The Terrestrialization Process: Modelling Complex Interactions at the Biosphere-Geosphere Interface (Geological Society Special Publication 339)

The Terrestrialization Process: Modelling Complex Interactions at the Biosphere– Geosphere Interface The Geological S...

Author: M. Vecoli | G. Clément | B. Meyer-Berthaud

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The Terrestrialization Process: Modelling Complex Interactions at the Biosphere– Geosphere Interface

The Geological Society of London Books Editorial Committee Chief Editor

BOB PANKHURST (UK) Society Books Editors

JOHN GREGORY (UK) JIM GRIFFITHS (UK) JOHN HOWE (UK) RICK LAW (USA) PHIL LEAT (UK) NICK ROBINS (UK) RANDELL STEPHENSON (UK) Society Books Advisors

MIKE BROWN (USA) ERIC BUFFETAUT (FRANCE ) JONATHAN CRAIG (ITALY ) RETO GIERE´ (GERMANY ) TOM MC CANN (GERMANY ) DOUG STEAD (CANADA ) MAARTEN DE WIT (SOUTH AFRICA )

Geological Society books refereeing procedures The Society makes every effort to ensure that the scientific and production quality of its books matches that of its journals. Since 1997, all book proposals have been refereed by specialist reviewers as well as by the Society’s Books Editorial Committee. If the referees identify weaknesses in the proposal, these must be addressed before the proposal is accepted. Once the book is accepted, the Society Book Editors ensure that the volume editors follow strict guidelines on refereeing and quality control. We insist that individual papers can only be accepted after satisfactory review by two independent referees. The questions on the review forms are similar to those for Journal of the Geological Society. The referees’ forms and comments must be available to the Society’s Book Editors on request. Although many of the books result from meetings, the editors are expected to commission papers that were not presented at the meeting to ensure that the book provides a balanced coverage of the subject. Being accepted for presentation at the meeting does not guarantee inclusion in the book. More information about submitting a proposal and producing a book for the Society can be found on its web site: www.geolsoc.org.uk. It is recommended that reference to all or part of this book should be made in one of the following ways: VECOLI , M., CLE´ MENT , G. & MEYER -B ERTHAUD , B. (eds) 2010. The Terrestrialization Process: Modelling Complex Interactions at the Biosphere–Geosphere Interface. Geological Society, London, Special Publications, 339. BLIECK , A., CLE´ MENT , G. & STREEL , M. 2010. The biostratigraphical distribution of earliest tetrapods (Late Devonian): a revised version with comments on biodiversification. In: VECOLI , M., CLE´ MENT , G. & MEYER -B ERTHAUD , B. (eds). The Terrestrialization Process: Modelling Complex Interactions at the Biosphere–Geosphere Interface. Geological Society, London, Special Publications, 339, 129– 138.

GEOLOGICAL SOCIETY SPECIAL PUBLICATION NO. 339

The Terrestrialization Process: Modelling Complex Interactions at the Biosphere – Geosphere Interface

EDITED BY

M. VECOLI Universite´ Lille, France

G. CLE´MENT Museúm national d’Histoire naturelle (MNHN), France

and B. MEYER-BERTHAUD UMR AMAP (botAnique et bioinforMatique de l’Architecture des Plantes), France

2010 Published by The Geological Society London

THE GEOLOGICAL SOCIETY The Geological Society of London (GSL) was founded in 1807. It is the oldest national geological society in the world and the largest in Europe. It was incorporated under Royal Charter in 1825 and is Registered Charity 210161. The Society is the UK national learned and professional society for geology with a worldwide Fellowship (FGS) of over 9000. The Society has the power to confer Chartered status on suitably qualified Fellows, and about 2000 of the Fellowship carry the title (CGeol). Chartered Geologists may also obtain the equivalent European title, European Geologist (EurGeol). One fifth of the Society’s fellowship resides outside the UK. To find out more about the Society, log on to www.geolsoc.org.uk. The Geological Society Publishing House (Bath, UK) produces the Society’s international journals and books, and acts as European distributor for selected publications of the American Association of Petroleum Geologists (AAPG), the Indonesian Petroleum Association (IPA), the Geological Society of America (GSA), the Society for Sedimentary Geology (SEPM) and the Geologists’ Association (GA). Joint marketing agreements ensure that GSL Fellows may purchase these societies’ publications at a discount. The Society’s online bookshop (accessible from www.geolsoc.org.uk) offers secure book purchasing with your credit or debit card. To find out about joining the Society and benefiting from substantial discounts on publications of GSL and other societies worldwide, consult www.geolsoc.org.uk, or contact the Fellowship Department at: The Geological Society, Burlington House, Piccadilly, London W1J 0BG: Tel. þ44 (0)20 7434 9944; Fax þ44 (0)20 7439 8975; E-mail: [email protected]. For information about the Society’s meetings, consult Events on www.geolsoc.org.uk. To find out more about the Society’s Corporate Affiliates Scheme, write to [email protected]. Published by The Geological Society from: The Geological Society Publishing House, Unit 7, Brassmill Enterprise Centre, Brassmill Lane, Bath BA1 3JN, UK (Orders: Tel. þ44 (0)1225 445046, Fax þ44 (0)1225 442836) Online bookshop: www.geolsoc.org.uk/bookshop The publishers make no representation, express or implied, with regard to the accuracy of the information contained in this book and cannot accept any legal responsibility for any errors or omissions that may be made. # The Geological Society of London 2010. All rights reserved. No reproduction, copy or transmission of this publication may be made without written permission. No paragraph of this publication may be reproduced, copied or transmitted save with the provisions of The Copyright Licensing Agency Ltd, Saffron House, 6 –10 Kirby Street, London EC1N 8TS, UK. Users registered with the Copyright Clearance Center, 222 Rosewood Drive, Danvers, MA 01923, USA: the item-fee code for this publication is 0305-8719/10/$15.00. British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library. ISBN 978-1-86239-309-7 Typeset by Techset Composition Ltd, Salisbury, UK Printed by CPI Antony Rowe, Chippenham, UK Distributors North America For trade and institutional orders: The Geological Society, c/o AIDC, 82 Winter Sport Lane, Williston, VT 05495, USA Orders: Tel. þ1 800-972-9892 Fax þ1 802-864-7626 E-mail: [email protected] For individual and corporate orders: AAPG Bookstore, PO Box 979, Tulsa, OK 74101-0979, USA Orders: Tel. þ1 918-584-2555 Fax þ1 918-560-2652 E-mail: [email protected] Website: http://bookstore.aapg.org India Affiliated East-West Press Private Ltd, Marketing Division, G-1/16 Ansari Road, Darya Ganj, New Delhi 110 002, India Orders: Tel. þ91 11 2327-9113/2326-4180 Fax þ91 11 2326-0538 E-mail: [email protected]

Contents V ECOLI , M., M EYER -B ERTHAUD , B. & C LE´ MENT , G. The terrestrialization process: modelling complex interactions at the biosphere –geosphere interface–Introduction

1

J ANVIER , P. Terrestrialization: the early emergence of the concept

5

V ERSTEEGH , G. J. M. & R IBOULLEAU , A. An organic geochemical perspective on terrestrialization

11

S TROTHER , P. K., S ERVAIS , T. & V ECOLI , M. The effects of terrestrialization on marine ecosystems: the fall of CO2

37

S TEEMANS , P., W ELLMAN , C. H. & G ERRIENNE , P. Palaeogeographic and palaeoclimatic considerations based on Ordovician to Lochkovian vegetation

49

M EYER -B ERTHAUD , B., S ORIA , A. & D ECOMBEIX , A.-L. The land plant cover in the Devonian: a reassessment of the evolution of the tree habit

59

P RESTIANNI , C. & G ERRIENNE , P. Early seed plant radiation: an ecological hypothesis

71

G ERRIENNE , P., M EYER -B ERTHAUD , B., L ARDEUX , H. & R E´ GNAULT , S. First record of Rellimia Leclercq & Bonamo (Aneurophytales) from Gondwana, with comments on the earliest lignophytes

81

A STIN , T. R., M ARSHALL , J. E. A., B LOM , H. & B ERRY , C. M. The sedimentary environment of the Late Devonian East Greenland tetrapods

93

C RESSLER , W. L. III, D AESCHLER , E. B., S LINGERLAND , R. & P ETERSON , D. A. Terrestrialization in the Late Devonian: a palaeoecological overview of the Red Hill site, Pennsylvania, USA

111

B LIECK , A., C LE´ MENT , G. & S TREEL , M. The biostratigraphical distribution of earliest tetrapods (Late Devonian): a revised version with comments on biodiversification

129

S ANCHEZ , S., S TEYER , J. S., S CHOCH , R. R. & D E R ICQLE` S , A. Palaeoecological and palaeoenvironmental influences revealed by long-bone palaeohistology: the example of the Permian branchiosaurid Apateon

139

L AURIN , M. & S OLER -G IJO´ N , R. Osmotic tolerance and habitat of early stegocephalians: indirect evidence from parsimony, taphonomy, palaeobiogeography, physiology and morphology

151

Index

181

The terrestrialization process: modelling complex interactions at the biosphere – geosphere interface – Introduction M. VECOLI1*, B. MEYER-BERTHAUD2 & G. CLE´MENT3 1

Universite´ Lille 1, FRE 3298 CNRS Geósyste`mes, Laboratoire de Paleóntologie, Cite´ Scientifique, F-59655 Villeneuve d’Ascq, France

2

UMR AMAP (botAnique et bioinforMatique de l’Architecture des Plantes), c/o CIRAD, TA-A51/PS2, Boulevard de la Lironde, 34398 Montpellier cedex 5, France 3

Museúm national d’Histoire naturelle (MNHN), De´partement Histoire de la Terre, UMR 5143 du CNRS, Paleóbiodiversite´ et Paleóenvironnements, Case Postale 38, 57 rue Cuvier, F-75231 Paris cedex 05, France *Corresponding author (e-mail: [email protected])

The invasion of the land by plants (‘terrestrialization’: Ordovician–Devonian) is one of the most significant evolutionary events in the history of life on Earth, and correlates in time with periods of major palaeoenvironmental perturbations. The development of a vegetation cover on the previously barren land surfaces impacted the global biogeochemical cycles and the geological processes of erosion and sediment transport. The terrestrialization process includes the rise of major new groups of animals such as arthropods and tetrapods. The latter number some 24 000 living species, including Homo sapiens. Mass extinction and radiation events observed in the marine fossil record appear to correlate significantly with bioevents recorded in the terrestrial realm, providing evidence of strong terrestrial –marine teleconnections. The evolution of early land plants also correlates with a dramatic decline in CO2 concentration in the atmosphere, testifying to a first-order disturbance in the global carbon cycle. The onset of the end-Devonian glaciation after a protracted period of ‘greenhouse’ climatic conditions also appears to be causally linked to the invasion of the continents by land plants. The major ecological role of land plant evolution on the previously barren landmasses and the conquest of the land by animal life have fascinated palaeontologists and Earth scientists since the birth of modern geoscience. Although much progress has been recently made in the understanding of the timing and mechanisms of the terrestrialization process (e.g. Gensel & Edwards 2001), a lot of unanswered questions remain. There is also a lack of interdisciplinary studies on the terrestrialization process, including the analysis of early tetrapod evolution in the context of the changing palaeoenvironment. This

is mainly due, in our opinion, to a cultural barrier separating vertebrate palaeontologists from a large part of the geoscience community, including the palaeobotanists and the invertebrate (micro-) palaeontologists. The application of new analytical techniques (e.g. analysis of biomarkers, applications of sequence stratigraphic concepts, palaeohistology, etc.) will radically change our views on many aspects of the complex series of events which led to the transition of life from water to land. This book contains a selection of papers reflecting the contributions to a workshop that was held at the Museum of Natural History of Paris (Museé National d’Histoire Naturelle) in autumn 2007. The workshop was sponsored by a special grant (ECLIPSE Environnement et Climat du Passe´: histoire et Evolution) from the INSU (Institut National des Sciences de l’Univers) department of CNRS (Centre National de la Recherche Scientifique). It was the intention of the organizers of this workshop (Marco Vecoli, Brigitte Meyer-Berthaud and Gae¨l Cle´ment) to bring together specialists from different fields of palaeontology and geoscience in order to achieve a comprehensive perspective on the various facets of terrestrialization. We think that it is only by a multidisciplinary approach that we can hope to gain new insights into the evolution of life and its environments through geological time. Accordingly, the present contributions cover aspects on palynology, palaeobotany, organic geochemistry, sedimentology, vertebrate palaeontology, palaeoecology and palaeobiogeography. The first contribution by Janvier presents a historical perspective on terrestrialization: he discusses how the idea defended by some pre-socratic philosophers that marine life preceded terrestrial life gained authority as science progressed, and how the concepts and methods embedded in the theory

From: Vecoli, M., Cle´ment, G. & Meyer-Berthaud, B. (eds) The Terrestrialization Process: Modelling Complex Interactions at the Biosphere– Geosphere Interface. Geological Society, London, Special Publications, 339, 1– 3. DOI: 10.1144/SP339.1 0305-8719/10/$15.00 # The Geological Society of London 2010.

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M. VECOLI ET AL.

of evolution made it a reality. Yet, despite intensive research primarily focusing on the vertebrate and embryophyte records, this reality is not fully understood. While the study of fossils remains essential, new developments in evo-devo (evolutionary developmental biology) should help to elucidate how some groups succeeded in their adaptation to terrestrial environments. A totally new approach to the investigation of the origin and early evolution of land plants is presented by Versteegh & Riboulleau, who explore how the physiological adaptations required by the transition from a fully aquatic habitat to a subaerial one might be tracked by the successive appearance of molecular biomarkers in the sedimentary record. In their contribution, Strother et al. link the drop in pCO2 calculated from the GeocarbIII model for the Palaeozoic to a stepwise increase of plant biomass related to three major evolutionary events: the origination of a bryophyte grade of land plants, the origination of vascular plants and the advent of trees. They hypothesize that, through the changes it induced in the atmospheric pCO2, this increase in terrestrial biomass had a profound effect on the evolution of the photosynthetic organisms in the ocean (with a lag response of about 10 million years for the latter). An updated synthesis of the changes in diversity and paleogeographical distribution of land plants during the 35 million year period of time separating the occurrence of the earliest cryptospore assemblages in Gondwana and the diversification of the tracheophytes in the early Devonian is presented by Steemans et al. According to their research, the migration of land plants from northern Gondwana to Baltica in the Late Ordovician was facilitated by the northward migration of Avalonia. The disappearance of the icy barrier that separated South America from the rest of Gondwana in the early Silurian might also be related to the spread of land plants from the northern Gondwanan regions to western Gondwana. The Aeronian-Telychian event seems to have triggered the evolution of the trilete spore-producing plants that are presumed to have been vascular and more efficiently adapted to their local habitats. The three successive articles by MeyerBerthaud et al., Prestianni & Gerrienne and Gerrienne et al. present new insights on land plant evolution in the Devonian. The increase in size of land plants and the advent of the seed habit are frequently cited as two cornerstones in the terrestrialization of the land plants which played a major role in the paleoenvironmental changes occurring at the end of the Devonian. MeyerBerthaud et al. discuss the constructional patterns and putative environmental needs of the two earliest types of trees (the pseudosporochnalean trees and

Archaeopteris). They make the point that, even at the dawn of arborescence, several contrasting strategies evolved for making tall plants but only one (the Archaeopteris strategy) may have impacted the Devonian environments significantly. Prestianni & Gerrienne report five different types of seeds in the Late Devonian which share the same type of mechanism, an apical extension of the nucellus, for trapping the pollen. The age and taphonomy of these records are reviewed. The authors agree with previous hypotheses suggesting that early seed plants preferred disturbed habitats, but they add a ‘shady’ context, analogous to that inferred by some authors for the earliest angiosperms some 300 million years later. Preceeding Archaeopteris and the seed plants within the lignophytes, the Aneurophytalean progymnosperms were widely distributed on the Euramerican and Siberian plates during the Middle and early Late Devonian. Gerrienne et al. report the first occurrence of the genus Rellimia in Gondwana which, amazingly, may also represent the oldest known occurrence of the clade in the late Early Devonian. The Early Devonian record of plants from Gondwana is scarce but this discovery indicates that Gondwana may be a good location to recover early lignophytes. Three more contributions are devoted to the palaeoecology and palaeogeography of Late Devonian tetrapod palaeoenvironments. Because of their diversity and exceptional preservation, Late Devonian vertebrate faunas from East Greenland play a key role in the current understanding of the morphology and evolution of early tetrapods. A critical question, which is crucial to understand how this group became adapted to terrestrial conditions, is the reconstruction of the environment and ecological needs of its major representatives. Astin et al. review the range of sedimentary environments present through the Celsius Bjerg Group. They suggest that the Acanthostega found in situ in the Britta Dal formation lived in a waterhole, but they account for the fact that this may not have been the ‘normal’ habitat of these organisms. After years of study, Cressler et al. provide an updated reconstruction of the Late Devonian landscape at Red Hill, an exceptional fossil deposit of Pennsylvania. This ancient alluvial floodplain, that was part of the Caskill Delta Complex on the southern margin of Laurussia, hosted a diverse fauna of vertebrates and invertebrates. This reconstruction allows the evaluation of the conditions in which this fauna thrived in different aquatic habitats, the proposal of hypotheses about the trophic relationships of the Red Hill ecosystem and the suggestion of a scenario of the selective pressures that may have lead the tetrapodomorphs to explore shallow water habitats.

INTRODUCTION

Accurate dating of the fossil record is essential to form hypotheses about the factors that may have triggered the diversification of a specific group. Blieck et al. provide an updated biostratigraphical review of tetrapod occurrences in the Late Devonian. This strengthens the recognition of two episodes of diversification and the probable link of the first episode to the low concentration of oxygen in the atmosphere during the GivetianFrasnian time slice. Based on their data, these authors also favour an ‘out of Euramerica’ scenario where tetrapods originate on the Old Red Sandstone palaeocontinent in a pre-Pangean configuration of landmasses. The last two contributions demonstrate how morphological, histological and taphonomical analyses of Palaeozoic tetrapods, in the context of their palaeogeographical occurrence, can contribute to constrain their habitats, palaeoenvironments and ecologic requirements. Sanchez et al. applied palaeohistological analyses to track changes in food availability, palaeoclimatic conditions and/or the presence of predators in the habitat of small

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temnospondyls from the Permian freshwater-lake deposits of the Saar-Nahe Basin in southwest Germany. Finally, the contribution by Laurin et al. presents a historical review of concepts and evidence of the habitat of extant amphibians as well as Palaeozoic sarcopterygians. The authors conclude that on the basis of current knowledge there is no definitive reason to expect early stegocephalians to have been confined to freshwater palaeoenvironments. They present evidence for a widespread tolerance of salt- and brackish waters in Palaeozoic stegocephalians. We hope that this book will stimulate further multidisciplinary investigations, developments and use of new analytical techniques as well as contribute to new ideas and approaches to the study of terrestrialization.

Reference Gensel, P. G. & Edwards, D. (eds) 2001. Plants Invade the Land: Evolutionary and Environmental Perspectives. Columbia University Press, New York.

Terrestrialization: the early emergence of the concept PHILIPPE JANVIER Museúm National d’Histoire Naturelle, UMR 5143 du CNRS, CP 38, 47, rue Cuvier, 75231 Paris Cedex 05, France (e-mail: [email protected]) Abstract: The transition from water to land is perhaps the most dramatic event in the history of life after the rise of photosynthesis, sexuality and predation. During the late Neoproterozoic and the early Palaeozoic, some green plants, fungi and animals happened to overcome the constraints that linked them to the primeval aquatic environment of life, became progressively adapted to the terrestrial, aerobic environment and finally contributed to its change through time. We do not know how many taxa initially survived this trial, but we have some indication of the result in extant life: a threefold world of pluricellular terrestrial organisms, all depending on each other to various degrees and surrounded by a cryptic world of bacteria and unicellular eukaryotes. Fossils provide us with acceptable information about the evolutionary history of only two of these worlds: embryophytes and bilateralian animals. The molecules of their living representatives can only begin to tell us how they gained the complexity that allowed them to achieve this remarkable adaptation to life on land and in air.

Is terrestrialization a ‘conquest’, as it is often referred to in popular works? Was it a conquest of land, more space, more food, more light, more oxygen or, conversely, more carbon dioxide? Which selection pressures might have driven some living beings away from the peaceful environment of the oceans that prevailed before predation arose in the late Neoproterozoic? How did – and do – terrestrialized organisms change the physical environment of Earth, triggering either global warming or cooling? These questions are still being debated, and are the subject of the present issue. Terrestrialization entailed adaptation to gravity, protection against deleterious ultraviolet light, survival at high oxygen pressures (a gas that most primitive aquatic animals only appreciate in small doses; Corbari et al. 2004) and the constant need for water, without which reproduction was initially impossible and life impossible forever. Life on land at the dawn of the Palaeozoic was as pleasant for aquatic organisms as a weekend on the Moon would be for us. In fact, terrestrialization is perhaps better depicted as an ensemble of contingent processes that started in the early Palaeozoic but could well have ended quickly after with the complete extinction of the major lineages that shape the extant living terrestrial world. However, as far as we know from fossil and living organisms, none of the major eukaryotic taxa that became adapted to life in air and on land (when adult) have ever returned to an entirely aquatic and nonaerobic life. Possible exceptions include, for example, planorbid snails whose relationship to other pulmonate snails remains obscure. The elucidation of the evolutionary transition from water to land is a long story that was intuitively

foreshadowed in Greek Antiquity. The idea that aquatic life has preceded terrestrial life was envisaged by Greek philosophers such as Anaximander of Milletus or Empedocles, and Aristotle’s ‘Scala Naturae’ also reflects this hierarchy. This is generally regarded as a more elaborate version of obscure, pre-existing mythologies or intuitions that were rooted in the deep past of earlier Eurasian human populations, from which the Biblical narrative of Genesis may also have been derived. The latter was the dominant narrative in the Christian world until the 18th century and the rise of new scenarios that involved transformations of the living beings through time. An example of such reputedly heretical views is Maillet’s (1755) extravagant theory of a speciesto-species correspondence between marine and terrestrial animals or plants. Sea anemones were precursors to flowers and parrot fishes precursors to parrots. However, the first argumented theories of historical relationships between primitively aquatic and terrestrial animals appear in Lamarck’s (1809) Philosophie Zoologique, in which inheritance of characters acquired by need is the only explanatory process. Although still strongly influenced by the Aristotelian Great Chain of Beings, Lamarck’s views were essentially based on the observation of characters and behaviours which suggested to him that marine organisms were, somehow, ancestral to land organisms. This was already foreshadowed in his symmetrical classification of plant and animals (Lamarck 1785). The pre-Darwinian 19th century also produced a number of comparative anatomy-based theories about the transition from aquatic to land organisms, notably for vertebrates, but most of these theories

From: Vecoli, M., Cle´ment, G. & Meyer-Berthaud, B. (eds) The Terrestrialization Process: Modelling Complex Interactions at the Biosphere– Geosphere Interface. Geological Society, London, Special Publications, 339, 5– 9. DOI: 10.1144/SP339.2 0305-8719/10/$15.00 # The Geological Society of London 2010.

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P. JANVIER

were still in the framework of a transcendental view of homology (e.g. Geoffroy Saint-Hilaire 1807; Owen 1861). Chambers’ (1844) Vestiges suggested a water-to-land transition that was inspired by the Lamarckian views but was closer to modern scenarios since it considered adaptation to environmental changes through time in a more elaborate geodynamic context. Miller (1849), although a creationist and catastrophist in the same vein as his mentor Louis Agassiz and many other naturalists of his time, also envisaged the transition of life from water to land in a detailed chronology-based sequence that was more accurate than Chambers’. However, Chambers viewed this transition as a continuum between for example, ‘sauroid’ fishes ‘calculated to breathe the atmosphere’ and ‘reptiles’ (then including amphibians), whereas Miller considered the earliest tetrapods (‘reptiles’) as the result of a ‘different creation’ in the Carboniferous.

Vertebrates and embryophytes: two radically different case studies Since the early 20th century, vertebrate history has been regarded as a good case study for the transition of animals from water to land. This is despite a discontinuous extant taxonomic record; that is, the phylogenetic pattern of the living taxa shows gaps which frustratingly correspond to major adaptive events (i.e. the agnathan-gnathostome, fishtetrapod, amphibian-amniote or reptile-bird gaps). This paucity of living ‘intermediate forms’ or, at any rate, forms that display ‘intermediate characters’, is the result of deep divergences between large clades and extensive extinctions (Donoghue & Purnell 2005). Such gaps seem to be frequent in metazoans, notably in protostomes and deuterostomes, but virtually absent in embryophytes (land plants) whose major classical living groups (e.g. bryophytes, pteridophytes and gymnosperms) are almost all paraphyletic (except for angiosperms) (Donoghue 2005). However, the monilophytes (ferns and horsetails), formerly unrecognized as a group, are now regarded as a clade, sister to the lignophytes (Pryer et al. 2001). Therefore, the progressive assembly of the bauplan of the most terrestrialized embryophytes, except for the homoplastic large leaves (megaphylls) of pteridophytes and gymnosperms, can be more readily reconstructed on the basis of the living taxa than that of land vertebrates (living amphibians and amniotes being clades, and only reptiles being paraphyletic). Conversely, ‘intermediate’ structures are perhaps more difficult, for material reasons, to infer from fossil embryophytes than from fossil vertebrates.

Notably, the order of appearance of the six synapomorphies of the earliest land plants (multicellular sporophyte, spore with sporopollenin, cuticle, stomatas, sporangia and gametangia) remains undocumented by fossils. In the case of vertebrate terrestrialization, lungfishes (and possibly the coelacanth since 1938) were for a long time the only available hints. The hesitation of the 19th century naturalists suggests that these hints were unconvincing (see review in Rosen et al. 1981). Vertebrates (and to some extent arthropods) have a relatively good and anatomically informative fossil record that fills the morphological gaps by providing examples of extinct character combinations, however. Before the discovery of such key fossil taxa, the rise of land vertebrates had been a highly controversial matter. Since Geoffroy St Hilaire’s publication (1807), living bichirs (polypteriforms) were regarded as the most likely closest living piscine relatives of tetrapods until the discovery of the living lungfishes and the controversies this raised. When finally recognized as tetrapod-like fishes (and not fish-like tetrapods), living lungfishes appeared as the sister group of tetrapods in the first evolutionary trees of vertebrates proposed by Haeckel (1866). This was soon followed by Darwin’s supporters, notably Huxley (1876). Huxley, however, failed to recognize the early fossil lungfishes and instead gathered them with his crossopterygians (lobe-finned fishes; now part of the sarcopterygians). A first important clue came with Baur’s (1896) discovery that the earliest tetrapods known at that time, the Carboniferous temnospondyls, were similar to some of the fossil crossopterygians, notably by their folded tooth structure. Watson (1912) then provided evidence for choanae (internal nostrils) in some crossopterygian fishes (Megalichthys and Eusthenopteron), which also happened to have somewhat limb-like paired fin skeletons. The assembly of the tetrapod-like characters of the late Devonian tetrapodomorph fish Eusthenopteron culminated with Jarvik’s (1942, 1980) detailed description of this now iconic fossil. Around much the same time, the Danish Greenland expeditions also yielded the fish-like tetrapod Ichthyostega (or ‘four-legged fish’) which combined limbs with digits and a caudal fin covered with fish-like fin rays that are composed of lepidotrichs (Jarvik 1952). The junction between fish and tetrapods was further completed by a number of new early tetrapod discoveries in the 1980– 1990s and the identification of elpistostegalians as the closest piscine relatives of tetrapods, thereby dethroning Eusthenopteron from this position (Clack 2002; Daeschler et al. 2006). Although the scenarios of the fish-tetrapod transition are diverse, their polarity is now firmly established: from fishes to

TERRESTRIALIZATION: THE CONCEPT

tetrapods within a single clade, the tetrapodomorph sarcopterygians. The transition from water to land among animals is now well supported by informative fossils for vertebrates, but frustratingly less so for arthropods and molluscs. The actual processes involved in this evolutionary transition remain largely elusive. As for vertebrates, at any rate, the fin-limb transition as currently outlined by palaeontologists is roughly consistent with the recent data provided by developmental genetics. The latter are far less informative, however; we understand which morphogenetic processes may have been involved but, to date, only fossils provide factual support for intermediate conditions (Coates et al. 2007).

Terrestrialization today The term ‘terrestrialization’ appeared in the mid-19th century but currently encompasses many different adaptive processes, depending whether it is considered by for example, anatomists, palaeontologists, ecologists or physiologists. Terrestrialization is in fact a transition between water and another fluid: air. For most of the plants and animals that underwent terrestrialization, the substrate remained basically the same from sea, river or lake bottom to land. What changed were essentially gravity, the mode of oxygen intake, water retention and conduction, sometimes the mode of locomotion (for animals) and the protection against ultra-violet rays. Among these constraints, water retention was the most difficult to overcome because an aquatic organism is merely an osmotically isolated part of its watery environment; that is, a bag of water in water. A terrestrial organism, however, is a bag of water in air. In common with all examples of evolutionary transition, the border between non-terrestrialized and terrestrialized organisms is not clear-cut. There are many instances of anatomical structures and functions that were once regarded as signatures of terrestrialized organisms, but are in fact exaptations of homologues which were perfectly functional in fully aquatic organisms. The tetrapod limbs is a classical example, but its selective advantage would be very obscure if it did not arise in conjunction with other anatomical or physiological innovations such as the choanae (internal nostrils). The latter turned up some tens of million years earlier, in fully aquatic forms (Clack 2002). Similar conjunctions of chronologically disconnected but adaptively consistent characters are also found in arthropods and embryophytes. The emphasis on vertebrates when dealing with terrestrialization in popular science gives the impression that all ideas regarding this event have

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been centred about a somewhat finalist conception of a conquest that culminates with land vertebrates, mammals and man; who finally survives due to the simultaneous terrestrial evolution of all other organisms which he depends on. A botanist (or a palaeobotanist) could say the same, considering how much seed plants are dependent on animals to disperse, reproduce and survive (Halle´ 2002). Apart from spermatophytes, however, land plants could in principle exist in the total absence of animals (as long as bacteria and fungi are there). Terrestrialization is in fact the result of independent, but sometimes remotely contingent, events. Similar crucial events in the history of life have occurred earlier, such as the rise of photosynthesis, motile benthic metazoans, predation, larval development (or metamorphosis) and the planktonic life in metazoans; that is, what we now call ‘marine ecology’ (Butterfield 2007; Peterson et al. 2007). Nowadays, molecules and fossils concur in providing us with a more consistent timing of the history of life. We are certainly a long way from the time when we will have a reliable picture of the very deep past of life on Earth, but we are aware of some key events in the past 2 Ga or so. We also understand the mechanisms that underlie the patterning of eukaryotic life for nearly 1 Ga, until the rise of ‘animals’ (Peterson et al. 2007). The rise of terrestrial ecosystems, however fascinating they may be for palaeontologists, is comparable to other preceding dramatic changes in the aquatic world.

Selection, adaptation and evolutionary radiations Current research in integrative palaeobiology throws some light on questions that have long been puzzling evolutionary biologists, namely the rise of phenotypic innovations and the biological processes that underlie major evolutionary radiations. The latter are generally conceived as the result of the selection of a specific character which happened to occur in a particular environmental context and soon ensured a selective advantage to a large number of species. In the case of terrestrialization, common knowledge suggests that almost all metazoan and metaphyte taxa were potential candidates for the conquest of land, in a context of increasing levels of atmospheric oxygen. In fact, as well as soil bacteria and some unicellular organisms, only four major clades comprise most of the fully terrestrialized life: fungi, embryophytes, arthropods and vertebrates. Annelids and gastropods are generally overlooked in the usual narrative of terrestrialization and there are conjectures about why, for example, there is no terrestrialized

8

P. JANVIER

bivalve or echinoderm (the open water vascular system of the latter is probably the reason). Terrestrial jellyfishes and octopuses remain only in the realm of science fiction! Adaptation is the long-term result of natural selection in a particular environmental framework. How adaptations became durably retained in a number of related species and rapidly generalized to larger clades is at the origin of the notion of adaptive radiation (e.g. amniotes or angiosperms). Biologists are currently trying to find the factors that regulate such macro-evolutionary patterns that is, whether such adaptive radiations could not be triggered by factors which increase the diversity and complexity of phenotypes, and on which natural selection could act. The expansion of taxa into an entirely new environment that entails a profound reconstruction of morphology and physiology may not be too different in the case of terrestrial and abyssal environments. Molecular biologists once put much weight on massive genome duplications in vertebrates as a possible explanation of their ‘bursts’ of organismal complexity, but it is now clear that this is due to a bias induced by massive extinctions of members of grades (Donoghue & Purnell 2005). Biologists are now discovering possible regulators of multiple gene expressions; that is, the highly conserved miRNAs (micro ribonucleic acids). The distribution of miRNAs is increasingly large in the major taxa that have taken part in the transition from water to land (e.g. embryophytes, arthropods and vertebrates), thanks to their phenotypic complexity (Sempere et al. 2006; Butterfield 2007; Heimberg et al. 2008). Is this an important clue or yet another illusion of molecular character distributions that seem beyond the bounds of chance? At any rate, miRNAs seem to regulate such a large number of gene expressions at the cellular level (thus structures and functions) that they may, to some extent, hamper character losses. In other words, once an organism is fully terrestrialized, it is forever. Return to water (as has occurred in angiosperms, arthropods or vertebrates) is generally at the cost of additional anatomical and physiological innovations and not mere ‘degeneracy’, as character loss was formerly referred to. Is terrestrialization a one-way ticket? Probably, and terrestrial organisms will continue to evolve and disperse aerobic life wherever there is just enough water, light and oxygen to survive, modifying the physical environment of Earth in various ways. Deciphering what has actually happened on land since the dawn of the Phanerozoic is enough for us palaeobiologists, but it may also provide clues for predicting how our physical environment may react to a future fluctuation

of biodiversity in the short term. Our data may eventually be of interest to the supporters of ‘terraforming’, who dream of exporting phototrophic life to other planets and thereby modifying the atmosphere in the same way as life did on Earth. But that is another story.

References Baur, G. 1896. The Stegocephali: A phylogenetic study. Anatomischer Anzeiger, 11, 657–675. Butterfield, N. J. 2007. Macroevolution and macroecology through deep time. Palaeontology, 50, 41– 55. Chambers, R. 1844. Vestiges of the Natural History of Creation. John Churchill, London. Clack, J. A. 2002. Gaining Ground: The Origin and Evolution of Tetrapods. Indiana University Press. Bloomington. Coates, M. I., Ruta, M. & Wagner, P. J. 2007. Using patterns of fin and limb phylogeny to test developmentalevolutionary scenarios. In: Bock, G. & Goode, J. (eds) Tinkering: The Microevolution of Development. Novartis Foundation Symposium 284, John Wiley & Sons, New York, 245– 261. Corbari, L., Carbonel, P. & Massabuau, J.-C. 2004. How a low tissue O2 strategy could be conserved in early crustaceans: the example of the podocopid ostracods. Journal of Experimental Biology, 207, 4415– 4425. Daeschler, E. B., Shubin, N. H. & Jenkins, F. A., Jr. 2006. A Devonian tetrapod-like fish and the evolution of the tetrapod body plan. Nature, 440, 757–763. Donoghue, M. J. 2005. Key innovations, convergences, and success: macroevolutionary lessons from plant phylogeny. Palaeobiology, 31, 77–93. Donoghue, P. C. J. & Purnell, M. A. 2005. Genome duplication, extinction and vertebrate evolution. Trends in Ecology and Evolution, 20, 312– 319. Geoffroy Saint-Hilaire, E. 1807. Premier me´moire sur les poissons, ou` l’on compare les pie`ces osseuses de leurs nageoires pectorales avec les os de l’extre´mite´ ante´rieure des autres animaux a` verte`bres. Annales du Museúm d’Histoire Naturelle, 9, 357–372. Haeckel, E. 1866. Generelle Morphologie der Organismen. Reimer, Berlin. Halle´, F. 2002. In Praise of Plants. Timber Press, Portland. Heimberg, A. M., Sempere, L. F., Moy, V. N., Donoghue, P. C. J. & Peterson, K. J. 2008. MicroRNAs and the advent of vertebrate morphological complexity. Proceedings of the National Academy of Sciences, 105, 2946–2950. Huxley, T. H. 1876. Contribution to morphology. Ichthyopsida No1. On Ceratodus forsteri, with observations on the classification of fishes. Proceedings of the Zoological Society of London, 1876, 24– 59. Jarvik, E. 1942. On the structure of the snout of crossopterygians and lower gnathostomes in general. Zoologiska Bidrag fra˚n Uppsala, 21, 235–675. Jarvik, E. 1952. On the fish-like tail in the ichthyostegid stegocephalians, with description of a new stegocephalian and a new crossopterygian from the Upper

TERRESTRIALIZATION: THE CONCEPT Devonian of East Greenland. Meddelelser om Grønland, 114, 1 –90. Jarvik, E. 1980. Basic Structure and Evolution of Vertebrates, Volume 1. Academic Press, London. Lamarck, J.-B. 1786. Me´moire sur les classes les plus convenables a` e´tablir parmi les ve´ge´taux, et sur l’analogie de leur nombre avec celles de´termineés dans le re`gne animal, ayant e´gard de part et d’autre a` la perfection gradueé des organes. Me´moires de l’Acade´mie Royale des Sciences, 1785, 437– 453. Lamarck, J.-B. 1809. Philosophie Zoologique. Dentu, Paris. Maillet, B. DE. 1755. Telliamed, ou entretien d’un philosophe indien avec un missionnaire français sur la diminution de la mer. Gosse, La Haye. Miller, H. 1849. Footprints of the Creator; or the Asterolepis of Stromness. Johnstone & Hunter, London. Owen, R. 1861. Paleontology or a Systematic Summary of Extinct Animals and their Geological Relations. 2nd edn. Adam and Charles Beck, London.

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Peterson, K. J., Summons, R. S. & Donoghue, P. C. J. 2007. Molecular palaeobiology. Palaeontology, 50, 775– 809. Pryer, K. M., Schneider, H., Smith, A. R., Cranfill, R., Wolf, P. G., Hunt, J. S. & Sipes, S. D. 2001. Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature, 409, 618–622. Rosen, D. E., Forey, P. L., Gardiner, B. G. & Patterson, C. 1981. Lungfishes, tetrapods, paleontology, and plesiomorphy. Bulletin of the American Museum of Natural History, 167, 159 –276. Sempere, L. F., Cole, C. N., McPeek, M. A. & Peterson, K. J. 2006. The phylogenetic distribution of metazoan microRNAs: insights into evolutionary complexity and constraint. Journal of Experimental Zoology, 306B, 575– 588. Watson, D. M. S. 1912. The largest coal measure amphibia. Memoirs and Proceedings of the Manchester Literary and Philosophical Society, 57, 1– 14.

An organic geochemical perspective on terrestrialization GERARD J. M.VERSTEEGH1* & ARMELLE RIBOULLEAU2 1

MARUM, Universita¨t Bremen, Leobenerstraße, D-28359 Bremen, Germany 2

Universite´ des Sciences et Technologies de Lille – Baˆt. SN5, UMR 8157 du CNRS Geósyste`mes, F-59655 Villeneuve d’Ascq Cedex, France *Corresponding author (e-mail: [email protected]) Abstract: The colonization of land required new strategies for safe gamete/diaspore dispersal, and to cope with desiccation, harmful radiation, fire and gravity. Accordingly, the morphology, behaviour and physiology of the organisms changed. Here, we explore to what extent physiological adaptations, reflected in the molecular content of the sediments, add to our understanding of the terrestrialization. Many compounds considered characteristic of land organisms do not provide valuable information from the fossil record since (1) they were not preserved; (2) they occur or correspond to substances that evolved prior to the terrestrialization (e.g. cutan vs. algaenan, cellulose); or (3) they have been changed diagenetically and/or catagenetically. The latter leads to geo(macro)molecules without a chemical fingerprint relating them to their original bio(macro)molecules despite, sometimes, excellent morphological preservation of the organic remains. Nevertheless, some molecular markers and their stable isotopes provide independent information on the terrestrialization process. The odd predominance of n-alkane surface waxes is a feature already apparent in early land plants and could, with caution, be used as such. Furthermore, fossil terpenoids and their derivatives are valuable for reconstructing the evolution of major plant groups. The radiation of the phenylpropanoid pathway with for example, sporopollenin and lignin seems to be closely related to the evolution of land plants.

As for other disciplines occupied with unravelling past life and environment, organic geochemistry relies heavily on the paradigm that the present provides a key to the past. For organic geochemistry, the biosynthetic pathways of living organisms provide such a key. The biosynthetic differences between organisms provide insight into the evolution of biosynthetic pathways and this can be applied to, and calibrated against, the fossil record. Evolution also implies adaptation and, by linking species ecology to their biochemistry, the adaptive value of the biosynthetic pathways and the biomolecules produced may be resolved. This biosynthetic link to environment can also be applied to the past. For instance, the notion that oxygen is required in steroid and non-hopanoid triterpenoid synthesis implies that analysis of steroids in ancient sediments may help to unravel the early evolution of the atmosphere (Summons et al. 2006). Analogous to the oxygenation of the Earth’s atmosphere, terrestrialization also required major adaptations of the terrestrializing organisms to the living conditions on land. The conquest of land required the development or strengthening of supportive structures such as skeletons, stems and roots to withstand Earth’s gravity without the support of water and to resist wind. It also demanded water-saving strategies such as arthropod and plant cuticles, vertebrate skin and cork to survive low

humidity environments and sometimes fire, as well as the development of water-conducting tissues in plants (roots, tracheids). Finally, the higher exposure to harmful radiation required sunscreens such as pigments, aromatic and other substances as UV filters. Whereas the endo- and exoskeletal adaptations are intrinsically based on the formation of large biopolymers, water saving and UV protection may be also realized by means of smaller molecules. Our working hypothesis is that the major changes in biosynthetic pathways which accompanied the terrestrialization of organisms are reflected in the molecular composition of the organic matter present in Palaeozoic sedimentary rocks. For instance, a minor change in the biosynthesis of sporopollenin may have led to lignin. In return, we can expect the changes in composition of the organic matter (OM) in Palaeozoic rocks to help determine following evolutionary trends. The question being asked is to what extent is our working hypothesis valid and what does this provide us with to understand terrestrialization? We restrict ourselves to primary producers and arthropods since they have a rich fossil record, both organic geochemically and as micro- and macroscopic remains. We exclude other terrestrial (heterotrophic) life forms (worms, snails, vertebrates, etc.) since they do not usually leave a chemically characteristic signature in the sediments.

From: Vecoli, M., Cle´ment, G. & Meyer-Berthaud, B. (eds) The Terrestrialization Process: Modelling Complex Interactions at the Biosphere– Geosphere Interface. Geological Society, London, Special Publications, 339, 11–36. DOI: 10.1144/SP339.3 0305-8719/10/$15.00 # The Geological Society of London 2010.

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G. J. M. VERSTEEGH & A. RIBOULLEAU

Organic matter analysis: lipids and macromolecules From an analytical point of view, bio- and geomolecules can be subdivided into two types of organic substances. The first type consists of relatively small molecules which dissolve in common organic solvents and form the lipids. These lipids can be analysed relatively easily using for example, gas or liquid chromatography. Examples are archaeal membrane lipids, higher plant cuticular waxes, long-chain alkenones from Haptophyta and steroids such as dinosterol from dinoflagellates, etc. Those lipids that have a relatively low biodegradability may fossilize as such and can be applied to reconstruct past environments and the (early) evolution of life (e.g. Brocks & Summons 2003). Apart from this, lipids and lipid ratios can be used to reconstruct the environment such as for long chain alkenones (Marlowe 1984; Brassell et al. 1986; Prahl & Wakeham 1987; Conte et al. 2006) and of archaeal glycerol dibiphytanyl glycerol tetraether membrane lipids (De Rosa & Gambacorta 1988; Schouten et al. 2003; Kim et al. 2008). These biomolecules can also become diagenetically or thermally modified but, as long as the resulting products can be reliably related to their source organisms, they may still provide important clues on past life and environment. For example, triaromatic dinosteroids are derived from the thermal modification of the dinoflagellate steroid dinosterol. Their presence in Palaeozoic sediments has been used as an argument for a Palaeozoic rather than Mesozoic origin of the dinoflagellates (Moldowan & Talyzina 1998; Empt 2004). The second type of molecules is of macromolecular nature and therefore insoluble in most solvents. In living organisms, the most abundant macromolecules are proteins and polysaccharides. The insoluble organic matter in the sediments, also termed ‘kerogen’, is poorly understood despite being by far the largest organic carbon pool on Earth (Berner 1989; Vandenbroucke & Largeau 2007) including all the particulate organic matter we see with the naked eye and through microscopes such as leaf and arthropod cuticles and palynomorphs. This kind of material provides considerable analytical problems with respect to structural elucidation and quantification. Non-destructive methods provide important structural information on the atomic level such as nuclear magnetic resonance (NMR) (Deshmukh et al. 2005) and at the level of functional groups such as (micro) Fourier transform infra-red (FTIR) spectroscopy (Marshall et al. 2005; Versteegh et al. 2007). Destructive methods fragment the macromolecules and these fragments also provide vital information needed to reconstruct the

original macromolecule. Of these, chemical degradation applies a series of chemical treatments whereby each successive treatment is able to break stronger chemical bonds than the previous treatment (Hunt et al. 1986; Gelin 1996; Blokker et al. 1998). Pyrolysis breaks down the molecule thermally in an inert atmosphere (Maters et al. 1977; Nip et al. 1987), however. For the characterization of fossil macromolecular organic matter and its preservation pathways, it is essential to combine several of these techniques. Despite these problems, studying this material is worthwhile (e.g. Briggs et al. 2000).

The biochemical signal from terrestrialization Desiccation management – long-chain aliphatics Simple lipids-waxes. Protection against a lack of water is of prime importance for land organisms. This can be achieved by resisting desiccation to keep a positive water balance, for example, by erecting an evaporative barrier at the organism surface and/or by developing desiccation tolerance. It seems reasonable to assume that adaptations to desiccation developed prior to the terrestrialization of plants and algae. It might be an important adaptation for freshwater species or species that live in smaller enclosed and coastal habitats to enable them to resist periods of dryness and allowing spreading from one watershed to another (e.g. by wind and animals). The earliest photosynthetic organisms on land were probably cyanobacteria possibly colonizing land as early as 2.6 Ga ago (Watanabe et al. 2000). They may have been present as single cells or filaments and, with time, colonized a variety of environments such as tidal zones, soils and desert crusts. Although emerging much later, this also accounts for photosynthetic microalgae such as Chlorophyta, Streptophyta, Bacillariophyta (diatoms), Eustigmatales and Dinoflagellata. Generally, these taxa survive dryness by tolerating dehydration as such, or by producing resting cysts (e.g. Zygnemataceae). Mostly they use sugars, lipids or proteins to stabilize the cell contents upon desiccation (Cardon et al. 2008). To our knowledge, there is no chemical fingerprint known of upon which this strategy may be reconstructed from the fossil record. Stable carbon and hydrogen isotopes of lipids can perhaps help here. The sister group of the Chlorophyta, the Streptophyta, gave rise to the Embryophytes (land plants), the only group which developed into macroscopic organisms with strategies to cope with the uneven and erratic water supply on land. The very first

TERRESTRIALIZATION: ORGANIC MOLECULES

evidence of land plants is indirectly documented by cryptospores (Strother 2000). Taylor & Strother (2008) describe Middle Cambrian palynomorphs which morphologically and ultrastructurally resemble cryptospores in many ways. However, their affinity with terrestrial or algal organisms is still under discussion; the earliest accepted occurrence of cryptospores is of Llanvirn age (middle Ordovician) (Strother et al. 1996). The earliest ‘megafossils’ are documented in the late Llandovery (Lower Silurian) (Wellman & Gray 2000; Edwards 2001) (Fig. 1). These plants were probably small (Wellman et al. 2003) and had no water conducting organs such as trachea or roots. In this respect, they were like the modern Bryophyta which are the most primitive land plants living today. According to Proctor (2000), many of the Bryophyta have three water components: symplast water (in the cells), apoplast water (in the ‘free space’ of the cell walls) and external capillary water which, for much of the time, exceeds the symplast water by a large but variable quantity. For these species, water and nutrient transport is therefore largely via the outside of the plant. This implies that for these very primitive plants, resistance to desiccation is mostly achieved by drought tolerance (although this seems not to be the case for their spores). However, not all bryophytes rely on external capillary water. Most thalloid liverworts and some erect growing mosses with waxy water repellent surfaces (e.g. many Polytrichaceae and Mniaceae) rely predominantly on internal water conduction (Proctor 2000), so that these organisms develop external coverings which function as water barriers. With few exceptions, lipids associated with external coverings are the principal water barrier component of land plants and animals (Hadley 1989). For plants, these lipids consist primarily of unbranched fully saturated linear hydrocarbon backbones with chain lengths of 20–40 carbon atoms. Typically these lipids are n-alkanes, n-ketones and secondary alcohols with a predominance of oddnumbered chain lengths and primary n-aldehydes, n-alcohols and n-fatty acids with a predominance of even-numbered chain lengths. Furthermore, a wide variety of C36 –C60 wax-esters has been detected. These aliphatic coatings are responsible for .99% of the water barrier efficiency in plants (Scho¨nherr 1976; Me´rida et al. 1981; Jetter et al. 2006). It is therefore no surprise that pollen are also covered with surface waxes (Piffanelli et al. 1998; Schulz et al. 2000). For arthropods (earliest evidence: late Cambrian; McNaughton et al. 2002) the strategy towards desiccation is similar to that of plants. Cuticular lipids are to a large extent identical but mono- and di-methyl alkanes also occur and may even dominate; for

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these organisms, they are also the primary passive barrier to evaporative water loss (e.g. Ramsay 1935; Hadley 1989; Gibbs 1998, 2002). Long-chain lipids are also synthesized by various algae such as long-chain mid-chain diols by Eustigmatophyta and diatoms (de Leeuw et al. 1981; Versteegh et al. 2000; Sinninghe Damste´ et al. 2003) long chain alkenones and alkenoates by Haptophyta (de Leeuw et al. 1980; Volkman et al. 1980; Rontani et al. 2007) or long-chain polyunsaturated alkenes by dinoflagellates (Mansour et al. 1999). However, the odd predominance of n-alkanes is a typical feature of land plants, though some microalgae such as Tetrahedron (Chlorophyta) or Nannochloropsis (Eustigmatophyta) also produce long-chain n-alkanes with a strong odd predominance (Gelpi et al. 1970; Gelin et al. 1997). Other algae also produce long-chain n-alkenes with odd predominance (Gelpi et al. 1970; see also Volkman et al. 1998) and it has been suggested that such alkadienes from the green alga Botryococcus braunii have given rise to an n-alkane odd-predominance in sediments (Lichtfouse et al. 1994; Riboulleau et al. 2007). Since the odd predominance of long chain n-alkanes already occurs in the cuticular waxes of primitive plants such as liverworts (Matsuo et al. 1974) and mosses (Nissinen & Sewoń 1994), it is interesting to investigate how this feature developed through the Palaeozoic. A marked odd predominance of n-alkanes with a maximum in C23 or C25 is observed in the extracts of early mature to mature coals of Permian age from Brazil and Australia (Casareo et al. 1996; Silva & Kalkreuth 2005). Contrastingly, the n-alkane distribution in the extracts of many coals of Carboniferous age is not characterized by a strong predominance of odd-numbered compounds; this feature can be ascribed to the maturity of the studied coal samples. However, even early mature coal samples only show a moderate odd predominance in the C25 –C31 range (e.g. Powell et al. 1976; Christiansen et al. 1989; Dzou et al. 1995; Fleck et al. 2001; Armstroff 2004). An exception is the marked predominance in the C25 – C33 range observed in the extracts of very immature early Carboniferous coals from the Moscow Basin (Armstroff 2004). The long-chain predominance is also visible in some Devonian samples, in particular when (mio)spores are present in significant amounts: C25 –C33 (max C25) in the immature Fammenian marls from Poland (Marynowski & Filipiak 2007); C23 –C31 (max C27) in the middle-late Frasnian early mature cannel coals from Melville Island, Arctic Canada (Fowler et al. 1991); C23 –C29 (max C25) in early mature Middle Devonian cutinite-rich humic coals from China containing Zosterophyllum remains (Sheng et al. 1992). These observations indicate that the characteristic signature of epicuticular

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Pennsyl vanian

Eudesmane MATH, MAPH, DAPH1, DAPH2 Phyllocladane

Mississippian

Cadalene

Retene ent-Kaurane ent-Beyerane Odd n-alkanes

Megafossils Trilete spores Trilete spores Cryptospores

Cryptospores Fig. 1. Currently documented earliest occurrences of fossil plant remains (in italics) and of characteristic terrestrial biomarkers (roman). Earliest occurrences of cryptospores and trilete spores indicated in grey from Strother (2000) and in black from Strother et al. (1996) and Steemans et al. (1996). Occurrence of plant megafossils from Wellman & Gray (2000) and Edwards (2001). See text for further references and explanations. Figure created with TS Creator (www. stratigraphy.org).


waxes was already acquired in the Middle Devonian. However, if we do not consider maturity problems, there seems to be a temporal evolution in the maximum of the n-alkane distribution which could be related to plant evolution: around C25 in the Devonian to C29 in the Carboniferous and C23 –C25 during the Permian. Present-day higher plants are characterized by a maximum in C29 –C31. Most coals older than the Devonian are liptinite-rich coals, which may derive from spores or from algae. Their n-alkane signature may therefore not be terrestrially derived. Due to the occurrence of odd-numbered n-alkanes in some algae, the n-alkane distributions must be interpreted with care. This is particularly true for samples older than Devonian where terrestrial debris is scarce. An odd-number n-alkane predominance has been previously observed in several Botryococcus richtorbanite of Permian age and was mainly attributed to a higher plant contribution (Araujo et al. 2003; Dawson 2006). These odd-numbered n-alkanes could also derive from the saturation of Botryococcus lipids, however (for an overview on Botryococcus lipids see Metzger et al. 2007). Slight odd predominances in the range C25 – C31 were also observed in the extracts of a Cambrian sediment from Tarim Basin (China) (Zhang et al. 2000) as well as in the extracts of several Proterozoic, Cambrian and Ordovician sediments from different basins in East China (Li et al. 2002). In the case of East China, this distribution was assigned to a contribution from cyanobacteria of the Spirula type (Li et al. 2002). Considering the stratigraphic distribution of microscopic higher plant remains (Fig. 1), a contribution from higher plant lipids is somehow questionable in the Cambrian and Ordovician samples. Since land-plant derived n-alkanes are (as far as C3 plants are considered) usually more enriched in 12C relative to 13C than their algal counterparts, comparison of the stable carbon isotopic composition of these alkanes with the isotopic composition of typical marine/aquatic biomarkers may aid in the identification of a land-plant signal. Macromolecules. In addition to simple lipids, protection against desiccation could also be offered by resistant biomacromolecules made of long-chain lipids (see also reviews by van Bergen et al. 2004; de Leeuw et al. 2006), although the exact role of these macromolecules is not entirely clear. Mono to tetra-functionalized long-chain alcohols and acids form the building blocks of cutin, a biopolymer present in the cuticles of most land plants (Kolattukudy 1981; Deshmukh et al. 2003). Pyrolysis shows that aliphatic lipids are also major building blocks of cutan (Tegelaar et al. 1989a; Boom et al. 2005) a macromolecule which occurs in the cuticles of plants with crassulacean acid

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metabolism (CAM), where it may be an evolutionary solution to severe drought stress (Boom et al. 2005). Nuclear magnetic resonance (NMR) analysis suggests that this aliphatic biopolymer also contains aromatic units (Deshmukh et al. 2005). Cutin and cutan should therefore be considered ‘terrestrial markers’ of higher plants. The preservation potential of cutin is, however, very low; the building blocks are cross-linked with relatively weak esters while stronger ether-bridges connect the cutan building blocks, which is more resistant. The production of aliphatic biopolymers was not invented by land plants but evolved much earlier. The analysis of the cell walls of a wide range of algae shows that some algae produce a resistant aliphatic biopolymer made of cross-linked longcarbon chains called algaenan (see review by Versteegh & Blokker 2004; Metzger et al. 2007). Algaenans resist harsh chemical treatment and they have a relatively high preservation potential which may account for the long fossil record of the Chlorophyta (Batten 1996; Batten & Grenfell 1996; Colbath 1996; Guy-Ohlson 1996; van Geel & Grenfell 1996; Wicander et al. 1996). Even although the exact biological role of algaenan is not known, it has been suggested that the highly aliphatic (plastic-like) algaenan may function as a relatively waterproof layer; it is interesting to note that apart from the marine eustigmatophyte Nannochloropsis, the development of algaenan mostly occurs in freshwater algae, notably Chlorophyta (e.g. Tetraedron, Scenedesmus, Pediastrum) which probably have the largest risk of desiccation. The similarities in structure and function between algaenan and cutin and cutan of land plants (all aliphatic biopolymers, which are both based on ether- or ester-linked long-chain fatty acids; van Bergen et al. 2004) may imply that they represent subsequent stages in the evolution of the same biosynthetic pathway. This could constitute an argument in favour of the freshwater algal origin of terrestrial plants. In sediments, cutan is difficult to discriminate from algeanan or from a highly aliphatic cutan-like geopolymer. The latter can be formed from common lipids by oxidative polymerization during early diagenesis discussed below (Boom et al. 2005; Gupta et al. 2006a, 2007a; de Leeuw 2007). This implies that fossil aliphatic biopolymers do not provide evidence for a landplant (cuticular) origin of the organic matter per se. In this case, stable carbon isotopic analysis of the aliphatic constituents may also be needed to obtain a conclusive answer.

UV protection, radiation damage Terrestrialization also involved an increased exposure to harmful radiation. Ultraviolet-B

16


(UVB) rapidly attenuates in water (penetration depth is of the order of millimetres) so protection to UVB had to increase considerably. The optical properties of plants (especially the effects of UV radiation on plants) have been intensively studied, partly in reaction to the recognition of the polar ozone holes in the atmosphere (Rozema et al. 2002a; de Bakker et al. 2005; Pfu¨ndel et al. 2006). In land plants, UV absorption is achieved by aromatic compounds such as the flavonoids and their derivatives (I –V) and other compounds produced via the phenylpropanoid pathway such as hydroxycinnamic acid (VI) and lignin. A wide diversity of flavonoids are already present in the Bryophyta. Flavonoids are absent in Hornworts (Stafford 1991; Rausher 2006) and have been found in one alga, the Charophyte Nitella (Markham & Porter 1969; Iwashina 2009). Flavonoids, or their derivatives in sediments, are of potential interest to elucidate the early terrestrialization of the embryophytes. Flavonoids were widely used during the 1970s for plant systematic as well as evolutionary studies, in particular for angiosperms, based on the distinction of ‘advanced’ v. ‘primitive’ characters (Crawford 1978; Giannasi 1978; Stuessy & Crawford 1983) (Fig. 2). However, it appeared that the advanced v. primitive distinction in flavonoids composition was not straightforward, and that one given compound could be synthesized via different pathways. Flavonoids may therefore not be fully reliable indicators for phylogenetic studies at higher taxonomic levels (Crawford 1978; Giannasi 1978). Flavonoids are known from Tertiary sediments such as Kaempferol (III) (Niklas & Giannasi

1977a, b) and their earliest record is of the biflavonoid 5-O-Methylginkgetin (II) from Cretaceous Ginkgo fossils (Zhau et al. 2006). Accordingly, despite their potential interest for the terrestrialization process, it seems that they are not preserved long enough in sediments to provide further insight into the early embryophyte evolution.

Suberin Suberin (Tegelaar et al. 1995) is another ether-based macromolecule produced by plants. It seems to be primarily used to form barriers between compartments or with the exterior. Depending on the place of deposition in the plant it protects against fire, desiccation and pathogens and limits ion transport and gas diffusion. It occurs in roots and tubers, bundle sheet cells of C4 plants and as cork in woody species that have secondary thickening (Enstone et al. 2002; Franke & Schreiber 2007). The biopolymer suberin consists of an aromatic domain. Aromatic building blocks are generated via the phenylpropanoid pathway such as p-coumaric, ferulic and sinapic acids (VII–IX) also found in sporopollenin and as alcohols in lignin (see below), as well as an aliphatic domain with aliphatic building blocks similar to those of the plant cuticle (discussed above). The aliphatic component is considered to reduce transport whereas the aromatic part has been suggested to inhibit pathogen invasion (Kolattukudy 2001; Bernards 2002; Franke & Schreiber 2007). Like lignin, suberin is not known from the most primitive embryophytes. Being ester cross-linked, suberin

3-OHanthocyanidins

D C

Pterocarpans

Flavan-3-ols 3-OH-PAs Flavan-3,4-diols

B

A

Flavonols

3-OH-flavanones

Isoflavones

3-deoxyanthocyanidins Flavan-4-ols

Biflavones Flavones

Flavanones

Fig. 2. Evolutionary scheme of the biosynthesis of the major subgroups of flavonoids with a 5,7-dihydroxy A-ring. Four levels, A, B, C, and D are shown. Levels A, B are found in bryophytes, C in ferns and fern allies and D in gymnosperms and angiosperms. PA: proanthocyanidin (modified after Stafford 1991). See supplementary information for molecular structures (structures I– V).


probably has a low preservation potential. Due to its mixture of aliphatic and aromatic monomers it may be difficult, if not even impossible, to deduce a specific suberin fingerprint from the fossil record. Suberan is a rather enigmatic highly aliphatic non-hydrolysable biopolymer. It has been described from bark (Tegelaar et al. 1995). Possibly, this polymer originates from oxidative polymerization of unsaturated lipids.

Signalling and warfare Living on land also required a new way of transmitting signals between organisms. Previously, signalling was restricted to water soluble compounds; on land, volatile compounds had to be developed. Here, nature has expanded in a myriad of molecules such as repellents, odours and pheromones. To be effective, these molecules need to provoke a reaction by the receiver, implying that the compounds must be biologically active. Often such compounds are already active at low concentrations. For warfare this is different; the toxins may remain on the organism outside or in the cells and tend to be lipid or water soluble. They need not be transportable by air. In this case, however, the compounds are also constructed to be biologically active and interfere with the physiology of the attacking organism. Many of these compounds are produced via the phenylpropanoid pathway which experienced a huge radiation with the adaptation of plants to land (Cooper-Driver & Bhattacharya 1998; Lewis & Davin 1999). Compounds produced via this pathway function for example, as antioxidants, have antifungal or antimicrobial properties or are insecticides, nematocides, antifeedants and poisons. These include the flavonoids mentioned above (I, III, IV) and their dimer (II) to polymers [the latter based on flavan-3-ols and/or flavan-3,4-diols as building blocks (I)], the proanthocyanidins or condensed tannins (V) (He et al. 2008). In addition, these all have a strong influence on soil structure and composition by retarding organic matter breakdown and capturing nutrients and, through this, substantially modifying the global carbon cycle (Kraus et al. 2009). Condensed tannins appear much later in evolution than the flavonoids (Fig. 2). They occur only in leptosporangiate ferns, gymnosperms and angiosperms (Popper & Fry 2004; Popper 2008), leaving a much smaller impact on the carbon budget for the early evolution of land plants. Such fossil tannins are only unequivocally known from brown coal (Wilson & Hatcher 1988). Two other groups of tannins exist; neither are derived from flavonoids (de Leeuw & Largeau 1993). These are the hydrolysable tannins typical for angiosperms (Okuda et al. 2000) but which

17

also occur in the filamentous green algae Spirogyra (Nishizawa et al. 1985) and the phlorotannins occurring in brown algae. Since neither group has direct relevance for the terrestrialization they will not be considered further. Another common and diverse group of products produced via the phenylpropanoid pathway are lignans (phenylpropanoid dimers), nor-lignans (with diphenylpentane carbon skeletons) and lignan oligomers which, in contrast to lignin (a polymer of monolignols), are non-structural components (Lewis & Davin 1999; Suzuki & Umezawa 2007). Lignans are known from bryophytes such as liverworths and hornworths (Lewis & Davin 1999) and are not known from algae (see also the lignin section below). Lignan remains may therefore have been preserved in the earliest land plants and could be used as tracers. Another protective strategy is the production of resins. Plant resins are used typically for protection (Langenheim 1995). Resin can be exuded passively (when a plant is wounded) or actively. Often resin emerges from canals or resin cells. Resin provides a mechanical and chemical protection against pathogens. When present on leaves, resin also acts as a barrier against desiccation and UV damage. Resins contain a complex mixture of nonvolatile compounds mainly consisting of di- or triterpenoids. In addition, resins contain volatile compounds, including mono- and sesqui-terpenoids, which can be dominant in fresh resins. These volatile compounds tend to disappear with time but a fraction can remain entrapped when the matrix polymerizes and becomes hard (Anderson & Crelling 1995). Resin- (and amber-) producing trees are present both among gymnosperms (e.g. conifers, cycads) and angiosperms. The most prolific genera all live in the tropical to subtropical region (Langenheim 1995). Plant resins have a rich fossil record in the form of amber or resinite. Amber and resinite are more or less synonymous terms describing geological material evolved from plant resin. The main difference lies in the fact that amber generally describes macroscopic remains, while resinite describes microscopic remains observed petrographically (Anderson & Crelling 1995). This may explain why ‘true’ amber is rarely described before the Cretaceous while resinite has been described in coal samples as old as Carboniferous (and maybe older). Among the oldest recognized ambers are Late Triassic ambers from Italy (Roghi et al. 2006), although some reports of Carboniferous amber exist (Smith 1896). This observation fits well with anatomical evidence that the earliest plants showing resin channels or resin-filled cells in their anatomy are members of the earliest but now extinct gymnosperm group, the Pteridospermopsida (Rothwell & Taylor

18


1972; Millay & Taylor 1977; Dunn et al. 2003). Although Pteridospermopsida emerge in the Late Devonian, the representatives with resin channels are from the Carboniferous. From this perspective, resin production seems to have evolved in the early gymnosperms. Analysis of the molecular composition of resinite and amber may therefore provide valuable information on the evolution of gymnosperms and angiosperms but is unlikely to elucidate the early evolution of land plants. Five chemical classes of ambers have been recognized (Anderson & Crelling 1995). A large majority of ambers is based on labdanoid diterpene (X) polymers (Class I amber). Less abundant are ambers based on cadinenes (XI) (sesquiterenoids) polymers (Class II ambers) (Anderson et al. 1992; Anderson & Crelling 1995). Class III–V resins are relatively anecdotic. While class I resins derive both from gymnosperms and angiosperms, class II resins only derive from Angiosperms, in particular the Dipterocarpaceae (Anderson et al. 1992). From this observation, the oldest resins and, in particular resinites from the Palaeozoic, should belong to class I and derive from gymnosperms. Amber or resinite samples older than the Cretaceous have often been studied by pyrolysis gas chromatography mass spectrometry (py-GC – MS) rather than by simple extraction. In the case of recent to Cretaceous resinous material, the py-GS– MS approach allows the successful identification of the structure and the class of the resin to be identified (Anderson et al. 1992; van Aarssen & de Leeuw 1992; Anderson & Botto 1993). The method has unfortunately proven much less successful in the case of older ambers or resinites, because most compounds liberated upon pyrolysis were poorly informative. In this way, Roghi et al. (2006) conclude that Triassic ambers from Italy have an affinity with class II or class I resins despite the fact that, due to their age, it is unlikely that these resins are class II. Similarly, the pyrolysates of Carboniferous resinlike material, that is, resinites isolated from coals (Crelling & Kruge 1998; Nip et al. 2009) and resin rodlets of pteridosperms (van Bergen et al. 1995) are dominated by alkane-alkene doublets, as well as alkylphenols and aromatics. This strongly contrasts with the pyrolysates of Cretaceous or younger resins. These results could reveal an ‘unknown extinct type of resin’ associated with Carboniferous plants (van Bergen et al. 1995). However, it seems highly plausible that, despite its reputation of excellent chemical preservation, amber also suffers from diagenetic aliphatization similarly to other macromolecular compounds (see below). As far as we know, no biomarker of taxonomic interest has yet been extracted from

Palaeozoic resinites. Amber and resinite still have to demonstrate their suitability for the study of terrestrialization. Elsewhere in plants (not only for plant resins), most of signalling and warfare is the matter of a large family of compounds: the terpenoids. The smallest compounds (the monoterpenoids) are highly volatile and therefore rarely preserved in sediments, the major exception being in amber. The terpenoids of higher molecular weight (referred to as sesqui-, di- and tri-terpenoids) are frequently observed in ambers and sediments. Monoterpenoids. Monoterpenoids mostly correspond to small odoriferous compounds incorporated in amber. Original monoterpenoids or their products of diagenetic transformation can therefore be observed. The extraction of amber frequently releases borneol, isoborneol and camphene (XII –XIV) (Armstrong et al. 1996; Czechowski et al. 1996). Monoterpenes found in amber could potentially be of taxonomic interest for plants of carboniferous or younger age, but not for the earliest plants (see above). In addition, this process would require that the plant which produced the resin is clearly identified. Sesquiterpenoids. Among the sesquiterpenoids, eudesmane and cadinanes are the most important for the study of terrestrialization. The eudesmane skeleton (XV) is present in many terrestrial plants, in particular angiosperms, but also in liverworts. Although it has also been described in a few sponges (Gross & Ko¨nig 2006), eudesmane is generally considered as a marker of terrestrial origin for petroleum and sediments (Philp 1994). Eudesmane is absent from petroleum older than Devonian age (Alexander et al. 1984), confirming its association with non-flowering plants. Often analysed with eudesmane is drimane (XV, XVI) which, however, very likely has a bacterial origin (Alexander et al. 1984) since it has been observed in Palaeoproterozoic sediments (Dutkiewicz et al. 2007). The presence of eudesmane in Palaeozoic coals is rarely reported. However, Dzou et al. (1995) observed significant amounts of eudesmane in Late Carboniferous coals from Pennsylvania. Although its presence was questioned by Borrego et al. (1999), eudesmane was also reported by del Rio et al. (1994) in late Carboniferous oil shales from Spain. These are the earliest reports of eudesmane in geological samples to our knowledge (Fig. 1), although we might expect an earlier appearance since this compound is present in some liverworts (Toyota & Asakawa 1990). The abundance of eudesmane in coal extracts decreases as maturity increases (Dzou et al. 1995), which might explain the rarity of reports of this compound in Palaeozoic sediments so far.


