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.

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.

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.

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.

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.

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.

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.

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.

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.