Bucklandiella lusitanica

The diversity of mosses is much higher than many people realise. Whereas some moss species have wide ranges that may cross between continents and hemispheres, others are unique to very specific regions and habitats. Among examples of the latter is the European species Bucklandiella lusitanica.

Illustrations of Bucklandiella lusitanica, from Ochyra & Sérgio (1992). Top left: habit; top right: section of stem of hair-leafed form when dry; lower left: section of stem of hairless form and sporophyte when wet.

Bucklandiella lusitanica was only described as a new species (under the name Racomitrium lusitanicum) in 1992 (Ochyra & Sérgio 1992), having gone unnoticed previously despite being a relatively distinctive species. Recent collections of the species have been identified from a single region, the Serra do Gerês mountain rainge and Parque Natural da Peneda-Gerês national park in the northwest of Portugal, at altitudes between 650 and 1000 metres. A single collection from the Serra do Estrela further south in the country was made in the mid-1800s though it went unidentified at the time. Its rarity is such that is has officially been listed as Endangered by the IUCN. Bucklandiella lusitanica is a rheophyte, which is to say that it grows in association with running water. It grows on acidic granite rocks that are periodically or permanently submerged, such as alongside streams and waterfalls. It is particularly abundant on steep rock faces, growing in association with closely related moss species.

Appearance-wise, Bucklandiella lusitanica is a medium-sized moss with irregularly branched stems growing 1.5 to 3.5 centimetres in length. Leaves are rigid, held tight to stem, and two or three millimetres long.One of the species' most distinctive features is a broad, fleshy margin to each leaf that is generally two or three cells thick whereas the lamina of the leaf is mostly only a single cell thick. The alar cells at the base of the sides of the leaf often form inflated, strongly coloured lobes. The leaves commonly end in a fine, colourless hair-point. The structure of the leaves is similar to that of Bucklandiella lamprocarpa, another aquatic moss species, but that species lacks the hair-points. The two species also differ in the form of their spores, those of B. lamprocarpa being larger and more ornate than those of B. lusitanica, and B. lamprocarpa has fatter and often shinier capsules than B. lusitanica.

I mentioned previously that Bucklandiella lusitanica was originally described as a member of the genus Racomitrium. The moss genus Racomitrium was long recognised by a distinctive array of features including leaf lamina cells with distinctly sinuous longitudinal cell walls, a calyptra (the cap of the developing capsule) that is basally frayed into several lobes, and teeth of the peristome (the teeth around the aperture of a mature capsule) that are split into two or more segments (Sawicki et al. 2015). Racomitrium in this sense was a diverse genus with over two hundred species having been named at one time or another, and somewhere between sixty and eighty species recognised as valid in recent years, As a result, Ochyra et al. (2003) proposed the division of Racomitrium in the broad sense between four separate genera. Bucklandiella, the largest of these segregate genera (with about fifty currently known species), was recognised for species with a smooth leaf surface (lacking papillae on the lamina) and relatively short, shallowly divided teeth in the peristome. The division of Racomitrium has not been universally accepted. Larrain et al. (2013) questioned the monophyly and diagnosability of Ochyra et al.'s segregates but Sawicki et al. (2015) reiterated their support for the new system (and added a fifh new segregate genus to boot). It is generally accepted that Racomitrium in the broad sense represents a monophyletic unit, so the question of whether lusitanicum should be assigned to Racomitrium or Bucklandiella may largely be considered a question of just how closely circumscribed you feel a genus should be.

REFERENCES

Larraín, J., D. Quandt, M. Stech & J. Muñoz. 2013. Lumping or splitting? The case of Racomitrium (Bryophytina: Grimmiaceae). Taxon 62 (6): 1117–1132.

Ochyra, R., & C. Sérgio. 1992. Racomitrium lusitanicum (Musci, Grimmiaceae), a new species from Europe. Fragmenta Floristica et Geobotanica 37 (1): 261–271.

Ochyra, R., J. Żarnowiec & H. Bednarek-Ochyra. 2003. Census Catalogue of Polish Mosses. Institute of Botany, Polish Academy of Sciences: Cracow.

Sawicki, J., M. Szczecińska, H. Bednarek-Ochyra & R. Ochyra. 2015. Mitochondrial phylogenomics supports splitting the traditionally conceived genus Racomitrium (Bryophyta: Grimmiaceae). Nova Hedwigia 100 (3–4): 293–317.

Define 'Trichostomum'

The moss in the above photo Icopyright Hermann Schachner) generally goes by the name of Trichostomum crispulum. Trichostomum is a cosmopolitan genus in the Pottiaceae, the largest recognised family of mosses with about 1500 species overall. But with great diversity comes great difficulty of identification. Pottiaceae tend to be small mosses that are common in harsh habitats. Features of pottiaceous mosses are often hard to distinguish and may be quite variable, making it difficult to confidently define taxa. As a result, Pottiaceae is a prime example of what I like to call 'taxonomic blancmange': something that tends to just get prodded nervously then backed away from when it wobbles ominously.

Characteristic features of Trichostomum as it is commonly recognised tend to include symmetric leaves with more or less plane margins, and with the basal cells of the leaf differentiated straight across the blade or in a U-shape. The peristome of the capsule also tends to be short and straight, and the sexual system is usually dioicous (with separate male and female plants) (Flora of North America). However, none of these features are entirely reliable, and some species have been the subject of extensive disagreement about whether they should be placed in Trichostomum, or in a related genus such as Weissia or Tortella.

To date, only a selection of Pottiaceae species have been subject to molecular analysis, but these analyses have confirmed the unsatisfactory nature of the current system. A molecular phylogenetic analysis of the pottiaceous subfamily Trichostomoideae by Werner et al. (2005) did not identify Trichostomum species as a monophyletic clade; instead, various representatives of the 'genus' were scattered throughout the subfamily. The type species of Trichostomum, T. brachydontium, was associated with a few close relatives such as T. crispulum in a broader clade containing numerous species of the genus Weissia. As a result, it has been suggested that the two genera should perhaps be synonymised, in which case the name Trichostomum would be absorbed by the older Weissia. But first, someone would need to work out just how such a genus could be recognised...

REFERENCE

Werner, O., R. M. Ros & M. Grundmann. 2005. Molecular phylogeny of Trichostomoideae (Pottiaceae, Bryophyta) based on nrITS sequence data. Taxon 54 (2): 361–368.

Hypno-Moss

Recent decades have seen a great deal of shifting around in the classification of mosses. As molecular data have become de rigeur in phylogenetic studies, a number of features previously used to distinguish higher groupings have proven to be more labile than previously appreciated. This has lead to a hunt to discern whether other features may be more reliable.

