The Rhynie Chert – our earliest terrestrial ecosystem revisited

The Rhynie Chert is a 407 million year old hydrothermal deposit that is world renowned as the earliest well-preserved terrestrial ecosystem.  Beginning in 1917, Kidston and Lang published a series of ground-breaking papers describing the permineralised remains of plants, algae, fungi and cyanobacteria, and they also proposed a broadly accurate interpretation of the depositional environment. Subsequently faunal elements were discovered and include arachnids, collembolans, nematodes and crustaceans. Following further excavations (1963-1971) blocks of fossiliferous chert became widely accessible leading to major discoveries that include new life cycle variants in land plants, mycorrhizal-like association, lichen-like associations, and the diversity and functions of the fungal, algal and cyanobacterial elements of the ecosystem. Beginning in the 1980s, an extensive programme of trenching, boreholes, geophysics, and geochemistry provided a much clearer understanding of the geology of the Rhynie Basin, the environments of deposition and the age of the sediments. The site is thus exceptional because of the quality of preservation of organisms and their associations and interactions. The plants have played a central role in our understanding of the early evolution of tissues and organ systems and they continue to do so in the modern era of developmental biology and genomics.

Professor Dianne Edwards CBE FRS, Cardiff University, UK

Professor Dianne Edwards CBE FRS, Cardiff University, UK

Dianne Edwards is a distinguished botanist renowned for her study of early plant life on Earth. Through carefully documented field work and painstaking laboratory analysis, she has helped shed light on one of the most important evolutionary events in our planet’s history — the colonisation of land by plants.

Her work on fossils discovered in Wales, Scotland and further afield has pinpointed the earliest known occurrences of biological features central to plant life. Through Dianne’s extensive contributions to the subject, we now understand plants in the Palaeozoic era to be far more complex and diverse than was previously imagined.

Dianne is a Founder Fellow of the Learned Society of Wales, and since 2001 has been a Fellow of the Royal Society of Edinburgh. Awarded the CBE for Services to Botany in 1999, she has more recently served as the President of the Linnean Society in London.

Siliceous hot spring deposits, such as the Lower Devonian Rhynie Chert are the surface expression of terrestrial hydrothermal systems which create gold/silver bearing low-sulfidation epithermal mineral deposits deeper in the crust. Eruption of hot spring waters and precipitation of silica create a range of terrestrial and aquatic environments such as sinter apron complexes and areas of geothermally influenced wetland. These provide habitats for ecosystems that may be preserved in situ and, via permineralization of tissues, with exquisitely preserved anatomy. Sampling at active sinter-depositing hot springs allows characterisation of the physicochemical properties of the waters responsible for the Rhynie exceptional preservation. Broadly, thermal waters had elevated temperatures (100oC - ambient), relatively high sodium and chloride content (brackish - ca. 1.5 ppt salt), high pH (typically 8-9) and carried a suite of phytotoxic elements (e.g. arsenic, mercury, zinc, antimony). Fluctuating water availability, created by cyclic periods of hot spring eruption and quiescence, add further to these stresses. Observations of analogues for Rhynie such as Yellowstone show that physicochemical conditions plus the distribution of plants and animals profoundly affect not only ecosystem ecology and ecophysiology but also organism preservation potential. Such data raise questions of adaptation, specialization, endemism, and ecological vs. preservation biases.

Dr Alan Channing, Cardiff University, UK

Dr Alan Channing, Cardiff University, UK

Alan Channing is a geobiologist and palaeontologist interested in the geochemistry and biota of hot spring areas and the physical and chemical challenges faced by hot spring influenced ecosystems.

His investigations of active hot spring areas worldwide have identified geothermally influenced wetlands as a key environment for the preservation of fossil hot spring floras. Here, plants (and animals) must cope with multiple stressors including elevated water temperature, pH, salinity and dissolved metal and metalloid concentrations.

Alan is currently investigating the biota of newly discovered fossil hot spring ecosystems ranging in age from the early Holocene to Lower Palaeozoic which link his modern analogue studies back through geological time to the early Devonian ecosystem entombed in the Rhynie Chert.

