Opisthokonta Articles 1

Giants of the Silurian

Published 11 April 2008

Compared to life in the water, life on land got off to a decidedly slow start. The seas had been swarming with life for hundreds of millions of years before the first tentative colonisation of the previously barren continents by small algae and plants in the Ordovician about 470 million years ago. Even then, it wasn’t until about the middle part of the Silurian, about 430 million years ago (give or take) that the first vascular plants and anything bigger than a moss put in an appearance. These early plants were still small by modern standards—one of the larger forms, Cooksonia, was practically a giant at heights of nearly a metre. The first really large land organism made its imposing appearance in the late Silurian.

Reaching heights of up to eight metres, Prototaxites would have loomed over anything else around at the time—something that is made pretty clear in the reconstruction above from Hueber (2001) (obtained via Hans Steur’s palaeobotany page, which has a far better analysis of Prototaxites than I’m about to give you). Prototaxites is known from fossils reminiscent of the trunk of a tree, and was originally described as such in 1859. However, the internal structure of Prototaxites is very different from that of any tree. Rather than the vascular cells of a tree, Prototaxites is composed of long filamentous tubes—large unbranched tubes that probably supplied structural support, and much smaller multi-branched tubes that ran among and around the skeletal filaments and probably held the structure together. This structure was compared to the filamentous structure of a number of modern algae, and for many years Prototaxites was considered a giant alga, probably related to the modern brown algae.

However, all known algae are aquatic whereas Prototaxites was found in association with terrestrial organisms and was undoubtedly terrestrial itself. In cross-section Prototaxites also lacks the orderliness of structure found in brown algae, with filaments arranged randomly in the trunk with no clear division between pith and cortex. Hueber (2001) therefore made the suggestion that instead of being an alga, Prototaxites might be a gigantic fungus. He compared it to the living perennial bracket fungi, which have a rigid structure and can also reach notable sizes (up to a metre in diameter) through cumulative growth over many years.

The main barrier to accepting Prototaxites as a fungus lies in the size of the filaments (which would then be hyphae). The skeletal filaments reach a diameter of up to 50μm while modern fungi will rarely be more than 10μm. The other major issue, of course, is its size overall. Where did such a large saprobic fungus gain its nutrients from? Despite the plausability of Hueber’s (2001) model of perennial growth, and his comparison with the gigantic size attained by hyphal masses in other modern fungi such as a specimen of Armillaria bulbosa covering an area of 15ha, Selosse (2002) pointed out that the modern taxa live in an environment with a much larger overall biomass. A purely saprobic Prototaxites would have required far more nutrition than could be supplied by the meagre vegetation of the Silurian. Selosse (2002) therefore suggested that, rather than being purely fungal, Prototaxites might have been a photosynthetic lichen-like symbiosis. The large skeletal filaments, he suggested, might still represent an algal form, contained and protected by the surrounding fungal hyphae. The idea of an eight-metre-tall lichen is still pretty amazing, but not incredible when we consider that there would have been relatively little competition in the Silurian compared to the modern environment. Prototaxites may have been a slow and inefficient grower, but there was little to exclude it. Hueber (2001) identified supposed reproductive structures on Prototaxites that he held indicated a position for it among the basidiomycetes, which include the bracket fungi. However, as pointed out by Selosse (2002), the reproductive nature of these structures is unconvincing.

No convincing evidence has been found for branching in Prototaxites. Many authors interpreting Prototaxites as a plant or alga have suggested that the flattened fossil Nematothallus found in the same deposits, which also has a filamentous structure, might represent leaves or leaf-like appendages of Prototaxites. However, the two have never been found directly attached. Graham et al. (2004) noted a similarity between Nematothallus and semi-decayed modern liverworts, and suggested that Nematothallus might belong to the latter group.

