Fossil Fungi

Fossil Fungi

Thomas N. Taylor

Department of Ecology and Evolutionary Biology and Natural History Museum and Biodiversity Institute, The University of Kansas, Lawrence, Kansas

Michael Krings

Department of Earth and Environmental Sciences, Palaeontology & Geobiology, Ludwig-Maximilians-University, and Bavarian State Collection for Palaeontology and Geology, Munich, Germany

Edith L. Taylor

Department of Ecology and Evolutionary Biology and Natural History Museum and Biodiversity Institute, The University of Kansas, Lawrence, Kansas

Table of Contents

Cover image

Title page

Copyright

Preface

Acknowledgments

About the Authors

1. Introduction

Scope of this Volume

What is Paleomycology?

History of Paleomycology

Naming Fossil Fungi

2. How Fungal Fossils Are Formed and Studied

Preservation

3. How Old are the Fungi?

Phylogenetic Systematics

Molecular Clocks

Early Fossil Evidence

Fungi and the First Land Plants

Symbiosis: A Critical Component of Life

4. Chytridiomycota

Fossil Chytrids

Chytrid Summary

5. Blastocladiomycota

Fossil Blastocladiomycota

6. Zygomycetes

Precambrian Microfossils

Rhynie Chert

Zygosporangium-Gametangia Complexes and Sporocarps

Amber Fossils

Ichnotaxa

Conclusions: Zygomycetes

7. Glomeromycota

Biology of Glomeromycotan Fungi

Glomeromycotan Characters

Glomeromycotan Reproduction

Fossil Glomeromycota

8. Ascomycota

Geologic History of Ascomycota

Mesozoic and Cenozoic Ascomycetes

Fungal Endophytes and Epiphylls

9. Basidiomycota

Fossil Basidiomycetes

Agaricomycotina

Pucciniomycotina

Ustilaginomycotina

Ectomycorrhizae

10. Lichens

Thallus Morphology and Structure

Lichen Reproduction

Lichen Evolution

Precambrian Evidence of Lichens

Paleozoic Lichens

Mesozoic Lichens

Cenozoic Lichens

Fossils that Might Be Lichens

11. Fungal Spores

Naming Fungal Spores

Fungal Spores in Stratigraphy

Fungal Spores in Paleoecology

Fungal Spore Taxa

Other Fungal Spores and Structures

12. Fungal Interactions

Fungus–Animal Interactions

Fungi and Arthropods

Fungi in Eggs

Trace Fossils (Ichnofossils)

Fungus-Fungus Interactions

Fungus–Plant Interactions

Fungus–Geosphere Interactions

13. Bacteria and Fungus-Like Organisms

Bacteria

Actinomycetes

Mycetozoa

Peronosporomycetes

Peronosporomycetes: Conclusions

Glossary

References

Index

Chart

Copyright

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Preface

After completing this volume, we now understand why there has been no prior attempt to fully document the fossil record of fungi. This statement, however, is not meant to lessen the impact of various papers, journal articles, and catalogs that have examined fossil fungi through time, which are discussed in this volume. What has made our attempt at chronicling fungi through geologic time such a challenge is the need to provide, on the one hand, a balance between fungi as they appear as fossils, including all the inherent limitations of preservation in the fossil record, and on the other hand, fungi as living organisms. There are many reasons that the discipline of paleomycology has not been at the forefront of paleobiology despite the importance of fungi and fungus-like organisms as driving forces in the evolution of other organisms and of ecosystems. One of these reasons certainly has been the idea that because fungi are relatively fragile organisms, the possibility that they are adequately preserved in the fossil record has been discounted. While this is certainly true with regard to certain modes of preservation, as we will present in the following pages, delicate fungal structures and entire organisms can, under certain circumstances, become preserved in extraordinary detail in the rock record.

Another significant factor in elucidating the fossil record of fungi concerns the interface between paleontologists, who study fossil organisms, and biologists, who study living fungi as well as other types of microorganisms. It comes as no surprise that most fossil fungi have been discovered by paleontologists by chance, while searching for and examining other organisms. Thus, the presence of fungal fossils may be less apparent when samples are collected and as a result may simply not be documented. The other component that we believe has adversely affected the growth of paleomycology concerns the background and wealth of knowledge among mycologists who study extant fungi and fungus-like organisms, knowledge that in most instances is lacking among paleobiologists. Thus, there is a major gulf between those who have the fungal fossils but lack knowledge about extant fungi, and those who have a wealth of knowledge about extant fungi, but lack the fossils. Added to this dilemma is the fact that those who might be in a position to collect certain types of fungal fossils probably discard the specimens that demonstrate what many fungi do best – degrade and decompose organic materials. How many times have you seen a slab of rock in a museum with scattered bits of organic matter that is labeled, example of a Carboniferous fern that has been degraded by a saprotrophic fungus? It is common practice in paleontology to collect the best-preserved specimens that provide the greatest amount of information about the particular fossil while at the same time discarding incomplete and poorly preserved specimens. The latter may be the result of fungal activity. Even in instances where the cells and tissue systems are preserved in great detail, such as in permineralized and petrified wood, symptoms of fungal activity, including poorly preserved cell walls, compacted wood, or even interruptions in the wood, may be discarded because complete and near perfect specimens are the basis of taxonomic or ecological descriptions. Occasionally an author may note that some of the cells contain fungal hyphae or symptoms of interactions with fungi, but this is not a common practice. Searching for perfect or the most diagnostic specimens is the operational mode in most paleobiological studies. For example, well-preserved leaf cuticles can provide information of various types based on the numbers, type, and patterns of epidermal cells that are faithfully reproduced in the cuticles. Many of the plants when they were alive, however, hosted various communities of microbes including fungi, some of which may still be preserved on the leaves, but they are often discarded for cleaner specimens.

Techniques used to study fossils, especially plants, have also hindered progress in paleomycology. While petrographic thin sections were once the primary source of information when examining permineralized plant material, this technique was largely replaced by acetate peels, which could be prepared far more quickly, required less instruction in the technique, and were of a more consistent thickness. The problem is that many fungi preserved in the rock matrix are dissolved away when making peels. Although numerous fungi have been described in acetate peels prepared from permineralized peats, it is now understood that the old-fashioned thin section is superior when searching for fossil fungi in these materials. It takes time and patience, however, to produce thin sections of adequate quality. Some new techniques and imaging systems have been used to study a variety of paleontological specimens, including fungal fossils; where appropriate, we have noted these approaches throughout the text.