Cadinane (XVII) is thought to derive from cadinenes and cadinols which are ubiquitous in plants, bryophytes and fungi (Bordoloi et al. 1989) and from fragmentation of polycadinene resins (class II) produced by angiosperms (van Aarssen et al. 1990). Cadinane is particularly present in gymnosperm (class I) resins (Simoneit 1986; Grimalt et al. 1988). The dimers of cadinane, bicadinanes, are often observed in oils. They are generated by maturation of angiosperm (class II) resins (van Aarssen et al. 1990; Stout 1995). Cadinanes are therefore well-characterized higher plant biomarkers which are often observed in Cretaceous or younger sediments (van Aarssen et al. 1990). So far, fully saturated cadinanes have not been observed in Palaeozoic sediments. However, their aromatic counterparts – cadalenes (XVII) – have been found in the extracts of different coals of Carboniferous age (del Rıó et al. 1994; Stefanova et al. 1995; Armstroff et al. 2006). Its earliest occurrence reported so far is Visean (Armstroff et al. 2006) (Fig. 1). Diterpenoids. Particularly abundant among conifers and their ambers are diterpenoids with abietane, pimarane, kaurane and podocarpane (XVIII –XX) skeletons. They are mostly produced by higher plants, though some marine algae also synthesize these compounds in a much functionalized form (Simoneit 1986). According to the review of Alexander (1987a), the different land plants can be recognized from their specific diterpenoids contribution. Bryophytes and pteridophytes differ from gymnosperms by their absence of abietane, beyerane and phyllocladane (XVIII, XXII, XXIII) skeletons. The appearance of these latter compounds in the sedimentary record could therefore document the transition from ‘horizontal’ to ‘vertical’ land plants. Phyllocladane, in particular, would be a specific biomarker for conifers. The occurrence of the fully saturated diterpenoids in Permian and Carboniferous coals is relatively frequent (e.g. Noble et al. 1985; Schulze & Michaelis 1990; Fleck et al. 2001; Fabianska et al. 2003; Piedad-Sańchez et al. 2004; Izart et al. 2006); phyllocladane, ent-beyerane and ent-kaurane (XX –XXV) are often reported in particular. The presence of phyllocladane and ent-beyerane in these samples is consistent with the evolved flora which existed in the Late Carboniferous. The study of Schulze & Michaelis (1990) on Carboniferous coals from Germany showed that ent-kaurane is more abundant in the Westphalian samples from the Ruhr, while ent-beyerane and phyllocladane are more abundant in the Westphalian and Stephanian coals from the Saar. The authors proposed that this change might be due to different inputs of higher plants, possibly related

19

to the different sedimentary settings (limnic in the Ruhr v. paralic in the Saar). Changes in the pentacyclic terpenoids were also documented in these coals (Vliex et al. 1994; Auras et al. 2006) (see below). The presence of ent-beyerane, ent-kaurane and phyllocladane in Lower Carboniferous sediments has led to the suggestion that a precursor of the conifers already produced these compounds at that time (Disnar & Harouna 1994). Since these compounds do not occur in the Pinaceae, it has been suggested that the Pinaceae separated early from the other conifers (Armstroff et al. 2006), implying that conifers had already evolved in the Early Carboniferous. Sheng et al. (1992) described an abundance of tetracyclic diterpanes in Middle Devonian humic coals from China. Among the identified compounds are 17-norphyllocladanes, ent-beyerane and entkaurane. This corresponds to the earliest reported occurrence of ent-kaurane and ent-beyerane (Fig. 1). Palaeobotanical data indicate that these Middle Devonian coals mainly derive from pteridophytes (Sheng et al. 1992). These are plants which, according to the review of Alexander et al. (1987a), should neither contain phyllocladane nor beyerane. The absence of phyllocladane from the Middle Devonian coals therefore appears consistent with the absence of conifers during this period, while the presence of ent-beyerane questions either the origin of this compound in the Devonian coals or its absence from pteridophytes (Sheng et al. 1992). As far as we know, the oldest reported occurrence of phyllocladane is Serpukhovian that is, late Early Carboniferous (Fabianska et al. 2003; Izart et al. 2006) (Fig. 1). Totally or partially aromatized compounds deriving from the tricyclic terpenoids are also frequently reported in sediments. The most common compounds are retene and simonellite (XXVI – XXVII) which are thought to derive from the aromatization of abietane. However, Alexander et al. (1987b) demonstrated in Miocene coals that retene and simonellite are more likely derived from phyllocladane and kaurane. Retene has been described in the extracts of numerous Carboniferous coals (del Rıó et al. 1994; Stefanova et al. 1995; Fabianska et al. 2003; Armstroff et al. 2006; Izart et al. 2006). Armstroff (2004) also describes the presence of retene in Frasnian cannel coals from Russia. To our knowledge, this is the earliest reported occurrence of retene which can be confidently associated with a terrestrial origin (Fig. 1). If, as proposed by Alexander et al. (1987b), retene from land plants derives from aromatization of kaurane, its presence in Devonian coals has no strong significance as kaurane is mostly associated with Bryophyta and Pteridophyta. Conversely, if it is demonstrated that retene only derives from abietane or from

20


phyllocladane, its presence in Devonian sediments would document that at least the biosynthesis of abietic acid (if not conifers) already existed in the Fammenian. Retene, however, has also been observed in the extracts of several Lower Palaeozoic to Precambrian carbonates, where inputs from terrestrial plants are not likely (Jiang et al. 1995; Zhang et al. 1999). An algal and/or bacterial source was proposed by these authors. Consistent with this conclusion, retene was also observed (although in low amounts) in the pyrolysates of a green alga and cyanobacterium cultures (Wen et al. 2000). Care is therefore recommended in the interpretation of the presence of retene in sediments where inputs from higher plants are low and, most particularly, in Ordovician– Silurian sediments. Triterpenoids. The triterpenoids are a very large family which comprises the well-known group of bacterial biomarkers, the hopanoids, as well as the hypersalinity biomarker gammacerane (XXVIII) (Simoneit 1986). Several higher plant biomarkers also belong to this family, the most famous compound being oleanane (XXIX) (Simoneit 1986). According to a recent review of the distribution of pentacyclic triterpenes by Jacob (2003), some skeletons are particularly widespread among angiosperms such as oleanane, lupane, friedelane and ursane (XXIX –XXXII). At least one skeleton, the serratane (XXXIII), would be characteristic of gymnosperms, mosses, ferns, lycopodiophytes and bryophytes. Although it has been observed in several angiosperms (and in particular Poaceae), fernane (XXXIV) is in particular present among ferns (Jacob 2003). In relation to their abundance in angiosperms, the occurrence of oleanane, lupane, ursane and their derived compounds is mostly restricted to Cretaceous or younger oils and sediments (Peters et al. 2005). The presence of oleanane in Carboniferous sediments has however been described by Moldowan et al. (1994). This was followed by a long investigation in order to identify the source of this compound in Palaeozoic sediments. Recent studies identified Gigantopterids as the source of oleanane in Palaeozoic sediments which, added to morphological arguments, would place the appearance of the angiosperm lineage before the Permian (Taylor et al. 2006). Apart from the rare reports of oleanane, the terrestrial triterpenoids more often described in Palaeozoic sediments are aromatic compounds belonging to the arborane/fernane family which have been recently named MATH (5-methyl10(4-methylpentyl)des-A-25-norarbora(ferna)-5,7,9triene), MAPH (25-norarbora(ferna)-5,7,9-triene), DAPH1 (24,25-dinorarbora(ferna)-1,3,5,7,9-pentaene) and DAPH2 (iso-25-norarbora(ferna)-1,3,5,

7,9-pentaene) (Vliex et al. 1994; Borrego et al. 1997; Izart et al. 2006) (XXXV –XXXVII; Fig. 1). The fact that only aromatic compounds are reported may be due to maturity as Paull et al. (1998) observed fernenes in very immature sediments of Triassic age. The aromatic arborane/fernane derivatives were observed to be present in Stephanian coals from Germany, but almost absent from the underlying Westphalian coals (Vliex et al. 1994; Auras et al. 2006). Vliex (1994) related this feature to the increase of Gymnospermopsida (Coniferales) in the vegetation, linked to a transition to a drier climate. Due to the imprecision on the exact structure of the molecules, arborane or fernane derivatives could either originate from higher plant fernenes or from isoarborinol (XXXIX). The latter is a compound present in a few angiosperms but which has been assigned a mostly bacterial origin (Hauke et al. 1992, 1995; Jaffe´ & Hausmann 1995). As a matter of fact, aromatic arborane/fernane derivatives have also been observed in several sediments where terrestrial inputs are seemingly inexistent (Hauke et al. 1992). According to Hauke et al. (1995), however, the compounds identified by Vliex et al. (1994) are true fernane derivatives. Recently, a detailed geochemical and botanical study of these Stephanian coals allowed Cordaites to be identified as the source of these fernane derivatives (Auras et al. 2006).

Skeletal materials Organisms living on land lack the support of water to overcome gravity and therefore have to strengthen or develop supportive tissues. If we consider the present-day skeletal biopolymers, which are potentially stable enough to survive in the fossil record on a regular basis and thus potentially leave a fingerprint of the terrestrialization process, we often observe these are at the boundary between the cell/organism inside and its outside and combine their structural function with protection, for example, cuticles. They consist of only four basic building blocks produced by ancient biosynthetic pathways common to Archaea, Bacteria and Eukarya (Kandler & Ko¨nig 1998). These building blocks are sugars, amino acids, long-chain lipids and aromatics. Sugars, amino acids and their polymers – chitin. Among the earliest such structures are probably the peptidoglycans (amino acid –sugar polymers) found in the cell walls of Bacteria and Archaea. Peptidoglycans are known to be resistant to degradation compared to proteins and are observed in recent sedimentary organic matter (Grutters et al. 2002; Nagata et al. 2003). However, they do not account for an important part of the organic matter


(Veuger et al. 2006). Although sugars and amino acids may severely crosslink and form degradationresistant polymers (Maillard 1912), they have not been used for evolutionary or environmental reconstruction. Probably, they are too omnipresent and taxon-unspecific for these purposes. Polysaccharide synthesis is also ancient. Cellulose is produced by cyanobacteria and proteobacteria. It has been suggested that the ability of vastly unrelated eukaryotic species to produce cellulose has been acquired via endosymbiosis with these bacteria and lateral gene transfer (Niklas 2004). Despite a large chemical diversity in peptidoglycans and polysaccharides among organisms, most are degraded. This explains why there is so little evidence of fossil bacterial polymeric products, despite the bacterial omnipresence. Only cellulose and chitin appear to be relatively resistant to biodegradation and form a considerable fossil record. The refractory character of these macromolecules is clearly related to the exact composition of the monomers and their stereoconfiguration in the polymer. This is demonstrated by comparing the extremely low fossilization potential of starch (poly 1 ! 4 b-d-Glucose) with that of cellulose (poly 1 ! 4 a-d-Glucose) (Fig. 3). The polysaccharide chitin (N-acetyl-d-glucosamine; Fig. 4) which is so abundant in arthropods and oomycetes today is not known from prokaryotes (Niklas 2004). The capability to synthesize chitin is

(a)

CH2OH

CH2OH

O

O

H H H

H H

H

H

OH

H

O

O

OH

(b)

H

OH

H H H

H H

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OH

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CH2OH H H

H

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OH

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OH

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CH2OH

β–D–glucose

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H

H H

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α–D–glucose

(c)

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CH2OH

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OH

therefore onsidered to have arisen much later in evolution compared to cellulose synthesis. Its presence in many marine organisms such as arthropods, molluscs and annelids places its evolution well before the evolution of land-adapted organisms, however. Studies on chitin preservation provide another argument as to why this substance is not suitable for unravelling the terrestrialization process. Laboratory experiments show that chitin belongs to the most degradation-resistant parts of arthropods (Baas et al. 1995; Briggs et al. 1995). At first sight, this is not surprising since arthropod cuticles are also abundant in the fossil record. But are these cuticles still made of chitin? The oldest known traces of the chitin marker D-glucosamine (XXXX) occur in extremely wellpreserved weevil cuticles (up to 0.6% of the organic matter) present in the 25 Ma lacustrine sediments from Enspel (Stankiewicz et al. 1997; Flannery et al. 2001). Less well-preserved or older arthropod cuticles show no such traces of chitin (Stankiewicz et al. 1998; Gupta et al. 2007a). This alone probably explains why chitin could not be detected in chitinozoans (Voss-Foucart & Jeuniaux 1972; Jacob et al. 2007); the biological affinity of the chitinozoa therefore remains unresolved. This also implies that a reassessment of the presence of chitin in Palaeocene dinoflagellate cysts (Belayouni & Trichet 1980) is called for. Mostly, chitin-barren

CH2OH H

21

H OH

H

H

OH

H OH

H

H

OH

H OH

H

H

OH

H OH

H

H

OH

O

O

O

O

O

Fig. 3. Structural formulas of (a) cellulose which is made of (b) glucose and (c) starch (which is also made of glucose).

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G. J. M. VERSTEEGH & A. RIBOULLEAU CH3 O

O NH

H O

H

CH2OH

NH

O CH3

H

H H

O

OH

H

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NH

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H O CH2OH

OH O

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H

OH O

H

OH

H

H H

CH2OH

NH

O H

H

H

CH2OH

NH

O

H

CH2OH

NH

OH

CH3 O

CH3

CH3

CH3

Fig. 4. Example structure of chitin.

fossil cuticles release series of alkanes and alkenes upon pyrolysis, suggesting that the chitin has been replaced and/or transformed by an aliphatic geopolymer. Experimental evidence suggests that these aliphatic compounds may in fact be lipids that have become attached to the biomacromolecule. These lipids are likely to originate from the closest source available, the organism itself (Gupta et al. 2006, 2007b; de Leeuw 2007).

via the phenylpropanoid pathway, namely the monolignols p-coumaryl, coniferyl and sinapyl alcohols (XXXXI –XXXXIII) (de Leeuw & Largeau 1993; Raven 2000) (Fig. 4). The polymerization reaction has long been considered to be a random process but this concept appears to be wrong (see reviews of both Lewis 1999; Davin & Lewis 2005). The corresponding degradation products are coumaryl, guaiacyl (or vanillyl) and syringyl moieties (XXXXIV –XXXXVI), respectively (Hedges & Mann 1979). Differences in the abundance of the structural lignin compounds are observed among higher plants: guaiacyl units dominate in gymnosperms wood, syringyl and guiacyl units are dominant in woody tissues of dicotyledonous angiosperms, p-coumaryl and guaiacyl dominate in woody tissues of monocotiledonous angiosperms and non-woody tissues are generally dominated by p-coumaryl units (Hedges & Mann 1979; Logan & Thomas 1985). Pteridophyte lignins are derived from sinapyl alcohol (Barcelo et al. 2007). From these observations, the respective abundance of the three units in sedimentary organic matter should change in parallel with the evolution of land plants (Logan & Thomas 1987). Although structural motifs of syringyl peroxidases (an enzyme in lignin synthesis) have been identified in Bryophytes (Ros et al. 2007), lignin is absent in these plants (Lewis & Yamamoto 1990). Lignin has also been reported from a red algae which is considered a case of parallel evolution of lignin synthesis (Martone et al.

Aromatics and their polymers – lignin. Aromatic polymers are lignin (Fig. 5) as are at least some sporopollenins (Boom 2004). There are some enigmatic algal biomacromolecules with high preservation potential such as the wall material of dinoflagellate cysts. The wall material is currently referred to by the cryptic name ‘dinosporin’. Although dinosporin has been suggested to be aromatic with the isoprenoid tocopherol as an aromatic building block (Kokinos et al. 1998), this view has been challenged by others (de Leeuw et al. 2006). The position of dinosporin in the scheme presented above therefore remains unclear. Apart from this single report of a possible aromatic signature in dinosporin and the increase of phenolic moieties in the algaenan of the Ordovician freshwater acritarch Gloeocapsamorpha prisca in relation to salinity increase (Derenne et al. 1992), the presence of aromatic moieties seems to be a feature of terrestrial biomacromolecular organic matter. Lignin is a macromolecule resulting from the polymerization of three phenolic units synthesized OH

OH

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OH

OH HO

HO

O HO

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OH O

O HO

HO

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HO O HO

O

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OH

O

OH

O O

OH

OH

HO

O

O

HO

O O O OH

Fig. 5. Example structure of lignin (based on Holtman et al. 2003).

OH

O

OH


2009). The results obtained by Logan & Thomas (1987) on different Carboniferous plants were consistent with this idea: guaiacyl oxidation products were mostly detected from Sigillaria ovata, a plant which contained woody tissues, while no guaiacyl units were obtained from Lepidodendron and Lepidophloios which were mostly non-woody plants. However, these results should be regarded with care since monolignols also are building blocks of lignans (Lewis & Davin 1999). As discussed above, these latter compounds are widespread among tracheophytes and are also present in bryophytes (Lewis & Davin 1999; Raven 2000). Consistently, the three lignin phenols were observed (although in low amounts) in the oxidation products of different bryophytes (Logan & Thomas 1985). A second problem with lignin phenols is that, during diagenesis, all three units degrade differently. The general order of resistance is p-coumaryl . guaiacyl . syringyl (Hedges et al. 1985; Logan & Thomas 1985; Orem et al. 1996). Among diagenetic/catagenetic transformations of wood are demethoxylations which also naturally lead to the diminution of syringyl and guaiacyl units, favouring p-coumaryl units in the remaining tissues (Orem et al. 1996; Hatcher & Clifford 1997). A significant contribution of p-coumaryl units was obtained by Logan & Thomas (1987) in the oxidation products of Carboniferous Sigillaria ovata. This feature could reflect both the diagenetic increase of these units due to decarboxylation of lignin units and the contribution of lignan from bryophytes. Several alkylphenols were observed in the flash pyrolysates of the Lower Devonian plants Renalia, Zosterophyllum and Psilophyton (Ewbank et al. 1996). Alhough these compounds may correspond to lignin pyrolysis products, in particular after diagenetic demethoxylation of lignin, their presence in the pyrolysates of Lower Devonian plants does not unequivocally attest for the presence of lignin in these early plants; they could also derive from the pyrolysis of condensed tannins (Ewbank et al. 1996). Despite its interest, the study of Ewbank et al. (1996) mostly demonstrated that, since pyrolysis products are poorly characteristic, flash pyrolysis is not suited to molecularly characterize the material of early land plants. The development of spores (and pollen) is an important requisite for terrestrialization since it enables dispersion of gametophytes through air. The effective UVB absorbance of aromatic rings (Pfu¨ndel et al. 2006) may play a role in protecting airborne pollen; variations in the aromatic content of fossil pollen have been proposed as a UVB proxy (Rozema et al. 2001, 2002b). However, this proxy is based on pyrolysis of the (fossil) pollen. The coumaric and ferulic moieties produced in this way are probably derived from sporopollenin-

23

type biopolymers in the pollen wall and not derived from compounds believed to regulate UV damage (de Leeuw et al. 2006). The structure of sporopollenin, the wall polymer of pollen and spores, has long been a matter of debate and it seems likely that both aliphatic and aromatic sporopollenins occur (de Leeuw et al. 2006). Although the structure of the aliphatic sporopollenins is unclear, the aromatic sporopollenin consists of coumaric, ferrulic and sinapic acids (VII –IX) as building blocks. These are the same building blocks for lignin but with propyl-acids in stead of propyl-alcohols (Boom et al. 2005). Biosynthetically, the lignols are formed from these carboxylic acids by reduction and it is interesting to note that, prior to the evolution of lignin synthesis, plants already were able to produce the biopolymer sporopollenin. Recently, it has been demonstrated that one of the key enzymes in the phenylpropanoid pathway needed to convert the phenylpropanoid acids into their alcohols, 4-coumarate:CoA ligase (4CL) (Ferrer et al. 2008) already occurs in the Bryophyte Physcomitrella patens (Silber et al. 2008). The presence of a similar enzyme cinnamate:CoA ligase (ScCCL) in the bacterium Streptomyces coelicolor (Kaneko et al. 2003) suggests that this part of the pathway has a much longer history than previously expected. It would be interesting to know to what extent the phenylpropanoid pathway had to evolve in order to arrive at sporopollenin synthesis and further to lignin biosynthesis. Another open question is why, later in evolution, lignin and not sporopollenin became a major structural element in vascular plants. Although apparently the earliest land plants already produced spores, it is not known where in evolution the synthesis of sporopollenin started. Sporopollenin has been claimed to be produced by Coleochaete (Delwiche et al. 1989), a member of the Characeae which is a sister group of Embryophytes (Waters 2003). However, due to a lack of insight in the nature of sporopollenin in the past and despite increasing insight into the nature of acid- (and acetolysis-) resistant algal walls (e.g. de Leeuw et al. 2006) this has not yet been resolved. One method of shedding light on sporopollenin evolution could be a systematic analysis of the structural diversity (if any) of sporopollenins of primitive land plants and their closest relatives.

Organic matter transformation Composition and preservation An important step in investigating the relation between fossil organic matter and its source organisms from a chemical point of view is assessing

24


the extent to which the biomolecules survive taphonomic processes. Knowledge of present degradative pathways also provides a key to the past, enabling the sedimentary organic molecules to be linked to their biological sources. Through this, the evolution of past life and environment can be reconstructed. Biological tissues are made of different types of molecules which can be broadly classified according to their chemical functions into carbohydrates (simple sugars and polymers among which cellulose), lipids, peptides (simple amino acids and their polymers, the proteins) and lignin, the principal component of wood. Although different from peptides, nucleic acids (which are the building blocks of DNA) have a fate which is similar to that of peptides during burial, and therefore can be assimilated to peptides. After organism death and during burial in sediments, the organic matter is bio- or chemically degraded. This results in an important loss of the organic material, but also to chemical modifications of the biomolecules. After this stage, the original material can be either totally unrecognizable or recognizable to a certain degree. During this transformation of biomolecules to geomolecules (the diagenesis), the fate of the different classes of compounds is very different: simple sugars and peptides are generally rapidly mineralized while lipids, complex sugars, sporopollenin and lignin are less easily degraded and therefore have a higher chance of being buried in sediments. The sedimentary environment is clearly of prime importance. Burial rates, primary productivity, oxygen availability, water depth, organic matter concentration and mineral composition all influence organic matter preservation (Tyson 2001; Burdige 2007; Rothman & Forney 2007). In addition, the initial chemistry of the organic matter is also important (Middelburg 1989; Sinninghe Damste´ et al. 2002; Versteegh & Zonneveld 2002; Prahl et al. 2003). From the study of the organic matter deriving from a wide variety of sedimentary and diagenetic environments, a series of preservation pathways has been proposed (de Leeuw & Largeau 1993; de Leeuw et al. 2006; de Leeuw 2007). The degradation–recondensation pathway (Tissot & Welte 1984) is based on the formation of macromolecular organic matter by random, post-mortem polymerization reactions of degradation residues. Because the organic matter involved in this pathway is generally highly degraded, the deduction of the biological affinities of the fossil organic matter preserved along this pathway is somehow complicated. In contrast to this, the selective preservation pathway (Philp & Calvin 1976; Tegelaar et al. 1989b) assumes that the biomolecules preserve as they have been synthesized. This pathway concerns

many lipids and a few specific biomacromolecules including lignin. Selective preservation of macromolecules is generally associated with the preservation of the morphology (Largeau et al. 1986) although the opposite, excellent morphological preservation, does not imply excellent chemical preservation (see review of de Leeuw et al. 2006; de Leeuw 2007; Gupta et al. 2007b). Biomolecules preserved through this pathway are highly recognizable, even after millions of years of burial (Derenne et al. 1988). The natural sulphurization (Sinninghe Damste´ & de Leeuw 1990) and oxidative polymerization pathways (Harvey et al. 1983; Versteegh et al. 2004; de Leeuw 2007; Gupta et al. 2007b) stress that free sulphur species and oxidizing agents cause condensation and crosslinking, respectively, of both lipids and macromolecules. This reduces the bioavailability of the material so that labile compounds that otherwise would have been mineralized may escape into the fossil record (Kok et al. 2000). Molecules preserved through this pathway can retain most of their original specificity, even after long periods of time (Koopmans et al. 1997; Versteegh et al. 2007). Clearly, due to the much higher availability of oxygen in air and much longer oxygen exposure times, the oxidative polymerization pathway is particularly likely to happen on land. Burial to important depth, or for long periods of time will also lead to the thermal modification of the organic matter (OM). This process, termed cracking, is the base of petroleum and natural gas formation. The particular organic matter becomes increasingly aromatic and cyclic by selective removal of the aliphatic components and by aromatization and cyclization of the residue. The more the compound is thermally degraded, the less will its original structure will recognizable. Although maturation of organic matter may play an important role in relatively young sediments (provided temperature is sufficiently high), this is a clear issue on Palaeozoic and older material (Roberts et al. 1995; Yule et al. 2000) where slow transformation at mild temperature conditions is compensated for by long periods of time. The same is true for changes in the composition of stable carbon and hydrogen in the organic matter. This results in a 13C depletion of the released compounds and a 13C enrichment of the kerogen (Schimmelmann et al. 2001). For hydrogen, changes are larger and depend on the compounds considered. In particular, hydrogen on tertiary carbons (e.g. in isoprenoids) is subject to exchange with the surrounding water (Pedentchouk et al. 2006). Nevertheless, shifts are minor compared to the natural variations in the distributions of these stable isotopes in organic matter (Schimmelmann et al. 2001; Pedentchouk et al. 2006).


Aliphatization and related problems Studies on the macromolecular nature of Palaeozoic and older acritarchs have shown both aliphatic and aromatic wall compositions (Kjellstro¨m 1968; Collinson et al. 1994; Arouri et al. 1999, 2000; Foster et al. 2002; Dutta et al. 2006). Others have concentrated on the biomarker lipids associated with the acritarchs (Moldowan & Talyzina 1998; Talyzina et al. 2000) and the host sediments (Meng et al. 2005), and have drawn conclusions on the biological affinities of the acritarchs. What are the consequences for the application of organic geochemistry to elucidating the terrestrialization of life? Considering both the diagenetic and catagenetic processes, attributing an aromatic or aliphatic contribution to an original biomacromolecular structure remains problematic. As long as the lipids which have become incorporated in the macromolecular matrix post mortem have been derived from the source organisms themselves, the approach of carefully releasing and analysing these lipids seems to be the more successful approach. Analogous to the transformation of chitinous biomolecules into aliphatic geomolecules (see above), sporopollenin and other biomacromolecules seem to transform chemically over time. Whereas fresh megaspores of Isoetes and Salvinia are purely aromatic, the fossil material consists of a mixture of aliphatic and aromatic moieties, again suggesting addition of long-chain aliphatic compounds (van Bergen et al. 1993; Boom 2004). Furthermore, the cyst walls of the recent dinoflagellate Lingulodinium polyedrum seem to be non-aliphatic (Kokinos et al. 1998) whereas fossil dinoflagellate cysts have been reported to contain mixed aromatic and aliphatic moieties (de Leeuw et al. 2006). An extreme case of aliphatization by condensation of aliphatic lipids has been described for ‘dinocasts’ from the Eocene of Pakistan: the relatively solid to spongy dinoflagellate-shaped structures occurring in the sediments are believed to represent the oxidatively polymerized cell contents of motile dinoflagellates (Versteegh et al. 2004). Although addition of aliphatic components modifies the signature of several aromatic biomacromolecules (chitin, sporopollenin) such processes seem to be absent for fossil lignin. This may result from the fact that, in most cases, the membrane lipids are very closely located to the biomacromolecule; in lignin there are no lipids around. As such, this may be an indirect and circumstantial piece of evidence for the oxidative polymerization pathway. It is not only aliphatics which are subject to oxidative polymerization. This process also applies to the terpenoids in resins, leading to resin hardening and amber formation. One may wonder to what extent the oldest ambers, which are dominated

25

by aliphatic moieties (van Bergen et al. 1995), were originally aliphatic or have become so by aliphatization. For initially aliphatic biomacromolecules such as cutin, cutan and algaenan, the post mortem aliphatization is intrinsically much more difficult to detect. The incorporation of free lipids to the naturally resistant algaenan of Botryococcus race A by oxidative cross-linking has been clearly demonstrated in coorongite (Gatellier et al. 1993), a rubbery material derived from the accumulation of algal remains on the shores of lakes. As Botryococcus free lipids and algaenans were both aliphatic, the aliphaticity of coorongite was very similar to that of the algaenan; however, the signature upon pyrolysis was significantly different (Gatellier et al. 1993). For Botryococcus braunii race B, the algaenan walls also incorporate polyacetals of polymethylsqualanes. This may provide a clear marker for the presence of cell walls of this taxon in sediments (Metzger et al. 2007). However, in this case assessment of the degree of change of the original biopolymer by the post mortem oxidative polymerization of membrane and other associated free lipids also remains problematic. One of the classical examples of the selective preservation pathway is the algaenan of fossil Tetraedron envelopes from the Messel Oil Shale. Apart from being strikingly well-preserved morphologically, the chemical fingerprint of these cuticles upon flash pyrolysis closely resembles its modern counterpart (Goth et al. 1988). But what difference would a contribution of aliphatic lipids from the organism have made? Similarly, oxidative polymerization of aliphatic lipids has been suggested to have played a role in the formation of the aliphatic algaenan of the Ordovician alga Gloeocapsamorpha prisca (Blokker et al. 2001), but it is difficult to ascertain to what extent this aliphatic material corresponds to the original cell walls. An analogous problem is illustrated on cutin and cutan. The ether cross-linked cutan of CAM plants is, chemically speaking, more stable than ester cross-linked cutin of most other higher plants: cutin is broken down into its original monomers upon base hydrolysis while cutan resists this treatment. Since the fossil plant cuticles also survive base hydrolysis, they have been considered to represent selectively preserved cutan (Tegelaar et al. 1989c). However, fossil non-hydrolysable cuticles are known from plants that do not produce cutan (Gupta et al. 2006b, 2007b; de Leeuw 2007). In fact, the depositional environment of CAM plants does not at all favour cutan preservation whereas several cutin-producing plants occur in or near excellent preservational environments. Laboratory experiments using elevated temperature and pressure have recently demonstrated that, similar

26


to chitin, lipids may become incorporated in cutin in due course (Gupta et al. 2006a). It finally appears that most of the previously observed fossil cutans in fact correspond to cuticle lipids which were oxidatively linked during diagenesis (van Bergen et al. 2004). Even relatively simple lipids are not always easy to relate to their source. Although structural modification such as loss of functional groups or changes in stereochemistry do not usually prevent assignment to their source organisms (e.g. Sinninghe Damste´ et al. 1997; Moldowan & Talyzina 1998) they may disappear from the analytical window. The corollary of aliphatization is that free lipids may become part of larger macromolecular structures so that extra analytical steps are required for their detection and identification (e.g. Adam et al. 2006). For the particular organic matter, we may have visual information on the biological affinities of the fossils at hand, but to what extent is this matched by the chemical composition of the fossils? It seems that much of the aliphatization is brought about by lipids from the immediate surroundings of the original biomacromolecule, that is, derived from the source organism. Moreover, our present understanding of the natural sulphurization and oxidative polymerization pathways imply that these added substances survived relatively undamaged structurally and isotopically. This means that there should still be a fair chance of obtaining information on the nature of the source organisms, provided the individual products released upon chemical degradation or (offline) pyrolysis can be related to a single source and metabolic pathway (van Dongen et al. 2002; van Bergen & Poole 2002; Poole et al. 2004). Aliphatization of macromolecular material from plants and animals therefore seems to be ineluctable, which complicates the identification of the molecular characteristics (and therefore the biosynthetic pathways) of very old organic matter.

Conclusion Organic geochemistry plays an important role in the elucidation of the history of early life (Brocks et al. 1999; Brocks & Summons 2003; Summons et al. 2006). Similarly, it should play a role in understanding the terrestrialization process, in particular for plants. Numerous molecular biomarkers of terrestrial plants, deriving either from structural tissues such as lignin phenols, from epicuticular waxes or from the large class of terpenoids exist, and they are widely used in Tertiary and recent sediments. The study of the terrestrialization process with organic geochemistry is associated with numerous

difficulties, however, in particular in assigning Palaeozoic fossil organic matter to its source. Apart from the fact that the samples have often suffered from thermal alteration, the difficulties mostly arise from a lack of taxonomic precision of the molecular biomarkers. Other difficulties arise from the frequent chemical modification of the material, despite excellent morphological preservation (e.g. aliphatization). All these difficulties easily explain the relatively large temporal gap which currently exists between the earliest microscopic plant remains documented in Middle Ordovician (Strother et al. 1996) and the earliest unambiguously documented terrestrial biomarkers in Middle Devonian (Sheng et al. 1992). Despite this, the set of currently identified molecules of terrestrial origin is already sufficiently good to discriminate changes in plant associations during the Carboniferous, revealing further information on the terrestrialization process. It is additionally hoped that condensation processes, which remove lipids from the pool of bioavailable products, may conversely facilitate the survival of specific lipids over long periods of time and, as such, record the biochemical evolution related to the terrestrialization in the sediments. Advancement of the assessment of the stable carbon and hydrogen isotopic compositions on lipids or (offline) pyrolysis products increasingly contributes to unravelling the evolution of biosynthetic pathways and diagenetic overprints. Great advances will also be made with the development of micro-scale techniques (microsampling, micro extractions and nano-SIMS). These techniques will allow the study of fossils present in very low amounts such as very early spores and cuticles, or the study of monospecific fossil associations. Another rapidly developing approach to resolving terrestrialization involves genomics: tracing the evolution of enzymes critical to the biosynthetic pathways involved in the terrestrialization process. Terrestrialization and earliest plants had previously failed to attract many organic geochemists. However, this is changing as demonstrated by several recent studies and review papers (van Bergen et al. 2004; Armstroff et al. 2006; Auras et al. 2006). It is therefore likely that the right compounds have not been looked at in the right place and with the right techniques – yet. We thank M. Vecoli (UST Lille) and G. Clement (MNHN, Paris) for inviting us to the ECLIPSE II Workshop: Terrestrialization Influences on the Palaeozoic Geosphere– Biosphere. We also thank J. de Leeuw (Utrecht University) and M. Vecoli for constructive comments on the manuscript. H. Kerp (Mu¨nster University) is thanked for his help on the occurrence of resin in early gymnosperms. Financial support for GJMV by the USTL (Lille) is gratefully acknowledged.


27

Appendix Structural formulae of the compounds mentioned in the text.

4'

O

7

A

C

2

5' 3

O

O O

II 5-O-Methylginkgetin (a biflavonoid)

OH; positive charge on C-ring Isoflavanone: Aryl migration to C3; R2, C=O

I Flavonoid backbone

O

O

Anthocyanidin: O1=C2; C 3=C4; R2, H or

R2

O

HO

HO

Flavonol: C2=C3; R1, OH; R2, C=O

R1

4

5

O

Flavanone: R1, H; R2, C=O 3-OH-Flavanone: R1, OH; R2, C=O Flavan-3-ol: R1, OH; R2, H Flavone: C2=C3; R1, H; R2, C=O

3'

B

OH OH HO

O

O

R OH O

HO

OH OH

R

OH

OH HO

IV Pterocarpan backbone

III Kaempferol

R

OH

O

O

n OH

O

O

OH

O

O

OH

O

OH

R OH

OH

V Anthocyanidin (condensed Tannin)

O OH

VI Hydrocynnamic acid

O

O

OH

VII p-Coumaric acid

OH

VIII Ferulic acid

IX Sinapic acid

H

H

OH

H

H OH

X Labdanoid backbone

XI Cadinane

H

XII Borneol

XIII Isoborneol

XIV Camphene

XV Eudesmane

H H

H H

H H

H H

H

XVI Drimane

XVII Cadalene

H

H

XVIII Abietane

XIX Pimarane

XX Kaurane

XXI Podocarpane

XXVI Retene

XXVII Simonellite

17

H H

XXII Beyerane

H

H

H

XXIII Phyllocladane

H

H

XXIV ent-Beyerane

XXV ent-Kaurane

28


H

H

H

H

H H

H

H

H

H

H

XXVIII Gammacerane

H

XXXI Friedelane

XXX Lupane

XXIX Oleanane

XXXII Ursane

H

H

XXXIII Serratane

XXXIV Fernane

XXXV MAPH

XXXVI MATH

O H 2N

OH OH

HO

XXXVII DAPH 1

OH

OH

O OH

XXXXI p-Coumaryl alcohol

XXXX D-glucosamine

XXXIX Isoarborinol

XXXVIII DAPH 2

OH

OH

O

O

O

OH

OH

XXXXII Coniferyl alcohol

XXXXIII Sinapyl alcohol

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XXXXIV p-Coumaryl unit

O OH

XXXXV Guiacyl / Vanillyl unit

O OH

XXXXVI Syringyl unit

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The effects of terrestrialization on marine ecosystems: the fall of CO2 PAUL K. STROTHER1*, THOMAS SERVAIS2 & MARCO VECOLI2 1

Palæobotany Laboratory, Weston Observatory of Boston College, Department of Geology and Geophysics, 381, Concord Road, Weston, Massachusetts 0493, USA 2

Universite´ Lille 1, FRE 3298 CNRS Geósyste´mes, Laboratoire de Paleóntologie, Cite Scientifique, F-59655 Villeneuve d’Ascq, France *Corresponding author (e-mail: [email protected]) Abstract: The rise of land plants during the early Palaeozoic had profound effects upon subsequent Earth history and evolution. The sequestration of standing biomass and carbon burial caused a primary shift in the distribution of active carbon within the biosphere and surficial Earth systems. This manifested itself in a dynamic decline in pCO2 during Silurian– Devonian time, affecting both terrestrial and marine ecosystems. We examined first-order correlations between terrestrialization and pCO2 by comparing the GEOCARB III data with time-constrained fossil events in the early evolution of land plants. We compared the same GEOCARB III data with the species/genus richness of lower Palaeozoic acritarchs. The correlation between the rise of woody plants and pCO2 is built into the GEOCARB model for the Late Devonian and later, but pCO2 begins to decline in the Cambrian long before the origin of woody trees (lignophytes). The influence of early phases in plant evolution may be seen in a two-stage pCO2 decline corresponding to fossil evidence for the origin of thalloid bryophytes in the Middle Cambrian and the origin of tracheophytes near the Ordovician–Silurian boundary. The decline of the acritarchs shows a highly correlated lag of about 10 Ma with respect to the pCO2 decline. The relation between pCO2 and acritarch species richness suggests a tight coupling between the evolution of the marine phytoplankton and atmospheric CO2, supporting previous suggestions that pCO2 was a significant causal factor in the near extinction of acritarchs by the end of the Devonian.

There are two periods in Earth’s history when biological innovation in photosynthetic organisms profoundly and irreversibly altered the global chemical environment. The first occurred with the evolution of oxygenic photosynthesis, which permanently shifted the redox chemistry of Earth’s surface by 2.2 Ga (Holland 1994; Rye & Holland 1998). The second period, beginning with the origin of wood in plants, permanently shifted the distribution of active carbon species within the global carbon cycle by the end of the Mississippian. By fixing carbon into the biologically inert cell walls of tracheids that constitute wood, the rise of a forested landscape transferred carbon from the atmosphere into terrestrial plant biomass. The subsequent increase in soil litter and eventual burial of that inert organic matter effectively trapped carbon for long enough to permanently reduce the mass of CO2 in the atmosphere. The evolution of a forested landscape is, of course, only part of the complex interconnected nature of the phenomenon of terrestrialization. Because of its fundamental result – the drawdown and resetting of equilibrium levels of atmospheric CO2 – it is however a component of terrestrialization that has profoundly altered

subsequent environmental and biological evolution on Earth. The shift in atmospheric CO2 that occurred during the middle part of the Palaeozoic is a prime example of biologically driven environmental evolution affecting both terrestrial and marine ecosystems. Since the mass of CO2 gas in the atmosphere must be in equilibrium with dissolved CO2(aq) in the surface oceans, on the geological timescale any shift in atmospheric CO2 must be matched by a corresponding shift in dissolved CO2(aq) in the oceans. Dissolved CO2(aq) in the oceans is a terminal component of the bicarbonate buffer that controls global pH, however; as pCO2 dropped in the atmosphere, there therefore must have been a corresponding increase in ocean pH. Most geochemists think of the cause and effect the other way around: it is the pH-dependent solubility of oceanic CO2(aq) that determines the concentration of CO2 in the atmosphere (Peng & Broecker 1980). This may be true today in terms of HCO2 3 as controlling the steady-state buffer, but during the terrestrialization interval in geological time, it was the drawdown of atmospheric CO2 that was driving both the ocean– atmosphere


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P. K. STROTHER ET AL.

equilibrium and the pH of the oceans. By the end of the Mississippian, the global carbon cycle had reached a new near steady state in which both pCO2 and ocean pH were reset to essentially modern levels. This dynamic component of the system, the change in pCO2 over time, is the direct effect of the terrestrialization process. This paper examines its roˆle as a causal agent in first-order evolutionary dynamics during this interval. We compare GEOCARB III model data of pCO2 with the rise of the land plants based on recent palaeobotanical discoveries that indicate a Lower Cambrian origin to the land plants. While the connection between the origin of trees and the dramatic decline of pCO2 during the Devonian is both well known and built into the model (Algeo et al. 1995, 2001; Algeo & Scheckler 1998; Berner 2001), GEOCARB III shows pCO2 beginning to decline in the Cambrian long before the origin of trees. The effect of the rise of the land plants on pCO2 includes both changes in the rates of weathering of parent rock and on the burial of refractory carbon (Berner 2001). Prior work on comparing the rise of land plants to the pCO2 decline is focused primarily on events that occurred during the Devonian and Mississippian (Algeo et al. 1995, 2001; Algeo & Scheckler 1998; Berner 2001). However, it could be that the influence of prevascular land plants may have started a cumulative process that began the CO2 decline which accelerated during the Devonian. We next examine the potential perturbations to the phytoplankton of the mid-Palaeozoic marine realm as CO2(aq) declined and as particulate organic matter (pom) and dissolved organic matter (dom) delivery to the shallow shelf increased nutrient flux to the oceans. These are the two most significant changes to the marine environment that occurred as a direct result of the terrestrialization process. They represent primary signals that could have potentially widespread evolutionary outcomes, particularly with respect to the phytoplankton. We use the fossil record of acritarchs as a proxy for the large phytoplankton of the Palaeozoic seas, following Strother (2008). Even although the acritarchs are a polyphyletic group, their sheer numbers (in terms of taxon richness and individual abundance within sampled fossil populations) provide a robust way to measure change in marine palaeoecosystems. Studies on general trends in Palaeozoic phytoplankton (Strother 1996, 2008) and more detailed, period-level analyses (Servais et al. 2004; Vecoli & Le He´risse´ 2004; Mullins & Servais 2008) provide examples of the value of acritarchs in deciphering palaeoecological trends in the fossil record. These works make use of moderately large databases of taxonomic occurrences. We continue in this manner in this paper, relying

principally on the Palynodata database (Palynodata Inc. & White 2008) as the source of taxon distribution values.

Methods: Creating the CO2 and acritarch diversity curves The pCO2 data from GEOCARB III (Berner & Kothavala 2001) is available at ftp://ftp.ncdc.noaa. gov/pub/data/paleo/climate_forcing/trace_gases/ phanerozoic_co2.txt. The rCO2 values are plotted in 10 Ma bins, which are roughly similar to the stagelevel bins used for our taxonomic data. The resolution of these two curves is therefore similar when plotted simultaneously. The basic method to produce the acritarch taxon (genera, species) richness distributions is to progressively clean taxon distribution data extracted from the Palynodata database. Developed originally as an extension of the work of Gerhard Kremp, this database was supported during the 1990s by a consortium of commercial sources, paid subscribers and the Canadian Geological Survey. Last updated in 2006, Palynodata is available as an unsupported download as Geological Survey of Canada Open File 5793 at http://geopub.nrcan.gc.ca/moreinfo_e.php?id=225704 (Palynodata Inc. & White 2008). Records of acritarch occurrences extracted from the Palynodata database were progressively filtered to produce a curve that includes only wellcharacterized acritarch species dated to the level of series or better (Strother 2008). This was done to remove questionable or illegitimate taxa as described in the Fensome et al. (1990) index, invalidly named taxa, certain poorly constrained typically long-ranging genera, taxa left in open nomenclature and synonymous taxa. The use of the above filtering set removed 558 genera (52%) and 3012 species (54%) from the acritarch taxa used in the global analysis. The filtered equal weight taxon distribution values are plotted in Figures 1 and 2. The absolute ages in Palynodata are based on an outdated timescale. We therefore used the relative, time-stratigraphic series and stage names as the basis of stratigraphic occurrence for acritarch taxa. The conversion of time-stratigraphic units to absolute dates was carried out using the values available on the website www.stratigraphy.org as of December 2008.

Results: Assessing the rise of land plants during the terrestrialization interval The effect of the rise of land plants on the carbon cycle has been twofold: (1) causing a drawdown of pCO2 due to the sequestration of Corg in refractory organic matter trapped in plant biomass, litter,

TERRESTRIALIZATION AND MARINE ECOSYSTEMS

39 900

Acritarch Species Richness (by Stage)

800

600 500 400 300

Number of Species

700

200 100

Pre C

C

O

S

500

600

D

M IP

P

J

400 300 200 Geological Time (Ma-Period)

K 100

0

N 0

Fig. 1. Acritarch species richness plotted per Stage. Acritarch species data acquired from the Palynodata database (Palynodata Inc. & White 2008) and then filtered (see text). The time bins are re-calibrated from Palynodata to the values at www.stratigraphy.org as of December 2008.

soils and buried in sediments and (2) increased weathering due to the retention of humic acids in a deeper rhizosphere. In this section we briefly address these two issues. We first review, briefly, the fossil record of land plant origins in terms of the timing and of the kinds of plants that first covered the land surface. Second, we estimate the relative impact on the carbon cycle of the evolution of plants during terrestrialization.

Study of extant plants and green algae has indicated quite clearly that all land plants are derived from charophycean algae (Graham 1993). Additionally, we know that the bryophyte groups are evolutionary intermediates between the algae and the tracheophytes (Qiu et al. 1998, 2006). The evolution of terrestrialization therefore began with terrestrial cyanobacteria and chlorophytic algae (a microbial mat phase), evolved through a bryophytic phase 14

Acritarch Genus Richness

12

8 6

r Genus

10

4 2

Pre C

600

C

500

O

S

D

M IP

P


J

K 100

N

0

0

Fig. 2. Acritarch generic richness plotted per Stage as ‘rGenera’ which is a relative value (linear transform) based on the number of genera in each bin divided by the smallest value (13) in the Mississippian. Acritarch species data as for Figure 1.

40


and culminated in the origin of tracheophytes that dominate subaerial habitats today. The tracheophytes (vascular land plants) have a fossil record beginning in the Wenlock (Edwards et al. 1983). Our understanding of the kinds of plants that lived on the land surface prior to that time is based almost entirely on the fossil record of cryptospores, dispersed spores of early land plants and probably ancestral algal forms that are widely distributed in marginal marine settings by Middle Cambrian (Strother & Beck 2000; Strother et al. 2004) and later (Steemans 2000; Wellman & Gray 2000; Steemans & Wellman 2003). The simplest model for the estimation of the evolution of terrestrialization is the notion of four successive terrestrial autotrophic floras or phases: a cyanobacterial-dominated microbial landscape (microbial mats), a bryophyte-dominated subaerial phase similar to posterlands sensu Retallack (1992) (thalloid bryophytes), a polysporangiophytic phase that includes both rhyniophytoids and tracheophytes which do not possess secondary xylem (tracheophtyes) and a forested phase composed of plants that possessed secondary xylem (lignophytes). These four phases represent the known stages in vegetative evolutionary succession that are distinct enough from each other that they can be modelled for the two factors that are of interest in quantifying the impact of terrestrialization on marine ecosystems: the sequestration of carbon in the stored biomass of vegetative tissues (biomass) and the effect of vegetative cover on weathering of parent rock (depth of the rhizosphere).

Timing of land plant origins We know enough from the fossil record to estimate the origination time duration of each of these successive phases. The microbial mat phase is of Precambrian origin. Perhaps terrestrial microbial mats were established by the time of the rise in O2 at 2.2 Ga, but there is very little direct evidence of organisms occupying terrestrial landscapes before about 1 Ga. The thalloid bryophyte phase is the least well known of the terrestrial phases, but there is evidence of bryophyte-grade structure in laminated cryptospore walls (Strother et al. 2004; Taylor & Strother 2008) in addition to other organic structures; this indicates the likelihood of thalloid bryophytes by the end of the Early Cambrian. We have placed the estimate of the beginning of plants of a bryophytic grade at the Early to Middle Cambrian boundary (513 Ma), but have plotted the origin as occurring in the interval 523– 513 Ma to account for the likely late Early Cambrian origin of related cryptospores. The origin of tracheophytes in the fossil record was, until recently, very tightly constrained to the

Homerian (Wenlock, Silurian) which spans 423– 426 Ma. This timing is based on the occurrence of small plant axes that occur by Wenlock time (Edwards et al. 1983). The Homerian origin of tracheophytes is supported by the rise of ornamented trilete spores, which appear synchronously in both Avalonian and Laurentian terrains (Beck & Strother 2008). These authors have argued that the synchronous occurrence of ornamented trilete spores, cryptospores and megafossil plant axes indicates that the origin of ornamentation in spores is tracking the origin of tracheophytes. However, Steemans et al. (2009) have recently recovered ornamented trilete spores from pre-Hirnantian sediments from the Arabian plate. This would then drop the timing of the tracheophyte phase to the late Katian, following the arguments in Steemans et al. (2009) that such spores are tracking the occurrence of tracheophytes. Although we have retained the Homerian interval as the estimated time of tracheophytes origins, it is possible that this phase in plant evolution began much earlier, perhaps by as much as 20 Ma. The last phase in the developing terrestrialization process is the origin of secondary wood and the rise of a forested landscape. This is likely to have taken place by the end of the Givetian (see discussions in Meyer-Berthaud et al. 2010). We have therefore estimated this phase to begin between 375–385 Ma, corresponding to the Frasnian stage. The rise of lignophytes is the last stage in the evolutionary primary succession of terrestrialization, but it is the only phase to be incorporated into the GEOCARB model for the Palaeozoic Eon. It is important to point out that the drop in pCO2 that is seen in the model is set by the parameters used in GEOCARB.

Assessing the effects of the primary radiation of the land plants on the carbon cycle Each successive phase represents a potential relative increase in standing carbon biomass. Even without knowing the actual biomass represented by the global values, we can predict a stepwise discrete increase in each phase. In other words, each transition represents a cumulative increase in biomass retention in the terrestrial landscape. This is not the case for the rhizosphere, because microbial and bryophytic cover would have had significant differences in producing roots or analogous structures that specifically penetrate parent rock. True roots probably evolved during the tracheophyte phase, but the significance of the earliest roots is extremely difficult to assess. The earliest fossil evidence of rooting organs in plants is found in the Baffin Island floras of Pragian-Emsian age described in Gensel et al. (2001). However, there is indirect evidence of rooting from palaeosols of


slightly younger material from the central Appalachians (Driese & Mora 2001). We can therefore assume that, by the Siluro-Devonian boundary, the effects of increased weathering due to the presence of a rhizosphere would just have begun to have an impact on the global carbon cycle. Rooting on the scale of depths up to 1 m have been described from rocks of Emsian age (Elick et al. 1998). Rooting of this depth should be correlated with the evolutionary origin of arborescence, which is known with confidence somewhat later in the Givetian– Frasnian (Stein et al. 2007). The palaeobotanical evidence indicates that the effects of both increased rooting and the increased retention of woody biomass on the continents would have been felt by Frasnian time. Also, as trees continued to evolve and expand, the effects of forestation would have continued to increase throughout the Famennian. Table 1 provides a summary of the estimates for each of the four successive terrestrial vegetative floras. There are two components to the relation between these successive stages in vegetative cover and their effect on pCO2 in the atmosphere. The first is the retention of standing carbon biomass. This is effectively the amount of carbon that has been transferred from the atmosphere via fixed carbon from oxygenic photosynthesis to biomass retained on the surface. There is an additional and, in reality, more important component: the buried Corg that accumulates during geological time due to the burial of vegetative biomass that accumulates in clastic sediments and is eventually incorporated into the lithosphere. The accumulation of buried carbon has a long history which is documented well into the Archaean (Reimer et al. 1979; Shidlowski et al. 1979). Once this component of the carbon cycle was established, the evolution of subaerial microbial ecosystems would only have incrementally increased the flux of Corg to the lithosphere. The palaeontological record of cyanobacteria shows essentially modern forms as early as 2.0 Ga (Hofmann 1976). Disparity of the cyanobacteria, as recorded in the systematics of cherty microbiotas, does not show a progressive increase through the remainder of the Precambrian.

41

It has been argued recently that the major groups of cyanobacteria diversified by 2450 to 2100 Ma (Tomitani et al. 2006). There is little indication in the fossil record of the cyanobacteria of a progressive increase in the intensity of weathering, in the accumulation of biomass or in the burial of Corg as a result of progressive evolution of cyanobacterial mats through Proterozoic time. It is also difficult to ascertain, based on the fossil record, when subaerial cyanobacterial mats established themselves on the continents. Kennedy et al. (2006) used changing clay mineralogy as a proxy for terrestrial weathering through the Neoproterozoic. They concluded that beginning around 750 Ma, siliciclastic sediments do record a progressive increase in weathering intensity, implying a concomitant increase in microbial cover (‘land biota’) on the land surface. Their results could be explained either by an increase in subaerial microbial mat activity or by the evolution of new elements such as thalloid bryophytes. However, given that the fossil record of cryptospores does not extend below the uppermost Lower Cambrian, we would suggest that a gradual expansion of cyanobacterial mat ecosystems into continental habitats would have been the more likely cause. Standing carbon biomass and the resultant flux to sediments to form buried Corg would have had an incremental increase from the origin of embryophytes (or their progenitors) some time in the Cambrian. This is based on the observations of Strother & Beck (2000) who first demonstrated the presence of cryptospores in rocks of Middle Cambrian age. There is evidence of a bryophyte-grade cover as early as the late Early Cambrian (Strother et al. 2004; Strother 2008) based on cryptospores which have wall ultrastructure related to liverworts (Taylor & Strother 2008). We cannot say that these early bryophyte-grade floras possessed plants with upright axial sporophytes (because these fossils are not found until the Wenlock), but we can assert that thalloid plants that were more complex than microbial mat dwellers appeared on land prior to the Middle Cambrian. This bryophyte-grade morphology generated an incremental increase in stranding carbon biomass on Earth’s surface. With

Table 1. Estimated parameters for each of the four successive terrestrial vegetative phases. The average height is a simple metric of differences in biomass and the rhizosphere depth. In addition, it is used to give a basic impression of the potential impact of changes associated with each of the successive floras Vegetation phase Lignophytes Tracheophytes Thalloid Bryophytes Microbial Mats

Origination (Ma)

Average height (cm)

Rhizosphere depth (cm)

375–385 423–426 513–523 2200–1000

5 102 2 2 1021 1 1021

10 – 102 0.1 0.0 0.0

42


that increase in standing carbon biomass came an incremental flux of Corg to marine sediments. As the bryophytes evolved, there would have been a substantial increase in the standing carbon biomass in subaerial habitats with respect to that of the microbial mat flora. The rationale behind this assertion is the observation that peats today are formed by peat moss (Sphagnum) and that the models of coal accumulation in the past are based on the notion that coals are primarily accumulations of buried peat. There is therefore an actualistic model of sedimentary organic accumulation of geologically significant proportions that is afforded by plants at the bryophyte grade of evolution. An incremental increase in the retention of Corg occurred as a result of the evolution of subaerial bryophyte-grade plants in the Cambrian. This represents the first significant change in the distribution of carbon biomass since the long-term establishment of the Neoproterozoic equilibrium of the microbial mat phase. The establishment of a subaerial, thallophytic vegetative cover in the Cambrian may not have significantly altered the previously established Precambrian level of chemical weathering, because bryophytes do not possess true roots that would have deeply penetrated parent rock. The effect of vegetative cover, with respect to chemical weathering, may have been both to produce organic acids and retain environmental water at the surface, effectively trapping acidic water at the surface of parent

rock. The organic acids produced by bryophytegrade plants may have been more effective at inducing weathering reactions in parent rock than in the previous microbial landscape, but there is no compelling reason to make such an assumption. We therefore may assume that any increase in chemical weathering during the Cambrian and first half of the Ordovician due to this effect would have been nil. However, as seen in Figure 3 where we have plotted the estimated origin times for each of the model stages in vegetative cover along with the data from GEOCARB III, there is substantial pCO2 decline beginning in the Middle Cambrian. This implies that the evolution of the thalloid bryophyte phase of terrestrialization substantially contributed to the increased weathering of parent rock.

Results: The pCO2 drawdown and the decline of the Acritarcha Strother (2008) has pointed out that the pCO2 curves for the Palaeozoic based on the GEOCARB models of Berner and his co-workers (Berner & Kothavala 2001; Berner 2004) closely precede the acritarch decline through the terrestrialization interval. The GEOCARB model data is very sensitive to the effects of increased weathering of parent rock due to the rise of land plants and, to some extent, this has been directly tested in modern settings

pCO2 and the Evolution of Terrestrial Vegetation 30 thalloid bryophytes

25

15

r value

20 tracheophytes lignophytes

10 5

Pre C

600

C

500

O

S

D

M IP

P


J

K 100

N

0

0

Fig. 3. pCO2 and the evolution of terrestrial vegetation. Estimated origin times are plotted with the GEOCARB III data showing the relation between plant evolution and its relation to the atmospheric CO2 model. Cryptospores and smaller plant fragments support the origin of thalloid bryophytes by the end of the Early Cambrian (523– 513 Ma). Tracheophyte fossils are found at the beginning of the Homerian (423– 426 Ma); if it turns out that trilete spores are indicative of the tracheophytic condition then their origin would plot at least back to the Ordovician–Silurian boundary (c. 440 Ma) and perhaps even earlier (Steemans et al. 2009). The origin of lignophytes is plotted as Frasnian, the time of the first recorded true forests (Meyer-Berthaud et al. 2010).


(Moulton et al. 2000). The middle Palaeozoic decline in atmospheric CO2 is corroborated by studies of palaeosols (e.g. Mora et al. 1996; Driese & Mora 2001), so there is direct geochemical evidence supporting the general tenets of the GEOCARB model. The question of causality remains to be demonstrated, but the data in its present form is entirely consistent with the hypothesis that the decline of the acritarchs is a direct consequence of the drop in pCO2that occurred as a result of the terrestrialization process (Strother 2008). The first step in the assessment of causality is to test for a correlation between the CO2 decline and the acritarch curve. Some form of normalization is necessary because we are trying to compare two different things (atmospheric CO2 concentration and standing acritarch diversity) whose dynamic through this interval is tabulated using two different metrics (rCO2 and number of taxa). We therefore normalized the taxon curve by dividing the taxon value in each bin by its minimum registered value in the Carboniferous, which was 13 genera. This linear transformation does not change the shape of the curve, but it brings the recorded values of acritarch genera into a comparative relative measure as that of CO2 that is, essentially a relative taxon assessment, or rGenus. A plot of rCO2 and rGenus for the entire Phanaerozoic is shown in Figure 4. The lines on the graph are the fifth-order polynomial approximations for each dataset as generated in Excelw. The similarity is quite remarkable, especially given the independent nature of these two datasets. The graphs appear to be offset from each other; acritarch taxon richness appears to lag behind rCO2, shifting

43

progressively from about 40 Ma at the base of the Cambrian to about 10 Ma in the Mississippian. We refer to this offset time interval as 1t. In order to examine the possible relation between the two curves for the terrestrialization interval, we extracted a subset of the data from 410 Ma to 300 Ma. This corresponds approximately to the Pragian –Gzhelian interval, which represents the time during which the effective primary terrestrialization occurred. To achieve a quantitative sense of how similar these curves really are, and to assign a value to 1t, we calculated the correlation coefficient between the two curves and then progressively shifted the x-axis values of the rGenus data in –10 Ma increments and recalculated the regression coefficient. In this way, the highest r value (which provides the statistically closest correlation) should represent the best approximation for 1t. Table 2 shows the result of progressively shifting the taxon richness curve back in time in five 10 Ma increments. The highest correlation coefficient (r ¼ 0.95) occurs at 1t ¼ –10 Ma, which supports our intuitive interpretation of the data. Because the data is assembled in 10 Ma bins, all we can say is that 1t is likely to be in the range 5 –15 Ma.

Discussion The progressive rise of terrestrial vegetation and the decline of atmospheric CO2 Katz et al. (2007) mention that the drawdown of Palaeozoic pCO2 was very likely caused, in part, by the sequestration of organic matter as buried

pCO2 and Acritarch Genera 30 rCO2 (from GEOCARB III)

25

rGenus (from Palynodata)

15

r value

20

10 5

Pre C

C 500

O

S

D 400

M IP

P

J

K

300 200 Geological Time (Ma–Period)

100

N

0

0

Fig. 4. CO2 concentration in the atmosphere modelled over Phanerozoic time as represented by the GEOCARB III model (Berner & Kothavala 2001) plotted with acritarch rGenera (the number of genera in each time bin normalized to the low value in the Mississippian). The smooth black and grey lines represent the fifth-order polynomial fits to rCO2 and rGenera, respectively.

44


Table 2. Regression coefficients between the GEOCARB and acritarch genus-richness curves. The acritarch genus data is progressively shifted to the left in 10 Ma increments and the regression coefficient is re-calculated to find the closest fit, which occurs at –10 Ma Offset (1t)

0 Ma

210 Ma

220 Ma

230 Ma

240 Ma

250 Ma

R r2

0.89 0.79

0.95 0.91

0.93 0.87

0.81 0.66

0.89 0.79

0.83 0.69

organic carbon. This is not a new observation. The relation between the composition of the gases in the atmosphere, photosynthesis and the burial of organic carbon (in the form of Carboniferous coal) was noted as early as 1844 by Spencer (1904). It acknowledges an important aspect of the relation between the biosphere and the carbon cycle, which is that the biosphere has played a significant roˆle in the distribution of carbon on the face of the Earth and in the atmosphere. It is therefore reasonable to expect that the evolution of progressively more complex terrestrial vegetative floras would have had a direct effect on the composition of the atmosphere. Each of the proposed stages in the progressive development of vegetative cover corresponds to a subsequent drop in palaeo-CO2 levels as established in the GEOCARB III model (Fig. 3). This is not an expected result of the estimates given in Table 1, because the primary effect of terrestrialization should not have been felt until the rise of the forests during the latter part of the Devonian. In fact, that section of the curve is determined by incorporating increased weathering estimates from the rise of forests in the Late Devonian. However, it seems a remarkable coincidence that both prior periods of the most significant drops in the pCO2 model begin at the time of the origin of each successive vegetative phase. The proposed origin of thalloid bryophyte cover, as evidenced by the first record of cryptospores, represents perhaps the more tenuous correlation because it is not based on a recovery of macroscopic plants in the fossil record but can only be inferred from the palynological record. However, the observation that the decline in atmospheric CO2 began during the Cambrian supports the notion that this was a significant period in plant evolution. The origin of multicellular plants (of a bryophytic grade) probably began the stage in Earth history when the bulk distribution of Corg associated with photosynthetic organisms became greater in terrestrial habitats than in the oceans. This is most certainly the case today when total terrestrial Corg is estimated at 1800 Pg (Brovkin et al. 2002) and living biomass is 600 –800 Pg (Woodwell et al. 1978) as compared to phytoplankton biomass of about 0.25–0.65 Pg (Falkowski & Raven 2007).

Secondly, there is no palaeobotanical model for the existence of a significant rhizosphere prior to the Silurian; the influence of rhizosphere depth on the Cambro–Ordovician portion of the atmospheric CO2 curve would perhaps have been nil. This could mean that if there was a feedback between palaeo pCO2 and the rise of a punctuated vegetative cover beginning in the Cambrian, it was associated with an increase in terrestrial biomass and not in weathering. But this result seems to indicate that the bryophytes may also be important in providing organic acids and a soil cover that substantially increased weathering rates on a global scale. At the very least, this should be taken into consideration when modelling the evolution of terrestrialization.

The decline of pCO2 and its effect on the large phytoplankton of the Early Palaeozoic oceans Our data in Figure 4 demonstrate that the standing diversity of acritarchs (genus-level taxon richness) is highly correlated with the decline in Palaeozoic pCO2 as modelled by Berner & Kothavala (2001). The correlation is highest when the acritarch values are subjected to a 10 Ma linear transform, which has the effect of mapping the acritarch curve into the rCO2 curve. This lag, 1t, is about 10 Ma which seems biologically reasonable in terms of a progressive forcing of phytoplankton extinctions as pCO2 declined. Is it possible that the decline in pCO2 could have caused the acritarch decline? Are the large phytoplankton, in an evolutionary sense, capable of responding to shifts in CO2 availability? In this case we can demonstrate that the phylogeny of the extant phytoplankton indicates that past speciation events include responses to CO2 availability. In addition, there is an experiment (Collins & Bell 2004) showing that extant algal populations responded to changing levels of CO2 in ways that included heritable changes. Their result showed clearly that changes in levels of pCO2 have the potential to lead to speciation in extant algae populations. Tortell (2000) first pointed out that the extant algae preserve evidence of selection for inorganic carbon (Ci) uptake over geological time. This idea


can also be gleaned from Falkowski & Raven (1997) who provided data showing significant differences in Rubisco efficiencies between different algal groups. For this to have occurred during evolution there must have been selection for Rubisco efficiency, which means that the incorporation of CO2 into the dark photosynthetic reactions was determinate for species survival. This is an important qualifier to algal evolution that has often been missed in previous discussions. It means that in the past, CO2 availability played a significant roˆle in algal evolution; CO2 concentration in the atmosphere and oceans was a potential factor in the determination of species survivability in the algae. This is very different from the roˆle played by CO2 in the ecology of the algae today, where algal growth is far more affected by the availability of N, P and, in a secondary way, Fe. The factors that affect algal ecology today need not be the determining factors in the evolution of algae in the past, however (Strother 2008). The acritarchs evolved as a group under conditions of high CO2(aq) without the need for evolving carbon concentration mechanism (CCM)s (Strother 2008). Both coccolithophorids and diatoms (groups that evolved later under conditions of lower ambient pCO2) possess CCMs that clearly facilitate their uptake of carbon, however. This is a second example of CO2 concentration in the environment affecting the outcome of algal evolution through natural selection. CCMs are used by algae to convert HCO2 3 into CO2 at the active site of Rubisco, the enzyme that fixes carbon. Photosynthesizers that possess CCMs can utilize the bicarbonate ion (HCO2 3 ) as an inorganic carbon source reducing their dependence on the diffusion of CO2(aq) as the sole source of carbon. The phytoplankton of the mid-Palaeozoic oceans, as represented by the organic-walled encysting forms, were susceptible to pCO2 as a selective factor in their evolution as there is a good correlation with declining pCO2 through the terrestrialization (Pragian –Gzhelian) interval. Moreover, the acritarchs lag the pCO2 decline by about 10 Ma (+5 Ma bin width). Today, atmospheric CO2 mixes quite rapidly with the upper oceans; equilibrium is reached in 3–6 years (Brovkin et al. 2002). The transfer of carbon into marine sediments takes place at a much longer time scale of 105 yr (Holmen 2000). It is this slower transfer that would have driven pCO2 down and, because atmosphereocean mixing is 4–5 orders of magnitude faster than the driving function, this would have subjected the phytoplankton of the Devonian seas to a period of declining CO2(aq) availability over many generations. This is sufficient time for Darwinian evolution to take place at the population to species to genus level. The quantitative effect of declining

45

genus and species-level taxa in the acritarch curve is consistent with an evolutionary response to declining dissolved CO2 in the oceans. The effects of declining dissolved CO2 in the oceans are more widespread than simply CO2 availability because CO2(aq) is one of the chemical species that determines ocean pH. It is therefore likely that the pH of the oceans increased substantially as carbon accumulated on land in terrestrial ecosystems. The effects of changing pH on phytoplankton physiology and evolution are not well known, but it is certainly likely to have changed both the nitrogen speciation and the solubility of potentially toxic cations (Royal Society 2005). One key element in the proposal of Strother (2008) and reiterated here is that the cause of the acritarch decline was not catastrophic – it was gradual, but progressively persistent. Both the species and genus-level taxon richness curves (Figs 1 & 2) show this trend quite clearly. The acritarchs show high rates of extinction during both the later Silurian and the later Devonian. The decline does not appear to be restricted to just the Frasnian –Famennian interval. The notion of a catastrophic acritarch decline at the end of the Devonian is most probably a residual effect caused by plotting data in Period/ System-level bins as seen in Tappan (1980) and Strother (1996). The acritarchs, as a proxy for the Palaeozoic phytoplankton, do not support the notion of Frasnian/Famennian extinctions caused by bolides, rapid sea-level fluctuations or other catastrophic events as reviewed in McGhee (1996).