Hypnum cupressiforme, from Andrew's Moss Site.

The Hypnales are one of the major moss groups: as currently recognised, about a third of mosses are Hypnales. They are a major subgroup of the clade of pleurocarpous mosses, i. e. those in which the reproductive sporophytes arise from the sides of gametophyte stems, as explained earlier in this post. In the past, the pleurocarpous mosses have been divided between three orders, the Hypnales, Hookeriales and Leucodontales, on the basis of features of branching habit and the peristome, the array of teeth surrounding the opening of the spore capsule. In the Hookeriales, the teeth of the endostome (the inner ring of the peristome) are connected by a high basal membrane, and molecular phylogenetic analyses have generally supported this order as monophyletic. The Leucodontales were defined by having reduced peristome teeth, and usually sympodial growth (as the primary shoot produces a side-branch, it ceases growing itself and the new branch becomes the new primary shoot). The Hypnales had well-developed peristome teeth, and their growth was generally monopodial (the primary shoot continues growing even after it produces side-branches). The distinction between these latter two orders also correlated with their choice of niches: Leucodontales were mostly epiphytes, whereas Hypnales mostly grew on the ground. However, molecular phylogenetic analyses have not supported the distinction between the Hypnales and Leucodontales, with features such as reduced peristome teeth apparently evolving multiple times with the united clade combining the two orders (Buck et al. 2000). As a result, recent authors have treated the Hypnales as including most members of both the prior orders Hypnales and Leucodontales. A smaller number of pleurocarpous mosses have been placed outside the clade including Hookeriales and Hypnales in the broad sense; there are now known as the Ptychomniales and Hypnodendrales. The broader Hypnales is less well defined morphologically, but its members tend to have differentiated alar cells (distinctly formed cells at the basal corners of the leaves) and smooth spore capsules (Huttunen et al. 2012).

A mat of Leucodon, from here.
This shuffling is not restricted to the higher levels, either. Relationships within the Hypnales remain poorly resolved; indications are that at some point this group went through a quite rapid diversification, resulting in a fairly high level of convergence between lineages and low support for molecular branches. Huttunen et al. (2012) found support for a large clade within the Hypnales including the majority of its Northern Hemisphere members, with a paraphyletic grade outside this containing mostly Southern Hemisphere taxa. Huttunen et al. suggested a Gondwanan origin for the Hypnales, with their diversification in the Northern Hemisphere (where the other pleurocarpous orders never made many inroads) related to the break-up of the Laurasian landmasses. Within the Northern Hemisphere clade, many previously recognised families appear to be polyphyletic; even the type genus of the order, Hypnum, contains species that seem to occupy widely separate places in the hypnalean family tree.

The Azores-endemic moss Echinodium renaudii, copyright Paulo A. V. Borges.

A good example of all this mess is the genus Echinodium, a small genus of six living species whose distinctive appearance lead to it being placed in a family all of its own. Echinodium species grow as fairly stiff plants with long leaves that taper to a narrow point and have thickened margins (the margins are two cell layers thick whereas the body of the leaf is only one cell thick). Echinodium mosses also have a very unusual distribution: two species are found in southeastern Australia and New Zealand, but the other four are restricted to the Macaronesian islands in the Atlantic (that is, the Canaries, the Azores and Madeira). When fossil Echinodium species were discovered in eastern Europe, it was suggested that the genus' current distribution could be a relict of a previously much wider one. However, a molecular analysis of the genus by Stech et al. (2008) identified another explanation: not only were the Australasian and Macaronesian Echinodium species widely separated geographically, they were widely separated phylogenetically. The Australasian species were placed in the family Neckeraceae, whereas the Macaronesian species were related to mosses of the family Lembophyllaceae. What is more, the Macaronesian species did not form a single clade within the Lembophyllaceae: at least one of the species was placed separately from the rest. The supposedly distinctive 'Echinodium' features, it seems, have evolved independently, possibly as an adaptation for wet habitats.

REFERENCES

Buck, W. R., B. Goffinet & A. J. Shaw. 2000. Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL-trnF and rps4 sequences. Molecular Phylogenetics and Evolution 16(2): 180–198.

Huttunen, S., N. Bell, V. K. Bobrova, V. Buchbender, W. R. Buck, C. J. Cox, B. Goffinet, L. Hedenäs, B.-C. Ho, M. S. Ignatov, M. Krug, O. Kuznetsova, I. A. Milyutina, A. Newton, S. Olsson, L. Pokorny, J. A. Shaw, M. Stech, A. Troitsky, A. Vanderpoorten & D. Quandt. 2012. Disentangling knots of rapid evolution: origin and diversification of the moss order Hypnales. Journal of Bryology 34 (3): 187–211.

Stech, M., M. Sim-Sim, M. G. Esquível, S. Fontinha, R. Tangney, C. Lobo, R. Gabriel & D. Quandt. 2008. Explaining the ‘anomalous’ distribution of Echinodium (Bryopsida: Echinodiaceae): independent evolution in Macaronesia and Australasia. Organisms Diversity & Evolution 8 (4): 282–292.

Polypodies: In the Fernery of the Senses

Common polypody Polypodium vulgare, copyright Paul Montagne.

I'm not sure if I've ever had cause before to present my concept of the Evil Old Genus. The Evil Old Genus is one that has been used in the past to refer to a massively broader concept than it does currently, and so has been used to refer to many more species in the past than now. This makes dealing with the taxonomy of the genus a major headache, as one has to consider a whole host of now hidden or forgotten combinations. I can't say what would be the most evil of the Evil Old Genera out there, but a definite leader has to be the fern genus Polypodium. When the name was used by Linnaeus way back in the mid-1700s, Polypodium referred to nearly the whole gamut of ferns. Over time, as botanists have come to appreciate that all ferns are not the same, Polypodium has been progressively cut down. Still, it seems that if you go back into the taxonomy of nearly any fern, you'll come up against a 'Polypodium' sooner or later.

