e20% just prior to the Cretaceous-Paleogene boundary. Accompanying this decrease is a relative increase in P. mawsonii from less than 10% of the flora in the early Maastrichtian rising to a peak of 30% for a short interval (30 m) about 180 m below the boundary. P. mawsonii collapses from this peak and then recovers to be 20% just prior to the Cretaceous-Paleogene boundary. Podocarpidites remains consistently high (around 30%) except in the interval when P. mawsonii peaks. Post-Cretaceous-Paleogene Nothofagus recovers dramatically (up to 30% of the flora) while P. mawsonii and Podocarpidites occur in lower frequencies. The only other change of note is Araucariacites, which is a negligible component throughout the Maastrichtian but increases in abundance post the Cretaceous-Paleogene boundary. The warm phase recognized leading up to the Cretaceous-Paleogene boundary (Bowman et al., 2014) includes records of Palmae, although these also occur sporadically lower in the sequences (Askin, 1994). However, other thermophilic taxa only occur in this upper part of the sequence. These include Anacolsidites (Olacacaee; Askin 1989), Sapindaceae (cupanioid forms, Askin 1989, 1990), and Bombacaceae (Bowman et al., 2014). Taken together this points to floristic exchange with South America (see later). Palynofacies analysis across the Cretaceous-Paleogene boundary reveals a transgressive-regressive cycle with maximum transgression just prior to the boundary. The initial transgressive phase, as evidenced by increased marine palynomorphs, has a terrestrial flora dominated by saccate conifers presumed to represent long-distance transport from upland areas (Rodríguez-Brizuela et al., 2007). The palynofacies associated with maximum marine flooding show an increased abundance of terrestrial material including woody debris, and an increase in diversity of the terrestrial spore pollen flora. As the sea retreats from the land a decrease in terrestrial clast size occurs but diversity remains high (Rodríguez-Brizuela et al., 2007). The pulses of wood into the basin have also been studied in detail and reveal a consistent pattern (Cantrill and Poole, 2005); that is, as each transgressive cycle proceeds the wood flora shifts from angiosperm-dominated to conifer-dominated, reflecting the initial incorporation of coastal plain vegetation into the basin followed by material from the hinterland

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(Cantrill and Poole, 2005). Both studies support the idea that the coastal plain consisted of a mixed angiosperm conifer forest system while the hinterland and upland areas were richer in conifers. The only other strata of this age exposed in Antarctica are found on Fildes Peninsula (King George Island) where the Half Three Point Formation has been radiometrically dated as 71.3 Ma. This contains palynomorphs and a small macroflora (Dutra and Batten, 2000), but based on recent dating of sequence in the Admirality Bay region (Nawrocki et al., 2010, 2011) may be Eocene. The emerging picture of vegetation through the Cretaceous-Paleogene transition in Antarctica is one subtle change prior to the boundary with the sporadic incursions of thermophilic elements. This is followed by major ecosystem disruption, low extinction followed by recovery of the flora but with assembly into different compositions (Bowman et al., 2014). Typical latest Cretaceous horizons are dominated by conifer (Podocarpaceae with lower Araucariaceae) and angiosperm assemblages usually rich in Nothofaceaee. Extinction rates are generally low, although many taxa disappear for a period of time post the Cretaceous-Paleogene boundary.

4. PALEOGENE VEGETATION Paleogene floras occur in the James Ross Basin and South Shetland Islands spanning the Paleocene and Eocene interval (Cantrill and Poole, 2012). In East Antarctica glacial erratics in the McMurdo Sound region (Stillwell and Feldmann, 2000) provide limited evidence of the Eocene vegetation (Askin, 2000; Francis, 2000; Pole et al., 2000) and along the Wilkes Land margin of East Antarctica early and middle Eocene palynofloras have been recovered from offshore sediments (Pross et al., 2012; Contreras et al., 2013). Post-Cretaceous-Paleogene boundary palynology indicates an increase in araucarians and Nothofagidites (Bowman et al., 2014) and is paralleled by changes in wood abundance (Cantrill and Poole, 2005; Pujana et al., 2015). The change in composition may simply reflect an increase in volcanism on the nearby volcanic arc that favors an Araucaria/Nothofagus alliance as seen in southern South America today where vegetation dynamics are strongly controlled by volcanism (Veblen et al., 1977). Some support for this comes from the Paleocene Cross Valley Formation (a volcaniclastic unit) that contains a wood flora dominated by conifers and rich in araucarians (56%) (Pujana et al., 2015). Leaf floras also occur in the Cross Valley Formation (Dusén, 1908; Cantrill et al., 2011; Tosolini et al., 2013) but are in need of revision. Dusén (1908) recognized 87 leaf types, many based on single specimens. To date 20 of the angiosperm taxa have been examined and reduced to 14 species (Tosolini et al., 2013). However, 27 taxa referred to

Phyllites sp. along with new leaf collections are still awaiting revision. Although the material is only preserved as impressions, fine details of the venation (and teeth) are discernible suggesting the presence of Lauraceae, Winteraceae, legumes, Proteaceae, Atherospermataceae, Nothofagacaee, Cunoniaceae, ?Moraceae, ?Myricaceae, and Illiciaceae (Tosolini et al., 2013). Many of these elements are found in the southern South America Valdivian forests today. Eocene floras are also known from the Larsen Basin in the La Meseta Formation and include wood (Cantrill and Poole, 2005) and leaves. Preliminary examination of the leaf floras have yielded largely Nothofagus dominated assemblages (Case, 1988; Doktor et al., 1996). This is supported by the wood assemblages that are dominated by Nothofagoxylon and Phyllocladoxylon, with fewer Podocarpaceae and Araucaraiaceae (Cantrill and Poole, 2005). More extensive early and middle Eocene floras are known from King George Island where they occur interbedded with volcanoclastic sequences (see Cantrill and Poole, 2012, for a full summary). Again Nothofagus is ubiquitous in these assemblages but the proportion varies from assemblages that are almost pure Nothofagus to those that contain a diversity of leaf morphotypes. Hunt (2001), in an analysis of middle Eocene floras on King George Island, recognized 85 leaf morphotypes, many related to families found in southern South America today. It is thought much of the variation in the assemblages can be related to ecological responses to volcanic disturbance and succession (Poole et al., 2001). On the Wilkes Land margin a change from early Eocene paratropical to more temperate vegetation dominated by Nothofagidities (Contreras et al., 2013) has been documented. It is important to note that Nothofagus is present throughout the sequence but the lower numbers in the lower paratropical part of the sequence is thought to represent a contribution from more upland areas. In east Antarctica Eocene glacial erratics have yielded pollen from Nothofagus, Podocarpaceae (Lagarostrobus, Dacrycarpus, Dacrydium, Microcachrys), Proteaceae with minor aruacarians (Askin, 2000). This is supported by sparse leaf remains of Araucaria, Nothofagus (including seeds) and a few indeterminate angiosperm fragments (Poole et al., 2000), as well as wood of araucarians, Podocarpaceae (Phyllocladoxylon), and Nothofagoxylon (Francis, 2000). While high diversity leaf floras (in excess of 80 taxa) are known from both the Paleocene and Eocene the overwhelming composition of the flora is Nothofagus and Podocarpaceae with minor amounts of araucarians. Angiosperms were diverse during certain periods (not well constrained) or at certain stages of ecological succession and included elements that can largely be related to the cool temperate forest of southern South America today. It should

Antarctic Cretaceous Paleogene Vegetation Chapter j 27

be noted, however, that Proteaceae are not particularly well developed in South America and so this element of the fossil Antarctic flora is likely to have affinities with Australia. A marked shift to glacial sedimentation at the Eocene-Oligocene boundary marks the demise of the temperate ecosystems on the continent.