Prototaxites was around for about 50 million years, a quite impressive amount of time, but it eventually became extinct during the Devonian. Perhaps as the terrestrial environment increased in complexity, the window of low competition that Prototaxites had occupied closed. More efficient plants supplanted Prototaxites, while increased numbers of herbivores may have eaten down growing hyphae faster than the organism could regrow them. Prototaxites‘ time had come to a close.

Prototaxites: a giant that never was?

Published 10 February 2010

Nearly two years ago, I wrote the above section on Prototaxites, a mysterious fossil of the late Silurian and the earliest truly large terrestrial organism known from the fossil record. I have discussed the possibility that Prototaxites might have represented a giant fungus but a recent publication by Graham et al. (2010a) presents a new alternative interpretation of Prototaxites. If they are correct, the Silurian may never be the same again.

In Graham et al.‘s estimation, Prototaxites should not be classed with the fungi but with the liverworts. Liverworts are small, often mosslike plants of moist habitats. Members of one group of liverworts, the thallose liverworts, lack any distinction between leaves and stem but grow as a flattened thallus anchored to the ground by rhizoids (rootlets) on the lower surface. Liverworts are one of the earliest diverging groups of land plants and they or their ancestors would have certainly been part of the Silurian flora. One group of Silurian plant fossils, the nematophytes, possess a microstructure of criscrossing tubular filaments; Graham et al. (2004) demonstrated that this structure was also found in the decaying remains of modern thallose liverworts, as the upper tissue of the thallus rotted away to leave the more resistant rhizoids and connective tissue. The microstructure of Prototaxites is also similar to that of nematophytes, to the extent that some palaeontologists have regarded nematophytes as Prototaxites leaves (this interpretation is not currently supported as nematophytes have never been found actually attached to Prototaxites). But modern liverworts lack strong supporting tissue and would be pushing to reach an inch in height – how could they have produced the eight-metre columns recorded for Prototaxites?

A transverse section of Prototaxites shows a ring structure like that found in a tree trunk. Hueber (2001), who interpreted Prototaxites as a perennial fungal fruiting body, felt that this ring structure also resembled tree rings in indicating discontinuous growth by the organism. Graham et al. (2010a) interpret the ring structure differently. They suggest that large mats of thallose liverworts covered the Silurian landscape. These mats could become detached from their substrate by agents such as wind and rain, and start to roll up as they decayed. As they rolled, they would form the large columns that, after being compressed by burial and fossilised, would eventually be identified as Prototaxites.

Under this interpretation of Prototaxites, the fungal hyphal structures identified by Hueber (2001) within Prototaxites sections would be those of fungi growing among the liverwort mats. Boyce et al. (2007) identified significant variations in carbon isotope ratios between Prototaxites individuals as supportive of fungal identification because they suggested heterotrophy (nutrients being obtained from the surrounding environment rather than being produced by the organism itself); however, Graham et al. (2010a) establish that thallose liverworts may grow heterotrophically when conditions encourage it. The liverwort interpretation is also more consistent with the size of most Prototaxites filaments (much larger than found in modern fungi) and also explains the occasional discovery of other land plants embedded in Prototaxites columns—these would have been growing among the mats and become swept up when the mats became rolled, like Silurian Cleopatras.

I find this new interpretation intriguing, if a little difficult to accept outright. Prototaxites is represented by a reasonable number of specimens (I don’t know the actual number, but thirteen species have been named from numerous localities around the world)—were the conditions that would have lead to mat-rolling common enough to have produced that number of fossils? I wonder if it would be worth investigating how Prototaxites specimens compare in abundance to nematophyte specimens and what that might tell us about the likelihood of ‘Prototaxites‘ formation from liverwort mats. Certainly, the only thing that could be more intriguing than the existence of these giant pillars from so early in the earth’s history would be if it turned out that they never existed at all.

Prototaxites revisited

Published 5 November 2012

Richard Bizley has been kind enough to allow me to reproduce the above painting, which he produced in response to discussion arising from the post above. It shows a ‘forest’ (for want of a better word) of the enigmatic Silurian-Devonian organism Prototaxites reconstructed as a giant fungus. Richard has asked if anyone has any comments to make on the final product. Is this environment plausible? Could Prototaxites have grown in clusters like this, or would nutrient restrictions been such as to prevent such large organisms from persisting in close proximity to each other?