At present, Polypodium refers to a group of ferns with creeping, often scaly stems. It is the appearance of these stems that gives them their genus name, meaning 'many feet', as well as the common vernacular name of polypody. The circumscription of the genus can still vary somewhat between authors: some would include about 250 species in the genus, but Smith et al. (2006) restricted Polypodium to only about 30 species found primarily in temperate regions of the Northern Hemisphere, and in Central America. Many of these belong to what is known as the Polypodium vulgare complex. Recognised in the past as a single species Polypodium vulgare, this complex is now recognised as including a number of species found across Eurasia and North America. Ten of these are diploids, but another seven are polyploids. The polyploid species are believed to have originated from hybridisations between the diploid taxa; for instance, the Eurasian Polypodium vulgare sensu stricto is a tetraploid derived from a hybridisation between the diploid species P. glycyrrhiza and P. sibiricum (Sigel et al. 2014). Sigel et al. (2014), investigating the relationships between its diploid species, estimated an early Miocene origin for the P. vulgare complex. A fossil species from the early Oligocene, P. radonii, may belong to the complex or may be closely related (Kvaček 2001).

Appalachian rockcap fern Polypodium appalachianum, copyright Jaknouse.

Distinguishing species of the P. vulgare complex is no easy task, often requiring evaluation of subtle differences in leaf or stem form, or close examination of sporangium morphology. Another feature that has been used in distinguishing Polypodium species, however, is taste: the stems of some species in the complex have distinctive flavours. The Eurasian P. vulgare has been used to impart its bittersweet flavour to confectionary, while the vernacular name of the licorice fern P. glycyrrhiza of North America and eastern Asia is fairly self-explanatory (but like licorice, does it also give you a good run for your money?) The key to Polypodium species in the Flora of North America contains the somewhat unexpected advice that "the reader is cautioned to taste clean rhizomes from uncontaminated soils". And honestly, who could argue with that?

REFERENCES

Kvaček, Z. 2001. A new fossil species of Polypodium (Polypodiaceae) from the Oligocene of northern Bohemia (Czech Republic). Feddes Repertorium 112 (3-4): 159-177.

Sigel, E. M., M. D. Windham, C. H. Haufler & K. M. Pryer. 2014. Phylogeny, divergence time estimates, and phylogeography of the diploid species of the Polypodium vulgare complex (Polypodiaceae). Systematic Botany 39 (4): 1042-1055.

Smith, A. R., H.-P. Kreier, C. H. Haufler, T. A. Ranker & H. Schneider. 2006. Serpocaulon (Polypodiaceae), a new genus segregated from Polypodium. Taxon 55 (4): 919-930.

The Urbaum

Reconstruction of Archaeopteris, from Beck (1962).

It appears that it's been over a month now since I last posted anything at this site. I'm not going to go back and check, but I think this may be the longest hiatus that Catalogue of Organisms has been through since I first launched it nearly eight years ago. I have my excuses all prepared: it's been a busy period, what with trips back home to New Zealand, general job-hunting type stuff, and construction work around the house*. Nevertheless, I have had subjects lined up to present here all that time (nothing to do with construction, I promise you), and so I've found myself looking up material on Archaeopteris.

*An enterprise absolutely guaranteed to transform you into mind-breakingly tedious company for everyone else.

Archaeopteris, I hasten to explain, is nothing to do with Archaeopteryx, though certain parallels could be drawn (albeit with a long bow). Archaeopteryx, of course, is the Jurassic fossil genus that has become renowned as the Urvogel, the original bird. Archaeopteris is a much older fossil, coming from the Late Devonian. And if Archaeopteryx is to be known as the Urvogel, then Archaeopteris can claim to be the Urbaum, the original tree. It was not the earliest arborescent plant: the slightly earlier cladoxylopsid (a distant relative of modern ferns) Wattieza reached a height of at least eight metres (Stein et al. 2007). But Wattieza, with a single central trunk bearing a crown of fronds, would have been more similar to a modern tree fern or palm. Archaeopteris, with substantial side branches arising from its trunk, would have been more similar to the classic image of a modern tree.

Section of Archaeopteris branch, from Beck (1962). The globular structures are sporangia.

When it was first described, from its foliage alone, Archaeopteris was also believed to be an early fern. It wasn't until the early 1960s that fossils were described associating the fern-like foliage to large conifer-like logs that had been described from the same period. The entire tree was estimated to reach heights of at least sixty feet (about 18 metres) (Beck 1962). Archaeopteris was not a fern, but a member of the lineage leading to modern seed plants. As well as its overall habit, Archaeopteris resembled a modern tree in the presence of secondary thickening: a layer of cambium (generative cells) around the outer part of the trunk produced new phloem (nutrient-conducting cells) outside itself and new xylem (water-conducting cells) on the inside, thus allowing the trunk of the tree to expand as it grew (compare that to a tree fern, which gets no broader as it gets taller). However, as well as its fern-like foliage, Archaeopteris still resembled a more primitive plant in one very important regard: rather than producing seeds like a modern tree, it still reproduced through spores. Modified fronds produced clusters of sporangia, with at least some Archaeopteris species showing signs of the production of distinct male and female spore types. Whether these spores produced independent gametophytes in the manner of modern ferns is unknown, and likely to remain so: not only would such gametophytes probably be small and unlikely to be preserved, but they would have few if any features to associate them with the lofty trees.

Archaeopteris also exhibited a few other noteworthy differences from a modern tree. Most recent trees are more or less monopodial: they have a central main shoot from which branches arise laterally as adventitious primordia. Archaeopteris' main mode of growth was pseudomonopodial: instead of lateral branches arising de novo, they developed from the uneven division of the central shoot, with one part continuing upwards and the other part turning outwards. Though the end result would have looked broadly similar, there are some different functional implications. Archaeopteris' growth form may have been more constrained than most modern trees. Because branches were produced in the same spiral as leaves, there could have been a certain fractal-ness to Archaeopteris' appearance, with each major branch being something of a miniature of the tree as a whole (albeit a somewhat lopsided one, as at least some species produced larger leaves on the upper side of branches than on the lower side). Also, a purely pseudomonopodial mode of growth would not allow for the replacement of lost branches or other appendages: Trivett (1993) compared this model of the growth of Archaeopteris to "an inflating balloon or an opening umbrella with its increasingly empty interior". At the same time, she presented evidence that Archaeopteris could have produced a certain degree of adventitious growth, though it may still have been less resilient to damage than recent analogues. There is some circumstantial evidence that Archaeopteris may have sometimes shed leaves or minor branches en masse, though whether this was a seasonal occurrence or a response to stress is unknown.

Despite being potentially more vulnerable to damage than a modern tree, Archaeopteris was undeniably successful. Various species of the genus were found pretty much around the world, and were the dominant large plant wherever they were found until their extinction around the beginning of the Carboniferous. Perhaps resilience was simply less of an issue for Archaeopteris than for modern trees. After all, it lived in a world where there would have probably still been no major herbivores, and the main causes of appendage loss would have been the weather or disease. Also, long-term resilience may have simply not been so important for a tree that probably produced spores by the millions every year. Who knows how many Archaeopteris sporelings or gametophytes there may have been at a time, simply waiting their opportunity to provide a replacement for a fallen senior?