5. DISCUSSION The Early Cretaceous is a convenient point to discuss the changing pattern of plant distribution in the Southern Hemisphere. Gondwana breakup was well advanced by this time with a split between east Gondwana (Australia, Zealandia, India, east Antarctica and the blocks that make up west Antarctica) and western Gondwana (South America and Africa); a large floristic Province covering this region is recognized in the pollen record (Herngreen et al., 1996). The pollen flora is dominated by bisaccate and trisaccate pollen grains (Podocarpaceae) and a variety of fern species. The Trisaccate Province is subdivided into two subProvinces based on pollen composition with western Gondwana containing the Cyclusphaera-Classopollis subprovince and Murospora subprovince (AustraliaeIndia) (Herngreen et al., 1996). The Trisaccate Province broadly parallels Permian and Triassic Provinces based on macroflora (McLoughlin, 2001). These broad floristic regions can be further subdivided if the macroflora is considered with four regions: Indo-northern Australia, southern Australiae New Zealand, South AmericaeAntarctica (Antarctic Peninsula), and southern Africa (McLoughlin, 2001). Although a common Gondwana flora can be recognized in the Early Cretaceous internal biogeographic patterns are present due to high sea levels isolating parts of the continental landmass (e.g., Australia) and continental fragmentation isolating other regions (e.g., Africa). As Gondwana breakup proceeded into the Late Cretaceous the vegetation modernized through the appearance of angiosperms that radiated form the equatorial latitudes (Friis et al., 2011, and references therein). New floral provinciality developed with a widespread province characterized by Nothofagidites/Proteacidites in the mid to high southern latitudes including Antarctica, southern Australia, and New Zealand. Further north in southern South America and northern Australia palynofloras mixed between the Proteacidites/Nothofagidites Province and the more northerly Palmae Province are found (Herngreen et al., 1996; Vajda and Bercovici, 2014). Traces of this floral exchange can be seen in the Antarctic during warm phases when megathermal elements (e.g., Palmae) occur in the palynological record (Askin, 1994) indicating that the floral Provinces are not fixed and that radiation into and out of these regions did occur. In contrast neither India nor Africa have evidence of Nothofagidites highlighting that both regions were isolated from Antarctica by early Campanian

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times when this group appeared, and that floral exchange was not occurring. The impact of the Cretaceous-Paleogene mass extinction is muted in Antarctica with low extinction but significant changes in the composition of the vegetation postrecovery. This parallels patterns seen in southern South America where extinction is estimated at below 10% (Barreda et al., 2012). However, like the Antarctic in southern South America there was a decrease in diversity and abundance, low extinction, a Classopollis spike above the boundary and reassembly of the ecosystem albeit with different compositional abundances (Barreda et al., 2012). The best preserved Cretaceous-Paleogene boundary in the southern hemisphere occurs in New Zealand, and here a similar pattern is also found with low extinction, major ecosystem disruption, a fern spike after the event, and then a period of recovery (Vajda et al., 2001; Vajda and Raine, 2003). This Proteacidites/Nothofagidites Province continued to characterize the southern mid to high latitudes of South America, Antarctica, and Zealandia (New Zealand, New Caledonia, and regions now below sea level) through the Paleogene as evidenced by fossil floras form these regions. During periods of increased warmth such as the Middle Eocene Climate Optimum the Nothofagus alliance was pushed both southward and into higher elevations being replaced by a more widespread megathermal rainforest (e.g., coastal Wilkes Land as described by Contreras et al., 2013 or Anglesea Coal Measures flora Christophel et al., 1987), both typified today by elements of the low land tropical rainforests of eastern Australia (and New Caledonia). Nevertheless the pollen signal particularly from Nothofagus is still present in most basins indicating that during periods of warmth when megathermal rainforest invaded the low lands this taxon migrated to more upland regions. The vegetation of the Proteacidites/Nothofagidites Province included a diversity of Podocarpaceae (related to Lagarostrobus, Dacrycarpus, Dacrydium), Nothofagaceae, Proteaceae, Cunoniaceae. Components of this flora are today found in the Valdivian rainforests of Chile and the microthermal rainforests of Australia and New Zealand. Strong similarities between southern South American Eocene floras and those of Australia confirm a common history with high latitude warmth enabling Transantarctic distributions to develop (Kooyman et al., 2014). However, extinction has resulted in increased dissimilarity through time with southern South American extinction being greater than that in Australia. Eastern survival occurs in several regions as components of the Gondwana rainforests shifted into different niches (e.g., montane northern Australian and New Guinea regions) (Kooyman et al., 2014). Analysis of Australian microthermal rainforests (Nothofagus) demonstrated that they contain a larger component of Gondwana

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relicts than the northern low land tropical forests of Australia (Sniderman and Jordan, 2011). This is largely due to the immigration of Asian rainforest components into the northern low land tropics (Sniderman and Jordan, 2011) postcollision of the Australian plate with Asia. In looking for modern analogues to the Eocene floras of the southern hemisphere the diverse tropical flora from southeastern Queensland have strong parallels with the Eocene floras of southern Australia (e.g., Angelsea Christophel et al., 1987), and elements of this flora are present in Patagonia (Wilf et al., 2003, 2013) and the Oligocene of New Zealand (Lee et al., 2012, 2016a,b). This is not to say that the southeast Queensland plant communities acted as a source, but rather that is where the greatest survival of these widespread Eocene (and earlier) lineages can be found today. Different trajectories of the southern continents postEocene has seen the divergence of floristic relationships from this once more widespread biota. In Antarctica the biota decreased in diversity through the late Eocene and declined dramatically in the Oligocene, finally being expatriated in the late Miocene (post 13.8 Ma; Lewis et al., 2008; Lewis and Ashworth, 2016). In Australia the northward movement of the continent, lack of mountain building to renew soil nutrient status, and the expansion of the arid zone in the Miocene all contributed to changes in the flora (Byrne et al., 2011). In contrast New Zealand was reduced to low-lying land in the Oligocene that saw the reduction of diversity prior to the uplift of the alps and recolonization and radiation. Our current understanding of the geological development of Antarctica implies continuous land through South America and into the Antarctic Peninsula until 55 Ma (Reguero et al., 2014), after which biotic exchange was limited. This has implications for biotic exchange driven by globally warm periods when thermophilic elements are driven into high latitudes (e.g., early Eocene, Pross et al., 2012; Contreras et al., 2013) and implies that the LPTM might have been the last main period of exchange across the southern continents. It may well be that the Eocene floras of Patagonia that are rich in Australian lineages (Wilf et al., 2003, 2013) represent a survival of a widespread Paleocene lineages. Many extant angiosperm families have distributions that imply an Antarctic role in biogeographic patterns. A number of angiosperm families have basal lineages preserved in either Australia or southern South America, which has led to an out-of-Gondwana interpretation for their evolutionary radiations (e.g., Apiaceae basal clades; Calviño et al., 2016). While basal members of some groups appear to have their oldest records in Antarctica (e.g., Asteraceae, Barreda et al., 2015), and hence imply radiation out of the high southern latitudes, other recent discoveries from the Antarctic include basal lineages such

