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

Chapter 4

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

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

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

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

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

49

50

Lower MN Group

Taxon

TM

1

TR

Culullitheca richardsonii

Cryptophytes

Fusiformitheca fanningiae

x

Grisellatheca salopensis

x

Lenticulatheca spp.

x

Partitatheca spp.

BT

Upper MN 5

CM

Cooksonia cambrensis

(x)

x

Cooksonia hemisphaerica

x

x x

ND

BZ AD

8

RW

(x) x

x

x

(x) (x)

(x)

x

Electorotheca enigmatica

x c

cf. Aberlemnia caledonica

x

x

x

Monnowella bennettii

x

(x)

x

Resilitheca salopensis

x

Sporathylacium salopense

x

cf. Horneophyton sp.

x

Salopella allenii

x

x

Salopella marcensis

x

x

cf. Sporogonites sp.

x (x)

(x)

x

x

(x)

x

Tarrantia salopensis

x

Tortilicaulis offaeus

(x)

x

x x

Tortilicaulis transwalliensis

x

Uskiella reticulata

x

Uskiella spargens

7

x

Concavatheca banksii

Paracooksonia spp.

Elongate/oval

CR

6

x b

Cooksonia pertoni

Bivalved

NBCH

4

x a

Discoidal

3

x

Ficoiditheca aenigma

Rhyniophytoids

Middle MN 2

(x) x

(x) (x) x

9

MBQ10

SECTION j I Early Land Plants: Innovations and Adaptations

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

Zosterophylls

Zosterophyllum cf. fertile

x

x

Deheubarthia splendens

x

x

Gosslingia breconensis

x

Craswallia haegensis Zosterophyllum sp.

Trimerophytes

x

x

x x x

Zosterophyllum llanoveranum

x

Dawsonites sp.

x

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

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SECTION j I Early Land Plants: Innovations and Adaptations

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

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

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

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

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

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

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

53

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

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

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SECTION j I Early Land Plants: Innovations and Adaptations

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

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

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

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

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

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

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

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

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SECTION j I Early Land Plants: Innovations and Adaptations

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

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

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

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SECTION j I Early Land Plants: Innovations and Adaptations

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

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

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

59

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

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

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

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

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

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

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

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

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

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

Geographical Area

Biozone/Age

Taphonomy

Freshwater West Fm.

Brecon Beacons

Lower MN Biozone; early Lochkovian

Compressions in distal fluviatile channel siltstones and sandstones1

Targrove

Clee Hills, Shropshire

Lower MN Biozone; early Lochkovian

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

North Brown Clee Hill

Clee Hills, Shropshire

Middle MN Biozone; middle Lochkovian

Charcoal in distal fluviatile siltstones4

Bryn Glas Tunnels

South Wales

Middle MN Biozone; middle Lochkovian

Compressions in distal fluviatile siltstones5

Cwm Mill

Black Mountains

Middle MN Biozone; middle Lochkovian

Compressions in distal fluviatile siltstones6

Craswall

Black Mountains

Middle-upper MN Biozone, middle-upper Lochkovian

Compressions in medial fluviatile siltstones and sandstones7

Newton Dingle

Clee Hills, Shropshire

Upper MN to BZ Biozone, late Lochkovian

Compressions in medial fluviatile sandstones8

Beacon Beacons

BZ Biozone, late Lochkovian

Compressions in medial fluviatile siltstones and sandstones9

Black Mountains

BZ Biozone, late Lochkovian

Compressions in medial fluviatile siltstones and sandstones9

Pembrokeshire

BZ Biozone, late Lochkovian

Compressions and permineralisations in medial fluviatile silty sandstones10

Locality Tredomen Quarry

Allt Ddu

Senni Fm.

Rhiw Wen Mascle Bridge Quarry

Llanstadwell Fm.

1

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

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

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

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

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

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

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

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

63

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

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

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SECTION j I Early Land Plants: Innovations and Adaptations

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

5.4 Technological Advances in Anatomical Investigations

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

5.4.1 Electron Microscopy and Synchrotron Tomography

5.4.2 Light Microscopy

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

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

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

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

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

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

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

REFERENCES Allen, J.R.L., 1964. Studies in fluviatile sedimentation: six cyclothems from the Lower Old Red Sandstone, Anglo-Welsh Basin. Sedimentology 3, 163e198. Allen, J.R.L., 1974. Sedimentology of the Old Red Sandstone (SiluroDevonian) in the Clee Hills area, Shropshire, England. Sedimentary Geology 12, 73e167. Allen, J.R.L., Crowley, S.J., 1983. Lower Old Red Sandstone fluvial dispersal systems in the British Isles. Transactions of the Royal Society of Edinburgh 74, 61e68. Allen, J.R.L., Dineley, D.L., 1976. The succession of the Lower Old Red Sandstone (Siluro-Devonian) along the RosseTewkesbury Spur Motorway (M.50), Hereford and Worcester. Geological Journal 11, 1e14. Allen, J.R.L., Tarlo, L.B., 1963. The Downtonian and Dittonian facies of the Welsh Borderland. Geological Magazine 100, 129e155. Allen, J.R.L., Williams, B.P.J., 1979. Interfluvial drainage on SiluroDevonian alluvial plains in Wales and the Welsh Borders. Journal of the Geological Society, London 136, 361e366. Allison, P.A., 1988. Konservat-Lagerstätten: cause and classification. Paleobiology 14, 331e344. Allison, P.A., Briggs, D.E.G., 1993. Exceptional fossil record: distribution of soft-tissue preservation through the Phanerozoic. Geology 21, 527e530. Ball, H.W., Dineley, D.L., 1961. The Old Red Sandstone of Brown Clee Hill and the adjacent area. I. Stratigraphy. Bulletin of the British Museum (Natural History) 5, 1e136.

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

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SECTION j I Early Land Plants: Innovations and Adaptations

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

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

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

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

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