REFERENCES

Beck, C. B. 1962. Reconstructions of Archaeopteris, and further consideration of its phylogenetic position. American Journal of Botany 49 (4): 373-382.

Stein, W. E., F. Mannolini, L. V. Hernick, E. Landing & C. M. Berry. 2007. Giant cladoxylopsid trees resolve the enigma of the Earth's earliest forest stumps at Gilboa. Nature 446: 904-907.

Trivett, M. L. 1993. An architectural analysis of Archaeopteris, a fossil tree with pseudomonopodial and opportunistic adventitious growth. Botanical Journal of the Linnean Society 111: 301-329.

Aequitriradites: The Mark of the Cretaceous

Diagram of Aequitriradites ornatus, from Upshaw (1963).

The Cretaceous period is best known in popular culture as the time of Tyrannosaurus and Triceratops, of Pteranodon and Quetzalcoatlus, of Elasmosaurus and mosasaurs. But it was also, in an arguably even more significant way, the time of Aequitriradites.

Aequitriradites is the fossil represented in the diagram at the top of this post. It is not very large: at its largest, the species shown above is about a tenth of a millimetre across (Upshaw 1963). It is, in fact, the spore from a liverwort. The vegetative parts of liverworts mostly do not have much of a fossil record, being soft and prone to decay, though long-time readers may recall a suggestion that this spotty fossil record was occasionally dramatic (alas, general opinion seems to have not been swayed). However, their spores are more resistent, and hence may be abundant as fossils. Because it is rarely possible to tell exactly which plant they came from, fossil spores (and pollen) are classified as form taxa, parallel to the classification of other plant fossils. Aequitriradites species are characterised by a membranous flange (a zona) running around the outside of the spore, together with a triradiate laesura pattern (the fissures that mark where the spore opens when it germinates) on one face. Depending on the species, the laesurae may be well-marked or faint. There may also be an opening in the spore wall at the apex of the face opposite the laesurae (Cookson & Dettmann 1961). It has been suggested that the otherwise unidentified liverworts that produced Aequitriradites spores were probably related to the modern liverwort order Sphaerocarpales, and Archangelsky & Archangelsky (2005) compared Aequitriradites to the spores of the aquatic genus Riella.

Alternate faces of specimens of Aequitriradites plicatus, from Archangelsky & Archangelsky (2005).

The abundance of plant spores and pollen is such that they are commonly used as 'index fossils', indicators of the age of the rock they are found in. Aequitriradites contains various species throughout the Cretaceous period (species assigned to this genus from the Triassic seem to have since been re-classified). Li (2014) identified the appearance of Aequitriradites spinulosus in the very latest Jurassic as one of the better indicators of the start of the Cretaceous period in the Qinghai-Xizang Plateau in China. Aequitriradites species seem to have been most abundant in the Early Cretaceous, becoming rarer in the Late Cretaceous. Establishing the latest appearance of a spore taxon in the fossil record can be difficult, because of the possibility of re-working (fossil spores being disassociated from their original deposit and re-buried in a later one), but non-reworked examples of Aequitriradites in the latter part of the Late Cretaceous were alluded to by Askin (1990). TLDR: If you've got Aequitriradites, you've got Cretaceous.

REFERENCES

Archangelsky, S., & A. Archangelsky. 2005. Aequitriradites Delcourt & Sprumont y Couperisporites Pocock, esporas de hepáticas, en el Cretácico Temprano de Patagonia, Argentina. Rev. Mus. Argentino Cienc. Nat., n. s. 7 (2): 119-138.

Askin, R. A. 1990. Cryptogam spores from the Upper Campanian and Maastrichtian of Seymour Island, Antarctica. Micropaleontology 36 (2): 141-156.

Cookson, I. C., & M. E. Dettmann. 1961. Reappraisal of the Mesozoic microspore genus Aequitriradites. Palaeontology 4 (3): 425-427, pl. 52.

Li, J. 2014. Upper Jurassic and Lower Cretaceous palynological successions in the Qinghai-Xizang Plateau, China. In; Rocha, R., et al. (eds) STRATI 2013, pp. 1197-1202. Springer Geology.

Upshaw, C. F. 1963. Occurrence of Aequitriradites in the Upper Cretaceous of Wyoming. Micropaleontology 9 (4): 427-431.

Rock Mosses

Black rock-moss Andreaea rupestris, photographed by Sture Hermansson.

Upon first examining the picture above, you might think that you were looking at a patch of moss. Which would not be an unreasonable assumption to make, because that is exactly what you are looking at. But this is not just any moss, but perhaps one of the most interesting mosses out there.

The hundred or so species of the genus Andreaea, found in cooler regions around the world, are commonly known as rock mosses or granite mosses in reference to their preferred growth habitat on acidic rocks. They can often look black or red rather than green (presumably relative to how dry they are), and they are often brittle. Glime (2013) notes that a characteristic feature of granite mosses is that a hand brushed over one will come away with small fragments stuck to it, and suggests that this may act as a method of vegetative dispersal. Usually, granite mosses are autoicous: a single plant has both male and female reproductive structures, but they are borne in separate clusters. What makes Andreaea really interesting, though, is how it produces spores. As explained in the diagram I used in an earlier post, mosses produce spores from a sporophyte (diploid plant) that grows supported by the gametophyte (haploid plant) that comprises the green, vegetative stage of the moss life cycle. In most mosses, the sporophyte holds itself up by means of a long stalk called a seta, and spores are released from the terminal capsule by the ejection of a covering operculum.

Capsules of Andreaea, photographed by David Tng.

Andreaea does things differently. In this moss, the capsule is not supported by its own stalk, but is instead lifted up on an extension of the gametophyte called a pseudopodium. And instead of popping off an operculum, the Andreaea capsule splits open longitudinally into a squashed crown. Andreaea shows its difference after the spores are released as well: while the spores of other mosses germinate into a filamentous protonema (the moss 'seedling', as it were), the protonema of Andreaea bears thalloid appendages.

Such is the distinctive of Andreaea that it has been classified in a separate class from most other mosses, the Andreaeopsida. Phylogenetic analysis has demonstrated that Andreaea is one of the earliest diverging of all mosses, being the next to diverge from the main moss lineage after the Sphagnopsida (the group that includes Sphagnum). In some classifications, the class Andreaeopsida is restricted to Andreaea alone, but there are two other small genera that have been grouped with it in the past.