as the Nymphaeales (Notonuphar, Friis et al., 2017), but these likely represent the last survivors of more widespread Cretaceous lineages. Few Nymphaeales are known from the southern hemisphere today and in Australia they form a clade sister to Asian taxa indicating that their biogeographic distribution is more likely a result of collision between Australia and Asia and a recent radiation. Understanding these modern distribution patterns will rely on improving our knowledge of the paleogeographic evolution of Gondwana fragments and the fossil record of Antarctica, particularly in the Late Cretaceous to Paleogene.

6. CONCLUSIONS The origins of present-day southern hemisphere biogeographic patterns are founded in the Late Cretaceous through Eocene vegetation history of the region. Origin and rise to ecological dominance of modern conifers (e.g., Lagarostrobus, Dacrydium, Dacrycarpus) in the Late Cretaceous were progressively accompanied by diversification of angiosperms including lineages that are regarded as Gondwanan (e.g., Cunoniacaeae, for a fuller list see Kooyman et al., 2014). The southward expansion of warm biotas into the southern high latitudes during the Paleocene probably allowed interchange between the main landmasses but by the latest Paleocene likely separation between South America and the Antarctic Peninsula limited range expansion during Eocene warm periods. Warm periods of Earth history allowed range expansions of megathermal elements into the Antarctica and provided the opportunity for exchange between eastern and western Antarctica although questions still remain about the paleogeographic configurations.

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Chapter 26

Functional Significance of Cambial Development in Vertebraria Roots: How Do Unusual Xylem Traits Serve Life at a High Latitude? Anne-Laure Decombeix1, 2 and Nicholas P. Rowe1 1

AMAP, Université de Montpellier, Montpellier, France; 2University of Kansas, Lawrence, KS, United States

1. INTRODUCTION Interpreting the functional attributes of long extinct fossil plants is a major challenge for understanding the adaptive and ecological scenarios that have shaped plant diversity. This is particularly true for plant life forms and organizations that no longer exist or that do not have structural analogues among living species. A range of approaches has been applied for inferring functional and mechanical attributes of fossil plants (Speck and Rowe, 1998, 1999a,b), which have investigated the likely size and form of early land plants (Speck and Vogellehner, 1988, 1992, 1994, Niklas, 1990), early lignophytes (Speck and Rowe, 2003) and seed plants (Rowe et al., 1993; Speck and Rowe, 1994; Masselter et al., 2006, 2007, 2009), but also the likely maximum height of different kinds of fossil tree (Mosbrugger, 1990; Niklas, 1992, 1994; Speck and Vogellehner, 1992), the potential diversity of different growth forms and their varying mechanical architectures (Rowe and Speck, 1998; Speck and Rowe, 1999a,b) and the hydraulic functioning of stems from plants that are long extinct (Roth et al., 1994; Roth and Mosbrugger, 1996; Roth-Nebelsick et al., 2000; Rowe and Speck, 2004). Two of the advantages of applying biophysical approaches to fossil plants are that (1) physical laws and constraints on solid materials have probably not changed over geological time, and (2) the approach can readily be applied for testing hypothesesdalong with appropriate assumptionsdin a quantitative manner. Unlike with many other fossil organisms, plant fossilization as permineralized and/or petrified material often allows for preservation of

Transformative Paleobotany. https://doi.org/10.1016/B978-0-12-813012-4.00026-7 Copyright © 2018 Elsevier Inc. All rights reserved.

soft as well as resistant tissues and thus enables relatively accurate reconstructions of geometrical and three-dimensional properties. This means that both geometrical and likely mechanical properties can be reasonably inferred for testing hypotheses on the functioning of stems, leaves, and roots that have no modern counterparts. The well-known Glossopteris plexus of morpho-species represents an important floral element that is widespread during the Permian across Gondwana, including India, Southern Africa, South America, Australia, New Zealand, and Antarctica (Taylor et al., 2009). Like many fossil plants, a complete and undisputed whole plant Glossopteris reconstruction along with detailed hypotheses of its ecology and life history is unknown to date. Schopf’s pioneering studies of the Antarctic flora in the 1960s and 1970s heralded a modern era of paleobotany on that continent (Schopf, 1962, 1967, 1970) that continues to this day following the decades of fruitful research lead by Tom Taylor and colleagues. Using permineralized fossils from the Transantarctic Mountains, Schopf (1965) provided for the first time a three-dimensional reconstruction of the anatomical organization of Vertebraria roots; for a full history of the discovery and interpretations of Vertebraria see Neish et al. (1993) and Decombeix et al. (2009). Following Schopf’s analyses, subsequent studies, especially by Gould (1975) on material from Australia, culminated in a putative reconstruction of the Glossopteris plant as a moderate-sized tree growing in a temperate to cold temperate swamp environment (Gould and Delevoryas, 1977; Retallack and Dilcher, 1988). This reconstruction and

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environmental paradigm still stands as the textbook representation of the Glossopteris plant (Taylor et al., 2009). A noticeable and unusual aspect of this reconstruction is that a typical aerial vegetative system, with a solid, cylindrical woody trunk with pycnoxylic conifer-like wood, was attached to a root system that showed highly derived cambial development. This included small bar-shaped to cross-shaped to fluted, star-shaped vascular organizations in transverse section. More recent studies based on many Vertebraria samples from the Skaar Ridge assemblage in the Transantarctic Mountains (Decombeix et al., 2009) clearly demonstrate that Vertebraria root development was highly derived, complex, and probably unique among woody gymnosperms. Ontogenetic reconstruction of the cambial development showed that the cross- and star-shaped secondary xylem configurations were derived from a delayed radial closing of infrafascicular areas of the root. In other words, cambial development and tangential divisions were limited to the fascicular regions for a large part of the developmental trajectory before later radial growth finally closed the gaps, leaving behind oval spaces. Cambial development of the root system in Glossopteris was therefore very different from that of the cauline system. Previous studies (e.g., Gould, 1975) suggested that the spaces within the wood of the roots might be consistent with a gas exchange system to permit oxygen diffusion down into the root system if the plant did indeed grow in water saturated swamp conditions. However, longitudinal sections of numerous individuals (Decombeix et al., 2009) indicate that the developmentally derived, so-called airspaces are in fact closed off distally and proximally, so they would not be able to diffuse gases along any significant length or connect with aerated parts of the plant. Since the latest studies seem to indicate that the unusual organization of the Vertebraria root system is most probably not there to optimize gaseous diffusion, the real function behind the highly derived three-dimensional structure is still a mystery. The organization is all the more unusual because in our experience there are many stem systems known across many phylogenetic groups that have cross-shaped, bar-shaped, and star-shaped vascular cylinders with either primary or secondary tissues or both. This includes representatives of early land plants (Speck and Vogellehner, 1988), early lignophytes (Scheckler, 1976), many groups of Palaeozoic ferns and pre-ferns (Taylor et al., 2009), and of course extant angiosperms, particularly among mechanically flexible lianas (Caballé, 1993). However, to our knowledge, cross- or star-shaped organizations of the wood are rare or unknown in roots and so their presence in the Glossopteris plant is interesting for three reasons. First, it is notable that Permian fossils from the Transantarctic Mountains, where Vertebraria is one of the most common elements, represent some of the most ancient