Conclusions Two general themes emerge from the examination of the links between changing pCO2 and the evolution of both marine and terrestrial photosynthetic organisms during the terrestrialization interval of the lower Palaeozoic. The first is a correspondence between a step-wise increase in terrestrial biomass accumulation as predicted by discrete phases in plant evolution and the decline in pCO2 as predicted in the GEOCARB III model. The second is a lag response between the decline of the acritarchs and the same pCO2curve. These observations appear to link the decline of the acritarchs to the rise of the terrestrial biota through the pCO2 curve. The timing of this linkage is entirely consistent with models of terrestrial carbon accumulation, based on the fossil record that predicts pCO2 changes in the atmosphere. The response of the acritarchs to declining pCO2 appears to be more speculative, but the evidence of a correlation between pCO2 and acritarch diversity as seen in Figure 4 is quite compelling. Although we have not discussed alternate proposals for the acritarch decline in detail, some of these have been recently reviewed by Strother (2008).

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Phytoplankton today is sometimes utilized as an ecological monitor of nutrient availability and therefore of eutrophication events associated with pollution or periodic upwelling. It is certainly the case that the distribution of phytoplankton biomass is correlated with nutrient from both upwelling and terrestrial runoff. We should not confuse productivity in ecological time with speciation in the geological past, however. Algal phylogeny, when compared to variations in Rubisco efficiency, indicate that the algae were subjected to selection pressure that concerned CO2 uptake (Tortell 2000; Strother 2008). The very existence today of CCMs that extract CO2 from inorganic HCO2 3 is an indication that the necessity of getting CO2 to the active site of carbon fixation was a factor in the evolution of photosynthetic organisms on Earth. The correlation between pCO2 levels and cyst-forming phytoplankton during the Palaeozoic confirms that the phytoplankton evolution was indeed sensitive to past pCO2 levels. The terrestrial and marine biospheres today are clearly linked through the carbon cycle and atmospheric CO2. That they show such strong correlations in the past, especially during the establishment of near-modern levels of carbon distribution during the terrestrialization process, is not surprising. However, the likely correlation between pCO2 and both terrestrial and marine proxies for biosphere evolution as noted here has not been emphasized in prior studies of correlated evolution between the terrestrial and marine realms (Vermeij 1987; Bambach 1993; Martin 1996). Our observations point out that pCO2 may have been a substantial environmental forcing factor contributing to the evolution of the large marine phytoplankton during the Palaeozoic. A chance encounter on an English train led to support for the senior author as a Professeur invite´ at Universite´ des Sciences et Technologies de (Lille 1), France. This support, along with discussions with T. Danelian and other colleagues in Geósyste`mes, is gratefully acknowledged. Additional funds for this research were provided by ECLIPSE-CNRS and C. Lenk. J. Michaud was responsible for initial data processing to produce taxon-richness curves from the Palynodata files. PKS would also like to thank J. Williams at the Natural History Museum in London for the unfettered use of his library and database. The comments of the reviewers, P. Kenrick and R. Wicander, were helpful in improving the manuscript. However, not all of the content of the manuscript is in agreement with their views. Finally, we would like to thank our editor, B. Meyer-Berthaud, for both her patience and clarification of some fundamental palaeobotanical issues.

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Palaeogeographic and palaeoclimatic considerations based on Ordovician to Lochkovian vegetation PHILIPPE STEEMANS1*, CHARLES H. WELLMAN2 & PHILIPPE GERRIENNE1 1

NFSR Research Associate, Paleóbotanique – Paleópalynologie– Micropaleóntologie, University of Lie`ge, Baˆt. B-18, Parking 40, 4000 Lie`ge 1, Belgium 2

Dept of Animal & Plant Sciences, University of Sheffield, Alfred Denny Building, Western Bank, Sheffield S10 2TN, UK *Corresponding author (e-mail: [email protected]) Abstract: This paper summarizes research on Ordovician to Lochkovian vegetation development in a palaeogeographic framework. A terrestrialization model is described. Palaeogeographic maps are modified to explain the vegetation migrations. Land plants first evolved on the Gondwana plate and colonized Avalonia and later Laurentia and Baltica when those plates were in close proximity (Ashgill–Llandovery). South America was colonized during the Llandovery following the collapse of the ice sheet centred on the southern pole which had previously been an impassable barrier for miospores. An Aeronian–Telychian event related to the global early Silurian transgression modified the vegetation by destroying biotopes where the earliest vegetation was thriving. During the regression, trilete spore-producing plants appear to have been more able to respond to environmental changes and dominated the vegetation from the Homerian. Cryptosporeproducing plants could survive under a wide range of climates, which helped them to survive during the Hirnantian glaciation. On the contrary, the earliest trilete spore-producing plants were probably climatically restricted, as suggested by latitudinal variation in assemblage composition. By the end of the Silurian, there were several phytogeographic units. Information on the earliest vegetation favours palaeogeographic reconstructions where plates are in close proximity.

The oldest miospores believed to have been produced by embryophytes (Steemans 1999, 2000; Steemans & Wellman 2004) are Ordovician in age, roughly 465 Ma (Le He´risse´ et al. 2007; Strother et al. 1996). They have been found in two localities from Saudi Arabia, in the Hanadir Member (Qasim Formation) of Llanvirn age. The assemblage contains monad, dyad and tetrad cryptospores, naked or enclosed within a laevigate membrane. Most of the cryptospore morphologies known in younger Ordovician strata are already present. Despite the absence of a detailed systematic description, around eleven taxa can be identified on the basis of the illustrations. Several tetrads and monads have also been reported from the Sˇa´rka Formation of Llanvirn age in the Czech Republic (Vavrdova´ 1984). A rich assemblage of cryptospores has been described from the Caradoc type area in the Welsh Borderland of south Britain (fig. 1 in Richardson 1988; Wellman 1996). The assemblage contains 13 genera and 17 species. A new assemblage, currently under investigation, has been observed in Saudi Arabia. Its age is still imprecise, however, and is thought to be either Caradoc or earliest Ashgill. Its cryptospore composition is similar to the UK assemblage.

Reports of cryptospore assemblages from Ashgillian layers are numerous. On the Gondwana plate they have been described from Libya (Richardson 1988), Chad (Le He´risse´ et al. 2004), Turkey (Steemans et al. 1996), Czech Republic (Vavrdova´ 1982, 1984, 1988, 1989) and Saudi Arabia (work in progress). An assemblage has also been published from a Chinese locality (Wang et al. 1997). On the Avalonia plate, cryptospores have been found in Belgium (Steemans 2001) and in south Wales (Burgess 1991). To our knowledge, no Ordovician diversified cryptospore assemblages have been published on the Laurentia and Baltica plates. All Ashgillian assemblages are very similar in composition: tetrads and dyads dominate; monads are not frequent; species enclosed within a membrane are abundant; spores of dyads and tetrads are usually tightly associated together. An important step in the evolution of vegetation is the inception of the first trilete spores. Rare Ambitisporites specimens have been found in the Ashgill (Hirnantian) from Turkey (Steemans et al. 1996). Trilete spores are also observed from Saudi Arabia in the latest Caradoc or earliest Ashgill up to the Ordovician –Silurian boundary (Steemans et al. 2009). Surprisingly, specimens of ornamented Synorisporites trilete spores are present. The earliest


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ornamented trilete spores previously reported were from the Homerian (Burgess & Richardson 1991). The Saudi Arabian material is currently under investigation. Rhuddanian assemblages are numerous on the Gondwana plate (North Africa, Saudi Arabia, South America), and on the Euramerican plate (USA and UK). Assemblages are similar to those from the Ashgill. During the late Aeronian there is an important decrease in cryptospore biodiversity. It continues during the Telychian where the first patinate trilete spores (Archaeozonotriletes spp.) occur (Richardson 1988; Wellman et al. 2000a; Steemans & Pereira 2002; Mendlowicz Mauller et al. 2004a). Data on the Wenlock are scarce, especially concerning the Sheinwoodian. They are mainly from the UK (e.g. Richardson & Lister 1969; Burgess & Richardson 1991; Wellman & Richardson 1993) and Libya (Richardson & Ioannides 1973). Biodiversity is still very low and assemblages are similar to those from the Telychian. Numerous inceptions of new trilete spores and cryptospores occur during the Homerian. Records exist from the UK (e.g. Richardson & Lister 1969; Burgess & Richardson 1991; Wellman & Richardson 1993; Burgess & Richardson 1995), from the Czech Republic (Dufka 1995) and from Libya (Richardson & Ioannides 1973), and so on. For the fist time, the biodiversity of trilete spores is greater than that of cryptospores. In the Ludlow, Pridoli and younger stratigraphic levels, data become more numerous. Trilete spores continue to diversify, and are generally more abundant and diverse than cryptospores. Data are mainly from the UK (e.g. Richardson & Lister 1969; Wellman 1993; Wellman & Richardson 1993; Burgess & Richardson 1995), from Libya (e.g. Richardson & Ioannides 1973; Rubinstein & Steemans 2002), from Turkey (Steemans et al. 1996), from Spain (Richardson et al. 2001), from Brazil (Steemans et al. 2008a) and so on. Clearly, trilete spores continued to rapidly diversify and dominate miospore assemblages. Finally, during the Lochkovian, data are very abundant and will not be exhaustively listed here.

Miospore biodiversity evolution A detailed analysis of the literature enables construction of a biodiversity curve from the Ordovician up to the Lochkovian (Steemans 1999, 2000; Steemans & Wellman 2004). Recently, a similar curve compiled by Strother has been published in Traverse (2007). This is generally consistent with the previous curves, although there are some small discrepancies that are probably a result of Strother’s wider cryptospore concept which includes all continental palynomorphs, that is, continental algae (Strother & Beck 2000).

The three main events of miospore evolution will be discussed in the following sections: the Hirnantian glaciation, the Aeronian-Telychian event and the early Lochkovian.

Hirnantian glaciation The Hirnantian glaciation is known to have been responsible for the strong decrease in biodiversity of most fossil groups (Webby et al. 2004). Ashgillian to lower Aeronian miospore assemblages are very similar in all localities, showing that the glaciation had little effect on miospore assemblages. This appears to be the case whatever the climatic conditions were, for example, close to the southern pole in Paraguay or Brazil (Le He´risse´ et al. 2001a; Steemans & Pereira 2002; Mendlowicz Mauller et al. 2004a, b) or in temperate regions on the Avalonia plate (Wellman 1996; Steemans 2001). No decrease in miospore biodiversity has been observed after the Hirnantian glaciation (Steemans & Wellman 2004): pre and post-glaciation assemblages are very similar. This has been explained by the ability of the earliest cryptosporeproducing land plants to grow and to reproduce under diverse climates (Steemans 2000; Wellman & Gray 2000). The areas where the vegetation was destroyed during the advancing glaciation were recolonized as soon as the ice retreated.

Aeronian – Telychian event The miospore diversity curve shows a minimum value during the Aeronian and the Telychian (Steemans 1999) because of a high rate of Aeronian extinction and the small number of inceptions of new species around the Llandovery –Wenlock transition. The low biodiversity value could reflect the global marine sedimentological conditions after the melting of the Hirnantian glaciers. It is probably partially true that miospore numbers are underestimates as reports from marine sediments dominate this interval. However, assemblages of miospores are very different before and after this ‘event’: (1) trilete spores which were previously rare become increasingly abundant, even if diversity remains low up to the Homerian; (2) cryptospores enclosed in a membrane (e.g. Velatitetras spp, Segestrespora spp., etc.) which were very abundant became rare after the event; (3) cryptospore tetrads and dyads from the mid Ordovician up to the middle part of the Aeronian had tightly adpressed spores (in younger strata these polyads consist of loosely adherent spores); and (4) monads which were previously rare became much more abundant. This strong cryptospore biodiversity decrease which was accompanied by a major change in the vegetation could be considered as a major event in

ORDOVICIAN TO LOCHKOVIAN VEGETATION

the evolution of vegetation. This has been interpreted as due to the early Silurian global transgression which could have destroyed, reduced or moved the habitats of the earliest plants (Steemans 2000). After this global transgression, a global regression was initiated up to the early Devonian. Plants colonized new areas which would have become progressively available during the regression. Most probably, plants producing trilete spores were better adapted to the new ecological conditions as they had increasingly dominated the vegetation since the Wenlock. According to the palaeobotanical record (Edwards & Richardson 2004), cryptosporeproducing plants were probably bryophyte-like stem group embryophytes and trilete sporeproducing plants were tracheophytes and their immediate ancestors (‘protracheophytes’). After the Aeronian– Telychian event the vegetation landscape radically changed; the previous vegetation dominated by very small bryophyte-like plants was replaced by a vegetation dominated by tracheophytes which colonized a wider range of biotopes and began to rapidly increase in size.

Early Lochkovian The biodiversity curve published in Steemans (1999) is based only on independently dated assemblages. They have been isolated from marine near-shore sediments in which there are other palynomorphs that is, chitinozoans and acritarchs, or macrofossils such as graptolites, and so on. However, some Lochkovian studies report on continental sediments for which there are no independent age controls. The contents of those assemblages were not included when constructing this biodiversity curve. This is important because cryptospore biodiversity in these continental deposits is much higher than in marine deposits. It has been shown that the near-shore marine miospore assemblages are dominated by trilete spores while continental ones are usually dominated by cryptospores (e.g. Richardson 1996; Wellman & Richardson 1996; Rubinstein & Steemans 2002; Steemans et al. 2007). This has been interpreted as resulting from differences in the biotopes in which the plants producing trilete spore and cryptospores grew. The latter probably lived in or around wet confined environments (lakes and swamps) with a low potential for their spores to be transported by rivers to the near-shore marine basins. This behaviour is still observed in the extant nature (van Zanten & Poćs 1981). On the other hand, trilete spore-producing plants may have inhabited valleys and alluvial plains; their spores were therefore disseminated more easily into rivers and transported out to sea. The ecology and habitats of the trilete

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spore and cryptospore producers has been much debated with slightly different scenarios developed by Steemans (1999), Wellman et al. (2000b) and Edwards & Richardson (2004).

Palaeogeographic considerations based on the earliest miospores: a model Generalities of cryptospore dispersion It has been explained in Steemans et al. (2007) how improbable effective cryptospore transport would be over long distances (at least several hundred kilometres). Effective transport implies that cryptospores survive during the transport, land in a suitable area where they will germinate and produce a viable gametophyte. Cryptospores are believed to be produced by bryophyte-like plants. Such plants now predominantly inhabit at least temporarily wet habitats. Their spores have a low resistance to desiccation, and therefore do not survive long distance transport by high altitude winds. The earliest bryophyte-like plants were of small size (a few millimetres high) limiting the probability of their spores being redistributed far by wind as they quickly fell down on a wet ground. Finally, cryptospores are usually of a large size diameter (.25 mm), further reducing their ability to be transported over long distances. According to those considerations, long distance transport of cryptospores is considered to be very improbable. However, as stated in Steemans et al. (2007): Considering long geological time spans, however, the possibility of long distance dispersal via a chance event is of course not impossible. Even if effective long-range dispersal of one species is possible, longrange relocation of a complete cryptospore assemblage is much less probable.

The palaeogeographic model developed below is therefore constructed on the basis of this hypothesis which implies that the terrestrialization of the tectonic plates is possible only if they are not separated by large distances.

The colonization of the land by the first embryophytes The oldest cryptospores believed to be produced by embryophytes are Llanvirn in age from Saudi Arabia on the Gondwana continent (Fig. 1a). Some specimens are also known from the Czech Republic. At that time, Avalonia was still a part of the Gondwana Plate or at least very close to it (Vecoli & Samuelsson 2001; Samuelsson et al. 2002). Diversified cryptospores are reported from the Caradoc of the UK by Wellman (1996). It is therefore possible that the earliest bryophytes

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Fig. 1. Schematic palaeogeographic maps from the Llanvirn up to the Lochkovian showing distributions of the miospore assemblages and their probable colonization of the lands. The list of publications is not exhaustive. (a), (b) and (c) Modified after Scotese (2003). (d) modified after Torsvik & Cocks (2004). (a) Llanvirn-Caradoc palaeogeographic map. 1: Saudi Arabia (Strother et al. 1996; Le He´risse´ et al. 2007 and Steemans et al. 2009); 2: The Czech Republic (Vavrdova´ 1984); 3: UK (Wellman 1996). (b) Ashgill palaeogeographic map. 1: China (Wang et al. 1997); 2: Saudi Arabia (Steemans et al. 2009); 3: Chad (Le He´risse´ work in progress at the Brest, Rennes and Lie`ge Universities); 4: Turkey (Steemans et al. 1996); 5: Libya (Richardson 1988); 6: The Czech Republic (Vavrdova´ 1988, 1989); 7: Belgium:(Steemans 2001); 8: UK (Burgess 1991). (c) Llandovery palaeogeographic map. 1: Saudi Arabia (Steemans et al. 2000; Wellman et al. 2000a); 2: Libya (Richardson 1988); 3: Brazil (Le He´risse´ et al. 2001b; Mizusaki et al. 2002); 4: Paraguay (Steemans & Pereira 2002; Mendlowicz Mauller et al. 2003); 5: Argentina (Rubinstein & Vaccari 2004); 6: UK (Burgess 1991). 7, 8: USA (Pratt et al. 1978; Strother & Traverse 1979; Johnson 1985). (d) Lochkovian palaeogeographic map. 1: Saudi Arabia (Steemans et al. 2007); 2: Libya (Rubinstein & Steemans 2002); 3: Brazil (Gerrienne et al. 2001); 4: Brazil (Rubinstein et al. 2005, 2008); 5: Bolivia (McGregor 1984); 6: Spain (Richardson et al. 2001); 7: Brittany (Steemans 1989); 8: UK (Richardson & Lister 1969; Wellman & Richardson 1996); 9 –12: USA and Canada (e.g. Johnson 1985; Pratt 1978; Strother & Traverse 1979; Strother & Beck 2000).

colonized Avalonia during the Early/Mid Ordovician. Avalonia migrated to the north and collided with Baltica during the Ashgill, transporting plants from Gondwana (Fig. 1b). This could explain the presence of similar cryptospore assemblages on both sides of the Rheic Ocean. During the Ashgill, new localities were colonized by the vegetation on the Avalonia Plate and on the eastern part of the Gondwana Plate (North Africa, peri-Gondwanan terranes, Arabian Platform). To date, no cryptospore assemblages have been observed in Ordovician palynological assemblages from South America. However, rare simple tetrads (Tetrahedraletes medinensis Strother & Traverse 1979) have been reported in several Ordovician localities from both South and North America

(Gray 1988; Ottone et al. 1999) and Baltica (Le He´risse´ 1989). This cryptospore species is known from the Llanvirn up to the Mid Devonian, under many kinds of climates and in a wide range of environments from marine near-shore to confined continental area for example, associated with a relict flora (Wellman & Richardson 1996). Frequently, this species is the only one seen in samples poor in cryptospores from either marine or continental sediment. T. medinensis has most probably been produced by highly opportunistic and cosmopolitan plant species. Simple tetrads and dyads appear to have colonized all of the continents very early, most likely in the Mid Ordovician, although some researchers (e.g. Strother et al. 2004) controversially suggest


an earlier appearance in the Cambrian (Wellman et al. 2003; Steemans & Wellman 2004). Plants producing more elaborate cryptospores invaded these areas following the Ordovician glaciation when the ice sheet that was a barrier to migration disintegrated. Numerous cryptospore assemblages are reported from the Llandovery in Brazil, Paraguay and Argentina (Fig. 1c). This delay in the colonization of South America by land plants could be the consequence of the presence of the ice sheet which isolated South America from the rest of the Gondwana. In addition, as the South American plate moved towards the north, the northern margin of this part of Gondwana moved away from the South Pole. The ice sheet may have disintegrated, opening a route for a step-by-step colonization by the plants during the Llandovery. The Iapetus Ocean narrowed and finally Avalonia-Baltica and Laurentia collided, leading to the emergence of the Caledonian mountains which formed a palaeogeographic barrier. Cryptospores then colonized Laurentia, where they are observed in abundance in Llandovery layers. The first occurrence of trilete spores (Fig. 2) is around the Caradoc–Ashgill boundary in Saudi Arabia (Steemans et al. 2008b; Wellman et al. 2008). Rare trilete spores (Ambitisporites spp.) are observed in Hirnantian layers from Turkey (Steemans et al. 1996). Ambitisporites is also known from the early Aeronian in Libya (Richardson 1988), from the upper Aeronian in Paraguay and Brazil (Le He´risse´ et al. 2001b; Steemans & Pereira 2002; Mendlowicz Mauller et al. 2004a),

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from the youngest Aeronian in the UK (Burgess 1991), from the Aeronian (possibly Telychian) on the Laurentia plate (Pratt et al. 1978; Strother & Traverse 1979) and from the Wenlock in Gotland (Le He´risse´ 1989). This suggests a progressive colonization by trilete spore-producing plants from the east to the west. As the Rheic Ocean was narrowing, trilete spore transport by winds from Gondwana to the Euramerican plate became possible in the Aeronian. Avalonia is the first to be colonized, then Laurentia and finally Baltica which is on the opposite side of the Caledonian mountains.

Phytopalaeogeographic considerations Comparisons of Lochkovian cryptospore and trilete spore assemblages between Saudi Arabia and the UK has led Steemans et al. (2007) to the conclusion: . . . that the Old Red Sandstone Continent and Gondwana were much closer than postulated in many palaeocontinental reconstructions, perhaps even connected, allowing easy migration of cryptosporeproducing plants. Differences in the trilete spore assemblages from the two continents probably relates to palaeoenvironmental (climatic) differences and not to endemism due to palaeogeographical isolation due to barriers such as a large Rheic Ocean.

The distribution of some biostratigraphically important trilete spores, that is, Streelispora newportensis (Richardson & Lister 1969) and Emphanisporites micrornatus var micrornatus (Steemans & Gerrienne 1984) is also favoured by the palaeogeographic reconstruction shown in Figure 1d.

Fig. 2. Schematic Llandovery map showing the first occurrences of the oldest trilete spores according to their palaeogeographic locations. 1: Caradoc/Ashgill boundary in Saudi Arabia (Steemans et al. 2008b; Wellman et al. 2008); 2: Hirnantian in Turkey (Steemans et al. 1996); 3: Early Aeronian in Libya (Richardson 1988); 4: upper Aeronian in Paraguay and Brazil (Le He´risse´ et al. 2001b; Steemans & Pereira 2002; Mendlowicz Mauller et al. 2004a); 5: youngest Aeronian in the UK (Burgess 1991); 6: Aeronian (possibly Telychian) on the Laurentia plate (Pratt et al. 1978; Strother & Traverse 1979); 7: Wenlock in Gotland (Le He´risse´ 1989).

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Both characterize the MN Biozone (Richardson & McGregor 1986; Streel et al. 1987; Steemans 1989). They are well known on the Old Red Sandstone Continent (ORSC). They are also frequent in peri-Gondwanan areas such as in Spain (Richardson et al. 2001) and in Brittany (Steemans 1989). On the contrary, they are extremely rare in North Africa and absent in South America and on the Arabian Platform. The close proximity of those land masses has also been suggested by a study on late Lochkovian layers from the Moesian Platform (Steemans & Lakova 2004). Indeed, Romanian and Bulgarian samples contain typical ORSC miospore assemblages. The authors concluded that this area belongs to the S-Z palaeophytogeographic province, whereas acritarch assemblage included a mixture of species with Gondwanan or Euramerican affinities (Lakova 2001). Chitinozoans showed strong Gondwanan affinities (Lakova 1995). However, it is now accepted that the Rheic Ocean did not act as an impassable barrier for either acritarchs (Le He´risse´ 2002) or chitinozoans (Jaglin & Paris 2002).

The plant meso- and megafossil records The comparison of the record of dispersed and in situ spores has sometimes been used to extrapolate the presence of a given plant macrofossil (Wellman et al. 2004). This is presumably true for highly characteristic spores, but caution should be expressed for morphologically simple spores. This is because different macrofossil genera may produce the same kind of spores (e.g. simple laevigate retusoid spores are found within a wide range of plants; see Allen 1980; Gensel 1980; Fanning et al. 1990) and plants with identical morphologies may produce different genera of spores (Fanning et al. 1988). The classification of miospore morphotaxa does not necessarily reflect a biological reality. It varies according to the preservation state and a continuous morphological intergradation can exist between different miospore taxa (Breuer et al. 2005, 2007a, b). The earliest land plants were very small and most are presumed to have a low fossilization potential. The fossil record of early land plant meso- and megafossils is therefore still scant, even although it has recently considerably improved (Kenrick & Crane 1997; Edwards et al. 2001; Raymond et al. 2006). Taphonomic biases also strongly affect the nature of the plant fragment collected. Moreover, the systematics and taxonomy of the earliest land plants are very difficult because they exhibit very few characters. Consequently, it is often impossible to ascertain the true relationship between floras, as apparent similarities in generic composition may

be caused by misidentification or simply reflect comparable grades of organization. Today, land plants (Embryophytes) include four clades: the non-vascular Hepatophyta, Anthocerophyta, Bryophyta and the Tracheophyta (vascular plants). Depending on the methodology, the age estimate for the crown group of land plants ranges from 748 Ma to 483 Ma (for a summary see Sanderson et al. 2004). The latter date is much more consistent with the palaeobotanical data: the earliest unequivocal mesofossil evidence of terrestrial plants comes from Oman and is considered to be Late Ordovician (Caradoc, c. 460 445 Ma) in age. It consists of fragments of sporangia containing large numbers of cryptospore naked permanent tetrads (Wellman et al. 2003). Those spores most probably have liverwort (Hepatophyta) affinities. This record is consistent with the basal position of the Hepatophyta in Embryophyte phylogeny as well as with the suggested liverwort affinities of the earliest cryptospores (Edwards et al. 1995). It also confirms that the earliest land plants probably first evolved on Gondwana. The oldest undisputable record of a land plant macrofossil is from the Mid Silurian (Homerian, c. 426–423 Ma) of Ireland (Edwards & Feehan 1980; Edwards & Wellman 2001). It mostly consists of small sporangia of the Cooksonia pertoni type, borne at the tip of sometimes dichotomous axes. Because the Lower Devonian representatives of Cooksonia pertoni are the oldest demonstrated vascular plants (Edwards et al. 1992), the Homerian specimens suggest that vascular plants had already evolved by the Mid Silurian. The pre-Late Silurian record of land plants is very poor. This makes any conclusions on global distribution highly conjectural and cannot yet provide significant palaeogeographical information. The Late Silurian and Lochkovian records are much more informative (Edwards & Wellman 2001). The Late Silurian record of land plants includes more than 30 localities. A recent analysis based on macrofossil genera and morphological traits yielded four phytogeographical units (Raymond et al. 2006): a North Euramerican (Northern Canada) unit close to the palaeoequator; a South EuramericanNorthwest Gondwanan unit (Great Britain, Podolia and Bolivia) at 18–758S; a Kazakhstanian unit located at the north of the palaeoequator and based on poorly known plants; and a Northeast Gondwanan (Australian) unit at 108S. The latitudinal zonation of the Late Silurian floras suggests that those plants were probably dependent on climate, as already suggested by the record of early trilete spores (Steemans et al. 2007). The existence of a South EuramericanNorthwest Gondwanan Late Silurian phytogeographical unit was strongly supported in Raymond


et al.’s (2006) analysis, and led those authors to propose several hypotheses (ecological, palaeogeographic, palaeoclimatic, data-biased) to explain the similarities between the analysed assemblages. They suggested ‘a true palaeogeographic proximity’ (allowing biological exchange by propagules) between Bolivian and British assemblages. This is consistent with the absence of a palaeogeographical barrier between the ORSC and Gondwana as proposed by Steemans et al. (2007). Plants of the South Euramerican-Northwest Gondwanan unit were very small and mostly characterized by narrow dichotomous axes with terminal sporangia (e.g. Cooksonia, Pertonella). On the contrary, plants from the equatorial North Euramerican and the Northeast Gondwanan units were characterized by much larger sizes. They belonged to the Lycophyta clade (zosterophylls or early Lycopsida). The simultaneous existence of floras at markedly different grades of organization adds another note of caution to the use of early land plants for biostratigraphical purposes. The early Lochkovian record of land plants is not significantly different from that of the Late Silurian (compare the floral lists of Raymond et al. 2006 for the late Silurian and of Edwards & Wellman 2001 for the Lochkovian). It includes various genera of diminutive plants with terminal sporangia (‘rhyniophytoids’) and plants of Lycophyta affinities. However, note that in the Lochkovian these Lycophyta had spread to higher latitudes and were no longer restricted to the equatorial zone. The Lochkovian assemblages from Great Britain (Wales, England, Scotland; see Edwards & Wellman 2001 or Edwards et al. 2001 for a summary) and from Brazil (Parana´ Basin; Gerrienne et al. 2001, 2006) bear a striking resemblance. At least five different taxa are found in both areas: Caia, Cooksonia, Pertonella, Tarrantia and a new genus to be created to accommodate the specimens assigned to Cooksonia caledonica (work in progress, University of Lie`ge). Those similarities imply major floral exchanges between Southern Euramerica and Gondwana that can probably be explained by a close proximity of those palaeocontinents as illustrated in Figure 1d.

Conclusions The colonization of the land by the earliest terrestrial vegetation can be explained by the close proximity of the different palaeoplates, from the migration of these plates and the collisions between them. Models that show large oceans, which would probably have been impassable barriers for the transport of miospores, cannot explain the progressive invasion of the continents through time.

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The Hirnantian glaciation had little observable effect on cryptospore biodiversity which suggests that the plants that produced them were adapted to a wide range of climates. In contrast, the destruction of biotopes by the global Early Silurian transgression strongly affected their biodiversity and favoured the emergence of the trilete sporeproducing plants which have been dominating the vegetation from the Homerian. The variability observed in trilete spore assemblages since the Lochkovian, compared to a lack of variability among cryptospore assemblages, is better explained by a latitudinal effect than by the presence of palaeogeographical barriers. The zonation of the Late Silurian land plant floras was probably climatically induced. Striking similarities between the Lochkovian assemblages from Great Britain and Brazil suggest major floral exchanges between Southern Euramerica and Gondwana, and a close vicinity of these palaeocontinents. This work is supported by the Eclipse II project ‘The terrestrialization process’. The authors are grateful to J. Marshall and the anonymous reviewer for improvement of the manuscript.

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Palaeogeography, Palaeoclimatology, Palaeoecology, 250, 237– 254. Steemans, P., Rubinstein, C. & Melo, J. H. G. 2008a. Miospore biostratigraphy of the Siluro–Devonian boundary, Urubu area, Western Amazonas Basin, northern Brazil. Geobios, 41, 263–282. Steemans, P., Wellman, C. H., Miller, M. A. & Al – Ruwaili, M., 2008b. An Ordovician cryptospore and trilete spore assemblage from Saudi Arabia, 12th International Palynological Congress. GeoUnion Alfred-Wegner-Stiftung, Bonn, August 30– September 5, 266. Steemans, P., Le Herisse, A. et al. 2009. Origin and radiation of the earliest vascular land plants. Science, 324, 353. Streel, M., Higgs, K., Loboziak, S., Riegel, W. & Steemans, P. 1987. Spore stratigraphy and correlation with faunas and floras in the type marine Devonian of the Ardenno– Rhenish regions. Review of Palaeobotany and Palynology, 50, 211–229. Strother, P. K. & Traverse, A. 1979. Plant microfossils from the Llandoverian and Wenlockian rocks of Pennsylvania. Palynology, 3, 1–21. Strother, P. K. & Beck, J. H. 2000. Spore-like microfossils from Middle Cambrian strata: expanding the meaning of the term cryptospore. In: Harley, M. M., Morton, C. M. & Blackmore, S. (eds) Pollen and Spores: Morphology and Biology. Royal Botanic Gardens, Kew, 413–424. Strother, P. K., Al– Hajri, S. & Traverse, A. 1996. New evidence for land plants from the lower Middle Ordovician of Saudi Arabia. Geology, 24, 55– 59. Strother, P. K., Wood, G. D., Taylor, W. & Beck, J. 2004. Middle Cambrian cryptospores and the origin of land plants. Association of Australasian Palaeontologists Memoir, 29, 99– 113. Torsvik, T. H. & Cocks, L. R. M. 2004. Earth geography from 400 to 250 million years: a palaeomagnetic, faunal and facies review. Journal of the Geological Society London, 161, 555– 572. Traverse, A. 2007. Paleopalynology. Topics in geobiology, 28. Springer, Dordrecht, The Netherlands. van Zanten, B. O. & Poćs, T. 1981. Distribution and dispersal of bryophytes. Advances in Bryology, 1, 479– 562. Vavrdova´, M. 1982. Recycled acritarchs in the uppermost Ordovician of Bohemia. Casopis pro Mineralogii a Geologii, 27, 337– 345. Vavrdova´, M. 1984. Some plant microfossils of the possible terrestrial origin from the Ordovician of central ˇ eske´ho geologicke´ho u´stavu, 59, Bohemia. Veˇstnı´k C 165– 170. Vavrdova´, M. 1988. Further acritarchs and terrestrial plant remains from the Late Ordovician at Hlasna Treban (Czechoslovakia). Casopis pro Mineralogii a Geologii, 33, 1 –10. Vavrdova´, M. 1989. New acritarchs and miospores from the Late Ordovician of Hlasna Treban, Czechoslovakia. Casopis pro Mineralogii a Geologii, 34, 403–420.

Vecoli, M. & Samuelsson, J. 2001. Quantitative evaluation of microplankton palaeobiogeography in the Ordovician– Early Silurian of the northern Trans European Suture Zone: implications for the timing of the Avalonia– Baltica collision. Review of Palaeobotany and Palynology, 115, 43– 68. Wang, Y., Li, J. & Wang, R. 1997. Latest Ordovician cryptospores from southern Xinjiang, China. Review of Palaeobotany and Palynology, 99, 61– 74. Webby, B. D., Paris, F., Droser, M. L. & Percival, I. G. 2004. The Great Ordovician Biodiversification Event. Critical Moments and Perspectives in Earth History and Paleobiology. Columbia University Press, New York. Wellman, C. H. 1993. A land plant microfossil assemblage of Mid Silurian age from the Stonehaven Group, Scotland. Journal of Micropalaeontolgy, 12, 47– 66. Wellman, C. H. 1996. Cryptospores from the type area for the Caradoc Series (Ordovician) in southern Britain. Palaeontology, 55, 103– 136. Wellman, C. H. & Richardson, J. B. 1993. Terrestrial plant microfossils from Silurian inliers of the Midland Valley of Scotland. Palaeontology, 36, 155–193. Wellman, C. H. & Richardson, J. B. 1996. Sporomorph assemblages from the ’Lower Old Red Sandstone’ of Lorne Scotland. In: Cleal, C. J. (ed.) Studies on early land plant spores from Britain. Special Papers in Palaeontology, Great Britain, 55, 41–101. Wellman, C. H. & Gray, J. 2000. The microfossil record of early land plants. Philosophical Transactions of the Royal Society of London– Series B: Biological Sciences, 355, 717–732. Wellman, C. H., Higgs, K. T. & Steemans, P. 2000a. Spore assemblages from a Silurian sequence in Borehole Hawiyah-151 from Saudi Arabia. In: Al-Hajri, S. & Owens, B. (eds) Stratigraphic Palynology of the Palaeozoic of Saudi Arabia. GeoArabia, Bahrain, Special Volume 1, 116– 133. Wellman, C. H., Habgood, K., Jenkins, G. & Richardson, J. B. 2000b. A new 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, 161–196. Wellman, C. H., Osterloff, P. L. & Mohiuddin, U. 2003. Fragments of the earliest land plants. Nature, 425, 282 –285. Wellman, C. H., Kerp, H. & Hass, H. 2004. Spores of the Rhynie chert plant Horneophyton lignieri (Kidston and Lang) Barghoorn and Darrah, 1938. Transactions of the Royal Society of Edinburgh: Earth Sciences, 94, 429–443. Wellman, C. H., Steemans, P. & Miller, M. A. 2008. Trilete spores from the Ordovician of Saudi Arabia: earliest evidence for vascular plants and their immediate predecessors (“protracheophytes”). Proceedings of 12th International Palynological Congress. GeoUnion Alfred-Wegner-Stiftung, Bonn, August 30–September 5, 2008, 304.

The land plant cover in the Devonian: a reassessment of the evolution of the tree habit B. MEYER-BERTHAUD1,2*, A. SORIA1 & A.-L. DECOMBEIX3 1

UM2, UMR AMAP (botAnique et bioinforMatique de l’Architecture des Plantes), c/o CIRAD, TA-A51/PS2, Boulevard de la Lironde, 34398 Montpellier cedex 5, France 2

CNRS, UMR AMAP, F-34398 Montpellier

3

Department of Ecology and Evolutionary Biology, University of Kansas, 1200 Sunnyside Avenue, Haworth Hall, Lawrence, Kansas 66045-7534, US *Corresponding author (e-mail: [email protected]) Abstract: This paper reviews information on the Devonian trees that evolved in the euphyllophyte clade with special focus on the Middle Devonian Pseudosporochnales. The morphology of pseudosporochnalean trees shows analogies with that of extant tree ferns, including the possession of an adventitious root system of limited extent at the base of the trunk. Direct evidence on how these trees were constructed is scarce. We propose a growth model integrating information from younger representatives of the same class known to reach large diameters. According to this model, trunk width in its aerial part results from the large size of its primary body where living tissues are abundant, a condition reached early during growth. Secondary xylem contributes little to trunk diameter. This model sharply diverges from that of the Late Devonian archaeopteridalean trees characterized by an extended root system and where trunk diameter and mechanical support are achieved by the substantial development of secondary vascular tissues. These differences suggest that pseudosporochnalean trees may have had a lesser impact on Devonian environments than the Archaeopteridales. The important investment in living tissues in the Pseudosporochnales probably made them vulnerable to drought and cold.

The diversification of early terrestrial plants has been compared to the Cambrian explosion for marine faunas in terms of intensity and importance for shaping modern ecosystems (Kenrick & Crane 1997a; Bateman et al. 1998). It is characterized by an intense phase of morphological innovation during the Devonian that resulted in the evolution of a large variety of growth forms. Several unrelated taxa adopted the tree habit, a form characterized by its extended lifetime and the possession of a tall, vertical trunk (Barthelemy & Caraglio 2007). This evolution was adaptive and provided large-sized plants with functional advantages over smaller ones in terms of reproduction and light interception (Niklas 1997). From a biophysical point of view, this increase in stature was a challenge as it created tremendous new constraints in terms of biomechanical support and water transport. The various groups that evolved trees resolved these problems by adopting specific strategies in relation to their own evolutionary history and inherited traits (Donoghue 2005) (Fig. 1a). The ‘Devonian plant hypothesis’ developed by Algeo and his collaborators in the past 15 years postulates a significant role of the vegetation in the series of biogeochemical events occurring in

the Late Devonian (major biotic crises, extensive deposition of black shale horizons, atmospheric CO2 level drop and global climate cooling) (Algeo et al. 2001). These authors hypothesize that reproduction by seeds increased the geographical distribution of plants by enabling the critical fertilization phase to take place in most habitats including dry ones. With the increase in maximal size of the plants documented in the Devonian, and the evolution of the tree habit, they postulate the formation of thicker litters and the development of larger root systems that penetrated the substrates more extensively. This resulted in the extensive formation of deeper and more mature palaeosols, a process that uses atmospheric CO2. The explicit network of feedbacks involving plant traits, CO2 and climate proposed by Beerling & Berner (2005) is not specific to the Devonian. It includes another factor thought to accelerate the drawdown of atmospheric CO2, the amount of organic carbon buried in the sediments such as that derived from lignous plants. Lignin is a polymer of phenylpropane that imparts rigidity to cell walls and is found in plant tissues such as xylem and sclerenchyma (Beck 2005). It is one of the most resistant plant components to biodegradation and


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(a)

(b)

Fig. 1. (a) Simplified phylogenetic tree of the Palaeozoic vascular land plants modified from Kenrick & Crane (1996). Derived traits in relation to the tree habit in italics. Stratigraphic extent of trees in black. Ages in millions of years, after the Internal Commission on Stratigraphy (http://www.stratigraphy.org/cheu.pdf). (b) Evolution of maximum axis diameter in the Devonian, modified from Chaloner & Sheerin (1979). Small black circles: non-arborescent plants; light grey circles: Lycopsida; grey squares: Cladoxylopsida; star: Equisetopsida; dark grey triangles: Archaeopteridales.

it is uncertain whether lignolytic organisms had evolved before the end of the Devonian (Stubblefield et al. 1985; Robinson 1996). The Beerling– Berner model also identifies processes linking

the extension of the root system to plant size and canopy size to leaf size that are pivotal for their effects on CO2 and on climate parameters such as rainfall and temperature.

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Much has been written concerning the large ‘modern’ Archaeopteris trees of the Late Devonian and information concerning these organisms has not progressed much in recent years (Beck & Wight 1988; Trivett 1993; Meyer-Berthaud et al. 1999). By contrast, there is a large amount of new data on the Cladoxylopsida, a class of plants that flourished in the Middle Devonian and includes the earliest trees. In addition to a review of the trees that evolved in this group, we propose a model of cladoxylopsid trees addressing some parameters that may feed the models cited above, for example, the growth potential of the trunk and root system and the amount of lignified tissues they produced.

When and in what groups did trees evolve? If entire trunks are rare in the fossil record, wide pieces of axes are common and they are used by palaeobotanists as evidence of trees. This is based on the mechanical relationship that links height to diameter in self-supporting columns with a known distribution of tissues/material. According to one of the most commonly used models (the elastic similarity model), it is predicted that the maximum height reached by a self-supporting column before it buckles under its own weight increases at the 2/3 power of its diameter (Mosbrugger 1990). Other models, and statistical analyses conducted on a wide range of axes from different taxonomic groups, confirm this relationship but differ by the scaling exponent (Niklas 1993). All studies predict that the wider a fossil stem is, the taller it might have been from a biomechanical point of view. In 1979 Chaloner & Sheerin showed that the maximum diameter of axes followed an increase that they described as ‘logarithmic’ through the Devonian. An arbitrary 10 cm threshold was reached in the early Middle Devonian (Fig. 1b). The earliest taxa to show such stems or branches belonged to Calamophyton and Pseudosporochnus, two pseudosporochnalean genera included in the Cladoxylopsida (Fig. 1a, b). Tall trees were present by the end of the Middle Devonian, represented by the stump casts of Eospermatopteris found in several localities near Gilboa (New York). These measure up to 1 m in diameter. In the Late Devonian, most wide axes belonged to two major but unrelated groups: the Lycopsida (i.e. Lepidosigillaria, Cyclostigma, Leptophloeum) and the progymnosperm Archaeopteridales (Fig. 1a, b). The Cladoxylopsida were still present but their stems did not reach the dimensions of the Pseudosporochnales. Indeed, those of Pietzschia, the largest known cladoxylopsid genus of Late Devonian age, did not exceed 16 cm in diameter

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(Fig. 1b). The Equisetopsida also evolved the tree habit, but in the latest part of the Devonian (Fig. 1a). The trunk of Pseudobornia was up to 60 cm wide (Fig. 1b), had distinctive nodes and produced three orders of branches. Nothing is known about the anatomy of these trees that, until now, has only been reported from the Famennian of Bear Island and Alaska (Mamay 1962; Schweitzer 1967; Fairon-Demaret 1986). Interestingly, and despite the intensive research conducted since then, Chaloner & Sheerin’s (1979) conclusions remain largely accurate in terms of trend and date for the earliest evidence of large sized plants (Middle Devonian) (Fig. 1b). One recent improvement, however, was the discovery of an archaeopteridalean trunk about 20 cm in diameter in a new Givetian (late Middle Devonian) locality near Ronquie`res in Belgium (Gerrienne & Meyer-Berthaud 2006). More importantly, the affinities of Eospermatopteris that have remained uncertain for more than 100 years have just been resolved. The trees supported by these stumps were not lepidosigillarian and related to the Lycopsida as suggested by Algeo et al. (2001) but, again, are pseudosporochnalean (Boyer & Matten 1996; Stein et al. 2007). The evidence, therefore, is that the earliest trees belong to the pseudosporochnalean cladoxylopsids followed by the progymnosperm Archaeopteridales with a period of overlap in the Givetian (Fig. 1b). The Cladoxylopsida and the Archaeopteridales are two major groups included in the euphyllophytes, a clade characterized by two derived characters related to architecture: (1) pseudomonopodial branching and (2) helically arranged branches (Kenrick & Crane 1997b) (Fig. 1a). The two branches issued from the pseudomonopodial division of an axis are not equal as for those resulting from the ancestral isotomous pattern of division. They differ in diameter and, generally, also in orientation (Fig. 1a). This pattern allows the differentiation of lateral branching systems that may become specialized to perform certain functions more efficiently, such as photosynthesis and reproduction. The helical arrangement of branches permits a wider range of spatial occupation than the strict arrangement of successive branches at 908 found in the ancestral taxa. The Cladoxylopsida are basal among a complex of taxa informally called ‘ferns s. l.’ that also comprises the Equisetopsida and diverse groups of Filicopsida. The Archaeopteridales are basal members of a strongly supported monophyletic group, the lignophytes, which also includes the seed plants (Fig. 1a). The derived character shared by the lignophytes is the possession of a cambium that produces both secondary xylem (i.e. wood) and secondary phloem, the latter tissue increasing the capacity for the long-distance transport of photosynthates.

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Morphology of pseudosporochnalean trees

The arborescent habit in the Cladoxylopsida The Cladoxylopsida evolved in the Early Devonian, were especially abundant and diversified in the Middle Devonian and became extinct in the Mississippian (Fig. 2). Morphologically, the Cladoxylopsida comprise several orders of branches but lack leaves, that is, determinate organs that are both twodimensional (2D) and with a photosynthetic lamina (Fig. 3a, b). The derived character shared by all members of the group is anatomical. It consists of a highly dissected vascular system, the most complex known among plants of this age (Fig. 3d, f, g). One question about this innovation is how this character may have been linked to the diversification of growth forms in the class and especially to the evolution of the pseudosporochnalean trees, the tallest plants of the Middle Devonian. In recent years, a large amount of morphological information briefly reviewed below has been accumulating on the Pseudosporochnales. This information has significantly increased our knowledge on how trees in this group may have looked like externally, in what habitat they grew and what kind of forests they may have formed. The structure and growth potential of their root system remains uncertain however, and information on the internal anatomy of the stem is still scarce (Leclercq & Lele 1968). Here, we propose a growth model integrating this information on the Pseudosporochnales together with the anatomical data we have accumulated in the past years on Pietzschia, a nonpseudosporochnalean genus that evolved largesized plants in the Late Devonian. We hypothesize that this model is applicable to a large range of Cladoxylopsida showing an erect habit. It may be used in further studies to estimate the amount of lignous tissues produced by pseudosporochnalean trees.

The Pseudosporochnales currently include four genera based on both vegetative and fertile material: Calamophyton, Pseudosporochnus, Wattieza and Lorophyton (Berry & Fairon-Demaret 2002) (Fig. 2). Although somewhat more accurate, the reconstruction of Calamophyton presented by Schweitzer (1973) has never been as popular as the amazing reconstruction of Pseudosporochnus elaborated by Leclercq & Banks (1962) and reproduced in many textbooks (Lemoigne 1988; Stewart & Rothwell 1993; Taylor & Taylor 1993). Evidence for the new reconstruction of Pseudosporochnus proposed by Berry & Fairon-Demaret (2002) comprises isolated pieces of trunks and branches of P. nodosus collected by Leclercq herself in the 1950s. The plant that these two authors reconstructed as a 3 m high tree is presumed to be a small representative of the genus. The tapering trunk measuring about 10 cm proximally and 6 cm distally bears densely inserted lateral branches that are shed as the tree grows. The younger branches, representing the photosynthetic modules of the tree, form a distal crown. Berry & FaironDemaret (2002) hypothesized that the basalmost part of the trunk in Pseudosporochnus was swollen based on the occurrence of bulbous bases in Bohemian specimens of P. verticillatus. This feature is known in two other pseudosporochnalean genera: Lorophyton and Calamophyton. In Lorophyton, roots radiate from the base (Fairon-Demaret & Li 1993). The recent reconstruction of the Gilboa trees whose crowns are referrable to Wattieza and swollen bases to Eospermatopteris (Fig. 3c) strengthens the concept of a pseudosporochnalean bauplan similar to Berry and Fairon-Demaret’s model of Pseudosporochnus (Fig. 5a). It also shows that such trees may have exceeded 8 m in

MISSISSIPPIAN Emsian

Foozia

Eifelian Givetian

Frasnian

Famennian

Tournaisian

Calamophyton Pseudosporochnus Wattieza Lorophyton Xenocladia

Pietzschia

Cladoxylon

Fig. 2. Stratigraphical distribution of the cladoxylopsid genera mentioned in the text. Pseudosporochnales in grey box. (Adapted from Lemoigne & Iurina 1983; Gerrienne 1992; Fairon-Demaret & Li 1993; Berry 2000; Edwards et al. 2000; Meyer-Berthaud et al. 2004; Soria & Meyer-Berthaud 2004; Cordi & Stein 2005.)

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Fig. 3. (a) Calamophyton, Pseudosporochnales. Digitate branch bearing 3D appendages. (b) Calamophyton, Pseudosporochnales. Detail of branches bearing 3D terminal appendages lacking lamina. (c) Eospermatopteris, Pseudosporochnales. Swollen base. (d) Pietzschia, Cladoxylopsida. Transverse section of axis showing a ring of radially elongated primary xylem strands around a very large pith. Small circular strands of primary xylem are also scattered in the pith. (e) Archaeopteris, Archaeopteridales, lignophytes. Transverse section of axis showing a significant amount of secondary xylem surrounding the central pith. (f) Cladoxylon, Cladoxylopsida. Transverse section of axis showing vascular strands containing radially aligned xylem tracheids compressing the surrounding pith cells (pc: primary cortex). (g) Xenocladia, Cladoxylopsida. Transverse section of axis showing discrete vascular strands containing radially aligned tracheids compressing pith cells.

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aligned xylem

aligned xylem pith

primary cortex (h)

cortex

(c)

vascular strands

pith

branches

(g)

(f)

genesis

DMP DMS

(a)

strands cortex

DMP

roots fused

genesis E genesis

pith A

roots free

(e)

primary cortex

Ground surface

DMP (b)

fused (d) roots

E

Fig. 4. Growth model for self-supporting cladoxylopsid stems. (a) Right: main primary growth phases (E, M, A) and their relative length. Two double arrows indicate the possibility for late tangential increase in the basal obconical part of the stem. Left: organs borne by the stem. After emission, roots run through stem tissues and emerge at base where they remain fused before separating distally. Roots increase in diameter proximally then become cylindical.

DEVONIAN TREES

height, had a relatively slender trunk tapering to a distal diameter of 13 –15 cm and had attached branches of about 1 m in length only (Stein et al. 2007). The latter formed a narrow crown. The regular shedding of branches contributed to the accumulation of a significant litter. Root casts preserved in the palaeosols at Gilboa do not exceed 3 cm in diameter and their vertical extension 30 cm (Driese et al. 1997).

Structure and growth patterns in Pietzschia The cladoxylopsid genus Pietzschia which comprises three species ranges from the Frasnian to the early Mississippian and has been recorded in Germany, USA and Morocco (Fig. 2). The two bestknown species in terms of growth patterns and anatomy are P. levis, consisting of stems that do not exceed 9 cm in diameter, and P. schulleri whose stems, up to 16 cm wide, are the largest known in the genus (Soria et al. 2001; Soria & Meyer-Berthaud 2004, 2005). Pietzschia differs from the Pseudosporochnales by conspicuous stem internodes and by a different morphology of the lateral branches. None of the specimens of Pietzschia examined show any secondary tissues. Anatomically, stems in cross-section are characterized by a ring of discrete, radially elongated, primary xylem strands organized at the periphery of a wide pith (Figs 3d & 4e). Some small circular xylem strands are also scattered within the pith. Depending on species and specimens, the cross-sectional surface area of xylem in Pietzschia ranges from 2.5 to 10% of the total crosssectional surface area of tissues in the stems (Soria et al. 2001; Soria 2003). This ratio is almost constant over single specimens. The outer cortex, presumed to be sclerenchymatous in the stem of P. levis, is less than 1 mm thick. In P. schulleri the crosssectional surface area of the outer cortex ranges from 17 to 24% of the total cross-sectional surface area of the stem but it is probably collenchymatous, therefore not lignous (Soria 2003; Soria & MeyerBerthaud 2005).

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Stem ontogeny in P. levis shows the two successive growth phases described as epidogenis and apoxogenesis in other plant taxa (Eggert 1961, 1962; Scheckler 1978) (Fig. 4d). The proximal part of the stem which is relatively short (10 –15 cm long) is obconical (i.e. shaped as an inverted cone) and corresponds to an increase in size of the primary body (epidogenetic growth) until it reaches its maximal diameter (DMP in Fig. 4d). The rest of the stem is conical and corresponds to a decrease in size of the primary body (apoxogenetic growth). The obconical part is surrounded by a thick mantle of adventitious roots that run through the stem cortex in the proximal part of their course. They emerge from the stem further down but remain partially fused and tightly packed outside the stem (Fig. 4d). The pattern of root production in P. levis is characterized by two traits: (1) there are few large roots produced at the very base of the stem and numerous small roots higher up; and (2) individual roots increase in size as they grow downwards (Soria & Meyer-Berthaud 2004). The result is that all individual roots appear similar in structure and dimension at any one level. They are wider at the base of the specimen. In outer morphology, this base looks swollen despite the fact that the stem itself is narrow (Fig. 4d). A biomechanical analysis following the approach of Rowe & Speck (1998) shows that the plant base is not self-supporting despite its thick root mantle, a result indicating that it was probably underground (Soria 2003). In the aerial conical part, the branch bases and stem cortex provide most of the support. Although it was expected that the dissected vascular system of the stem located in a relatively peripheral position (Fig. 4e) significantly increased stem stiffness, the mechanical tests indicate that it contributed little to its rigidity (only 3.3 to 12.3% of total flexural stiffness; Soria 2003). All the available stem specimens of P. schulleri are incomplete at both ends and the root system in this species in unknown. Ontogenetical studies show that the primary body is wider proximally and decreases in size distally (apoxogenesis),

Fig. 4. (Continued) (b) Growth patterns in the basalmost part of the stem. Right: tangential enlargement of stem base leading to formation of a swollen base, dissociation of roots and increased root spacing. (c) Hypothesized transverse section of stem above DMP showing the potential development of a secondary type of vascular tissue (radially aligned tracheids) inside a boundary defined by the primary cortex. Primary vascular strands in black. Central strands not shown here. (d, e) Stem structure and development in Pietzschia. (d) Stem showing two main primary growth phases (A and E). Basalmost part showing a thick mantle of fused roots around the obconical part of stem. Distalmost part of roots not preserved. (e) Diagramatic transverse section of Pietzschia stem above DMp, containing primary tissues only. Central strands, root traces and branch traces not shown here. (f, g, h) Stem structure and development in pseudosporochnalean trees. (f) Interpretative diagram of Eospermatopteris/Wattieza stem showing separated roots radiating from enlarged base. Possible part corresponding to epidogenetic phase limited by dotted line. (g) Diagrammatic transverse section of Eospermatopteris, adapted from Boyer (1995). (h) Diagrammatic transverse section of Duisbergia, adapted from Mustafa (1978). DMP: maximal diameter of stem resulting from primary growth; DMS: maximal diameter of basal part of stem resulting from late tangential enlargement.

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(a)

Pseudosporochnales (Cladoxylopsida)

(c)

Archaeopteris

leaves

leafless branches short-leaved branches

(b)

primary cortex

long-leaved branches

(d) secondary

cortex

Fig. 5. Compared arborescent strategies in the Cladoxylopsida as hypothesized in this paper (a, b) and in Archaeopteris (c, d). (a, c) Main morphological characters; triangles indicating significant growth potential. (b, d) Main anatomical characters of stems in cross-section; primary xylem in black, secondary type of xylem (i.e. containing radially aligned tracheids) in grey.

possibly after a growth phase where its diameter remains constant (menetogenesis; Soria & MeyerBerthaud 2005). As for P. levis, the dissected and peripheral vascular system contributes little to the rigidity of the stem (8.5 to 10.4% of total flexural stiffness; Soria 2003). These results on the genus Pietzschia show that it is not necessary to have secondary tissues to be big in the Cladoxylopsida. An unpublished biomechanical analysis by Soria & Speck (pers. comm., 2005) suggests that P. levis may have reached 7.5 m in height and P. schulleri 10 m. These results also show that, if the dissected vascular system of Pietzschia is an adaptive trait providing some

physical advantage to the evolution of tall plants, it is not related to biomechanical support.

Stem growth model for self-supporting Cladoxylopsida This model is aimed at providing a set of growth rules, expected to be shared by a wide range of cladoxylopsid taxa, that explain the record of morphologies they display. Our main argument for proposing this model is the similarity in the anatomical stem organization of Pietzschia, Eospermatopteris and Duisbergia, the presumed base of Calamophyton (Berry & Fairon-Demaret 2002)

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(Fig. 4e, g, h). From a three-dimensional analysis of casts, Boyer (1995) and Boyer & Matten (1996) recognized three zones in Eospermatopteris: a wide featureless pith-like part in the centre (17 cm wide in a stem exceeding 20 cm in diameter), a narrow zone comprised of vascular strands and an outer cortical zone (Fig. 4g). They interpreted the vascular strands as small, numerous and consisting entirely of primary tissues. Ongoing investigations by Stein et al. (2008) show, however, that all strands are surrounded by secondary-like tissue (i.e. comprised of radially aligned tracheids) and that the most peripheral strands are radially elongated. The Duisbergia stems described by Mustafa (1978) are compressed but their anatomical structure follows the same general organization. The remarkable traits shared by Eospermatopteris, Duisbergia and Pietzschia are the large amount of ground-like tissue in the central part of the stem and the peripheral location of the radially elongated vascular strands. One difference is the lack of secondary-like tissues in Pietzschia. Berry and Fairon-Demaret (2002) hypothesized that the possession of a secondary type of vascular tissue consisting of radially aligned tracheids may have contributed significantly to the realization and support of large stems in the Pseudosporochnales. Our opinion is different, based on indirect evidence from non-pseudosporochnalean cladoxylopsids. In the specimens of Xenocladia and Cladoxylon (Fig. 2) that we observed, the development of aligned vascular elements around each primary vascular strand is accompanied by the compression of the surrounding soft-walled cells of the ground tissue (Fig. 3f, g). When this development is extensive, pith cells are no longer visible. The vascular strands that were separate when composed of primary tissues only come into contact when surrounded by a secondary type of xylem. Secondary development of the vascular tissues in these genera is accommodated by the compression of the voluminous pith and remains within the limits of the primary body, determined by the primary cortex (Fig. 3f). The lack of evidence for secondary cortex (periderm) in all known cladoxylopsid (except one Mississippian specimen from Montagne Noire referrable to Cladoxylon taeniatum) adds credit to this alternative hypothesis (Soria et al. 2006). A biomechanical analysis was precisely realized on that species. Calculation of Young’s modulus of Cladoxylon taeniatum for different stages of growth shows that stem stiffness decreases with the development of the secondary cortex, despite the large amount of secondary xylem produced (Soria et al. 2006). This loss of stiffness occurred when the increase in girth due to the secondary tissues exceeded the limits of the primary body. This example, taken in the Cladoxylopsida, indicates that the development of secondary vascular tissues is not necessarily

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linked to increased performances in terms of support. The hypothesis that we defend here is that the strategy for building large-sized plants in the Cladoxylopsida was different from that in the lignophytes such as Archaeopteris (Fig. 5b, d). The development of secondary vascular tissues was, at most, moderate compared to that in the arborescent lignophytes. The major advantages which such tissues provided to large-sized cladoxylopsids were probably more significant in terms of water transport than mechanical support. The model for stem growth that we propose for self-supporting Cladoxylopsida (Fig. 4a–c) integrates the anatomical, morphological and developmental information reviewed above. Basic features of this model are as follows. 1. The stem shows two main growth phases of unequal importance (Fig. 4a). The epidogenetic phase where the primary body increases in size and forms an obconical base is short. It is mostly or entirely underground. The apoxogenetic phase where the primary body decreases in size is the longest and corresponds to most, if not all, of the aerial part of the stem that bears branches. A third menetogenetic phase where the size of the primary body remains constant may follow the epidogenetic phase and precede apoxogenesis. 2. The maximum diameter of the stem above ground (labelled DMP in Fig. 4a, d, f ) results from the large size of the primary body. This condition is reached early during growth, at the end of the short epidogenetic phase. 3. Roots are adventitious and tightly packed around the obconical base (Fig. 4a, d). 4. The obconical base is the only part that may undergo some late tangential expansion outside the limits of the primary body (Fig. 4a, b, f). This increase in girth may be due to a proliferation of the living cells of the stem. The stem base, then, may take a swollen shape. Its maximum diameter (labelled DMS in Fig. 4f) may exceed DM and individual roots become separated from each other. 5. A secondary-type of xylem comprising radially aligned tracheids may develop around the individual vascular strands. This development does not contribute significantly to the tangential enlargement of the stem in its aerial part, above the level of DMP (Fig. 4c).

Habitat and geographical distribution of the pseudosporochnalean trees By analogy with extant trees, the reduced size and narrow shape of the crown of the Gilboa trees

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suggests that they were closely spaced; this distribution is confirmed by the spatial arrangement of in situ stumps (Banks et al. 1985; Driese et al. 1997). However, these trees that lacked laminar leaves may not have formed completely closed canopies (Stein et al. 2007). Allochtonous plant remains associated with the in situ casts represent smaller sized plants such as bushy Aneurophytales and herbaceous lycopsids. It is currently uncertain whether these remains were components of the forest understory or if they were washed up into the fossil deposits during floods or other catastrophic events. The Gilboa trees lived in the Catskill delta, either on levees that were periodically flooded (Banks et al. 1985; Boyer 1995) or in a wet, poorly-drained coastal margin setting (Driese et al. 1997). The climate is thought to have been tropicaldry with possible heavy seasonal rainfalls (Banks et al. 1985). Remains of pseudosporochnaleans are abundant in Laurussia on both sides of the Acadian mountains (Berry & Fairon-Demaret 2001). They have been reported to be common in Middle Devonian deposits of Siberia and Kazakhstan (Iurina 1988) but Meyen (1987) questioned the validity of the identification of fossil plants from these areas. In Gondwana, where Devonian plant localities are few and do not yield well-preserved remains, there are no records of pseudosporochnaleans apart from the Wattieza described from the Lower Member of the Campo Chico Formation in Sierra de Perija´, Venezuela (Berry 2000). It is not certain, however, that the Sierra de Perija´ terrane was already part of Gondwana in the Middle Devonian (Berry et al. 2000). Pseudosporochnaleans are unknown in North China (Cai & Wang 1995) and all previous records of Pseudosporochnus from South China have recently been dismissed (Berry & Wang 2006a). The closest genus found in South China is Rhipidophyton, which is common in Yunnan where it is represented by axes measuring up to 9 cm in diameter (Berry & Wang 2006b).

Conclusion The pseudosporochnalean trees and the Archaeopteridales that evolved in the Devonian form two types of euphyllophyte trees which contrast not only morphologically but also structurally and developmentally. Morphologically, recent discoveries demonstrate that the pseudosporochnalean trees resemble tree-ferns, that is, that they possess a trunk bearing adventitious roots at base and topped by a narrow crown of deciduous branches (Stein et al. 2007) (Fig. 5a). Individual roots are a few centimetres wide and have a limited vertical extent. Above ground, the only perennial organ

(i.e. the only organ able to grow significantly) is the trunk. The supply of branches that are regularly replaced may not have changed significantly during the lifetime of the tree. In the arborescent pseudosporochnaleans, branches lack leaves. By contrast, Archaeopteris trees possess leaves and have long-lived roots and branches (Fig. 5c). Their growth can be qualified as three-dimensional by comparison to the essentially vertical growth of the pseudosporochnalean trees (Algeo et al. 2001; Meyer-Berthaud & Decombeix 2007). With the developmental model that we propose for the arborescent Pseudosporochnales, we challenge the idea defended by Berry & Fairon-Demaret (2002) of a lignophytic model of growth for these trees. We hypothesize that their large size, or more specifically the large diameter of their trunk above ground, results from the large size of their primary body (Fig. 5b). Secondary vascular tissues contribute little if anything to trunk diameter and support. The maximal width of the primary body is reached early during growth. This strategy where the large size of the trunk is reached early during growth and does not necessitate the development of secondary vascular tissues for mechanical support is very different from that shown in the lignophyte trees such as Archaeopteris. The latter invest essentially in secondary xylem (wood) to achieve diameter and mechanical support as well as water transport (Figs 3e & 5d). In the arborescent lignophytes, the maximal diameter of the trunk is reached late during growth. Considering both Algeo’s Devonian plant hypothesis (Algeo et al. 2001) and the Beerling & Berner (2005) model, the differences assessed in terms of root system, biomass allocation during growth and amount of lignous tissues in these two euphyllophyte strategies suggest that they probably impacted the environment differently. In addition, the limited extent of the root system and large amount of living cells forming the trunk in pseudosporochnalean trees suggest that (1) these plants probably inhabited areas with no water limitation during the growth season and (2) that they avoided climates with freezing temperatures. The gymnosperm type of vegetative body of archaeopteridaleans was adapted to a wider range of conditions including cold climates. The pseudosporochnalean trees were well represented in a low south latitude warmtemperate zone in the Middle Devonian (Stein et al. 2007). Archaeopteridaleans were cosmopolitan in the Late Devonian. The former considerations may explain these differences in terms of palaeogeographical distribution. We thank L. VanAller Hernick, F. Mannolini, B. Stein and C. Berry for permission to visit their working collections of plants from Gilboa. These fossils are housed in the

DEVONIAN TREES New York State Museum at Albany. We thank P. Gerrienne for permission to publish the photographs illustrated in Figures 3a, b and B. Stein for the photograph in Figure 3c. The comments and suggestions of two anonymous reviewers were highly appreciated. This research was funded by two projects: Eclipse II ‘Terrestrialization’ and ANR ‘Accro-Earth’. AMAP (Botany and Computational Plant Architecture) is a joint research unit which associates CIRAD (UMR51), le CNRS (UMR5120), l’INRA (UMR931), l’IRD (R123) and l’Universite´ de Montpellier 2 (UM27) (http://amap.cirad.fr/).

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(Middle Devonian, Belgium): preliminary results. 7th European Palaeobotany –Palynology Conference, Prague. Abstracts, 46. Iurina, A. 1988. The Middle and Late Devonian floras of northern Eurasia. Transactions of the Palaeontological Institution, Academy of Sciences SSSR (in Russian), 227, 1– 175. Kenrick, P. & Crane, P. 1996. Embryophytes. Land Plants. Version 01 January 1996 (temporary). http:// tolweb.org/Embryophytes/20582/1996.01.01 in The Tree of Life Web Project, http://tolweb.org/. Kenrick, P. & Crane, P. 1997a. The origin and early evolution of plants on land. Nature, 389, 33–39. Kenrick, P. & Crane, P. 1997b. The Origin and Early Diversification of Land Plants: A Cladistic Study. Smithsonian Institution Press, Washington D.C. Leclercq, S. & Banks, H. P. 1962. Pseudosporochnus nodosus sp. nov., a Middle Devonian plant with cladoxylalean affinities. Palaeontographica B, 110, 1 –34. Leclercq, S. & Lele, K. M. 1968. Further investigation on the vascular system of Pseudosporochnus nodosus Leclercq et Banks. Palaeontographica B, 123, 97–112. Lemoigne, Y. 1988. La flore au cours des temps geólogiques. Geóbios, Me´moire Spećial, 10, 1 –356. Lemoigne, Y. & & Iurina, A. 1983. Xenocladia medullosina Ch. A. Arnold (1940) 1952 du De´vonien Moyen du Kazakhstan (URSS). Geobios, 16, 513 –547. Mamay, S. H. 1962. Occurrence of Pseudobornia Nathorst in Alaska. Palaeobotanist, 11, 19–22. Meyen, S. 1987. Fundamentals of Palaeobotany. Chapman and Hall, London. Meyer-Berthaud, B. & Decombeix, A.-L. 2007. A tree without leaves. Nature, 446, 861– 862. Meyer-Berthaud, B., Scheckler, S. E. & Wendt, J. 1999. Archaeopteris is the earliest modern tree. Nature, 398, 700–701. Meyer-Berthaud, B., Ru¨cklin, M., Soria, A., Belka, Z. & Lardeux, H. 2004. Frasnian plants from the Dra Valley, southern Anti-Atlas, Morocco. Geological Magazine, 141, 675– 686. Mosbrugger, V. 1990. The tree habit in land plants. In: Bhattacharji, S., Friedman, G. M., Neugebauer, H. J. & Seilacher, A. (eds) Lecture Notes in Earth Sciences. Springer–Verlag, Berlin. Mustafa, H. 1978. Beitra¨ge zur Devonflora III. Argumenta Palaeobotanica, 5, 91– 132. Niklas, K. J. 1993. The scaling of plant height: a comparison among major plant clades and anatomical grades. Annals of Botany, 72, 165 –172. Niklas, K. J. 1997. The Evolutionary Biology of Plants. The University of Chicago Press, Chicago. Robinson, J. M. 1996. Atmospheric bulk chemistry and evolutionary megasymbiosis. Chemosphere, 33, 1641–1653. Rowe, N. P. & Speck, T. 1998. Biomechanics of plant growth forms: the trouble with fossil plants. Review of Palaeobotany and Palynology, 102, 43–62.