Despite our training primarily in paleobotany, we have tried to include enough factual information about extant fungi to make the discussion about the fossils more compelling, and to offer sufficient detail to our paleontological colleagues to expand their knowledge base about fungi, appreciate the potential in their research, and know what to look for. If an introductory course counts, the three of us have had some formal training in mycology, but we are certainly not professional mycologists. In trying to provide a volume that attempts to include both mycology and paleontology, and the various subdisciplines that intersect at multiple levels, we have provided what may sometimes be interpreted as overly basic information in either of these broad disciplines. In our writing we have tried to frame the discussion by asking whether a paleobiologist would understand this about living fungi, and conversely, whether a mycologist would understand that about paleobiology. In some instances readers might wonder, depending on their professional expertise, why we have provided so much information, especially about living fungi. The answer is not simply that we are fascinated by them but that we have tried to emphasize various features or hypotheses that might be identified in or applied to fossil fungi that have not yet been recorded. A simple example might be the consistent occurrence of a particular fungus in fossilized wood of a certain species that has an extensive record in both time and space. Is the co-occurrence a result of some type of coevolution, and do the host and the fungus show any independent evolutionary trends? We have also suggested questions that might be addressed if a larger data set of fossil fungal materials were available to be investigated, or incorporated into a broader picture of organism evolution, e.g., symbiosis. To that end we have provided an extensive and straightforward glossary of terms, with the intention that it will also assist those from other disciplines. We have included numerous illustrations of fossil fungi, many from our own papers and our previous volume – Paleobotany: The Biology and Evolution of Fossil Plants, which not only illustrate important characters preserved as fossils but also serve to demonstrate the kinds of features that can occur in the fossil record.

Another reason for our attempt to assemble information about fossil fungi within a single volume is that reports of fossil fungi in the literature have historically been published just about everywhere. In some instances articles on fossil fungi have occurred in journals that primarily cover living fungi, focus on applied mycology (e.g. brewing), or even in horticultural publications. When the focus is more aligned with the physical results of fungal activity in the rock record, research is presented in outlets that contain articles in geology, geobiology, and other closely related disciplines. Other reports about fossil fungi occur in journals that specialize in various subdisciplines in paleontology and paleobotany. Thus, tracking down the scattered information about fossil fungi is an issue for those interested in paleomycology. Another problem is the fact that, especially in older literature, references to fungi co-occurring with plant or animal fossils were often made in a cursory manner. Since key wording and extended indexing were not common practice at that time, such information is largely inaccessible to those who are not familiar with this style of report. Preparing this volume and examining the primary literature where possible has given us the opportunity to review some systematic interpretations and, where necessary, offer alternative or more up-to-date hypotheses.

Perhaps the most significant challenge we faced concerns the placement of various subject areas that we wanted to include in the volume. For example, does one talk about mycoparasitism within the context of when it first appears in the fossil record (i.e. in the discussion of Rhynie chert chytrids) or under a broader discussion of parasitism? Alternatively, is it better for the reader if the description of fossil basidiomycetes occurs within the phylogeny of the group today, or should they be discussed when the first fossils appear in geologic time? Even among ourselves we have had three different opinions – and they have constantly shifted regarding subject placement. This has resulted in a text that has attempted to present both perspectives while at the same time trying not to duplicate information.

We have also discussed a variety of fungus-like organisms, some of which were once included in the kingdom Fungi. However, we have limited this segment of the book (Chapter 13) to groups of organisms that are morphologically very similar to true fungi, and thus easily can be, and probably have been, confused with the latter. Examples of these might be the Peronosporomycetes and Actinomycetes. The inclusion of fungus-like organisms in this book is also used to underscore a major problem faced by anyone attempting to identify fungal fossils – morphological similarity does not necessarily imply relatedness.

One of the major shortcomings of paleomycology is its inherent limitation to morphology as a tool in identification and systematic assignment. In addition to the above-mentioned factors that have resulted in the neglect of fungi in the fossil record, the inability to make confident systematic assignments has certainly rendered paleomycology unattractive to many paleobiologists and mycologists. We also appreciate that the phylogeny and classification of modern fungi, based primarily on molecular data, is a constantly changing target that can never be directly correlated with fossils; however, we see some movement in the appreciation of fossil forms relative to certain structural and morphological characters and their first appearance in time and space. In some cases our taxonomy differs from a phylogenetic classification, but we see the contents of this volume only as a starting point on a continuum of incorporating the geological history of fungal lineages with the diversity expressed by living fungi irrespective of the tools and techniques used.

Acknowledgments

We owe an enormous debt of gratitude to many people who have influenced this work and contributed to the final product. This includes current and past colleagues who have freely contributed illustrations and unpublished data, and numerous professional organizations, publishers, and professional societies who have helped us in so many ways.

R. Agerer • L. Axe • F. Baron • D. Barr • K. Bauer • C. Beimforde • M.L. Berbee • J.A. Bergene • J.L. Black • J.E. Blair • R.A. Blanchette • J. Błaszkowski • B. Bomfleur • P. Bonfante • J.P. Braselton • G. Breton • A.W. Bronson • M.C. Brundrett • N. Butterfield • M.J. Cafaro • S.R.S. Cevallos-Ferriz • V. Chazottes • K. Clay • C.P. Daghlian • Y. Dalpé • J. Danek • R. Day • T. Demchuk • M.W. Dick • D.L. Dilcher • H. Dörfelt • N. Dotzler • D. Edwards • A. Galitz • J. Danek • J. Galtier • J.L. Garcia-Massini • J.F. Genise • T. German • P. Gerrienne • S. Golubic • A.K. Graham • C.J. Harper • S.T. Hasiotis • H. Hass • C. Haufler • D.L. Hawksworth • D.S. Hibbett • T.J. Hieger • H.-M. Ho • M. Holder • R. Honegger • V.B. Hosagoudar • J.M. Houts • J.J.C. Hower • A. Jumpponen • P. Kabanov • R.M. Kalgutkar • B. Kendrick • P. Kenrick • H. Kerp • S. Klavins • A.A. Klymuik • L. Krishtalka • C.C. Labandeira • J.D. Lawrey • B.A. LePage • R.W. Lichtwardt • J. Longcore • R. Lücking • P.C. Lyons • S.R. Manchester • K.K.S. Matsunaga • D.J. McLaughlin • S. McLoughlin • M.A. Millay • C.E. Miller • N.P. Money • S. Naugolnykh • A. Nel • G. Norris • J.M. O’Keefe • G.J. Ortiz • J.M. Osborn • M.G. Parsons • R.L. Peterson • C. J. Phipps • V. Podkovyrov • G. Poinar, Jr. • M.J. Powell • D. Redecker • M. Remshardt • R. Remy • W. Remy • G.J. Retallack • J. Rikkinen • G.W. Rothwell • G. Samoring • R. Saxena • A.R. Schmidt • J.W. Schopf • A. Schüßler • A.B. Schwendemann • M.-A. Selosse • R. Serbet • B.J. Slater • S.Y. Smith • D. Southworth • R.A. Stockey • P.K. Strother • C. Strullu-Derrien • S.P. Stubblefield • A.R. Sweet • S. Taliferro • J.V. Tassell • J.W. Taylor • A.M.F. Tomescu • J.M. Trappe • N.B. Trewin • N.H. Trewin • S.K.M. Tripathi • R.W.J.M. Van der Ham • K. Vogel • B.M. Waggoner • C.A. Wagner • C. Walker • H. Wang • T. Wappler • J.F. White, Jr. • If we have missed anyone, we sincerely apologize.