high latitude forests; growth of large-bodied, woody plants thus would surely have been highly influenced by strongly seasonal environmental conditions (Cantrill and Poole, 2013). Second, the assemblages are dominated by trunks, roots, and leaves of Glossopteris (Cúneo et al., 1993), suggesting that whatever the structural-functional role(s) of this unusual stem/root combination, it was at that time one of very few large plants to have solved long-term growth and survival in this environment. Third, previous authors have noted a certain conservatism of vegetative organization compared to the diversity of fertile organs known for Glossopteris (e.g., Ryberg, 2009), perhaps further suggesting that the stem/root structure was relatively fixed among different species of Glossopteris. This could putatively represent an adaptive peak owing to strong functional constraints on the vegetative system. But what were these constraints and what were the functional attributes that permitted this stem/root organization to prevail? In this study we explore the possible functional roles of the root system in Vertebraria and discuss what significance these might have had for interpreting its growth and environment. We investigate a wide sample of Vertebraria roots from Skaar Ridge and explore potential functional attributes that would be consistent with the ontogenetic and developmental scenario described by Decombeix et al. (2009). Root function can be broadly placed into three overall groups, which include (1) mechanical anchorage, (2) absorption of water and nutrients, and (3) energy storage (Ennos, 2000). Research on root biomechanics has greatly progressed since the studies of Schopf and Gould, with recent approaches that have identified the diversity and likely complexity of root function from distal fine roots to larger structural roots and their respective roles in anchoring the plant in different environments. Such studies have now gone beyond early ideas emphasizing that root mechanical function was mostly related to tensile strength (Coutts, 1983). One area of fossil plant biomechanics developed over the last 20 years requires an ontogenetic approach whereby the gradient from young to old stages of growth can be compared and quantified (Speck and Rowe, 1999a,b). In this study we carry out a comparable ontogenetic approach for elucidating the likely functioning of Vertebraria roots. We use an expanded sampling of fossil root specimens at different developmental stages and with a variety of forms. We make quantitative measurements of cross-sectional area, of second moment of area of the vascular tissues, and we investigate how such forms vary in their optimization for rigidity compared with hypothetical forms corresponding to a typical root structure. To our knowledge it is the first time that this approach has been applied to a fossil root system. We then discuss how the geometry and likely mechanical optimization of Vertebraria might be

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consistent with high latitude wet-land environments that are highly constrained by a short growing season.

2. MATERIAL AND METHODS 2.1 Fossil Material This study is based on the observation of numerous anatomically preserved axes of Vertebraria found in silicified peat and wood from the locality of Skaar Ridge, Central Transantarctic Mountains, Antarctica (84 49919.10S, 163 20928.00E; 2289 m elevation). The Skaar Ridge silicified peat appears to be derived from small lenses or possibly fluvially rafted mats of peat associated with volcaniclastic sediments (Taylor et al., 1989; McManus et al., 2002). At the site, the fossil peat occurs as black to dark brown siliceous blocks scattered among dolerite boulders in lowrelief hummocks. The abundant Vertebraria axes within the blocks are especially conspicuous thanks to the contrast between the white infilling of the spaces in their wood structure and the rest of the block. The plant remains found in the peat blocks are largely dominated by glossopterid organs, with Vertebraria and Glossopteris leaves being the most common. The Skaar Ridge silicified peat occurs within the Buckley Formation of the Beacon Supergroup and is considered to be Late Permian in age, based on palynomorphs and associated compression floras (Farabee et al., 1991). For this study, we used scanned acetate peels (Galtier and Phillips, 1999) of the surface of blocks #10947 (slices A, B, C, D1, D3); 11154 (A, C, D, E, F, G); 11198A; 11309D; 11654; 11155 (B, C) to select a diversity of 10e20 mm wide Vertebraria roots with various protoxylem configurations. We cannot be sure whether all the roots belong to the same genus/species of glossopterid, but a similar diversity of protoxylem configuration is known to occur within a single root system in extant plants (e.g., Wang et al., 1994). Line drawings of 40 of these roots (Fig. 26.1) were used to make measurements of diameter, cross-sectional area, and axial second moment of area. In addition, we used the slides mounted for the Decombeix et al. (2009) study to make additional observations and measurements, including measurements of wood cells. These slides were made from peat blocks #11324, 11642, 11645, 11648, 11654, 15479, 15491, 15529, 15542, 15549, 15630, 15695, 15855, CB44, and CB461, and have the accession numbers 23150e23256 and 26367e26373. Additional information was also provided by thin sections (Hass and Rowe, 1999) made from a silicified trunk (#17918) with roots growing inside the wood. All of these specimens, peels, and slides are deposited in the Paleobotanical Collections, Natural History Museum and Biodiversity Research Center, University of Kansas. In addition to scanned peels (Plates I, 1,12 and II, 1), digital images appearing in Plates I and II of this chapter

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were taken using a Sony XCDU100CR digital camera attached to an Olympus BX51 compound microscope (Plate I, 4 and 5) or a Leica DC500 digital camera attachment on a Leica DM5000B compound microscope (all other images). Plates were composed with Adobe Photoshop CS5 version 12.0 (Adobe Systems, San José, California, USA). Transformations made in Photoshop include cropping, rotation, and adjustment of brightness and contrast for the whole image. Cell measurements were made using ImageJ software (Schneider et al., 2012).

2.2 Maximal Diameter and Cross-Sectional Area Maximal diameter (d) (mm) and surface area (A) (mm2) calculations were carried out for all secondary xylem configurations. Surface area measurements were then used to compute how maximal diameter of bar-shaped, crossshaped, star-shaped, and entire configurations compared with maximal diameters of equivalent surface areas based on a circular cross section largely characteristic of most woody plant roots. Since root diameter is known to play a role in facilitating root penetration at the root apex (Abdalla et al., 1969; Materechera et al., 1991), our main aim was to see whether the geometrical configurations we observed would significantly increase stem diameter compared to simple circular sections.