Scheckler, S. E. 1978. Ontogeny of progymnosperms. II. Shoots of Upper Devonian Archaeopteridales. Canadian Journal of Botany, 56, 3136– 3170. Schweitzer, H. P. 1967. Die Oberdevon-Flora der Bareninsel. 1. Pseudobornia ursina Nathorst. Palaeontographica B, 120, 116 –137. Schweitzer, H. P. 1973. Die Mitteldevon-Flora von Lindlar (Rheinland). 4. Filicinae- Calamophyton primaevum Kraüsel & Weyland. Palaeontographica B, 140, 117 –150. Soria, A. 2003. Structure, de´veloppement et fonctionnalite´s des formes chez les premie`res fouge`res s.l.: le genre de´vonien Pietzschia Gothan (Cladoxylopsida). PhD. Thesis, University of Montpellier II. Soria, A. & Meyer-Berthaud, B. 2004. Tree fern growth strategy in the Late Devonian cladoxylopsid species Pietzchia levis from the study of its stem and root system. American Journal of Botany, 91, 10–23. Soria, A. & Meyer-Berthaud, B. 2005. Reconstructing the Late Devonian cladoxylopsid Pietzchia schulleri from new specimens from southeastern Morocco. International Journal of Plant Sciences, 166, 857–874. Soria, A., Meyer-Berthaud, B. & Scheckler, S. E. 2001. Reconstructing the architecture and growth habit of Pietzchia levis sp. nov. (Cladoxylopsida) from the Late Devonian of southeastern Morocco. International Journal of Plant Sciences, 162, 911–926. Soria, A., Rowe, N. P., Galtier, J. & Speck, T. 2006. Having or lacking secondary growth: consequences on the mechanical architecture of Paleozoic cladoxylopsids (fern-like plants). 5th Plant Biomechanics Conference, Stockholm, 43– 48. 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, 904– 907. Stein, W. E., Berry, C. M., Mannolini, F., Hernick, L. V., Landing, E. & Boyer, J. S. 2008. Development of early tree form in pseudosporochnalean cladoxylopsid plants. 12th International Palynological Congress & 8th International Organisation of Palaeobotany Conference, Bonn, Abstract volume, 266. Stewart, W. N. & Rothwell, G. W. 1993. Paleobotany and the Evolution of Plants. Cambridge University Press, Cambridge. Stubblefield, S. P., Taylor, T. N. & Beck, C. B. 1985. Studies on Paleozoic fungi: IV Wood-decaying fungi in Callixylon newberryi from the Upper Devonian. American Journal of Botany, 72, 1765–1774. Taylor, T. N. & Taylor, E. L. 1993. The Biology and Evolution of Fossil Plants. Prentice Hall, Englewood Cliffs. Trivett, M. L. 1993. An architectural analysis of Archaeopteris, a fossil tree with pseudomonopodial and opportunistic adventitious growth. Botanical Journal of the Linnean Society, 111, 301–329.

Early seed plant radiation: an ecological hypothesis C. PRESTIANNI* & P. GERRIENNE Universite´ de Lie`ge, unite´ P.P.M., Alleé du 6 aouˆt, B18/P40, 4000 Lie`ge *Corresponding author (e-mail: [email protected]) Abstract: The earliest steps of seed plant evolution have been extensively studied during the past 25 years. There is a growing body of evidence indicating that the first major spermatophyte radiation occurred during the Late Devonian. At least fourteen Late Devonian species are now recognized, and our knowledge of the diversity of those early seed plants has dramatically increased. Five morphotypes of seeds have been defined, mostly based on cupule morphology and on the number and degree of fusion of the integumentary lobes. In this paper, we critically discuss the abundant environmental information in order to characterize the environment in which this radiation occurred. Sedimentological information indicates that seed plants evolved in disturbed environments. It is suggested that early seed plants thrived in the shade of the dominating Archaeopteris, and that their evolution was canalized by this strong biotic pressure. We also confirm the previous suggestion that the variability of seed morphotypes can be explained by the weak abiotic selective pressure that existed in the Archaeopteris understory.

The seed habit is the most complex and efficient plant reproductive strategy. It has been set up as early as 380 Mya during the Middle Devonian (Gerrienne et al. 2004; Gerrienne & MeyerBerthaud 2007). Since then, seed plant evolution is an uncontested success story still in the making. The earliest steps are however obscure and the subject of much speculation (Chaloner & Pettitt 1987; DiMichele et al. 1989; Stewart & Rothwell 1993; Herr 1995). The very early changes that allowed the seed habit evolution are complex. The fossil record is still scarce and incomplete and is as difficult to understand as Darwin’s ‘abominable mystery’ of angiosperm development. The welldocumented Lower Carboniferous wide range of ovular type morphologies has long been considered as first radiation of seed plants (Long 1975; DiMichele et al. 1989, 2006). However, prior to this, Upper Devonian floras included an already diversified spermatophyte community (Hilton 1998a; Prestianni 2005). This rapid radiation of seed plants is the subject of palaeobotanical investigations (DiMichele et al. 1989) as well as seed plant broader evolutionary studies (Rydin et al. 2002; Rai et al. 2003). The present paper discusses the Upper Devonian spermatophyte evolution within the palaeoenvironmental context. The earliest occurrences of seed plants or of supposedly close relatives are found in the Givetian of Poland, Greenland and Belgium (Arkhangelskaya & Turnau 2003; Marshall & Hemsley 2003; Gerrienne et al. 2004; Turnau & Prejbisz 2006). Granditetrasporites zharkovae, Spermasporites allenii and Runcaria heinzelinii represent a ‘complex’ of seed-megaspores and proto-seed that

are representative of the first stages of the evolution of seed plant and of their putative sister groups. They presumably witnessed a set of Middle Devonian palaeoenvironmental deep changes such as the first forests (Meyer-Berthaud & Decombeix 2008), biotic crisis in the marine realm (McGhee 1996) and continental aridity crisis (Marshall et al. 2007). However, these changes will not be discussed here as their complexity requires an independent treatment beyond the scope of this paper. The Frasnian and Lower Famennian fossil records are strikingly scarce and no seed plants have been recorded so far (Prestianni 2005). A single occurrence of the seed species Moresnetia zalesskyi (see below) is reported from the Petino (or Petin) horizon near Semiluki, Russia (ThchirkovaZalesskaıä 1957; Jurina 1988). This record was dated Upper Frasnian (Smirnova 1974) on the basis of a palynological study. A recent review (Avkhimovitch et al. 1993) of the western Russia palynological record has correlated several localities, including Petino, at a large scale. This work attributed this horizon to the Middle Frasnian OG zone, more precisely to the CVe subzone. Even although the age seems to be accurate and recording a very early occurrence of Moresnetia, the identification of the plant material still needs to be confirmed. A rapid and already diversified assemblage of seed plant species occurs during the Upper Famennian VCo and VH biozones (Fig. 1) (Hilton 1998a; Prestianni 2005). Seeds of that age have mainly been collected from Belgium and northeast USA (Fig. 2). In Belgium, most of the fossiliferous outcrops belong to the Evieux Formation, Condroz


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C. PRESTIANNI & P. GERRIENNE

Fig. 1. Biostratigraphical chart of Famennian miospore zones (right-hand column). Note presence of dotted lines at the base of the VH miospore biozone that express the uncertainty of correlations. Left-hand column: the absolute ages (Gradstein et al. 2004) (stratigraphical chart modified from Thorez et al. 2006).

group (Fairon-Demaret 1996a). This Formation was deposited onto a shallow epicontinental platform in an alluvio-lagoonal context. Restricted marine or emerging lagoonal ponds characterizes the Evieux Formation palaeoenvironments that were thus strictly neritic (Thorez et al. 2006). The palaeoflora is very diverse: Stockmans (1948) collected and named 25 different taxa, but currently only 14 species have been formally recognized (FaironDemaret 1996a). The flora has been attributed to the VCo palynozone (Thorez et al. 2006). The northeast American outcrops are found in the Hampshire Formation at Elkins (Rothwell et al. 1988) and in the Catskill Formation at Red Hill (Cressler 2006). The occurrences at Elkins of coal beds with roots and bioturbated zones beneath suggest a continental environment deposited in a fluvial to deltaic context (Scheckler 1986). Sedimentation at Red Hill occurred in an upper alluvial plain context (Diemer 1992). Elkins and Red Hill localities have both been attributed to the VH palynozone, suggesting an age slightly younger than that of the Belgian deposits (Scheckler 1986; Traverse 2003). However, several correlation issues exist between American and European sediments (Streel & Marshall 2007). As palynofloras are continental markers, but also distributed in marginal sea where they can be sometimes calibrated by the conodont stratigraphy, intercontinental correlations depend on the availability of that calibration. Richardson & Ahmed (1988) suggest a delayed first occurrence of the characteristic spores of the

Fig. 2. Palaeogeographical distribution of Upper and Uppermost Devonian seed plant localities. 1, Condroz sandstones; 2, Elkins, Red Hill and Port Alleghany; 3, Taffs Well, Baggy Beds and Avon Gorge; 4, Kerry Head; and 5, Oese (map modified from Scotese 1999).

EARLY SEED PLANT RADIATION

VCo palynozone between American and European deposits, the VCo palynozone starting first in the USA. This situation might be attributed to contrasted climates for the two regions (Streel & Marshall 2007). It happens however that the northeast American miospore/conodont calibration is far from being conclusive (Streel & Loboziak 1994). An alternative climatic v. correlation challenge is still considered by Blieck et al. (2010). Consequently, the VH and VCo biozones will be treated here as a single biozone and the localities as being more or less synchronous. ‘Uppermost’ Famennian localities are found in the US, Ireland, England and Germany (Fig. 2). In the northeast American Catskills, the Oswayo Formation has historically yielded the first recognized Devonian seed (Pettitt & Beck 1969). In Ireland, several localities are recorded; Kiltorkan Hill and Hook Head will not be discussed as the seeds that were collected there have not yet been described and are poorly understood and/or controversial (Chaloner et al. 1977). Ballyheigue, however, probably provides the best preserved in terms of quality of the preservation Upper Devonian flora (Matten et al. 1980; Matten et al. 1984). This anatomically preserved silicified flora is dominated by spermatophytes. This specific facies containing in situ plants is interpreted as levee or crevasse deposits in a marginal to channel environment. English Devonian seeds have been collected from three main localities from southwest Great

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Britain. The Baggy Beds and Taffs Well are of similar age (LL-LE) (Higgs et al. 1988; O’Liathaìn 1992) but represent two distinct palaeoenvironments. The Baggy Beds are interpreted as the shallow marine part of an inner shelf or barrier complex (Goldring & Langenstrassen 1979). Taffs Well deposition occurred in a more continental context and has been interpreted as non-marine, with a low flow regime, or as a freshwater lake (Gayer et al. 1973). The slightly younger (LN) Avon Gorge locality is sedimentologically poorly understood, but a distal fluvial environment is proposed (Hilton 1998a). Finally, the youngest known Famennian seed locality is in the German Hangenberg Sandstein at Oese. Seeds have been found in shales containing highly fragmentary plant meso-debris (Rowe 1997). This assemblage is interpreted as a high energy offshore deposit and attributed to the LN palynozone (Higgs & Streel 1984).

Early seed plant diversity and habit Seed plants were already diversified during the Late Devonian (Hilton 1998b; Prestianni 2005). Fifteen species are now described. Based on their morphology and anatomy, seeds have been classified into five different types (Prestianni 2005): the Moresnetia-type, Aglosperma-type, Dorinnothecatype, Condrusia-type and Warsteinia-type (Fig. 3). They share an apically modified nucellus, a lobed integument (except Condrusia) and a cupule (not

Fig. 3. Schematic reconstruction at the same scale of the different Upper and Uppermost Devonian seed morphological types. (a– d) Nucellus in dark grey and shown by transparency and (e) ovule is shown in dark grey and by transparency. (a) Moresnetia-type, (b) Dorinnotheca-type, (c) Warsteinia-type, (d) Aglosperma-type and (e) Condrusia-type.

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present in Warsteinia paprothii Rowe). The taxonomy of those early seed representatives is based mainly on variation in the integument, including various degrees of fusion of the integumentary lobes and/or characteristics of the cupule. The apical modification of the nucellus is remarkably uniform (see Fig. 3). The nucellar apex is modified into a pollen chamber (Gordon 1941) closed by a pollen chamber floor and extended by a cylindrical structure (Hilton & Edwards 1996) referred to as a salpinx (Gordon 1941); the pollen chamber contains a central dome of parenchymatous cells. This combination of traits characterizes the hydrasperman reproductive syndrome (Rothwell 1986; Rothwell & Scheckler 1988). The Moresnetia-type includes Archaeosperma arnoldii (Pettitt & Beck 1968), Elkinsia polymorpha (Rothwell et al. 1989 emend. Serbet & Rothwell 1992), Glamorgania gayerii (Hilton 2006), Kerrya mattenii (Rothwell & Wight 1989), Lenlogia krystofovichii (Petrosyan in Lepekhina et al. 1962 emend. Krassilov & Zakharova 1995), Moresnetia zalesskyi (Stockmans 1948 emend. Fairon-Demaret & Scheckler 1987) and Xenotheca devonica (Arber & Goode 1915 emend. Hilton & Edwards 1999). It is characterized by a four-unit cupule, formed by two successive cruciate dichotomous divisions (Prestianni 2005) (Fig. 3a). Cupules define a wellcircumscribed space where up to four seeds (exceptionally six, Matten et al. 1980) are found. The hydrasperman nucellus is surrounded by several variably fused integumentary lobes. Which exact part of this plant is dispersed remains unknown. The fossil record includes Moresnetia-type parts ranging from large branching systems to isolated cupules. The branching systems are probably not the propagules (dispersed part of the plant). Rather, they represent whole plants that have been buried before dispersal of their seeds (FaironDemaret & Scheckler 1987). Indeed, a close observation of the cupules shows that many of them lack seeds (Fairon-Demaret & Scheckler 1987). Additionally, the collected branching systems are of variable size and range from 1 time dichotomizing axe to up to 15 times dichotomizing axis, highlighting the random break of these axes. These observations suggest that seeds are presumably the propagules of the Moresnetia-type plants. No dispersed seeds of this type have yet been recognized in the fossil record, however, but this may reflect sedimentation and/or collecting bias. The cupules and integuments of all the plants of the Moresnetia-type do not show clear dispersion traits. A notable exception is the seed from Port Alleghany Archaeosperma arnoldii, where the lower part of the integument is covered by spines or hairs which have been interpreted as being related to dispersal (Pettitt & Beck 1968).

As with most of the seeds of the Moresnetiatype, no clear modification for dispersal is observed in Aglosperma-type seeds, comprising Aglosperma quadrapartita (Hilton & Edwards 1996), Aglosperma avonensis (Hilton 1998b), Pseudosporogonites hallei (Stockmans 1948) and Xenotheca bertrandii (Stockmans 1948) (Fig. 3d). In this type, the integument is formed by three to four flat lobes fused up to their lower third. The cupule is a tiny structure that inconspicuously covers the base of the integument. Similarly, many extant seeds (or fruit) do not present any evident morphological traits (Ridley 1930). Dispersal of these may be performed by rain or wind in the case of sufficiently small seeds. Zoochory (dispersal by animals) cannot be dismissed. During the Late Devonian, arthropods are the only putative dispersal candidates as vertebrates were confined to aquatic environments. Labandeira (2006) has divided the evolution of plant-arthropod associations into four phases based on functional feeding groups. The Famennian conforms to the end of the first phase (420 –360 Ma). This phase is characterized by small herbivorous myriapods and apterygotes. Since these two groups do not have a strong dispersal potential and no adaptation to arthropod attraction is observed on seeds, we consider zoochory unlikely in early seed plant dispersal. Other seed types suggest adaptations for wind dispersal. Seeds of the Dorinnotheca-type are represented by a single species, Dorinnotheca streelii (Fairon-Demaret 1996b). They show an ovular morphology similar to that of the Aglosperma-type with three to four lobes (Fig. 3b). However, the cupule is much larger and is composed of eight proximally fused parts forming a cup, with the distal segments divided into at least 40 free endings. In this, the cupule is interpreted to be part of the propagule as all dispersed seeds were still closely attached to it. This dispersal apparatus can be compared to the Corolline or Sepaline fruits described by Ridley (1930), which are related to wind dispersal. Similarly, seeds of the Condrusia-type – Condrusia rumex (Stockmans 1948), C. minor (Stockmans 1948) and C. brevis (Petrosyan in Lepekhina et al. 1962) – are enclosed in a welldeveloped wing which is composed of two flat cupule segments adpressed against each other (Fig. 3e). This wing is interpreted as a dispersal apparatus. Finally, the Warsteinia-type, represented by Warsteinia paprothii (Rowe 1997), has been found devoid of cupules and hence is considered as acupulate (Fig. 3c). The integument is made up of four winged lobes adnate to the nucellus. The presence of integumentary wings is strongly suggestive of anemochory, even although hydrochory cannot be totally dismissed.


Seed dispersion Even although morphology often indicates the general means of dispersal, an apparently obvious modification for dispersal may not always predict the actual process (Howe & Smallwood 1982). Many studies on the ecology of seed dispersal (Howe & Smallwood 1982; Willson & Traverset 2000) agree on the complexity of the mechanisms involved. Propagule dispersal can only be well interpreted in natural environments with direct observations. Pioneering works (Ridley 1930) as well as recent studies (Cain et al. 2000; Tackenberg et al. 2003) have however provided much information on living plants that can be used to infer about fossils. Even although Upper Devonian seeds encompass a wide range of morphological variations, nearly all observed morphologies point to wind as the major dispersal agent. Other means cannot be excluded, but the available information is poor. DiMichele et al. (1989) discussed for Tournaisian spermatophytes a similar diversity pattern centred on integument architecture only. In their model, seed plants are seen as having evolved in an ‘open’ selective landscape; natural selection does not appear to have strongly influenced early seed plant diversification. This low interspecific competition allowed seed plants to explore various morphologies and thus radiate. The underlying hypothesis is that seed plants established in large areas with reduced or no biotic competition; survival in such ecosystems was controlled by abiotic selection processes. In order to correctly understand this abiotic selection context, the environment has to be characterized. Geology, and more precisely sedimentology, is the only available tool.

Early seed plant ecology Rothwell & Scheckler (1988) were the first to tentatively locate early seeds in the Upper Devonian environments. They used the geological settings to extrapolate early seed plant ecology and concluded that the earliest gymnosperms were ‘pioneer colonizers of newly emerged, primary successional habitats near shorelines’. They based this assumption on a particular succession of autochotonous to hypoautochtonous beds at Elkins. First mats of only seed plants are observed, then monotypic Rhacophyton (early fern) layers and, finally, a diverse allochtonous assemblage. The successions present in Belgium, at the Langlier quarry, are roughly similarly organized (Thorez J. pers. comm., 2006), and provided some of the best preserved specimens of Moresnetia (Fairon-Demaret & Scheckler 1987). This succession begins with an almost pure bed of Archaeopteris (progymnosperm) followed by a thick bed of profusely branched

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large specimens of Moresnetia replaced by pure Rhacophyton layers. Since this succession occurs within less than 1 m of sediment, we tentatively conclude that it represents an ecological succession; this is a reasonable support for the Rothwell & Scheckler’s (1988) hypothesis. Cressler (2006) investigated the Upper Devonian landscape and its biotic associations at the extensive Red Hill locality. He studied the sedimentology of the different layers from Red Hill precisely. He was then able to place the various fossiliferous layers in the landscape, identify the plant fossiliferous layer as a floodplain pond and locate the parautochtonous plant fossils in both successional sequence and distance from the shore. This precise positioning, coupled with a layer by layer statistical study of plant remains provided the spatial organization of these deposits. Considering all deposition biases, Cressler (2006) was able to estimate the original growth position of the vegetation on the landscape. His model proposes that niche partitioning occurred at a high taxonomic level during the Upper Devonian, exactly as suggested by DiMichele & Bateman (1996) for the Carboniferous. Due to a well-documented argumentation, they were able to demonstrate ecological affinities of entire clades at the class level. The terrestrial surface was thus divided in sub-environments within each class-level taxa. The Upper Devonian environment predates this organization with Progymnosperms (Archaeopteris) established on the well-drained areas, ferns (Rhacophyton) growing as monotypic populations widespread in the surrounding landscape, lycopsids living on the edge of ponds and spermatophytes being opportunistic pioneer plants in burned areas. Taffs Well and the Baggy Beds in Great Britain represent continental and marine deposits, respectively. The Taffs Well continental deposits present a more diverse assemblage, seed plants included. Only one species, Xenotheca devonica (belonging to the Moresnetia-type), is represented at Baggy Beds (Hilton & Edwards 1999). The occurrence of the single Moresnetia-type in the most distal deposits has been interpreted as an isolated event that drifted one particular population of that plant. This is probably not the case, as the extensive, mainly neritic Belgian deposits gave similar results with seed plants of the Moresnetia-type being the most common. The enormous fossil plant material collected by François Stockmans, who did one of the most complete and systematic Upper Devonian fossil plant collections, comes from 25 quarries and outcrops. In this collection, Moresnetia represents 60% of the spermatophyte remains. The remaining 40% are covered by the other seed types present in Belgium (Condrusia-type, Dorinnotheca-type and

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Aglosperma-type). This dominance of the Moresnetia-type over other seed types in the Belgian neritic deposits confirms the British observations, and thus contradicts the isolated event hypothesis. It is tempting to conclude that the Moresnetiatype dominated, with its abundance in the fossil record corresponding to its Upper Devonian abundance. The fossil record is however strongly biased. The Belgian Upper Devonian deposits are all mostly marine. The fossil assemblage is thus drifted, sometimes quite far from its growing site. Moresnetia has often been found in connection with its branching system. In contrast, the other Belgian seeds (Aglosperma type, Dorinnothecatype and Condrusia-type) are most often found as isolated seeds. This suggests that the relative abundance of the Moresnetia-type is more likely due to preferential fossilization than to its original abundance in the environment. Rothwell & Sheckler’s (1988) inferences on the Upper Devonian ecological successions were mainly based on Moresnetia-type plants. Their conclusions might only apply to this morphological type, with those plants being pioneer colonizers of newly emerged, primary successional habitats near shorelines. This concept could probably also be extended to river margins. By contrast, the other seed-types are never or very rarely collected in attachment to extensive branching systems, suggesting that they were probably thriving in other habitats. Their ecology and precise environment are however impossible to characterize precisely.

Seed plants and their environment: an ecological hypothesis Chaloner & Sheerin (1981) suggested that the increase of seed size in the Carboniferous could be explained by the progressive switch from r selection to K selection. This r/K selection model classifies organisms into equilibrium (K) and opportunistic (r) species (Pianka 2000). Upper Devonian and Lower Carboniferous small-sized seeds would therefore be considered as r-selected and the Upper Carboniferous large-sized seeds as K-selected. All subsequent studies which focused on the earliest seeds confirmed this trend (Rothwell & Scheckler 1988; Rowe 1997; Cressler 2006). Most Upper Devonian spermatophytes probably roughly conform to the Elkinsia polymorpha reconstruction (Serbet & Rothwell 1992), that is, moderate-sized plants producing a large number of small seeds. These characteristics conform to the morphology associated with pioneer opportunistic species. Recent researchers have discussed the predictive and explanatory limitations of the r/K model

(Ziehe & Demetrius 2005; Demetrius & Ziehe 2007). They propose instead a new set of parameters named the ‘Directionality theory’. In this model, populations are compared to a thermodynamic process and their characterization is based on a parameter called demographic entropy. This allows the quantification of the population parameters that can then be compared to each other. Plant populations that spend most of their life history in stationary growth (vegetative growth) are characterized by high demographic entropy values. By opposition, plant populations that spend most of their life history in the exponential growth phase are characterized by low demographic entropy values. This model can be qualitatively applied to the Upper Devonian environment. As discussed above, the landscape was ecologically partitioned at a high taxonomic level that is, in habitats ranging from those devoted to opportunistic species to those occupied by equilibrium species. Archaeopteris populations were probably defined by the highest demographic entropy values as shown by the large trunks and the extensive photosynthetic apparatus. By contrast, the herbaceous plants such as Eviostachya hoegii or Gillespieae randolphensis had very low if not the lowest demographic entropy values. Rhacophyton and/or seed plants had middling values. The Upper Devonian environment was therefore probably much more complex than currently recognized. Indeed, using a quantitative palynology approach, Streel (1999) was able to demonstrate the occurrence of at least four distinct ecological niches in Laurentian terrestrial environments. Moreover, all fossil plant communities considered in the present paper, including continental localities as well as the sediments studied in Streel (1999), only record nearshore environments. The outstanding records of the Refrath borehole are an exception to this assessment, however (Fairon-Demaret & Hartkopf-Fro¨der 2004). The Refrath borehole was drilled in Germany near Cologne and passed through marlstone/mudstone sediments attributed to the upper Knoppenbissen Formation (Fairon-Demaret & Hartkopf-Fro¨der 2004). The core has been dated palynologically and assigned to the LL biozone (Hartkopf-Fro¨der 2004). A slow and light maceration of the immature sediments yielded a rich and diverse plant mesofossil association. It revealed the occurrence of an unexpected diversity with many leaf types, advanced sporangial morphologies and several xylem types occurring. They all document morphologies still unknown in Upper Devonian assemblages attributed to virtually unexplored vegetations. This assemblage most probably provides a glimpse of a presumably more continental (‘upland’) flora and, by extension, a completely unconsidered set of


ecological niches (Fairon-Demaret & HartkopfFro¨der 2004). Famennian spermatophytes are characterized by extensive branching systems bearing a very large number of small seeds and very rarely presenting secondary growth (Fairon-Demaret & Scheckler 1987; Serbet & Rothwell 1992; Prestianni C. pers. comm., 2009). In the Famennian environment, seed plants were confined to low entropy values which are characterized by an early age of sexual maturity and a large net progeny set (Demetrius & Ziehe 2007). The forest builder Archaeopteris dominated the highest demographic entropy values, and consequently excluded seed plants from them. The biotic environment thus acted as a selective force that limited the outcome of higher entropy values in spermatophyte populations. As demographic entropy is linked to the age of sexual maturity and to the number of propagule produced, variations that do not modify these values are therefore allowed. Consequently, seed plant evolution within the limitations of their demographic entropy values was probably only triggered by abiotic constraints with low or no interspecific competition corresponding to n-selection (DiMichele et al. 1989). This type of selection favoured the establishment of the wide cupular and ovular morphological range of Famennian seeds as these variations only had a limited impact on demographic entropy values. In contrast, all seed plant vegetative systems correspond to the stereotypic morphologies mentioned above. The modification of these is directly linked to the age of sexual maturity and the number of propagule produced. As a consequence, instead of being an illustration of a nonselective evolution (which can be concluded from the observation of seeds only), their radiation more probably illustrates a ‘canalized’ evolution that is, one confined by other plants to restricted entropy values. If we only consider the fossil record, we can hypothesize that upper Devonian seed plants diversified in ecospaces left free by the dominating vegetation. If the hypothesis that all seed plants are opportunistic species is correct, they should be confined to disturbed environments. These environments are diverse: seashore, river margins, disturbed parts of forests and fern glades, forest margins, and so on. The morphological array of these basal spermatophytes potentially illustrates adaptations to the different types of disturbed environments as suggested by the differential morphological partitioning in the fossil record. Such a hypothesis is however difficult to test. Finally, it is notable that the largest spermatophyte diversity is recorded in Belgium (Fairon-Demaret 1996a; Prestianni 2005; Cressler 2006). The Belgian Famennian environment (Blieck et al., 2010) was characterized by a

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generally arid climate with periodic rain falls. This may provide an additional, indirect support for the opportunistic (disturbance) theory. The ‘dark and disturbed’ hypothesis (Feild et al. 2004) explains early angiosperm establishment as an adaptation to disturbed tropical understory environments. Ancestral angiosperms were, as hypothesized by Feild et al. (2004), shrubs or trees with particular adaptations to shaded conditions (f. e. leaf anatomy). It allowed angiosperms to ‘gain a root-hold in the well-established Mesozoic plant communities’ (Feild et al. 2004). The early seed plant evolution and its subsequent establishment might have occurred in a comparable way. However, we possess drastically less information about early spermatophytes than about early angiosperms. Any physiological assumptions are therefore dangerous to infer. Indeed, if we have a general idea of early seed plant morphology, very little is known about their anatomy. Moreover, all ecological information tentatively summarized here is very indirect and all biased by geological processes. Although different, the ecology of the Upper Devonian forest can nevertheless be compared with that of the Mesozoic gymnospermdominated environment. This suggests that the very early angiosperms adapted to shade disturbed understory environments might have simply repeated what their ancestors did in the Upper Devonian disturbed environments.

Conclusion The upper Devonian seed plant radiation was rapid and led to the establishment of a whole set of cupular, integumentary and ovular morphologies. These reflect the particular conditions in which early spermatophytes evolved. We here tentatively apply the concept of demographic entropy to the Famennian Archaeopteris-dominated forest. This progymnosperm occupied the highest demographic entropy values where the lowest values were occupied by populations of herbaceous plants. In that environment, seed plants and ferns were confined to middling values. This leads to the development of a canalized type of evolution with a strong biotic pressure that limited the available habitats but with only weak abiotic selective pressure inside specific niches. Seed plant thus evolved a stereotypical morphology corresponding to the biotic pressure. This monotonous plant architecture bears surprisingly variable seed types corresponding to the weak abiotic selective pressure. We suggest that this evolution occurred in disturbed environments and that it was comparable to the Cretaceous ‘dark and disturbed’ pattern of angiosperm evolution.

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We thank B. Meyer-Berthaud, S. A. Little and M. Streel for critically reviewing and improving an earlier version of the manuscript. CP holds a FRIA grant. PG is a NFRS Research Associate.

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EARLY SEED PLANT RADIATION Hilton, J. 1998a. Review of the fossil evidence for the origin and earliest evolution of the seed-plants. Acta Botanica Sinica, 40, 981– 987. Hilton, J. 1998b. Spermatophyte preovules from the basal Carboniferous of the Avon Gorge, Bristol. Palaeontology, 41, 1077–1091. Hilton, J. 2006. Cupulate seed plants from the Upper Devonian Upper Old Red Sandstone at Taffs Well, South Wales. Review of Palaeobotany and Palynology, 142, 137– 151. Hilton, J. & Edwards, D. 1996. A new Late Devonian acupulate preovule from the Taff Gorge, South Wales. Review of Palaeobotany and Palynology, 93, 235–252. Hilton, J. & Edwards, D. 1999. New data on Xenotheca devonica Arber and Goode, an enigmatic early seed plant cupule with preovules. In: Kurmann, M. H. & Hemsley, A. R. (eds) The Evolution of Plant Architecture, Royal Botanic Garden, Kew, 75–90. Howe, H. F. & Smallwood, J. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13, 201–228. Jurina, A. L. 1988. The Middle and Late Devonian floras of northern Eurasia. Transactions of the Palaeontological Institute, Moscow, 227, 176 [in Russian]. Krassilov, V. A. & Zakharova, T. V. 1995. Moresnetialike plants from the Upper Devonian of Minusinsk basin, Siberia. Paleontological Journal, 29, 35– 43. Labandeira, C. C. 2006. Plant-arthropods associations in deep time. Acta Geologica, 4, 409–438. Lepekhina, V. G., Petrosjan, N. M. & Radczenko, G. P. 1962. The most important Devonian plants of the Altay-Sayan mountain province. Vsesoyuznogo Nauchno– Issledovatel’skogo, Geologicheskogo Instituta (VSEGEI), Trudy, (Novaya Seriya), Leningrad, 70, 189. Long, A. G. 1975. Further observations on some Lower Carboniferous seeds and cupules. Transactions of the Royal Society of Edinburgh, 69, 267–293. Marshall, J. E. A. & Hemsley, A. R. 2003. A Mid Devonian seed-megaspore from East Greenland and the origin of the seed plants. Palaeontology, 46, 647–670. Marshall, J. E. A., Astin, T. R., Brown, J. F., Mark-Kurik, E. & Lazauskiene, J. 2007. Recognizing the Kaca´k Event in the Devonian terrestrial environment and its implications for understanding land–sea interactions. Geological Society, London, Special Publications, 278, 133– 155. Matten, L. C., Lacey, W. S., May, B. I. & Lucas, R. C. 1980. A megafossil flora from the Uppermost Devonian near Ballyheigue, Co. Kerry, Ireland. Review of Palaeobotany and Palynology, 29, 241–251. Matten, L. C., Tanner, W. R. & Lacey, W. S. 1984. Additions to the Silicified Upper Devonian/Lower Carboniferous flora from Balliheigue, Ireland. Review of Palaeobotany and Palynology, 43, 303–320. McGhee, G. R., Jr. 1996. The Late Devonian Mass Extinction. Columbia University Press, New York. Meyer-Berthaud, B & Decombeix, A.-L. 2008. L’e´volution des premiers arbres: les strate´gies de´voniennes. Comptes Rendus Palevol, doi: 10.1016/ j.crpv.2008.08.002.

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O’Liathaìn, M. 1992. Stratigraphic palynology of the Upper-Devonian–Lower Carboniferous succession in North Devon, Southwest England. Annales de la Socie´te´ geólogique de Belgique, 115, 649–660. Pettitt, J. M. & Beck, C. B. 1968. Archaeosperma arnoldii – A Cupulate Seed from the Upper Devonian of North America. Contributions from the Museum of Paleontology, The University of Michigan, 22, 139– 154. Pianka, E. R. 2000. Evolutionary Ecology. Harper and Collins, New York. Prestianni, C. 2005. Early diversification of seeds and seed-like structures. In: Steemans, P. & Javaux, E. (eds) Pre-Cambrian to Palaeozoı¨c Palaeopalynology and Palaeobotany, Carnets de Geólogie/Notebooks on Geology, Brest, Abstract 06. Rai, H. S., O’Brien, H. E., Reeves, P. A., Olmstead, R. G. & Graham, S. W. 2003. Inference of higherorder relationships in the cycads from a large chloroplast data set. Molecular Phylogenetics and Evolution, 29, 350 –359. Richardson, J. B. & Ahmed, S. 1988. Miospore zonation and correlation of Upper Devonian sequences from western New York State and Pennsylvania. In: McMillan, N. J., Embry, A. F. & Glass, D. J. (eds) Devonian of the World., Canadian Society of Petroleum Geologists Me´moire, 14, Calgary, 541– 558. Ridley, H. N. 1930. The Dispersal of Plants Throughout the World. L. Reeve & Co. Ltd., Ashford, Kent. Rothwell, G. W. 1986. Classifying the earliest gymnosperms. In: Spicer, R. A. & Thomas, B. A. (eds) Systematic and Taxonomic Approaches in Paleobotany. Oxford University Press, Oxford, 137– 161. Rothwell, G. W. & Scheckler, S. E. 1988. Biology of Ancestral Gymnosperms. In: Beck, C. B. (ed.) Origin and Evolution of Gymnosperms. Columbia University Press, New York, 85–134. Rothwell, G. W. & Wight, D. C. 1989. Pullaritheca longii Gen-Nov and Kerryia mattenii Gen-Nov Et Sp-Nov, Lower Carboniferous Cupules with Ovules of the Hydrasperma –Tenuis-Type. Review of Palaeobotany and Palynology, 60, 295– 309. Rothwell, G. W., Scheckler, S. E. & Gillespie, W. H. 1989. Elkinsia Gen-Nov, a Late Devonian Gymnosperm with Cupulate Ovules. Botanical Gazette, 150, 170– 189. Rowe, N. P. 1997. Late Devonian winged preovules and their implications for the adaptive radiation of early seed plants. Palaeontology, 40, 575– 595. Rydin, C., Kallersjo, M. & Friist, E. M. 2002. Seed plant relationships and the systematic position of Gnetales based on nuclear and chloroplast DNA: Conflicting data, rooting problems, and the monophyly of conifers. International Journal of Plant Sciences, 163, 197–214. Scheckler, S. E. 1986. Geology, floristics and paleoecology of Late Devonian coal swamps from appalachian Laurentia (USA). Annales de la Socie´te´ geólogique de Belgique, 109, 209–222. Scotese, C. R. 1999. Digital Paleogeographic Map Archive on CD-Rom. Paleomap Project, Arlington, TX. Serbet, R. & Rothwell, G. W. 1992. Characterizing the most primitive seed ferns .1. A Reconstruction of

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First record of Rellimia Leclercq & Bonamo (Aneurophytales) from Gondwana, with comments on the earliest lignophytes P. GERRIENNE1*, B. MEYER-BERTHAUD2, H. LARDEUX3 & S. RE´GNAULT4 1

Paleóbotanique, Universite´ de Lie`ge, B18, Sart Tilman, B-4000 LIEGE, Belgium 2

Universite´ Montpellier 2, UMR AMAP, Montpellier, F-34000 France

3

Laboratoire de Geólogie, IRFA-UCO, B.P. 808, F-49008 Angers cedex 1, France 4

Museum d’Histoire Naturelle, Rue Voltaire, 12, F-44000 Nantes, France *Corresponding author (e-mail: [email protected])

Abstract: The lignophytes (Embryophytes that possess a bifacial cambium) evolved during the Devonian period and include seed plants. Their advent was a major event in the history of life and had a profound impact on terrestrial environments. Recent reinvestigations of a Devonian locality, Dechra Aı¨t Abdallah in Central Morocco, led to the discovery of a rich assemblage of fossil plants and Tentaculita. This paper focuses on a single specimen of the lignophyte Rellimia Leclercq & Bonamo. Rellimia (Aneurophytales) is a monospecific genus reported from a large number of Middle Devonian localities from western Europe (Belgium, Czech Republic, Germany and Scotland) and America. Its fertile organs are highly distinctive and borne helically on branches. They consist of a basal stalk that dichotomizes once near the base, the resulting branches dividing pinnately and bearing elongated sporangia terminally on ultimate divisions. According to the late Emsian age indicated by our sample of Tentaculita, this Moroccan specimen is to date the earliest representative of both the genus and the lignophytes. If confirmed, this occurrence suggests a possible origin of the Aneurophytalean lignophytes in Gondwana and their rapid and widespread colonization in the Middle Devonian towards Laurussia.

The lignophytes are the plants that possess a bifacial vascular cambium, producing secondary phloem (inner bark) towards the outside and secondary xylem (wood) towards the inside. Thanks to this innovation, lignophytes have the ability to achieve the largest and most complex woody bodies in the plant kingdom. The advent of the lignophytes is therefore a major event in the history of life. It occurred in the Devonian period and had a profound impact on terrestrial environments. The evolution of the tree habit in the lignophytes allowed those plants to reach greater heights with an increased mechanical stability and greater efficiency of propagule dispersion and light interception. It was also accompanied by the acquisition of long-lived roots (Meyer-Berthaud & Decombeix 2007; MeyerBerthaud et al. 2010) which had major implications on the elaboration of early soils and complex microbial communities (Algeo et al. 2001). The earliest remains of lignophytes are included in the Aneurophytales (Middle to Upper Devonian) and possibly in the Stenokoleales (Middle Devonian to Lower Carboniferous; Beck & Stein 1993). Members of both orders were medium-sized plants or shrubs. The earliest arborescent representatives of the lignophytes belong to the Archaeopteridales, an order reported from the late Middle Devonian to the earliest Carboniferous. Archaeaopteris was a

large tree with webbed leaves; it was heterosporous, but did not produce seeds. Archaeaopteris experienced an extraordinary success during the Late Devonian, dominating the forest ecosystems and having a cosmopolitan distribution (Edwards et al. 2000). According to most of the current palaeogeographical reconstructions (Scotese 2003; Cocks & Torsvik 2006), north Africa had a very central position within the emerged land masses during most of the Palaeozoic. Renewed interest in Devonian palaeobotany in north Africa has resulted in the discovery of new localities with interesting fossil contents in Morocco from Lower Devonian (FaironDemaret & Re´gnault 1986; Gerrienne et al. 1999; Meyer-Berthaud & Gerrienne 2001) and from Upper Devonian (Meyer-Berthaud et al. 2000, 2004; Soria et al. 2001; Soria & Meyer-Berthaud 2005) localities. These publications highlight the occurrence, in these localities, of plant assemblages possessing a significant number of genera in common with those of eastern Laurussia. The Devonian plant assemblage consisting of compressions from the marine sequence of limestone beds at Dechra Aı¨t Abdallah (central Morocco; Fig. 1) was first reported by Termier & Termier (1950) who emphasized its abundance and diversity. They assigned it to the Eifelian on the basis of associated Tentaculita and Phacopidae.


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Fig. 1. Location of Dechra Aı¨t Abdallah, the fossiliferous locality in Morocco.

They identified seven taxa: Asteroxylon elberfeldense Krau¨sel & Weyland, Psilophyton princeps Dawson, Hyenia cf. elegans Krau¨sel & Weyland, Aneurophyton maroccanum nov. sp., Scougouphyton abdallahense nov. gen. nov. sp., Cordaianthus devonicus Dawson, ‘Archaeopteris’ rotundifolia nov. sp. and incertae sedis specimens. Several authors do not recognize A. maroccanum as a valid species of Aneurophyton (Schweitzer & Matten 1982; Fairon-Demaret & Re´gnault 1986). The recognition of Cordaianthus in Devonian beds is problematic and that of Archaeopteris foliage in supposedly Eifelian deposits is suspicious. The diversity of this assemblage and the obvious need for its taxonomic revision encouraged us to revisit the locality during a field trip organized in 2000 where we collected a various assemblage of fossil plants together with some new Tentaculita. Despite the report of supposedly fertile specimens by Termier & Termier (1950), we found that such remains were very rare at Dechra Aı¨t Abdallah. This fact seriously limited the accurate taxonomic identification of the specimens. The present paper focuses on the coalified compression of a fertile plant showing the distinctive features of the aneurophytalean progymnosperm Rellimia (Leclercq & Bonamo 1973). The occurrence at the locality of this specimen had already been signalled (Gerrienne et al. 2002), but had not been illustrated. Its report in north Africa is a contribution to the elaboration of a more complete Devonian plant database than those currently available today. The bearing of the occurrence of Rellimia to Devonian phytogeography is discussed.

Locality and stratigraphy The Dechra Aı¨t Abdallah plant beds are situated in Central Morocco (Fig. 1), about 40 km SW of

Azrou and 10 km NW of M’rirt. The locality is described in Termier & Termier (1950). It consists of a 30 m thick section of marine grey-to-dark laminated limestones. Several plant beds have been discovered (work in progress at Montpellier), but the specimen described here was collected from a loose block found near the base of the section. Several Tentaculita specimens have been collected from seven successive layers. They belong to the genera Styliolina Karpinsky (Styliolinida) and Viriatellina Boucˇek (Nowakiida). Most of them are too badly preserved for any firm specific attribution. Nevertheless, some specimens from a level at the very base of the section, below the Rellimia level, could be identified as Viriatellina pseudogeinitziana armoricana Lardeux, a subspecies of V. pseudogeinitziana (Boucˇek 1964) that indicates a late Emsian age (late Lower Devonian; Lardeux 1969). This is consistent with the discovery, close to Rellimia and within a lower horizon of the section, of a trilobite assignable to Struveaspis maroccanum, a species ranging from the late Emsian to the early Eifelian (R. Feist, pers. comm., 2008). All attempts to recover identifiable spores from the sediments were unsuccessful.

Methods Only one specimen was collected; the counterpart is missing. The plant fossil was studied using standard palaeobotanical methods for compressions, mainly de´gagement (Fairon-Demaret et al. 1999). The specimen was then embedded and macerated in hydrofluoric acid (transfer technique of Banks et al. 1972) in order to obtain information on anatomy and spores. This attempt was unsuccessful, but allowed a better image of the fertile part of the specimen (Fig. 2b). The specimen was photographed using a Nikon D70 camera with a polarized light source. The contrast between plant and matrix was enhanced by wetting the specimen with distilled water.

Description and identification of the specimen The specimen consists of a 6.5 cm long portion of a main axis bearing at least three lateral fertile organs in spiral order (Fig. 2a, A – C). Both ends of the main axis are missing, but the size and conicity of the specimen suggest that it may correspond to a distal portion. The main axis is about 2.5 mm wide proximally and tapers to a diameter of 1.5 mm distally. Intervals separating the three fertile organs labelled A –C average 1 cm in length. The fertile organs are about 2 cm long and are adaxially recurved towards the main axis. They comprise

THE LIGNOPHYTE RELLIMIA FROM GONDWANA

83

Fig. 2. Specimen n8 DAA 123. Rellimia sp. (a) Gross view of the specimen; fertile organs are labelled A to C; scale bar: 1 cm. (b) One fertile organ (after transfer); note the elongate slender sporangia; one single sporangium is indicated by the arrow; scale bar: 1 mm. (c) Fertile organ A of Figure 2a, enlarged; A1 and A2 are the two halves of the fertile organ; the two first order axes (arrows) are visible; scale bar: 5 mm.

an axis that branches once proximally into two first-order axes. Such a dichotomy is observed in the face view for the most proximal fertile organ (Fig. 2a, A; Fig. 2c, A1 & A2). Each first-order axis bears second- and third-order axes in a pinnate (i.e. lateral) alternate arrangement (Fig. 2b; a

schematic reconstruction of a fertile organ is proposed in Fig. 3). Masses of sporangia (Fig. 2b) are borne on the ultimate divisions. Sporangia are elongate and slender and possess an acute apex (Fig. 2b, arrow). They are up to 6.0 mm long and 0.3 –0.4 mm wide. The specimen is poorly

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Fig. 3. Schematic reconstruction of a fertile organ of Rellimia.

preserved: information on vegetative appendages is lacking, and no anatomical data could be obtained. The fertile organs of the Moroccan specimen have typical aneurophytalean morphology in being recurved adaxially. They demonstrate a complex branching system comprising one level of dichotomy proximally and pinnate branching distally (Fig. 3). On the basis of its spirally inserted, profusely branched lateral fertile appendages, terminated in narrow axes bearing dense masses of slender elongate sporangia, this specimen is assigned to the genus Rellimia Leclercq & Bonamo 1973. This genus includes the single species R. thomsonii (Dawson) Leclercq & Bonamo (1973), but the Moroccan specimen is not well preserved enough to be unequivocally assigned to that species. Possible differences are the number of pinnate orders of branches and the size of individual sporangia that seems larger in the specimen described here (Table 1). The Moroccan specimen will therefore be referred to as Rellimia sp.

Comparison with other Aneurophytales The morphology of aneurophytalean fertile organs is highly distinctive, but shows a range of variation. Fertile organs in the Moroccan specimen are much larger and more complex than those of Aneurophyton Kraüsel & Weyland (Serlin & Banks 1975; Schweitzer & Matten 1982). They also differ from

those of Triloboxylon Matten & Banks emend. Scheckler & Banks (1971a) in having two pinnate orders of branches and in being inserted distally. Moreover, fertile organs in Triloboxylon show two proximal dichotomies and sporangia are both shorter and wider than those of the Moroccan specimen (Table 1). Fertile organs in the latter compare better to those of the genera Tetraxylopteris Beck emend. Hammond & Berry (2005) (Table 1). However, branching in Tetraxylopteris is not helical but typically opposite and decussate, a pattern recognizable in both the vegetative and fertile parts of this genus (Bonamo & Banks 1967; Hammond & Berry 2005). A second difference in the Moroccan specimen is that the proximal axis of the fertile organ in Tetraxylopteris dichotomizes twice rather than once, as in Triloboxylon. Middle Devonian sediments of Imouzzerdu-Kandar, a close locality from Central Morocco (70 km NE of Dechra Aı¨t Abdallah), yielded partially permineralized branch systems of aneurophytalean type (Fairon-Demaret & Re´gnault 1986). According to these authors, distinctive aneurophytalean characteristics were the branching pattern, the vascular architecture of the three-lobed stele and the presence of thickened cortical cells. Due to the lack of fertile remains, no generic designation was assigned to this material. However, it is interesting to note here that the resemblance of one specimen with Rellimia was discussed (Fairon-Demaret & Re´gnault 1986, plate 3).

Discussion The earliest representative of the lignophytes? The lignophyte clade includes the Euphyllophytes (Fig. 4) that have the ability to produce secondary phloem and xylem due to the presence of a lateral meristem called vascular cambium. In current phylogenies, the lignophytes encompass the paraphyletic progymnosperms (Aneurophytales, Archaeopteridales and Protopityales, not represented in Fig. 4) and the monophyletic spermatophytes (Crane 1985). The earliest lignophytes belong to the Aneurophytales and, possibly, to the Stenokoleales. The plants included in the Stenokoleales Beck & Stein are distributed within the two genera Stenokoleos Hoskins & Cross and Crossia Beck & Stein. Those plants are known exclusively from permineralizations and range from Middle Devonian to Lower Carboniferous (Beck & Stein 1993). The Stenokoleales have mostly been described from US localities; an occurrence of Crossia at Ronquie`res (mid-Givetian, Belgium; Gerrienne et al. 2004) is currently under investigation at Liege University. Those plants are characterized by a three-ribbed

Table 1. Compared characters of fertile organs in the Aneurophytales (Aneurophyton excluded) Taxon

Tetraxylopteris schmidtii

Tetraxylopteris reposana

Triloboxylon ashlandicum

Bonamo & Banks 1967

Hammond & Berry 2005

Scheckler 1975

Position of fertile organs on main axis Arrangement of fertile organs on main axis (organotaxy) Length of fertile organs (cm) Number of proximal dichotomies Number of pinnate orders of branches Sporangial attachment

Distal

Distal

Opposite decussate

Opposite decussate

Between vegetative regions Helical

.2

2

2

Moroccan specimen

Leclercq & Bonamo 1971; Bonamo 1977 Distal

This paper

Helical

Helical

1.5 – 2.0

1–4

2

2

2

1

1

3

3 –4

1 (sporangial stalks)

3–4

2

Singly

Singly

Singly or in pairs

Size of sporangia (mm)

2–5 long, 0.4 –0.8 wide

Shape of sporangia

Oblong-oval, acute apex

2 – 3.5 long, 0.5– 0.8 wide elongate, apex apiculate

Dehiscence unknown

Longitudinal dark line; dehiscence line opposite Rhabdosporites langii

0.9– 2.6 long, 0.2– 0.6 wide Elongate, acute to slightly rounded apex Longitudinal dark line; possibly dehiscence –

In pairs; also singly or in 3-4 Average 3.5 long, 0.5 wide Elongate, acute apex

Spores

Longitudinal dark line; dehiscence longitudinal –

Longitudinal dark line; possibly dehiscence Rhabdosporites langii

Probably distal

– Up to 6 long, 0.3– 0.4 wide Elongate, acute apex


References

Rellimia thomsonii

– –

85

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P. GERRIENNE ET AL.

Fig. 4. Schematic phylogenetic position of the Aneurophytales and the Lignophytes in the Eutracheophytes.

protostele, numerous protoxylem strands including a central one and others arranged along the midplanes of the arms of the protostele, pairs of traces to lateral appendages and a helical phyllotaxis of those pairs of appendages. Secondary xylem is sometimes present in small amounts (Matten 1992; Beck & Stein 1993), but has not yet been described in detail. In the absence of morphological data, especially on reproductive parts, the Stenokoleales are currently left as incertae sedis. They are not represented in Figure 4. The Aneurophytales Kraüsel & Weyland includes seven genera (Table 2) known from adpressions and/or permineralizations. Before this work, their occurrences ranged from the late Eifelian to the Frasnian (Table 1). Members of the order are characterized by three-dimensional branching systems with lateral dichotomous appendages in helical or decussate arrangement. The primary vascular system consists of a deeply lobed mesarch protostele, with a central protoxylem strand and others occurring along the mid-planes of the lobes and near their tip. The sporangia are borne on ultimate divisions of the much-branched lateral fertile appendages. Aneurophytales are homosporous. Their

phylogenetic position is currently under debate but, on the basis of their homosporous status, they are often considered as sister to a group including the heterosporous Archaeopteridales and the spermatophytes (Fig. 4). Rellimia is one of the oldest known Aneurophytales. This monospecific genus has been reported from a number of Middle Devonian localities in Western Europe (Scotland, Belgium, Germany and Czech Republic) and north America (Table 2). Rellimia sp. was briefly reported in Venezuela by Berry et al. (2000), but the specimens are probably those recently described as Tetraxylopteris reposana (Hammond & Berry 2005). The Rellimia specimen described here consequently represents the first occurrence of the genus in Gondwana. In our current state of knowledge, it documents the earliest occurrence of both the genus Rellimia and the order Aneurophytales, and also represents the earliest lignophyte occurrence.

Palaeogeographical implications The spore taxon Rhabdosporites langii (Eisenack) Richardson has been found in the sporangia of

Table 2. Main occurrences of Aneurophytales Genus Aneurophyton

Species germanicum

Selected references Kraüsel & Weyland (1923, 1926, 1929, 1938) Serlin & Banks (1975)

cf. germanicum sp.

Leclercq (1940)

cf. Aneurophyton Cairoa

lamanekii

Berry & Fairon-Demaret (2001) Iurina (1988) Iurina (1988) Matten (1973)

Proteokalon

petryi

Reimannia

aldenense

Rellimia

thomsonii sp.

Scheckler & Banks (1971b) Arnold (1935) Stein (1982) Dawson (1871, 1878) Krejci (1880) Stockmans (1968) Leclercq & Bonamo (1971) Schweitzer (1974) Mustafa (1975) Bonamo (1977)

Country

Age (based on)

Position on Figure 5

Mostly adpressions

Germany

Possibly Late Eifelian/ Early Givetian

1

Adpressions/ permineralizations Adpressions/ permineralizations – Adpressions

USA

2

Adpressions/ permineralizations Adpressions/ permineralizations

Belgium

Frasnian (field relations) Possibly Late Eifelian/ Early Givetian Possibly Givetian Late Famennian (field relations) Late Givetian (spores)

Belgium

Latest Eifelian (spores)

4

– – Permineralizations

Siberia Ukrainia USA

5 6 2

Permineralizations

USA

Permineralizations

USA

Possibly Givetian Possibly Late Givetian Givetian (field relations) Early Frasnian (field relations) Givetian (invertebrates)

Adpressions

Scotland

Adpressions Adpressions Adpressions

Czech Republic Belgium Belgium

Adpressions Adpressions/ permineralizations Adpressions/ permineralizations

Germany Germany

Germany Russia Belgium

USA

Possibly Middle Devonian Possibly Early Givetian Givetian (spores) Latest Eifeilian (spores) Middle Eifelian (spores) Late Eifelian (field relations) Late Eifelian/early Givetian (spores)

1 3 4

2 2 7 8 4 4


olnense

Schweitzer & Matten (1982) Iurina (1988) Stockmans (1948)

Conservation

1 1 2

87

(Continued)

88

Table 2. Continued Genus

schmidtii

Selected references Dannenhoffer & Bonamo (1989, 2003) Dannenhoffer et al. (2007) Lessuise & Fairon-Demaret (1980) Schweitzer & Matten (1982) Iurina (1988) Iurina (1988) This work Beck (1957) Bonamo & Banks (1967) Scheckler & Banks (1971b) Mustafa (1975)

Triloboxylon

Indetermined

Conservation

Country

Age (based on)

Position on Figure 5

Adpressions

Belgium

Givetian (spores)

4

Adpressions/ permineralizations – – Adpressions Adpressions/ permineralizations Adpressions/ permineralizations Mostly permineralizations Permineralizations

Germany

Possibly Late Eifelian/ early Givetian Possibly Givetian Possibly Givetian Late Emsian Upper Devonian (field relations) Early Frasnian (field relations) Early Frasnian (field relations) Late Eifelian (field relations) Possibly Early Frasnian (field relations; spores) Givetian (field relations)

1

Russia Siberia Morocco USA USA USA Germany

reposana

Hammond & Berry (2005)

Adpressions

Venezuela

arnoldii

Matten (1974)

Permineralizations

USA

ashlandicum

Stein & Beck (1983) Matten & Banks (1966)

Permineralizations

USA

Early Frasnian (field relations)

Scheckler & Banks (1971a) Scheckler (1975) Fairon-Demaret & Re´gnault (1986)

Adpressions/ permineralizations

Morocco

Givetian (faunas)

9 5 10 2 2 2 1 11 2 2

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Tetraxylopteris

Species


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Fig. 5. Distribution of main occurrences of Lignophytes. Palaeogeographical reconstruction for the Middle Devonian redrawn from Scotese (2003). 1, Germany (Late Eifelian to early Givetian: Kraüsel & Weyland 1923, 1926, 1929, 1932, 1938; Mustafa 1975; Schweitzer & Matten 1982). 2, New York, USA (Late Eifelian to Frasnian: Bonamo 1977; Dannenhoffer & Bonamo 1989, 2003; Dannenhoffer et al. 2007). 3, Russia (possibly Givetian: Iurina 1988). 4, Belgium (Latest Eifelian to Givetian: Stockmans 1968; Leclercq & Bonamo 1971; Lessuise & Fairon-Demaret 1980). 5, Siberia (possibly Givetian: Iurina 1988). 6, Ukrainia (possibly Late Givetian: Iurina 1988). 7, Scotland (Middle Devonian: Dawson 1871, 1878; Lang 1926). 8, Czech Republic (Early Givetian: Krejci 1880; Kraüsel & Weyland 1933). 9, Russia (possibly Givetian: Iurina 1988). 10, Morocco (possibly Late Emsian). 11, Venezuela (possibly Late Givetian/Early Frasnian: Hammond & Berry 2005).

Rellimia thomsonii (Leclercq & Bonamo 1971) and Tetraxylopteris schmidtii (Bonamo & Banks, 1967). Until now, the species has not been discovered in situ in any other plant. Rhabdosporites langii is known from localities distributed worldwide and, in Gondwana, it has been identified in Middle/ early Late Devonian strata from Algeria, Iran, Libya, Morocco, Tunisia and Saudi Arabia (P. Breuer, pers. comm., 2008). Those various occurrences suggest that Aneurophytales were probably widespread on the Gondwana even although macrofossil evidence is poor. Accumulating evidence suggests that Gondwana might be seen as ‘the place where everything started’, at least from the botanical point of view. The earliest known cryptospores are described from Saudi Arabia (northern Gondwana; Lower Middle Ordovician; Strother et al. 1996). The earliest unequivocal terrestrial plant sporangia come from Oman (northern Gondwana) and are considered to be Late Ordovician in age (Wellman et al. 2003). The earliest occurrence of trilete spores is around the Caradoc/Ashgill boundary in Saudi Arabia (Steemans et al. 2009). As a result, Gondwana is today generally considered as the probable centre of origin of land plants (during the Ordovician) (Steemans et al. 2010). On the basis of the early Rellimia occurrence described here, and of the numerous occurrences of Rhabdosporites langii, it is possible that northern Gondwana was the centre of origin of the lignophytes during the end of the Lower Devonian.

The palaeogeographical distribution of the Aneurophytales is restricted to the eastern part of Laurussia and to NW Gondwana; their absence in China and neighbouring areas is noteworthy (Table 2; Fig. 5). The presence of Aneurophytales on both sides of the Rheic ocean suggests that the latter was not large enough during Lower/Middle Devonian times to prevent plant exchanges between Laurussia and Gondwana. Among the palaeogeographical hypotheses proposed for that period, these results are best explained by the reconstructions developed by Scotese & McKerrow (1990) and within Scotese’s PalaeoMap project (http://www.scotese.com/). Localities yielding Aneurophytales have a wide palaeolatitudinal distribution (Fig. 5). This suggests either that those plants could have wide ecological tolerances or that the palaeoclimatic conditions were rather uniform or at least favourable during the Middle Devonian. This is consistent with the period of global warming episode (Hot House conditions) proposed by Scotese et al. (1999) for the first part of the Devonian. It could also mean that the Laurussia constituents (Laurentia and Baltica) and Gondwana were grouped closer to the equator than suggested by current palaeogeographical reconstructions. We thank the Ministe`re de l’Energie et des Mines (Rabat, Morocco) for the issue of a working permit, permission to export samples and logistical advice. We also thank Mr M. Mohammed for permission to collect fossils at his

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property at Dechra Aı¨t Abdallah. This work is supported by the Eclipse II project ‘The terrestrialization process’ and the ANR project ‘AccroEarth’. P. Gerrienne is a FRS-FNRS research Associate. AMAP (Botany and Computational Plant Architecture) is a joint research unit with associates CIRAD (UMR51), CNRS (UMR5120), INRA (UMR931), IRD (R123) and Montpellier 2 University (UM27) (http://amap.cirad.fr/).

References Algeo, T. J., Scheckler, S. E. & Maynard, J. B. 2001. Effects of the Middle to Late Devonian spread of vascular land plants on weathering regimes, marine biotas and global climate. In: Gensel, P. G. & Edwards, D. (eds) Plants Invade the Land. Evolutionary & Environmental Perspectives. Columbia University Press, New York, 213– 236. Arnold, C. A. 1935. Some new forms and new occurrences of fossil plants from the Middle and Upper Devonian of New York State. Bulletin of the Buffalo Society of Natural Sciences, 17, 1 –12. 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, 19– 40. Beck, C. B. 1957. Tetraxylopteris schmidtii gen. et sp. nov., a probable pteridosperm precursor from the Devonian of New York. American Journal of Botany, 44, 350–367. 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 B, 229, 115– 134. Berry, C. M. & Fairon-Demaret, M. 2001. The Middle Devonian flora revisited. In: Gensel, P. G. & Edwards, D. (eds) Plants Invade the Land: Evolutionary and Environmental Perspectives. Columbia University Press, New York, 120 –139. Berry, C. M., Morel, E., Mojica, J. & Villarroel, C. 2000. Devonian plants from Colombia, with discussion of their geological and palaeogeographical context. Geological Magazine, 137, 257–268. Bonamo, P. M. 1977. Rellimia thomsonii (Progymnospermopsida) from the Middle Devonian of New York State. American Journal of Botany, 64, 1272–1285. Bonamo, P. M. & Banks, H. P. 1967. Tetraxylopteris schmidti: its fertile parts and its relationships within the Aneurophytales. American Journal of Botany, 54, 755– 768. Boucˇek, B. 1964. The Tentaculites of Bohemia. Publishing House of the Czechoslovak Academy of Science, Prague. Cocks, L. R. M. & Torsvik, T. H. 2006. European geography in a global context from the Vendian to the end of the Palaeozoic. In: Gee, D. G. & Stephenson, R. A. (eds) European Lithosphere Dynamics. Geological Society, London, Memoirs, 32, 83– 95. Crane, P. R. 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanical Garden, 72, 716–793.

Dannenhoffer, J. M. & Bonamo, P. M. 1989. Rellimia thomsonii from the Givetian of New York: secondary growth in three orders of branching. American Journal of Botany, 76, 1312– 1325. Dannenhoffer, J. M. & Bonamo, P. M. 2003. The wood of Rellimia from the Givetian of New York. International Journal of Plant Sciences, 164, 429–441. Dannenhoffer, J. M., Stein, W. E. & Bonamo, P. M. 2007. The primary body of Rellimia thomsonii: integrated perspective based on organically connected specimens. International Journal of Plant Sciences, 168, 491 –506. Dawson, J. W. 1871. On new tree ferns and other fossils from the Devonian. Quarterly Journal of the Geological Society, London, 27, 269– 275. Dawson, J. W. 1878. Notes on some Scottish Devonian plants. Canadian Naturalist and Quarterly Journal of Science, 8, 379–389. Edwards, D., Fairon-Demaret, M. & Berry, C. M. 2000. Plant megafossils in Devonian stratigraphy: a progress report. Courier Forschungsinstitut Senckenberg, 220, 25–38. Fairon-Demaret, M. & Re´gnault, S. 1986. Macroflores de´voniennes dans le Nord du Maroc (Boutonnie`re d’Imouzzer-du-Kandar, Sud de Fe`s). Etude paleóbotanique – Implications stratigraphiques et paleógeógraphiques. Annales de la Socie´te´ Geólogique de Belgique, 109, 499–513. Fairon-Demaret, M., Hilton, J. & Berry, C. M. 1999. Surface preparation of macrofossils (de´gagement). In: Jones, T. P. & Rowe, N. P. (eds) Fossil plants and spores. Modern Techniques. The Geological Society, London, 33– 35. Gerrienne, P., Fairon-Demaret, M., Galtier, J., Lardeux, H., Meyer-Berthaud, B., Re´gnault, S. & Steemans, P. 1999. A Plant-Tentaculites association in a new Early Devonian locality from Morocco. Abhandlungen Geologischen Bundesanstalt Austria, 54, 323 –335. Gerrienne, P., Meyer-Berthaud, B., Moreno Sanchez, M. & Re´gnault, S. 2002. Dećouverte du genre Rellimia Leclercq & Bonamo (Aneurophytales) en Afrique: un apport a` la paleógeógraphie du De´vonien Moyen. Organisation Francophone de Paleóbotanique Informations, 27, 11–12. Gerrienne, P., Meyer-Berthaud, B., FaironDemaret, M., Streel, M. & Steemans, P. 2004. Runcaria, a Middle Devonian Seed Plant Precursor. Science, 306, 856– 858. Hammond, S. E. & Berry, C. M. 2005. A new species of Tetraxylopteris (Aneurophytales) from the Devonian of Venezuela. Botanical Journal of the Linnean Society, 148, 275–303. Iurina, A. L. 1988. Flore du De´vonien Moyen et Supe´rieur en Eurasie du Nord. Academia U.R.S.S., 227, 1– 176. Kraüsel, R. & Weyland, H. 1923. Beitra¨ge zur Kenntnis der Devonflora. Senckenbergiana Lethaea, 5, 154–184. Kraüsel, R. & Weyland, H. 1926. Beitra¨ge zur Kenntnis der Devonflora II. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, 40, 115– 155. Kraüsel, R. & Weyland, H. 1929. Beitra¨ge zur Kenntnis der Devonflora III. Abhandlungen der

THE LIGNOPHYTE RELLIMIA FROM GONDWANA Senckenbergischen Naturforschenden Gesellschaft, 41, 317–359. Kraüsel, R. & Weyland, H. 1932. Pflanzenreste aus dem Devon II. Senckenbergiana Lethaea, 14, 185–190. Kraüsel, R. & Weyland, H. 1933. Die Flora des Bo¨hmischen Mitteldevons. Palaeontographica B, 78, 1–46. Kraüsel, R. & Weyland, H. 1938. Neue Pflanzenfunde im Mitteldevon von Elberfeld. Palaeontographica B, 83, 172–195. Krejci, J. 1880. Notiz u¨ber die Reste von Landpflanzen in der Bo¨hmischen Silurformation. Sitzungsberichte der ko¨niglichen bo¨hmischen Gesellschaft der Wissenschaften Prague, 1879, 201– 204. Lang, W. H. 1926. Contributions to the study of the Old Red Sandstone flora of Scotland. III. On Hostimella (Ptilophyton) thomsoni, and its inclusion in the new genus Milleria. Transactions of the Royal Society of Edinburgh, 54, 253–272. Lardeux, H. 1969. Les Tentaculites d’Europe occidentale et d’Afrique du Nord. Cahiers de Paleóntologie, Edition du Centre National de la Recherche Scientifique, Paris. Leclercq, S. 1940. Contribution a` l’e´tude de la flore du De´vonien de Belgique. Acade´mie Royale de Belgique, Me´moire in 48, 12, 3 –65. Leclercq, S. & Bonamo, P. M. 1971. A study of the fructification of Milleria (Protoperidium) thomsonii Lang from the Middle Devonian of Belgium. Palaeontographica B, 136, 83– 144. Leclercq, S. & Bonamo, P. M. 1973. Rellimia thomsonii, a new name for Milleria (Protopteridium) thomsonii Lang 1926 emend. Leclercq & Bonamo 1971. Taxon, 22, 435–437. Lessuise, A. & Fairon-Demaret, M. 1980. Le gisement a` plantes de Niaster (Aywaille, Belgique): repe`re stratigraphique nouveau aux abords de la limite Couvinien-Givetien. Annales de la Socie´te´ Geólogique de Belgique, 103, 157– 181. Matten, L. C. 1973. The Cairo flora (Givetian) from eastern New York. I. Reimania terete axes, and Cairoa lamanekii gen. et sp. nov. American Journal of Botany, 60, 619– 630. Matten, L. C. 1974. The Givetian flora from Cairo, New York: Rhacophyton, Triloboxylon and Cladoxylon. Botanical Journal of the Linnean Society, 68, 303–318. Matten, L. C. 1992. Studies on Devonian plants from New York State: Stenokoleos holmesii n. sp. from the Cairo flora (Givetian) with an alternative model for lyginopterid seed fern evolution. Courier Forschungsinstitut Senckenberg, 147, 75–85. Matten, L. C. & Banks, H. P. 1966. Triloboxylon ashlandicum gen. et sp. n. from the Upper Devonian of New York. American Journal of Botany, 53, 1020–1028. Meyer-Berthaud, B. & Gerrienne, P. 2001. Aarabia, a new Early Devonian vascular plant from Africa (Morocco). Review of Palaeobotany and Palynology, 116, 39–53. Meyer-Berthaud, B. & Decombeix, A.-L. 2007. A tree without leaves. Nature, 446, 861– 862. Meyer-Berthaud, B., Scheckler, S. E. & Bousquet, J. 2000. The development of Archaeopteris: new

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evolutionary characters from the structural analysis of an early Famennian trunk from Southeast Morocco. American Journal of Botany, 87, 456– 468. Meyer-Berthaud, B., Ru¨cklin, M., Soria, A., Belka, Z. & Lardeux, H. 2004. Frasnian plants from the Dra Valley, southern Anti-Atlas, Morocco. Geological Magazine, 141, 675–686. 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., Cle´ment, G. & Meyer-Berthaud, B. (eds) The Terrestrialization Process: Modelling Complex Interactions at the Biosphere–Geosphere Interface. Geological Society, London, Special publications, 339, 59–70. Mustafa, H. 1975. Beitra¨ge zur Devonflora I. Argumenta Palaeobotanica, 4, 101–133. Scheckler, S. E. 1975. A fertile axis of Triloboxylon ashlandicum, a progymnosperm from the Upper Devonian of New York. American Journal of Botany, 62, 923– 934. Scheckler, S. E. & Banks, H. P. 1971a. Anatomy and relationships of some Devonian progymnosperms of New York. American Journal of Botany, 58, 737– 751. Scheckler, S. E. & Banks, H. P. 1971b. Proteokalon, a new genus of progymnosperms from the Devonian of New York State and its bearing on phylogenetic trends in the group. American Journal of Botany, 58, 874– 884. Schweitzer, H.-J. 1974. Zur mitteldevonnischen Flora von Lindlar (Rheinland). Bonner Palaöbotanische Mitteilungen, 1, 1 –9. Schweitzer, H.-J. & Matten, L. C. 1982. Aneurophyton germanicum and Protopteridium thomsonii from the Middle Devonian of Germany. Palaeontographica B, 184, 65–106. Scotese, C. R. 2003. Paleomap Project. World Wide Web Address: http://www.scotese.com/mdevclim.htm. Scotese, C. R. & McKerrow, W. S. 1990. Revised world maps and introduction. In: McKerrow, W. S. & Scotese, C. R. (eds) Palaeozoic Palaeogeography and Biogeography. Geological Society, London, Memoirs, 12, 1–21. Scotese, C. R., Boucot, A. J. & McKerrow, W. S. 1999. Gondwanan palaeogeography and palaeoclimatology. Journal of African Earth Sciences, 28, 99–114. Serlin, B. S. & Banks, H. P. 1975. Morphology and anatomy of Aneurophyton, a progymnosperm from the Late Devonian of New York. Palaeontographica Americana, 8, 343– 359. Soria, A. & Meyer-Berthaud, B. 2005. Reconstructing the Late Devonian cladoxylopsid Pietzschia schulleri from new specimens from southeastern Morocco. International Journal of Plant Sciences, 166, 857– 874. 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 south-eastern Morocco. International Journal of Plant Sciences, 162, 911– 926.

