Thalloid organisms and the fossil record

Abstract

Thalloid body plans occur in several groups of organisms, including bryophytes, lichens and algae. While many aspects of the biology and ecology of extant thalloid organisms are well understood today, knowledge about the evolutionary history, palaeobiology and palaeoecology of these life forms remains limited. The recently discovered thalloid fossil Litothallus ganovex from the Triassic of Antarctica consists of fused vertical cell filaments forming a pseudoparenchymatous crust-like body, and most likely represents a freshwater macroalga. Other cuticle fragments from Antarctica are tentatively interpreted as remains of thallose liverworts. These unexpected new finds indicate that thalloid organisms are more frequent in the fossil record than previously assumed, and contribute to a better understanding of the palaeobiodiversity of ancient nonmarine ecosystems.

Based on the seemingly simple organization of extant thalloid organisms (e.g., thalloid liverworts, lichens and algae), it has historically been believed that primitive thallophyte communities had colonized the terrestrial realm long before the first appearance of vascular land plants in the Silurian.^1,2 This hypothesis is continuously substantiated by an increasing number of reports of (crypto)spores, phytodebris and biogeochemical signals attributable to thalloid organisms that predate the earliest unequivocal axial land plant fossils by at least 40 million years.^3–7 However, with the exception of marine calcified algae, the macrofossil record of thalloid organisms is meagre throughout Earth history. This is commonly explained by the general absence of sclerified stabilizing and conducting tissues in thalloid bodies that drastically reduces the fossilization potential.

We recently published an account on an exceptionally well-preserved non-marine thalloid organism from the Triassic of the Transantarctic Mountains.⁸ This organism, Litothallus ganovex, occurs as compressions of rosette-like thalli (Fig. 1A) with associated cellular sheets (Fig. 1C and D). The exquisite preservation of the fossils enabled a detailed study of the peculiar anatomy of the organism. The thallus of L. ganovex consists of densely spaced, vertical cellular filaments that are laterally fused to form a sheet- or crust-like structure (Fig. 1B). Thalloid bodies containing such pseudotissues only occur in certain algae and lichens. It appears most likely that L. ganovex represents a freshwater macroalga based on its striking resemblance to certain extant freshwater representatives of the red algal order Hildenbrandiales. We speculated that L. ganovex may have been a widespread constituent of certain Triassic freshwater ecosystems that was simply overlooked by earlier workers because of its inconspicuous appearance; Litothallus superficially resembles a coaly film on a sediment bedding plane. Recently we had the opportunity to study the large collection of Mesozoic plant fossils from various localities in Antarctica housed at the Natural History Museum and Biodiversity Research Center of the University of Kansas, Lawrence, KS. It appeared that many slabs with Triassic plant fossils also contain abundant Litothallus specimens, which demonstrates that this organism was in fact more common than we had originally envisaged. In some of the slabs large accumulations of thalli may even form thin coaly layers in the sediment.

Figure 1.

The putative freshwater macroalga Litothallus ganovex (A–D) and other recently discovered enigmatic cuticular remains (E–I) from c. 225–195 million-year old sediments of the Transantarctic Mountains. (A) two thalli of L. ganovex. (B) UV epifluorescence-microscopic image of a thallus in cross section showing the (sub)vertical arrangement of cellular files. (C) SEM image of L. ganovex. (D) light-microscopic image of an isolated cellular sheet of L. ganovex. (E) Dorsal cuticle of a yet unidentified organism here interpreted as a liverwort. (F) SEM image of slit-like cavity in the dorsal cuticle surface, lined with papilla-like protrusions. (G) detail of several papilla-like protrusions at the bottom of a cavity, showing surface relief of helical ridges and furrows. (H) detached ventral cuticle showing the orthogonal cell pattern with intercalated pore-bearing cells. (I) detail showing intercalated roundish cells bearing tube-like pores with thickened rims. Scale bars: (A) = 1 cm; (B, D and I) = 50 µm; (E) = 500 µm; (C and F) = 100 µm; (G) = 20 µm; (H) = 200 µm.