The Rhynie Chert is our most complete example of an early terrestrial ecosystem, but the extent to which it is representative of the vegetation of the time remains conjectural. Physical, chemical and sedimentological evidence indicates that it was a geothermal wetland, and comparisons with similar modern environments (e.g., Yellowstone hot-springs system) highlight the presence of thermal gradients and brackish and potentially toxic surface water. The plants may therefore have been highly adapted and confined to the hot-springs system or perhaps they were more widespread elements of the regional biota but preadapted to survive in unstable stressed environments. It seems highly unlikely that the plants represented a relictual (primitive) population as is sometimes invoked for wetland communities. Comparison with contemporary megafossil remains found at other sites provides very limited support for a regional element to the flora. Integrated analysis of in situ and dispersed spores offers an opportunity to test these hypotheses and favours an interpretation of preadaptation for at least some of the plants.

Professor Charles Wellman, University of Sheffield, UK

Professor Charles Wellman, University of Sheffield, UK

Charles Wellman is Professor of Palaeobiology in the Dept. of Animal & Plant Sciences of the University of Sheffield. He received a B.Sc. in Geology from the University of Southampton in 1987 and a Ph.D. from Cardiff University in 1991. Charles’ Ph.D. research involved a study of early land plant microfossils from Scottish Silurian-Devonian ‘Lower Old Red Sandstone’ deposits. Subsequently Charles’ research has diversified to investigate diverse aspects of the colonisation of the land, including work on both living and fossil material, and a consideration of what lived on the land before the land plants.

Professor Dianne Edwards CBE FRS, Cardiff University, UK

Professor Dianne Edwards CBE FRS, Cardiff University, UK

Dianne Edwards is a distinguished botanist renowned for her study of early plant life on Earth. Through carefully documented field work and painstaking laboratory analysis, she has helped shed light on one of the most important evolutionary events in our planet’s history — the colonisation of land by plants.

Her work on fossils discovered in Wales, Scotland and further afield has pinpointed the earliest known occurrences of biological features central to plant life. Through Dianne’s extensive contributions to the subject, we now understand plants in the Palaeozoic era to be far more complex and diverse than was previously imagined.

Dianne is a Founder Fellow of the Learned Society of Wales, and since 2001 has been a Fellow of the Royal Society of Edinburgh. Awarded the CBE for Services to Botany in 1999, she has more recently served as the President of the Linnean Society in London.

Understanding ecosystems of the past is different from investigating modern day ones. Many properties of now-gone ecosystems can only be indirectly inferred, whereas in modern ecosystems simple observations or measurements would provide a direct access. Indirect access in fossil ecosystems is provided by the life habits of the extinct organisms that have been living in these ecosystems. The life habits of an extinct organism can finally be inferred by reconstructing the functional morphology, based on the morphological details observed in fossils in comparison to modern counterparts. Such investigations gain precision when exceptionally well-preserved fossils are studied, like those of the Lower Devonian Rhynie and Windyfield Chert. These deposits preserve a diverse range of arthropod groups, partly with terrestrial, partly with aquatic, non-marine lifestyle. Among aquatic forms especially crustacean fossils have become known, such as the famous Lepidocaris rhyniensis. The preservation of the crustacean fossils provides details of their feeding apparatus down to the sub-micron-range, including different types of setal structures. Based on these observations we can infer that crustaceans in the Rhynie and Windyfield Chert performed a variety of different feeding strategies. The biota thus contained a rich and differentiated non-marine aquatic fauna already 400 million years ago.

Dr Carolin Haug, Ludwig Maximilians University of Munich, Germany

Dr Carolin Haug, Ludwig Maximilians University of Munich, Germany

Carolin Haug studied biology at the Julius-Maximilians-Universität Würzburg (focus: animal ecology, sociobiology, palaeontology). She received her diploma in 2005 and moved to the University of Ulm for her Ph.D. thesis. In the work group Biosystematic Documentation she investigated the ontogeny and evolution of the arthropod head shield and developed new imaging techniques or modified existing methods, for example, composite imaging, stereo photography or auto fluorescence macro- and microscopy. In 2011, Carolin defended her Ph.D. thesis and became a postdoctoral researcher at Yale University and at the Ernst-Moritz-Arndt-Universität Greifswald.