Andreaeobryum macrosporum, photographed by Masaki Shimamura.

Andreaeobryum macrosporum is a single unusual moss species found in north-west North America. Like Andreaea, it is found growing in rocks, though its preference is for basic rocks such as limestone. It also resembles Andreaea in having a spore capsule that opens through slits, though in the case of Andreaeobryum the apex of the capsule eventually wears off as well and the capsule splays fully open. The biggest difference between Andreaea and Andreaeobryum is that the capsule of the latter is not raised on a gametophytic pseudopodium, but possesses its own supporting seta like that of typical mosses (albeit a particularly short and stubby one). The phylogenetic position of Andreaeobryum remains uncertain: a molecular analysis by Chang & Graham (2011) recovered an Andreaea-Andreaeobryum clade, but with very low support.

Takakia lepidozioides, from here.

The real wild-card in basal moss phylogeny, however, is the little green monster known as Takakia. Takakia is a genus of two species found in western North America and eastern Asia. It was first discovered in the Himalayas and described in 1861—as a liverwort. This is a bit like being presented with a new species of snake, and describing it as a type of eel. But it has to be pointed out that Takakia possesses some very un-moss-like features. It has finely divided leaves, a feature common in liverworts but not known from any other moss. Its leaves contain oil bodies: again, unlike any other moss, but like many liverworts. Matters were not helped by the fact that Takakia was first described from vegetative material only, and it was not until the description of sporophytes in the 1990s that Takakia was conclusively accepted as a moss (Renzaglia et al. 1997).

Even so, its position within the mosses remained uncertain. A relationship with Andreaea has been suggested, as the capsule (though borne on a seta rather than a pseudopodium) opens through a single spiral slit. However, recent phylogenetic analyses have not supported a direct relationship between the two. Chang & Graham (2011) found in the analysis of their data that its position was vulnerable to the analytical model used: it could be placed as the sister taxon to all other mosses, or it could be the sister to the Sphagnopsida (with the two together being the basalmost moss clade). We have not heard the last of little Takakia.

REFERENCES

Chang, Y., & S. W. Graham. 2011. Inferring the higher order phylogeny of mosses (Bryophyta) and relatives using a large, multigene plastid data set. American Journal of Botany 98 (5): 839-849.

Glime, J. M. 2013. Bryophyta - Andreaeopsida, Andreaeobryopsida, Polytrichopsida. Chapt. 2-6. In: Glime, J. M. Bryophyte Ecology. Volume 1. Physiological Ecology. Ebook sponsored by Michigan Technological University and the International Association of Bryologists. Last updated 29 June 2013 and available at .

Renzaglia, K. S., K. D. McFarland & D. K. Smith. 1997. Anatomy and ultrastructure of the sporophyte of Takakia ceratophylla (Bryophyta). American Journal of Botany 84 (10): 1337-1350.

Pitchfork Mosses

Dicranum flagellare, photographed by Sue. The upright green stalks are the brood branches.

The subject of today's post is the cosmopolitan moss genus Dicranum, sometimes known as fork mosses or, apparently, wind-blown mosses. Dicranum species are characterised by elongate narrow leaves and an erect, often forked growth habit. In some habitats, Dicranum species may form reasonably extensive turfs. The genus name comes from the Greek word for a pitchfork and apparently refers to the teeth of the peristome (the ring of teeth around the opening of the spore capsule) though, if this is true, naming these mosses after a feature of the spore capsule may not necessarily have been the best idea. Many Dicranum populations produce sporophytes relatively rarely (a diagram of the moss life cycle was included in this post). Instead, these populations more commonly reproduce asexually through the production of vegetative propagules by the gametophyte. Once such species, the Holarctic Dicranum flagellare, produces terminal clusters of reduced branches, called 'brood branches'. If detached from the parent plant, these brood branches can grow into a new moss. A notable dispersal agent for brood branches, as it turns out, is slugs (Kimmerer & Young 1995). Brood branches break off the parent plant as the slug crawls past them, adhering to the slug by means of its slime. The trail of slime left by the slug also greatly improves the chance of a brood branch adhering to a suitable substrate once it becomes separated from its transport.


Dicranum scoparium, photographed by Li Zhang.

Because of the rarity of sporophytes, species of Dicranum are mostly distinguished by features of the leaves. Dicranum leaves may be straight or curved, the edge of the leaf may be smooth or toothed, and the blade of the leaf may be composed of one or two cell layers. Many species are characterised by the shape of the leaf in transverse section (Hedenäs & Bisang 2004). When sporophytes are produced, Dicranum species are dioicous: that is, they have separate male and female plants. However, in a number of species, the male plants are reduced in size and grow epiphytically on the leaves or rhizoids of the larger female plants. At least one species, Dicranum scoparium, has both dwarf and full-sized males (Hedenäs & Bisang 2004). Some Dicranum species have wide distributions, with a number found almost throughout Eurasia and North America, but others have more restricted distributions (D. transsylvanicum, for instance, is known from a single location in western Romania). Dicranum species are often very selective habitat-wise, with species differing in their choice of habitat, and they have been used as indicators of environmental conditions. This habitat selectivity can result in fragmented species distributions: for instance, Dicranum muehlenbeckii (which grows in dry, calcareous or mineral-rich environments) is found in central Europe, but is also known from a single locality in central Sweden. Dicranum scoparium, a more generalist species found in both humid and dry conditions, is widespread in Eurasia and North America, but is also known from New Zealand and a single region of Australia, near Mt Kosciuszko in New South Wales. As noted in a previous post, much ink has been spilled as regards the biogeographic processes underlying disjunct distributions in moss taxa. In that light, it should be pointed out that, while Australian and New Zealand specimens of Dicranum scoparium do tend to be less robust than the average Holarctic specimen, no molecular differences have yet been identified between the populations (Klazenga 2012).

REFERENCES

Hedenäs, L., & I. Bisang. 2004. Key to European Dicranum species. Herzogia 17: 179-197.

Kimmerer, R. W., & C. C. Young. 1995. The role of slugs in dispersal of the asexual propagules of Dicranum flagellare. The Bryologist 98 (1): 149-153.

Brachythecium salebrosum: Some Like It Temperate

Brachythecium salebrosum, photographed in Slovakia by M. Lüth.