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The sedimentary environment of the Late Devonian East Greenland tetrapods T. R. ASTIN1, J. E. A. MARSHALL2*, H. BLOM3 & C. M. BERRY4 1

School of Human and Environmental Science, The University of Reading, Whiteknights, PO Box 217, Reading, RG6 6AH, UK 2

School of Ocean and Earth Science, National Oceanography Centre, University of Southampton, European Way, Southampton, SO14 3ZH, UK

3

Evolutionary Organismal Biology, Department of Physiology and Developmental Biology, Norbyva¨gen 18A, SE-752 36 Uppsala, Sweden 4

School of Earth and Ocean Sciences, Cardiff University, Main Building, Park Place, Cardiff CF10 3YE, Wales *Corresponding author (e-mail: [email protected]) Abstract: The Late Devonian early tetrapods in East Greenland occur in the Celsius Bjerg Group. Key occurrences are located in a detailed stratigraphic section used here to interpret the sedimentary palaeoenvironments. The palaeoenvironment for the Britta Dal Formation (which contains both Ichthyostega and Acanthostega) is reinterpreted. The Britta Dal Formation channels have flat bases, are poorly channelized, are of low sinuosity and are part of a very major distributory system that periodically experienced extreme flooding. The tetrapod fossils were recovered from an ephemeral system that was not permanently habitable in the immediate area. Plant megafossils are poorly preserved casts and impressions dominated by lycopsids and fern-like plants. The overbank siltstones are dominated by arid soil forming processes and comprise a spectacular sequence of vertisols. The 1174 m in situ Ichthyostega locality in Paralleldal was relocated and occurs just below the midpoint of the second megacycle in the Britta Dal Formation.

The Late Devonian Celsius Bjerg Group of East Greenland is internationally famous for the tetrapods Ichthyostega and Acanthostega. Although these are no longer the earliest known tetrapods, they still remain the best understood and the evolutionary benchmark against which the older discoveries are compared (Clack 2006; Ahlberg et al. 2008). Importantly, the East Greenland tetrapods are known from over 500 specimens (Blom et al. 2005) throughout a long stratigraphic section. An earlier contribution (Marshall et al. 1999) clarified the age of these tetrapods which had been controversial (Westoll 1941; Jarvik 1948; Hartz et al. 1997; Stemmerik & Bendix-Almgreen 1998) ever since their original discovery. This contribution provides an integrated account of the range of sedimentary environments present throughout the Celsius Bjerg Group. Importantly, it significantly revises the published environmental interpretation (Bendix-Almgreen et al. 1988) for the habitat of Acanthostega.

Geological setting and methods The general stratigraphy and tetrapod field localities are well described in a number of recent

publications. Those of Olsen (1993) and Olsen & Larsen (1993) documented the sedimentary environments and their stratigraphy and spatial distribution within the basin. Subsequently Larsen et al. (2008) reviewed, updated and integrated their original publications with an account of the vertebrate assemblages. In addition, Blom et al. (2005) provided a detailed review of the tetrapod localities and their stratigraphical distribution. A more general account is given by Henriksen (2008). The most specific account of the in situ Stensio¨ Bjerg Acanthostega locality is given by Bendix-Almgreen et al. (1988, 1990). The sequences studied in this contribution (Figs 1 & 2) included a complete vertical section logged in detail through the Celsius Bjerg Group from the mountains of Wimans Bjerg, Nathorst Bjerg and Stensio¨ Bjerg on Gauss Halvø. Particular attention was paid to the in situ Acanthostega locality from the Britta Dal Formation on Stensio¨ Bjerg (fig. 14 in Blom et al. 2005). The most famous Ichthyostega locality (Blom et al. 2005) is at an altitude of 1174 m on Sederholm Bjerg in Paralleldal. This was relocated in the field and a stratigraphic section measured. This was then correlated


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Fig. 1. (a) Location of East Greenland Main Devonian Basin and (b) field sections investigated in East Greenland (Ø is island). Compiled from the GMT database.

using palaeoclimate cycles to the new sections from Nathorst Bjerg and Stensio¨ Bjerg. All the sections (totalling over 1000 m) were directly logged on a 10 cm scale (Fig. 2) with particular attention paid to rock colour and sediment cycles. All GPS co-ordinates are from UTM zone 27X with altitudes determined by both an altimeter calibrated to sea level and by GPS in 2006.

The Celsius Bjerg Group Elsa Dal Formation The Elsa Dal Formation, the oldest in the Celsius Bjerg Group, is a c. 160 m thick interval of yellow cross-bedded amalgamated sandstones (Figs 2 & 3). As shown by Olsen & Larsen (1993) it represents the deposits of a sandy alluvial braid-plain system. In the uppermost part of the formation there are thin intercalations of black mudstone that contain the only known palynomorphs (late Famennian GF zone, Marshall et al. 1999) found in the lower part of the Celsius Bjerg Group. These mudstones occur in Agda Dal between Nathorst Bjerg and Gunnbjørn Bjerg (in a section with the base of the Elsa Dal Formation at 0434020 8143084) and in Paralleldal (0426915 8158861, 856 m altimeter), that is, are regional in extent. They represent an

Fig. 2. Detailed measured section of the Celsius Bjerg Group from Stensio¨ Bjerg, Wimans Bjerg and Nathorst Bjerg on Gauss Halvø. The cyclicity is determined from the sediment colours. The red and purple colours are shown by the pattern of black blocks on the depth scale. The Britta Dal part of the log is from Nathorst Bjerg so the position of Acanthostega can only be approximate.

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Fig. 3. Celsius Bjerg Group palaeoenvironmental interpretations. The range of Retispora lepidophyta defines the latest Devonian with the Devonian– Carboniferous boundary occurring within the Obrutschew Bjerg Formation (OBF). The Harder Bjerg Formation log is from southwestern Celsius Bjerg.

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Fig. 4. Field photographs of Celsius Bjerg Group sedimentary environments. (a) In situ brecciation in the Wimans Bjerg Formation showing evidence for aridity. (b) Wave-rippled surface from the Wimans Bjerg Formation with gypsum pseudomorphs. The paler (ochreous) colour reflects the dolomitic content. (c) Spectacular exposure of red, purple and green (paler colour) vertisol cycles from Britta Dal Formation, Nathorst Bjerg (height of section c. 70 m);


interval where the system flooded sufficiently to allow the deposition of thin mudstone layers in shallow temporary lakes that were then preserved under a decreasing sedimentation rate.

Aina Dal Formation The overlying 45 m thick Aina Dal Formation (Figs 2 & 3) marks a transition to meandering rivers (Olsen & Larsen 1993) with a significant proportion of more mud-dominated overbank deposits. The evidence for the higher sinuosity is lateral accretion within channel sandstones including several point bar sequences. There is pervasive brecciation throughout the formation which together with the more typical desiccation cracks indicates that the climate was becoming increasingly arid. Many Ichthyostega specimens have been found from Aina Dal Formation scree together with a single Acanthostega specimen (Bendix-Almgreen et al. 1990; Blom et al. 2005) from a loose block that is also entirely characteristic of Aina Dal Formation lithology.

Wimans Bjerg Formation The Aina Dal to Wimans Bjerg contact is an upward transition through a drab-coloured (but nonpalyniferous) interval of siltstone. The Wimans Bjerg Formation (c. 160 m, Figs 2 & 3) is characterized (Olsen & Larsen 1993) by parallel laminated siltstones and thin sandstones with abundant wave ripples. These are interbedded with dolomitic siltstones that are also wave rippled and with abundant brecciation (Fig. 4a), desiccation cracks and gypsum pseudomorphs (Fig. 4b). The environment (Fig. 3) represents an alternating lacustrine and inland playa with a fluctuating but generally high water table giving rise to the dark sediment colour. Despite this dark colour, however, the formation is devoid of preserved organic matter (102 barren palynological samples in the Wimans Bjerg and Britta Dal Formations).

Britta Dal Formation The Britta Dal Formation is a c. 460 m interval (Figs 2 & 3) that comprises a spectacular cyclic

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sequence (Fig. 4c) of red, green and purple siltstones. The cyclicity when fully developed is defined by the rock colour with the alternation (Fig. 4d) from green through purple to red and then back to purple and green. These differently coloured beds define the characteristic ‘banks’ of Sa¨ve-So¨derbergh (unpublished m/s discussed in Blom et al. 2005, p.17) that were used to internally sub-divide and correlate the tetrapod-bearing intervals within the formation. In Paralleldal, some of these green siltstone beds (Fig. 5d) contain thin sandstone stringers which show that it was these drab units that were the wetter parts of the cycle. The cyclicity is systematically variable as the green siltstones can be missing from parts of the sequence where the cycles alternate between red and purple colours. All the different coloured siltstones contain conspicuous arcuate and sub-horizontal crack systems (Figs 4d –f & 5c) expressed as a very pervasive brecciation (Fig. 4f) that represents continuous in situ shrinkage and expansion. No calcrete nodules were found in these siltstones. These siltstones are entirely characteristic of vertisols (Retallack 1997; Ahmad & Mermut 2006) and represent an extensive mud-rich floodplain dominated by soil-forming processes. These are arid soils where there was successive seasonal wetting and drying. There are some 196 vertisol cycles present within the Wimans Berg to Britta Dal interval on Gauss Halvø and, as such, these formations represent a major sustained episode of aridity. These cycles are grouped into 6 megacycles of c. 20 vertisol cycles defined by systematic changes in the relative thickness of the green and red silts. The Britta Dal Formation on the mountain of Celsius Bjerg (Ymer Ø, Fig. 1; see also Clack & Neininger 2000) is much more proximal in character and contains significant sandstone beds (Fig. 4h) that replace the green intervals within a sequence of red-coloured palaeosols. On Gauss Halvø the Britta Dal Formation contains fine-grained sandstones that are laterally very extensive (Fig. 6a –c) and have flat bases (i.e. they were weakly to non-erosive). This demonstrates their origin as unconfined (i.e. poorly channelized) major flood events that spread across an extensive alluvial plain. Many of these sand bodies are

Fig. 4. (Continued) the red (darker colour) vertisol cycles can be seen to thicken in the middle part of the exposure. (d) Single vertisol cycle, Britta Dal Formation, Nathorst Bjerg. The green colour is paler middle section, purple is the darkest colour beneath this, red the upper darker layer. (e) Close-up of green-purple-red colour boundary (green is the lower two thirds, red the uppermost darker colour, purple the intermediate band between red and green) showing arcuate cracks and in situ brecciation, Britta Dal Formation, Nathorst Bjerg. (f) Bedding plane view of green vertisol cycle showing in situ brecciation, Britta Dal Formation, Nathorst Bjerg. (g) Fluvial sandstone in the Britta Dal Formation showing lateral change to green colours (right hand side of the sandstone) as soil turbation mixes the sand with floodplain mudstones, Nathorst Bjerg. (h) Britta Dal Formation from Celsius Bjerg, Ymer Ø. This shows the replacement proximally of the green, wetter vertisol cycles by fluvial sandstones.

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Fig. 5. The 1174 m Ichthyostega locality from Sederholm Bjerg, Paralleldal. (a) Profile Ravine showing formations and location of 1174 m Ichthyostega locality. (b) Close-up of 1174 m locality showing residual blocks of sandstone left by earlier expeditions. Henning Blom for scale. (c) Vertisol fracture surface from Britta Dal Formation showing brecciation caused by expansion and contraction cycles. (d) Red-green (dark-pale) vertisol cycle from Profile Ravine. Thin sandstone stringers (immediately above and below field notebook) occur within the green-coloured silts, indicating these to be the relatively wetter units. (e) Part of Britta Dal Formation section measured from Parallel Ravine showing vertisol cyclicity. These vertisol cycles together with the sandstones are the ‘banks’ used for correlation by Johansson (Jarvik) 1935 and Sa¨ve-So¨derbergh (m/s cited in Blom et al. 2005).


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Fig. 6. Fluvial sandstones from the Britta Dal Formation, Nathorst Bjerg. (a) Sequence of sandstone beds showing flat bases indicating origin as extensive flooding events that were not channelized. (b) Group of fluvial sandstones showing their significant lateral extent. Sandstone bed thicknesses are c. 1 m. (c) and (d) Single sand body showing combination of flat base and wide lateral extent; (d) has been annotated to show the lateral scour surfaces. Height of sandstone body c. 1.5 m.

composite events with major internal reactivation surfaces (Fig. 6c, d). These include very large scours (Fig. 6c, d) that developed prior to flood waning, channel abandonment and vertical

accretion of sediment. There is no evidence for lateral accretion within these sand bodies in contrast to the Aina Dal Formation. The Britta Dal Formation sandstones can occur anywhere within

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individual vertisol cycles although they are often grouped together within the sequence (e.g. Fig. 2 at c. 800 m) and represent generally wetter intervals. Lateral continuity of the sandstones is often interrupted as individual channel complexes become tinted green and fade out laterally (Fig. 4g). This is the result of intense soil turbation mixing the channel sandstones with the floodplain silts and providing confirmation of the dominance of arid climate processes. A good analogue for the Britta Dal Formation is Cooper Creek, Australia, where a very large multichannel ephemeral river system runs to internal drainage (Rust 1981; Nanson et al. 1986; Fagan & Nanson 2004; Kingsford 2006). Water flow in Cooper Creek is irregular with rare (i.e. decadal) but very intense flooding events when the water volumes become sufficient to sustain temporary lakes in the terminal fan area (Lake Eyre) for over a year (i.e. at least through the following dry season). During these flooding events, the local fauna expands (Kingsford et al. 1999) to occupy the system before becoming restricted to waterhole refugia that remain in the deeper sections of the channels. These waterholes (billabongs) remain as independent ecosystems through the intervening dry season, although most have dried out after two seasons (Hamilton et al. 2005; Bunn et al. 2006a). They form important habitats for fish, amphibians and reptiles (Kingsford et al. 2006) which can survive through successive dry seasons. Plants (Brock et al. 2006) are present within these systems and include aquatic benthic algae (Bunn et al. 2006b) which form an important part of the waterhole food chain. In normal seasons the extensive downstream fan area remains dry with water only present in the low water anastomosing channels in the upper reaches of the system. These low level channels can fill with water during flow pulses events, when the waterholes can be recharged but the floodplain is not inundated (Bunn et al. 2006a). The Cooper Creek system contains an extensive silt/clay floodplain that is dominated by vertisols with characteristic deep cracking and surface undulations known as gilgai (e.g. Mermut et al. 1996). Developed over much of the floodplain are a pattern of surface channels that are only active during flooding. In the modern (i.e. more recently than 40 ka, Maroulis et al. 2007) Cooper Creek system sediment movement includes transport as mud aggregate particles that behave as sand grains (Maroulis & Nanson 1996) which are deposited within channels that are present on the floodplain surface. The most common pattern to these floodplain surface channels is an anastomosing network where channels isolate and define small braided islands or braid bars. Vertisol processes are active

and, following soil turbation, these mud-within-mud features will have minimal preservation within older sediments. In Cooper Creek it was prior to 40 ka (Maroulis et al. 2007) that the channels within the system were sand dominated, demonstrating a much more active phase of sand sheet deposition. In the Britta Dal Formation the dominant sediments are the silt vertisols. The Cooper Creek analogy would suggest an origin from rare flood events that moved silt particle aggregates through the system in a braided network of channels. These would not necessarily originate from a major lowwater sand-filled channel cut into the floodplain but, more distantly, via a network of silt-within-silt floodplain surface channels. However, for much of the times vertisol or intermittently active vertisol processes would have dominated the floodplain environment. The intensive cracking and re-wetting would have caused total loss of original depositional fabrics. The presence of the much rarer but grouped sandstones parallels the pre-40 ka development of sand sheets in Cooper Creek. In the Britta Dal Formation, these were deposited during the very major flood events that brought sand into the system. These sand-sheets would have spread over the floodplain surface of silt in an anastomosing pattern but with only parts of the system active at any one time in a channel and braid bar pattern. The same sand sheet would have periodically re-flooded with the production of multiple scoured surfaces, migrating the channels and bars. At these times, the system would have flooded across much of the floodplain and a lake formed at the terminal fan. Again, analogies with both Cooper Creek and Lake Eyre suggest that this system lasted more than a single season and would have become occupied by both fish and tetrapods with the distinct possibility of ephemeral plants growing along the watercourses. The tetrapods could therefore have actively moved through the system post-flooding to inhabit the dry season waterholes, been swept along during the flood as dead or dying animals (like domesticated cattle and other tetrapods in Cooper Creek) or been sourced from an upstream accumulation of bone debris. Figure 7 is a cartoon reconstruction of the Britta Dal Formation fluvial system. The reconstruction is during a wetter interval following a major flood event. The palaeoflow direction is from south to north (Olsen 1993) with a sand-dominated sequence in northern Traill Ø as seen in the Rebild Bakker section (fig. 7 in Vigran et al. 1999; the sandstone sequence beneath the first occurrence of Retispora lepidophyta in sample 334804). To the north on southern Ymer Ø, the sandstones have become interbedded with red vertisols. Further to the north on Gauss Halvø the channels become more


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Fig. 7. Cartoon reconstruction of the Britta Dal Formation palaeoenvironment. The system is reconstructed as a large-scale ephemeral fluvial system flowing northwards. The braid system is only partially active during major floods. On Gauss Halvø the braids have become widely separated and the system is dominated by a silt-rich floodplain with extensive development of vertisols.

dispersed both laterally and vertically within the section. They are also laterally equivalent to the green-coloured vertisols. Further to the north there is no reported Britta Dal Formation, but the facies should be represented by shallow perennialto-ephemeral lake sediments.

Stensio¨ Bjerg Formation The Stensio¨ Bjerg Formation is defined by an end to the thick monotonous sequence of vertisols. Instead there are now palaeosols (aridisols) with calcrete nodules and more rarely individual calcrete beds. There are also numerous fluvial sandstone beds that represent wetter intervals. Also present are dark-coloured mudstones rich in organic matter that were deposited in stratified permanent lakes when the system became flooded sufficiently to establish deep perennial lakes. The prevailing climate of the Stensio¨ Bjerg Formation was therefore more variable including periods varying from aridity through to humidity, in marked contrast to the monotonous vertisols of the Britta Dal Formation. It is now been shown (Royer 1999) that it is not possible to make simple quantitative interpretations of palaeoprecipitation directly from palaeosols. However, it is most likely that the Britta Dal vertisols represent more sustained aridity with an average annual palaeoprecipitation of ,100 mm. The calcretes in the Stensio¨ Bjerg Formation, although still an indicator of aridity (,760 mm annual rainfall; Royer 1999),

require greater annual precipitation as both the source for the Ca2þ and to move it through the soil so that it becomes concentrated within the nodular layer. The East Greenland Devonian Basin is at an estimated palaeolatitude of c. 158S within the southern hemisphere arid zone. The mechanism by which annual precipitation can increase within this system is by a strengthening of the seasonal monsoon (e.g. Olsen 1990, 1993; Marshall et al. 2007). The seasonal monsoon is driven by the summer insolation maximum which, if strong enough, can draw in moist oceanic air that then produces intense rainfall. The simplest mechanism to increase summer insolation is to have a greater seasonal contrast with hotter winters and colder summers. Spore assemblages occur just beneath the base of the Stensio¨ Bjerg Formation and their appearance is coincident with the ending of the sustained aridity that characterizes the Britta Dal Formation. The spore assemblage is characterized by locally abundant Retispora lepidophyta (sometimes in excess of 60%) which are clearly latest Famennian in age (e.g. Streel et al. 1987; Maziane et al. 2002).

Obrutschew Bjerg Formation The thickest of the black mudstone and calcrete pairs defines the overlying Obrutschrew Bjerg Formation where 4–6 m of laminated organic-rich sediments with limestones was deposited. It

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represents a single, deep, permanent lake of considerable size and stability. It contains quite a different vertebrate assemblage that lacks the otherwise ubiquitous placoderms and contains only the actinopterygian fish Cuneognathus (Friedman & Blom 2006). This lake is coincident with the Devonian – Carboniferous boundary with the interval immediately beneath the organic-rich sediments containing a LN* spore assemblage, whereas the upper part of the Obrutschew Bjerg Formation contains VI spores (Streel & Marshall 2006).

Harder Bjerg Formation This interval is truncated by Permian sandstones on Gauss Halvø but is more fully developed on the mountain of Celsius Bjerg on Ymer Ø. It marks a return to a sequence of thick fluvial sandstones with minor calcretic mudstone intervals.

The 1174 m Ichthyostega locality on Sederholm Bjerg, Paralleldal The 1174 m Ichthyostega locality in Paralleldal (Fig. 5a) was relocated (2006) in Profile Ravine (Jarvik 1996, fig. 1B; Blom et al. 2005, figs 3, 4 & 10, section 11) at 0427913 8159913 and at an estimated altitude of 1198 m (GPS) or 1182 m (altimeter). The first sandstone in the section occurred at 1180 m (altimeter). The bed with the in situ Ichthyostega is the thickest sandstone seen within the section and contains bone fragments and abundant plant debris. It occurs in the lower part of the Britta Dal Formation within a sequence of red, green and purple mudstones. The 1174 m bed is still present in the ravine (Fig. 5b) but the exposure is now very reduced, presumably by extensive fossil collecting (Jarvik 1996). This 1174 m bed is at a high altitude close to the flat-topped summit of Sederholm Berg, such that the exposure is generally reduced to the block crop typical of Arctic mountain tops apart from in the ravine itself. However, a correlative section (Fig. 5e) has been measured on a prominent spur of red, green and purple-coloured siltstone on the eastern side of Profile Ravine. The base of the section is placed at the last thin grey dolostone unit, that is, the top of the Wimans Bjerg Formation, (0427933 8159551, height GPS 1079 m, altimeter 1044 m) and terminated along strike from the 1174 m locality at 0428102 8159778. The different-coloured siltstone cycles in the section were measured in an identical manner to those defined from the section on Nathorst Bjerg. The thicknesses of the individual cycles were measured from the base of a green siltstone through red/purple siltstones to the base of the overlying green siltstone. The thicknesses of

the individual cycles can then be plotted against cycle number through the section. This enables a correlation with the Nathorst Bjerg section (Fig. 8). The datum for the correlation is the top of the Wimans Bjerg Formation. This places the peak in cycle thickness at the top of megacycle 1 in Gauss Halvø exactly coincident with a peak in Paralleldal. The peak with the bundle of sandstones grouped around 1174 m is coincident with the first occurrence of a single sandstone bed and associated sand stringers in Gauss Halvø. This shows that the position of the 1174 m sandstone is about half way through the second megacycle. The poor condition of the remaining outcrop of the 1174 m sandstone prevents any direct study of its immediate environment. However, along strike it is represented by a 1.6 m thick sandstone which has a flat basal contact with the underlying siltstone. The sandstone is largely parallel bedded but does contain inclined scour surfaces. Also present are scattered bone fragments together with abundant plant debris at its base. Some of these plant fragments are in good condition and are fern-like, perhaps suggestive of a local short-lived vegetation that grew adjacent to the active fluvial systems following floods. Interestingly, a similar thick sandstone occurs at about this stratigraphical level on northern Nathorst Bjerg (916 m altimeter; 904 m GPS, 0422863 8156887) where it is the second sandstone above the base of the Britta Dal Formation. This sandstone contains both abundant basal shale clasts (darkcoloured silts but barren of palynomorphs) and numerous vertebrate fragments which include Holoptychius scales. It would appear to be a more proximal equivalent of the sandstone in Paralleldal.

The Acanthostega locality on the Stensio¨ Bjerg Ridge The well-documented (Bendix-Almgreen et al. 1988, 1990; Blom et al. 2005) in situ occurrence of many articulated individuals of Acanthostega is from the SE ridge of Stensio¨ Bjerg. It occurs at an altitude of 759 m (GPS) or 785 m (altimeter) with GPS co-ordinates 0429827 8146803. These occur within a sandstone bed towards the top of megacycle 6. The sandstone was described in Bendix-Almgreen et al. (1990) as typical of the Stensio¨ Bjerg Formation. The sandstone was described as two-storied and dominantly parallel laminated, although with low angle bedding in the lower storey indicative of lateral accretion on a point bar. The upper storey was again stated to have low-angle bedding of inferred point bar origin overlaid by a fine-grained channel fill. The two storeys were regarded as probably superimposed by downstream


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Fig. 8. Thickness of climatic cycles (base green through red/purple to base green) plotted against cycle number for the base Britta Dal Formation in Paralleldal (Broad Ravine) and Gauss Halvø (Nathorst Bjerg). The horizontal bars are sandstones. The base of the section measured in Paralleldal is at the top of the Wimans Bjerg Formation. On Gauss Halvø the cycle measurements started in the Wimans Bjerg Formation, hence the higher cycle numbers. The sections are tied at the top Wimans Bjerg Formation, cycle peaks (e.g. cycle 17 and 51) and troughs (20 and 54) show a clear correlation together with the position of the sand bodies. This shows the 1174 m locality to be located at a level just below the midpoint of megacycle 2.

migration of channel bends within a moderate to high sinuosity system. The fossil vertebrates were recorded as restricted to the low-angled sets, that is, the point bar deposits. The interpreted palaeoenvironment was therefore an ephemeral meandering stream of moderate to high sinuosity. This interpretation has proved to be very influential and underpinned many environmental reconstructions and arguments (Coates & Clack 1995; Clack 2002, 2006; Larsen et al. 2008) concerning the habitat of these early tetrapods. In 1996 this locality was briefly logged during an altimeter traverse up the SE ridge of Stensio¨ Bjerg carried out to place it within the new measured stratigraphical section. The main Britta Dal Formation log was made on the better exposed section that is present on Nathorst Bjerg. However, it should be noted that on Nathorst Bjerg the Stensio¨ Bjerg

Formation is truncated by erosion with the overlying Obrutschew Formation only being preserved on the mountains of Stensio¨ Bjerg and Wimans Bjerg. In 2006 the tetrapod locality was restudied to produce a digital photomontage (Fig. 9). The Acanthostega-bearing sandstone was seen as slightly different to most other sand bodies within the Stensio¨ Bjerg Formation. However, its situation is entirely typical of the Britta Dal Formation sand bodies as it occurs just beneath a major sandstone body that is laterally extensive, flat-based and with internal scoured surfaces. Figure 9 shows the sand body on both the western (Fig. 9a) and eastern (Fig. 9c, tetrapod locality) sides of the ridge together with the exposure (Fig. 9b) on the ridge crest. There is now less information available from the exposure as the inclined low-angle sets that contained

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Fig. 9. The sandstone on the SE ridge of Stensio¨ Bjerg, Gauss Halvø that contained the in situ specimens of Acanthostega: (a –c) compiled from digital photomontages using PTgui. (a) Channel sandstone from west side of ridge, to 0128. (b) The same sandstone on the ridge and c. parallel to palaeoflow, to 3428. (c) The Acanthostega locality on the eastern side of the ridge, to 3008 (compare fig. 13 from Blom et al. 2005). (d) The three sections shown in plan view. (e) Isometric reconstruction of the three sections compiled from photomontages and video. This shows the SW– NE axis of this minor channel. Inclined bedding was only recorded from the western side of (a) as shown in (d).

the tetrapods have largely been removed. However, the following conclusions can be drawn. The sandstone is a minor sand body with a channel form. It therefore differs somewhat from the much larger flat-based Britta Dal Formation sandstones.

It is a composite bed with the two storeys separated by a mudstone that is bright red in colour. This is a vertisol and represents a significant time gap. The two storeys are therefore not part of a continuously migrating single river system. They instead represent two separate and distinct flood events along the same channel.


The lower storey is laterally persistent and dominantly planar bedded. There are minor components of lateral accretion, represented here at the northern channel edge on the western ridge exposure. The upper sandstone is planar bedded, sheet-like and fills large scours at its base. The interpretation preferred here is therefore a minor channel that is part of, and peripheral to, a major sandstone body within the Britta Dal Formation. During at least two major flood events the Acanthostega sandstone was part of this major system. Its channelled morphology suggests that, rather than being a floodplain surface channel, it was an anastomosing inset low-water channel. This means that it was more likely to contain water for longer following flood events, that is, a waterhole. The tetrapods were found within a unit with inclined bedding, that is, a scoured depression, in a small marginal channel peripheral to a major channel system, and were almost certainly transported or migrated downstream during or following a major flooding event. As the flood waters receded, the individuals would either not been able to, or not chosen to, return upstream and were eventually forced to seek out the remaining water pools (i.e. refugia) that filled the basal scours. It was here, trapped by the receding waters level, that they died. This provides an explanation as to why so many articulated Acanthostega individuals are found together: they congregated in the remaining water in the river that was present in the basal scours. The alternative to passive transport is less likely as it requires many intact, that is, fresh carcasses to be carried into an orientated assemblage where the other vertebrates are disarticulated bones and scales (Clack 2002). It is therefore inferred that for most of the time Acanthostega lived in smaller, more permanent and likely more upstream parts of the river system which persisted for the years between the major flood events. It remains an interesting speculation as to how long Acanthostega remained in this part of the Britta Dal fluvial system and whether it could inhabit such waterhole refugia for long parts of the intervening dry season. However, such low-water sand-filled channels are rare within the full thickness of the Britta Dal Formation on Gauss Halvø and could never have been the major habitat for Acanthostega. This new interpretation presented here contradicts that generally portrayed for the Britta Dal Formation where these sandstones have been interpreted as a more permanent meandering fluvial system. The implication of this new interpretation means that Acanthostega has yet to be found within its normal habitat.

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Plant macrofossils Plant fossils from the Celsius Bjerg Group are generally rare, of low diversity and poorly preserved. They generally do not yield characters suitable for identifying them to generic level. The macrofossils are more common in the Stensio¨ Bjerg Formation. The best-preserved fossils are found in the Obrutschew Bjerg Formation lake deposits, but diversity remains low.

Britta Dal Formation plant macrofossils There have been very few reports of plants from the Britta Dal Formation (e.g. Larsen et al. 2008, p. 289). Poorly preserved lycopsids up to 50 mm in diameter were noted from the channel deposits of the Acanthostega locality on Stensio¨ Bjerg (Bendix-Almgreen et al. 1990, p. 134) and scraps of non-lycopsids were also noted in 2006. A more concentrated plant assemblage was found at the base of the 1174 m Ichthyostega sandstone in the Profile Ravine measured section. This yielded numerous axial plant fossils of less than a centimetre diameter (Fig. 10b, h, i). Most have no distinguishing features (Fig. 10b). One example shows a swollen base and probable spine bases (Fig. 10h) and another shows sub-opposite branching with lateral structures on the daughter axes. These are suggestive of fern-like plants such as Cephalopteris (e.g. Schweitzer 2006). This bed is one that should be noted for future investigation. Clack and others (Larsen et al. 2008, p. 289) collected a single branched specimen on Central Mount Celsius at 400 m altitude (Fig. 10c). This poorly preserved impression shows probable sub-opposite branching and a main axis (6 mm) impression with a central ridge. The most proximal branching point on the left-hand side (line drawing, arrow) is notable because the surface of the slab reveals that there are two vertically superposed lateral branches. These features together suggest a quadriseriate insertion of laterals [as found in, e.g. Rhacophyton (fern-like)], rather than an archaeopteridalean progymnosperm affinity for this structure which also lacks preserved leaves. Available evidence therefore suggests the presence of a transported, poorly preserved mixed lycopsid and ‘fern’ assemblage from the source area of the Britta Dal Formation.

Stensio¨ Bjerg Formation plant macrofossils Fossils from this formation seemed more abundant in the field. However, all the material found belonged to lycopsids. These were predominantly the internal casts of the inner and middle cortex, with the surface features suggestive of leaf traces

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going into the outer cortical layers (Fig. 10a, d, f ). These plants would have decayed to the state of hollow tubes before being infilled with sediment. Such casts are impossible to identify to generic level, but the large size of some of these trunks should be noted (up to 145 mm diameter); these undoubtedly represent the trunks of moderately tall lycopsid trees. One lycopsid showed detail which is more likely to be the outer surface of the plant, showing inverted U-shaped leaf attachments lacking further details (Fig. 10e). These are superficially similar to some preservational states of Cyclostigma from Bear Island (Bjørnøya) as illustrated by Nathorst (1902, plate 12, fig. 19a) although diagnostic features are missing.

Obrutschew Bjerg Formation plant macrofossils Plants have been noted on the south side of Mount Celsius since the 1950s (Blom et al. 2007, p. 129). Plants found in 2006 are mainly flattened axes but often retain carbon and/or impressions of the cuticle/epidermis (Fig. 10g). This, the only specimen to show branching, is identical in its stem surface details to the specimen illustrated by Schweitzer (2006, plate 42, fig. 2) as Cephalopteris tunheimensis from the Misery Series of Bear Island. Although lacking any other diagnostic features, the specimen should only be recognized as belonging to this grade of organization.

Plants and the tetrapod palaeoenvironment Stratigraphically below the Obrutschew lake, the preservation of plant fossils is very poor but shows the existence of lycopsid trees and various fern-like taxa. The fossils show high levels of de-cortication and a lack of identifying features such as leaves. Large logs, such as those to be expected from archaeopteridalean trees, are so far absent. The vegetation, which probably existed some distance upstream from where it was transported, may therefore have been dominated by lycopsids and fern-like plants rather than Archaeopteris. No evidence was found of in situ plants (e.g. plant rooting structures) despite the evidence of terrestrial surfaces and soils.

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This contrasts with the Red Hill tetrapod locality in Pennsylvania (Cressler 2006) where a diverse Archaeopteris-dominated flora has been recorded. It should be noted that the Red Hill flora is mainly found in a fine-grained floodplain pond; such subenvironments were not identified in the Celsius Bjerg Group.

Conclusions A detailed measured section is presented for the Celsius Bjerg Group, East Greenland. The sand bodies in the Britta Dal Formation are laterally extensive, flat based and aggraded prominently vertically. They are reinterpreted as the deposits of a large fluvial system that was subject to occasional very large flood events when parts of the system became active. At other times, soil processes dominated the silt-rich floodplains to produce a succession dominated by a spectacular sequence of vertisols. The sand body that contains in situ Acanthostega from the Britta Dal Formation on Stensio¨ Bjerg was part of this ephemeral system and not the deposits of a high sinuosity river channel that the tetrapods could have inhabited permanently. The famous 1174 m Ichthyostega locality in Paralleldal is a flood-event sandstone of similar origin that occurs just below the midpoint of megacycle 2 in the Britta Dal Formation. The fossil plants are generally restricted to the poorly preserved remains of lycopods and fern-like plants. Their preservation is entirely consistent with both an origin as a transported assemblage in common with the tetrapod fossils and with the model for the Britta Dal Formation sedimentary environment. The continued support of CASP is gratefully acknowledged, in particular the assistance of the other members of the 2006 expedition (C. Johnson and S. Johnson). M. Vecoli provided the impetus to complete this contribution via the CNRS-sponsored Eclipse II meeting on Terrestrialization Influences on the Palaeozoic Geosphere– Biosphere. J. Clack kindly provided the specimen illustrated in Figure10c.

Fig. 10. (Continued) Plant macrofossils from the Celsius Bjerg Group. Scale bar for (a– f) is 50 mm, for (g– i) 10 mm. (a) Lycopsid internal mould, 903 m altitude, Stensio¨ Bjerg Formation, southwestern Celsius Bjerg. (b) Indeterminate axial plant fossils, Britta Dal Formation, 1174 m horizon, Profile Ravine, Paralleldal. (c) Fern-like quadriseriate frond. Arrow shows vertically superposed lateral axes (collected by Clack and others in 1998 at 400 m altitude from east end of Central Celsius Bjerg scree, presumably Brita Dal Formation). (d) and (e) Two lycopsids from a single block in scree (probably Stensio¨ Bjerg Formation) from the bottom of the Aina Dal ravine, 555 m altitude. (f ) Lycopsid internal mould, Stensio¨ Bjerg Formation, Nathorst Bjerg (432709, 8144714, GPS 927 m). (g) Fern-like branching axis, 1094 m altitude, Obrutschew Bjerg Formation, southwestern Celsius Bjerg. (h) and (i) Indeterminate axial plant fossils, (h) showing enlarged frond base and spine bases on surface and (i) showing sub-opposite branching. Britta Dal Formation, 1174 m horizon, Profile Ravine, Paralleldal.

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References Ahlberg, P. E., Clack, J. A., Luksevics, E., Blom, H. & Zupins, I. 2008. Ventastega curonica and the origin of tetrapod morphology. Nature, 453, 1199–1204. Ahmad, N. & Mermut, A. 1996. Vertisols and technologies for their management. Developments in Soil Science, 24, 1–549. Bendix-Almgreen, S. E., Clack, J. A. & Olsen, H. 1988. Upper Devonian and Upper Permian vertebrates collected in 1987 around Kejser Franz Joseph Fjord, central East Greenland. Rapport Grønlands Geologiske Undersøgelse, 140, 95–102. Bendix-Almgreen, S. E., Clack, J. A. & Olsen, H. 1990. Upper Devonian tetrapod palaeoecology in the light of new discoveries in East Greenland. Terra Nova, 2, 131 –137. Blom, H., Clack, J. A. & Ahlberg, P. E. 2005. Localities, distribution and stratigraphical context of the Late Devonian tetrapods of East Greenland. Meddelelser om Grønland Geoscience, 43, 1– 50. Blom, H., Clack, J. A., Ahlberg, P. E. & Friedman, M. 2007. Devonian vertebrates from East Greenland: a review of faunal composition and distribution. Geodiversitas, 29, 119–141. Brock, M. A., Capon, S. J. & Porter, J. L. 2006. Disturbance of plant communities dependent on desert rivers. In: Kingsford, R. T. (ed.) Ecology of Desert Rivers. Cambridge University Press, Cambridge, 100–132. Bunn, S. E., Thoms, M. C., Hamilton, S. K. & Capon, S. J. 2006a. Flow variability in dryland rivers: boom, bust and the bits in between. River Research and Applications, 22, 179–186. Bunn, S. E., Balcombe, S. R., Davies, P. M., Fellows, C. S. & McKenzie-Smith, E. J. 2006b. Aquatic productivity and food webs of desert river ecosystems. In: Kingsford, R. T. (ed.) Ecology of Desert Rivers. Cambridge University Press, Cambridge, 76–99. Clack, J. A. 2002. Gaining Ground: The Origin and Evolution of Tetrapods. Indiana University Press, Bloomington, Indiana. Clack, J. A. 2006. The emergence of early tetrapods. Palaeogeography, Palaeoclimatology, Palaeoecology, 232, 167– 189. Clack, J. A. & Neininger, S. L. 2000. Fossils from the Celsius Bjerg Group, Late Devonian sequence, East Greenland: significance and sedimentological distribution. In: Friend, P. F. & Williams, B. P. J. (eds) New Perspectives on the Old Red Sandstone. Geological Society, London, Special Publications, 180, 557– 566. Coates, M. I. & Clack, J. A. 1995. ROMER’s gap: tetrapod origins and terrestriality. Bulletin du Museúm national d’Histoire naturelle, 4e`me se´rie – section C, 17, 373–388. Cressler, W. L. 2006. Plant palaeoecology of the Late Devonian Red Hill locality, north-central Pennsylvania, an Archaeopteris-dominated wetland plant community and early tetrapod site. Geological Society of America Special Paper, 399, 79–102. Fagan, S. D. & Nanson, G. C. 2004. The morphology and formation of floodplain-surface channels, Cooper Creek, Australia. Geomorphology, 60, 107– 127.

Friedman, M. & Blom, H. 2006. A new actinopterygian from the Famennian of East Greenland and the interrelationships of Devonian ray-finned fishes. Journal of Paleontology, 80, 1186–1204. Hamilton, S. K., Bunn, S. E., Thoms, M. C. & Marshall, J. C. 2005. Persistence of aquatic refugia between flow pulses in a dryland river system (Cooper Creek, Australia). Limnology and Oceanography, 50, 743– 754. Hartz, E. H., Torsvik, T. H. & Andresen, A. 1997. Carboniferous age for the East Greenland “Devonian” basin: paleomagnetic and isotopic constraints on age, stratigraphy, and plate reconstructions. Geology, 25, 675–678. Henriksen, N. 2008. Geological History of Greenland. Geus, Copenhagen, Denmark. Jarvik, E. 1948. Note on the Upper Devonian Vertebrate Fauna of East Greenland and on the age of the Ichthyostegid Stegocephalians. Arkiv fo¨r Zoologi, 41, 1– 8. Jarvik, E. 1996. The Devonian tetrapod Ichthyostega. Fossils & Strata, 40, 1 –213. Johansson, A. E. V. [Jarvik, E.] 1935. Upper Devonian fossiliferous localities in Parallel Valley on Gauss Peninsula, East Greenland, investigated in the summer of 1934. Meddelelser om Grønland, 96, 1– 37. Kingsford, R. T., Curtin, A. L. & Porter, J. 1999. Water flows on Cooper Creek in arid Australia determine ‘boom’ and ‘bust’ periods for waterbirds. Biological Conservation, 88, 231– 248. Kingsford, R. T. 2006. Ecology of Desert Rivers, Cambridge University Press, Cambridge. Kingsford, R. T., Georges, A. & Unmack, P. J. 2006. Vertebrates of desert rivers: meeting the challenges of temporal and spatial unpredictability. In: Kingsford, R. T. (ed.) Ecology of Desert Rivers. Cambridge University Press, Cambridge, 154–200. Larsen, P.-H., Olsen, H. & Clack, J. A. 2008. The Devonian basin in East Greenland– Review of basin evolution and vertebrate assemblages. In: Higgins, A. K., Gilotti, J. A. & Smith, M. P. (eds) The Greenland Caledonides: Evolution of the Northeast Margin of Laurentia. Geological Society of America Memoir, 202, 273 –292. Maroulis, J. C. & Nanson, G. C. 1996. Bedload transport of aggregated muddy alluvium from Cooper Creek, central Australia: a flume study. Sedimentology, 43, 771–790. Maroulis, J. C., Nanson, G. C., Price, D. M. & Pietsch, T. 2007. Aeolian– fluvial interaction and climate change: source bordering dune development over the past c. 100 ka on Cooper Creek, central Australia. Quaternary Science Reviews, 26, 386–404. Marshall, J. E. A., Astin, T. R. & Clack, J. A. 1999. The East Greenland tetrapods are Devonian in age. Geology, 27, 637 –640. Marshall, J. E. A., Astin, T. R., Brown, J. F., Kurik, E. & Lazauskiene, J. 2007. Recognising the Kacˇa´k Event in the Devonian terrestrial environment and its implications for understanding land-sea interactions. In: Becker, R. T. & Kirchgasser, W. T. (eds) Devonian Events and Correlations. Geological Society, London, Special Publications, 278, 133– 155.

EAST GREENLAND TETRAPOD ENVIRONMENTS Maziane, N., Higgs, K. T. & Streel, M. 2002. Biometry and paleoenvironment of Retispora lepidophyta (Kedo) Playford 1976 and associated miospores in the latest Famennian nearshore marine facies, eastern Ardenne (Belgium). Review of Palaeobotany and Palynology, 118, 211– 226. Mermut, A. R., Dasog, G. S. & Dowuona, G. N. 1996. Soil Morphology. In: Ahmad, N. & Mermut, A. (eds) Vertisols and Technologies for their Management. Developments in Soil Science, 24, 89–114. Nanson, G. C., Rust, B. R. & Taylor, G. 1986. Coexistent mud braids and anastomosing channels in an aridzone river: Cooper Creek, central Australia. Geology, 14, 175–178. Nathorst, A. G. 1902. Zur Oberdevonischen Flora der Ba¨ren-Insel. Kungliga Svenska Vetenskapsakademiens Handlingar, 36, 1– 60. Olsen, H. 1990. Astronomical forcing of meandering river behaviour: Milankovitch cycles in the Devonian of East Greenland. Palaeogeography, Palaeoclimatology, Palaeoecology, 79, 95– 115. Olsen, H. 1993. Sedimentary basin analysis of the continental Devonian basin in North-East Greenland. Bulletin of the Grønlands Geologiske Undersøgelse, 168, 1 –80. Olsen, H. & Larsen, P.-H. 1993. Lithostratigraphy of the continental Devonian sediments in North-East Greenland. Bulletin of the Grønlands Geologiske Undersøgelse, 165, 1–108. Retallack, G. J. 1997. A Colour Guide to Paleosols. Wiley, Chichester. Royer, D. L. 1999. Depth to pedogenic carbonate horizon as a paleoprecipitation indicator? Geology, 27, 1123–1126 (see also Forum, Geology, 28, 572– 573).

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Rust, B. R. 1981. Sedimentation in an arid-zone anastomosing fluvial system: Cooper’s Creek, central Australia. Journal of Sedimentary Petrology, 51, 745– 755. Schweitzer, H.-J. 2006. Die Oberdevon-Flora de Ba¨reninsel 5. Gesamtu¨bersicht. Palaeontographica B, 274, 1– 191. Stemmerik, L. & Bendix-Almgreen, S. E. 1998. Carboniferous age for the East Greenland “Devonian” basin: paleomagnetic and isotopic constraints on age, stratigraphy, and plate reconstructions: comment. Geology, 26, 284–285. Streel, M. & Marshall, J. E. A. 2006. DevonianCarboniferous boundary global correlations and their paleogeographic implications for assembly of Pangaea. In: Wong, Th. E. (ed.) Proceedings of the XVth International Congress on Carboniferous and Permian Stratigraphy. Utrecht, the Netherlands, 10– 16 August 2003. Royal Netherlands Academy of Arts and Sciences, 481– 496. Streel, M., Higgs, K., Loboziak, S., Riegel, W. & Steemans, P. 1987. Spore stratigraphy and correlation with faunas and floras in the type marine Devonian of the Ardenne-Rhenish regions. Review of Palaeobotany and Palynology, 50, 211–229. Vigran, J. O., Stemmerik, L. & Piasecki, S. 1999. Stratigraphy and depositional evolution of the uppermost Devonian-Carboniferous (Tournaisian-Westphalian) non-marine deposits in north-east Greenland. Palynology, 23, 115–152. Westoll, T. S. 1941. Contribution to discussion on the boundary between the Old Red Sandstone and the Carboniferous. Reports of the British Association for the Advancement of Science, no. 2 (1939–1940), 258.

Terrestrialization in the Late Devonian: a palaeoecological overview of the Red Hill site, Pennsylvania, USA WALTER L. CRESSLER III1*, EDWARD B. DAESCHLER2, RUDY SLINGERLAND3 & DANIEL A. PETERSON3 1

Francis Harvey Green Library, 25 West Rosedale Avenue, West Chester University, West Chester, PA 19383, USA 2

Vertebrate Paleontology, Academy of Natural Sciences, 1900 Benjamin Franklin Parkway, Philadelphia, PA 19103, USA

3

Department of Geosciences, The Pennsylvania State University, University Park, PA 16802, USA *Corresponding author (e-mail: [email protected]) Abstract: Alluvial floodplains were a critical setting during the Late Devonian for the evolution of terrestriality among plants, invertebrate and vertebrates. The Red Hill site in Pennsylvania, US, provides a range of information about the physical and biotic setting of a floodplain ecosystem along the southern margin of the Euramerican landmass during the late Famennian age. An avulsion model for floodplain sedimentation is favoured in which a variety of inter-channel depositional settings formed a wide range of aquatic and terrestrial habitats. The Red Hill flora demonstrates ecological partitioning of the floodplain landscape at a high taxonomic level. In addition to progymnosperm forests, lycopsid wetlands and zygopterid fern glades, the flora includes patches of early spermatophytes occupying sites disturbed by fires. The Red Hill fauna illustrates the development of a diverse penecontemporaneous community including terrestrial invertebrates and a wide range of vertebrates that were living within aquatic habitats. Among the vertebrates are several limbed tetrapodomorphs that inhabited the burgeoning shallow water habitats on the floodplain.

Although the process was already well underway by the Silurian (Edwards & Wellman 2001; Shear & Selden 2001), the Late Devonian was a time of key evolutionary innovations that made possible the further terrestrialization of life. For example, it was during the Late Devonian that seed reproduction fully evolved in plants and the fin-to-limb transition occurred in vertebrates (Rothwell & Scheckler 1988; Clack 2002). Each of these evolutionary events occurred in association with the aquatic ecological context of their ancestral conditions. The appearance of novel features can be seen in hindsight to have predisposed these lineages to additional physiological and morphological changes that promoted terrestrialization. As life expanded over the landscape new ecological guilds emerged, the trophic structure of continental ecosystems became more complex (DiMichele et al. 1992) and the resulting transformations in the transfer of matter and energy changed the dynamics of biogeochemical cycles in the sea and atmosphere as well as on land (Algeo et al. 2001). Significant aspects of the early stages of this global transition can be documented through observation and analysis of the physical and biotic

conditions present on Late Devonian alluvial plains. The sedimentary sequence at the Red Hill site in Clinton County, Pennsylvania (Fig. 1) was deposited during the late Famennian age within the alluvial plain of the Catskill Delta Complex along the southern margin of the Euramerican (Larussian) landmass. The site preserves a rich sample of plants and animals that lived penecontemporaneously in floodplain habitats. Red Hill therefore provides a comprehensive glimpse of a continental ecosystem at this important stage in the terrestrialization of life.

Background Evolutionary and ecological events on Devonian continents Early Devonian land-plant communities were characterized by a patchwork landscape of lowstature plants growing in monotypic clonal stands along watercourses and coastal zones (Griffing et al. 2000; Hotton et al. 2001). During the Mid Devonian, the competition for light and spore dispersal led several plant lineages to develop secondary


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Fig. 1. Location of the Red Hill site, Clinton County, Pennsylvania, US.

growth and robust architectures for enhanced height (Berry & Fairon-Demaret 2001). These included large cladoxylopsid trees (Stein et al. 2007), aneurophytalean shrubs, lepidosigillarioid lycopsids and, by the late Middle Devonian, archaeopteridaleans (Scheckler 2001). Plant-community structure reached even greater levels of complexity and biomass production during the Late Devonian (Algeo & Scheckler 1998). By then, plant communities included gallery-forest trees, shrubs, herbaceous ground cover, vines and specialized wetland plants (Scheckler 1986a, Greb et al. 2006). Archaeopteridalean forests became widespread from boreal to tropical latitudes (Beck 1964). All primary and secondary plant tissues, other than the angiosperm endosperm, had evolved by the end of the period (Chaloner & Sheerin 1979). The major phylogenetic plant groups that appeared during the Late Devonian and Early Mississippian correspond broadly to distinct ecological positions in the landscape (Scheckler 1986a). While apparent niche partitioning took place among plants earlier in the Devonian, it occurred within a more limited number of groups and within a narrower range of environments (Hotton et al. 2001). By the Late Devonian, isoetalean lycopsids occupied permanent wetlands, zygopterid ferns were widespread in ephemeral wetlands, spermatophytes occupied disturbed sites and archaeopteridalean progymnosperms predominated along the betterdrained overbanks and levees (Scheckler 1986a, b; Rothwell & Scheckler 1988; Scheckler et al.

1999). Once the archaeopteridaleans became extinct and the zygopterids diminished in importance at the end of the Devonian, a new pattern of ecological distribution at a high phylogenetic level had emerged (Peppers & Pfefferkorn 1970). Rhizomorphic lycopsids dominated in wetlands, ferns in disturbed environments, sphenopsids in aggradational environments such as point bars and spermatophytes on well- to poorly-drained clastic substrates (DiMichele & Bateman 1996). Even with this phylogenetic turnover and dominance shift, the general pattern of landscape partitioning by plants at a high phylogenetic level persisted. This lasted from its origin in the Late Devonian until the drying of the global climate following the Mid Pennsylvanian. By the Permian, spermatophytes dominated in almost all vegetated environments and have done so ever since (DiMichele & Bateman 1996). The Late Devonian evolution of the seed eventually led to the adaptive radiation of spermatophytes because plants were no longer constrained to water for transfer of sperm during fertilization (Stewart & Rothwell 1993). Sexual reproduction in free-sporing plant lineages is dependent on available surficial water for its success. Numerous plant lineages evolved heterospory, in which a spore that produces female gametophytes is larger than a spore producing male gametophytes (Bateman & DiMichele 1994). Within the lignophytes, heterospory was the evolutionary precursor for the seed habit that involves the retention of megasporangia containing the female megagametophytes upon the sporophyte. Fertilization follows contact (pollination) between the wind-borne or animal-borne microspore (pre-pollen or pollen) and the retained megasporangium, after which an embryo develops within the protected environment of a seed (Rothwell & Scheckler 1988). While this decoupling of sexual reproduction from dependence on water permitted spermatophytes to radiate into dry environments, the selection pressures for retention of the megasporangium on the sporophyte took place within the periodically wet environments in which seed plant precursors evolved from their free-sporing ancestors. Factors other than success in dry environments must have been driving the unification of the gametophyte and sporophyte generations in the ancestors of spermatophytes. Therefore, during the time of their earliest diversification in the Late Devonian, seed plants were probably still minor components of plant communities that were restricted to wetlands and floodplains (DiMichele et al. 2006). The earliest animals to emerge onto land were arthropods: mainly arachnids, myriapods and some hexapods (Shear & Selden 2001). Most early terrestrial arthropods were predators and detritivores, but

LATE DEVONIAN PALAEOECOLOGY AT RED HILL

feeding behaviour included herbivory on spores and plant stems (Labandeira 2007). The Late Devonian provides little evidence that the array of functional feeding types among terrestrial arthropods diversified much beyond the few that originated in the Late Silurian and Early Devonian. Despite the evolutionary appearance of true roots, leaves, wood and seeds by the Late Devonian, these plant tissues do not show evidence of extensive herbivory until the Late Mississippian-Early Pennsylvanian boundary (Labandeira 2007). Early and Mid Devonian vertebrates are best known from ‘red bed’ deposits formed in marine and estuarine settings along continental margins. During the Early Devonian these strata were dominated by lineages of agnathans and acanthodians that appeared during the Silurian (Janvier 1996). Importantly, placoderms emerged in many Early Devonian faunas, and sarcopterygians also became more predominant. The dipnomorph clade first appeared and includes durophagus lungfish and predatory porolepiforms (Janvier 1996). The diversity and abundance of gnathostomes continued to increase during the Mid Devonian with placoderm and acanthodian radiations. Early actinopterygians appeared and tetrapodomorph sarcopterygians diversified to fill a wide variety of predatory aquatic niches. By the Late Devonian, many of these groups were well established in non-marine habitats associated with vegetated floodplains. It is during the Late Devonian that several groups of placoderms, including phyllolepids, groenlandaspidids and bothriolepids, were common in continental and marginal settings, although these groups disappeared by the end of the period. A diverse array of sarcopterygians, including porolepiforms, dipnoans, rhizodontids and ‘osteolepiforms’ were also found in continental and marginal deposits. Elpistostegalian sarcopterygians first appear in the late Mid Devonian (Givetian). By the latter part of the Late Devonian (Famennian), the fossil record documents a variety of early limbed forms from a range of fluvial and near-shore depositional settings across the globe (Blieck et al. 2007; Astin et al. 2010). Some lineages of tetrapodomorph sarcopterygians show morphological specializations in the pectoral girdles and fins that reflects experimentation in the use of the appendage for substrate locomotion. Among the rhizodontids and some ‘osteolepiforms’, pectoral fins were used to push off from the substrate (Davis et al. 2004). Within the basal elpistostegalian lineage, pectoral fins developed a limb-like endoskeletal configuration and other specializations that may have allowed these animals to move through very shallow waters via substrate contact (Daeschler et al. 2006). It is within the elpistostegalian lineage that this configuration of fins with wrist, elbow and shoulder joints

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leads to the development of limbs with digits and therefore to the origin of tetrapods. The Late Devonian witnessed early tetrapods that were still linked closely to aquatic ecosystems (Clack & Coates 1995; Clack 2002). As the record of the fin-to-limb transition has improved, we have gained a better understanding of the sequence of anatomical changes with the goal of reconstructing the acquisition of features that eventually allowed terrestriality. Fully terrestrial vertebrates do not appear in the fossil record until the Visean (352 – 333 Ma). The period between the origin of limbs (in the Late Devonian) and fully terrestrial habits (in the Visean) has been called Romer’s Gap. More data are slowly emerging which will elucidate details of this critical interval in tetrapod history (e.g. Clack & Finney 2005). According to recent models, the large increase in plant biomass and corresponding increase in depth of rooting and soil formation on Late Devonian floodplains led to a significant alteration of biogeochemical cycles. Enhanced weathering on the continents and the influx of plant detritus into fluvial systems increased nutrient availability in aquatic environments, and were possibly a causal factor for periodic marine anoxia (Algeo & Scheckler 1998). Black shale deposition in the epicontinental seaways record the anoxic episodes possibly resulting from these eutrophic conditions (Algeo et al. 2001). The Late Devonian black shale horizons are global in extent and are associated with major marine extinctions, particularly of stromatoporoidtabulate reef communities (McGhee 1996). The decline of CO2 levels in the atmosphere and subsequent climate cooling have also been attributed to this weathering and burial of organic carbon, resulting in a brief glacial episode at the end of the Devonian (Caputo 1985; Algeo et al. 2001). Models of fluctuating atmospheric O2 levels for the Devonian and Carboniferous have been used recently to invoke causal mechanisms for terrestrial diversification patterns (Ward et al. 2006; Labandeira 2007). After their first major diversification in the Late Silurian-Early Devonian, low oxygen levels during the Mid-to-Late Devonian are postulated as a cause for the suppression of further diversification of terrestrial arthropods until the late Mississippian (Labandeira 2007). The suppression of evolutionary diversification by low oxygen levels has also been invoked as an explanation for Romer’s Gap, the 15 Ma interval between the Late Devonian and late Mississippian with few known tetrapod fossils (Ward et al. 2006). In contrast, Clack (2007) points to the diverse Visean East Kirkton tetrapod fauna that demonstrates significant evolutionary advancements during the Romer’s Gap interval which simply has not been preserved or recovered from the fossil

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record. Because atmospheric oxygen levels are higher than contemporaneous aquatic oxygen levels, Clack (2007) postulates that anoxic conditions caused by decaying plant matter in freshwater ecosystems were a driving force in the evolution of air breathing in tetrapodomorph fishes and their limbed descendents. These varying causal models represent ongoing efforts to relate evolutionary and ecological events to global biogeochemical changes in the Earth system.

Tectonics and depocentres in the Late Devonian The evidence for Late Devonian evolutionary and ecological terrestrial events is derived from sedimentary basins at the convergent and extensional margins of Late Devonian land masses (Friend et al. 2000). The Late Devonian land surface consisted of Euramerica (Laurussia) and Gondwana and the smaller continents of Siberia, Kazakhstan, North China and South China as well as numerous microcontinents and islands (Scotese & McKerrow 1990). These landmasses were generally converging as part of the assembly of the supercontinent Pangaea during the Mid Palaeozoic. By the Late Devonian, major sedimentary basins were well developed between components of Laurussia and Gondwana as the Iapetus Ocean closed between them. Many classic Late Devonian fossil sites in the Appalachian Basin of North America, East Greenland, Arctic Norway, the United Kingdom, Ireland, Belgium, Germany, the Baltics and Russia are located in sediments resulting from Caledonide tectonic activity or post-orogenic collapse (Friend et al. 2000).

By the Late Devonian, the onset of subduction along the northwestern edge of Euramerica resulted in the Antler and Ellesmerian Orogenies and in the western edge of Gondwana resulted in the Bolivarian Orogeny (Scotese & McKerrow 1990). This activity resulted in sedimentary deposits with fossils of Late Devonian terrestrial organisms in western North America, Arctic Canada, Venezuela and Colombia. Smaller scale tectonic activity occurred on the eastern end of Gondwana and among the nearby microcontinents which created basins in Australia, Central Asia, North China and South China (McMillan et al. 1988).

Depositional setting at Red Hill Catskill Formation The Red Hill site is a road cut exposure of the Duncannon Member of the Catskill Formation (Woodrow et al. 1995). During deposition, sedimentation in Pennsylvania was dominated by a westward prograding shoreline complex with three deltaic depocentres (Dennison & Dewitt 1972; Rahmanian 1979; Smith & Rose 1985; Williams & Slingerland 1986), one of which occupied the centre of the state (Fig. 2). These were fed by rivers that arose in the Acadian Highlands to the east, and flowed westwards across a proximal alluvial plain (Sevon 1985; see Bridge & Nickelsen 1986 for an alternative view) onto a vast lowgradient coastal plain where sediments were deposited within an upper deltaic or lower alluvial plain setting. The alluvial plain rivers across the border in New York State are documented to have been low sinuosity, perennial, laterally migrating single

Fig. 2. General depositional setting of the Appalachian basin during deposition of the strata at Red Hill. The illustration represents the position of the shoreline during the Frasnian Stage. By the Fammenian, when the strata at Red Hill were deposited, the shoreline had prograded further west and the locality lay in the upper alluvial to lower coastal plain.


channels (Bridge & Gordon 1985). Bankfull discharges calculated at four cross-sections, thought to be within about 10 km of the shoreline, ranged from 40 to 115 m3 s21. Although similar small rivers are recognized in eastern Pennsylvania (Sevon 1985), by the time the coastal plain had prograded through central Pennsylvania the rivers were fewer in number and larger in dimension (Rahmanian 1979; Williams 1985). The low palaeolatitude (less than 208) resulted in a tropical climate with alternating wet and dry seasons along the southern edge of the Euramerican landmass (Woodrow & Sevon 1985).

Depositional model Traditional views of sedimentation in upper alluvial and coastal plain settings envision a single-thread meandering river continually feeding fine-grained sediment to a slowly aggrading floodplain as the alluvial ridge accumulates coarser-grained sediment. However, recent studies of modern fine-grained fluvial systems that are experiencing avulsions show that these systems cycle through two stages with a typical period of the order 1000 years (Smith et al. 1989; Slingerland & Smith 2004; Soong & Zhao 1994). Stage I begins when a channel changes course by permanently breaching its levee. Here, a sediment wedge is constructed, headed at (or near) the

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avulsion site and prograding down-current as additional sediment is transported and deposited at the margins. Intense alluviation of the floodplain is fuelled by the large drop in energy as the system evolves from a single channelized flow into rapidly evolving distributary channels of the alluvial wedge. These channels, in turn, debouche into waters ponded on the floodplain, the result of preexisting channel levees and the high friction of floodplain vegetation (Fig. 3). Deposition proceeds by basinward extension of coalescing splays and lacustrine deltas fed by anabranching networks of distributary channels. The splays and deltas build into the transient lakes created by flooding due to the avulsion. In the process of progradation, new channels form by crevassing and bifurcation at channel mouths, and others lengthen by basinward extension. Both serve to deliver new sediment to the flooded basin so that further progradation can continue. Deposits of this stage are commonly: (1) coarser-grained crevasse splays assuming a variety of lobate, elliptical or elongate shapes and usually containing multiple and variously sized distributary channels that route water and sediment to and beyond the splay margins (O’Brien & Wells 1986; Smith 1986; Bristow 1999); and (2) finer-grained lake and distal splay deposits in which rapid burial has preserved organic debris from oxidation. Stage II of the avulsion cycle is marked by distributary channels that begin to flow sub-parallel to the

Fig. 3. Depositional environments during Stage I of the avulsion model envisioned for Red Hill sedimentation. Watercolour from Cumberland Marshes of the Saskatchewan River, SK, Canada. Evolutionary innovations described in the text are thought to have arisen in a similar terrestrial setting.

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parent channel, once again following the regional slope. Small channels on the floodplain are abandoned as flow is captured into a new trunk channel similar in scale to the parent channel that initially avulsed (Smith et al. 1989). Sedimentation rates are low, allowing peat and soil formation to resume on the floodplain. The new trunk channel incises into its earlier avulsion deposits, creating a new meander belt that has a width about twice the meander amplitude. Incision occurs because all of the water is now collected into one channel of steeper slope than existed in Stage I. This meander belt width is relatively narrow and only a small fraction of the floodplain deposits are reworked into meander belt deposits; the bulk of the floodplain deposits consists of Stage I avulsion fill (Fig. 4). In the Red Hill outcrop, Stage I deposits are characterized by packages of red hackly weathering mudstones, faintly laminated siltstones with gently inclined bedding and very fine sandstones exhibiting cross-bedding cut-and-fill structures and flatbased convex-upwards bars that pinch-out laterally over tens of metres (ribbon sandstones of Fig. 4). The bars are flat-laminated and thinly bedded, with bedding surfaces often littered with plant debris. These sandstones are interpreted as deposits of proximal splays and splay-channel complexes while the siltstones and mudstones accumulated in ponds and more distal portions of the splay. The Stage I deposits at Red Hill contain the fossil-bearing facies with a variety of articulated, closely associated and isolated skeletal remains. Stage II sedimentation is represented by floodplain palaeosols identified by increased clay content, extensive slickenside surfaces, abundant caliche nodules up to 1 cm in diameter and root traces. Whether peats of palaeosols form during this stage depends upon whether the water table in the avulsion deposits remains high or is lowered as waters are collected into the more efficient single-thread

channel of the newly forming meander belt. At the western end of the outcrop channel belt deposits are found. There are four avulsion cycles within the sequence exposed at the east end of the Red Hill outcrop. The earliest of these cycles (Fig. 5) shows the most extensive Stage I deposits (around 3 m thick) and is the primary fossiliferous zone at Red Hill, the source of the material on which this palaeoecological analysis is based. The thickness of the Stage I deposits in this cycle may reflect greater proximity to the parent channel at the time of that particular avulsion event. Successive Stage I packages are thinner (less than 2 m thick).