2.3 Second Moment of Area Second moment of area (I) is a geometrical property of a beam in bending that describes the amount of crosssectional area and its distance from the centroid and neutral axis of a beam in bending (Niklas, 1992; Ennos, 2012). In general, material that is placed further away from the center of the section is exponentially more effective at resisting bending forces. In plants, the geometric positioning of plant tissues within the stem, leaf, and root to best increase or reduce rigidity has been a keystone trait during the course of vascular plant evolution (Niklas, 1992; Rowe and Speck, 2004). Digitized line drawings of root cross sections were orientated so that the widest axis of the vascular cross section was orientated parallel to the vertical y-axis. The image processing software OPTIMAS plug-in t_inertie (developed by T. Almeras, Montpellier; for further details contact N. Rowe) (Paul-Victor and Rowe, 2011) was then used to calculate the second moment of area (I) (mm4) of the root secondary xylem. We calculated the mean second moment of area (Iy þ Ix)/2 of the variable cross-sectional shapes and entire root configurations where Iy and Ix represent the two orthogonal orientations of the overall root cross section. The approach applied here quantifies only the secondary xylem component of the root cross sections since our

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FIGURE 26.1 Line drawings of the vascular system in cross section in 40 young Vertebraria roots illustrating the diversity of shapes generated in the young developmental stages by the discontinuous cambial activity. Specimens are ordered vertically by increasing number of protoxylem strands in the primary structure (2e8) and horizontally by increasing diameter. Note that #14 is a root with four primary xylem strands like #15, but the structure is obscured by a trace to a lateral that fills the space between two of the arms. Drawings made from scanned peels of blocks 10947 (slices A, B, C, D1, D3); 11154 (A, C, D, E, F, G); 11198A; 11309D; 11654; 11155 (B, C). Scale bar ¼ 1 cm.

observations indicate that remaining tissues were thin-walled cortex and/or parenchyma and phloem and would thus offer little to the mechanical rigidity of the cross section. The direct approach that we use differs from previous studies in which centrisymmetrical models were first constructed for entire stem cross sections (Speck and Rowe, 2003). The Skaar Ridge material represents a silicified soil and swamp matrix and all the roots we inspected showed little distortion or deformation. We therefore preferred to measure second moment of area of the root sections as they were preserved and simply measure the maximum value and that orthogonally to it. In addition, we suspect that different arm-lengths and orientations of the

vascular tissue correspond to adaptive growth of the root in a heterogeneous matrix and thus we believe that approximations of second moment of area for a given volume of tissue would be better reflected for the unmodeled sections. Values of second moment of area were used to compare the bending efficiency of the different cross-section configurations represented by bar-shaped, cross-shaped, and star-shaped sections. We compared to what extent these cross-sectional shapes showed increased second moments of areas compared to circular cross sections of more typical woody roots. Overall, we aimed to test to what extent delayed interfascicular cambial development would have affected the

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PLATE I (1) General view of a surface of a silicified peat block showing several Vertebraria roots about 10e20 mm in diameter with various cross-sectional shapes. Note the different geometry between a diarch root (upper left, D) and the polyarch ones (right). Scanned peel of peat block 11198. Scale bar ¼ 1 cm.

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geometrical factor contributing to root rigidity for a given cross-sectional area and for the relative cost of woody tissue biomass. A second aim was to evaluate how second moment of area changed from young to old root segments and whether (1) the values were optimized in young roots for rapid development of rigidity above the root apex for soil penetration and (2) whether second moment of area was optimized for higher rigidity in older portions of root that were closer to the stem/root transition and thus probably needed to be optimized for compressive and bending forces rather than being purely resistant in tension.

3. RESULTS 3.1 Matrix Vertebraria roots are a main component of most peat blocks from Skaar Ridge. The roots are densely distributed in the matrix and oriented in all directions. In addition to roots occurring freely in the matrix or among degraded organic matter (Plate I, 1 and 2), young specimens are also abundant inside other Vertebraria roots (e.g., Plate I, 3) in the spaces between the woody arms. In addition, we observed several examples of roots growing inside wood fragments, including a portion of trunk (Plate I, 4 and 5). The anatomy of the trunk shows an Australoxylon type of wood, typical of the Glossopteris stems and roots found at Skaar Ridge.

3.2 Ontogeny The observed roots have a variety of protoxylem configurations, ranging from diarch to roots with eight protoxylem strands (Plate I; Fig. 26.1). Secondary xylem is produced in the zones between these protoxylem poles and the cambium remains discontinuous, giving the characteristic shapes of Vertebraria. The variation of the number of protoxylem strands leads to an additional variety of cross-sectional shapes in young stages of development (Plate I; Fig. 26.1). Diarch roots develop two fan-shaped wedges of wood that

give them a strong bilateral symmetry (e.g., Plate I, 1, 2, and 6). Roots with higher numbers of protoxylem strands (3e8) are star-shaped. They tend to have a radial symmetry although wood development is often unequal between the different arms (Plate I, 11). In most cases, the width of the arms does not increase significantly in polyarch roots, and the arms remain radially slender, unlike the broader fan-like cross sections of the bilateral ones. Adjacent arms of the star-shaped wood cross sections are occasionally interconnected when a trace to a lateral root is produced in the zone facing a protoxylem strand (Plate I, 2; Fig. 26.1 root #14). In the earliest stages of root development parenchymatous tissue is present between the developing arms of wood (Plate I, 8), which later in development, shows signs of mechanical straining (Plate I, 3). Since primary-formed parenchymatous tissue in the infrafascicular regions is fixed and does not undergo compensatory divisions to keep pace with the secondary growth of the arms, the tissue inevitably strains and fails forming open spaces (Plate I, 9 and 11). The voided areas between the arms therefore represent actual voids during the development of the root rather than representing nonpreserved soft tissue. In later developmental stages, the vascular cambium becomes continuous around the entire circumference of the axis (Plate I, 12). This does not seem to be correlated with root diameter and does not always take place simultaneously around a given axis, as attested by specimens that are not entirely surrounded by a ring of wood (Fig. 26.1). Once wood has been produced all around the axis, the cross-sectional organization is transformed from a star-shaped organization to an entire circular one that encloses the oval-shaped voids. Besides the change in geometry the overall ratio of wood to void space therefore changes significantly from young to old stages of development (Plate I, 12). Young roots are surrounded by a parenchymatous cortex; in older specimens there is a thin periderm (Plate I, 3, 9, and 11). This tends to form around the outside contour of the xylem arms rather than as an approximately circular area surrounding them. As a result the entire cross section

=(2) Portion of peat with younger roots than in 1, a diarch (top left) and a tetrarch one (bottom right). The two upper arms of the tetrarch root are still partly connected (arrow) following the emission of lateral roots visible just above. Peat block 15695. Scale bar ¼ 200 mm. (3) Young triarch Vertebraria with little development of secondary tissues and a younger root (R) growing between two of the arms of wood. Peat block 15491. Scale bar ¼ 200 mm. (4) Young Vertebraria roots (arrows) growing inside the wood of a trunk (T). Block 17918. Scale bar ¼ 2 mm. (5) Detail of a young Vertebraria root with six arms showing the deformation of the surrounding trunk wood (T). Block 17918. Scale bar ¼ 500 mm. (6) Detail of a young diarch root showing a strong bilateral symmetry and unequal development of the wood. Peat block 15695. Scale bar ¼ 200 mm. (7) Very young tetrarch root with a cross-shaped primary xylem and no secondary tissues. Peat block 15491. Scale bar ¼ 200 mm. (8) Tetrarch root just starting to produce secondary xylem, also showing how the space between the arms is not initially empty but filled with parenchymatous tissue. Peat block 15491. Scale bar ¼ 200 mm. (9) Slightly older tetrarch root illustrating how the secondary xylem repeats the shape of the primary xylem (compare to 7). Note the very different symmetry with 3. Peat block 15491 Scale bar ¼ 200 mm. (10) Young pentarch root with a little amount of wood. Peat block 15491. Scale bar ¼ 200 mm. (11) Slightly older pentarch root showing how the arms tend to retain the same tangential width but can reach different radial lengths, leading to an asymmetrical shape. Peat block 15491. Scale bar ¼ 200 mm. (12) Detail of the central part of a very old pentarch root in which the cambium has produced continuous layers of wood around the star-shaped central part. Note the extreme difference in tissue distribution between the two stages of development. Peat block CB461. Scale bar ¼ 5 mm. C, cortex; D, diarch root; P, periderm; R, rootlet; T, trunk wood; X1, primary xylem; X2, secondary xylem.