She is interested in fossilised development (see also http://www.palaeo-evo-devo.info) and in the evolution of tagmosis. For this purpose, she investigates mainly arthropods from different deposits yielding exceptional preservation, such as the 'Orsten', Burgess Shale, Rhynie chert, Mazon Creek, or Solnhofen Lithographic Limestones, always in comparison to their extant relatives. Carolin moved to Munich in 2013 to continue her research there at the Ludwig-Maximilians-Universität.

The Early Devonian Rhynie and Windyfield cherts remain a key locality for understanding early life on land. They host the oldest unequivocal nematode worm (Nematoda), which may also offer the oldest evidence for herbivory via plant parasitism. The trigonotarbids (Arachnida: Trigonotarbida) preserve the oldest book lungs and were probably predators with evidence for liquid feeding. The oldest mites (Arachnida: Acariformes) are represented by taxa known to include mycophages and predators on nematodes today. The oldest harvestman (Arachnida: Opiliones) includes the oldest tracheae and male and female genitalia. Myriapods are represented by a scutigeromorph centipede (Chilopoda: Scutigeromorpha), probably a cursorial predator on the substrate, as well as putative millipedes (Diplopoda). The oldest springtails (Hexapoda: Collembolla) probably acted as mycophages. The oldest true insects (Hexapoda: Insecta) are represented by a species known from chewing (non-carnivorous?) mandibles and another with a gut infill of phytodebris. Coprolites also offer insights into diet, and previous assumptions that several taxa were spore-feeders is challenged. Rhynie appears preserve a largely intact community of terrestrial animals, but some expected groups are absent. As has been argued for plants, Rhynie may be sampling an atypical ecosystem characterised by invertebrates adapted to life on the hot springs margins.

Dr Jason Dunlop, Museum fur Naturkunde, Germany

Dr Jason Dunlop, Museum fur Naturkunde, Germany

Jason Dunlop studied zoology at the University of Leeds and palaeontology at the University of Manchester. His PhD, supervised by Paul Selden, focussed on an extinct group of arachnids called trigonotarbids; especially well-preserved examples of which were restudied from the Rhynie Chert.  His research focuses on fossil arachnids and their relatives, integrating data from living organisms with the fossil record to better understand the origins, early evolution and functional morphology of terrestrial arthropods. He has published several papers on Rhynie Chert fossils, including the discovery of the oldest harvestman and a restudy of the oldest lungs known from any terrestrial animal. Since 1997 he has been curator of arachnids and myriapods at the Museum für Naturkunde Berlin. He is also Secretary of the International Society of Arachnology and Vice-President of the European Society of Arachnology.

One of the most surprising discoveries in the Rhynie Chert was a completely new variant of the land plant life cycle in which both the gamete-bearing (haploid) and the spore-bearing (diploid) phases were independent, free-living plants of similar morphological and histological complexity. Sporophytes were distinguishable by their sporangia; gametophytes by their gametangia, which were often borne on distinctive bowl-shaped apices. In two species, gametophytes were significantly smaller than the sporophytes, whereas in others they were of comparable size. Otherwise, both phases were leafless, axial structures possessing rhizoids, vascular tissues and stomates. These discoveries have relevance to understanding the early evolution of the land plant life cycle, but their significance depends on precisely how the fossils relate to the plant tree of life. The leading hypothesis indicates that these fossils are stem group vascular plants, providing direct evidence that early life cycles were markedly different in form and ecology to those of modern pteridophytes. Divergence in size and growth architecture of gametophyte and sporophyte – a feature of modern pteridophytes – had begun by 407Ma, but the extent to which this life cycle variant persisted in early vascular plants floras remains an open question.