Brachythecium salebrosum is a species of moss found in many temperate regions of the world. It often grows in drier habitats than other mosses; in a study of the effects of human disturbance on forest moss communities in Estonia, B. salebrosum made up slightly less than a tenth of the moss flora in unmanaged forests, but accounted for more than a quarter of the flora in managed forests (Vellak & Paal 1999). Brachythecium salebrosum is known from Eurasia, North America, southernmost Africa and Australasia. Interestingly, it hasn't yet been recorded from South America (Delgadillo 1993), and an explanation for its distribution would need to explain how it came to disperse (or vicariate) between North America and South Africa yet bypass South America and northern Africa. Another oddity in its distribution can be seen in comparison to the similar species Brachythecium rotaeanum: while both species are found in Eurasia and North America, B. salebrosum is more common in the western part of each continent while B. rotaeanum dominates in the east (so as one travels east from Europe, the distribution bands are salebrosum-rotaeanum-salebrosum-rotaeanum) (Ignatov et al. 2008). Some authors (particularly European ones) have expressed scepticism about the distinction between these two species, but they are distinguished by both morphological and molecular characters according to Ignatov et al. (2008).

Individual leaf of Brachythecium salebrosum, photographed by Russ Kleinman & Karen Blisard.

Distinguishing Brachythecium salebrosum from related species is, admittedly, not a simple task. Specimens of this species can vary quite significantly across their range. Generally, however, B. salebrosum has plicate leaves (i.e. they are folded longitudinally like an accordion) that are more or less falcate in shape with serrated margins. There is a clearly distinct group of small subquadrate cells at the lower corners of the leaf. The spore capsules are held more or less horizontally, and the seta supporting the capsule is generally about two centimetres high (Ignatov et al. 2008).

REFERENCES

Delgadillo M., C. 1993. The Neotropical-African moss disjunction. The Bryologist 96 (4): 604-615.

Ignatov, M. S., I. A. Milyutina & V. K. Bobrova. 2008. Problematic groups of Brachythecium and Eurhynchiastrum (Brachytheciaceae, Bryophyta) and taxonomic solutions suggested by nrITS sequences. Arctoa 17: 113-138.

Vellak, K., & J. Paal. 1999. Diversity of bryophyte vegetation in some forest types in Estonia: a comparison of old unmanaged and managed forests. Biodiversity and Conservation 8: 1595-1620.

Mosses Have a Place for Reproduction

A Rhizogonium photographed in the Philippines by Leonardo L. Co.

The Rhizogoniaceae are a family of mosses found in tropical and subtropical parts of the world, with a concentration of diversity in the Southern Hemisphere. Many species in the family are epiphytic; in particular, many show a preference for growing on the trunks of tree ferns (O'Brien 2007). The family has been defined by features such as sharply toothed, usually bistratose (i.e. with two cell layers) leaves and sporophytes located in the basal half of the erect stems, but molecular studies have indicated that the Rhizogoniaceae in the broad sense are para- or polyphyletic, and for this post I'll be using Rhizogoniaceae in a more restricted sense, corresponding to the 'clade C' of O'Brien (2007), including genera such as Rhizogonium, Cryptopodium, Calomnium, Goniobryum and Pyrrhobryum. One member of the Rhizogoniaceae, Pyrrhobryum dozyanum, is often used in moss gardens (it appears that there may also be a moss doing the rounds under this name in the European aquarium trade, though I haven't found anything to confirm whether this species, also being referred to as "Mayaca fern" or "Indonesiae bogoriensis", is actually P. dozyanum. Many bryophytes and other such plants in the aquarium trade have been misidentified, sometimes dramatically so).

View under microscope of leaf of Pyrrhobryum dozyanum, showing the toothed margins characteristic of Rhizogoniaceae. Image from here.

Most attention on Rhizogoniaceae from an evolutionary point of view has focused on what they might say about the relationship between acrocarpy and pleurocarpy. To explain what these terms mean, we'll start with the following diagram (from here):

Like other plants, mosses go through an alternation of generations, with both haploid and diploid multicellular stages. The haploid stage of the life cycle, the gametophyte, is the leafy green part of the moss. The gametophyte produces perichaetia, whorls of modified leaves within which the gamete-producing organs are contained. When a female gamete is fertilised, the resulting diploid zygote grows into the sporophyte, the brown thread-like structure you will often see growing out of a moss. The sporophyte produces haploid spores that will be dispersed to grow into new leafy gametophytes.

The diagram above shows an acrocarpous moss, in which the perichaetium is produced at the end of a growing branch of the gametophyte. Other mosses, however, are pleurocarpous, with perichaetia produced on the side of a branch. Whether a moss is acrocarpous or pleurocarpous is one of the first things a botanist will look at when attempting to identify it. However, many Rhizogoniaceae do not easily fall on either side of the acrocarpous/pleurocarpous distinction. They are what is called cladocarpous: the perichaetia are produced at the ends of small side-branches. However, lest any moss enthusiasts accuse me of overly simplifying things, I must point out that a great deal has been written on the exact distinctions between acrocarpous vs cladocarpous vs pleurocarpous. Like so many distinctions in nature, there are examples that blur the distinction between these states. As the perichaetia-bearing side-branches in a cladocarpous moss get progressively shorter, they become less and less distinguishable from pleurocarpy. In light of this, recent authors have suggested that the distinction between cladocarpy vs pleurocarpy should be defined by whether or not the side-branch bearing a perichaetium also bears normal vegetative leaves. If it only bears perichaetial leaves, then it is pleurocarpous: by this definition, some Rhizogoniaceae (including the genus Rhizogonium) are truly pleurocarpous (Bell & Newton 2007).

Goniobryum subbasilare, photographed by David Tng.

The vast majority of pleurocarpous mosses belong to a clade called the Hypnanae, which is massively speciose (probably about half of living mosses are hypnanaens). Because the hypnanaen mosses are so successful, there is a lot of interest in their relationships with other mosses. And as it turns out, the Rhizogoniaceae (with their combination of cladocarpous and pleurocarpous members) are closely related to the Hypnanae. Indeed, the Hypnanae are nested within the older, paraphyletic grade referred to the Rhizogoniaceae (O'Brien 2007). The acrocarpous state is the plesiomorphic one for mosses, with cladocarpy evolving in numerous lineages. Pleurocarpous mosses, it seems likely, have then evolved from cladocarpous ancestors, though either a number of times or with a number of reversals.

REFERENCES

Bell, N. E., & A. E. Newton. 2007. Pleurocarpy in the rhizogoniaceous grade. In: Newton, A. E., & R. S. Tangney (eds) Pleurocarpous Mosses: systematics and evolution pp. 41-64. CRC Press.

O'Brien, T. J. 2007. The phylogenetic distribution of pleurocarpous mosses: evidence from cpDNA sequences. In: Newton, A. E., & R. S. Tangney (eds) Pleurocarpous Mosses: systematics and evolution pp. 19-40. CRC Press.