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PLATE II (1) Detail of one of the woody arms in the central part of the old root illustrated on Plate I, 12. Peat block CB461. Scale bar ¼ 1 mm. (2) Detail of the secondary xylem in cross section in the inner part of a large root. Peat block 11648. Scale bar ¼ 25 mm. (3) Detail of the secondary xylem in cross section in the outer part of a large root. Peat block 11648. Scale bar ¼ 25 mm.

tends to be approximately star-shaped, in keeping with the outline of the vascular tissue.

3.3 Cross-Sectional Area and Root Diameter in Young Roots The maximal diameters of young Vertebraria roots, 10e20 mm in diameter, were compared to hypothetical circular roots having the same cross-sectional area. For the 40 young specimens illustrated in Fig. 26.1, maximal diameter varies from 6% to 45% greater for a given Vertebraria root

section compared with an equivalent circular model, showing an average gain of 28% (Figs. 26.2 and 26.3). Gains above 40% were observed in roots with four, five, and six arms, while the lowest gain was among diarch and triarch roots. Low gains were also observed in tetrarch roots in which continuous production of wood and tangential closing off of spaces started (Fig. 26.3). This is readily seen, for example, in a comparison of two tetrarch roots with the same diameter (roots #13 and 14 in Fig. 26.1 and Fig. 26.3). One root section (root 13) with entirely free xylem arms has a diameter gain of 45% compared to a circular model. The

FIGURE 26.2 Diameter of the 40 Vertebraria roots in Fig. 26.1 (black) showing the increase in diameter compared to hypothetical normal roots with a circular cross-sectional area (gray).

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FIGURE 26.3 Differences in tissue distribution between the 40 Vertebraria illustrated in Fig. 26.1 and classical, full cylinder roots. Black bars represent the loss in wood cross-sectional area compared to hypothetical classical roots with a same diameter. Gray bars represent the gain in diameter compared to hypothetical normal roots with a same cross-sectional area. Asterisks indicate roots with a closed cambium. Arrows indicate two roots with the same diameter.

second root section (root 14), in which infrafascicular development is producing xylem tissue between xylem arms, shows a gain in diameter of only 17% compared to a circular model. Overall, in terms of diameter optimization, results indicate that diameter optimization for a given crosssectional area of wood tended to be highest in relatively early stages of growth and for sections developing several slender xylem arms (Fig. 26.3).

3.4 Second Moment of Area Axial second moment of area (I) varies significantly between different sizes and shapes of Vertebraria roots illustrated in Fig. 26.1 (Fig. 26.4). Diarch roots show a strong difference between Ix and Iy, reflecting their strong bilateral symmetry and an optimization for increased rigidity in one direction. When compared with hypothetical circular roots having the same cross-sectional area, all Vertebraria roots show a gain in average second moment of area (Fig. 26.5) and on average are 44.5% higher than an equivalent circular section. For a given cross-sectional area of wood produced, root rigidity is thus increased in Vertebraria. Roots in which the cambium has started to close have higher values of I than those in which the wood production is still discontinuous. Comparing two tetrarch roots with the same

diameter (13 and 14 of Fig. 26.1), the root with an entirely free xylem arms has an average I of 4575 mm4, while the one with closed cambium has an average I that is a little over twice that value (9906 mm4).

3.5 Wood Anatomy Secondary xylem of all the root specimens observed is composed only of tracheids and parenchymatous rays (Plate II, 1e3). The latter are relatively sparsely distributed in tangential sections, 1e10 cells high and typically uniseriate. About 70% of rays observed in tangential section are composed of only a single cell. Tracheids have mixed pitting on their radial walls typical of the wood morphotype known as Australoxylon (Marguerier, 1973) characterized by araucarian, abietinean, and spaced pits. Measurements of 300 tracheids in 11 specimens show an average diameter of 21 mm (radial)  20 mm (tangential), with a wall thickness of 1.6 mm. Average tracheid diameter varies between specimens, from 12 to 35 mm, as does wall thickness, from 1 to 3.5 mm. Measurements on later developmental stages show no significant differences in tracheid diameter and wall thickness between the wood of the inner arms (Plate II, 2) and that of the later formed wood that joins up the xylem arms across the infrafascicular spaces (Plate II, 3). The mean ratio of double wall thickness to lumen diameter measured on 11 specimens 10e20 mm in

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FIGURE 26.4 Second moment of area (I) in the 40 Vertebraria illustrated in Fig. 26.1. Black bars represent Iy (mm4) and gray bar Ix (mm4). Asterisks indicate roots with a closed cambium. Arrows indicate two roots with the same diameter.

FIGURE 26.5 Gain in average second moment of area in the 40 Vertebraria specimens illustrated in Fig. 26.1 compared to hypothetical roots having equivalent cross-sectional areas but with a circular outline in transverse section. Asterisks indicate roots with a closed cambium.

diameter is 0.15 (0.12e0.2). When compared to the values found by Pittermann et al. (2006) for the wood of small (8e12 mm) stems and roots of extant conifer, the values for Vertebraria fall within the range of root wood, typically lighter than that of corresponding stems (Fig. 26.6). This light wood structure is also found in the outside part of two very large roots from Skaar Ridge, one with closed airspaces (#CB461) and one with open arms (#CB447). In these two specimens the ratio is 0.16 and 0.17, respectively, indicating that even large specimens keep this typical light structure in the outer wood.

moment of area and stem rigidity compared with a circular wood cylinder (Figs. 26.2 and 26.5). In terms of hydraulic conductivity, theoretical values would remain the same whether the wood cross-sectional area is comprised of xylem arms or a circular geometry. However, the results show that theoretical conductance would increase following tangential wood formation in the later stages of growth for correspondingly little increase in stem diameter.