We are especially appreciative to Carla J. Harper and Rudolph Serbet for their extraordinary and invaluable help in the many tasks associated with assembling and photographing the specimens and illustrations used throughout the volume. Whether sizing illustrations, adding bar scales, searching for references or any of the myriad other tasks associated with completing this book, Rudy and Carla did so at the highest level of accomplishment and professionalism. Thank you both so very much. Also, a special thanks to Tim Hieger for his many contributions to this project. We are indebted to Sara Taliaferro who redrew the many illustrations of the fungal spores and fossil microthyriaceous ascocarps that appear in Chapters 8 and 11. Her dedication to detail and ability to view fossil specimens in a biological context is extraordinary. Of special acknowledgment is Jeannie Houts who has been associated with this project from the outset. Her dedication to the book and skillful assistance in so many ways has made the completion of this volume possible. Especially noteworthy has been her painstaking attention to the details associated with assembling the bibliography.

Professor Frank Baron and his colleagues at the Max Kade Center for German-American Studies and Department of Germanic Languages and Literature at the University of Kansas gave us assistance that is greatly appreciated. We acknowledge the wonderful hospitality provided by the Center when MK visited KU during phases of the writing of this book. Most importantly we value the friendship that has developed with Frank Baron.

We are grateful to the National Science Foundation and Alexander von Humboldt-Stiftung for providing financial assistance to our research and scholarship programs over the years that have contributed to studies of fossil fungi. Not only have these programs allowed us the opportunity to collect and study fossil fungi, but they have also provided the financial assistance to allow us to work together, to present research results at professional meetings, and to expand the network of biologists and geologists interested in fossil fungi and their activities.

Taking a book from the manuscript to the finished volume takes extraordinary talent that far exceeds that of the authors. We are especially appreciative for the help and guidance we have received from Ceinwen Sinclair, Freelance Copyeditor, and Roderick Crews, Freelance Proofreader, for their attention to detail during the editing stages. Melissa Read, Freelance Project Manager, kept all of the activities on time and skillfully organized. Working with Kristi Gomez, Acquisitions Editor, and Pat Gonzalez, Editorial Project Manager, both of Elsevier Inc., has been a genuine pleasure. These extraordinary individuals have given this project enormous assistance, and have done so with a level of professionalism and expertise that sets a very high standard. Kristi and Pat, thank you so very much – we simply could not have completed this project without your help.

We particularly wish to acknowledge the support from our families, friends, and colleagues. You have been patient, supportive, and loyal as we have trudged on with this project, sometimes never taking the time to say thank you. The institutions where we are employed – the University of Kansas, Lawrence, KS (USA), and both the Ludwig-Maximilians-University and the Bavarian State Collection for Palaeontology and Geology in Munich, Germany – have assisted in numerous ways for which we are grateful. Providing the opportunity for us to pursue our research and scholarship with fossil fungi has been a joyous opportunity. We extend a special acknowledgment to Hagen Hass, University of Münster, who has been the driving force in discovering many of the fossil fungi and fungal-like organisms in the Rhynie chert, to Renate and the late Winfried Remy who made some of our early studies possible, and to Hans Kerp for making recently discovered specimens available.

Numerous individuals, through their research interests and early studies, have influenced our pursuit of understanding the biology and evolution of fossil fungi and how they functioned in ancient ecosystems. Of special note are a few of the pioneers in paleomycology: David Dilcher, William Elsik, Jan Jansonius, Ramakant Kalgutkar, Robert Kidston, William Lang, Aloysius Meschinelli, Julius Pia, Kris Pirozynski, Sara Stubblefield, Bernard Renault, and Bruce Tiffney. During our careers we have been especially fortunate in having extraordinary teachers and colleagues who have always provided encouragement, loyalty, and unwavering support for us in our personal and professional activities. Thank you for always being there.

About the Authors

Thomas N. Taylor is a member of the National Academy of Sciences and holds the title of Distinguished Professor in the Department of Ecology and Evolutionary Biology, and Curator of Paleobotany in the Natural History Museum and Biodiversity Institute at the University of Kansas. He also has a courtesy appointment in the Department of Geology. He received his Ph.D. in botany from the University of Illinois and was a National Science Foundation postdoctoral fellow at Yale University. His research interests include Permian and Triassic biotas of Antarctica, early land plant–fungal interactions, the origin and evolution of reproductive systems in early land plants, symbiotic systems through time, and the biology and evolution of fossil microbes.

Michael Krings is Curator for Fossil Plants at the Bavarian State Collection for Palaeontology and Geology (BSPG) in Munich, Germany, and Professor of Plant Palaeobiology at the Ludwig-Maximilians-University, Munich. He also holds an affiliate faculty position in the Department of Ecology and Evolutionary Biology at the University of Kansas. He received his Ph.D. in botany from the University of Münster, Germany, and was an Alexander von Humboldt Foundation postdoctoral fellow at the University of Kansas. His research interests include Carboniferous, Permian, and Triassic seed plants from Europe and North America, and the biology and ecology of microorganisms in late Paleozoic terrestrial ecosystems.

Edith L. Taylor has held the title of Professor of Ecology and Evolutionary Biology and Senior Curator of Paleobotany in the Natural History Museum and Biodiversity Institute at the University of Kansas since 1995, and also serves as a Courtesy Professor of Geology. She received her Ph.D. in paleobotany from the Ohio State University, where she was an American Association of University Women Dissertation Fellow. She is the author of seven books or edited volumes, more than 180 publications, and is a fellow of the American Association for the Advancement of Science. Her research interests include fossil wood growth and paleoclimate, Permian and Triassic permineralized plants from Antarctica, distribution and diversity of Permian–Triassic Antarctic floras, the structure and evolution of fossil phloem, and fossil microorganisms.