From Tree Moss to Tree Ferns

Close-up of Davallia canariensis frond showing terminal sori. Photo from here.

Epiphytes seem to be the way to go here at CoO lately: after having covered a family of epiphytic mosses last week, I'm going to move on to a family of epiphytic ferns. The Davalliaceae are found in tropical and warm-temperate parts of the Old World. A few species are terrestrial but the majority are good old tree-huggers, either climbing up a suitable tree from roots attached to the ground or living entirely free of the tyranny of soil.

Habitus of Araiostegiella perdurans. Photo from here, where it is identified as 'Araiostegia' perdurans. Members of the previously recognised genus Araiostegia were redistributed by Kato & Tsutsumi (2008) between the genera Davallodes and Araiostegiella.

As a group, Davalliaceae are characterised by their elongate sori (spore-pouches) in marginal positions on the fronds at the junction of branching veins. The sori are covered by an indusium prior to maturity. Like other epiphytic ferns, the Davalliaceae also have creeping rhizomes covered by closely appressed scales. The most recent generic revision of the family recognises five genera (Kato & Tsutsumi 2008) but this aspect of Davalliaceae has always been unsettled. Phylogenetically, the Davalliaceae seem to belong in a clade that also includes the families Polypodiaceae and Grammitidaceae (Tsutsumi & Kato 2006). As these families are also primarily epiphytic, it seems likely that this lifestyle was ancestral for this clade. This would make the polypodioid-davallioid clade the largest assemblage of epiphytes among the ferns. It is also worth noting that these families probably diverged from each other some time in the early Tertiary (Schneider et al. 2004). Something that really does not get enough appreciation is that, despite the linear presentation of plant evolution that plagues most textbooks (bryophytes being replaced by ferns, which are shoved aside by conifers, that bow down before the all-conquering flowering plants), a significant percentage of the major fern lineages around today are actually much younger than the major flowering plant lineages.

Humata pectinata. Photo from here.

One final detail that's of patriotic interest to me: fossil Davalliaceae are known from the Miocene of New Zealand (Conran et al. 2010). These days Davalliaceae hang on in New Zealand by the skin of their rhizomes, with only a single species represented in the northernmost part of the country by asexually-reproducing individuals only (many fern species are able to survive by reproducing asexually in habitats where conditions do not permit sexual reproduction). This means that, along with coconuts, cone shells and crocodiles, Davalliaceae were part of a diverse biota that inhabited New Zealand during the balmy Miocene, only to decline and disappear as conditions became cooler.

REFERENCES

Conran, J. G., U. Kaulfuss, J. M. Bannister, D. C. Mildenhall & D. E. Lee. 2010. Davallia (Polypodiales: Davalliaceae) macrofossils from Early Miocene Otago (New Zealand) with in situ spores. Review of Palaeobotany and Palynology 162 (1): 84-94.

Kato, M., & C. Tsutsumi. 2008. Generic classification of Davalliaceae. Acta Phytotaxonomica et Geobotanica 59 (1): 1-19.

Schneider, H., E. Schuettpelz, K. M. Pryer, R. Cranfill, S. Magallón & R. Lupia. 2004. Ferns diversified in the shadow of angiosperms. Nature 428: 553-557.

Tsutsumi, C., & M. Kato. 2006. Evolution of epiphytes in Davalliaceae and related ferns. Botanical Journal of the Linnean Society 151 (4): 495-510.

The Trials and Tribulations of Tree Moss

Weymouthia cochlearifolia, photographed by Juan Larraín.

The Lembophyllaceae are a family of mosses found most abundantly in the Australasian region, though species are also found in other parts of the world such as Asia and South America. Most members of the family are epiphytic (growing on trees) or epilithic (growing on rocks). The composition of the family has varied significantly over the years, and as currently circumscribed the various Lembophyllaceae lack any reliable shared morphological characters and are united on the basis of molecular data (Olsson et al. 2009). Lembophyllaceae usually have concave leaves, loosely appressed to terete shoots, that lack a clearly differentiated leaf margin (Olsson et al. 2009).

Capsules of Isothecium alopecuroides, photographed by Hermann Schachner.

In the broader context, Lembophyllaceae are placed among the pleurocarpous mosses of the order Hypnales ('pleurocarpous' means that the reproductive structures are produced on small side branches rather than at the top of the main stalk), probably as the sister group to the bulk of the Neckeraceae (Olsson et al. 2009). Merget & Wolf (2010) reported finding Lembophyllaceae as polyphyletic but a closer look at the supplementary figures shows that only two of their four clades ('Lembophyllaceae III' and 'IV') actually correspond to the current concept of the family established by Quandt et al. (2009); the remainder represent genera removed to other families. More to the point, Merget & Wolf were using that most wretched of molecular methods, neighbour joining, and despite their use of a large number of source taxa it is difficult to accord their results much significance.

Spruce trees with a covering of Isothecium myosuroides in Olympic Natural Park, USA. Photo from here.

One genus of Lembophyllaceae, Weymouthia, contains two species found in Australia, New Zealand and South America. Such disjunct distributions have been the subject of much debate in moss biogeography. Some authors attribute them to a Gondwanan ancestry, indicating that the modern species must have arisen prior to the separation of these landmasses through continental drift. Others would see them as the result of post-separation dispersal. Supporters of the former explanation point to the supposed inability of moss spores to survive extended environmental exposure, and the correlation of numbers of shared species with age of geological separation rather than current distance (Blöcher & Frahm 2002; e.g. South America shares more species with New Zealand than southern Africa, despite being closer geographically to the former). Supporters of the latter point to the low levels of morphological and molecular differentiation between individuals from disjunct populations.

REFERENCES

Blöcher, R., & J.-P. Frahm. 2002. A comparison of the moss floras of Chile and New Zealand. Tropical Bryology 21: 81-92.

Merget, B., & M. Wolf. 2010. A molecular phylogeny of Hypnales (Bryophyta) inferred from ITS2 sequence-structure data. BMC Research Notes 3: 320.

Olsson, S., V. Buchbender, J. Enroth, S. Huttunen, L. Hedenäs & D. Quandt. 2009. Evolution of the Neckeraceae (Bryophyta): resolving the backbone phylogeny. Systematics and Biodiversity 7 (4): 419-432.

Quandt, D., S. Huttunen, R. Tangney & M. Stech. 2009. Back to the future? Molecules take us back to the 1925 classification of the Lembophyllaceae (Bryopsida). Systematic Botany 34 (3): 443-454.