Dr Paul Kenrick, The Natural History Museum, London, UK

Dr Paul Kenrick, The Natural History Museum, London, UK

Paul Kenrick is a research scientist at The Natural History Museum, London. His interest in the evolution of land plants was sparked by an early encounter as a student with the tiny fossil plant Cooksonia. His career has been based in museums, including The Swedish Museum of Natural History, Stockholm, and The Field Museum, Chicago, where he integrated fossil evidence on early plants with the emerging phylogenetic picture based on living species. From 2008 to 2011 he was visiting professor in Plant Sciences at the University of Oxford. Kenrick has received several awards including the Henry Allan Gleason Award of The New York Botanical Garden and the Bicentennial Medal of the Linnean Society of London. He has authored two books and over 70 peer-reviewed publications.

Tissue and organs are composed of cells, and the development and resulted life cycle reflect the dynamics of cell behavior. Since the same or similar regulatory mechanisms at the cellular level can be repeatedly used in different developmental processes, changes of cellular characters and mechanisms can change multiple developmental processes with pleiotropic effects. Furthermore, new morphology originated from changes at the cellular level induces further morphological changes. However, genetic regulations of cellular characters and mechanisms especially deeply related to the evoluiton of land plant body plan have not been well studied. In this presentation, I will talk some examples to connect the evolution of development and life cycle to the changes at the cellular level. (1) The life cycle of Physcomitrella patens is a series of changes in stem cell characters. (2) Changes of stem cell characters switch body plants between gametophyte and sporophyte generations. (3) Sporophyte generation can be extended by the elongation of stem cell longevity. (4) Extended longevity of stem cells form new stem cells to be branches. (5) Periclinal cell divisions producing inner and outer tissue in antheridia, archegonia, and sporangia as well as water conducting tissue are regulated by the same molecular mechanisms, suggesting the partial homology of these organs.

Professor Mitsuyasu Hasebe, National Institute for Basic Biology, Japan

Professor Mitsuyasu Hasebe, National Institute for Basic Biology, Japan

Professor Mitsuyasu Hasebe received his Ph.D. from the University of Tokyo in 1992 for the molecular phylogeny of extant gymnosperms and ferns, which includes the first inference of the monophyly of extant gymnosperms and the phylogeny of leptosporangiate fern families. He started EvoDevo of floral homeotic genes in non-flowering plants during his stay in Jody Banks’s laboratory using the fern Ceratopteris in Purdue University. He expanded his EvoDevo works with the moss Physcomitrella, when he moved to National Institute for Basic Biology. He was a Japanese leader of the international consortium for the lycopod Selaginella moellendorffii and the moss Physcomitrella patens genome projects. His group worked on the evolution of development, life cycle, and stem cell formation in land plants. He is now interested in the evolution of complex and novel traits including land plant development, carnivorous plants, seismonastic movement of Mimosa pudica.

The publication of Kidston and Lang’s monograph on the silicified plants from the Rhynie chert (1917–1921) is a real milestone in palaeobotany, because it was the first time that plants showing a great amount of anatomical detail were described from rocks as old as Early Devonian. The plants are often found in life position. Moreover, the often pristine preservation of very delicate short-lived developmental stages indicates a rapid preservation in silica. Therefore, the Rhynie chert provides a series of unique snapshots of an early terrestrial ecosystem. Between 1917 and 1920 Kidston and Lang described five land plants from the chert in great detail. Although all, except for Asteroxylon mackiei, look at first glance quite similar as they all consist of dichotomously branching naked axes, a detailed look shows striking differences between the individual taxa. However, several of these differences would never have been revealed by the much more common compression fossils. Even a century after the publication of the first part of Kidston and Lang’s monumental monograph the Rhynie chert continues to yield important new information. In the 1980s and 1990s Winfried Remy and his co-workers published several papers on gametophytes of Rhynie chert plants. In later years additional ones were described and life cycles could be reconstructed in more detail. Gametophytes are now known of four of the seven Rhynie chert plants, i.e. Aglaophyton major, Rhynia gwynne-vaughanii, Horneophyton lignieri and Nothia aphylla. The first two had rather simple gametophytes, whereas those of the latter two taxa are more complex. More recently published papers deal with vegetative structures in Rhynia gwynne-vaughanii and the sporangia-bearing axes of Asteroxylon mackiei, the largest and most complex plant from the Rhynie chert, which superficially looked quite similar to the modern lycopsid Huperzia selago. Currently, the development of the vascular strand in the underground parts and the aerial axes of Asteroxylon mackiei and the ontogenetic development of aerial axes of Aglaophyton major and Rhynia gwynne-vaughanii are subjects of research. Apart from the taxa described by Kidston and Lang, two other taxa have been described from the Rhynie and the nearby Windyfield chert localities. These are, however, not preserved in such great detail as the ones originally described by Kidston and Lang. This presentation will therefore focus on the well-studied taxa and give an overview of the various organs, rhizomatic and aerial axes, life stages and tissues.