Taphonomic considerations The source of fossil remains at Red Hill is a vertically narrow (3 m) but laterally broad (c. 200 m exposed) sequence of fossiliferous strata. There is considerable lateral variation within this fossiliferous zone reflecting the heterogeneity produced by the variety of depositional facies in the avulsion model. Four different taphofacies preserve fossil material: sorted microfossil horizons, basal lags, channel-margin and standing water deposits. Wellsorted microfossil accumulations and basal lag deposits contain abundant, but fragmentary, vertebrate material that may be allochthonous and therefore have poor time and ecological fidelity. The channel-margin taphofacies contains isolated and associated vertebrate material, often in discrete lenses. The character of the entombing sediments indicates that the fossils accumulated along the strandline of the aggrading margins of temporary channels in overbank areas after avulsion episodes. Deposits of this sort have the potential to accumulate relatively quickly, and the fact that the taphofacies shows little or no abrasion or predepositional weathering of accumulated material indicates that the associated taxa were living

Fig. 4. Schematic cross-section of alluvial deposits showing stratigraphic relationships of Stages I and II. Fossiliferous strata discussed in text originate from Stage I deposits.


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Fig. 5. Graphic log of the earliest and thickest Stage I deposits at Red Hill showing location of fossiliferous zone with respect to these avulsion deposits. See text for details.

penecontemporaneously in the areas near the site of deposition. The standing water taphofacies is represented by green-grey siltstones with abundant plant material and an occasional occurrence of

arthropod and vertebrate remains. The vertebrate remains from this setting are black and ‘carbonized’ suggesting different water chemistry and diagenetic conditions (perhaps more acidic) than other

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taphofacies at Red Hill. These deposits represent low-energy, reducing environments such as floodplain ponds and distal splay settings that can provide excellent temporal and ecological fidelity.

Distribution of habitats at Red Hill The floodplain habitats at Red Hill provided a range of conditions for the cohabitation of plants and animals. Plant communities were partitioned on the floodplain across a range of environments from elevated and better-drained levees to low, wetland habitats (Cressler 2006). The aquatic settings include open river channels, shallow channel margins, anastomosing temporary channels and floodplain ponds in interfluves that were subject to periodic flooding. This heterogeneity is expressed even on the local scale at the Red Hill site, as might be expected with the avulsion model of floodplain aggradation. Seasonal flooding and drying probably had a significant role in the annual cycles of plants and animals.

Age of the deposit Palynological analysis has placed Red Hill within the poorly calibrated VH palynozone (Traverse 2003), but it is less ambiguously attributed to the VCo palynozone (sensu Streel et al. 1987) within the Famennian Stage, Late Devonian Period. This zone is defined by the first occurrence of the palynomorph index species Grandispora cornuta Higgs and Rugispora flexuosa (Juschko) Streel, among others (Richardson & McGregor 1986; Streel & Scheckler 1990). A revision of Late Famennian zonation in Belgium will possibly place Red Hill firmly within the VH Spore Zone (Maziane et al. 1999) and therefore within the trachytera to middle expansa Conodont Zones of the upper Famennian Substage (Streel & Loboziak 1996).

Red Hill flora and fauna Floral diversity The floral characteristics of the site are typical of a Late Devonian plant assemblage, a subtropical Archaeopteris forest (Table 1). Four Archaeopteris leaf morphospecies are dominated by A. macilenta and A. hibernica (Fig. 6a). This progymnosperm tree is an index fossil for the Late Devonian (Banks 1980), as is the second most abundant set of plant remains at Red Hill, the zygopterid fern assigned to Rhacophyton (Fig. 6c). The early diversification of arborescent lycopsids are represented by numerous decorticated stems, some identifiable as Lepidodendropsis. Well-preserved remains of cormose isoetalean bases and stems, described as

Otzinachsonia beerboweri (Cressler & Pfefferkorn 2005), are also present. Spermatophytes are present as both Moresnetia-like cupules (Fig. 6b) and Aglosperma sp (Cressler 2006). The palynological age of the strata make it coeval with the ages of other sites with earliest recorded spermatophytes in Belgium and West Virginia (Fairon-Demaret & Scheckler 1987; Rothwell et al. 1989). Other minor floral elements include the stauripterid fern Gillespiea and a variety of barinophytes (Cressler 2006). Major plant groups found at other Late Devonian sites but not yet discovered at Red Hill are the sphenopsids and cladoxylaleans.

Faunal diversity Table 2 presents a list of Red Hill fauna recognized to date. The arthropod fauna is likely only a very limited subset of the invertebrate community that was in the floodplain ecosystem. A trigonotarbid arachnid (Fig. 6f ) and an archidesmid myriapod (Fig. 6e) have each been described from the standing water taphofacies, but greater diversity is evidenced by enigmatic body impressions, burrow traces and walking traces (Fig. 6d). The vertebrate assemblage represents a diverse community that was living in aquatic habitats within the alluvial plain of the Catskill Delta Complex. These include bottom feeders, durophages, filter feeders and a wide range of predators. The placoderm assemblage is dominated by the small groenlandaspidid, Turrisaspis elektor, one of the most common taxa from the site (Daeschler et al. 2003). Fin spines and pectoral girdle elements of the acanthodian Gyracanthus (cf. G. sherwoodi) are also quite common. Among the bony fish fauna (osteichthyans), the small palaeoniscid actinopterygian Limnomis delaneyi (Fig. 6h) and the large tristichopterid sarcopterygian Hyneria lindae are the dominant components. Early tetrapod remains are very rare and are represented by isolated skeletal elements, although recent analysis suggests that at least three penecontemporaneous taxa are present (Daeschler et al. 2009).

Palaeoecological setting at Red Hill Vegetation A previous palaeoecological analysis of the Red Hill plant community characterized the vegetation as a subtropical Archaeopteris floodplain forest interspersed with lycopsid wetlands and widespread stands of Rhacophyton on the floodplain and along water margins (Cressler 2006). Taphonomic and fossil-distribution evidence was derived from the systematic sampling of the floodplain pond deposit containing plant fossils that had undergone little or


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Table 1. Red Hill flora (classification scheme based on Stewart & Rothwell 1993) Plantae Tracheophyta Zosterophyllopsida Probarinophytales cf. Protobarinophyton sp. Barinophytales Barinophyton obscurum (Dun) White Barinophyton sibericum Petrosian Lycopsida Isoetales Otzinachsonia beerboweri Cressler and Pfefferkorn cf. Lepidodendropsis Lutz Filicopsida Zygopteridales Rhacophyton ceratangium Andrews and Phillips Stauropteridales Gillespiea randolphensis Erwin and Rothwell Progymnospermopsida Archaeopteridales Archaeopteris macilenta (Lesq.) Carluccio et al. Archaeopteris hibernica (Forbes) Dawson Archaeopteris obtusa Lesquereaux Archaeopteris halliana (Go¨ppert) Dawson Gymnospermopsida Pteridospermales cf. Aglosperma quadrapartita Hilton and Edwards Duodimidia pfefferkornii Cressler, Prestianni, and LePage

no transport. The evidence provided in the prior study was interpreted to support a model of habitat partitioning of the landscape by the plants at a high phylogenetic level, a characteristic of mid-Palaeozoic plant communities (DiMichele & Bateman 1996). The pattern of plant distribution at Red Hill was similar to that seen in other Late Devonian palaeoecological studies (Scheckler 1986a, b; Rothwell & Scheckler 1988; Scheckler et al. 1999). Lycopsids dominated the wettest portions of the floodplain, whereas Rhacophyton dominated the poorly drained floodplain margins. Archaeopteris grew in the better-drained areas of the landscape and seed plants grew opportunistically. At Red Hill they apparently flourished following fires that cleared the Rhacophyton groundcover. This is indicated by a succession of Rhacophyton-to-charcoal-to-spermatophyte remains within the small-scale stratigraphic profile (Cressler 2006).

The interpretation of distinct habitat-partitioning among the plants relies upon taphonomic and fossil distribution evidence and is thus indirect. Other studies further suggest a patchwork mosaic of monotypic stands of vegetation in the Late Devonian. For example, the dense accumulation of shed deciduous branches (Scheckler 1978; DiMichele et al. 1992) on the floor of Archaeopteris forests could have prevented or restricted understory growth. Palaeosol and root-trace distribution has been used to suggest that deeply-rooted Archaeopteris and shallowly rooted plants of other species were growing in different parts of the landscape (Retallack 1997).

Fire dynamics The occurrence of abundant charcoal at Red Hill is evidence of the importance of wildfires in the

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Fig. 6. Examples of floral and faunal elements from the fossiliferous zone: (a) Archaeopteris sp.; (b) spermatophyte cupule; (c) Rhacophyton ceratangium; (d) unidentified arthropod trackway; (e) Orsadesmus rubecollus; (f ) Gigantocharinus szatmaryi; (g) unidentified dipnoan toothplate; (h) Limnomis delaneyi; (i) unidentified rhizodontid sarcopterygian; (j) shoulder girdle of Hynerpeton bassetti. Black scale bars: 2 cm; white scale bars: 5 mm.


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Table 2. Red Hill fauna Animalia Chelicerata Arachnida Trigonotarbida Palaeocharinidae Gigantocharinus szatmaryi Shear Myriapoda Diplopoda Archidesmida Zanclodesmidae Orsadesmus rubecollus Wilson Vertebrata Placodermi Phyllolepida Phyllolepididae Phyllolepis rosimontina Lane and Cuffey Arthrodira Groenlandaspididae Groenlandaspis pennsylvanica Daeschler Turrisaspis elektor Daeschler Incertae Sedis Acanthodii Climatiiformes Gyracanthidae Gyracanthus cf. G. sherwoodi Newberry Chondrichthyes Ctenacanthiformes Ctenacanthidae Ctenacanthus sp. Insertae Sedis Ageleodus pectinatus (Agassiz) Osteichthyes Actinopterygii Palaeonisciformes Limnomis delaneyi Daeschler Sarcopterygii Dipnoi Indet. Crossopterygii Rhizodontidae cf. Sauripterus sp. Indet. Megalichthyidae Indet. Tristichopteridae Hyneria lindae Thomson Amphibia Ichthyostegalia Hynerpeton bassetti Daeschler Densignathus rowei Daeschler Whatcheeridae Indet.

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ecology of this early forest ecosystem (Cressler 2001, 2006). Previous work based on light microscope and SEM analysis of preserved xylem in the charcoal samples only showed evidence of Rhacophyton being burned in this landscape (Cressler 2001). An earlier ecological interpretation suggesting that the shallowly rooted Rhacophyton became desiccated during the dry season and became vulnerable to burning, whereas the deeply rooted Archaeopteris was relatively unaffected by fire, is perhaps unfounded. The abundance of small fragments of Rhacophyton-derived charcoal in the floodplain pond sediments reflects taphonomic sorting bias in the earlier sampling (Cressler 2001, 2006). Since these previous publications, a 2 cm piece of charcoal has been found in a sandstone lens at Red Hill that most likely came from Archaeopteris (Callixylon) wood. Furthermore, reflectance analysis on Red Hill charcoal (mean Ro ¼ 4.4%; mode ¼ 4.75%) indicates that the fires were predominantly 575 8C and within the temperature range of modern forest crown fires (Hawkins 2006). A similar phenomenon may have existed among Archaeopteris forests. Nevertheless, the pattern of centimetre-scale succession in the sampled plant horizon at Red Hill shows the appearance of spermatophytes following the burning of Rhacophyton in presumed ground fires on a local scale. Perhaps spermatophytes were able to establish themselves quickly in burned patches due to their unified sporophyte and gametophyte generations. Obstructions imposed on their airborne pollination mechanism by surrounding dense vegetation also would have been reduced. In any case, fire became an important factor in the dynamics of Late Devonian plant communities, contributing to the frequently changing spatio-temporal distribution of plants in the patchwork mosaic of this landscape.

Role of organic debris The increase in size and distribution of land plants in the Late Devonian increased the amount of organic matter available for burning, nutrient availability and burial in depositional systems (Algeo et al. 2001). Evidence for high organic detrital influx into the fluvial regime is readily apparent at Red Hill. Floodplain pond deposits contain a high density of organic matter consisting of well-preserved foliage and stems of plants, fragmented debris and charcoal. Many of the bedding surfaces within the reduced siltstone facies are dark in colour (Munsell N 4/*) due to organic content. Along with organic debris, mineral nutrients entered the aquatic ecosystem at an increased rate due to increased soil weathering by plants (Algeo & Scheckler 1998). Evidence for nutrient-laden

waters in the Catskill Delta system, and the microorganisms that were supported, can be found at other localities where dense concentrations of filter feeding bivalves (cf. Archanodon sp.) are preserved in living position (Remington et al. 2008). The increase in stature and rooting depth of riparian vegetation not only stabilized floodplains and affected the dynamics of channel and floodplain pond formation, but the influx of large plant debris into the aquatic ecosystem also had structural implications for underwater habitats. Smaller organisms had more complex areas in which to hide, and larger organisms had more complex substrates over and through which to move. While the influx of organic matter enriched these environments and supported diverse aquatic ecosystems, it also created enhanced conditions for anoxia (Algeo & Scheckler 1998).

Trophic structure of the Red Hill ecosystem The following is a hypothetical model of trophic relationships based on evidence from sedimentology, taphonomy and the interpretation of functional morphology. This model is necessarily simple in order to avoid over-interpretation. By the Late Devonian there was an increase in primary productivity on land that became a source of a large volume of organic debris that was metabolized by micro-organisms in freshwater ecosystems. Aquatic invertebrates were probably taking advantage of this resource, but the evidence at Red Hill is limited to the activity of trace makers. There is no evidence of herbivory on living plant tissues but detritivores are in evidence, including the myriapods Orsadesmus rubecollis (Fig. 6e) and a putative myriopod trackway (Fig. 6d). Predatory terrestrial invertebrates included the trigonotarbid Gigantocharinus szatmaryi (Fig. 6f ), as well as reported remains of scorpions which have not yet been described. Among vertebrates, the groenlandspidids Groenlandaspis pennsylvanicus and Turrisaspis elektor were small- to moderately-sized placoderms with ventrally oriented mouths suggesting that these animals were detritus feeders at the water –sediment interface. Their head-and-body shape also suggests a hydrodynamic design for staying close to the substrate. The same feeding mode also may apply to the phyllolepid placoderm, Phyllolepis rosimontina, which is less common at the site. The large gyracanthid acanthodian, Gyracanthus (cf. G. sherwoodi), was probably an open-water filter feeder, subsisting on primary producers and small primary consumers within the water column. The small chondrichthyan, Ageleodus pectinatus, is known only from isolated teeth found primarily in the microfossil taphofacies. The teeth show no sign of wear facets (Downs & Daeschler 2001) and the


autecology of this form is poorly known although the teeth reflect a function to process soft-bodied prey. The presence of a single dorsal fin spine of Ctenacanthus sp. suggests an aberrant occurrence of this chondrichthyan that is known primarily from marine deposits including the Cleveland Shale, a distal equivalent of the Catskill Formation. The palaeoniscid actinopterygian Limnomis delaneyi (Fig. 6h) was small (4–6 cm total length) and best preserved in the floodplain pond taphofacies where large numbers of articulated individuals have been collected. Some beds within the channel margin and microfossil taphofacies also contain a large amount of disarticulated material from L. delaneyi, or similar palaeoniscid(s). These primitive actinopterygians had sharp teeth and presumably ate small invertebrates and perhaps a variety of organic debris, providing an important link between the invertebrate and vertebrate components of the ecosystem. Dipnoan (lungfish) toothplates (Fig. 6g) are rare at Red Hill and have been found primarily in the potentially transported or reworked material of the microfossil taphofacies. Significant dipnoan skull material or scales have not been recognized. The tooth plates were presumably for a durophagous diet. Several articulated specimens of a distinctive rhizodontid sarcopterygian (Fig. 6i), not yet described, have only been recovered from the plant-rich siltstone of the floodplain pond taphofacies. These large (50 cm long) rhizodontids are the only articulated sarcopterygians known in this depositional setting. Its occurrence in pond sediments and the presence of large dentary, coronoid and palatal fangs imply that this rhizodont was a predator that specialized in ponded backwater settings on the floodplain. The remaining sarcopterygian fauna are also medium- to large-sized predators. At least one taxon of megalichthyid is present, although there is cosmine-covered skull material and scales that represent a range of body sizes with estimated total lengths 30–100 cm. The tristichopterid Hyneria lindae was the largest of the sarcopterygians, reaching a length of up to 3 m, and was the top predator in the ecosystem. This taxon may have fed upon all other fish and early tetrapod species. Although taphonomic bias due to preservational and collecting factors may influence the sample, the scales and teeth of H. lindae are among the most commonly encountered fossils at Red Hill. The early tetrapods were also predatory animals, eating fish and perhaps invertebrates. As with other coeval tetrapods, particularly those known from relatively complete remains such as Acanthostega gunnari and Ichthyostega sp., these animals probably relied on aquatic ecosystems and had a limited capacity for effective terrestrial locomotion.

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Red Hill is the only Late Devonian site that has produced at least three penecontemporaneous early tetrapod taxa (Daeschler et al. 2009). Densignathus rowei was the most robust taxon with a wide lower jaw including large coronoid fangs as found in more primitive tetrapodomorphs and some early tetrapods such as Ventastega curonica (Ahlberg et al. 1994, 2008; Daeschler 2000). The shoulder girdle of Hynerpeton bassetti (Fig. 6j) indicates a smaller taxon with a pectoral girdle similar to Acanthostega gunnari (Daeschler et al. 1994, 2009). Several small skull elements of a whatcheerid-like early tetrapod have recently been recognized. These indicate a more derived, steep-sided skull shape that may reflect modifications to the mechanics of respiration and prey capture (Daeschler et al. 2009). The diversity of early tetrapods at Red Hill, though known from only fragmentary material, indicates ecological specialization even at this early stage in tetrapod evolution. It seems likely such diversity is a reflection of the diverse ecological opportunities that were present on the floodplains where a range of habitats were formed by shifting geomorphic regimes and lowland vegetation. The Red Hill faunal assemblage is uniquely diverse in the Catskill Formation and includes several taxa that are not known from other sites in the formation. Also of interest is the notable absence of the antiarch placoderm Bothriolepis and the porolepiform sarcopterygian Holoptychius at Red Hill. Bothriolepis and Holoptychius remains are very common in most other Catskill Formation sites, and are common components of Late Devonian freshwater and marginal deposits around the world. The absence of these forms at Red Hill may be a reflection of the palaeoenvironmental setting rather than a significant biostratigraphic difference. As far as can be judged from palynomorph biostratigraphy, the Red Hill assemblage is the same age as many Bothriolepis and Holoptychius-bearing sites in the Catskill Formation and so we must conclude that the Red Hill ecosystem was not suitable for these taxa. The fact that Red Hill produces a unique fauna and that some taxa that are common at most other Catskill Formation sites are absent at Red Hill suggests that the palaeoenvironmental setting at Red Hill is rare among Catskill Formation sites.

Discussion Palaeobiogeographic distribution of the Red Hill flora and fauna Archaeopteris forests were distributed nearly globally and their fossil remains are known from nearly every sedimentary basin with Late Devonian terrestrial deposits. This includes many North

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American localities in the Appalachian Basin (Scheckler 1986b; Cressler 2006) as well as Alberta (Scheckler 1978) and Arctic Canada (Andrews et al. 1965); South American localities in Venezuela (Berry & Edwards 1996); Eurasian localities in Great Britain and Ireland (Chaloner et al. 1977), Belgium (Kenrick & Fairon-Demaret 1991), Svalbard (Nathorst 1900, 1902), Eastern Europe and Russia (Snigirevskaya 1988, 1995), Siberia (Petrosyan 1968) and China (Cai 1981, 1989; Cai et al. 1987); African localities in Morocco (Gaultier et al. 1996; Meyer-Berthaud et al. 1997) and South Africa (Anderson et al. 1995); Australian localities (White 1986); and possibly Antarctica (Retallack 1997). Archaeopteris, and to some extent Rhacophyton, are worldwide floral biomarkers for the Late Devonian. When considered with other floral elements, the plant assemblage at Red Hill most closely resembles coeval assemblages elsewhere in the Appalachian Basin, especially Elkins, West Virginia (Scheckler 1986c). They share many elements, including a variety of Archaeopteris species, Rhacophyton, Gillespiea, Barinophyton sibericum, arborescent lycopsids and spermatophytes. The Elkins locality is more diverse, preserving both sphenopsids and a cladoxylalean. Elkins is interpreted as a deltaic shoreline deposit (Scheckler 1986c) in contrast to the alluvial plain interpretation for Red Hill. Perhaps a more important factor in their similarity is their geographic and temporal proximity. The localities of the Evieux Formation in Belgium are also of coeval palynozones, and have the most similar plant assemblages to their North American counterparts (Kenrick & Fairon-Demaret 1991). Dispersal between these sites would have occurred over a single landmass during the Late Devonian. Such general and qualitative biogeographic assessments need to be followed by quantitative analyses of floral assemblage similarity to test further hypotheses of biogeographic origin and dispersal. Wilson et al. (2005) recognized Late Devonian biogeographic continuity in archipolypodan millipedes from the Euramerican landmass, including Orsadesmus rubecollus from Red Hill. The Appalachian vertebrate fauna has biogeographic affinities to Famennian sites from both the Euramerican and Gondwanan landmasses. These similarities are particularly striking with groenlandaspidid and phyllolepid placoderms, gyracanthid acanthodians, the chondrichthyan Ageleodus pectinatus and the large tristichopterid sarcopterygian, Hyneria lindae, which is closely related to Eusthenodon spp., a taxon with a global distribution in the Famennian. This cosmopolitan Famennian fish fauna is in contrast to Frasnian faunas in which the Euramerican and Gondwanan landmasses do not share significant elements. This pattern of Frasnian

endemism and Famennian cosmopolitanism is presumably a reflection of tectonic processes bringing Euramerican and Gondwanan landmasses into close enough contact to allow dispersal of organisms that were unable to cross marine barriers.

The use of ecological models to explain the origins of tetrapods This palaeoecological profile of the Red Hill site provides a view of the status of terrestrialization towards the end of the Late Devonian. The range of depositional settings at the site and the penecontemporaneous nature of the deposits provide a diversity of fossil evidence for the interpretation of a relatively in situ ecosystem. As seen here and in other Late Devonian deposits, plants had established complex communities by this time and invertebrates had a well-established terrestrial foothold. Even although many morphological characteristics important for terrestrial life had evolved among tetrapodomorphs, all vertebrates were still essentially aquatic. The conditions at Red Hill can more confidently be said to reflect selective pressures among tetrapodomorphs for life in shallow, obstructed and fluctuating waters rather than for full terrestriality. Multiple lines of evidence, as provided here, can help in the construction of palaeoecological models of the physical and biotic interactions in which early tetrapods evolved and diversified, eventually becoming fully terrestrial. By the Late Devonian, the extensively vegetated alluvial floodplains provided enhanced landscape stabilization by means of deeper rooting depth, habitat amelioration through shading, nutrient enrichment of adjacent waters and increased complexity of shallow water habitats through plant debris accumulation. The avulsion cycles created floodplain geomorphologic regimes that provided a dynamically shifting range of habitats, accompanied by an annual wet-and-dry seasonality that altered access to shallow water habitats and resources in the shorter term. This range of habitats includes shallow channel and wetland interfluve settings that supported productive ecosystems. Access to shallow water habitats could have provided a refuge for the earliest tetrapods to escape predation from larger (and perhaps faster swimming) sarcopterygians. The resources in these habitats may have been out of reach of most largebodied sarcopterygian predators, except for those that could navigate with appendages capable of support and locomotion across the shallow water substrates. Other morphological changes along the tetrapodomorph lineage, such as loss of scale cover and median fins and development of a neck, may also have been related to locomotion and


successful prey capture in these habitats (Daeschler et al. 2006). The hypotheses outlined above need to be tested further. As the study of tetrapod terrestriality proceeds, it will be necessary to develop palaeoecological models based on multiple lines of evidence including sedimentology, taphonomy, functional morphology, developmental biology, biogeochemistry and other disciplines that can be synthesized to provide a holistic picture of these ancient nonanalogue ecosystems.

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The biostratigraphical distribution of earliest tetrapods (Late Devonian): a revised version with comments on biodiversification A. BLIECK1*, G. CLE´MENT2 & M. STREEL3 1

Universite´ de Lille 1, Sciences de la Terre, FRE 3298 du CNRS, Geósyste`mes, Equipe de Paleóntologie et Paleógeógraphie du Paleózoı¨que (LP3), F-59655 Villeneuve d’Ascq cedex, France

2

Museúm national d’Histoire naturelle (MNHN), De´partement Histoire de la Terre, UMR 7207 du CNRS, Centre de Recherche sur la Paleóbiodiversite´ et les Paleóenvironnements, Case Postale 38, 57 rue Cuvier, F-75231 Paris cedex 05, France 3

Universite´ de Lie`ge, De´partement de Geólogie, Unite´ de recherche PaleóbotaniquePaleópalynologie-Micropaleóntologie, Sart Tilman, B18, B-4000 Lie`ge 1, Belgium *Corresponding author (e-mail: [email protected]) Abstract: The 13 presently known genera of Late Devonian tetrapods are situated in the recently completed miospore zonation of Western Gondwana and Euramerica, in relation to the standard conodont zonation. Some of them are still unprecisely dated. The stratigraphic sequences of East Greenland, North China and East Australia are briefly reviewed to discuss the age of the tetrapods collected there and to analyse consequences in relation to the Frasnian–Famennian and Devonian–Carboniferous boundaries. Two episodes of biodiversification seem to have occurred: the first in the Frasnian and the second in the late and latest Famennian. Due to the currently known fossil evidence, the consensus scenario advocates a late Middle Devonian to early Late Devonian origin of tetrapods on the Old Red Sandstone Continent (Euramerica) at a time of warm climate and recovering atmospheric oxygen level during the building of a pre-Pangaean configuration of landmasses.

The transition of life from water (either marine or fresh) to land, that is, terrestrialization, is certainly one of the most debated topics in evolutionary biology. Most recent results in palaeontology have shown that this event happened at various periods in Earth’s history: Precambrian for bacteria, fungi and algae involved in the first palaeosoils (e.g. Altinok 2006), Ordovician for land plants (Early Ordovician for cryptospores and Late Ordovician for trilete spores; see Steemans et al. 1996; Strother et al. 1996), Silurian (or earlier in the Cambrian– Ordovician) for many invertebrates (annelids, arthropods, etc.; see MacNaughton et al. 2002) and Devonian –Carboniferous for vertebrates. Here, we focus on the Late Devonian, the earliest phase of vertebrate terrestrialization, when limbed vertebrates with digits (i.e. tetrapods) first appeared in the fossil record. Several papers have recently reviewed various aspects of this earliest diversification of tetrapods either in terms of its palaeobiological context (e.g. Clack 1997, 2002, 2006, 2007; Schultze 1997, 2004; Ruta & Coates 2003; Ruta et al. 2003; Lebedev 2004; Long & Gordon 2004; Ahlberg et al. 2008) or its geological context (Young 2006;

Blieck et al. 2007). A correct evaluation of the first diversification and adaptive radiation of tetrapods is in need of a well-controlled biostratigraphical framework of its successive steps (accurate dating of the fossiliferous localities) (Blieck et al. 2007). We return to this necessary precise biostratigraphy because new data have since been published. We will also explore some of the consequences that this biostratigraphical framework has upon the interpretation of the biodiversity and radiation of earliest tetrapods after the most recently published phylogenetic analysis (Ahlberg et al. 2008).

Biostratigraphical distribution Blieck et al. (2007) have reviewed the Late Devonian tetrapod-bearing localities that have yielded bone remains (not the traces and trackways that are reviewed by Clack 1997, 2002). They commented upon the biostratigraphical dating of those localities to give the most precise ages possible to the various taxa of tetrapods. Among the oldest, three still have rather unprecise ages, namely: Sinostega (N. China) originally thought to be Famennian


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in age, but most probably Frasnian; Elginerpeton (Scotland) which is middle or late Frasnian in age; and Metaxygnathus (Australia) which is Frasnian or Famennian. All the taxa were plotted against the southeastern Euramerican miospore zonation (Blieck et al. 2007, fig. 1). However, new data have been published since that publication. Among them, the southeastern Euramerican miospore zonation has been completed for the transitional late Frasnian to early Famennian time slice (Streel 2009). The interval of informal biozones IV, V and poorly defined biozone GH used by Blieck et al. (2007, fig. 1) is replaced by the two newly defined Oppel Zones BA and DV (Fig. 1). The Oppel Zone BA is subdivided into three new interval zones. Its uppermost subdivision, the plicabilis interval zone, extends across the Frasnian – Famennian boundary (Streel 2009). Note that the vertical bars of Figure 1 (where the radiochronologic scale has been updated after Gradstein et al. 2004) do not correspond to the actual age distribution of tetrapods, but to the age duration of conodont or spore zones in which the taxa have been collected (Marshall et al. 1999). Because most early tetrapod finds are from only a single stratigraphical horizon, their fossil record is more

sparse than what is indicated by Figure 1. The exception to this is in East Greenland (for Ichthyostega, Acanthostega and the new genus and species) where the sampling has been much more abundant (review in Blom et al. 2007).

Comments on the East Greenland localities The recent paper of Blom et al. (2007) has reviewed the stratigraphical distribution of vertebrates in the Old Red Sandstone series of the east coast of Greenland and provides additional information on the age of the tetrapods. Fossiliferous localities are on Gauss Peninsula (Gauss Halvø) and Ymer Island (Ymer Ø). They have provided 50 different vertebrate taxa for the Middle and Upper Devonian (Blom et al. 2007, fig. 2), including the most diversified Late Devonian tetrapod fauna with Acanthostega gunnari, three species of Ichthyostega (I. stensioei, I. watsoni, I. eigili after the revision of Blom 2005) and a third, yet undescribed genus (Clack et al. 2004). Contrary to our proposal (Blieck et al. 2007, fig. 1), both Acanthostega and Ichthyostega have the same stratigraphical distribution which spans the upper part of the Famennian from the Aina

Fig. 1. Revised biostratigraphical distribution of Devonian tetrapods after Blieck et al. (2007). Each vertical bar illustrates the age duration of the conodont or miospore zones in which the corresponding taxon has been collected. Dashed lines with arrows indicate uncertainties in dates. (1) Radiochronologic scale of Gradstein et al. (2004, fig. 14.2); (2) standard conodont zones of Ziegler & Sandberg (1990, fig. 1); (3) older conodont zones after Ziegler & Sandberg (1990); and (4) miospore zones in the eastern part (now west Europe) of the south Euramerican area after Streel (2009). Palaeogeographic occurrences: C: North China; G: East Gondwana (Australia); all others are from the Old Red Sandstone Continent (Euramerica, Laurussia, Laureuropa).

LATE DEVONIAN TETRAPODS BIOSTRATIGRAPHY

Dal to the Britta Dal formations that have been correlated to the GF to LN spore zones (Marshall et al. 1999) (Fig. 1). The third tetrapod genus (Tetrapoda n. gen. et sp. on Fig. 1) is less securely dated; it comes from specimens collected on the south side of Celsius Bjerg, but it is not possible to assign these specimens to a precise stratigraphical level between the Aina Dal and the Britta Dal formations (see Blom et al. 2007, pp. 132 and 136; Clack et al. in press). The East Greenland series highlights a problem: some of the vertebrate material, including Holoptychius sp. and Groenlandaspis mirabilis, has been collected in the uppermost part of the series (Bendix-Almgreen 1976; Schultze 1993). The sixth assemblage or Gro¨nlandaspis Series (Blom et al. 2007, p. 136) is assumed to be earliest Carboniferous in age. This Gro¨nlandaspis Series or Gro¨nlandaspis Group is stratigraphically above the black shales (of the Obrutschew Bjerg Formation) containing actinopterygian material (Cuneognathus gardineri, Friedman & Blom 2006) which marks the Devonian –Carboniferous boundary on the south side of Celsius Bjerg (Marshall et al. 1999; Blom et al. 2007, pp. 128 –129). This would therefore correspond not only to the only record of these taxa (Holoptychius and Groenlandaspis) in the Carboniferous (Blom et al. 2007, p. 128), but also to the only record of post-Devonian porolepiform sarcopterygians and placoderms. This point concerns a more general problem of dating the last occurring placoderms which are usually assumed not to have survived the Devonian (see dating some of the Late Devonian Old Red Sandstone-like localities of Australia – references in Denison 1978; Long 1993; Young 1993, 2006, 2007). According to Blom et al. (2007), in East Greenland it is either a problem of taxonomic identification of the material or of dating the Devonian– Carboniferous boundary (DCB) in the stratigraphical sequence (or both). Indeed, the assertion that “the Devonian –Carboniferous boundary can be confidently placed within the Obrutschew Bjerg Formation” (Marshall et al. 2002) can be challenged. The miospore/conodont data in the Sauerland (Germany) demonstrate that the LN/VI miospore boundary level is clearly below but not at the DCB. The Obrutschew Bjerg Formation might well be entirely Devonian (Streel & Marshall 2006, table 2, level 15).

Comments on the North Chinese locality Zhu et al. (2002) have published a locality of Late Devonian age from the Ningxia autonomous region of NW China, with a partially preserved mandible called Sinostega. It comes from the Zhongning Formation which is classically

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considered Late Famennian in age (Pan et al. 1987). This formation is well known for its fish assemblage together with plants and miospores. The fish assemblage is known as the Sinolepis assemblage (Macrovertebrate Assemblage XI of Zhu et al. 2000) and it includes Galeaspida indet., Bothriolepis sp., Remigolepis major, R. microcephala, R. sp., R. xiangshanensis, R. xixiaensis, R. zhongmingensis, R. zhongweiensis, Sinolepis szei and Sarcopterygii indet (Pan et al. 1987; Zhu 2000). In this assemblage Sinolepis is a typically endemic placoderm genus for China and Australia (Ritchie et al. 1992). This assemblage with Remigolepis and Bothriolepis is comparable to that in east Greenland where it spans both the Frasnian and Famennian (Blom et al. 2007). Miospores have also been prepared from the Zhongning Formation and published by Gao (Pan et al. 1987). They come from the topmost part of the Shixiagou section (bed 27) of the Zhongning Formation, and thus constrain the age of the top of this formation. Among them, on a total of 32 species, some have a more significant biostratigraphical value such as Apiculatisporites microconus, Geminospora lemurata, Verruciretusispora magnifica and Archaeozonotriletes variabilis (Pan et al. 1987). The age of this assemblage is within the interval Mid Givetian to Frasnian (Ritchie et al. 1992) or probably Frasnian (S. Loboziak pers. comm., 1989) and not Famennian (Blieck et al. 2007). This dating of the Zhongning Formation has a consequence in the interpretation of the Frasnian – Famennian (FF) biotic event (crisis). If Famennian in age, the galeaspid of the Zhongning Formation would be the only post-Frasnian ostracoderm confirmed (e.g. Blieck 1991; Janvier & Blieck 1993; Janvier 1996). However, if the Zhongning Formation is Frasnian in age, as we believe, there is no post-Frasnian galeaspid in China, no postFrasnian ostracoderm worldwide and the FF event is an actual crisis for armoured jawless vertebrates.

Comments on the SE Australian localities Three tetrapod-bearing localities (two with trackways and one with Metaxygnathus; see Fig. 1) are known from the Devonian of Victoria and New South Wales, SE Australia (Young 2006, 2007). The Genoa River fish-tetrapod trackway assemblage (Bothriolepis sp., Remigolepis sp., Groenlandaspis sp., an osteolepiform and two tetrapod trackway types; Warren & Wakefield 1972; Clack 1997, 2002; Young 2007) comes from the Combyingbar Formation (formerly known as the Genoa River beds) of easternmost Victoria. This formation is aligned with the Twofold Bay Formation of southeastern-most New South Wales, and is therefore dated as Frasnian (Young 2007) as originally

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suggested by Warren & Wakefield (1972). The makers of the Genoa River trackways are unknown. The Metaxygnathus lower jaw comes from the Cloghnan Shale at Jemalong quarry, central New South Wales, very often cited as Famennian (Ahlberg & Clack 1998; Clack 2006; Young 2006). Associated with Metaxygnathus is a fish assemblage which includes Soederberghia groenlandica, Bothriolepis, Remigolepis, Groenlandaspis, phyllolepids and possibly holoptychiid scales. This fits very well with the lower part of the fifth assemblage of Blom et al. (2007), that is, the Remigolepis series which also yielded Acanthostega and Ichthyostega. This is dated as Famennian because of palynological data from above and below the formations of this series (Marshall et al. 1999; Blom et al. 2007, fig. 2). However, new geological mapping and lithostratigraphical correlations as well as comparison of the Jemalong fish-tetrapod fauna with the Canowindra fish assemblage (about 80 km east of Jemalong in New South Wales) led Young (2006) to suggest that the age of the Jemalong assemblage is not very different from that at Canowindra, and is also likely to be Frasnian. Both the Jemalong and Canowindra fish assemblages have been grouped by Young (1993) under the Macrovertebrate Fauna MAV13, originally dated as Famennian (Young 1993, fig. 9.2) and then considered as Frasnian (e.g. Young & Turner 2000, figs 2 & 3). We remain unconvinced by the Frasnian age of the Jemalong fauna which biostratigraphically correlates rather well with the fifth assemblage of Blom et al. (2007) and is more likely to be Famennian, and therefore consider the age of Metaxygnathus as unresolved (Fig. 1; Blieck et al. 2007). One of the consequences of the supposed Frasnian age of the Canowindra-Jemalong fauna is that it constitutes one of the arguments used by Young (2003) to indicate that several groups of placoderms (including bothriolepids and phyllolepids) dispersed from eastern Gondwana to Euramerica (Laurussia); they would indeed be older (Frasnian) in Gondwana than in Euramerica (Famennian). However, if older ages for some of the Australian faunas are not confirmed, this contradicts Young’s (2003) scenario. The third SE Australian locality which is assumed to have yielded Devonian tetrapod remains (a trackway) is the courtyard of Glenisla Homestead in the Grampians Mountains, western Victoria (Warren et al. 1986). The source of the courtyard flagstones and their age have recently been resolved: they come from the Major Mitchell Sandtone of the Grampians Group, underlying the Silverband Formation (Gouramanis et al. 2003; Young 2006) which yielded turiniid thelodont scales and poracanthodid acanthodian scales and tooth whorls suggestive of a Late Silurian to Lochkovian (Early Devonian) age (Turner 1986; Young

& Turner 2000, fig. 2 and p. 459: Microvertebrate Zone MV1; Burrow 2003). The Glenisla trackway is therefore either Late Silurian or earliest Devonian at the youngest (Young 2006, p. 418) and would be the oldest tetrapod remains known. The only problem with the above theory is that it may not be a tetrapod. For Clack (1997), the tetrapod interpretation is very doubtful due to the lack of symmetry of the trackway and the absence of clear alternation in its assumed manus and pes tracks. For Gouramanis et al. (2003), it is attributable to a Diplichnites species made by an arthropod. Doubt therefore remains on what type of animal may have formed this trackway (Young 2006). The proper identification of the Glenisla Homestead track maker will have a huge impact on interpretations of the origin of tetrapods as discussed below.

Earliest diversification of tetrapods The results of Figure 1 are used to plot the taxa included in the most recent phylogenetic (cladistic) analysis by Ahlberg et al. (2008). They are shown on Figure 2.

Comments on the origin of tetrapods As already commented by various authors, a consensus arose on the age of origin of tetrapods which, based upon presently available evidence, would be late Givetian to early Frasnian. The earliest known fossil bony elements of tetrapods are Frasnian in age, and the elpistostegid (panderichthyid) sarcopterygians (now considered as paraphyletic, but including Tiktaalik þ Elpistostege, the sister-group of tetrapods: (Daeschler et al. 2006, Ahlberg et al. 2008) are late Givetian at the oldest (Clack 2002, 2007; Schultze 2004; Blieck et al. 2007). However, the recent paper of Young (2006) has highlighted the unresolved trackway from Glenisla, Victoria (Australia), originally described by Warren et al. (1986) and thought to be Early Devonian or even Silurian in age. After new geological and palaeontological information published, the age of this trackway is confirmed as being either Late Silurian, or earliest Devonian at the youngest (Young 2006, p. 418). If confirmed as a tetrapod trackway, this would immediately introduce a long ghost range of ca. 30 Ma for the elpistostegids, from the Silurian –Devonian boundary to the late Givetian. Discussing uncertainties regarding the phylogenetic relationships of sarcopterygian fishes (including the rhizodontids, the osteolepiforms, the actinistians and basal taxa from the Lower Devonian of China), Young (2006) suggests the possibility

velifer

marginifera

marginifera

rhomboidea

rhomboidea

crepida

crepida

triangularis

triangularis

GF

G

DV

C

Hynerpeton

Tulerpeton

Ichthyostega

Tetrapoda n. gen. et sp . ?

(6) uppermost Famennian quick changing climate

upper Famennian climatic vs. correlation challenge

Obruchevichthys

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linguiformis

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Sinostega

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VI LN LE

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expansa

kockeli

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praesulcata

Acanthostega

CARBONIFEROUS (3) (4)

Ventastega

(2)

Elginerpeton

(1)

Densignathus


lower-middle Famennian vegetation crisis

BA late Frasnian warm climate

gigas

jamieae

A. triangularis

BM

asymmetricus

BJ

hassi punctata transitans

falsiovalis

GIVETIAN

TCo

Fig. 2. Chronological, phylogenetic and global (climatic) context of earliest diversification of tetrapods. (1)–(4): as for Figure 1; (5) phylogenetic relationships (after Ahlberg et al. 2008; Tetrapoda n. gen. et sp. is MGUH VP 6088; taxa which are not included in this phylogenetic analysis are kept aside on the right; and (6) southeastern Euramerican climatic conditions after Streel (2007a, b). Note that the so-called ‘upper Famennian climatic versus correlation challenge’ is not yet solved due to contradiction in the relation conodont/miospore in the western part (now USA) of the south Euramerican area.

that tetrapod origins could date back to the earliest differentiation of these major clades sometime in the Silurian –Early Devonian. Young considers this hypothesis as a plausible alternative hypothesis to the present paradigm of the elpistostegids including the sister-group of tetrapods. This alternative is, of course, strongly supported by the age of the Glenisla trackway. However, the Glenisla trackway may instead be that of a large arthropod (a type of misinterpretation already encountered for other tetrapod tracks, Clack 1997), disproving Young’s hypothesis. As shown on the phylogenetic relationships in Figure 2, the most basal tetrapods are from the Old Red Sandstone Continent (Euramerica). Sinostega, from the Frasnian of China, is too incomplete to be included in a phylogenetic analysis and Metaxygnathus, from the Frasnian or Famennian of Australia, is assumed to be more derived than Densignathus and Ventastega (Ahlberg et al. 2008). Because the sister-group of tetrapods, namely Panderichthys (Tiktaalik, Elpistostege) or elpistostegids, is exclusive to the same palaeocontinent (e.g. Daeschler et al. 2006), a consensus arose

on an out-of-Euramerica scenario for the origin of tetrapods (Clack 2002; Blieck et al. 2007). In seeking an alternative to the consensus hypothesis, Young (2006) recalled that Late Devonian tetrapods are very frequently collected among fish assemblages that include placoderms (phyllolepids and antiarchs – Remigolepis and Bothriolepis; Leriche 1931; Clack 2006, table 1 where the locality of Strud, Belgium, has no placoderm mentioned but did yield placoderms: Phyllolepis, Bothriolepis, and Groenlandaspis), acanthodians (gyracanthids a.o.), dipnoans (Soederberghia being significantly known from Euramerica and Australia, Ahlberg et al. 2001), porolepiforms (Holoptychius being the most widespread), osteolepiforms and others. Considering various hypotheses for the palaeogeographical origins of those taxa, Young (2006) concludes that ‘The various possibilities for faunal connection (“migration”, “dispersal”) between known tetrapod localities [his fig. 4] cannot be resolved on the available evidence’ and that we should focus again ‘on the possibility of a Gondwanan or Asian origin for the first land animals’.

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Sinostega is from North China and appears to be older than originally published (Fig. 1). If it also appears to be a very basal taxon (unsolved on Fig. 2), this could of course be used to sustain the Asian origin. Nevertheless, we should not forget that Elginerpeton, a limbed tetrapod, is already in Scotland in the Frasnian. We consider here that the presently known fossil evidence is in favour of the out-of-Euramerica hypothesis for tetrapods in the globally distributed exchange of fish-tetrapod faunas (now known as the Great Devonian Interchange) between the major Late Devonian landmasses (Young 2006, p. 423).

Comments on the biodiversity of Late Devonian tetrapods From data included in Figure 2, it seems that we are facing two episodes of diversification (one in the Frasnian and one in the late and latest Famennian) with a single record in between that is, Jakubsonia. All genera are monospecific except Ichthyostega (three species: Blom 2005), so that we would have four species for the Frasnian, one for the lower Famennian and ten for the upper-uppermost Famennian (Fig. 2). Even when removing the taxa which are not included in Ahlberg et al.’s (2008) phylogenetic analysis, two episodes of radiation appear: from the Frasnian and the late-latest Famennian. However, several critical remarks must be made: † As long as the phylogenetic relationships of several taxa are unknown, this scheme is incomplete. For example, Obruchevichthys is out from Ahlberg et al.’s (2008) scheme, but was considered as the sister-group of Elginerpeton in some earlier analyses (e.g. Ahlberg 1995; Schultze 2004) where it was an element of the most basal group of tetrapods and hence characterized their very first diversification. It would also be interesting to know what groups Sinostega (Zhu et al. 2002) and the ichthyostegid of Strud (Belgium: Cle´ment et al. 2004) are related to. † We know that the fossil record of early tetrapods is incomplete. Undescribed Late Devonian taxa are awaiting description (e.g. Clack et al. 2004, in press, pers. comm., 2007) and the ca. 15 Ma long interval with almost no tetrapod remains in the Lower Carboniferous (Romer’s Gap) may simply be due to a lack of fossil collection, related to the lack of suitable continental (stratigraphical) sequences for that period (Clack 2007, p. 11). This is perhaps also the case for the Lower Famennian. The apparent rarity of Early Famennian tetrapods might be a bias caused by lack of an extensive rock record

from that interval, compared to more abundant Frasnian and late Famennian units (E. B. Daeschler, pers. comm., 2007). † Most reviews of Late Devonian tetrapods usually include only those taxa named after preserved bony elements (e.g. Clack 2006, 2007; Ahlberg et al. 2008) because no phylogenetic analysis can be based upon tracks. Since the review of Clack (1997) it appears that a series of trackways are known from the Late Devonian and are still to be attributed to actual animals, making the fossil record (Figs 1 & 2) largely underestimated.

Comments on the global (climatic) context of earliest diversification of tetrapods Several attempts at correlating the origin and early diversification of tetrapods to global events have been made (e.g. Clack 2002, 2006, 2007; Long & Gordon 2004; Carroll et al. 2005; Ward et al. 2006). One recent tendency is to try to link this to climatic changes in relation to plate tectonic/orogenic global events. Late Devonian tetrapods occurred during a period of intense tectonic activity (Acadian–Ligerian orogeny) due to the collision of major landmasses, reduction of most oceanic domains and building of a pre-Pangaean configuration of the Earth (Averbuch et al. 2005; Blieck et al. 2007). At a global scale, the transition from fish to tetrapod occurred during the Givetian through Frasnian time slice which corresponds to a low level of atmospheric oxygen, rather high temperature (remember that the Givetian –Frasnian period corresponds to the maximum development of marine reefs in the fossil record) and a major time of plant diversification (increase in penetration depths of vascular plant roots in the soils and increase in the main axis diameter of land plants) (Ward et al. 2006; Algeo et al. 2007; Clack 2007). The earliest diversification of tetrapods is bracketed by the two first radiations of terrestrial arthropods: the first in the Early Devonian and the second in the Middle and Late Mississippian (Ward et al. 2006). However, putting such different events on a single diagram does not mean that there are causal relations between those events. For instance, when Ward et al. (2006, fig. 1) plot the earliest phases of diversification of terrestrial arthropods and of tetrapods together, they simply show that both phases apparently follow a period of low atmospheric oxygen rate which might be the trigger for the development of respiratory organs in air; it does not imply a trophic relation between terrestrial arthropods and earliest tetrapods which are now interpreted as aquatic animals (e.g. Clack 2002).


The earliest radiation of tetrapods is seen as a consequence of the increase in capacity of air breathing of their closely related fishes during a period of low oxygen rate (Clack 2007). After that episode, Frasnian –Famennian tetrapods radiated in a period of increasing oxygen level (Ward et al. 2006; Clack 2007) which might have some relation to the increasing rate of diversification of the vegetation (Streel 2007a, 2009). The earliest tetrapods are contemporaneous with a late Frasnian warm climate phase on West Gondwana and Euramerica while their second phase of diversification in the late and latest Famennian occurs in a period of rapid climatic changes with fast (c. 100 –200 ka long) sea-level changes (Fig. 2; Streel 2007a, b). The latter may have caused quick changes in the development of nearshore marine platforms and had impacts on the coastal plains and alluvial deposits with niches favourable to early tetrapods. However, such cooccurrences of events do not imply direct causal relationships between them. The global situation was certainly more complex and implied trophic relationships between the tetrapods and their locally associated fishes in very different environments from true freshwater to true coastal marine (e.g. Lebedev 2004). Between the two phases of biodiversification, the lower-middle Famennian vegetation crisis phase (Fig. 2) was controlled by a high climatic gradient between cool polar areas and a very warm, intertropical area (Streel 1992). This may have been unfavourable for the diversification of tetrapods, which are rare at that time.

Conclusions The primary aim of this paper is to update the biostratigraphical scale in which most of the Late Devonian tetrapod-bearing localities worldwide can be placed (Fig. 1). Uncertainties still remain for several basal taxa such as Elginerpeton, Metaxygnathus and Sinostega (if the latter is basal). As several taxa are very incompletely known (either solely as lower jaws e.g. Metaxygnathus, Sinostega and the ichthyostegid from Strud, or as trackways) they cannot yet be integrated in a general phylogenetic analysis (Fig. 2). Despite such limitations, a consensus scenario arises where tetrapods seem to have originated on Euramerica in the Middle to Late Devonian transitional period. This was a time of warm climate and increasing atmospheric oxygen level, during the building of a pre-Pangaean configuration of landmasses (Young 2006; Blieck et al. 2007). As is now well known for the fossil record in general (e.g. Sheehan 1977), such scenarios are the result of the interpretation of sparse

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fossil data from discontinuous surfaces of preserved sediments that have been sampled in an incomplete geographical frame (N. America, Europe, Australia and China in the case of earliest tetrapods). As pointed out by Young (2006), alternative hypotheses to the consensus scenario may be envisaged. It might be that the out-of-Euramerica scenario (Clack 2002) is simply the scenario for western palaeontologists. When reviewing the biostratigraphical ages of Late Devonian tetrapod-bearing localities, it appears that this has impacts on interpreting the Frasnian– Famennian (FF) biotic crisis and Devonian –Carboniferous (DC) event. Re-dating the Sinostega locality of N. China as Frasnian implies that there is no post-Frasnian ostracoderms (the galeaspid which comes from the same locality as Sinostega being also Frasnian, not Famennian) and that the FF crisis has been real for ostracoderms. Re-dating the East Greenland Middle to Late Devonian Old Red Sandstone sequence (Marshall et al. 1999; Blom et al. 2007) places the DCB in the Obrutschew Bjerg Formation. This implies that Groenlandaspis and Holoptychius still exist in the very Early Carboniferous, which is astonishing because placoderms and porolepiform sarcopterygians are usually thought to have disappeared before or at the DCB. This would mean that the DC event was not a total extinction for placoderms and porolepiforms, except if the DC boundary is higher in the East Greenland sequence. We thank P. E. Ahlberg (Uppsala University, Sweden) who provided us with the latest phylogenetic analysis of early tetrapods which was in press at the time of writing this paper (Ahlberg et al. 2008) and A. A. Warren (La Trobe University, Victoria, Australia) who sent a reprint of Gouramanis et al.’s (2003) paper. P. Janvier (CNRS, Paris) helped with information concerning the genus Groenlandaspis. This paper is a contribution to IGCP Project 491 (Middle Palaeozoic Vertebrate Biogeography, Palaeogeography and Climate) and to the ECLIPSE II Programme of CNRS ‘The terrestrialization process: modelling complex interactions at the biosphere-geosphere interface’. We also thank both referees J. A. Clack (Cambridge University, UK) and E. B. Daeschler (Academy of Natural Sciences of Philadelphia, Pennsylvania, USA).

Note added in proof While this paper was in the process of editing, Niedzwiedzki et al. (2010) have published a series of early Eifelian (Middle Devonian) tracks and trackways from the northern Lysogory region of the Holy Cross Maintains, Poland. This discovery confirms the recent paradigm that the earliest tetrapods have to be found before the Late Devonian, say at least in the Middle Devonian. This discovery as

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well as the re-appraisal of the supposed Early Devonian track from Australia (Warren et al. 1986) will be interpreted in another paper.

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Palaeoecological and palaeoenvironmental influences revealed by long-bone palaeohistology: the example of the Permian branchiosaurid Apateon SOPHIE SANCHEZ1,2*, J. SE´BASTIEN STEYER1, RAINER R. SCHOCH3 & ARMAND DE RICQLE`S4 1

UMR 5143 CNRS, De´partement Histoire de la Terre, Museúm national d’Histoire naturelle, CP 38, 57 rue Cuvier, 75005 Paris, France 2

UMR 7179 CNRS, De´partement Ecologie et Gestion de la Biodiversite´, Museúm national d’Histoire naturelle, CP 55, 55 rue Buffon, 75005 Paris, France 3

Palaöntologische Abteilung, Staatliches Museum fu¨r Naturkunde, Stuttgart, Germany

4

UMR 7179 CNRS, Case 7077, Colle`ge de France and Universite´ Pierre et Marie Curie, Paris 6, 2 place Jussieu, 75005, Paris, France *Corresponding author (e-mail: [email protected]) Abstract: Apateon, a small temnospondyl from the Permian freshwater-lake deposits of the SaarNahe Basin (SW Germany), is known by exceptionally well-preserved material. Here we report the first palaeohistological analysis of Apateon that focuses on its life-history traits and palaeoenvironments. Different samples (different localities and horizons) of Apateon caducus and Apateon pedestris have been analysed. Their stylopod histology shows different growth rhythms that might be correlated to changes in palaeoecosystems: food availability and/or presence of predators. Palaeoenvironmental influences are also recognized during the limb-bone osteogenesis by the expression of simple and/or double patterns of Lines of Arrested Growth (LAG). A doubleLAG pattern expresses hibernating and aestivating arrests of growth in extant newts. The fossil samples from the two stratigraphically oldest horizons preserved a similar double-LAG pattern, suggesting that they may have hibernated and aestivated every year because of harsh climatic conditions. The Saar-Nahe lake system probably passed from a higher altitude zone into a lower one, possibly because of subsidence and/or erosion. It could also be correlated to the size of the lakes that differs from one locality to another, inducing different responses of the organisms to the climatic variations.

Apateon Meyer, 1844 is a well-known dissorophoid from the Carboniferous and Permian of Europe (France, Germany and Czech Republic) (Boy 1972, 1987; Heyler 1994; Boy & Sues, 2000). Hundreds of well-preserved specimens, falling into different growth classes interpreted as growth series, have been collected in the Permian of Germany. This has permitted studies of the branchiosaurid anatomy (e.g. Boy 1986), palaeobiology (e.g. Boy & Sues 2000), ontogeny (Schoch 1992, 2004; Fro¨bisch et al. 2007), palaeoecology (e.g. Boy & Sues 2000; Werneburg 2002) and phylogeny among temnospondyls (e.g. Boy 1987; Steyer 2000). Branchiosaurids form a speciose clade probably closely related to the Amphibamidae (Schoch & Milner 2008), a group of small dissorophoids that has been hypothesized as lissamphibian stem-group by some authors (Milner 1993; Ruta et al. 2003; Schoch & Milner 2004) or at least closely related

to batrachians (Anderson 2007; Anderson et al. 2008). Regarding the palaeoecology of Apateon, numerous hypotheses have been put forward. Some of them suggest that this small aquatic branchiosaurid was an opportunist and adapted to lacustrine environments (e.g. A. pedestris) or even to mountainous streams (e.g. A. dracyiensis) (Werneburg 2002) according to the size of external gills and the body shape. It has also been considered as an R-strategist (Boy & Sues 2000; Werneburg 2002). So far, these palaeoecological inferences were exclusively based on anatomical and morphological features of Apateon in comparison with those of living amphibians. The palaeohistology of Apateon has never been observed, although the available material is very promising and would be an extraordinary source of information (Ricqle`s et al. 2004). Indeed, new data on time recording


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(e.g. Sanchez et al. 2008), biomechanics (e.g. Margerie et al. 2005), environments (e.g. Steyer et al. 2004) and development (e.g. Ricqle`s 1983) can be obtained from the study of the microstructural organization of bone. The current study is focused on the bone histology of a very well-preserved branchiosaurid material. This represents different taxa of Apateon, found in four different localities of three different stratigraphical horizons within the SaarNahe Basin. The objectives of these histological and skeletochronological analyses are: (1) analyse bone microstructure with respect to life-history traits of Apateon, and (2) elucidate the palaeoecology of this genus.

Materials and methods The material consists of growth series based on 21 specimens of Apateon from lacustrine environments of the Lower Permian of SW Germany (Scha¨fer & Sneh 1983; Boy & Sues 2000). The studied samples represent two species: Apateon caducus (n ¼ 6) and Apateon pedestris (n ¼ 15) (Table 1). They come from four localities of the Saar-Nahe Basin: Niederkirchen, n ¼ 7; Erdesbach, n ¼ 7; Odernheim, n ¼ 6; and Rehborn, n ¼ 1 (Table 1, Fig. 1). The four localities represent three different horizons within the Lower Permian section of the Lower Rotliegend (Autunian), falling within the Meisenheim Formation (Fig. 1). They range from the L-O-6-horizon (Niederkirchen) through L-O-7 (Erdesbach) to L-O-8 (Odernheim, Rehborn) (L-O: Lauterecken-Odernheim). L-O-6 and L-O-7 represented small lakes (5–10 km in diameter), while L-O-8 formed a large lake in the 70 –80 km range (Boy et al. 1990; Boy & Sues 2000). The specimens are housed in the collections of the Staatliches Museum fu¨r Naturkunde, Stuttgart (identified as SMNS or GPIM-N) and the Museum fu¨r Naturkunde, Berlin (identified as MB.Am.). Stylopods of the hind- and forelimbs were extracted from three-dimensionally preserved specimens. Limb bones were embedded in a polyester resin. Thin sections were made, using an annular diamond-powder saw, and were observed under ordinary and polarized light through an optical microscope (Nikon Eclipse 80i). Diaphyseal histology of 12 humeri and 9 femora was observed and analysed in the three sets of Apateon. Life history traits were advanced according to the interpretation of bone microstructural organization. A skeletochronological analysis was carried out to assess the individual ages and determine the longevity. This analysis was rigorously compared to the skeletochronological data obtained on extant tetrapods (Caetano et al. 1985; Caetano & Castanet

1993; Castanet et al. 1993). When some inner cortical regions of the bone shafts were resorbed in oldest individuals, the somatic age was assessed by retrocalculation that is, taking into account the position of the LAGs deposited during the early life in the innermost region of the periosteal cortex and observable in juveniles (e.g. Leclair & Castanet 1987; Castanet et al. 2003).

Mid-shaft palaeohistology and bone deposition in the stylopods of Apateon taxa Stylopod diaphyseal histology Apateon pedestris from Odernheim. Humerus (Fig. 2a): The diameter of the forelimb-stylopod at mid-shaft ranges from 280 to 650 mm (Table 1). The cortex is relatively thick (up to 300 mm thick in the largest individual SMNS 54988, Table 1). However, the marrow cavity is distinct and free of any bone trabeculae. The periosteal cortical tissue, made of primary bone, is rather compact. It is only involved by a primary sparse vascularization, essentially longitudinally oriented. The vascular canals are mostly distributed in the innermost half of the periosteal cortex. Numerous relatively large and flattened osteocytic lacunae, with canaliculi, are associated with lamellar tissues. These bone-cell lacunae become rounder toward the periphery. Some remodelling processes occur at the periphery of the medullary cavity: the residual line left by the endosteal resorption irregularly delimits the small endosteal deposition from the rest of the cortex. This endosteal deposition comprises fine lamellar bone. The Katschenko’s line, which constitutes some remains of the former cartilaginous shaft (Castanet et al. 2003), is still present in large individuals such as SMNS 54981. Femur: The diameter of the femoral diaphysis varies from 435 to 720 mm (Table 1). The cortex is thick (up to 320 mm thick in the largest individual SMNS 54980, Table 1). The marrow cavity remains empty. The periosteal bone is made of a primary bone matrix. It is crossed by a poor vascularization, essentially constituted of large longitudinal vascular canals homogeneously distributed in the thickness of the compacta. The density of osteocytic lacunae is relatively high. They are mostly flattened. A centripetal bone deposition forms a thin endosteal layer made of lamellar bone, which is separated from the periosteal bone by the Katschenko’s line. Apateon caducus from Erdesbach. Humerus (Fig. 2b): The bone diameter of humeral mid-shafts varies from 375 to 570 mm (Table 1). The diaphyseal cortex is thick (up to 260 mm thick in the largest individual GPIM-N 1572, Table 1), not allowing an expanded medullary cavity which

Table 1. Summary of the LAG account and LAG pattern of each specimen (the skull length is used as a measure of reference for body size) Locality

Niederkirchen

Apateon pedestris

Apateon caducus

Individual

Skull length (cm)

Long bone in which LAG pattern is observed

Diaphyseal diameter (mm)

Cortical thickness (mm) not totally preserved not totally preserved not totally preserved not totally preserved 210 180 not totally preserved

LAG account

GPIM-N 1471

0.5

Humerus

flattened

SMNS 55016

0.6

Femur

flattened

SMNS 55019

0.7

Femur

flattened

MB.Am.1247

0.7

Femur

flattened

SMNS 55018 SMNS 55017 SMNS 55015

0.8 – 0.8

Humerus Humerus Femur

580 500 flattened

GPIM-N 1589

0.6

Humerus

375

GPIM-N 1680

0.7

Femur

415

GPIM-N 1560

1.3

Humerus

flattened

GPIM-N 1297 GPIM-N 1572

1.5 estimated around 1.6

Humerus Humerus

550 570

not totally preserved not totally preserved not totally preserved 220 260

GPIM-N 1602

1.8

Humerus

flattened

250

13

LAG pattern

Age estimation

4

doubling

2

3 visible LAGs in periphery indeterminable

doubling

3

indeterminable

4

1 visible LAG in periphery 11 17 12 visible LAGs in periphery

indeterminable

incomplete

doubling doubling doubling

6 9 incomplete

6

doubling

3

4 visible LAGs in periphery indeterminable

doubling

4

indeterminable

indeterminable

simple doubling pattern ending in a simple pattern doubling pattern ending in a simple pattern

6 7

6 11

8

Erdesbach

Apateon pedestris

GPIM-N 1389

0.6

Humerus

285

not totally preserved

2

simple

2

Odernheim

Apateon pedestris

SMNS 54963 SMNS 56136 A

0.8 0.8

Humerus Femur

280 435

4 6

0.8

Humerus

flattened

simple

incomplete

SMNS 54981 SMNS 54988 SMNS 54980

0.9 1.1 –

Femur Humerus Femur

590 650 720

4 3 visible LAGs in periphery 2 visible LAGs in periphery 7 7 6

simple simple

SMNS 56136 B

75 not totally preserved not totally preserved 240 300 320

simple simple simple

7 7 6

MB.Am.1217

–

Femur

flattened

not totally preserved

4 visible LAGs in periphery

simple

5

Rehborn

Apateon pedestris

141

“ –” skull of fossil specimen is not conserved.

ECOLOGICAL INFLUENCES ON LIMB HISTOLOGY

Erdesbach

Species

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Fig. 1. Localization of the studied localities (Odernheim, Rehborn, Erdesbach and Niederkirchen) of the Saar-Nahe Basin in Germany, through geological time. (a) Stratigraphical range chart giving the relative age of the localities among the Late Carboniferous and Early Permian formations discovered in the Saar-Nahe Basin; and (b) geological map placing the localities within the Saar-Nahe Basin.


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Fig. 2. Humeral diaphyseal bone histology of representative specimens among the largest of each Apateon taxa from the Permian of the Saar-Nahe Basin, Germany. (a) Apateon pedestris (SMNS 54988, skull length SL 1.06 cm) from Odernheim; (b) Apateon caducus (GPIM-N 1572, SL ¼ 1.6 cm) from Erdesbach and (c) Apateon pedestris (SMNS 55018, SL ¼ 0.76 cm) from Niederkirchen (b.t.: bone trabecula; e.b.: endosteal bone; LAGs: lines of arrested growth; o.: osteocytes; v.: vascularization). Scale bars of thin sections: 0.1 mm; scale bars of fossil specimens: 1 cm.

remains free of trabeculae. The periosteal cortex comprises primary bone tissue and the matrix is essentially of lamellar bone. It contains numerous round osteocytic lacunae, which are of the same shape and size all along the cortex. The vascularization, predominantly longitudinal (sometimes radially arranged), is relatively dense and the larger canals are mostly located in the deepest part of the cortex. In the periphery of the marrow cavity, a secondary endosteal deposition made of lamellar bone is highlighted by a line of resorption. The Katschenko’s line is preserved between this endosteal layer and the periosteal cortex. Femur: Only femoral cross-sections of one juvenile were available for this histological study. The diaphyseal diameter is of 415 mm (GPIM-N 1680, Table 1). The cortex is not totally preserved, preventing the complete cortical thickness, the shape of the medullary cavity and the amount of remodelling from being estimated. Even if only the peripheral region of the cortex is still preserved, it is nevertheless informative as it is constituted of lamellar bone and remnants of calcified cartilage; it shows relatively large and flattened osteocytic lacunae but no vascularization. A. pedestris from Niederkirchen. Humerus (Fig. 2c): Mid-shaft sections show diameters ranging from 500 to 580 mm (Table 1). The stylopod cortex is rather thick at the diaphyseal level (up to 210 mm thick in the largest individual SMNS 55018, Table 1). The marrow cavity is therefore relatively small and free from any medullary trabeculae. The periosteal cortex, made of lamellar bone, is very compact. Very few small primary osteons (e.g.

only two in the humerus of SMNS 55018) run longitudinally, essentially in the area situated at mid-thickness of the cortex. The numerous oval osteocytic lacunae are randomly localized. Against the medullary wall, the endosteal coating is very thin. There is no Katschenko’s line. Femur: The femoral diaphyseal sections are too flattened to allow a significant estimation of the diameter. Nevertheless, the cortex is relatively thick (at 155 mm thickness in the largest individual SMNS 55015), even if not completely preserved. The innermost cortical region is not preserved in any thin section. The preserved compacta is made of lamellar bone and crossed by one longitudinal primary vascular canal in SMNS 55015. The osteocytic lacunae are flattened and homogeneously distributed in the periosteal cortex.

Differential diaphyseal bone-growth features The organization of different bone microstructures is representative of the bone-growth rate such as the density, size and shape of the cellular bone lacunae and the density of vascularization (Amprino 1947). When the diaphyseal bone deposition is relatively slow, bone cells are mostly flattened and the vascularization is reduced or absent. When the diaphyseal bone deposition is relatively fast, bone cells are rounder, more numerous and the vascularization is fairly denser. According to these criteria, it is suggested that the mid-shaft bone deposition in the stylopod long-bones of A. caducus was actually faster than in the long-bones of both sets of A. pedestris. The cellular shape would suggest a slightly

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Fig. 3. (a)–(c) Skeletochronological evidences in the cortical assemblages arranged from the youngest individual to the oldest (as oriented by the curved arrows) of diaphyseal thin sections, made in limb bones of Apateon taxa from the Permian of the Saar-Nahe Basin, Germany (scale bars of arrangements: 0.1 mm; of detailed thin sections: 0.5 mm) and (d) their distribution. (a) Apateon pedestris from Odernheim (humeral cortices of SMNS 54963, SMNS 56136 B, SMNS 54988; femoral cortices of SMNS 56136 A, SMNS 54980, SMNS 54981); femoral (F) and humeral (H) sections bring the same skeletochronological information and can therefore be used without any discrimination to assess the age of individuals. (b) Apateon caducus from Erdesbach (humeral or femoral cortices of GPIM-N 1589, GPIM-N 1680, GPIM-N 1560, GPIM-N 1297, GPIM-N 1572, GPIM-N 1602); and (c) Apateon pedestris from Niederkirchen (humeral or femoral cortices of GPIM-N 1471, SMNS 55016, SMNS 55019, SMNS 55018, SMNS 55017, SMNS 55015).


faster bone deposition in the set from Niederkirchen than in that from Odernheim.

Skeletochronological analysis Growth marks are well preserved at the diaphyseal level (Fig. 3), allowing a skeletochronological analysis. Allochronies (Castanet et al. 1996a) between limb bones in Apateon do not permit a skeletochronological analysis of every bone. Thus, only stylopod long-bones (humerus and femur) of Apateon species have been indifferently used as bones of reference to account for the total number of growth marks. Lines of arrested growth (LAGs), usually bordering each growth mark, are structures expressing a stop during the osteogenesis followed by a sudden resumption of growth. They are expressed among living poikilotherms during annual aestivations and/or hibernations (Castanet 1985; Castanet et al. 1993). LAG patterns in long bones of Apateon are similar to those of living tetrapods, indicating that one LAG in Apateon may also have been the consequence of a quiescent osteogenesis occurring during a lethargic period. Usually, extant tetrapods only enter into a lethargic period once a year (Castanet et al. 1996b; Bruce & Castanet 2006). They therefore express annually a so-called ‘simple-LAG pattern’. However, it was shown that some extant newt populations of Triturus marmoratus hibernate and aestivate each year (e.g. Caetano & Castanet 1993). In this case, such cyclical life habits are reflected by a peculiar spatial pattern of growth marks in the limb bones called the ‘doubleLAG pattern’; this indicates two phases of growth and lethargy per year (Caetano et al. 1985).