1

Introduction

Fungi are fundamental to the health and success of almost every ecosystem in the world today, and they certainly played equally important roles in ancient ecosystems. We now know that there is an extraordinary abundance of fungal remains in the fossil record; however, systematic studies of fungal lineages based on fossils are lacking to date, owing primarily to the inherent problems and limitations connected to the fossil record of the fungi. Moreover, when fungi were reported in the past they were rarely placed within a broader context. Today, however, there is an increasing interest in fossil fungi and their importance in ancient ecosystems, which has been stimulated by a generally growing scientific awareness of the microbial world and the interrelatedness of all organisms. This book chronicles the fossil record of fungi through geologic time, places them within a systematic context where possible, and describes various types of fungal associations that existed in ancient ecosystems. Paleomycology is defined and discussed within the historical context of both extant and fossil fungi, and linked to other closely interrelated disciplines dealing with fungi and fungus-like microorganisms.

Keywords

anamorph; biodiversity; decomposition; fungi; fossil; geobiology; heterotrophs; holomorph; mutualists; paleomicrobiology; paleomycology; teleomorph; geologic time

Outline

Scope of this Volume 3

What is Paleomycology? 4

History of Paleomycology 5

Naming Fossil Fungi 10

Fungi are extraordinary. Although fungi represent the largest life forms on Earth (Angier, 1992), and are instrumenta to the health and success of almost every ecosystem, they are perhaps the most underappreciated group of organisms. There are approximately 100,000 species of fungi and fungal-like organisms currently recognized, and as a result of molecular techniques it is estimated that there may be more than 5 million species of fungi inhabiting the Earth (e.g. Blackwell, 2011). Since there are estimated to be more than 400,000 species of flowering plants (angiosperms), the group we depend upon for food (e.g. Joppa et al., 2011), this means that there are more than 10 times more fungi than angiosperms. To realize and accurately document the biodiversity of fungi in the future it will be as important to develop and integrate data-based platforms (e.g. Halme et al., 2012) as it will be to document fungi in tropical forests and unexplored habitats (Hawksworth, 2004). Fungi impact just about every aspect of life and have played a major role in the evolution of life on land (e.g. Blackwell, 2000). In fact, the colonization of land by plants is hypothesized to have occurred as the result of symbiotic interaction(s) between a fungus and a photosynthesizing organism. Today this association continues in the form of mycorrhizae, which occur in and around the roots of vascular plants and increase nutrient uptake in an estimated 90% or more of all plant species.

Fungi range from single celled to complex multicellular organisms and can be found in all aerobic ecosystems where they colonize numerous substrates and perform multiple functions, some of which are poorly understood (e.g. Cantrell et al., 2011). For example, they occur in habitats ranging from Antarctica (e.g. Onofri et al., 2007; Kochkina et al., 2012) to salt flats to laminated organo-sedimentary ecosystems termed microbial mats. They have even been reported as epiphytes on unicellular or multicellular plant hairs or trichomes (Pereira-Carvalho et al., 2009), in deep-sea ecosystems (e.g. Schumann et al., 2004; Le Calvez et al., 2009; Nagano and Nagahama, 2012), and in 100 m of deep sea mud (Biddle et al., 2005). Fungi are the primary degraders of complex organic compounds such as lignin and cellulose and, through this recycling, are important in returning minerals to the soil. As a result of decomposition, carbon dioxide is returned to the atmosphere. They are especially important decomposers in acidic soils where bacteria often cannot exist. Fungi also bind soil particles to their mycelium, thus contributing to soil structure. In all of these functions they are crucial in the maintenance of the biosphere. Fungi, together with soil fauna, roots, and other microorganisms, are major drivers of ecosystems and in this capacity are involved in the critical processes of landscape sustainability, including nutrient cycling, in which they accumulate, store, and distribute minerals and carbon (e.g. Johnston et al., 2004). Most are filamentous, which allows them to readily explore and exploit new habitats including their own parental hyphae (e.g. Gadd, 2007).

Because fungi are carbon heterotrophs they have, by necessity, mastered various levels of cooperation with other organisms: they partner with certain types of algae and cyanobacteria to form lichens, and their intimate relationships with land plants include mycorrhizal associations. They also occur as endophytes in some vascular plants and in such cases can be involved in contributing to pathogen resistance. What may be interpreted as the dark side of the fungal kingdom is that as plant pathogens they impact broad areas of agriculture by infecting all major crop plants and producing various mycotoxins involved in food contamination and in some cases human disease. Fungi are also known to negatively affect animals and humans as causative agents of diseases (e.g. Sternberg, 1994; Fisher et al., 2012). One of these diseases, chytridiomycosis, has made it into the news because it is believed to have caused the decline and even extinction of some amphibian populations on several continents (e.g. Longcore et al., 1999; Weldon et al., 2004).

In buildings, fungi and other microbes contribute to altering and erasing cultural structures by deteriorating historical stone in the form of statues, tombstones, historic buildings, and archaeological sites (McNamara and Mitchell, 2005; Mitchell and McNamara, 2010; Steiger and Charola, 2011). In addition, microbial activities and fungi are involved in the deterioration of paintings, wood, paper, textiles, metals, waxes, polymers, and various types of coatings (Koestler et al., 2003; Martin-Sanchez et al., 2012). Fungi also show no respect for some of the pillars of our modern society such as utility poles (Wang and Zabel, 1990).

Fungi also enter into mutualistic associations with animals; some even thrive within the animal, in anaerobic environments (Mountford and Orpin, 1994). Especially interesting are fungi that play a pivotal role in the rumen by physically and enzymatically attacking the fibrous plant material ingested by the ruminant animal (e.g. Kittelmann et al., 2012). By breaking down plant cell wall carbohydrates, such as cellulose and hemicellulose, these anaerobic fungi deliver readily accessible nutrients, mainly acetate, propionate, and butyrate, to their ruminant hosts (e.g. Gordon and Phillips, 1998).