Professor Hans Kerp, Institut fur Geologie und Palaeontologie, Germany

Professor Hans Kerp, Institut fur Geologie und Palaeontologie, Germany

Hans Kerp (1954; Venlo, The Netherlands) studied geology in Utrecht and obtained his MSc with a thesis on the lower Permian flora of Sobernheim, Saar-Nahe Basin, Germany. His PhD thesis “On Callipteris Brongniart from the European Rotliegend basins” (Utrecht, 1986) dealt with the systematics, ecology and biostratigraphy of a genus of fossil fern-like foliage that was originally regarded as a marker for the lower Permian. After his PhD he was appointed as lecturer at the Laboratory of Palaeobotany and Palynology in Utrecht. Early 1989 he moved to Philadelphia, where he accepted a position as research associate at the Department of Geology at the University of Pennsylvania. Mid-1990 he returned to Utrecht where he accepted a position as research scientist. In 1991 he was appointed as professor for palaeobotany/geology at the University of Münster Germany) as the successor of Winfried Remy (1928–1995). Via Winfried Remy, his research technician Hagen Hass and Thomas N. Taylor, he became involved in Rhynie chert research on which he published over 30 papers and book chapters, initially mostly in cooperation with Hagen Hass and Thomas N. Taylor, and later with Michael Krings (Munich). These papers mainly concentrated on the anatomy of poorly known taxa such as Nothia and Asteroxylon, life cycles of land plants, and on fossil microorganisms. Another major research topic is the evolution of Carboniferous, Permian and Triassic floras, notably systematics, whole-plant reconstructions, ecology, vegetation dynamics and distribution patterns. Special attention is given to gymnosperms with cuticle preservation. He published over 200 papers and book chapters, including over 130 papers in peer-reviewed journals. Since 1994 Hans Kerp is editor-in-chief of the Review of Palaeobotany and Palynology and he serves as editorial board member of several other journals such as Fossil Record, Palaeontographica Abt. B and The Palaeobotanist. Since 2013 he is vice-president of the Paläontologische Gesellschaft and since 2016 a standing member of the review panel for geology and palaeontology of the German Science Foundation (DFG).

The evolution of vascular plants from their bryophyte-like precursors underpinned a ten-fold increase in species numbers and changes the course of plant and animal evolution. Whilst living bryophytes and vascular plants have widely disparate forms, fossil intermediaries reveal stepwise morphological innovations priming the radiation of vascular plant forms, including the innovation of branching. The genetic pathways that regulate branching are well characterised in flowering plants and are conserved within the land plants, predating the origin of branching. This talk will discuss the genes involved in the evolution of branching.

Dr Jill Harrison, University of Bristol, UK

Dr Jill Harrison, University of Bristol, UK

The conquest of land by plants over 450 million years ago was one of the most significant events in our planet's history, and was underpinned by a series of key innovations in plant architecture during evolution. My group aims to identify the developmental and genetic basis of two such innovations- three dimensional shoot growth and branching. To this end we are using a range of model systems representing different stages of plant evolution such as liverworts, mosses and lycophytes.