Since I produced my earlier post on the possible re-interpretation of Prototaxites as representing rolled ground-cover mats (Graham et al. 2010a), the proposal has been criticised in print by Boyce and Hotton (2010) and Taylor et al. (2010), and defended by Graham et al. (2010b). Boyce and Hotton regard it as taphonomically implausible that such rolls could form, while Taylor et al. also point out that the major tubes making up Prototaxites are arranged longitudinally down the ‘trunk’, not radiating outwards. Graham et al. have pointed out how they feel this is not incompatible with their liverwort mat hypothesis.

Prototaxites, it should be pointed out, was just one of a number of Silurian-Devonian organisms called nematophytes. Nematophytes are united by their similar internal structure, composed of hypha-like tubes. However, other nematophytes did not have the gigantic columnar form of Prototaxites: Nematothallus, for instance, was an encrusting lichen-like form, while Nematasketum fossils are only a couple of centimetres in size. Edwards and Axe (2012) have recently published a study on Nematasketum and supported comparisons between nematophytes and fungi. In particular, they compare Nematasketum to root-like anchoring and foraging structures called rhizomorphs produced by some large modern basidiomycetes. Hillier et al. (2008) nominated Prototaxites as potentially connected to root-like casts found in the Anglo-Welsh Old Red Sandstone, but admitted that the grounds for connection were slight.

References

Boyce, C. K., & C. L. Hotton. 2010. Prototaxites was not a taphonomic artifact. American Journal of Botany 97 (7): 1073.

Boyce, C. K., C. L. Hotton, M. L. Fogel, G. D. Cody, R. M. Hazen, A. H. Knoll & F. M. Hueber. 2007. Devonian landscape heterogeneity recorded by a giant fungus. Geology 35: 399–402.

Edwards, D., & L. Axe. 2012. Evidence for a fungal affinity for Nematasketum, a close ally of Prototaxites. Botanical Journal of the Linnean Society 168: 1–18.

Graham, L. E., M. E. Cook, D. T. Hanson, K. B. Pigg & J. M. Graham. 2010a. Structural, physiological, and stable carbon isotopic evidence that the enigmatic Paleozoic fossil Prototaxites formed from rolled liverwort mats. American Journal of Botany 97 (2): 268–275.

Graham, L. E., M. E. Cook, D. T. Hanson, K. B. Pigg & J. M. Graham. 2010b. Rolled liverwort mats explain major Prototaxites features: response to commentaries. American Journal of Botany 97 (7): 1079–1086.

Graham, L. E., L. W. Wilcox, M. E. Cook & P. G. Gensel. 2004. Resistant tissues of modern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils. Proceedings of the National Academy of Sciences of the USA 101 (30): 11025–11029.

Hillier, R. D., D. Edwards & L. B. Morrissey. 2008. Sedimentological evidence for rooting structures in the Early Devonian Anglo-Welsh Basin (UK), with speculation on their producers. Palaeogeography, Palaeoclimatology, Palaeoecology 270 (3–4): 366–380.

Hueber, F. M. 2001. Rotted wood–alga–fungus: the history and life of Prototaxites Dawson 1859. Review of Palaeobotany and Palynology 116 (1–2): 123–158.

Selosse, M.-A. 2002. Prototaxites: a 400 myr old giant fossil, a saprophytic holobasidiomycete, or a lichen? Mycological Research 106 (6): 642–644.

Taylor, T. N., E. L. Taylor, A.-L. Decombeix, A. Schwendemann, R. Serbet, I. Escapa & M. Krings. 2010. The enigmatic Devonian fossil Prototaxites is not a rolled-up liverwort mat: comment on the paper by Graham et al. (AJB 97: 268–275). American Journal of Botany 97 (7): 1074–1078.