Fungi affect our lives in innumerable ways; some are even believed to have shaped civilizations (e.g. Money, 2007; Dugan, 2008). For example, mushrooms are quite frequently depicted in ancient, medieval, and modern fine art. A group of ethnomycological rock paintings in the Sahara Desert (Tassili n’ Ajjer National Park, Algeria) – the work of pre-Neolithic early hunter-gatherers some 7,000–9,000 years old – shows the offering of mushrooms, and large masked gods covered with mushrooms, suggestive of an ancient hallucinogenic mushroom cult (Figures 1.1, 1.2). These paintings may reflect the most ancient human culture yet documented in which the ritual use of hallucinogenic mushrooms is explicitly represented (Samorini, 1992). The Temptation panel in Mathias Grünewald’s famous Isenheim Altarpiece, painted between 1510 and 1515, is believed to represent a depiction of ergot poisoning from rye flour contaminated by the fungus Claviceps purpurea (e.g. Battin, 2010). Ergot poisoning has also been suggested to be the reason for the strange behavior of women accused of witchcraft in Salem, Massachusetts Colony, in the late 1690s (Caporael, 1976), although some have refuted this hypothesis (Spanos and Gottlieb, 1976). Ergotism is known to cause jerky movements, which are characteristic of Sydenham’s chorea or St. Anthony’s fire, as it was called in the Middle Ages (Lapinskas, 2007). Today fungi are also used in criminal investigations, i.e. forensics (Hawksworth and Wiltshire, 2011).

Figure 1.1 Outline of ethnomycological rock painting from the Sahara Desert Matalem-Amazar site dated at 9,000–7,000 BP showing man (a shaman?) with masked head and numerous mushrooms scattered over the body (figure ~0.8 m tall). (Courtesy G. Samorini.)

Figure 1.2 Original prehistoric painting from the site in Figure 1.1. (Courtesy G. Samorini.)

The extraordinary modern dance company Pilobolus is named after the phototropic, mucoralean dung fungus of the same name that has the capacity to propel a cluster of spores a great distance. Other fungi are simply inspirational and actually reach into the stratosphere (Wainwright et al., 2006)! Some fungi simply make you feel good by their production of non-hallucinogenic indole compounds and derivatives including serotonin (Muszyńska et al., 2013); others, such as some common mushrooms, sometimes called magic mushrooms, contain hallucinogenic compounds that can alter thought and mood. A number of people get great pleasure simply dressing up in homemade mushroom costumes at the annual Telluride Mushroom Festival in Telluride, Colorado, USA, an event that also includes a feast of mushrooms collected by the revelers and prepared by expert chefs (Lincoff, 1996).

Fungi are known to improve the acoustic quality of violins by degrading the cell walls of the wood of Picea abies (Norway spruce) and Acer pseudoplatanus (European sycamore maple), which is used to make the top plates of the instruments. As a result of treating the wood with wood-decay fungi that break down cell wall components, the decrease in cell wall thickness makes the violin not only louder but capable of producing more resonant tones (Schwarze et al., 2000). Infection by the ascomycete fungal parasite Phaeoacremonium parasiticum (formerly Phialophora parasitica; Crous et al., 1996) of the heartwood of the trunk and roots of evergreen trees (Aquilaria, Gyrinops) results in the formation of what is termed agarwood. This unique fungal-infected wood is known by multiple names (e.g. ud, oud in Arabic countries; black eaglewood in Tibet; gaharu in Indonesia; agar in Pakistan) depending on the culture. As a result of infection the tree produces an aromatic resin that becomes embedded in the heartwood making it more dense and black in color. The resin has been highly sought after because of its distinctive fragrance in perfume, incense, and aromatherapy products and can be very expensive (Hansen, E., 2000). One can only wonder whether some of the fungal-infected fossil woods held such olfactory properties.

While most fungi are involved in organic material decomposition, others are involved in formation of a variety of materials in an indirect way. For example, dried mycelia have been suggested as a substitute for Styrofoam and for making bricks that can be used in construction. Mycotecture, architecture based on the structure of the mycelium, has also been used in art and the manufacture of furniture. Others have employed living fungi as templates in the synthesis of highly ordered structures of nanoparticles (e.g. Bigall and Eychmüller, 2010; Sabah et al., 2012).

Scope of this Volume

In order to document the number of living fungi, the mycological community has continued to enlist the help of an increasing number of biologists to record fungal diversity (e.g. Blackwell, 2011). Today this diversity is being measured in a number of ways, including molecular approaches that sample genome diversity within a phylogenetic framework. With increasing attention directed to fungal genomics there can be little doubt that these data will provide an unparalleled opportunity to better understand the biology and evolution of the fungal kingdom (e.g. Galagan et al., 2005). In addition, researchers are assembling these data into larger networks and using a coordinated infrastructure to address problems of fungal identification (Bruns et al., 2008). While these techniques are not applicable to examining the diversity of fossil fungi, we do believe that increasing the awareness of the fossil record of fungi will greatly expand the database of reports of these organisms in time and space. What makes the study of fossil fungi especially difficult is that the report of these organisms has generally been a secondary focus of paleontological studies until recently. Further compounding the dilemma of understanding the diversity of fossil fungi is that reports of their existence are not focused within specific disciplines but are found in broadly defined areas of biology and geology and the numerous subdisciplines within these areas.

What is inescapable, however, is the fact that fungi and fungal-like organisms were present in the earliest ecosystems on the Earth. As is true today, they were primary drivers of many crucial ecosystem functions and their record parallels, and sometimes predates, the diversity of other life forms in time. The challenge of recording the history of fungi through time is the primary focus of this book, but we will also be demonstrating some of the numerous interactions with other components of the ecosystems in which they lived and discussing abiotic aspects of the environment that fungi occupied. Nevertheless, there will continue to be new groups of extant eukaryotic organisms described that have some of the features of fungi but lack others and thus do not conform to the typical fungal realm. For example the Cryptomycota are an ecologically widespread and highly diverse group once thought to lack chitin in the cell wall and therefore not thought to be fungi (Jones et al., 2011a); now, however, they are considered to be members of the fungal kingdom (Jones et al., 2011b). Recording all of these evolutionarily successful organisms in the fossil record may be impossible using the techniques available today; however, having an appreciation of their existence in modern ecosystems will be significant as ideas about the fungal tree of life continue to evolve.

What is Paleomycology?

We define paleomycology as the study of the accumulated fossil evidence of fungi and their activities as measured in geologic time. The field includes study of fossilized fungi themselves as well as the full complement of their activities, which range from mineral weathering to both direct and indirect effects and interactions on and with other organisms. In this book we have also included the evidence of activities of a variety of fungus-like organisms, some of which at one time were grouped with the fungi but today are classified in other groups, as these organisms also have a fossil record. Thus, paleomycology is at the intersection of a number of disciplines, many of which overlap, some to a large degree.

