New plant taxa from the Lower Devonian (Lochkovian) of the Welsh Borderland, with a hypothesis on the relationship between hilate and trilete spore producers

doi:10.1016/j.revpalbo.2011.06.007

Review of Palaeobotany and Palynology

Volume 167, Issues 1–2, September 2011, Pages 51-81

https://doi.org/10.1016/j.revpalbo.2011.06.007 Get rights and content

Abstract

A detailed investigation of charcoalified Lochkovian mesofossils, undertaken to circumscribe diversity and disparity in early land vegetation, has revealed a number of discoidal spore masses, enveloped by a featureless cuticular layer. The specimens are interpreted as incompletely preserved terminal sporangia. Based on haptotypic features of the spores, two groups of sporangia are recognised: the first contains alete sculptured monads, the separated products of dyads that are assigned to the dispersed cryptospore genus Cymbohilates Richardson; the second contains laevigate and apiculate trilete monads, the products of tetrads that are assigned to the dispersed genera Ambitisporites Hoffmeister, Streelispora (Chaloner and Streel) Richardson and Lister, and Aneurospora Streel. A new genus, Lenticulatheca, with four new species, L. magna, L. mesodeca, L. variabilis, and L. allenii, has been erected for the cryptospore producers, distinction being based on species and varieties of Cymbohilates. The trilete spore producers, which were far more numerous, have been assigned to a second new genus, Paracooksonia, to emphasise similarities with Cooksonia Lang, both in gross morphology of the spore mass and in situ spore genera. Paracooksonia apiculispora is erected for specimens with in situ apiculate spores and Paracooksonia ambitispora is erected for laevigate in situ spores. Similarities in the bilayered exospore and sculpture, together with those of gross morphology have led to the hypothesis that the two new genera are closely related, the major distinction arising from changes in the timing of cytokinesis during meiosis that resulted in either dyads or tetrads. Information on missing vegetative features is essential to elucidating unequivocally the proximity to the tracheophytes, but similarities with the Cooksonia complex suggest that the two new genera should be considered rhyniophytoids.

Highlights

► New discoidal spore masses with cuticular coverings interpreted as terminal sporangia.► Lenticulatheca contain species of Cymbohilates, alete monads separated from dyads.► Paracooksonia contain trilete spores e.g. Streelispora, separated from tetrads. ► Similarities between genera include morphology, spore sculpture and ultrastructure. ► Hypothesis that new taxa were closely related, differing in the timing of meiosis.

Introduction

One of the most intriguing aspects of evidence relating to the early history of terrestrial plants is the presence of dyads, together with more familiar tetrahedral tetrads, in palynomorph assemblages from Ordovician to Lower Devonian rocks (e.g. Richardson, 1992, Rubinstein et al., 2010, Steemans and Wellman, 2004, Strother and Traverse, 1979, Wellman, 1996). It was the description of ultrastructure in dyads, not tetrads, that contributed the most convincing fossil evidence to the hypothesis that the earliest embryophytes had hepatic affinity (Taylor, 2000), although many workers have emphasised that provided by the permanent tetrads as in certain extant hepatics (e.g. Gray, 1985). Ambiguity on the affinities of dyads and alete monads led one of us to coin the term cryptospores (Richardson, 1985, Richardson et al., 1984). Further discussions on their nature have led to a plethora of definitions for such palynomorphs (e.g. Steemans, 2000, Strother, 1991, Strother and Beck, 2000) that would certainly benefit from knowledge of the parent plants. To this end we have been screening thousands of the earliest of such fossils (mesofossils) available to us, albeit from relatively recent Lochkovian strata, in an attempt to find in situ cryptospores. Success to date has centred on laevigate hilate monads, most assigned to the Laevolancis complex (Wellman et al., 1998a), permanent laevigate dyads (Wellman et al., 1998b), and smooth and sculptured permanent tetrads (Edwards et al., 1999). Here we report on mesofossils containing sculptured hilate monads, the separated products of dyads that are assignable to members of the Cymbohilates complex (Richardson, 1996a). At the outset we should emphasise that the erection of new taxa on a very limited number of specimens is a practice we should not normally wish to follow, but are of the opinion that the importance of these specimens supersedes such reservations in this case. By contrast, a second group of terminal sporangia of similar shape and peripheral ‘tissue’, but bearing trilete spores with similar construction and sculpture to the hilate monads, contains numerous representatives and has allowed analysis of variation in sculpture and features of the proximal surface.