Identification of LAG patterns in individuals from different localities Odernheim and Rehborn (L-O-8-horizon). All the sampled specimens from Odernheim (n ¼ 6) and Rehborn (n ¼ 1) belong to A. pedestris (Table 1). They all show a simple-LAG pattern (in humerus and femur; Figs 2a & 3a, d), reflecting only one quiescent phase of osteogenesis per year. Consequently, these specimens underwent only one reduction of growth-rate per year, expressing a

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period of torpor (hibernation or aestivation) annually. Erdesbach (L-O-7-horizon). One specimen of A. pedestris from Erdesbach presents a simple-LAG pattern (Fig. 3d). However, all the studied specimens of A. caducus from Erdesbach have limb-bone diaphyseal cortices that sometimes express simple LAGs and, in other circumstances, double LAGs. In the latter case, a pattern showing distinct pairs of LAGs (Figs 2b & 3b, d) can be observed, suggesting two arrests of growth per year. Such a double-LAG pattern has already been observed in extant populations of T. marmoratus from high elevations that undergo two periods of drastic environmental conditions every year, forcing them to annually hibernate and aestivate (Caetano et al. 1985; Caetano & Castanet 1993). This suggests that the specimens from Erdesbach presenting a double-LAG pattern needed to stop their growth twice per year (to aestivate and hibernate) because of peculiar and perhaps drastic environmental conditions (Figs 2b & 3b, d). Niederkirchen (L-O-6-horizon). All the specimens of A. pedestris from Niederkirchen show a doubleLAG pattern (Figs 2c & 3c, d), which again suggests that they hibernated and aestivated throughout their development.

Determination of the individual age The age of these fossil individuals can be assessed by skeletochronology in the same way as it is used to estimate the somatic age of living tetrapods. Indeed, the LAG patterns observed in long bones of Apateon’s individuals are identical to that of small extant tetrapods. This allows us to consider that one growth mark, that is, one LAG and the immediately neighbouring bone layer record, is the time during which a seasonal and biological cycle was achieved; this is usually equivalent to one calendar year (Castanet et al. 1993). However, there are peculiar ecological situations in which one biological yearly cycle is split by two close arrests of osteogenesis, that is, expressed by two close LAGs in extant tetrapods (corresponding to aestivation and hibernation; e.g. Caetano et al.

Fig. 3. (Continued) Annual biological cycles indicated by LAGs (e.g. (a) SMNS 54988, (b) GPIM-N 1572 and (c) SMNS 55018) are highlighted by the small black and white arrows. When the cortices are incomplete, the position of LAGs of annual cycles are reconstructed by dotted lines, thereby allowing a retrocalculation to estimate the somatic age. (d) Comparison of the different LAG patterns observed in limb bones of few samples of Apateon taxa (A. pedestris and A. caducus) from the Permian of the Saar-Nahe Basin, Germany. Individuals from Niederkirchen (humerus of SMNS 55018) always present a double-LAG pattern; from Erdesbach (humeri of GPIM-N 1389 and GPIM-N 1572) both a double- and simple-LAG patterns; from Odernheim (femur of SMNS 54980) and Rehborn (femur of MB.Am.1217) always a simple LAG pattern (scale bars of thin sections: 0.1 mm).

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1985). The expression of this double-LAG pattern leads to the assessment of the somatic age on the basis of accounting two LAGs per year. A. pedestris from Odernheim. The skeletochronological analysis shows that the number of growth marks in this set of A. pedestris varies between four and seven (Fig. 3a). This indicates that the youngest specimen (SMNS 54963) was at least four years old whereas the oldest one (SMNS 54988) was at least seven years old when it died. A. caducus from Erdesbach. According to the skeletochronological analysis, the number of growth marks varies from three to eight (Fig. 3b), suggesting that the youngest specimen (GPIM-N 1589) was three years old whereas the oldest one (GPIM-N 1602) was eight years old when it died. A. pedestris from Niederkirchen. The earliest individual was two years old when it died (GPIM-N 1471) and the oldest one was nine years old (SMNS 55017).

Palaeoecological and palaeoclimatic implications Most authors agree with the fact that the Saar-Nahe and adjacent basins held intermountainous positions within the vast Variscan Orogen, at an altitude of at least several hundred metres (Ziegler & Gibbs 1996). Schultze & Soler-Gijoń (2004) suggested a marine influence on the sediments of the Saar-Nahe Basin, inferred largely from the ecological preferences of modern sharks. However, as the fossil amphibians could have lived in various water environments (from freshwater to marine environments; Steyer 2002), we prefer to leave this question of the marine influence unanswered. From a geological perspective, there is little doubt that the SaarNahe Basin was levelled at high altitude and was indeed lacustrine (Scha¨fer & Stamm 1989; Boy and Sues 2000), but we do not exclude any episodic marine influence by storms, tsunamis, winds, etc. (as this would depend on various factors such as topography, distance from the coast, climate, etc.). As the Saar-Nahe Basin was situated in the tropics during the Late Carboniferous and Early Permian (Poplin 1994; Fluteau 2003; Roscher & Schneider 2006), the studied branchiosaurid samples represent populations that inhabited the same large-scale climatic zone. These populations fall in three different time slices (L-O-6, L-O-7, L-O-8 of Meisenheim Formation) that might have spanned a total time interval of around one million years (Fig. 1). Bone microstructures and LAG patterns, which differ between the studied samples (Fig. 3d), may

add complementary suggestions to the current knowledge on the palaeoecological, palaeoaltitudinal and palaeoclimatic reconstructions of the basin.

Palaeoecological influence on bone growth of studied populations The current histological data show some variations in the diaphyseal bone-growth rate that could partially explain the body size differences between the studied taxa; the specimens of A. caducus from Erdesbach are on average larger than those of A. pedestris from Odernheim and Niederkirchen. Moreover, it seems that these bone-growth differences could also be correlated with the different palaeoecological living conditions of the sampled populations. Indeed, Boy (1977, 1987) and Boy et al. (1990) concluded that the Niederkirchen lake (L-O-6) and the Erdesbach lake (L-O-7) were probably rich in planktonic nutrients. However, the Niederkirchen lake was dominated by large sharks while the Odernheim lake (L-O-8) (even if large and dominated by small temnospondyls) offered poorer living conditions. Hence, the differences in bone-growth rate might also reveal differences in overall living conditions of the freshwater lakes, especially regarding food supply and trophic chain.

Palaeoclimatic influence on biological cycles of Apateon individuals All the specimens from Odernheim (A. pedestris) show a simple-LAG pattern whereas the specimens from Erdesbach (A. caducus and A. pedestris) sometimes show double LAGs. The sampled set of A. pedestris from Niederkirchen throughout preserves a double-LAG pattern. Finally, the populations from Rehborn (A. pedestris), even if represented by a very tiny sample, seem to express a simple LAG pattern (Fig. 3d). Different hypotheses (described below), or their combination, could explain the observed localityspecific variation in LAG patterns. Clines of palaeoenvironmental conditions through geological time. A skeletochronological study has been conducted on low- and high-elevation populations of the extant newt T. marmoratus from the Northern Mountains (National Park of Peneda Gereˆs) of Portugal (Caetano et al. 1985; Caetano & Castanet 1993). This skeletochronological analysis showed that populations living at elevations of 1.5 km hibernate during winters because of the very low local temperature and aestivate during summers because of high temperature and drought. However, populations living at elevations between 650 m and 1 km only sometimes show a


double-LAG pattern, indicating occasional drastic climatic conditions. At elevations of lower than 550 m, the newt populations do not encounter such ecological conditions and only hibernate each year. A similar situation could explain the different LAG patterns observed in the studied lacustrine populations of Apateon. It can be assumed that Niederkirchen (which yielded individuals with a double-LAG pattern) may have been at a higher elevation than Erdesbach (which yielded individuals with only occasional double LAGs), which may have been at a higher elevation than Odernheim and Rehborn (where no individuals present any double-LAG patterns). Such data are consistent with the current model on the Variscan orogen (Wagner & Lyons 1995) and the Rotliegend lake systems (Scha¨fer & Stamm 1989; Stapf 1989), where elevations of up to 2 km have been calculated in the palaeoaltitudinal models (e.g. Ziegler & Gibbs 1996). The crucial point is that these localities also represent different stratigraphical time intervals (Fig. 1). When they are ranked according to their stratigraphical age, Niederkirchen, which is hypothesized to be at the highest altitude, is the oldest locality (L-O-6). Erdesbach has an intermediate age (L-O-7) and altitude while Odernheim and Rehborn are both the youngest localities (L-O-8), which are also assumed to be at the lowest altitude. This may indicate that during their existence, the Saar-Nahe lake systems probably passed from a higher altitude climatic zone to a lower one, possibly because of subsidence and/or erosion. According to this scheme, this would have occurred 297 million years ago throughout a period lasting one million years. The double-LAG pattern also suggests a significant seasonality in the tropical Saar-Nahe Basin. This palaeoclimatic scenario should of course be tested with further bone sections of different vertebrates from the Saar-Nahe fauna. However, up to now, sedimentological (Schneider & Gebhardt 1993; Clausing & Boy 2000) and palaeobotanical (Ziegler 1990) analyses of this Carboniferous– Permian European basin have supported the hypothesis of a strong seasonality. Changes in palaeoecological conditions. The palaeoecology of the lakes from the different localities has been studied by Boy (1977, 1987) and Boy et al. (1990) who concluded that the Niederkirchen lake (L-O-6) was rather deep and small (10 km) while the Odernheim lake was much larger (70– 80 km). The Erdesbach lake was probably intermediate in size and similar to the (stratigraphically much younger) Kappeln lake described by Boy (1987). In this context, the current skeletochronological data would suggest

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that the palaeoecosystem of the small lake from Niederkirchen would be more responsive to high climatic fluctuations (obliging populations of Apateon to hibernate and aestivate) while the palaeoecosystems of Erdesbach, and more particularly Odernheim, were more stable (less sensitive to seasonal variations), because of their respective sizes.

Conclusions Bone histology and skeletochronology of Apateon, an abundant Carboniferous and Permian dissorophoid temnospondyl from Europe, have been analysed for the first time. This analysis is based on extensive samples of well-preserved growth series of A. pedestris and A. caducus from the Lower Permian of the Saar-Nahe Basin, Germany. It completes previous anatomical data by assessing the somatic age and the growth rhythms. Moreover, this analysis also allows a better understanding of the life-history traits of this key dissorophoid, often considered to be phylogenetically close to lissamphibians. The diaphyseal LAG organization of Apateon is similar to that of extant urodeles and shows a double-LAG pattern in some populations, similar to that of individuals of T. marmoratus living at relatively high altitudes in the Portuguese mountains. The latter hibernate and aestivate every year because of the strongly seasonal climate. This therefore suggests (1) some populations of Apateon could probably have hibernated and aestivated every Permian year; (2) the specimens presume a relatively high palaeoaltitude of the fossiliferous localities where they come from (especially Niederkirchen and Erdesbach); (3) the probable occurrence of subsidence or erosion 297 million years ago; (4) the confirmation of palaeoecological variations in the different lacustrine systems; and (5) a strongly seasonal local palaeoclimate. (Points 2, 4 and 5 are confirmed by sedimentological and palaeobotanical studies on the Saar-Nahe Basin.) This is the first time that a bone palaeohistological analysis has such clear implications for palaeoenvironments, landscapes and palaeoclimates. The authors acknowledge the Museum fu¨r Naturkunde (Berlin, curator O. Hampe) for providing a part of the fossil material and allowing the material from the collections to be sectioned; A. Abourachid (Museúm national d’Histoire naturelle and UMR 7179, Paris) for support; B. Le Dimet and M. Lemoine (Museúm national d’Histoire naturelle and UMR 5143, Paris) for casting the specimens and preparing thin sections; P. Loubry (Museúm national d’Histoire naturelle and UMR 5143, Paris) for the pictures of the specimens; T. Schindler (Landesamt fu¨r Denkmalpflege, Mainz) and R. Weitz (Germany) for fruitful

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comments; and A. Milner and F. Witzmann for their reviews which improved the manuscript. SS was funded by a Research Fellowship of the Ministry of Education and Research (MENRT, France), by the Synthesys European Program for the visit of the Museum fu¨r Naturkunde (Berlin) and by the UMR 7179 and UMR 5143 (CNRS, Paris) for the visits to the Staatliches Museum fu¨r Naturkunde (Stuttgart).

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ECOLOGICAL INFLUENCES ON LIMB HISTOLOGY Ricqle`s, A. De. 1983. Cyclical growth in the long limb bones of a Sauropod dinosaur. Acta Palaeontologica Polonica, 28, 225 –232. Ricqle`s, A. De., Castanet, J. & Francillon-Vieillot, H. 2004. The ‘message’ of bone tissue in paleoherpetology. Italian Journal of Zoology Suppl., 1, 3– 12. Roscher, M. & Schneider, J. W. 2006. PermoCarboniferous climate: Early Pennsylvanian to Late Permian climate development of central Europe in a regional and global context. In: Lucas, S. G., Cassinis, G. & Schneider, J. W. (eds) Non– Marine Permian Biostratigraphy and Biochronology. The Geological Society, London, 95– 136. Ruta, M., Jeffery, J. E. & Coates, M. I. 2003. A supertree of early tetrapods. Proceedings of the Royal Society of London, Series B 270, 2507– 2516. Sanchez, S., Klembara, J., Castanet, J. & Steyer, J.-S. 2008. Salamander-like development in a seymouriamorph revealed by palaeohistology. Biology Letters, 4, 411–414. Scha¨fer, A. & Sneh, A. 1983. Lower Rotliegend fluviolacustrine sequences in the Saar-Nahe Basin. International Journal of Earth Sciences, 72, 1135–1145. Scha¨fer, A. & Stamm, R. 1989. Lakustrine Sedimente im Permokarbon des Saar-Nahe-Beckens. Zeitschrift der Deutschen Geologischen Gesellschaft, 140, 259 –276. Schneider, J. W. & Gebhardt, U. 1993. Litho- und Biofaziesmuster in intra- und extramontanen Senken des Rotliegend (Perm, Nord- und Ostdeutschland). Geologisches Jahrbuch A, 131, 57–98. Schoch, R. R. 1992. Comparative ontogeny of Early Permian Branchiosaurid amphibians from Southwestern Germany: Developmental Stages. Palaeontographica Abteilung A 222, 43–83. Schoch, R. R. 2004. Skeleton Formation in the Branchiosauridae: a case study in comparing ontogenetic trajectories. Journal of Vertebrate Paleontology, 24, 309–319. Schoch, R. R. & Milner, A. R. 2004. Structure and implications of theories on the origin of lissamphibians. In: Arratia, G., Wilson, M. V. H. & Cloutier, R. (eds) Recent Advances in the Origin and Early Radiation of Vertebrates. Verlag Dr. Friedrich Pfeil, Mu¨nchen, 345–377.

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Schoch, R. R. & Milner, A. R. 2008. The interrelationships of the Permo-Carboniferous temnospondyl family Branchiosauridae. Journal of Systematic Palaeontology, 6, 409– 431. Schultze, H. P. & Soler-Gijoń, R. 2004. A xenacanth clasper from the ?uppermost Carboniferous-Lower Permian of Buxie`res-les-mines (Massif Central, France) and the palaeoecology of the European PermoCarboniferous basins. Neues Jahrbuch fu¨r Geologie und Palaöntologie Abhandlungen 232, 325– 363. Stapf, K. R. G. 1989. Biogene fluvio-lakustrine Sedimentation im Rotliegend des permokarbonen SaarNahe-Beckens (SW Deutschland). FACIES, 20, 169– 198. Steyer, J.-S. 2000. Ontogeny and phylogeny in temnospondyls: a new method of analysis. Zoological Journal of the Linnean Society, 130, 449–467. Steyer, J.-S. 2002. The first articulated trematosaur ‘amphibian’ from the Lower Triassic of Madagascar: implications for the phylogeny of the group. Palaeontology, 45, 771– 793. Steyer, J.-S., Laurin, M., Castanet, J. & Ricqle`s, A. De. 2004. First histological and skeletochronological data on temnospondyl growth: palaeoecological and palaeoclimatological implications. Palaeogeography, Palaeoclimatology, Palaeoecology, 206, 193– 201. Wagner, R. H. & Lyons, P. C. 1995. Upper Pennsylvanian (Stephanian) hiatus in the Appalachian and North European paralic area. 13th International Congress on Carboniferous-Permian. Krakov, Poland. Werneburg, R. 2002. Apateon dracyiensis – eine fru¨he Pionierform der Branchiosaurier aus dem Europaïschen Rotliegend Teil 2: Palaöo¨kologie. Vero¨ffentlichungen Naturhistorisches Museum Schleusingen, 17, 17– 32. Ziegler, A. M. 1990. Phytogeographic patterns and continental configurations during the Permian Period. In: McKerrow, W. S. S. & Scotese, C. R. (eds) Palaeozoic Palaeogeography and Biogeography. Geological Society, London, 363– 379. Ziegler, A. M. & Gibbs, M. T. 1996. Approaches to Permian world climates and biogeography. Permophiles, 29, 44–46.

Osmotic tolerance and habitat of early stegocephalians: indirect evidence from parsimony, taphonomy, palaeobiogeography, physiology and morphology ´ N3 M. LAURIN1,2* & R. SOLER-GIJO 1

CNRS, UMR 7179, Case 19, Universite´ Paris 6, 4 place Jussieu, 75005 Paris, France

2

(Present address) UMR 7207, Museúm National d’Histoire Naturelle, De´partement Histoire de la Terre, Baˆtiment de Geólogie, Case Postale 48, 43 rue Buffon, 75005 Paris, France 3

Museum fu¨r Naturkunde – Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Section Palaontology, Invalidenstrasse 43, D-10115 Berlin, Germany *Corresponding author (e-mail: [email protected]) Abstract: There are probably many reasons for the widespread belief that temnospondyls and other early stegocephalians were largely restricted to freshwater, but three of the contributing factors will be discussed below. First, temnospondyls have been called amphibians (and thought to be more closely related to extant amphibians than to amniotes). Some authors may have simply concluded that, like extant amphibians, temnospondyls could not live in oceans and seas. Second, under some phylogenies, temnospondyls are more closely related to anurans (and possibly urodeles) than to gymnophionans and could be expected, for parsimony reasons, to share the intolerance of all extant amphibians to saltwater. Similarly, ‘lepospondyls’ are often thought to be more closely related to gymnophionans than to anurans, and could also be expected to lack saltwater tolerance. Third, extant lungfishes live exclusively in freshwater, and early sarcopterygians have long been thought to share this habitat. These interpretations probably explain the widespread belief that early amphibians and early stem-tetrapods were largely restricted to freshwater. However, these three interpretations have been refuted or questioned by recent investigations. A review of the evidence suggests that several (perhaps most) early stegocephalians tolerated saltwater, even although they also lived in freshwater.

The environment represented by several continental Palaeozoic fossiliferous localities has long been controversial. This is not surprising, because the presence of strictly or mostly marine taxa shows convincingly in several cases that a locality was marine (usually coastal, if it is located on a continental plate), but the absence of such clearly marine indicators does not necessarily imply that the locality represents a freshwater environment (Schultze 1995). Most marine organisms support only with great difficulty important variations in salinity of the water (Barnes 1987, p. 3) or large sedimentation rates, which are common in deltaic environments. The latter hampers determination of the salinity of the water that deposited many sediments. Thus, some of the most salt-tolerant lissamphibians normally coexist along with only a few of the most euryhaline metazoans normally found in the seas (Annandale 1907). Some seas surrounded by land may have much lower salinity than most oceans and seas, and may be a hostile environment for many marine taxa. This is demonstrated by the

low biodiversity of the Baltic sea and the strong, salinity-dependent biodiversity gradient in that sea (Bonsdorff 2006; Zettler et al. 2007). Most sediments of the northern Baltic sea, which are devoid (or nearly so) of echinoderms, cnidarians (a few species may be abundant, such as Aurelia aurita and Mnemiopsis leidyi) and most other typically marine taxa (Bonsdorff 2006), would therefore presumably be wrongly interpreted as freshwater using the faunal association criteria which led to freshwater interpretation of many Permo-Carboniferous localities. This raises the possibility that many localities devoid of fossils of such marine taxa represent coastal, brackish water environments. Because of this, there is considerable uncertainty about the environment (marine, brackish water or freshwater) of early stegocephalians and of their finned forerunners. Most authors have considered Palaeozoic stegocephalians a largely freshwater and terrestrial group (Hunt 1993, p. 93; Poplin 1994, p. 299; Cuny 1995, p. 57; Schoch 1995, p. 113),


152

Ń M. LAURIN & R. SOLER-GIJO

whereas a few authors have argued that there is substantial evidence for widespread saltwater (and brackish water) tolerance in early stegocephalians (Schultze & Maples 1992; Schultze et al. 1994; Schultze 1995, 1999; Laurin & Soler-Gijoń 2001, 2006). The latter point of view was eloquently summarized by Schultze (1985, p. 2): Vertebrate remains are commonly used as terrestrial or freshwater indicators, even all the fish. . . This traditional interpretation is mainly based on the fact that complete vertebrates most commonly occur alone, rather than together with invertebrates. In many cases, this isolation results from preservational biases (calcium phosphate v. calcium carbonate), and not palaeoecological differences. Sometimes, the association of isolated elements of vertebrates with marine invertebrates has been explained as allochthonous, with the vertebrate remains having been washed in. No recent example of such association has been recorded.

We provide a historical review of ideas and recent evidence of the habitat of extant amphibians and lungfishes and of Palaeozoic finned sarcopterygians in a phylogenetic context. We demonstrate that in the late 19th and early 20th century, palaeontologists had objective reasons to expect early stegocephalians to be stenohaline, freshwater forms. The review also shows that these objective reasons have been refuted, and that there is no reason to expect early stegocephalians to have been confined to freshwater. We show how all data converge to suggest a marginal marine habitat for the earliest stegocephalians, and a long and widespread retention of salt- and brackish water tolerance in Palaeozoic stegocephalians.

Parsimony and habitat of extant and extinct sarcopterygians: a historical perspective In this section, we will consider how ideas about stegocephalian phylogeny, observations of the habitat of extant sarcopterygians and more recent information about the habitat of early sarcopterygians (especially dipnomorphs) may have influenced our expectations about the habitat of early stegocephalians, using parsimony as a criterion. Parsimony may not have been explicitly invoked in early works on this problem but (at least implicitly) it has probably been used as a general scientific principle. In this section, we will disregard direct evidence about the habitat of early stegocephalians, which will be presented separately (below). This section can be seen as an attempt to use parsimony to infer habitat of early stegocephalians (globally) in the context of various phylogenies. It is analogous (except in the inclusion of data on habitat of early

dipnomorphs) to an application of Witmer’s (1995) extant phylogenetic bracket. Extant amphibians (almost all of which are freshwater or terrestrial) have been thought to be polyphyletic (Fig. 1a) for much of the 20th century (Moodie 1916, pp. 46–49). More recently, this point of view was developed by Carroll & Holmes (1980) and Carroll & Currie (1975), who argued for independent origins of urodeles and gymnophionans from ‘lepospondyls’ whereas anurans were thought to be derived from ‘temnospondyls.’ More recently, Schoch & Carroll (2003) suggested, based on developmental data, that anurans and urodeles are temnospondyls whereas gymnophionans are ‘lepospondyls’. Schoch (2006) subsequently reached different conclusions, based on a much more rigorous analysis of developmental data. Furthermore, early sarcopterygians were thought to have inhabited only freshwater, as the extant lungfishes (Romer 1966). Only reptiliomorphs were thought to include a large number of saltwater-tolerant forms, as shown by the large number of marine amniotes. For instance, Neill (1958) listed 273 species or subspecies of ‘reptiles’ (in his usage, contrary to ours, this excluded birds) which lived at least occasionally in salt- or brackish water. Given such premises, the parsimony criterion (although it may not have been explicitly used) suggested that most early stegocephalians were restricted to freshwater and that saltwater tolerance appeared within reptiliomorphs (Fig. 1a). This does not imply that all reptiliomorphs tolerated saltwater; these data and phylogeny make no prediction about stem-reptiliomorphs which, at the time (Romer 1966), were thought to include embolomeres, seymouriamorphs, gephyrostegids, Solenodonsaurus and diadectomorphs. Later, the environments in which many early sarcopterygians were found (including lungfishes) were reinterpreted as coastal, deltaic or marine (Carroll 1988; Janvier 1996; Schultze 1999). Schultze (1997) even suggested that stegocephalians originated in an intertidal environment. Thomson (1980) also argued, on the basis of palaeogeographic arguments, that most groups of early sarcopterygians were either marine or euryhaline; in most cases, extinct stegocephalians of these two ecological categories cannot be distinguished. The term euryhaline is therefore used in this study, but it should be understood that this only means that the taxon could live in saltwater; this does not exclude the possibility that it could also live in freshwater and on land. Under such conditions, the intolerance to the marine environment could be seen as a specialization of the clade that includes at least the last common ancestor of gymnophiones, urodeles and anurans and all its descendants. Under the phylogenies advocated by Carroll & Holmes

Salientia Salientia Salientia

Caudata

"temnospondyls" Caudata

Gymnophiona "temnospondyls"

Caudata

"lepospondyl 2" "lepospondyls"

Reptiliomorpha Gymnophiona

"lepospondyls"

Actinistia

153

Seymouriamorphs

Gymnophiona Seymouriamorpha

Reptiliomorpha

Caudata

Salientia Salientia

Caudata

(f) Gymnophiona

Gymnophiona

"lepospondyls 1"

Reptiliomorpha Temnospondyli

Dipnoi Dipnoi Dipnoi

Salientia

"temnospondyls"

"lepospondyls 2"

Caudata

"temnospondyls"

(b)

(d)

"temnospondyls"

Seymouriamorphs

"lepospondyls"

Reptiliomorpha

(e)

Dipnoi

"lepospondyls 1"

Gymnophiona

"lepospondyls"

Dipnoi Dipnoi

(c)

Reptiliomorpha

(a)

Reptiliomorpha

HABITAT OF EARLY STEGOCEPHALIANS

euryhaline or marine stenohaline, freshwater equivocal

Fig. 1. Habitat of early stegocephalians which could be inferred on the basis of parsimony, of the habitat of extant tetrapods, of extant and extinct sarcopterygians and according to various phylogenies. (a) Hypothesis that prevailed until the 1980s. Early lungfishes were thought to have lived in freshwater, like extant lungfishes (Romer 1966). (b) Hypothesis taking into consideration recent data on the habitat tolerance of early lungfishes (Janvier 1996). (c) Hypothesis reflecting the first phylogenies proposed in a cladistic framework (Panchen & Smithson 1988; Trueb & Cloutier 1991; Ahlberg & Milner 1994). Computer-assisted phylogenetic analyses (d) suggest a monophyletic origin of extant amphibians among ‘lepospondyls’ (Laurin & Reisz 1997; Laurin 1998a), (e) among temnospondyls (Ruta et al. 2003; Ruta & Coates 2007), or (f) a polyphyletic origin (Anderson 2007). Extant taxa are in bold type; paraphyletic groups are identified by quotation marks and are not capitalized. Reptiliomorpha is euryhaline, as shown by the presence of amniotes in both freshwater and in saltwater. The trees were drawn using MacClade 4 (Maddison & Maddison 2003).

(1980) and Carroll & Currie (1975), this clade included all known amphibians (or at least, all temnospondyls and most lepospondyls) (Fig. 1b). With the advent of cladistics, earlier suggestions (Bolt 1969; Schultze 1970) that extant amphibians

form a monophyletic group (that excludes all known Palaeozoic tetrapods) became much more widely accepted (Trueb & Cloutier 1991). These ideas should have cast doubts about the environmental preferences of early (stem) amphibians,

154


because the parsimony criterion no longer suggested that they should have been restricted to freshwater (Fig. 1c). The intolerance to saltwater, which characterizes most lissamphibians (but not all; see Schmidt 1957; Garland et al. 1997), could have appeared as early as the first amphibian or as late as the last common ancestor of all lissamphibians. Schultze (1985) had already reached similar conclusions, and Milner (1987, pp. 500– 501) stated that . . .most recent workers believe the living amphibians to form a clade (usually referred to as the Lissamphibia) definable by a series of unique characteristics, most of which are not known in any Palaeozoic amphibian-grade tetrapod (see Rage & Janvier 1982 for a recent discussion). It can thus no longer be assumed that the freshwater dependence of most living amphibians is an inheritance from the Palaeozoic amphibian-grade tetrapods; it may represent a specialization acquired later in the early stages of lissamphibian evolution.

Several recent and comprehensive computerassisted phylogenetic analyses of tetrapods suggest that temnospondyls, formerly thought to be early amphibians, are stem-tetrapods (Laurin & Reisz 1997, 1999; Laurin 1998a; Anderson 2001; Vallin & Laurin 2004; Marjanovic´ & Laurin 2009). Therefore, the parsimony criterion actually suggests that this group tolerated saltwater (Fig. 1d); some temnospondyls may have lived in freshwater and others probably inhabited the coastal marine environment at least during juvenile and adult stages (see also Schult 1994; Schultze et al. 1994). The discovery of well-preserved remains of the temnospondyl Iberospondylus in a coastal environment (Laurin & Soler-Gijoń 2001, 2006) should not therefore be viewed as anomalous. However, this phylogeny makes no prediction about habitat preference in early amphibians (‘lepospondyls’). Ruta et al. (2003) and Ruta & Coates (2007) proposed a monophyletic origin of extant amphibians among temnospondyls, and placed ‘lepospondyls’ among reptiliomorphs (Fig. 1e). According to that phylogeny, seymouriamorphs and ‘lepospondyls’ can be expected to retain the ancestral saltwater tolerance, but no inferences can be drawn about habitat preferences in temnospondyls. Anderson (2007) proposed a diphyletic origin of extant amphibians, with batrachians (anurans and urodeles) nested within temnospondyls, and gymnophionans nested among ‘lepospondyls’, which form a clade with seymouriamorphs and reptiliomorphs (Fig. 1f). Under this phylogeny, reptiliomorphs include only amniotes and diadectomorphs (and perhaps Solenodonsaurus, which was not included in the analysis). Under that phylogeny, no inferences can be drawn about the habitat preferences of most early stegocephalians (temnospondyls,

‘lepospondyls’, embolomeres and seymouriamorphs). This phylogeny is probably less supported than other recent alternatives because it conflicts with all published molecular phylogenies (and most morphological ones) which support the monophyly of Lissamphibia with respect to Amniota (Laurin 2002). Other recent phylogenies do not fit the patterns presented above. For instance, McGowan (2002) suggests that many ‘lepospondyls’ are part of the amphibian crown (and hence should have been mostly freshwater forms) but, since his analysis does not include amniotes or reptiliomorphs, it is impossible to determine whether temnospondyls are stem-amphibians or stem-tetrapods under his proposal. His phylogeny suggests that most ‘lepospondyls’ did not tolerate salt or brackish water, but makes no prediction about environmental preferences of temnospondyls. This phylogeny was recently shown to be based on questionable anatomical interpretations (Marjanovic´ & Laurin 2008b, 2009). To summarize, in the context of phylogenies proposed early in the 20th century, parsimony suggested (Fig. 1) that Palaeozoic amphibians did not tolerate saltwater (Fig. 1a, b). More recent phylogenies usually suggest that Lissamphibia excludes all or most Palaeozoic amphibians (Fig. 1c–e), which implies no intolerance (but not necessarily tolerance either) to saltwater in amphibians (Fig. 1c –f). These trees suggest that some taxa traditionally attributed to Amphibia are stem-tetrapods (Fig. 1d) or reptiliomorphs (Fig. 1e), and this increases further the number of taxa which can be expected to have tolerated saltwater.

Habitat of early stegocephalians and their close relatives A review of the palaeoecological interpretations of the environment of early stegocephalians reveals much uncertainty and controversy (Tables 1 & 2). We have compiled the prevailing interpretations of the environment of these taxa. When considerable uncertainty exists, the states which were plausibly present all appear separated by slashes. However, interpretations which appear to be significantly less plausible are not considered, simply because the amount of uncertainty might be such that little signal could be extracted. For example, Tulerpeton was found in a marine environment located at least 200 km from the nearest land and, given the completeness and good preservation of the specimen, it plausibly lived in the sea (Lebedev & Clack 1993). Nevertheless, Long & Gordon (2004, p. 704) suggest that the recovered bones represent a carcass which has

Table 1. Habitat of early stegocephalians and other early sarcopterygians. Taxa are listed in phylogenetic and stratigraphic order. Habitat 0: marine; 1: brackish water; 2: freshwater (and potentially terrestrial, in many cases). Terrestrial taxa are excluded from this analysis since the purpose is to determine if aquatic or amphibious taxa inhabited fresh, brackish or saline water, and a terrestrial habitat cannot readily be inserted into an ordered salinity gradient. The locality information is not necessarily exhaustive; at least one is given for each taxon Taxa Youngolepis praecursor Diabolepis speratus Powichthys thorsteinssoni

Habitat

Geological age

Qujing Xian, Yunnnan, China Qujing Xian, Yunnnan, China Drake Bay Formation, Prince of Wales Island, Canada Tangil-e-Ab-Garm, Iran Miguasha, Escuminac Formation, Canada

0/1 0/1 0

Lochkovian Lochkovian Lochkovian

Chang (1982, p. 6) Chang (1982, p. 6) Jessen (1980); Cle´ment & Janvier (2004, p. 93)

0 0/1

Frasnian Frasnian

0 1

Frasnian Frasnian

0/1

Frasnian

Janvier & Martin (1979, p. 508); Janvier (1980, p. 228) Chidiac (1996); Cloutier et al. (1996); Schultze & Cloutier (1996); Clack (2007) Clack (2007, p. 514) Luksevics (1992); Vorobyeva & Kuznetsov (1992); Schultze & Cloutier (1996); Luksevics & Zupins (2004); Clack (2007, p. 512) Chidiac (1996); Cloutier et al. (1996); Schultze & Cloutier (1996); Clack (2007, p. 512) Long & Gordon (2004, p. 703) Daeschler et al. (2006)

Gogonasus Panderichthys

Gogo, Australia Lode, Ketleri Formation, Latvia; Rybnica, Orel region, Russia

Elpistostege

Miguasha, Escuminac Formation, Canada

Livoniana Tiktaalik

? 2

Givetian Frasnian

Obruchevichthys Elginerpeton

Ligatne, Gauja Formation, Latvia Bird Fiord, Ellesmere Island, Fram Formation, Canada Ketleri, Latvia Scat Craig, Scotland

? 1/2

Frasnian Frasnian

Metaxygnathus

Jemalong, New South Wales, Australia

1/2

Frasnian

Jakubsonia Sinostega Ventastega

Gornostayevka quarry, Russia Ningxia Hui autonomous region, China Pavari, Ketleri Formation

1 1/2 0/1

Frasnian Frasnian Famennian

Acanthostega

East Greenland

2

Famennian

Ichthyostega

East Greenland

2

Famennian

Densignathus

Red Hill, USA

1/2

Famennian

Hynerpeton

Red Hill, USA

1/2

Famennian

Reference for habitat

Ahlberg (1998, p. 133); Long & Gordon (2004, p. 703); Blieck et al. (2007, p. 221) Lebedev (2004; state 1); Long & Gordon (2004, p. 703; state 2); Blieck et al. (2007, p. 221) Lebedev (2004, p. 93) Zhu et al. (2002; state 2); Lebedev (2004; state 1) Luksevics & Zupins (2004); Lebedev (2004, p. 92); Clack (2006, p. 183); Clack (2007, p. 512) Long & Gordon (2004, p. 703); Blom et al. (2005, p. 46) Long & Gordon (2004, p. 703); Blom et al. (2005, p. 46) Daeschler et al. (1994; state 2); Lebedev (2004, p. 92; state 1); Long & Gordon (2004, p. 703; state 2) Daeschler et al. (1994; state 2); Lebedev (2004, p. 92; state 1); Long & Gordon (2004, p. 703; state 2)

155

(Continued)


Osteolepididae Eusthenopteron

Locality or formation

156

Table 1. Continued Taxa


Habitat

Geological age

Andreyevka-2, Tula, Russia Delta, Iowa, USA Dora bone bed, Scotland

0 1/2 1/2

Famennian Viseán Viseán

Loxomma allmanni

Gilmerton ironstone, Scotland

1/2

Viseán

Loxomma rankini

Drumgray coal, Castlehill, Scotland

1/2

Bashkirian

Loxomma acutirhinus

Airdrie, Lanarkshire, Scotland

1/2

Moscovian

Megalocephalus pachycephalus Megalocephalus lineolatus Baphetes planiceps

Several, Coal Measures, UK

1/2

Bashkirian, Moscovian

Linton, Ohio, USA

1/2

Moscovian

Albion mine, Stellarton, Nova Scotia

1/2

Moscovian

Baphetes kirkbyi

Pirnie Colliery, Airdrie, Bradford Coal Group, Scotland Linton, Ohio, USA Nyrany, Czech Republic

1/2

Moscovian

1/2 1/2

Moscovian Moscovian

Spathicephalus Doragnathus Pholidogaster pisciformis Greererpeton burkemorani Colosteus scutellatus

Dora bone bed, Scotland Dora bone bed, Scotland Gilmerton Ironstone, Scotland Greer, West Virginia, USA

1/2 1/2 1/2 1/2

Viseán Viseán Viseán Viseán and Serpukhovian

Linton, Ohio, USA

1/2

Moscovian

Dendrerpeton acadianum

Joggins, Nova Scotia, Canada

1/2

Bashkirian

Acroplous Trimerorhachis insignis

Keats, Riley county, Kansas, USA Thrift bonebed, Wichita county, Texas, USA Newsham, UK Mazon Creek, USA Puertollano, Spain Thrift bonebed, Wichita county, Texas, USA

0/1 0/1

Gzhelian Sakmarian

1 1 1/2 1/2

Moscovian Moscovian Gzhelian Sakmarian

Baphetes lintonensis Baphetes bohemicus

Eugyrinus Saurerpeton Iberospondylus Eryops

Lebedev & Clack (1993) Bolt et al. (1988); Lombard & Bolt (1995) Panchen (1973, p. 190; state 2); Unwin (1986; state 2); Milner (1987, p. 501; state 1) Beaumont (1977, p. 30; state 2); Milner (1987, p. 501; state 1) Beaumont (1977, p. 30; state 2); Milner (1987, p. 501; state 1) Beaumont (1977, p. 30; state 2); Milner (1987, p. 501; state 1) Beaumont (1977, p. 30; state 2); Milner (1987, p. 501; state 1) Beaumont (1977, p. 30; state 2); Milner (1987, p. 501; state 1) Beaumont (1977, p. 30; state 2); Milner (1987, p. 501; state 1) Beaumont (1977, p. 30; state 2); Milner (1987, p. 501; state 1) Beaumont (1977, p. 30) Beaumont (1977, p. 30); Schultze & Maples (1992, p. 234) Unwin (1986; state 2); Milner (1987, p. 501; state 1) Unwin (1986; state 2); Milner (1987, p. 501; state 1) Milner (1987, p. 501) Schultze & Bolt (1996) Schultze & Maples (1992, p. 234); Poplin (1994, p. 316) Milner (1987, pp. 496– 497; state 2); Poplin (1994, p. 315; state 1) Schultze (1985, p. 11; 1999, p. 385; states 0/1) Parrish (1978, p. 235; states 0/1); Milner (1987, p. 501; state 1); Schultze (1999, p. 385; states 0/1) Milner (1987, p. 501; state 1) Milner (1987, pp. 502– 503; state 1) Laurin & Soler-Gijoń (2001, 2006) Parrish (1978, p. 235; states 1/2)


Tulerpeton Whatcheeria deltae Crassigyrinus


Onchiodon (formerly called Actinodon) frossardi Cheliderpeton vranyi Zatrachys Branchiosaurus petrolei Micromelerpeton Amphibamus

Montceau-les-Mines, France

1/2

Gzhelian

Broumov, Sudetic basin, Czech Republic Thrift bonebed, Wichita county, Texas, USA Mazon Creek, Montceau-les-Mines, Nyrany, Czech Republic Montceau-les-Mines, France

1/2 1/2

Asselian Sakmarian

Schultze & Maples (1992, p. 234; state 2); Poplin (1994; state 1); Poplin et al. (2001, p. 299; state 1); Werneburg & Steyer (1999; synonymy) Poplin (1994, p. 307) Parrish (1978, p. 235; states 0/1)

1/2

Moscovian

Schultze & Maples (1992); Poplin (1994)

1/2

Gzhelian

Schultze & Maples (1992, p. 234; state 2); Poplin (1994; state 1); Poplin et al. (2001, p. 299; state 1) Schultze & Maples (1992)

Moscovian

1/2 1/2 1/2 1/2

Serpukhovian Viseán Viseán and Serpukhovian Bashkirian

Archeria

Archer City bonebed, USA

1/2

Sakmarian

Discosauriscus

Montceau-les-Mines, France; Boskovice furrow, Czech Republic

1/2

Gzhelian

Lethiscus Ophiderpeton Phlegethontia Ptyonius Sauropleura Diplocaulus

Wardie Shales, Scotland Mazon Creek, Linton, USA; Nyrany Linton, Nyrany, Czech Republic Mazon Creek, Linton, USA Linton, USA; Nyrany, Czech Republic Thrift bonebed, Wichita county, Texas, USA

1/2 1/2 1/2 1 1/2 1/2

Viseán Moscovian Moscovian Moscovian Moscovian Artinskian

Euryodus

Speiser shale, Wreford Megacyclotherm, Kansas, USA Joggins, Canada

1

Artinskian

1/2

Bashkirian

Trachystegos megalodon Leiocephalikon problematicum Hylerpeton dawsoni

Joggins, Canada

1/2

Bashkirian

Joggins, Canada

1/2

Bashkirian

Ricnodon

Joggins, Canada

1/2

Bashkirian

Hyloplesion

Tremosna, Czech Republic

2

Moscovian

Milner (1987, p. 501) Unwin (1986; state 2); Milner (1987, p. 501; state 1) Schultze & Bolt (1996) Milner (1987, pp. 496– 497; state 2); Poplin (1994, p. 315; state 1) Parrish (1978, p. 235; states 1/2); Milner (1987, p. 501) Schultze & Maples (1992, p. 234; state 2); Poplin (1994, pp. 295, 307, 308; states 1/2); Poplin et al. (2001, p. 299; state 1) Milner (1987, p. 501; state 1) Schultze & Maples (1992) Schultze & Maples (1992) Schultze & Maples (1992) Schultze & Maples (1992) Parrish (1978, p. 235; states 1/2); Milner (1987, p. 501; state 1); Schultze (1985, p. 11; 1999, p. 385; states 0/1) Schultze (1985, p. 11)


1/2

Caerorhachis bairdi Eoherpeton Proterogyrinus scheelei Calligenethlon watsoni

Mazon Creek, Linton, Nyrany, Czech Republic Loanhead, Scotland Dora bone bed, Scotland Greer, West Virginia, USA Joggins, Canada

Milner (1987, pp. 496– 497; state 2); Poplin (1994, p. 315; state 1) Milner (1987, pp. 496– 497; state 2); Poplin (1994, p. 315; state 1) Milner (1987, pp. 496– 497; state 2); Poplin (1994, p. 315; state 1) Milner (1987, pp. 496– 497; state 2); Poplin (1994, p. 315; state 1) Milner (1987, p. 496– 497) 157

(Continued)

158

Table 1. Continued Taxa


Habitat

Geological age

Nyrany, Czech Republic

1/2

Moscovian

Brachydectes elongatus

Several localities in Texas and Oklahoma, USA Florence, Nova Scotia, Canada

1&2

Artinskian

1/2

Moscovian

Limnostygis relictus Limnoscelis paludis Limnoscelis dynatis Desmatodon hesperis Archaeothyris florensis Ophiacodon

El Cobre Canyon, Cutler Formation, New Mexico, USA Badger Creek Quarry, Howard, Sangre de Cristo Formation, Colorado, USA Badger Creek Quarry, Howard, Sangre de Cristo Formation, Colorado, USA Florence, Nova Scotia, Canada Thrift bonebed, Wichita county, Texas, USA

Beaumont (1977, p. 30); Milner (1987, p. 502); Schultze & Maples (1992, p. 234); Poplin (1994, p. 307; state 1) Schultze (1985, p. 11; 1999, p. 385; states 0/1)

2

Gzhelian and/or Asselian

2

Gzhelian

Carroll et al. (1972, p. 54; state 1); Milner (1987, pp. 496– 497) Vaughn (1969, p. 405); Berman et al. (1985, pp. 7 – 8; 1987, p. 1772); Eberth & Berman (1993) Vaughn (1969, p. 405)

2

Gzhelian

Vaughn (1969, p. 405)

1/2

Moscovian

0/1

Sakmarian

Carroll et al. (1972, p. 54; state 1); Milner (1987, pp. 496– 497; state 2) Parrish (1978, p. 235)


Microbrachis pelikani



159

Table 2. Palaeoecological interpretations of selected fossiliferous localities which have yielded early stegocephalians or other tetrapodomorphs. The habitat attributed to each locality is scored on the basis of the data presented in the paper, rather than on the interpretation of the authors of the cited references. Habitat: as for Table 1; N/A, not applicable (terrestrial localities). Not all interpretations found in the literature have been inserted; the emphasis is on interpretations which are supported by several studies Locality

Habitat

Geological age

Miguasha, Escuminac Formation

0/1

Frasnian

Scat Craig, Scotland

1/2

Frasnian

Gogo, Australia Lode, Latvia

0 1

Frasnian Frasnian

Bird Fiord, Ellesmere Island, Fram Formation, Canada Pavari, Ketleri Formation, Latvia

2

Frasnian

Strud, Belgium Jemalong, New South Wales, Australia Gornostayevka quarry, Russia Red Hill, Pennsylvania, USA East Greenland

0/1/2

Famennian

2 1/2

Famennian Frasnian

1

early Frasnian

1/2

Famennian

2

Famennian

Gilmerton Ironstone, Scotland Dora bone bed, Scotland

1/2

Viseán

1/2

Viseán

Delta, Iowa, USA

1/2

Viseán

Glencartholm, Scotland Wardie, Scotland

0/1 1/2

Viseán Viseán

East Kirkton, Scotland

1/2

Viseán

Greer, West Virginia, USA Loanhead, Scotland Joggins, Nova Scotia, Canada

1/2

Viseán and Serpukhovian

1/2 1/2

Serpukhovian Bashkirian

Swisshelm Mountains, Arizona, USA Florence, Nova Scotia, Canada Mazon Creek, USA Linton, Ohio, USA

1

Bashkirian

1/2

Moscovian

0/1

Moscovian

1/2

Moscovian

Reference for habitat Chidiac (1996); Cloutier et al. (1996); Schultze & Cloutier (1996); Clack (2007) Ahlberg (1998, p. 133); Long & Gordon (2004, p. 703); Blieck et al. (2007, p. 221) Clack (2007, p. 514) Luksevics (1992); Vorobyeva & Kuznetsov (1992); Schultze & Cloutier (1996); Clack (2007, p. 512) Daeschler et al. (2006) Luksevics (1992); Luksevics & Zupins (2004); Lebedev (2004, p. 92; state 1); Long & Gordon (2004, p. 703; states 0/1/2); Clack (2006, p. 183; states 0/1); Blieck et al. (2007, p. 221); Clack (2007, p. 512) Blieck et al. (2007, p. 221) Lebedev (2004; state 1); Long & Gordon (2004, p. 703; state 2) Lebedev (2004, p. 93); Blieck et al. (2007, p. 221) Lebedev (2004, p. 92); Long & Gordon (2004, p. 703); Blieck et al. (2007, p. 221) Long & Gordon (2004, p. 703); Blom et al. (2005, p. 46); Blieck et al. (2007, p. 221) Milner (1987, p. 501) Unwin (1986; state 2); Milner (1987, p. 501; state 1) Bolt et al. (1988); Lombard & Bolt (1995); Schultze & Bolt (1996) Poplin (1994, p. 314) Milner (1987, p. 501; state 1); Poplin (1994, p. 314; state 2) Milner (1987, p. 501; state 1); Poplin (1994, p. 314; state 2) Schultze & Bolt (1996) Milner (1987, p. 501) Milner (1987, pp. 496 –497; state 2); Poplin (1994, p. 315; state 1); Schultze (1995, p. 257; states 0/1) Milner (1987, p. 498) Carroll et al. (1972, p. 54; state 1); Milner (1987, pp. 496 – 497; state 2) Schultze & Maples (1992, p. 234); Poplin (1994, p. 316; states 0/1) Schultze & Maples (1992, p. 234); Poplin (1994, p. 316) (Continued)


160

Table 2. Continued Locality Nyrany, Czech Republic

Habitat

Geological age


1/2

Moscovian

2

Moscovian

Beaumont (1977, p. 30; state 2); Milner (1987, p. 502; state 2); Schultze & Maples (1992, p. 234); Poplin (1994, p. 307; state 1) Milner (1987, p. 496– 497)

1/2

Moscovian to Gzhelian

Poplin (1994, p. 308)

0/1 0/1 0/1 1/2

Kasimovian Gzhelian Gzhelian Gzhelian

Puertollano

1/2

Gzhelian

Kinney Quarry, Pine Shadow member, Wild Cow Formation, New Mexico Badger Creek Quarry, Howard, Sangre de Cristo Formation, Colorado Sudetic basin, Czech Republic Saale basin, Germany El Cobre Canyon, Arroyo de Agua, Cutler Formation, New Mexico Boskovice furrow, Czech Republic Bromacker, Tambach basin, Germany Dolese Brothers quarry, Fort Sill, Oklahoma, USA

1/2

Gzhelian

Schultze & Maples (1992, p. 234) Schultze & Maples (1992, p. 234) Schultze & Maples (1992, p. 234) Schultze & Maples (1992, p. 234; state 2); Poplin (1994; state 1); Poplin et al. (2001, p. 299; state 1); Schultze & Soler-Gijoń (2004; state 1) Laurin & Soler-Gijoń (2001, 2006); Soler-Gijoń & Moratalla (2001) Hunt et al. (1992, pp. 211, 218 – 219)

2

Gzhelian

Vaughn (1969, p. 405)

Gzhelian and Asselian

Poplin (1994, p. 307)

Gzhelian and Asselian Gzhelian and/or Asselian

Poplin (1994, p. 310) Vaughn (1969, p. 405); Berman et al. (1985, pp. 7 – 8; 1987, p. 1772); Eberth & Berman (1993)

Asselian

Tremosna, Czech Republic Kladno and Rakovnice basins Garnett, Kansas Hamilton, Kansas Robinson, Kansas Montceau-les-mines

1/2 2 2

1/2 N/A

Artinskian

Poplin (1994, p. 308); Schultze & Soler-Gijoń (2004; state 1) Eberth et al. (2000)

N/A

Artinskian

Sullivan & Reisz (1999)

floated over a long distance. While this is not strictly impossible, this opinion is not considered further here (Table 1) for two reasons: 200 km is a very long distance to float, and this hypothesis seems to be based on pre-conceived ideas. Furthermore, Hunt et al. (1992, p. 219) stated that ‘Tertiary freshwater frogs and salamanders are never found in lagoonal environments (A. R. Milner, pers. comm. 1991).’ Extant lissamphibians are coded as stenohaline freshwater forms because that appears to be the case in most species (see below). On the contrary, mammals, saurians and turtles are considered euryhaline because many species of these taxa are found in freshwater as well as in the seas (cetaceans, seals, sea lions, sea otters and some sirenians among

mammals; mosasaurs, marine snakes, the Galapagos iguana and several extant and extinct crocodilians among saurians; the green and leatherback turtles, among many others), as well as in freshwater. The review (Table 1) suggests that some of our distant finned relatives, such as Eusthenopteron, Panderichthys and Elpistostege lived in marginal marine environments, presumably in salt or brackish water. More crownward taxa, from the Frasnian Tiktaalik to most Permo-Carboniferous stegocephalians, appear to have more frequently inhabited brackish to freshwater bodies. Nevertheless, a few Devonian stegocephalians appear to have lived in a marine environment. Thus, the Ketleri Formation in which Panderichthys and Ventastega were found may represent a marginal marine environment


Salientia

Caudata

Gymnophiona

"lepospondyls"

Temnospondyli

Dipnoi

Salientia

Caudata

(b) Gymnophiona

"temnospondyls"

"lepospondyls"

Dipnoi

(a)

Reptiliomorpha

Earlier studies which suggested that PermoCarboniferous stegocephalians were freshwater inhabitants led him to suggest that a storm had caused a massive influx of saltwater into the pond, and that ‘Fresh-water species intolerant of marine salinities would have been placed in double jeopardy.’ This hypothesis of the origin of at least some of the stegocephalian fossils is plausible because sudden and important variations in salinity can be lethal, even for euryhaline species such as Fejervarya cancrivora (Gordon et al. 1961, p. 662) or Bufo viridis (Gordon 1962). However, perhaps a massive influx of freshwater (quite likely to occur in a coastal pond during or after a storm) into a brackish to hypersaline pond might have nearly as deleterious effects on the fauna. In any case, Parrish (1978) suggested that some early stegocephalians probably tolerated brackish to saltwater. Among earlier studies, only Vaughn (1969, p. 403) came close to suggesting brackish water tolerance in some early stegocephalians

Reptiliomorpha

. . .the strong possibility exists that the fauna [which inhabited a former mudflat pond located only about 3 km from the sea and included abundant Trimerorhachis insignis, as well as less numerous remains of Xenacanthus, Eryops, Zatrachys, Archeria, Diplocaulus, Ophiacodon and Dimetrodon] was capable of tolerating brackish, if not marine, salinities.

by recognizing ‘crossopterygians’, Diplocaulus, Seymouria and Dimetrodon as ‘truly deltaic markers’, but he did not comment on water salinity. Several other recent studies raise doubts about the interpretation of most Permo-Carboniferous localities yielding stegocephalians as freshwater environments (Table 2). This applies particularly to North American localities such as Garnett, Hamilton and Robinson (Kansas, USA) and Las Cruces (Robledo Mountains, New Mexico, USA), and suggests that many groups of early stegocephalians inhabited marginal marine environments (at least occasionally). Thus, they may have been euryhaline (Schultze & Maples 1992; Schult 1994; Schultze et al. 1994; Schultze 1995, 1999). If the results of these studies are accepted, there is actual evidence that the widespread (but not universal) intolerance of lissamphibians to the marine environment is a relatively recent feature (it probably arose in the Late Carboniferous or in the Permian) because their closest known relatives have been found in coastal environments. This conclusion can be drawn whether a traditional phylogeny (Fig. 2a) such as Panchen & Smithson (1988) or Lombard & Sumida (1992) or a more recent phylogeny such as Laurin (1998a) or Anderson (2001) is used (Fig. 2b), since both presumed sister groups of lissamphibians (lysorophids, among lepospondyls and various dissorophoids, among temnospondyls) appear to have tolerated saltwater (Schultze 1995). This is supported not only by body fossils, which could conceivably have been transported into deltas and lagoons by rivers and streams, but also by trace fossils such as burrows and trackways (Schult 1994, 1995a, b). In his studies of the Lower Permian Speiser Shale fauna from Kansas, Schultze (1985, 1999) Seymouriamorpha

(Luksevics 1992; Clack 2006). As mentioned above, Tulerpeton was probably marine. One of the first to question the freshwater, stenohaline tolerance of all Permo-Carboniferous stegocephalians was Parrish (1978). His thorough sedimentological, faunal and taphonomic study of the Thrift bonebed in Wichita county (Texas) led him to propose that

161

euryhaline or marine stenohaline, freshwater equivocal

Fig. 2. Habitat of early stegocephalians inferred on the basis of parsimony and a review of the literature on their habitat. Whether lissamphibians are part of (a) temnospondyls (Panchen & Smithson 1988; Lombard & Sumida 1992) or of (b) ‘lepospondyls’ (Laurin 1998a; Vallin & Laurin 2004), a freshwater (or terrestrial) habitat is an autapomorphy of Lissamphibia. Under both phylogenies, the limited evidence of salt- or brackish water tolerance in early stegocephalians suggests that this taxon retained the saltwater tolerance inherited from their finned ancestors.

162


reported remains of Acroplous and Trimerorhachis (two trimerorhachid temnospondyls) and Diplocaulus and Brachydectes (two amphibians or ‘lepospondyls’) in coastal burrows. These would presumably have been exposed to salt- or brackish water during the tidal cycle. It could be objected that the environment represented by that locality is uncertain because Hembree et al. (2005) re-interpreted the locality as deposits of sporadic ephemeral ponds in a coastal plain and the burrows as a response of the tetrapods to seasonal droughts. However, despite the two different palaeoenvironmental conclusions, the deposits of the Speiser Shale represent a good example of palaeozoic transitional environments close to or connected to the sea (Park & Gierlowski-Kordesch 2007) where the organisms have to adapt to a wide range of salinities as a consequence of the combination of palaeoenvironmental (tidal cyclicity, marine incursions) and climatic factors. Interestingly, Sequeira (1998) argued that salinity tolerance was the limiting factor explaining the patchy distribution of saurerpetontids. According to Sequeira (1998, p. 257) the saurerpetontids ‘were part of a group of salinity-tolerant tetrapods, capable of living either in coastal water-bodies with some saline input, however low, or in periodically drying water-bodies which might have varying salt-content’. The Late Carboniferous coal fields of Joggins (Nova Scotia, Canada) and Puertollano (Ciudad Real, Spain) present stegocephalians (tracks and skeletal remains) and numerous evidence (geochemical, sedimentological and palaeontological) of marine influence. Joggins represents part of the sedimentation in a large microtidal embayment of an extensive epicontinental sea (analogous in many aspects to the Baltic Sea) which was connected to the Tethyan Ocean (Archer et al. 1995; Falcon-Lang 2005; FalconLang et al. 2006; Falcon-Lang & Miller 2007). Agglutinated foraminifera (Trochammina, Ammobaculites, Ammotium and cf. Textularia) and a metazoan trace-fossil assemblage (xiphosurian trackways Kouplichnium and cf. Limulocubichnus and annelid traces Arenicolites, Gordia, Haplotichnus, Plangtichnus, Cochlichnus and Treptichnus) indicate an ‘open water brackish bay’ environment for at least parts of the Joggins Formation (Archer et al. 1995; Falcon-Lang 2005, fig. 2; Falcon-Lang et al. 2006, table 1 and fig. 4). The stegocephalian Baphetes occurred in the brackish bay together with other osteichthyans (Falcon-Lang et al. 2006, table 1 and fig. 5), numerous chondrichthyans (Xenacanthus, Ctenacanthus, Ctenoptychius and Callopristodus) and acanthodians (Gyracanthus). In addition, temnospondyls (e.g. Dendrerpeton acadianum) and lepospondyls appeared to have

populated subaerial areas of the brackish-influenced coastal plain as indicated by stegocephalian trackways in a heterolithic sandstone facies showing tidal influence (Falcon-Lang et al. 2006, table 2 and fig. 6). The Puertollano basin preserves a formal coastal, marine or at least brackish environment, as shown by the presence of tidal rythmites (a sedimentary structure which forms only in intertidal and prodeltaic environments; Mazumder & Arima 2005), acritarchs, aliphatic hydrocarbons and other geochemical evidence (Laurin & Soler-Gijoń 2006, p. 295). The trackway of Puertollanopus microdactylus, which was produced by a small stegocephalian (pes length of about 20 mm), was left on intertidal sediments which must have been soaked with brackish water (Soler-Gijoń & Moratalla 2001). The exact identity of the small trackmaker is not known because the locality in which these trackways were found did not yield skeletal remains of a size and shape matching those of the trackways. The only stegocephalian represented by skeletal remains is the much larger Iberospondylus schultzei (Laurin & Soler-Gijoń 2001, 2006), whose skull length is about 15 cm. However, the dimensions and proportions of the tracks and size and morphology of the impressions of manus and pes suggest a microsaur or a small reptile. At least one (perhaps two) species of stegocephalians therefore ventured into salt or brackish water in Puertollano in the Stephanian C, which is equivalent to early Gzhelian, about 304–302 Ma (Davydov et al. 2004). Similar conclusions were expressed by Milner (1987, p. 501), who stated that This reasoning [which implies that many localities previously interpreted as freshwater were possibly brackish] applies to all but one of the other amphibianproducing localities [Newsham was already discussed and argued to probably preserve a euryhaline fauna] from the Coal Measures of England and Scotland, which are characterized by embolomeres (Panchen 1970), loxommatids (Beaumont 1977) and the occasional keraterpetontid (Milner 1980) and lysorophid (Boyd 1980). The only exception is the Carre Heys locality which was offshore deltaic [i.e. with even more marine influence] and has produced Eugyrinus, a member of the Trimerorhachoidea, the other group suggested by Parrish (1978) and Schultze (1985) to be euryhaline.

Numerous Late Carboniferous –Early Permian localities with stegocephalians from western and central Europe (Massif Central in France, Saale and Saar-Nahe basins and Do¨hlen in Germany, Bohemian basins and Boskovice Furrow in Czech Republic) (see Table 1) have long been considered to represent intermontane freshwater basins, palaeogeographically far from the sea and located at high


altitude (Poplin 1994; Boy & Schindler 2000; Boy & Sues 2000; Sanchez et al. 2010). However, Schultze & Soler-Gijoń (2004) have recently suggested marine influence in these European basins because of the presence of several brackish or saline water indicators: marine calcareous algae (dasycladaceans and udoteaceans), annelids, euthycarcinoids, xiphosurans, euryhaline sharks (xenacanths, Sphenacanthus and Lissodus), the actinopterygians Bourbonnella and haplolepiforms, myxinoids (Poplin et al. 2001) and shark egg capsules (Fayolia, Palaeoxyris, Vetacapsula). According to Schultze & Soler-Gijoń (2004), the analysis of the distribution of fossil egg capsules in the basins is a powerful tool for the determination of palaeosalinities. This suggestion is based on the fact that no recent oviparous shark is known to deposit egg capsules in freshwater. In contrast, the few recent elasmobranchs adapted to more or less permanent life in freshwater (i.e. stenohaline freshwater) are viviparous (e.g. potamotrygonid rays). Chondrichthyan egg capsules (Palaeoxyris and Vetacapsula) have been reported in Mazon Creek and Hamilton, both localities with evidence of tides, and egg capsules have been described from Commentry (Massif Central) and from several localities of Saar-Nahe, Saale and Bohemian basins, which suggests a connection to marine areas of the Palaeotethys (Schultze & SolerGijoń 2004). Palaeotopographic features of the Variscan mountain chain and altitude of the western and central Permo-Carboniferous basins have important implications in the study of development and growth pattern of stegocephalians. Recently, Schoch & Fro¨bisch (2006) and Fro¨bisch & Schoch (2009) explained neoteny, very common in branchiosaurids from Saar-Nahe basin, by the high elevation (up to 2000 m or more above sea level) of the lakes where those stegocephalian lived. Sanchez et al. (2010) explained a double growth line pattern in bones of Apateon as the consequence of hibernation-estivation events similar to those which affect recent amphibians living in mountain lakes at temperate latitude (several localities in north of Portugal). Both studies are based on a model of limnic basins located at a very high altitude (a few thousands of metres) as proposed by Becq-Giraudon et al. (1996) for the Stephanian basins of the Massif Central. However, recent estimations of the altitudes of the basins indicate a relative low topography (Oplusˇtil 2005a, b; Roscher & Schneider 2006; Schneider et al. 2006), which suggests that the environmental factors which induced heterochrony in branchiosurids were not low temperature; perhaps fluctuations in the salinity of the waters is a more plausible cause.

163

Studies of the euryhaline toad Bufo calamita and other recent amphibians (Gomez-Mestre & Tejedo 2002, 2005; Gomez-Mestre et al. 2004) which are adapted to a brackish environment show variations of thyroid hormone linked to increase in the salinity (see below for more information about salt tolerance of recent amphibians). Furthermore, double growth patterns as described in Apateon are also shown in several groups of recent tropical actinopterygians living in low altitudes in coastal and estuarine areas. For example, two annuli and two zones per year have been described in bones of teleosts (Ariidae, Anastomidae and Serrasalmidae) from French Guyana; the annual growth marks have been connected to the existence of two dry seasons and a bimodal rainfall pattern (Lecomte et al. 1986, 1993; Meunier et al. 1994). The growth pattern of the tropical stegocephalian Apateon (probably a stem-tetrapod, although many authors consider it a stem-amphibian), which probably lived in a low altitude as indicated by the most recent analyses of the Permo-Carboniferous basins, probably results from factors other than the growth pattern of recent lissamphibians of Portugal living at a temperate latitude and in high altitude. For Oplusˇtil (2005a), the recent analogue of the Late Palaeozoic continental basins of central and western Bohemia is the Tasek Bera Basin in central Peninsular Malaysia; this is a dendritic basin, located at about 38N, 35 m above sea level, surrounded by lowland hills rising up to 240 m above sea level. For localities of the Cutler Formation from New Mexico, other localities which yielded seymouriamorphs (Berman et al. 1987; Klembara & Mesza´ros 1992; Berman & Martens 1993) and the Sangre de Cristo Formation from Colorado, we are not aware of clear evidence of marine influence. However, many of the taxa found there (such as xenacanthiform chondrichthyans, acanthodians and dipnoans) are also known from marine and brackish environments (Table 2). Even the seymouriamorphs are also found in other, presumably brackish environments (Montceau-les-Mines, Texas redbeds). Nevertheless, the great abundance of seymouriamorphs in basins showing the least marine influence, and their lesser abundance or absence from basins which show more marine influence, suggests that they may have been less tolerant of brackish and saltwater than many other early stegocephalians. Vaughn’s (1969) palaeogeographic reconstructions placed some localities in New Mexico and Colorado in ‘somewhat more upland’ environments in contrast to other localities located in the ‘truly deltaic’ environments (or ‘coastal plain’, as proposed by Berman & Reisz 1980). In the Cutler Formation, the abundance of caliche (Berman et al. 1985, 1987), a hardened deposit of calcium

164


carbonate, raises the possibility that at least some of the still water bodies were brackish, even if the sea was far away. Furthermore, Eberth & Berman (1993, p. 46) seem to have interpreted the presence of the dipnoan Sagenodus and the osteolepidid Lohsania as freshwater indicators. Sagenodus was probably euryhaline, however, and is thought to have occurred in marine and freshwater environments (Schultze & Chorn 1997). We have found no detailed data on the presumed habitat of Lohsania but, given the general reinterpretation of osteolepidids from freshwater to marine and euryhaline forms, the freshwater interpretation of the Cutler Formation does not appear to be supported by faunistic criteria. We have provisionally accepted the conclusions of Eberth & Berman (1993) but it would be interesting to study the mollusks, arthropods and other metazoans from that formation.