One of these overlapping subject areas is paleomicrobiology, defined as the detection, identification, and characterization of microorganisms in ancient remains (Drancourt and Raoult, 2005). In general, these studies focus on the diagnosis of past infectious diseases in human populations caused by bacteria, viruses, and parasites, and principally involve the use of molecular techniques. Other people, however, would broadly define paleomicrobiology as the study of microbial communities and their activities through time. Paleomicrobiology overlaps with paleopathology, which is defined as the study of ancient diseases based primarily on skeletal remains (Aufderheide and Rodríguez-Martín, 1998). The discipline has also been expanded to include plant paleopathology, which is defined as the consequence of physical and chemical responses by plants to invasive microorganisms (e.g. viruses, bacteria, nematodes, and fungi) or to imbalances in nutritional or environmental conditions (Labandeira and Prevec, 2013).

Another area that includes the activities of fungi in geologic time is geobiology, a discipline initially defined by Teilhard de Chardin (Galleni, 1995) that builds on a broad range of interdisciplinary and disciplinary research focusing on the interactions between the biosphere and geosphere, and ranging from biomarkers to paleontology (e.g. Knoll et al., 2012). Some define geobiology as knowledge of the interface between life and the Earth’s environment. Geomicrobiology is concerned with the roles of microorganisms in geological and geochemical processes (e.g. Ehrlich and Newman, 2008), while geomycology is the scientific study of fungi in the processes of fundamental importance to geology, including weathering, soil formation, decomposition, mineral deposition, nutrient cycling, the influence on proliferation of microbial communities in mineral substrates, and several other processes (e.g. Burford et al., 2003a, b; Rosling et al., 2009a, b; Gadd et al., 2012). Some view geomycology as a subdiscipline of geomicrobiology (e.g. Gadd, 2007; Rosling et al., 2009a) and as a smaller component of geobiology, which includes all of the biotic interactions on physical aspects of the Earth system including climatic, atmospheric, oceanic, and geospheric (e.g. Beerling, 2009; Rosling et al., 2009a).

Not only is the documentation of fossil fungi the only method to gain some appreciation for the diversity of these organisms through geologic time (e.g. Sherwood-Pike, 1991), but paleomycology also is the only way to plot the occurrence of fungal apomorphies in certain groups and thus test the validity of molecular clock assumptions about divergence rates and evolutionary lineages. In addition, fungal occurrences that are associated with particular groups of plants, and certain species, provide a necessary framework to consider a wide range of outcomes ranging from the coevolution of host and parasite to insights about the climate and other environmental parameters in which the fungus lived. Fossil fungi also provide an indirect measure of interactions with other organisms and a time frame for when some of these interactions initially occurred in geologic time.

History of Paleomycology

It is impossible to know exactly who recorded the first fossil fungus. The majority of early reports on fossil fungi were from Carboniferous rocks, especially those from Great Britain. One of these is by Steinhauer (1818) who reported on some longitudinal configurations that he suggested might be tissues of a plant or evidence of decay. Sternberg (1820) described Carpolithes umbonatus, which has been interpreted as some type of ascomycete, and Algacites intertextus, also thought be fungal but now interpreted as of uncertain affinity. Daedaleites volhynicus is a name credited to Eichwald (1830) that has been used as an early example of a basidiomycete. While these names, and other species, are included in the Index Fungorum (http://www.indexfungorum.org/), mostly within the category Fossil Fungi, it is difficult to be certain what they represent.

Another early account of a probable fungus was by Lindley and Hutton (1831–1833), who described an oval structure, approximately 2.5 cm in diameter, with what were interpreted as perhaps growth increments of a fungal basidiocarp. They used the name Polyporites bowmanni and with some reluctance suggested it was perhaps the hymenium of some polypore. However, P. bowmanni and a similar specimen, reported by Lesquereux (1877) (Figure 1.3) from the Carboniferous of North America, were later determined to be fish scales (Carruthers, 1889). Another early report (Göppert, 1836) (Figure 1.4) identified small structures on Carboniferous foliage as leaf-inhabiting fungi, and it is reported that Robert Brown, then Keeper of Botany at the British Museum, showed Charles Darwin a piece of silicified wood containing fungal hyphae sometime during the 1840s (Smith, W.G., 1884). Studies of fossil wood, perhaps of roots, sometimes included a note that there were hyphae in some of the cells (e.g. Conwentz, 1880). Generally, these were not given names or described in any detail. In his benchmark review of paleomycology, Kris Pirozynski (1976a) (Figure 1.5) noted that most of the early reports and descriptions of fossil fungi were based on observations using a hand lens or the naked eye rather than transmitted light.

Figure 1.3 Leo Lesquereux.

Figure 1.4 Heinrich Robert Göppert.

Figure 1.5 Kris A. Pirozynski. (Courtesy Ottawa Geological Survey.)

Historically, perhaps Berkeley (1848) was one of the first to examine microfungi with a compound microscope. The specimens he described were included in preparations of Eocene Baltic amber. Although he provided descriptions and illustrations, and included them in the genera Penicillium and Streptothrix, and a new genus, Brachycladium, these assignments were only tentative and today are dismissed. Other early reports from the Carboniferous include structures thought to represent fungi in the form of variously sized ramifying tubes and occasional oval spores at the ends of hyphae and within the matrix (Hancock and Atthey, 1869, 1870). Described as several species of Archagaricon, it is difficult to determine whether these specimens are in fact fungi, a concept that was later challenged (Smith, W.G., 1877). More convincing examples of fungi, or perhaps Peronosporomycetes, were described and illustrated from a permineralized specimen of the Carboniferous lycopsid Lepidodendron (Smith, W.G., 1877, 1878). These fossils consist of septate hyphae within the tracheids together with spherical units approximately 50 μm in diameter termed oogonia. Within the oogonia are seven or eight structures interpreted as zoospores, but the small number and size suggest that these are more likely oospores, if in fact the spore-like bodies are oogonia (James, 1893a, b). Another interpretation is that the internal contents represent some type of mycoparasite. Septate hyphae in some of the ground tissue cells of the fern Zygopteris from the Lower Coal Measures (Lower Pennsylvanian) of Halifax, West Yorkshire, have also been thought to represent some type of peronosporomycete (Cash and Hick, 1879).

There are a number of so-called fungi described in the late 1800s for which neither the description nor the illustration afford any suitable detail to suggest that the structure is a fungus. One of these, Rhizomorpha ‘sigillaria,’ a structure described from the shales of the Darlington Coal Bed in Beaver County, Pennsylvania (USA), and thought to represent a fungus (Lesquereux, 1877), was later interpreted as perhaps some insect burrow beneath the periderm of Sigillaria (James, 1885). This may also be the actual biological identity of Incolaria securiformis (Herzer, 1893b), the name applied to a putative fungus that comes from fissures in the extraxylary tissues of the Carboniferous lycophyte Sigillaria. Another Carboniferous form attached to a trunk and reported from the then No. 5 Coal from Tuscarawas County, Ohio (USA) consists of what is interpreted as a series of parallel tubes that form the pileus (Herzer, 1893a). No tissues or spores were recovered from Dactyloporus archaeus (Figure 1.6), and thus the affinities to some polypore were conjectural at best. Often these descriptions and sometimes generic designations are related to other supposedly fungal structures that were described earlier, but they are also dubious in terms of biological affinities.