Section snippets

Geological setting

The fluvial rocks containing the mesofossils were collected from a stream section on the north side of Brown Clee Hill, Shropshire (Edwards, 1996). They occur in the lower and middle parts of the Ditton Formation (Ball and Dineley, 1961). Dispersed spore assemblages from middle parts of the sequence, logged and studied by Richardson (unpublished), belong to the middle sub-biozone of the micrornatus-newportensis Sporomorph Assemblage Biozone (Richardson and McGregor, 1986) and indicate an early

Material and preparation

Coalified mesofossils were extracted from a pale grey unconsolidated siltstone by gentle disaggregation in water, followed by treatment with concentrated hydrochloric acid for 24 h, diluted with water (1 day) and then subjected to commercial strength (40%) hydrofluoric acid (3 days) to remove residual grains. Centrifugation was never used. Spores were isolated by conventional palynological techniques (Wood et al., 1996), followed by treatment with concentrated HNO₃ or Schulze solution.

Most of the

Hilate spore producers

Lenticulatheca Morris, Edwards, Richardson, Axe, Davies gen. nov.

Diagnosis: Terminal sporangium containing a lens-shaped mass of numerous alete monads. Mass limited by a single non-cellular, cuticular layer. Exospore bilayered. Distal and proximo-equatorial surfaces with microsculpture.

Derivation: Lenticularis (L) lens shaped (based on lens = lentil). Theca (L) = container.

Type species: Lenticulatheca magna Morris, Edwards, Richardson, Axe, Davies sp. nov.

Lenticulatheca magna Morris et al. sp.

New taxa containing hilate monads

All specimens comprise discoidal spore masses, partially covered by a single layer of amorphous material, but lacking any evidence for a cellular sporangial wall or subtending axes. The spores are monads with sculptured distal surfaces and proximal hila, some laevigate and some with ridges. Spores from all specimens can be assigned to Cymbohilates, a dispersed genus for proximally hilate cryptospore monads with sub-equatorial and distal sculptures (Richardson 1996a). As few specimens comprise

Relationships between Lenticulatheca and Paracooksonia

The taxa show strong similarities in spore ultrastructure and sculpture, in morphology of the spore mass and in the presence of an enveloping cuticular layer with similar structural features. They differ in haptotypic characters which reflect differences in spore configurations before separation. In common with other authors (e.g. Fanning et al., 1991, Hemsley, 1994, Strother, 1991, Wellman et al., 1998a, Wellman et al., 1998b) we consider that dyads were produced following cytokinesis after

Conclusions

(i)
Two new groups of mesofossils are described that share similarities in discoidal gross morphology, non-cellular cuticular coverings and ± subtending axes or attachment sites on the proximal surfaces. They differ in spore type (hilate and trilete spores), hence justification for their separation and assignment to Lenticulatheca and Paracooksonia.
(ii)
The hilate and trilete spores show broad similarities in ultrastructure and distal sculpture but have no exact counterparts.
(iii)
We consider that the two

Acknowledgments

This study was funded by a Leverhulme Trust Research Project Grant and The Gatsby Charitable Foundation. Acknowledgments go to U. Fanning for preliminary work on some specimens and to Suzanne Feist Burkhardt for photography of spore holotypes. The authors thank the reviewers who provided helpful comments.

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Research paperNew plant taxa from the Lower Devonian (Lochkovian) of the Welsh Borderland, with a hypothesis on the relationship between hilate and trilete spore producers

Abstract

Highlights

Introduction

Section snippets

Geological setting

Material and preparation

Hilate spore producers

New taxa containing hilate monads

Relationships between Lenticulatheca and Paracooksonia

Conclusions

Acknowledgments

Rev. Palaeobot. Palynol.

Rev. Palaeobot. Palynol.

Rev. Palaeobot. Palynol.

Rev. Palaeobot. Palynol.

Rev. Palaeobot. Palynol.

Bot. J. Linn. Soc.

The Old Red Sandstone of Brown Clee Hills and the adjacent area. I. Stratigraphy

Bull. Br. Mus. Nat. Hist. Geol.

Silurian cryptospores and miospores from the Wenlock, Shropshire, England

Palaeontology

The ultrastructure of spores of Cooksonia pertoni

Palaeontology

Tetrads in sporangia and spore masses from the Upper Silurian and Lower Devonian of the Welsh Borderland

Bot. J. Linn. Soc.

Cryptic evolution in an early land plant

Evol. Trends Plants

A review of in situ spores in Silurian land plants

A new definition and a lectotypification of the genus Cooksonia Lang 1937

Int. J. Plant. Sci.

The microfossil record of early land plants: advances in understanding of early terrestrialization, 1970–1984

Phil. Trans. R. Soc. B

New perspectives on Cooksonia from the Lower Devonian of the Welsh Borderland

Bot. J. Linn. Soc.

The origin of the land plant sporophyte: an interpolational scenario

Biol. Rev.

Abnormal reductional and non-reductional meiosis in Ceratopteris: alternatives to homozygosity and hybrid sterility in homosporous ferns

Am. J. Bot.

Structure and ontogeny of plant cuticles

On the plant-remains from the Downtonian of England and Wales

Phil. Trans. R. Soc. B

Research paper
New plant taxa from the Lower Devonian (Lochkovian) of the Welsh Borderland, with a hypothesis on the relationship between hilate and trilete spore producers