Evolutionary analysis of habitat in early stegocephalians A time-calibrated supertree was compiled from the literature (Figs 3 & 4). Given the large time-span encompassed by the tree (Givetian to Roadian on the figure, but it really extends to the Holocene), all terminal taxa were placed within the proper geological stage. No attempt was made to achieve greater stratigraphic precision, for various reasons. First, the gained precision would not be visible on the figure, unless a non-linear timescale was used. Second, given the stratigraphic uncertainties on the age of many fossils and the still greater uncertainty about the actual (as opposed to observed) stratigraphic range of most terminal taxa (Marshall 1997; Marjanovic´ & Laurin 2008a), the gains in precision would be more apparent than real. Among many arbitrary branch length values that could have been used, we set both terminal branches to a minimal length of 1 Ma and internal branches to a minimal length of 2 Ma. We placed the end of the stratigraphic range of all terminal taxa at the top of the geological stage to which they belong, as was done by Laurin (2004) and Marjanovic´ & Laurin (2007). Given the large number of terminal taxa (86) and of polytomies included in the tree, this procedure results in reasonable ages for the hypothetical ancestors. Presumed terrestrial taxa were excluded because the distinction between salt and freshwater habitats does not apply to them. Early amniotes are therefore represented by Ophiacodon, which may have been amphibious to aquatic (Romer 1958; Germain & Laurin 2005). Hylonomus is included (but not coded for habitat) to provide a temporal calibration of this part of the tree only. The tree is not exhaustive but, during its compilation, it became clear that given the

uncertainties about the palaeoenvironmental interpretation of many localities, adding more taxa would not have changed the global pattern. Furthermore, the information presented in Table 2 enables any interested palaeobiologist to expand the analysis to additional taxa. To determine if character optimization yields reliable information on ancestral states, the presence of a phylogenetic signal should be assessed (Laurin 2004). The high number of polytomies constrains the choice of randomization procedure because the number of steps required by trees which include soft or hard polytomies, and of trees with randomly resolved polytomies, differs. An appropriate randomization procedure is to reshuffle terminal taxa randomly on the tree in which topology and branch lengths are kept constant, as was done by Laurin (2004). In this case, all random trees include the same number and type of polytomies. Another solution would have been to randomly resolve the polytomies several times (ten or more) to investigate the phylogenetic signal in all of these trees and to average the probabilities; that solution would be more time consuming and potentially less accurate, however (unless a much greater number of random resolutions were examined). In both cases, the probability that the distribution of the character states is independent of the phylogeny is given by the number of random trees (produced by reshuffling) which implies the same number (or fewer) transitions as the reference tree, divided by the total number of random trees (here, 10 000). The three states (0: marine; 1: brackish; and 2: freshwater) were ordered according to a salinity gradient. Given the controversies surrounding palaeoenvironmental interpretations of most Palaeozoic fossiliferous localities in which stegocephalians were found, two optimizations of habitat are presented. The first presents the most traditional interpretation: many localities are interpreted as freshwater environments or, when clearly marine or brackish water, stegocephalian remains are interpreted as allochtonous elements brought in by rivers (Fig. 3). Since the phylogenetic signal is highly significant ( p ¼ 0.0002), the character can be optimized. This optimization suggests that the first sarcopterygians and tetrapodomorphs lived in a brackish or marine environment (which is not new, of course) and that the move to freshwater environments took place before the last common ancestor of Tiktaalik and stegocephalians. The few Palaeozoic stegocephalians which tolerated brackish water represent returns to a marginal marine environment. The second optimization presents the alternative interpretation of a more marine (or at least brackish) environment of most fossiliferous localities. Under


165

Lissamphibia

Euryodus Brachydectes elongatus

Diplocaulus

Diapsida

Amphibia

268.0 270.6 Roadian Kungurian 275.6

Desmatodon hesperis Limnostygis relictus Limnoscelis paludis Limnoscelis dynatis

Brachydectes newberryi

Ptyonius Sauropleura Microbrachis pelikani Leiocephalikon problematicum Trachystegos megalodon Ricnodon Hylerpeton dawsoni Hyloplesion

Ophiderpeton Phlegethontia

Artinskian

Adelogyrinidae Lethiscus

Hylonomus

Ophiacodon Archaeothyris florensis

Whatcheeria deltae Crassigyrinus Doragnathus Pholidogaster pisciformis Greererpeton burkemorani Colosteus scutellatus Spathicephalus Loxomma allmanni Loxomma rankini Loxomma acutirhinus Megalocephalus pachycephalus Megalocephalus lineolatus Baphetes planiceps Baphetes kirkbyi Baphetes lintonensis Baphetes bohemicus Acroplous Saurerpeton Trimerorhachis Eugyrinus Dendrerpeton acadianum Amphibamus Micromelerpeton Branchiosaurus petrolei Zatrachys Onchiodon frossardi Eryops Cheliderpeton vranyi Iberospondylus Caerorhachis bairdi Eoherpeton Calligenethlon Archeria Proterogyrinus scheelei Discosauriscus

Therapsida

Parareptilia

Reptiliomorpha

284.4 Sakmarian 294.6 299.0

Asselian

Gzhelian 303.9 306.5 Kasimovian Moscovian 311.7 Bashkirian 318.1 Serpukhovian 326.4

Osteolepididae Eusthenopteron Gogonasus Panderichthys Elpistostege

Tiktaalik Obruchevichthys Elginerpeton Metaxygnathus Jakubsonia Ventastega Acanthostega Sinostega Ichthyostega Densignathus Hynerpeton Tulerpeton

Amphibia Amphibia Tetrapoda Tetrapoda Tetrapoda Move onto land?

Visean

345.3

Tournaisian Loss of caudal lepidotrichia Appearance of pentadactyly

359.2

Famennian

Stegocephali Stegocephali Stegocephali

Powichthys thorsteinssoni Diabolepis speratus Youngolepis praecursor

Livoniana

374.5 Appearance of the limbs

Frasnian 385.3 Givetian 391.8 Eifelian 397.5 Emsian 407.0 411.2

Tetrapodomorpha Tetrapodomorpha Tetrapodomorpha

416.0

Pragian Lochkovian

Fig. 3. Time-calibrated supertree of sarcopterygians emphasizing early tetrapodomorphs showing the evolution of habitat according to traditional interpretations. White: marine; grey (green in the electronic version): brackish water; black: freshwater. States were ordered. The phylogeny was compiled using the Stratigraphic Tools (Josse et al. 2006) for Mesquite 2.01 (Maddison & Maddison 2007) using the geological timescale of Gradstein et al. (2004) with trees and taxonomies from Smithson (1980), Foreman (1990), Laurin (1998a, c), Beaumont & Smithson (1998), Laurin et al. (2000), Zhu et al. (2001), Ruta et al. (2002, 2007), Zhu & Yu (2002), Anderson et al. (2003), Laurin (2004), Lebedev (2004), Long & Gordon (2004), Vallin & Laurin (2004), Clack & Finney (2005), Laurin & Soler-Gijoń (2006), Clack (2007) and Ruta & Coates (2007).

that interpretation, most stegocephalian remains are interpreted as autochtonous elements which were not transported far from their habitat. This character includes a strong phylogenetic signal ( p , 0.0001). This optimization differs from the former in that the move from a marine environment to a marginal marine environment probably took place in the smallest clade which includes panderichthyids and stegocephalians. That marginal marine environment appears to have been the cradle of stegocephalian diversification, although that may well be a

taphonomic artefact (this is the environment into which most fossiliferous sediments in which stegocephalians could be preserved were deposited). There is little evidence that some early stegocephalian species were freshwater stenohaline forms, although this could reflect the same taphonomic artefact and could result from the difficulty of demonstrating the freshwater nature of a locality. If we take this evidence at face value, the relative intolerance of most lissamphibians to moderately saline brackish (more than about 10‰) water or


Lissamphibia

Euryodus Brachydectes elongatus

Diplocaulus

Diapsida

Amphibia

268.0 270.6

Kungurian

Ptyonius Sauropleura Microbrachis pelikani Leiocephalikon problematicum Trachystegos megalodon Ricnodon Hylerpeton dawsoni Hyloplesion

Ophiderpeton Phlegethontia

Artinskian

284.4 Sakmarian

294.6 299.0

Tiktaalik Obruchevichthys Elginerpeton Metaxygnathus Jakubsonia Ventastega Acanthostega Sinostega Ichthyostega Densignathus Hynerpeton Tulerpeton

Livoniana

Osteolepididae Eusthenopteron Gogonasus Panderichthys Elpistostege Powichthys thorsteinssoni Diabolepis speratus Youngolepis praecursor

Asselian Gzhelian

303.9 306.5

Kasimovian Moscovian

311.7 Bashkirian

318.1 Serpukhovian

326.4

Visean

Tetrapoda Move onto land?

Roadian

275.6

Adelogyrinidae Adelogyrinidae Lethiscus

Desmatodon hesperis Limnostygis relictus Limnoscelis paludis Limnoscelis dynatis

Hylonomus

Ophiacodon Archaeothyris florensis

Whatcheeria deltae Crassigyrinus Doragnathus Pholidogaster pisciformis Greererpeton burkemorani Colosteus scutellatus Spathicephalus Loxomma allmanni Loxomma rankini Loxomma acutirhinus Megalocephalus pachycephalus Megalocephalus lineolatus Baphetes planiceps Baphetes kirkbyi Baphetes lintonensis Baphetes bohemicus Acroplous Saurerpeton Trimerorhachis Eugyrinus Dendrerpeton acadianum Amphibamus Micromelerpeton Branchiosaurus petrolei Zatrachys Onchiodon frossardi Eryops Cheliderpeton vranyi Iberospondylus Caerorhachis bairdi Eoherpeton Calligenethlon Archeria Proterogyrinus scheelei Discosauriscus

Therapsida

Parareptilia

Reptiliomorpha

Brachydectes newberryi

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345.3

Tournaisian

Loss of caudal lepidotrichia Appearance of pentadactyly

359.2

Famennian

374.5 Frasnian

Appearance of the limbs Stegocephali

385.3 Givetian

391.8 Eifelian

397.5 Emsian

407.0 411.2 Tetrapodomorpha

Pragian Lochkovian

416.0

Fig. 4. Time-calibrated supertree of sarcopterygians emphasizing early tetrapodomorphs showing the evolution of habitat according to recent works (Tables 1 & 2) which reinterpret several localities as marginal marine environments. See Figure 3 for more information. White: marine; grey: brackish water; black: freshwater.

saltwater is an autapomorphy of Lissamphibia which may have appeared in the late Carboniferous or in the Permian (Fig. 4). Even though both optimizations are presented, this does not imply that both are equally supported or plausible. The first (Fig. 3) is presented mostly for its historical interest, and to show how much interpretations have changed in the last 20– 30 years. The traditional interpretation (Fig. 3) is inconsistent with several recent discoveries of clear evidence of at least moderate marine influence of several localities (see above). The alternative (Fig. 4) appears to be much better supported

although it remains, to an extent, conjectural as is usually the case in palaeobiological and palaeoecological studies. The conclusions drawn from the evolutionary analysis of habitat in early stegocephalians were anticipated by Milner (1987, p. 503) who stated that . . .it appears to be most parsimonious to argue that the plesiomorphic tetrapod condition was to be euryhaline. Restriction to freshwater appears to have been a secondary specialization developing once or more within the Temnospondyli and at least once with the non-lysorophian microsaurs.


Similarly, Schultze (1999, p. 388) concluded that ‘The tetrapods entered the terrestrial realm through the intertidal and supratidal zones.’

Palaeobiogeographic evidence Saltwater tolerance for early stegocephalians would resolve the paradox of their extremely wide distribution in the Devonian (Daeschler 2000) at a time in which at least some members of this group have been argued to have been still strictly aquatic (Clack & Coates 1995). Indeed, the first undisputed record of stegocephalians dates from the Frasnian. By the Famennian, they had reached a nearly worldwide distribution; they are found in most of the Old Red Continent (eastern Greenland, European Russia, Latvia, Scotland, North America), in Australia (which was then part of Gondwana; Milner 1993; Daeschler et al. 1994) and northern China which was then isolated (Zhu et al. 2002). Given that the Frasnian and Famennian probably lasted a total of about 26 Ma (Gradstein et al. 2004) and that Australia (and the rest of Gondwana) and northern China may have been isolated from Laurentia and Baltica by a fairly broad oceanic basin (Li et al. 1993), it is difficult to conceive how a stenohaline freshwater group could have spread so far and so fast. However, this difficulty disappears if early stegocephalians were euryhaline (Laurin & Soler-Gijoń 2001; Parker & Webb 2008). Of course, the distribution of the various continental plates in the Late Devonian is still controversial, and Scotese & McKerrow (1990) have argued for close positions of all the land masses on which early stegocephalians have been found. Milner (1993, p. 328) used the maps of Scotese & McKerrow (1990) to argue that terrestrial or freshwaterbased dispersal of stegocephalians could have taken place. Scotese & McKerrow (1990, p. 1) explained that their maps differed from previous maps in that ‘a narrow (rather than a wide) ocean is shown between Laurentia (North America) and Gondwana during the Devonian’. It appears that most of Gondwana was cut off from Laurentia and Baltica by an epicontinental sea (Klapper 1995, fig. 1), even if all these plates were in contact. Therefore, the hypothesis of a strictly terrestrial or freshwater dispersal of stegocephalians and their close relatives in the Devonian does not appear to be supported by the current palaeogeographic evidence, as previously argued by Thomson (1980). The presence of skeletal remains (Metaxygnathus) and of trackways of a stegocephalian in Devonian rocks of Australia (Warren & Wakefield 1972; Campbell & Bell 1977) can best be explained by dispersal through a coastal marine environment. More recently, Daeschler (2000, p. 307) raised the possibility that

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early stegocephalians ‘retained a tolerance of marine conditions and dispersed via marine routes’, based on palaeogeographic arguments. Bray (1985) provided compelling geological and physiological arguments in support of a marine origin of stegocephalians. He pointed out that the palaeoecological interpretation of many fossiliferous localities in which Devonian stegocephalians have been found were dubious. Most of these were previously interpreted as fluviatile, but they could represent tidally influenced environments. Furthermore, many Devonian inland (‘freshwater’) basins may have had higher ion concentrations than most of today’s freshwater bodies because the vegetation cover may have been low; this would have resulted in faster weathering and leaching than in more recent times. The difference in salinity between the marine and ‘freshwater’ environments may therefore have been smaller than today. Thomson (1980) had assumed that inland basins were synonymous with freshwater basins (but still argued that most early sarcopterygians were marine or euryhaline), but Bray (1985) argued that this assumption is unwarranted because these basins could have communicated with marine basins. For instance, a wrench fault system may transect a continent and bring marine influences, as was argued for the East Greenland Basin that was far from the edges of the Old Red Sandstone continent in the Upper Devonian (Ziegler 1981, 1982). These geological arguments by Bray (1985) seriously question the validity of the traditional scenario proposing freshwater origin of stegocephalians.

Physiological and morphological evidence Recent chondrichthyians, lungfishes, coelacanths and lissamphibians possess a full complement of enzymes for the ornithine pathway for producing urea. Furthermore, these taxa share the presence of uraemia (the retention of urea in the blood to increase its osmotic pressure and thereby prevent dehydration in a marine or terrestrial environment). Bray (1985) have argued that this evidence suggests a marine origin for these groups (and of course, two of these still live in the oceans). Actinopterygians generally have an incomplete complement of enzymes for the ornithine pathway, and Bray (1985) interprets this as a partial loss resulting from the long history of this group in freshwater (it is argued that all marine actinopterygians are derived from freshwater ancestors). In this respect, the presence of a full complement of enzymes for this pathway in lissamphibians suggests that amphibians have left the marine environment more recently than actinopterygians (which is congruent with the optimization of

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saltwater tolerance presented above, which suggests that lissamphibians have been restricted to freshwater for less than 330 Ma). Alternatively, this suggests that the ornithine pathway has been retained because of selective pressures exerted by the terrestrial environment (but this explanation applies only to relatively terrestrial lissamphibians). In any case, the presence of an ornithine cycle in lissamphibians suggests either a direct passage from the marine to the terrestrial environments, or only a short intermediate period in which stemamphibians inhabited freshwater environments. When reviewing evidence on whether airbreathing in osteichthyans had appeared in a freshwater or a marine environment and whether the conquest of land among sarcopterygians had started in a freshwater or a marine environment, Graham (1997) found no conclusive answers to these questions. Hypoxia is more often and more regularly a problem in stagnant freshwater than in oceans but sheltered bays, lagoons and even enclosed seas can experience hypoxia. Furthermore, hypoxia is not the only selective pressure that can favour the appearance and maintenance of air-breathing. Farmer (1997, p. 361) indicated that ‘lungs may have evolved in early fishes to support an active lifestyle by supplying oxygen to the heart and enhancing cardiac performance’. This author also pointed to the fact that air breathing is not restricted to (or even highly correlated with) hypoxic freshwater environments. Among actinopterygians several air-breathing groups inhabit coastal areas where this ability enables them to exploit parts of the habitat and resources unavailable to other actinopterygians (Graham 1997). Similar selective pressures may have driven the evolution of early stegocephalians, in which case there is no reason to expect that they would have been stenohaline freshwater forms. In the lissamphibians that tolerate salt- or brackish water, osmotic regulation may involve the external gills. This is suggested in Fejervarya cancrivora (formerly known as Rana cancrivora) by the fact that tadpoles regulate their osmotic concentration. This varies from only 250 m-osmoles/l (milliosmoles per litre; this means 0.001 mole of solute per litre) to more than 900 m-osmoles/l when confronted with an increase in environmental osmotic pressure (Gordon & Tucker 1965, p. 439, fig. 1). On the contrary, the adults are osmoconformers (Gordon et al. 1961). This shows that neither gills nor impervious skin are required for amphibians to tolerate saltwater; the skin of adult Fejervarya cancrivora is fairly permeable (Gordon et al. 1961, p. 663). Study of various ontogenetic stages shows that tadpoles of stages IV to XIX maintain an internal osmotic concentration of about 490 m-osmoles/l

in 80% seawater. In the same environment, that concentration rises from stages XX to XXV (the latter is a fully metamorphosed froglet lacking gills) to become isosmotic with the environment at stage XXV (Gordon & Tucker 1965, p. 441, fig. 2). Since the gills of teleosts are known to be involved in active salt transport, and since the loss of osmoregulation in F. cancrivora coincides with loss of gills in its ontogeny, Gordon & Tucker (1965) suggest that the gills of F. cancrivora are involved in osmoregulation. More recent studies show that, unsurprisingly, kidneys are also important in osmoregulation. They retain urea to increase osmosis in dry or hypersaline environments, at least in Rhinella marina (called Bufo marinus by Konno et al. 2006). Fejervarya cancrivora is probably the lissamphibian with highest saltwater tolerance (Gordon 1962); Gordon et al. (1961, p. 665) reported that tadpoles can tolerate slightly hypersaline concentrations (up to 39‰ salinity, a salt concentration about 20% higher than seawater). Thus, it is probably among the most relevant lissamphibian species to understand saltwater tolerance (or lack thereof) in lissamphibians. External gills are useful for osmoregulation in amphibians, but the presence of gills does not necessarily confer osmoregulatory abilities. Indeed, most tadpoles and anuran larvae have gills, but most cannot tolerate saltwater. Nevertheless, the presence of external gills in larvae of temnospondyls, seymouriamorphs and at least some amphibians (Microbrachis and possibly adelogyrinids and lysorophians) raises the possibility that it conferred these taxa osmoregulatory ability. Along with the occurrence of some body fossils, trackways or burrows of these taxa in brackish or saltwater environments (Schultze 1985; Laurin & Soler-Gijoń 2001, 2006), this suggests that these taxa tolerated saltwater. When they lived in the same environments and lacked gills (which apparently disappeared in ontogeny in seymouriamorphs and probably in most temnospondyls), the adults may have been osmoconformers if they had permeable skin. However, such a relatively permeable skin (a superficial layer of lipids strongly reduces its permeability in some species) may be an autapomorphy of the Lissamphibia. The facts that the most aquatic lissamphibians have a lower skin permeability to water than most terrestrial lissamphibians (Yorio & Bentley 1978) and that even desert anurans can extract moisture from soil in their estivation burrows and secrete cocoons only when the soil becomes especially dry (Cartledge et al. 2006) support this suggestion; skin permeability appears to be adaptative, rather than disadvantageous, for lissamphibians in many terrestrial environments. The skin of stem-tetrapods


and some of the earliest amphibians was probably an effective barrier against water and ion flux (at least in water) for most actinopterygians (Bond 1979), aquatic lissamphibians (Yorio & Bentley 1978) and in amniotes (Pough et al. 2004, p. 236). This issue should not be confused with the problem of dessiccation on land; evaporative water loss in air was probably important in the first terrestrial vertebrates because the differences in efficiency and mechanism of waterproofing of the skin in lissamphibians and amniotes (Lillywhite 2006) suggests that impermeability was achieved independently in amphibians and in reptiliomorphs. Waterproofing structures in the skin of mammals and reptiles also differ, but both possess a series of layers of keratin and lipids in the stratum corneum, which was plausibly present in their last common ancestor. The intolerance to salt- and brackish water in lissamphibians is not nearly as universal as the palaeontological literature suggests (Hunt 1993, p. 93; Poplin 1994, p. 299; Cuny 1995, p. 57; Schoch 1995, p. 113). Some reports of brackish water tolerance in lissamphibians are fairly old (e.g. Hardy 1943; Spuraway 1943) with a few from the 19th century (reviewed in Schmidt 1957), but these works may not have received the attention that they deserve from palaeontologists. Similarly, Pough et al. (2004, p. 234) reported that about a dozen species of urodeles and 60 species of anurans have been reported to inhabit or tolerate brackish water. At least one species (Ambystoma subsalsum) appears to be endemic to the brackish (8.283‰ salinity) lake Alchichica in Puebla, Mexico (Neill 1958, p. 9). Given the low number of herpetologists who study saltwater tolerance of extant lissamphibians and the common neglect of brackish and marginal marine environments by herpetological collectors (Neill 1958, p. 3), this number may still underestimate saltwater tolerance in this taxon.

Discussion The danger of model organisms This review illustrates the need to study a broad variety of extant taxa to understand extinct taxa. Gordon et al. (1961, p. 659) stated that One result of the relatively narrow range of amphibians investigated has been the development of a firm belief that amphibians in general cannot survive for more than a few hours in external media more concentrated than about 300–350 milliosmolar. . . ‘This belief ignores repeated observations in many parts of the world of the occurrences of a variety of [A]mphibia, virtually all anurans, in brackish and even marine environments. . .’

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Milner (1987, p. 500) stated: ‘With a few exceptions, notably the crab-eating frog Rana cancrivora, which inhabits mangrove swamps, all living amphibians are intolerant of brackish or salt water.’ Such statements may underestimate variability in osmotic tolerance in lissamphibians. In fact, even lissamphibian species that lack adaptations for brackish water tolerance (such as Rana pipiens or Rana esculenta) can usually tolerate a salinity of up to 10‰ as adults, although eggs normally require a salinity of less than 5‰ to develop normally (Ruibal 1959).

The importance of nomenclature This paper illustrates the importance of a precise nomenclature and of recognizing only monophyletic taxa (at least, above the species level); osmotic tolerance of lissamphibians differs substantially from that of Palaeozoic amphibians and of limbed stem-tetrapods, which are often called ‘amphibians’ in the literature. It is possible that the recognition of a paraphyletic taxon Amphibia played a role in suggesting and maintaining the long-admitted idea that early stegocephalians were strictly freshwater and terrestrial forms, as suggested by Milner (1987, p. 500).

Vague similarities, phylogeny, parsimony and habitat: a proposed research program Previous interpretations of Palaeozoic fossiliferous localities are difficult to test for several reasons. In some cases, justification for an interpretation was not sufficiently explicit (the lack of obvious marine indicators is implicitly accepted to indicate freshwater). In others, vague similarities with extant taxa coupled with an equally vague nomenclature may have been implicitly used. This may explain many previous statements (Hunt 1993, p. 93; Poplin 1994, p. 299; Cuny 1995, p. 57; Schoch 1995, p. 113) that ‘early amphibians’ (stegocephalians) were essentially freshwater forms. Several other taxa previously used as freshwater and marine indicators may need to be reassessed. For instance, Taylor & Vinn (2006) showed that Palaeozoic calcareous tube-worms previously attributed to the extant annelid Spirorbis (and other related forms) are actually spirorbiform microconchids, an extinct taxon plausibly related to phoronids; the latter are marine lophophorates (Temereva & Malakhov 2006). Although several authors questioned the presence of true Spirorbis in Palaeozoic facies in the 1970s (e.g. Burchette & Riding 1977; Taylor & Vinn 2006), the genus Spirorbis has been included in faunal lists of Palaeozoic localities and palaeoenvironmental implications discussed (see e.g. Falcon-Lang et al. 2006). Extant Spirorbis is a stenohaline marine form

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so that the presumed presence of this genus in Permo-Carboniferous localities has been considered an indication of marine influence (e.g. Cassle et al. 2006). The persistence of a taxon traditionally ranked as a genus from the Carboniferous to the present should in any case have been suspect, since even Lingula, often considered a living fossil, does not occur in the Palaeozoic; fossils previously attributed to this taxon have been reassigned to other genera of the Lingulidae (Emig 2003). Nevertheless, this change in classification of lingulids illustrates, to an extent, the subjective nature of absolute (Linean) ranks (Laurin 2008). Interestingly, Palaeozoic Spirorbis (a microconchid) is a euryhaline form which occurs in the microtidal Joggins (Falcon-Lang et al. 2006), SaarNahe, Saale and Bohemia (Schultze & Soler-Gijoń 2004). Extant (genuine) Spirorbis, and more generally serpulids (which include Spirorbis) and at least some other marine annelids, tolerate a wide range of salinity (Ushakova 2003). It might be useful if the parsimony criterion were used in an explicit phylogenetic context (Fig. 1) to reassess the significance of palaeoenvironmental markers whenever possible. This might be feasible for at least some mollusks, brachiopods and arthropods. Also, all metazoans which do not belong to the crown-groups which appeared before the Devonian (and in some cases, well after) may plausibly have been marine, given that the oceans and seas appear to be the cradle of early metazoan diversification (Barnes 1987; Clarkson 1998). In the absence of the contrary, a marine habitat is a more reasonable null hypothesis than a freshwater habitat, although it should always be tested. Detailed phylogenies are now available for many relevant clades, and some of these include extinct taxa (Wheeler et al. 1993; Waggoner 1996) or include enough morphological characters to enable inference of the position of extinct taxa (Jenner & Schram 1999; Giribet et al. 2001; Collins 2002; Jacobs et al. 2005; Collins et al. 2006); use of parsimony and of an explicit phylogeny might therefore yield additional data. For instance, the tenuous interpretations by vertebrate palaeontologists of several Palaeozoic localities as freshwater environments may have influenced other palaeontologists. The suggestion that in the Devonian, ‘spirorbiform microconchids began to inhabit brackish and freshwater environments in addition to marine settings’ (Taylor & Vinn 2006, p. 227) may rest partly on the interpretation of palaeoenvironmental preferences of stegocephalians. It would be useful to try to resolve the phylogenetic position of microconchids and use the parsimony criterion to assess their environmental preferences. Given the number of problems (noted above) which have marked the freshwater/marine

controversy, such an approach might yield useful new insights. Note that much of the discussion above has treated saltwater tolerance as a discrete character because, when little detailed information is available, this is the only applicable technique. When more quantitative data are available (as for salinity tolerance in some species of lissamphibians and Nereis) however, squared-change parsimony and independent contrasts could conceivably be used to estimate environmental tolerance with confidence intervals. Such techniques were recently used to study body size evolution (Laurin 2004). Another possible approach to determine habitat preference and breadth of ancient organisms might be inference models built upon observable characters which can be shown to be correlated to the relevant environmental variable. However, such models should be applied only within the clades in which such correlations have been tested, as suggested by an extension of the extant phylogenetic bracket principle to continuous characters (Laurin et al. 2004, p. 607).

Habitat and the fossil record The frequent, relative intolerance of lissamphibians to saltwater could explain (at least partly) why their fossil record is so much poorer than that of most other groups of stegocephalians. Stem-amphibians closer to lissamphibians than to lysorophians (or dissorophoids) may have lived away from the coast, possibly in upland environments, from which the fossil record is generally poor. Sediments deposited inland, above the sea level, are much more likely to be eroded quickly than sediments deposited in coastal areas, just below the sea level. Even rocky shores have an extremely poor fossil record because, despite their low altitude, they are areas of erosion (Schultze 1999, p. 373). This could explain the large stratigraphic gap between presumed sistergroups of lissamphibians (which appear in the middle Upper Carboniferous, such as lysorophians and dissorophoids) and the oldest known lissamphibians, such as Triadobatrachus (Rage & Rocek 1989) and Czatkobatrachus (Evans & BorsukBialynicka 1998), from the Early Triassic. That poor record hampers direct comparisons between molecular and palaeontological estimates of the age of Lissamphibia (Zhang et al. 2005), although indirect comparisons show no incompatibility and suggest that the record is sufficiently good to assess the age of origin of several lissamphibian taxa (Marjanovic´ & Laurin 2007).

Habitat of early stegocephalians This review attempts to shed new light on the longdebated problem of the original environment


(marine v. freshwater) of our aquatic ancestors. The problem is far from solved because there is considerable uncertainty about the environment represented by many fossiliferous localities; some authors (Schultze 1985; Schultze & Maples 1992; Cunningham et al. 1993; Schultze et al. 1994; Lebedev 2004) interpret as brackish or marine several localities which are interpreted by others (Zhu et al. 2002; Long & Gordon 2004; Hembree et al. 2005) as freshwater. For instance, Campbell & Bell (1977, p. 372) interpreted as overbank deposits (hence, presumably freshwater) the locality in which Metaxygnathus was found. Yet, some horizons, including the most fossiliferous ones, contain ‘calcareous algal structures of the kind previously reported by Wolf & Conolly (1965)’ (Campbell & Bell 1977, p. 371). These ‘calcareous algal structures’ cannot be identified with certainty; hence, their palaeoenvironmental implications are uncertain (Wolf & Conolly 1965, p. 99). Some stromatolites (oncoids) formed by communities of cyanobacteria, which are often considered ‘algae’, occur in freshwater environments (Ha¨gele et al. 2006). However, calcareous macrophytic ‘algae’ such as rhizophytes are usually found in marine settings (Prothero 2004, p. 440; Biber & Irlandi 2006), normally require high constant salinity to thrive and are major contributors of carbonates (Wefer 1980). Metaxygnathus may therefore have tolerated saltwater. We have revealed many uncertainties and inconsistencies in the palaeoenvironmental interpretation of several Permo-Carboniferous fossiliferous localities. Even only a few fossils of typically marine organisms shed serious doubt about the freshwater nature of a locality, since the bodies of such organisms cannot move far upstream to freshwater continental environments. Tides could conceivably move them slightly upstream of their normal habitat, but only into an estuary where the water would in any case be mainly salty or brackish (freshwater only appears in the uppermost (proximal) zone of the estuary, close to the fluvio-estuarine transition). On the other hand, stegocephalians deposited in such environments may in many cases have been carried at least a short distance by rivers. Nevertheless, the reinterpretation of several localities formerly interpreted as freshwater environments as marine to brackish environments might make more sense to the extent that most sediments deposited relatively high above the sea level in intramontane basins should be far more subject to erosion than sediments deposited slightly below the sea level. Thus, the traditional interpretation of many Permo-Carboniferous localities which have yielded stegocephalians as freshwater, inland and (sometimes) intramontane environments is perhaps

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not the most plausible, in this respect. This question might be profitably explored using sophisticated geological models. The evidence of marine influence in many classical Permo-Carboniferous localities is not all recent. Some evidence has been available for a long time, but was dismissed. For instance, fossils attributed apparently wrongly (Burchette & Riding 1977; Taylor & Vinn 2006) to the marine annelid Spirorbis have been known to occur in Joggins since the mid-19th century (Dawson 1845, 1853). Perhaps the expectation that ‘amphibians’ lived in freshwater led to these interpretations. Schultze (1995, p. 260) similarly explained earlier interpretations of Robinson (Gzhelian, Kansas, USA) as a freshwater locality despite the presence of marine indicators. This would explain why mostly vertebrate palaeontologists interpreted the localities of Robinson and Hamilton as freshwater deposits (Schultze 1995, p. 269). It is not always clear if the stegocephalians lived in the environment into which their remains were deposited. Long-distance transport can usually be ruled out when specimens are well-preserved, complete and articulated, but short transport is extremely difficult to detect. Given the fact that many early stegocephalians were found in coastal areas, it is possible that some were transported a short distance from freshwater bodies near the coast.

The move onto land: from where? It may be appropriate to discuss some recent evolutionary scenarios about the origin of limbed vertebrates and of a terrestrial lifestyle in vertebrates. Graham & Lee (2004, p. 720) recently argued that . . .selection pressures imposed by life in the intertidal zone are insufficient to have resulted in the requisite aerial respiratory capacity or the degree of separation from water required for the vertebrate land transition. The extant marine amphibious fishes, which occur mainly on rocky shores or mudflats, have reached the limit of their niche expansion onto land and remain tied to water by respiratory structures that are less efficient in air and more vulnerable to dessiccation than lungs.

This argument is weak because the failure of amphibious teleosts to colonize more inland habitats may simply result from the presence of tetrapods in these habitats, as indirectly suggested by the extent and diversity of adaptations to life on land in this taxon (Gordon et al. 1969; Graham 1997). Here, an analogy with arthropods may be the best line of argument. Several groups of crustaceans have become terrestrial, but only isopods have succeeded in invading terrestrial habitats located far from the coasts. Most terrestrial crabs live on the coast; several of the most notable exceptions are

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found on islands located sufficiently far from the nearest continent to have few insects and arachnids (such as Guadeloupe; personal observation), although some occur on the continent such as Potamon in the Alborz range (Iran; P. Janvier, pers. comm., 2009). Yet, several primitively marine crustaceans have perfectly functional walking appendages that can be used to walk on land with little or no modification. In this respect, it should be less difficult for arthropods to adapt to terrestrial locomotion than for teleosts, whose paired fins are poorly suited for this task. Despite all this, very few crustaceans have invaded inland habitats, presumably because numerous insects and arachnids already occupy these habitats. This suggests that the failure of mudskippers (Periophthalmidae and close relatives) and other amphibious teleosts to become more fully terrestrial may reflect competitive exclusion, rather than intrinsic limitations of their bauplan or incompatible evolutionary pressures exerted by the intertidal environment. Another possibility is that these teleosts never acquired metabolic adaptations as good as those found in tetrapods to deal with nitrogen excretion outside the water. This possibility is raised by recent works which shows that most amphibious teleosts are ammonotelic (they produce ammonia, which is toxic and difficult to excrete in air) rather than ureotelic (Ip et al. 2004, p. 774). One of the few exceptions is Periophthalmus sobrinus, which excretes about as much urea as ammonia and can shift towards ureotelism when out of the water (Gordon et al. 1969). The infrequent occurrence of ureotelism in amphibious actinopterygians appears to be linked partly to its metabolic cost, which may be prohibitive in most teleosts species which developed alternative strategies for dealing with nitrogenous waste when out of the water (Ip et al. 2004). Finally, Graham & Lee’s (2004) analysis seems to rest on the hypothesis of ‘tetrapod land life selection being driven by alternating (likely seasonal) periods of rain and drought.’ That scenario was popular through much of the 20th century but has been discarded because, among other reasons, the redbeds on which that hypothesis rests are now known not to require seasonal aridity to form (Czyscinski et al. 1978; Laurin et al. 2007). This therefore deprives Graham & Lee’s (2004) hypothesis from geological support. Other arguments against a marine origin of terrestrial vertebrates proposed by Graham & Lee (2004) are similarly of limited value. Their argument (p. 727) that the waves exert an evolutionary pressure to increase body density is interesting, but it would not apply to most mangrove and lagoonal habitats. It might also apply less to large taxa (about 1 m body length) than to the much smaller

mudskippers, most of which are less than 15 cm in length (Graham & Lee 2004, p. 727). Thus, the reliance of extant tetrapods on lung ventilation is not a strong argument against their origin from coastal areas because the lung is probably an osteichthyan synapomorphy (Sullivan et al. 1998). It is not established that Devonian stegocephalians had larger or more complex lungs than their finned sarcopterygian relatives. Lung complexification in tetrapods may have occurred shortly before the origin of the crown-group, whose composition is controversial (Laurin 1998a, b; Ruta et al. 2003; Vallin & Laurin 2004; Ruta & Coates 2007) but which probably appeared only in the Early Carboniferous. Under some topologies, a terrestrial lifestyle may have been acquired in stem-tetrapods well before the origin of the crown because seymouriamorphs and several temnospondyls, which may be stem-tetrapods, appear to have had terrestrial adults (Sumida et al. 1998; Sullivan & Reisz 1999; Laurin 2000; Laurin et al. 2004). This brief discussion suggests a marginal-marine origin of terrestrial vertebrates, and reveals weaknesses in arguments that were presented to refute this hypothesis. However, the large amount of uncertainty in the data plainly shows that much additional work is required to reach a wellcorroborated resolution. This will probably not be easy because similar controversies affect the habitat of other Palaeozoic taxa such as ostracodes; the oldest (Devonian) occurrence of that taxon in presumed freshwater is partly supported by association with ‘freshwater fishes’ (Friedman & Lundin 2001, p. 73)! We thank P. Janvier and G. Cle´ment for numerous suggestions which substantially improved the text. This research was funded by the CNRS and the French Ministry of Research (grants to UMRs 7179 and 7207). Funds for work in the Puertollano basin were provided by DGES projects PB95-0398 and PB98-0813 (MEC, Spain) and BET2002-1430 (Spanish Science and Technology Ministry).

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Index Page numbers in italic denote figures. Page numbers in bold denote tables. abietane 19, 27 acanthodians 113 Acanthostega 130, 133 habitat 155 Stensio¨ Bjerg 93, 97, 102–105 Acanthostega gunnari 123, 130 acritarchs and decline of pCO2 38, 42–43, 44–46 genus and species richness 39, 44 Acroplous, habitat 156, 161– 162 actinopterygians 113, 123, 167–168 adaptation evolutionary 8 for terrestrialization 11, 12–15 Aeronian cryptospores 50 miospore colonization 53 Aeronian-Telychian event, miospore biodiversity 50–51 aestivation 145, 146, 147 Africa, north, Devonian, plant assemblage 81– 82 Agda Dal Formation 94, 95 Ageleodus pectinatus 121, 122, 124 Aglosperma 118 Aglosperma avonensis 74 Aglosperma quadrapartita 74, 119 Aglosperma-type seeds 73– 74, 76 agnathans 113 Aina Dal Formation 94, 95, 97 air-breathing 114, 134, 168, 172 algae, charophycean, origin of land plants 39 algaenan 15, 25 aliphatization 25–26 amber 17– 18, 25 Ambitisporites 49, 53 Ambystoma subsalsum 169 ammonotelism 172 Amphibamus, habitat 157 amphibians osmoregulation 168 phylogeny 152–154 see also lissamphibians anemochory 74 Aneurophytales 68, 81, 84, 85, 86 Gondwana 89 Aneurophyton germanicum 87 Aneurophyton maroccanum nov. sp. 82 comparison with Rellimia 84 Aneurophyton olnense 87 anoxia 113–114 anurans 152, 154, 169 Apateon 139–147 bone histology 140, 141 bone-growth rate 143, 144, 145 palaeoecological influences 146– 147, 163 skeletochronology 145–146 Apateon caducus 140 bone-growth features 144, 145 influence of palaeoecology 146

palaeohistology and bone deposition 140, 141, 143 skeletochronology 146 Apateon pedestris 140 bone-growth features 144, 145 bone-growth features, influence of palaeoecology 146 palaeohistology and bone deposition 140, 141, 143 skeletochronology 146 Apiculatisporites microconus 131 apoxogenesis 64, 65, 67 arachnid, trigonotarbid 118 arborane 20 arborescence 41 Archaea, skeletal material 20 Archaeopteridales 60, 61, 81 Archaeopteris 60, 61, 63, 66, 67, 81 ecology 75, 76, 77 Red Hill 119, 120, 122, 123– 124 Archaeopteris halliana 119 Archaeopteris hibernica 118, 119 Archaeopteris macilenta 118, 119 Archaeopteris obtusa 119 ‘Archaeopteris’ rotundifolia nov. sp. 82 Archaeosperma arnoldii 74 Archaeothyris florensis, habitat 158 Archaeozonotriletes 50 Archaeozonotriletes variabilis 131 Archanodon 122 Archeria, habitat 157, 161 aromatics 22–24 arthropods chitin 21–22 desiccation management 13 herbivory 112 –113 Red Hill 118, 120 seed dispersal 74 trackways 118, 120 water-land transition 7, 171–172 Ashgill cryptospores 49 miospore colonization 52, 53 Asteroxylon elberfeldense 82 Australia, SE, tetrapods, biostratigraphic distribution 131–132 Avalonia, first embryophytes 51– 52, 53 avulsion cycles 115–116 Bacteria, skeletal material 20–21 Baggy Beds, spermatophytes 73, 75 Ballyheigue, spermatophytes 73 Baltica, miospore colonization 52, 53 Baphetes bohemicus, habitat 156 Baphetes kirkbyi, habitat 156 Baphetes lintonensis, habitat 156 Baphetes planiceps, habitat 156 barinophytes 118, 119 Barinophyton obscurum 119 Barinophyton sibericum 119, 124

182 Baur, G. The Stegocephali (1896) 6 Belgium placoderms 133 spermatophytes 71– 72, 75–76, 77 beyerane 14, 19, 27 biodiversity, evolution, miospores 50–51 biogeochemical cycles 113 biomass, carbon 40–42 biopolymers aliphatic 15– 17 skeletal 20–24 biosynthesis, pathways, and terrestrialization 11, 15 Bohemian basin, palaeoenvironment 162, 163 bones, Apateon bone-growth rate 143, 144, 145 palaeoecological influence 146–147, 163 palaeohistology 140, 141, 143 Boskovice Furrow 160, 162 Bothriolepis 123, 131, 132, 133 Botryococcus braunii desiccation management 13 organic molecules 15, 25 Brachydectes elongatus, habitat 158, 162 branchiosaurids 139 Branchiosaurus petrolei, habitat 157 Britta Dal Formation 93, 94, 95, 97 climatic cycles 97, 100, 103 plant macrofossils 105, 106 sand bodies 97, 99–100, 103 sedimentary environment 96, 97, 98, 99–101 vertisols 97, 98, 100, 101, 104 bryophytes desiccation management 13 thalloid 39, 40, 41–42, 44 Bufo marinus see Rhinella marina cadalene 14, 19, 27 cadinane 18, 19, 27 Caerorhachis bairdi, habitat 157 Cairoa lamanekii 87 Calamophyton 60, 61, 62, 63, 66 Calligenethlon watsoni, habitat 157 cambium bifacial 81 vascular 84 Canowindra fish assemblage 132 Caradoc cryptospores 49 miospore colonization 53 carbon, sequestration 38, 41, 43–44 carbon cycle 40–41, 44 carbon dioxide atmospheric drawdown 59–60 effect of terrestrialization 37–46 fluctuation 113 and terrestrialization 37–46 oceanic 37 see also pCO2 Catskill Delta Complex, Red Hill 111– 125 Catskill Formation 114 –115 cellulose 21 Celsius Bjerg Group 93–107 plant macrofossils 105, 106, 107

INDEX sedimentary environments 94, 96, 97 tetrapod environments 102– 107, 131 Cephalopteris 105 Cephalopteris tunheimensis 107 Chambers, R. Vestiges of the Natural History of Creation (1844) 6 charcoal, Red Hill 119, 122 Cheliderpeton vranyi, habitat 157 China, North, tetrapods 131 chitin 20–22 Chlorophyta, desiccation management 12, 15 choanae 6, 7 Cladoxylon 62, 63, 67 Cladoxylon taeniatum 67 Cladoxylopsida 60, 61, 62 arborescent habit 62–67, 66 stem growth model 64, 66– 67 structure and growth patterns 65–66 vascular system 62, 63, 64, 65– 67 Cloghnan Shale 132 CO2 see carbon dioxide coal diterpenoids 19– 20 n-alkanes 13, 15 Colosteus scutellatus, habitat 156 Combyingbar Formation 131 Condrusia brevis 74 Condrusia minor 74 Condrusia rumex 74 Condrusia-type seeds 73, 74, 75, 76 Cooksonia caledonica 55 Cooksonia pertoni 54 Cooper Creek, analogue for Britta Dal Formation 100 coorongite 25 Cordaianthus devonicus 82 Cordaites, fernane 20 cortex 67 coumaryl 22–23, 28 cracking 24 Crassigyrinus, habitat 156 Crossia 84 crossopterygians 6 cryptospores 13, 14, 40 dispersal 51 oldest 49, 51– 52 Ordovician 49 Ctenacanthus 121, 123, 162 Cumberland Marshes, Saskatchewan River, analogue for Red Hill sedimentation 115 Cuneognathus 102 Cuneognathus gardineri 131 cupules, seed plants 74, 120 cutan 15, 25–26 cutin 15, 25– 26 Cutler Formation, palaeoecology 163– 164 Cyanobacteria desiccation management 12 in evolution of land plants 39, 40, 41 mats 40, 41 Cyclostigma 60, 61, 107 Czatkobatrachus 170 Dechra Aı¨t Abdallah, Devonian plant assemblage 81– 82 degradation, organic matter 24

INDEX degradation-recondensation pathway 24 Dendrerpeton acadianum, habitat 156, 162 Densignathus 133 habitat 155 Densignathus rowei 121, 123 depocentres, late Devonian 114 desiccation management lipids 12– 15 long-chain aliphatics 12–16 vertebrates 169 Desmatodon hesperis, habitat 158 detritivores, Red Hill 122 Devonian miospores 51 plant assemblages, North Africa 81– 89 ‘plant hypothesis’ 59 trees 59– 68, 60 height-diameter relationship 61 Devonian, Late extinctions 113 palaeoecology, Red Hill site 111 –125 seed plants, radiation 71–77 tectonics and depocentres 114 tetrapods, East Greenland 93–107 Devonian-Carboniferous boundary 131 Diabolepis speratus, habitat 155 diagenesis 24 Dimetrodon, habitat 161 dinoflagellates, aliphatization 25 dinosporin 22 dinosteroids, triaromatic 12 Diplocaulus, habitat 157, 161, 162 dipnomorph clade 113 Discosauriscus, habitat 157 dispersal cryptospores 51 seed plants 74, 75 diterpenoids 19– 20 Doragnathus, habitat 156 Dorinnotheca streelii 74 Dorinnotheca-type seeds 73, 74, 75, 76 drimane 18, 27 Duisbergia, stem 64, 66– 67 East Kirkton tetrapod fauna 113– 114 ecosystems, marine, effect of terrestrialization 37–46 Eifelian, Dechra Aı¨t Abdallah 81– 82 Elginerpeton 130, 133, 134 habitat 155 Elkins, spermatophytes 72, 75, 124 Elkinsia polymorpha 74, 76 elpistostegalians 6, 112 –113, 132 –133 Elpistostege, habitat 155, 160 Elsa Dal Formation 94, 95, 97 embryophytes desiccation management 12 oldest cryptospores 49, 51, 54 origin 41 phylogeny 6, 54 Emphanisporites micrornatus var. micrornatus 53–54 Emsian, Dechra Aı¨t Abdallah 82 entropy, demographic 76– 77

Eoherpeton, habitat 157 Eospermatopteris 60, 61, 63 growth patterns 64, 66– 67 epidogenesis 64, 65, 67 Equisetopsida 60, 61 Eryops, habitat 156, 161 eudesmane 14, 18–19, 27 Eugyrinus, habitat 156 Euphyllophytes 60, 61 Euramerica, tetrapods 133 –134 Euryodus, habitat 157 Eusthenodon 124 Eusthenopteron 6 habitat 155, 160 Eutracheophytes 86 Evieux Formation, spermatophytes 71–72, 75–76, 124 Eviostachya hoegii 76 extinction, Late Devonian 113 Famennian fish 132 Red Hill 118, 124 spermatophytes 71– 73, 77 stegocephalians 167 tetrapods 130, 134, 135 Fejervarya cancrivora 161, 168, 169 femur, Apateon 140, 141, 143, 144 fernane 20, 28 Filicopsida 60, 61 fin-limb transition 6– 7, 113 fish-tetrapod transition 6–7, 131, 132, 134 climate 134– 135 flavonoids 27 signalling and warfare 17 UV protection 15–16 Foozia 62 forestation 41 fossils see macrofossils; mesofossils; taphofacies Frasnian fish 132 spermatophytes 71 stegocephalians 167 tetrapods 129–130, 134, 135 Frasnian-Famennian biotic event 131 friedelane 20, 28 galeaspids, Zhongning Formation 131 gametophyte generation 112 gammacerane 20, 28 Gauss Halvø 93, 94, 97, 102 climatic cycles 97, 100, 103 tetrapod biostratigraphy 130– 131 Geminospora lemurata 131 gene expressions 8 Genoa River trackway assemblage 131 GEOCARB III model 38–46 geochemistry, organic 11–27 Geoffroy St Hilaire, E., on evolution of fish 6 Gigantocharinus szatmaryi 120, 121, 122 Gilboa trees 61, 67–68 Gillespiea 118, 124 Gillespiea randolphensis 76, 119 gills, osmotic regulation 168

183

184 Givetian origin of tetrapods 132 spermatophytes 71 Glamorgania gayerii 74 Glenisla tetrapod trackway 132– 133 Gloeocapsamorpha prisca 25 gnathostomes 113 Gogonasus, habitat 155 Gondwana Aneurophytales 89 colonization by land plants 51, 52, 53, 54–55 Late Devonian 167 Granditetrasporites zharkovae 71 Greenland, East Late Devonian tetrapods 93– 107 tetrapods, biostratigraphical distribution 130–131 Greererpeton burkemorani, habitat 156 Groenlandaspis 132 Groenlandaspis mirabilis 131 Groenlandaspis pennsylvanica 121, 122 guaiacyl 22–23, 28 gymnophionans 152, 154 Gyracanthus cf. Gyracanthus sherwoodi 118, 121, 122 Haeckel, E., Generelle Morphologie der Organismen (1866) 6 Hangenberg Sandstein, spermatophytes 73 Harder Bjerg Formation 95, 102 Heptophyta, earliest mesofossil 54 herbivory, arthropods 112–113 heterospory 112 hibernation 145, 146–147 Hirnantian glaciation, miospore biodiversity 50 Holoptychius 102, 123, 131, 133 Homerian, cryptospores 50 hopanoids 20 humerus, Apateon 140, 141, 143, 144 Huxley, T.H., fish classification 6 hydrochory 74 Hyenia cf. elegans 82 Hylerpeton dawsoni, habitat 157 Hylonomus, habitat 164 Hyloplesion, habitat 157 Hyneria lindae 118, 121, 123, 124 Hynerpeton 130, 133 habitat 155 Hynerpeton bassetti 120, 121, 123 hypoxia 168 Iberospondylus, habitat 156, 162 Ichthyostega 6, 93, 97, 130, 133 habitat 155 Sederholm Bjerg 93, 94, 98, 102 Ichthyostega eigili 130 Ichthyostega stensioei 130 Ichthyostega watsoni 130 Isoetales 119 Jakubsonia 130, 133, 134 habitat 155 Jemalong fish-tetrapod assemblage 132 Joggins, habitat 159, 162

INDEX Katschenko’s line 140 kaurane 14, 19, 20, 27 Kerrya mattenii 74 kidneys, osmoregulation 168 Knoppenbissen Formation, Refrath borehole 76 Lamarck, J.-B. Philosophie Zoologique (1809) 5 Laurentia, miospore colonization 52, 53 Laurussia Aneurophytales 89 Pseudosporochaleans 68 Leiocephalikon problematicum, habitat 157 Lenlogia krystofovichii 74 Lepidodendropsis 118, 119 Lepidosigillaria 60, 61 lepospondyls, salt tolerance 152– 154, 161– 162 Leptophloeum 60, 61 Lethiscus, habitat 157 Libya, miospore colonization 52, 53 lignans 17 lignin 22–24, 25, 59– 60 lignophytes 60, 61, 81– 89 distribution 89 heterospory 112 origin 40, 41 phylogenetics 86 limbs see fin-limb transition Limnomis delaneyi 118, 120, 121, 123 Limnoscelis dynatis, habitat 158 Limnoscelis paludis, habitat 158 Limnostygis relictus, habitat 158 lipids aliphatization 25–26 analysis 12 long-chain, desiccation management 12–15 lissamphibians habitat 154, 160– 161, 163, 165–166, 169– 170 ornithine pathway enzymes 167– 168 osmoregulation 168 Livoniana, habitat 155 Llandovery, miospore colonization 52, 53 Llanvirn, cryptospores 49, 51–52 Lochkovian cryptospores 51 miospore assemblages 55 miospore biodiversity 50–51 trilete spores 50, 51 Lohsania, habitat 164 Lorophyton 62 Loxomma acutirhinus, habitat 156 Loxomma allmanni, habitat 156 Loxomma rankini, habitat 156 Ludlow, trilete spores 50 lungfish 6, 113, 123, 152 lungs 168, 172 lupane 20, 28 Lycophyta 55, 60 lycopsids 60, 61, 68, 112 Celsius Bjerg Group 105, 106, 107 Red Hill 118, 119 macrofossils 54– 55 plant, Celsius Bjerg Group 105, 106, 107

INDEX macromolecules 16–17, 20– 22, 24, 25–26 analysis 12 desiccation management 15 Maillet, B. de, Telliamed (1766) 5 Massif Central, palaeoenvironment 162, 163 megafossils 14, 54– 55 desiccation management 13, 15– 16 Megalichthys 6 Megalocephalus lineolatus, habitat 156 Megalocephalus pachycephalus, habitat 156 megasporangia 112 menetogenesis 64, 67 mesofossils 54– 55 Metaxygnathus 130, 131, 132, 133 habitat 155, 167, 171 microbial mats see Cyanobacteria, mats Microbrachis pelikani, habitat 158 Micromelerpeton, habitat 157 Miller, H. Footprints of the Creator (1849) 6 miospores biodiversity evolution 50– 51 colonization of land 51–53 Ordovician-Lochkovian 49–50 Zhongning Formation 131 miRNAs 8 monilophytes 6 monoterpenoids 18 Moresnetia zalesskyi 71, 74 Moresnetia-type seeds 73–74, 75– 76, 118 Morocco, Devonian plant assemblage 81–82 mudskippers, habitat 172 myriapod, archidesmid 118 n-alkanes, desiccation management 13, 14, 15 Nannochloropsis, n-alkanes 13 Nathorst Bjerg 93, 94, 96, 99, 102, 103 Obruchevichthys 130, 133, 134, 155 Obrutschew Bjerg Formation 94, 101– 102 Devonian-Carboniferous boundary 131 plant macrofossils 106, 107 Old Red Sandstone Continent 133 miospore assemblages 54, 55 oleanane 20, 28 Onchiodon, habitat 157 Ophiacodon, habitat 158, 161, 164 Ophiderpeton, habitat 157 Ordovician, cryptospores 49, 52 organic matter analysis 12 degradation 24 preservation 24– 25 Red Hill 122 sequestration 38, 41, 43– 44 ornithine pathway 167– 168 Orsadesmus rubecollus 120, 121, 122, 124 osmoregulation 168 osteogenesis Apateon 145 Osteolepididae, habitat 155 Otzinachsonia beerboweri 118, 119 oxygen, atmospheric, fish-tetrapod transition 134– 135

palaeobiogeography, stegocephalians 167 palaeoecology and bone-growth, Apateon 146–147 Red Hill 111–125 sedimentation 114–118 stegocephalians 154, 155–160, 160–172 palaeogeography, miospore distribution 52 Palynodata database 38, 39 Panderichthys 133 habitat 155, 160 Paralleldal 93, 94, 97 climatic cycles 97, 103 Ichthyostega 102 parsimony, sarcopterygians 152– 154, 170 pCO2 37–38 and decline in Acritarcha 38, 42– 43, 44– 45 and rise of land plants 38– 42, 43–44 peptidoglycans 20–22 Permian, Apateon 139–147, 142 pH, oceanic 37–38 Phacopidae 81 phenols, lignin 22–23 phenylpropanoid pathway 17, 22, 23 Phlegethontia, habitat 157 phloem, secondary 61, 81, 84 phlorotannins 17 Pholidogaster pisciformis, habitat 156 photosynthesis, earliest 12 phyllocladane 14, 19, 20, 27 Phyllolepis rosimontina 121, 122 phytoplankton, decline of pCO2 38, 44–46 Pietzschia 60, 61, 62, 63 structure and growth patterns 64, 65– 66, 67 Pietzschia levis 65 Pietzschia schulleri 65 pimarane 19, 27 placoderms 113, 118, 122 age 132, 133 last occurring 131 plants, land and decline of pCO2 38–42, 43– 44 Devonian 59– 68, 60 origin 39– 40 Palaeozoic, phylogenetic tree 60 see also seed plants podocarpane 19, 27 pollen 23 polymerization, oxidative 24, 25, 26 polypteriforms 6 polysaccharides 21–22 porolepiforms 113 Powichthys thorsteinssoni, habitat 155 preservation pathways, organic matter 24– 25 Pridoli, trilete spores 50 proanthocyanidins 17 Probarinophyton 119 Profile Ravine 98 progradation 115 propagules 74, 77 dispersal 75 Proteokalon petryi 87 Proterogyrinus scheelei, habitat 157 Pseudobornia 60, 61

185

186 Pseudosporochnales distribution 68 habit 67– 68 morphology 62, 63, 65 Pseudosporochnus 60, 61, 62, 68 Pseudosporogonites hallei 74 Psilophyton princeps 82 Pteridospermopsida 18 Ptyonius, habitat 157 Puertollano Basin, habitat 156, 160, 162 Puertollanopus microdactylus 162 radiation, evolutionary 7– 8 Rana cancrivora see Fejervarya cancrivora Red Hill age of deposit 118 fauna 118, 120, 121 flora 118, 119, 120 habitat distribution 118 palaeoecology 111–125 fire dynamics 119, 122 organic debris 122 trophic structure 122 –123 vegetation 118– 119 sedimentation model 114–116 spermatophytes 72, 75 taphofacies 116–118 Refrath borehole 76 Reimannia aldenense 87 Rellimia, Dechra Aı¨t Abdallah 82–89, 83, 84, 85 comparison with other Aneurophytales 84 fertile organs 84, 85 Rellimia thomsonii 84, 85, 87–88 Remigolepis 132, 133 Remigolepis major 131 Remigolepis microcephala 131 Remigolepis xiangshanensis 131 Remigolepis xixiaensis 131 Remigolepis zhongningensis 131 Remigolepis zhongweiensis 131 reptiliomorphs, saltwater tolerance 152, 154 resinite 17–18 resins 17–18 retene 14, 19–20, 27 Retispora lepidophyta 95, 101 Rhabdosporites langii 85, 86, 89 Rhacophyton 75, 76, 118, 119, 122, 124 Rhacophyton ceratangium 119, 120 Rhinella marina, osmoregulation 168 Rhipidophyton 68 rhizosphere 40–41, 44 Rhuddanian, cryptospore assemblages 50 Ricnodon, habitat 157 Romer’s Gap 113, 134 rooting 40– 41 roots 64 Pietzschia 65 and plant size 59– 60 Rubisco efficiency 45, 46 Runcaria heinzelinii 71 Saale basin, palaeoenvironment 160, 162, 163 Saar-Nahe Basin Apateon 140, 142 palaeoecology 146 –147, 162–163

INDEX Sagenodus, habitat 164 salinity, and biodiversity 151 saltwater, tolerance of, stegocephalians 151 –172 sand bodies, Britta Dal Formation 97, 99– 100, 103 sandstone, Stensio¨ Bjerg, Acanthostega 103– 105 sarcopterygians 6 –7, 113, 120, 123 elpistostegalian 6, 112– 113, 132– 133 habitat evolution 165, 166 parsimony 152– 154 Saudi Arabia, miospore colonization 49, 50, 51, 52, 53 Saurerpeton, habitat 156 saurerpetonids, salt tolerance 162 Sauropleura, habitat 157 Scougouphyton abdallahense 82 Sederholm Bjerg, Ichthyostega site 93, 94, 98, 102 sedimentation, Red Hill 114–116 seed plants Aglosperma-type 73, 74, 76 Condrusia-type 73, 74, 75, 76 dispersal 74, 75 Dorinnotheca-type 73, 74, 75, 76 early ecology 75–76 ecological hypothesis 76– 77 Moresnetia-type 73–74, 75– 76, 118 radiation 71– 77, 112 Warsteinia-type 73, 74 selection, evolutionary 7 sequestration, carbon 38, 41, 43– 44 serratane 20, 28 sesquiterpenoids 18– 19 Seymouria, habitat 161 seymouriamorphs, habitat 154, 163 shale, black 113 signalling, molecular 17– 18 Silurian macrofossils 54 miospores 50 simonellite 19–20, 27 Sinolepis assemblage 131 Sinolepis szei 131 Sinostega 129 –130, 131, 133, 134 habitat 155 skeletochronology, Apateon 145– 146 skeletons 11, 20–24 Soederberghia groenlandica 132 Spathicephalus, habitat 156 Spermasporites allenii 71 spermatophytes see seed plants Spirorbis 169, 170 spores 23 trilete, Ordovician 49–50, 53 sporophyte generation 112 sporopollenin 11, 22, 25 synthesis 23 stauripterids 118, 119 Stauripterus 121 stegocephalians palaeoecology 154, 155–160, 160–164 evolutionary analysis 164–167 palaeobiogeography 167 parsimony 152– 154 saltwater tolerance 151– 172 stem-tetrapods 154, 169 stems cladoxylopsida 64

INDEX growth model 66– 67 Pietzschia 65–66 Stenokoleales 81, 84 Stenokoleos 84 Stensio¨ Bjerg 93, 94 Acanthostega 93, 97, 102– 105 Stensio¨ Bjerg Formation 94, 95, 101 plant macrofossils 105, 106, 107 sandstone 103– 105 Streelispora newportensis 53–54 Struveaspis maroccanum 82 Styliolina 82 stylopod diaphyseal palaeohistology, Apateon 140, 143 suberin 16–17 sulphurization pathways 24, 26 Synorisporites 49 syringyl 22–23, 28 Taffs Well, spermatophytes 73, 75 tannins 17, 27 taphofacies, Red Hill 116– 118 tectonics, late Devonian 114 teleosts, habitat 172 Telychian, miospores 50 biodiversity 50–51 temnospondyls 6, 139–147, 152–154, 161 Tentaculita 81, 82 terpenoids 17, 18–20 terrestrialization 7– 8 early ideas 5 –6 evolution 39–40 and organic geochemistry 11–27 Tetraedron, algaenan 25 Tetrahedraletes medinensis 52 tetrapods biostratigraphical distribution 129–135 earliest diversification 132– 135 ecological models 124– 125 environments, East Greenland 93– 107 evolution 6, 113 origin 132–133 Red Hill 123 water-land transition 6 –7 Tetraxylopteris, comparison with Rellimia 84 Tetraxylopteris reposana 85, 86, 88 Tetraxylopteris schmidtii 85, 88 Tiktaalik, habitat 155, 160, 164 Tournaisian, seed plant dispersal 75 tracheophytes earliest macrofossil 54 origin 40, 41 Trachystegos megalodon, habitat 157 trackways arthropod 118, 120 tetrapod 131, 132 –133, 134, 162 trees, Devonian 59– 68 height-diameter relationship 61 Triadobatrachus 170 Triloboxylon, comparison with Rellimia 84 Triloboxylon arnoldii 88 Triloboxylon ashlandicum 85, 88 Trimerorhachis insignis, habitat 156, 161– 162 triterpenoids 20 Triturus marmoratus, bone-growth features 145, 146– 147

Tulerpeton 130, 133 palaeoecology 154, 156, 160 Turrisaspis elektor 118, 121, 122 Twofold Bay Formation 131 United Kingdom, miospore colonization 49, 50, 52, 53 uraemia, marine environment 167 urea, osmoregulation 167, 168 ureotelism 172 urodeles 152, 154, 169 ursane 20, 28 UV protection adaptation 11 flavonoids 15– 16 vegetation evolution 38–42, 42, 43– 44 Ordovician-Lochkovian 49–55 Ventastega 130, 133 habitat 155, 160 Ventastega curonica 123 Verruciretusispora magnifica 131 vertebrates Devonian 113 Red Hill 118, 122– 123, 124 water-land transition 6– 7, 171 –172 vertisols, Britta Dal Formation 97, 98, 100, 101, 104 Viriatellina 82 Viriatellina pseudogeinitziana armoricana 82 Viseán, terrestrial vertebrates 113 warfare, molecular 17– 18 Warsteinia paprothii 74 Warsteinia-type seeds 73, 74 water-land transition 5 –8, 113, 171– 172 Wattieza 60, 62, 68 stem 64 wax, desiccation management 13, 15 weathering, chemical, and root growth 41, 42 Wenlock cryptospores 50 miospore colonization 53 Whatcheeria deltae, habitat 156 Wimans Bjerg Formation 94, 95, 96, 97 wind, seed disperal 74 Xenacanthus 161, 162 Xenocladia 62, 63, 67 Xenotheca bertrandii 74 Xenotheca devonica 74, 75 xylem 64, 66 Pietzschia 65 secondary 61, 67, 84, 86 Ymer Ø, Britta Dal Formation 96, 100 tetrapods, biostratigraphical distribution 130– 131 Youngolepis praecursor, habitat 155 Zatrachys, habitat 157, 161 Zhongning Formation, biostratigraphy 131 zoochory 74 Zosterophyllum 13 zygopterids 112, 119

187

The invasion of the land by plants (‘terrestrialization’) was one of the most significant evolutionary events in the history of life on Earth, and correlates in time with periods of major palaeoenvironmental perturbations. The development of a vegetation cover on the previously barren land surfaces impacted on the global biogeochemical cycles and the geological processes of erosion and sediment transport. The terrestrialization of plants preceded the rise of major new groups of animals, such as insects and tetrapods, the latter numbering some 24 000 living species, including ourselves. Early land-plant evolution also correlates with the most spectacular decline of atmospheric CO2 concentration of Phanerozoic times and with the onset of a protracted period of glacial conditions on Earth. This book includes a selection of papers covering different aspects of the terrestrialization, from palaeobotany to vertebrate palaeontology and geochemistry, promoting a multidisciplinary approach to the understanding of the co-evolution of life and its environments during Early to Mid-Palaeozoic times.

The Terrestrialization Process: Modelling Complex Interactions at the Biosphere-Geosphere Interface (Geological Society Special Publication 339)

Geological Data Management (Geological Society Special Publication)

Geoarchaeology: Exploration, Environments, Resources (Geological Society Special Publication, No. 165) (Geological Society Special Publication, No. 165)

Australian Landscapes (Geological Society Special Publication 346)

Martian Geomorphology (Geological Society Special Publication 356)

Sustainable Groundwater Development (Geological Society Special Publication,)

Early Precambrian Processes (Geological Society Special Publication)

Phanerozoic Ironstones (Geological Society Special Publication)

Slope Tectonics (Geological Society Special Publication 351)

Structurally Complex Reservoirs - Special Publication no 292 (Geological Society Special Publication)

The Physics of Explosive Volcanic Eruptions (Geological Society Special Publication)

The Making of the Geological Society of London (Geological Society Special Publication No. 317)

Human Interactions with the Geosphere: The Geoarchaeological Perspective (Geological Society Special Publication 352)

The Evolving Continents: Understanding Processes of Continental Growth - Special Publication 338 (Geological Society Special Publication)

Orogenic Processes: Quantification and Modelling in the Variscan Belt (Geological Society Special Publication, No. 179)

Sedimentary Response to Forced Regression (Geological Society Special Publication)

Volcanic Degassing (Geological Society Special Publication No. 213)

Fractured Reservoirs (Geological Society Special Publication no 270)

Hydrocarbons in Contractional Belts (Geological Society Special Publication 348)

History of Palaeobotany: Selected Essays (Geological Society Special Publication)

Palaeoproterozoic Supercontinents and Global Evolution (Geological Society London, Special Publication)

Forensic Geoscience: Principles, Techniques And Applications (Geological Society Special Publication)

Confined Turbidite Systems (Geological Society Special Publication No. 222)

Deformation of Glacial Materials (Geological Society Special Publication No. 176)

Lacustrine Petroleum Source Rocks (Geological Society Special Publication)

Palaeozoic Reefs and Bioaccumulations: Climatic and Evolutionary Controls - Special Publication no 275 (Geological Society Special Publication)

Devonian Events and Correlations : Special Publication no 278 (Geological Society Special Publication)

Communicating Environmental Geoscience - Special Publication no 305 (Geological Society Special Publication) (No. 305)

Fractal Analysis for Natural Hazards - Special Publication No 261 (Geological Society Special Publication)

Mineral Deposits & Earth Evolution (Geological Society Special Publication)

Sedimentary Response to Forced Regression (Geological Society Special Publication)

The Terrestrialization Process: Modelling Complex Interactions at the Biosphere-Geosphere Interface (Geological Society Special Publication 339)

Geological Data Management (Geological Society Special Publication)

Geoarchaeology: Exploration, Environments, Resources (Geological Society Special Publication, No. 165) (Geological Society Special Publication, No. 165)

Australian Landscapes (Geological Society Special Publication 346)

Martian Geomorphology (Geological Society Special Publication 356)

Sustainable Groundwater Development (Geological Society Special Publication,)

Early Precambrian Processes (Geological Society Special Publication)

Phanerozoic Ironstones (Geological Society Special Publication)

Slope Tectonics (Geological Society Special Publication 351)

Structurally Complex Reservoirs - Special Publication no 292 (Geological Society Special Publication)

The Physics of Explosive Volcanic Eruptions (Geological Society Special Publication)

The Making of the Geological Society of London (Geological Society Special Publication No. 317)

Human Interactions with the Geosphere: The Geoarchaeological Perspective (Geological Society Special Publication 352)

The Evolving Continents: Understanding Processes of Continental Growth - Special Publication 338 (Geological Society Special Publication)

Orogenic Processes: Quantification and Modelling in the Variscan Belt (Geological Society Special Publication, No. 179)

Sedimentary Response to Forced Regression (Geological Society Special Publication)

Volcanic Degassing (Geological Society Special Publication No. 213)

Fractured Reservoirs (Geological Society Special Publication no 270)

Hydrocarbons in Contractional Belts (Geological Society Special Publication 348)

History of Palaeobotany: Selected Essays (Geological Society Special Publication)

Palaeoproterozoic Supercontinents and Global Evolution (Geological Society London, Special Publication)

Forensic Geoscience: Principles, Techniques And Applications (Geological Society Special Publication)

Confined Turbidite Systems (Geological Society Special Publication No. 222)

Deformation of Glacial Materials (Geological Society Special Publication No. 176)

Lacustrine Petroleum Source Rocks (Geological Society Special Publication)

Palaeozoic Reefs and Bioaccumulations: Climatic and Evolutionary Controls - Special Publication no 275 (Geological Society Special Publication)

Devonian Events and Correlations : Special Publication no 278 (Geological Society Special Publication)

Communicating Environmental Geoscience - Special Publication no 305 (Geological Society Special Publication) (No. 305)

Fractal Analysis for Natural Hazards - Special Publication No 261 (Geological Society Special Publication)

Mineral Deposits & Earth Evolution (Geological Society Special Publication)

Sedimentary Response to Forced Regression (Geological Society Special Publication)

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