Figure 1.6 Representative figures of the putative Carboniferous polypore Dactyloporus archaeus showing distribution of the specimens and tube-like organization of the fungus. Bar=1.0 cm. (From Herzer, 1893a.)

In addition to fungi being reported in shales and coals, there are some early reports of fungi in amber discovered in certain coal seams. One of these is from the Ayrshire Coal Field (Great Britain) and includes rounded amber inclusions of various sizes that contain several types of plant parts and what are referred to as microfungi (Smith, J., 1896). Some of these consist of what may be hyphae with some type of attached reproductive unit; for these types the generic names Peronosporoides and Leptonema were established (Smith, J., 1896). Some of these drawings are extraordinary and leave little doubt as to the affinities of some forms (e.g. Smith, W.G., 1884). The fact that amber has also been found in the Carboniferous (Bray and Anderson, 2009) indicates that some of the plants at that time produced resins like those found today in some conifers and angiosperms, and that such deposits also represented a potential trap for fungi and other microorganisms.

With the increased use of the compound microscope there were a number of studies that looked at the detail of fungi preserved in various types of cherts, especially those from the Carboniferous of central France. Foremost among the researchers was the French paleobotanist Bernard Renault (Figure 1.7), who meticulously documented the morphology of a number of microorganisms including their distribution in plant tissues from permineralized cherts. Renault was not only a skilled technician who produced high quality thin sections; he was also interested in the correct systematic placement of the organisms he studied. Among his many studies are reports of algae (1903), Peronosporomycetes (1895b), and several types of fungi (1894a, 1895a,b, 1896b,c, 1899, 1900, 1903) (Figure 1.8). He also described a number of structures that he interpreted as bacteria (1894b, 1895c, 1896a–d, 1897, 1898, 1899, 1900, 1901); some of these are probably crystal patterns.

Figure 1.7 Bernard Renault.

Figure 1.8 Oochytrium lepidodendri. Carboniferous, France. Bar=20 µm. (From Renault, 1896.)

What is arguably the first compendium of fossil fungi was assembled by Meschinelli (1892, 1898) in which he recorded more than 60 genera and 350 species (Figure 1.9). This study emphasized descriptive taxonomy, but many of the identifications and interpretations were based on association of a particular type of symptom or characters that are no longer used (Pirozynski and Weresub, 1979). Meschinelli is also credited with adding "-ites" to the ending of modern generic names for fossil specimens he considered the same as living forms. Seward (1898) (Figure 1.10) was a little less charitable in noting that certain species are of no botanical value, and should have no place in any list which claims to be authentic. In his four volume series, Fossil Plants, Seward (1898) provided a detailed analysis of many of the fossil fungi described to that date and challenged a number of the reports and their taxonomic placement. The nomenclatural status of several names allocated by Meschinelli, indicating they were believed to be fossil fungi (such as Agaricites), were also challenged (e.g. Holm, 1959). While many of these early reports may be suspect, perhaps what is most important is that rocks of varying ages were being examined for evidence of microorganisms like fungi (e.g. Ellis, D., 1915).

Figure 1.9 Title page of Meschinelli’s compendium on fossil fungi.

Figure 1.10 Albert C. Seward.

Many of the early reports of fossil fungi are presented systematically by Julius Pia in Max Hirmer’s textbook, Handbuch der Paläobotanik (von Pia, 1927) (Figure 1.11), including reproduced line drawings and, in several instances, photographs from the original papers. Of particular significance is the inclusion of the various forms within a higher taxonomic system at the family level. There are other scattered reports of fossil fungi that are catalogued within a taxonomic framework (e.g. Brabenec, 1909; Němejc, 1959).

Figure 1.11 Julius von Pia.

The next major reference to fossil fungi was completed by the paleobotanists Tiffney and Barghoorn (1974) (Figures 1.12, 1.13). They provided a listing of more than 500 fossil fungal species that was annotated in detail and, for the first time, the families were placed within a stratigraphic context. This contribution was later updated with additional fossil species, while others were modified or deleted (Taylor, T.N., 1993a). A slightly different approach was used by Stubblefield and Taylor (1988), who discussed fossil fungi relative both to their stratigraphic occurrence and to their possible roles as mutualists, saprotrophs, and parasites, hypothesizing a link between nutritional mode and environment. Also included was a brief discussion of techniques used to study fossil fungi and the nomenclatural approaches in naming them. Aspects of the nutritional modes of fossil fungi were also discussed in The Biology and Evolution of Fossil Plants (Taylor and Taylor, 1993) together with the inclusion of some of the new fossil representatives. Much of this information was further updated, and new fossil fungal reports included, in Paleobotany: The Biology and Evolution of Fossil Plants (Taylor et al., 2009). Many of the early accounts of fossil fungi occurred in volumes that focused on paleobotany; only a few books centering on living fungi have included fossils at all (e.g. Wolf and Wolf, 1947; Alexopoulos et al., 1996) (Figure 1.14).

Figure 1.12 Bruce H. Tiffney.

Figure 1.13 Elso S. Barghoorn.

Figure 1.14 Constantine J. Alexopoulos.

In addition there have been multiple contributions that have considered the history of paleomycology (e.g. Pirozynski, 1976a), nomenclature (Wolf, 1969a; Pirozynski and Weresub, 1979; Ramanujam, 1982), specific groups of fungi (e.g. Pirozynski and Dalpé, 1989), fungi from particular regions (e.g. Teterevnikova-Babayan and Taslakhchian, 1973; Germeraad, 1979) or continents (Herbst and Lutz, 2001), specific fungi based on preservational mode (e.g. amber; see Poinar, 1992) (Figure 1.15), fungi as components of coal (e.g. Beneš, 1956, 1960; Lyons, 2000; Hower et al., 2010), and their stratigraphic position in multiple units within a narrow geographic setting (e.g. Singh et al., 1986). Publications have included discussions of basic terminology (e.g. Elsik, 1983) (Figure 1.16), collaborative approaches (Sherwood-Pike, 1990), sampling techniques (fungal palynomorphs) (e.g. Elsik, 1996; Kalgutkar and Jansonius, 2000 [Figures 1.17, 1.18]; Saxena and Tripathi, 2011), fungi associated with certain types of fossil plants (e.g. Rodríguez de Sarmiento et al., 1998), biodiversity (Dilcher, 1965), and fungi used as proxy indicators of certain events in Earth history, including continental drift (Nease and Wolf, 1975) and mass extinction (Visscher et al., 2011). There are also brief discussions of the evolution of fungi (e.g. Tripathi, 2012) and summaries of the major groups (Taylor et al., 2014). There are numerous other reports of fossil fungi in addition to these that deal with a variety of subject areas and these will be introduced in the appropriate chapters of this volume.