4. DISCUSSION

3.6 Hydraulics/Surface

4.1 Implications of a Derived Cambial Development

The cross-sectional geometries of wood in young stages of Vertebraria show an increased diameter and second

The derived vascular cambium present in Vertebraria resulted in a complex geometrical organization that likely

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FIGURE 26.6 Ratio of double wall thickness versus lumen diameter in Vertebraria (asterisk) compared to several extant conifer roots (lowercase names) and stems (uppercase names). aa/AA, Agathis australiana; AI, Araucaria laubenfelsii; CO, Juniperus osteosperma; cq/CQ, Sequoia sempervirens; CS, Juniperus scopulorum; ct/CT, Taxodium distichum; OP, Prumnopitys ferruginea; OR, Retrophyllum minor; pa/PA, Abies lasiocarpa; pc, Pinus caribea; pe/PE, Picea engelmanii; pm/PM, Pinus monophylla; Pr, Picea mariana. Extant data from Pittermann et al. (2006).

had a significant effect on the functional biology and life history of the whole Glossopteris plant. The ensemble of developmental motifs behind this structural organization in Vertebraria is a remarkable example of how simple changes in developmental timing can lead to (1) a strong departure from a typical anatomical structure, (2) a wide diversity of geometries and shapes between developmental stages, and (3) potentially major changes in mechanical and hydraulic functioning between young and old stages and from the distal to proximal parts of the root system. So just what are the functional implications of these changes? How can they be interpreted at the level of the whole plant? And to what extent can they represent adaptations for life in high-latitude wetlands in the Palaeozoic?

4.2 Comparisons With Typical Gymnosperm Roots: Cylinders Versus StarShaped Cross Sections The star-shaped cross sections of young stages means that for a similar area and volume and physiological cost of wood tissue produced, Vertebraria roots reached a larger diameter (of mechanically resistant tissue) than a full cylinder root. In other words, a given root diameter can

be achieved with a smaller amount of biomass invested, allowing a cheaper increase in size of the young roots. This strategy can have key implications for the spatial and temporal establishment of the root system. A large diameter reduces soil resistance in front of the root apex and facilitates the opening of the matrix at the apex (Abdalla et al., 1969; Materechera et al., 1991; Clark et al., 2003). In the case of young Vertebraria, this phase of exploration and growth in length can be completed with less biomass invested per individual root. A larger root diameter also provides better anchorage behind the growing zone (Clark et al., 2003). Of course, we are unsure of the exact position of the earliest stages of growth in relation to the actual growing apex. In very early stages of root growth, parenchymatous tissue and cortex constitute a large portion of the cross-sectional area (e.g., Plate I, 8). Our observations suggest that the subsequent mechanical straining, tissue collapse, and voiding of tissue in infrafascicular areas would remove hydrostatic support around the relatively slender xylem arms (e.g., Plate I, 9 and 11). This suggests that xylem arms would probably only adequately withstand compression and bending forces that were relatively weak at each given point along a given xylem arm. It must also be noted that the structure was punctually reinforced by the

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transverse structures corresponding to vascular traces to lateral roots (Plate I, 2).

4.3 Rapid Establishment in Perturbed Environments Another implication of the young Vertebraria structure is that a given root diameter could be achieved more rapidly than in a typical cylindrical root, allowing a more rapid establishment. Such a strategy can be found in cases of competition and/or constrained environmental conditions. For example, seedlings of extant bald cypress (Conner et al., 1986) as well as trees living in flooded Amazonian forests (de Oliveira Wittmann et al., 2010 and references therein) must grow fast enough after germination to keep at least part of their crowns above floodwaters for the rest of the growing season. Conversely, in some Salicaceae a rapid root expansion allows seedlings to keep pace with a falling water table (Karrenberg et al., 2002). While in the case of the Vertebraria from Skaar Ridge we have no information about possible variations in water level, the strong seasonality of their high-latitude/polar environment must have put strong temporal constraints on plant establishment and growth.

4.4 Significance of In Situ Growth in a Wood Matrix The observations of new Vertebraria specimens found growing within a trunk fragment (Plate I, 4 and 5) clearly show how the arms of Vertebraria xylem are radially deforming the surrounding wood, rather like an expansion rawl plug or like the anchors with various numbers of expandable lobes that are used, for example, to put power line poles in unstable soils. This demonstrates that the starshaped configurations were capable of forcing openings in a wood matrix and likely provided good anchorage. The arms of these cross-shaped young roots were probably at risk of deforming, particularly in the development time between the loss of the hydrostatic support of the interarm parenchyma and the development of the full circumference of wood in later stages. Despite this, these in situ examples clearly demonstrate that small-scale roots were capable of invading what is probably softened or mushy wood within the soil or swamp matrix.

4.5 Developmental Motifs Underlying Diverse Cross-Sectional Geometries The pronounced cross-shaped and star-shaped vascular systems of young Vertebraria roots without a doubt influenced a range of functional processes. Roots of many phylogenetically diverse species typically develop a starshaped configuration of primary vascular tissues and, in

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many extant taxa, as in Vertebraria, variations in protoxylem strand number between different axes of the root system are common (e.g., Wilcox, 1962a,b; Wang et al., 1994, and references therein). Most roots, however, develop a continuous cambium very early in ontogeny, with the result that secondary growth obscures the initial star-shape to form a more-or-less cylindrical outline in transverse section. In Vertebraria on the other hand, bilaterally symmetrical, diarch xylem and radial star-shaped secondary xylem tissue develops, and the shape of the primary xylem is retained during early secondary growth. In young roots where secondary growth was just starting, the double star-shape of primary and secondary xylem led to an increased number of lobes of vascular tissues that might have provided increased strength to the structure. More generally, this developmental template not only ensures complex geometries well after the onset of secondary growth, but can also result in differential radial growth between different xylem arms (e.g., Plate I, 9 and 11). We think that this is likely to provide functional plasticity in terms of physical contact with the surrounding matrix.

4.6 Higher Mechanical Stability Toward the Stem Base Older developmental stages of Vertebraria possess, in terms of geometry, a potentially more rigid structure. The continuity of the vascular cambium around the axis reinforces it by strut-like interconnections between the arms, which then thicken, surely providing more rigidity to the root. Since the outermost tissues provide the more rigidity because of their higher second moment of area, the empty spaces left in the center of the axis by the discontinuous cambium stage are not mechanically significant for these older roots. This change in rigidity in later developmental stages is consistent with a role of mechanical support, closer to the base of a self-supporting tree. Such structures would therefore accommodate the increasing need for resisting compression and bending forces at the base of the growing Glossopteris plant.

4.7 Marked Homogeneous Wood Structure at the Cellular Level While its geometry is unique, the analysis of the secondary xylem of Vertebraria at the cellular level does not show any notable peculiarity. The pycnoxylic wood with narrow, low rays is very similar to that of extant conifers. Apart from the small difference in pitting on the radial wall of the tracheids (mixed vs. araucarian), the wood of Vertebraria is similar to Agathoxylon (¼Araucarioxylon; see Rößler et al., 2014), a plesiomorphic type of wood found in a large range of woody taxa from the Devonian to the present. Mean tracheid diameter measured in Vertebraria is within the typical

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10e40 mm range observed in extant conifer wood (e.g., Sperry et al., 2006). The ratio of tracheid wall thickness to lumen diameter also falls within the range observed in extant conifer roots, which is typically smaller than in corresponding stems (Fig. 6; Pittermann et al., 2006). Given all these qualitative and quantitative similarities in wood anatomy, it appears that the differences between Vertebraria and a typical gymnosperm root only take place at a higher level of organization; that is, the only specificity of the Vertebraria secondary vascular system is the delayed occurrence of cambium continuity around the axis.