We have also discovered other enigmatic organic remains of putative thalloid organisms in a similar mode of preservation. For example, bulk macerations of Early Jurassic (c. 195–200 million-year old) sediments from Section Peak in North Victoria Land, Antarctica, have yielded a particularly interesting fossil that consists of a dorsiventally organized cuticle with upper and lower surfaces still in physical association. Neither of the surfaces shows stomata or indications of vein courses. Instead, the upper surface (Fig. 1E) bears slit-like cavities that are lined with large hollow protrusions of the epidermal cells (Fig. 1F). Some of these protrusions possess an interior microrelief of helical ridges and furrows (Fig. 1G). The lower cuticle is comparatively thin and displays an orthogonal pattern of rectangular cells with intercalated roundish cells bearing peculiar tube-like, thick-rimmed pores of about 25 µm diameter (Fig. 1H and I). Remotely similar cuticle-like remains of unknown affinity have been reported from Silurian and Devonian deposits.⁹ Graham et al. have attempted to clarify the identity of these enigmatic Palaeozoic fossils by comparing them with experimentally degraded liverwort thalli.¹⁰ Extant liverworts were therefore subjected to a series of degradation treatments simulating the effects of decay and burial. These treatments produced isolated ventral cuticles with thick-rimmed tubular pores, which represent the remnants of broken-off rhizoids.¹⁰ While the purported similarity between the artificially degraded liverwort remains and the Silurian/Devonian cuticle-like fossils has later been questioned, it is interesting to note that some of the liverwort fragments illustrated by Graham et al. are almost identical to the Jurassic cuticle from Section Peak. At present we can only speculate about the biological affinities of the Section Peak fossil, but we suggest that it may represent a fragment of a thallose liverwort. In this context it is worth to draw attention to the extant liverwort genus Monoclea. In contrast to most other complex thallose liverworts, Monoclea thalli lack air pores and a clearly defined midrib.¹¹ Rhizoids with diameters of 9 to 35 µm are scattered over the entire ventral surface.¹¹ Moreover, Monoclea produces archegonia embedded between mucilage hairs in flask-shaped archegonial cavities on the dorsal side.¹¹ Although highly speculative at present, the slit-like cavities of the Jurassic fossil may have had a similar function. We hope to obtain additional material from Section Peak that permits more detailed analyses and comparisons to further test our hypothesis regarding this highly remarkable Jurassic fossil.

The current perception of thalloid organisms in the fossil record remains strongly biased for several reasons. Traditionally, intentional search for fossil thalloid organisms focuses almost exclusively on the Palaeozoic, and aims at resolving the earliest history of plant life on land. Reports on thalloid fossils from younger periods of Earth history are comparatively sporadic and often merely the result of incidental finds. Moreover, impression and compression fossils of thalloid organisms have often been misidentified (e.g., as fern aphlebiae, conifer twigs, arthropod cuticles or trace fossils), and consequently have been grouped together with superficially similar fossils that belong to entirely different organisms.¹² The general scarcity of uncalcified thalloid organisms in the fossil record may therefore to a certain degree also be a result of these strong biases in collecting, identifying and ultimately in studying these often inconspicuous fossils. The search for fossil thalloid organisms, especially from post-Palaeozoic deposits, can greatly contribute to a more accurate reconstruction of the diversity and functioning of ecosystems through time. We hope that our recent discoveries of Litothallus and other wellpreserved, yet enigmatic thalloid fossils provide a stimulus for a reappraisal of this largely disregarded segment of life in the past.

Addendum to: Bomfleur B, Krings M, Kaštovský J, Kerp H. An enigmatic non-marine thalloid organism from the Triassic of East Antarctica. Rev Palaeobot Palynol. 2009;157:317–325.