Figure 1.15 George O. Poinar, Jr.

Figure 1.16 William C. Elsik.

Figure 1.17 Ramakant M. Kalgutkar.

Figure 1.18 Jan Jansonius.

Naming Fossil Fungi

One discussion that directly concerns paleomycology relates to how fungi are named, an issue that will continue to impact our understanding of both living and fossil taxa (Hawksworth, 2011) (Figure 1.19). Historically, fungi were named based on features associated with sexual reproduction; however, some fungi only produce asexually, and still others reproduce both sexually and asexually. The majority of these forms are included in the Ascomycota, some in the Basidiomycota. This resulted in different names for the asexual stage (anamorph) and the sexual counterpart (teleomorph) if the stages could not be related to one another. More recently, the problem of fungal anamorphs has been exacerbated by the use of molecular tools linking the different stages (with different names) as parts of the same organism (holomorph) (e.g. Cannon and Kirk, 2000). For example, if a fungus has a name for both the anamorph and teleomorph, the holomorph assumes the name of the teleomorph, or sometimes the anamorph if certain conditions are met. Adding difficulty to this problem in paleomycology is the fact that fragmentation and other effects brought about by the fossilization process often lead to incomplete preservation of the individual stages.

Figure 1.19 David L. Hawksworth.

While fossil anamorphs and parts thereof are treated by the paleomycologist in a uniform manner, they in fact represent the result of various biological mechanisms within the life histories of ascomycete fungi (Seifert and Samuels, 2000). The fact that anamorphs are probably not homologous introduces another level of problems, especially when fungal palynomorphs are used to characterize taxa and thus identify species, and the presence of certain fungi (anamorphs) is used in defining stratigraphic and ecological conditions in deep time. The designation synanamorph is used for two or more morphologically distinct anamorphs produced by the same fungus (Hughes, 1979). Seifert and Samuels (2000) suggest the use of specific types of anamorphs to insure that those described are in fact homologous. For example, mycelial anamorphs lack stromatic elements but go through repeated cycles of asexual sporulation. A mononematous (i.e. production of conidia from superficial, exposed conidiogenous cells arising separately from vegetative hyphae or cells) anamorph, which is characteristic of many hyphomycetes included in the Moniliales, has well-differentiated conidiophores anchored in the substrate, but there are no stromatic elements. In conidial anamorphs there are fruiting bodies, while the designation germinating anamorph is used for conidiogenous cells emerging from ascospores or conidia. Thick-walled propagules termed sclerotia, aleuriospores, and chlamydospores are termed survival anamorphs. Yeast-like anamorphs are accumulations of blastically budding cells, while dispersive conidia that do not germinate are spermatial anamorphs. Where no propagules are produced, the term vegetative mycelium anamorphs is used. Teleomorph stages in fossil fungi are often far more characteristic and thus easier to name and classify systematically; however, fragmentation and the limits of optical resolution may hamper the definitive assignment. As a result morphology-based genera and species are used with fossil fungi that are defined based on morphological features of the teleomorph.

The problem of naming fungi, whether living or fossil, is far more complex than presented here, but since 2013 a single fungus has only one name, based on the nomenclatural principle of priority in which the oldest genus and species names must be combined irrespective of whether they were instituted as anamorph or teleomorph names (International Code of Nomenclature for Algae, Fungi and Plants [ICN], Melbourne Code; see McNeill et al., 2012). With regard to fungal fossils this means that isolated parts of the life cycle, anamorphs, and teleomorph stages must be merged into one biological species (a fossil fungus). This, however, is generally impossible based on the inherent limitations of the fossil record of fungi.

Throughout the book, the ages for geologic time periods have been taken from the most recent International Chronostratigraphic Chart (v. 2013/01, inside covers), prepared by the International Commission on Stratigraphy (IUGS) and available from www.stratigraphy.org. These dates are approximate, as they are defined by Global Boundary Stratotype Sections and Points (GSSPs) and not (in most cases) by absolute (radiometric) dating. They are also subject to change. See the website for updates and further information. See also Gradstein et al. (2012).

2

How Fungal Fossils Are Formed and Studied

Evidence of the existence of biological systems at various points in geologic time can be recorded in the fossil record in many ways. While everyone has a visual image of dinosaur bones or the remains of mammoths that once roamed the Earth, invertebrate shells, or plant leaves, what about fossil fungi and other types of microorganisms? What do fossil fungi and other microorganisms look like? Where are these found, how are they preserved, and what methods can be used to study aspects of the fossilized microbial world? In this section we present the most common modes of preservation for fossil fungi, discuss how some of these organisms are studied, and how they contribute to our understanding of past ecosystems.

Keywords

fossil fungi; amber; coal; coal balls; compressions; coprolites; geochemical; lignite; mummified wood; permineralizations; petrifactions; Rhynie chert; spores

Outline

Preservation 13

Impressions 13

Compressions 14

Coal 15

Charcoal 17

Casts 18

Petrifactions and Permineralizations 18

Unaltered Material 23

Rock Surfaces 25

Nodules 25

Carbon Spherules 25

Unusual Preservation Types Containing Fungal Remains 26

Preservation

Evidence of the existence of biological systems at various points in geologic time can be recorded in the fossil record in many ways. Almost everyone has a visual image of dinosaur bones, or of the remains of mastodons that once roamed the Earth, which, having been carefully excavated were then reassembled to show the actual appearance of the organism. Some have collected fossils in the form of invertebrate shells or plant leaves, or have seen examples of these organisms as images or in museums or in private collections. But what about fossil fungi and other types of microorganisms? Where are these found, how are they preserved, and what methods can be used to study aspects of the paleomicrobial world? In this section we present the most common modes of preservation in which fungi might be found, and then discuss how some of these organisms are studied. Additional information about the preservation of plant fossils is available in Taylor, T.N., et al. (2009).

Impressions

Impressions represent the negative relief of an organism that at one time was covered by sediment and