4.8 Changing Properties Through Development Young stages of Vertebraria roots may be referred to as having a light architecture, where less biomass is invested than in a classic root for a given diameter and furthermore, is more optimized for higher rigidity. In terms of potential constraints on a given biomass allocation, this would likely favor more rapid growth and faster initial establishment growth of the root system. In addition, slender, crossshaped, and star-shaped organizations would be sufficiently rigid in a soft mushy matrix since they can grow through pycnoxylic wood tissue in the peat matrix. In a second stage, the closing of the xylem arm configuration by the cambium changes the distribution of tissues, leading to a stronger, more hydraulically efficient structure, comparable to that of a typical root. What caused that change? We hypothesize that as the root system became established, mechanical and/or physiological factors at the scale of the whole plant triggered the transition to the production of a continuous wood cylinder in the roots. This would be consistent with the variability observed in the time of closing of the cambium as well as the fact that it occurs independently of other ontogenetically defined traits including root diameter and protoxylem configuration. So how does this unique developmental trajectory of the roots fit with the environment and growth conditions reconstructed for the Skaar Ridge glossopterid trees?

4.9 The Swamp Hypothesis A number of geometrical and mechanical traits we have considered for Vertebraria are consistent with growth in a peat swamp or mire and in conditions demanding rapid growth in a short growing season. We list three potentially key functional traits that we infer as being adapted to life in a wetland environment with a short growing season. 1. Light architecturedrapid establishmentdlow cost Early root growth with slender xylem arms probably only resisted relatively small bending forces before deformation of the arms themselves. This is consistent

with growth in a soft or mushy soil matrix such as peat or the decomposing/water saturated dead wood produced by successive generations of plants. The production of light-structured fine roots is also consistent with a soft matrix soil since it is more efficient for a plant to have an anchoring system based on many light roots rather than fewer mechanically robust roots. If the matrix is weak, it would be a false economy to develop overly strong roots since the matrix would mechanically fail under low to medium loads. This scenario is consistent with the light architecture of the young roots, with a reduced biomass per given diameter compared with circular root geometries of more robust forms with higher proportions of mechanical tissue. The strong reduction in wood cross-sectional surface for a given diameter means that about twice the length/number of roots could be produced for a given amount of biomass, allowing the plant to allocate resources into the production of more, lighter roots and a longer and/or denser root network. These properties of young Vertebraria roots are also consistent with growth in a strong seasonal climate in which the plants would have to establish quickly during the favorable season. With a comparable investment in biomass there are more roots produced for anchorage and/or exploration of the matrix, allowing a faster establishment of young individuals. 2. I-beam organization of roots conferring stability Root ontogeny also leads to the formation of roots with a bilateral geometry. This is similar to the I-beam-like organization of buttress roots that develop around the base of the trunk in many extant trees. Extant conifer roots growing on peaty soils tend to develop such roots with an I-beam shape by asymmetrical development of the secondary xylem (Büsgen and Münch, 1929). North American conifer species growing in Sphagnum moss in wet conditions (Rigg and Harrar, 1931) are known to develop bilaterally symmetrical roots comparable to I-beams. Scots pine (Pinus sylvestris L.), lodgepole pine (Pinus contorta Dougl.), birch (Betula sp.), oak (Quercus sp.), and Sitka spruce (Picea sitchensis (Bong.) Carr.) growing on waterlogged peat in the British uplands are also all known to produce I-beamlike roots (Nicoll et al., 2006). Such a strategy implies that Glossopteris produced a lot of fine roots, a fact that is consistent with the huge amount of these roots found in the permineralized peat at Skaar Ridge but also in the Prince Charles Mountains (Slater et al., 2015). 3. Feedback and interaction between (1) light architecture, (2) weak and heterogeneous matrix, and (3) smart anchorage: Implications for biomimetics The abundance of Glossopteris plant remains in the Permian peat deposits of Antarctica points to the

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likelihood that the Glossopteris plant was by far the most dominant element of the polar peat swamp forests. We suspect that Glossopteris roots of Vertebraria are present in large numbers in many sites simply because they were present in large numbers in life and were particularly well adapted to anchoring in a soft and almost certainly heterogeneous matrix. We suspect that dominance by the Glossopteris plant was at least partly mediated by its highly efficient rooting system in weak possibly unstable, organic rich soils, which was in fact largely composed of light-structured rooting structures. Finally, we also suspect that differential xylem-armlength development served as an efficient anchoring device in heterogeneous weakly cemented soils. In compact homogeneous soils, roots with circular cross sections might provide an optimal surface closure with the surrounding matrix. However, in weak and highly heterogeneous soils, cross-shaped and star-shaped forms with adaptive arm elongation would offer better contact and anchorage within irregular spaces in the soil. Root functioning, in particular root diameter increase to optimize root penetration, has recently been used as a model for biomimetic applications for optimizing tunneling devices in sediments (Sadeghi et al., 2014). The example of Vertebraria potentially offers one of a few examples of potential biomimetic applications from fossil plants. In this case, adaptive enlargement of a lobed structure might be abstracted for optimizing anchoring devices in heterogeneous, weak substrates.

5. CONCLUSION Perhaps to the chagrin of many of us who have had the privilege to search for plant fossils in the Late Permian sediments of Antarctica, fossil roots of Vertebraria are among some of the most common and abundant of plant fossils. An exchange between field workers such as “what have you got over there in that block guys?”. “Oh nothing mate, just a bunch more Vertebraria” has possibly rung out over the ice and crags many times over the years. The functional relationship of these roots with the apparently unremarkable, dense, woody trunks and branches of the Glossopteris has always been something of a mystery. This study on the geometry and functional mechanics of Vertebraria was initially suggested by Tom Taylor, who had a deep curiosity for what this peculiar organization actually meant. As Tom suspected, our new observations suggest that Vertebraria fossils are anything but an uninteresting root fossil to be put aside for later. Their light architecture and specialized organization for rapid growth took place at a low physiological cost and high anchoring potential. This possibly explains how moderate-sized self-supporting woody plants at high

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latitudes managed to develop and maintain an anchoring system via a relatively simple developmental modification of cambial activity. Furthermore, we speculate that the production of an abundant light-structured rooting system possibly provided a feedback loop where soils of light heterogeneous matrix largely composed of Glossopteris roots could only be effectively colonized by more of the samedVertebraria roots. Finally we subscribe to the view that lightly built, directionally adaptable, cross-shaped and star-shaped wood symmetries of Vertebraria potentially provide an interesting model for the abstraction of adaptive biomimetic anchoring devices in weak and heterogeneous substrates.

ACKNOWLEDGMENTS Rudy Serbet (University of Kansas, Lawrence) patiently scanned and sent images of peel sections. Dorothée Letellier (Montpellier) prepared the thin-sections of the trunk colonized by young roots. We also thank three anonymous reviewers for their detailed and helpful comments. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. The material used in this study was collected over several Antarctic expeditions led by Thomas N. Taylor and/or Edith L. Taylor and funded by NSF grants. The authors are honored to have had the chance to be part of some of these unique opportunities to collect in Antarctica and to study this material.

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