Some Like It Cold (Taxon of the Week: Saccogynidium vasculosum)

I haven't introduced the Taxon of the Week post with a Name the Bug challenge this week because (a) even I'm not evil enough to make you try and identify liverworts, and (b) I haven't been able to find any illustrations of the specific liverwort concerned. The figures below from Gao et al. (2001) show other species in the same genus from China:



Leafy liverworts are small plants that are superficially similar in appearance to mosses. Like mosses, they grow in moist localities and lack well-developed supporting vascular tissue. Leafy liverworts can often be distinguished from mosses by having a different arrangement of leaves (liverwort leaves often grow in lateral rows, moss leaves in spirals), lacking a median vein in the leaf and potentially having teeth or lobes on the edge of the leaf. Liverworts also have different reproductive structures from mosses; instead of opening with a cap, liverwort spore capsules usually split down the sides.

Saccogynidium vasculosum is a species of liverwort restricted to the Falkland Islands and the very southernmost part of South America (Engel, 1990; Frey & Schaumann, 2002). Earlier authors referred to it as Lophocolea vasculosa but this was due to confusion with a different species, L. elata, from which it can be distinguished by the presence of small papillae (bumps) covering the leaves, a feature of the genus Saccogynidium (Engel, 1978). Saccogynidium is also distinguished from related genera by producing the female reproductive organs inside a fleshy protective covering called a marsupium (one is shown in the lower part of the figure above). Saccogynidium vasculosum is distinguished from other species in the genus by having finer papillae on the leaves, and having the tips of the leaves narrowly rounded rather than two-pointed.

Whar's really notable about Saccogynidium is its distribution (Schuster, 1972). As well as S. vasculosum, the Falkland Islands are home to S. australe, a species also found in New Zealand. Other species are found in Tasmania and south-east Asia. Interesting questions could be asked whether the current distribution of Saccogynidium is due to Gondwanan ancestry (in which case the disjoint distribution of S. australe might argue for incredibly slow rates of evolution) or to more recent dispersal, something some authors seem to have dismissed out of hand.

REFERENCES

Engel, J. J. 1978. A taxonomic and phytogeographic study of Brunswick Peninsula (Strait of Magellan) Hepaticae and Anthocerotae. Fieldiana: Botany 41.

Engel, J. J. 1990. Falkland Islands (Islas Malvinas) Hepaticae and Anthocerotophyta: a taxonomic and phytogeographic study. Fieldiana: Botany, new series 25.

Frey, W., & F. Schaumann. 2002. Records of rare southern South American bryophytes. Studies in austral temperate rain forest bryophytes 18. Nova Hedwigia 74 (3-4): 533-543.

Gao, C., T. Cao & M.-J. Lai. 2001. The genus Saccogynidium (Geocalycaceae, Hepaticae) in China. Bryologist 104 (1): 126-129.

Schuster, R. M. 1972. Continental movements, "Wallace's Line" and Indomalayan-Australasian dispersal of land plants: some eclectic concepts. Botanical Review 38 (1): 3-86.

Prototaxites: A Giant that Never Was?

Reconstruction of Prototaxites as columnar perrenial fungus from Hueber (2001), painted by Mary Parrish.

Nearly two years ago, I presented a post on Prototaxites, a mysterious fossil of the late Silurian, the earliest truly large terrestrial organism known from the fossil record. In that post (which I'd recommend reading before this one) I discussed the possibility that Prototaxites might have represented a giant fungus but a recent publication by Graham et al. (2010) presents a new alternative interpretation of Prototaxites. If they are correct, the Silurian may never be the same again.


Thalli of the liverwort Marchantia. Photo from here.

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?


The largest known Prototaxites fossil (at least as of 2001), photographed by Charles Meissner in Saudi Arabia. From Hueber (2001).

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. (2010) 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.


Reconstruction by Kandis Elliot of Silurian liverwort mats being rolled by wind, gravity and/or water movement to form 'Prototaxites'. From Graham et al. (2010).

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. (2010) 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.

REFERENCES

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.

Graham, L. E., M. E. Cook, D. T. Hanson, K. B. Pigg & J. M. Graham. 2010. 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., 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.

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.

Mosses: Not as Simple as You Think (Taxon of the Week: Ectropothecium)

Ectropothecium sandwichense, a moss species with a scattered, mostly tropical distribution on islands in the South Pacific. Photo from here.

I have to admit to becoming increasingly glad that I don't work on mosses. The new Taxon of the Week is a moss, and looking up stuff on it has driven me into a strange world of unfamiliar terminology and fine-scale features. If I mess anything up here, I only hope that the legions of moss fans out there* forgive my transgressions.

*Do not doubt that they're out there. As I've commented before, bryologists are a dedicated bunch.

Ectropothecium is a genus of mostly hydrophytic mosses found worldwide (hydrophytic plants grow either in water or in completely waterlogged soil; some Ectropothecium species do the former, others the latter). It belongs to a clade of mosses known as the pleurocarpous mosses; while other (acrocarpous) mosses branch only rarely and produce terminal archegonia (the female reproductive organs - see the diagram at the posts linked to above) at the end of the stem, pleurocarpous mosses produce lateral archegonia on highly branched and extensively interwoven stems (Shaw & Renzaglia, 2004). Pleurocarpous mosses are divided molecularly into three orders, Ptychomniales, Hookeriales and Hypnales; Ectropothecium belongs to the Hypnales which have a smooth spore capsule with a calyptra (protective cap) that usually opens by splitting along one side (Buck et al., 2004). Within the Hypnales, Ectropothecium is placed in the family Hypnaceae; however, phylogenetic studies of Hypnales (e.g. De Luna et al., 2000) suggest that members of the Hypnaceae may be para- or polyphyletically placed within the order.


Ectropothecium zollingeri, a species with a distribution centred in south-east Asia. Photo from here.

Ectropothecium itself is distinguished by having spore capsules that are very small (usually less than 1 mm long) and almost spherical (Buck & Tan, 2008), non-decurrent leaves (not extending down the stem where they join), short and broad leaf cells and filamentous pseudoparaphyllia that are two or three cells wide at the base (Ireland, 1992). Pseudoparaphyllia are small outgrowths of the stem that cluster around the base of new side-branches (as opposed to paraphyllia which are normally scattered more evenly along the entire stem); they may be thread- or blade-shaped. See Ignatov & Hedenäs (2007) for a review of the distinctions between paraphyllia, pseudoparaphyllia and proximal branch leaves, though to be honest if you understand the difference you're somewhat ahead of me (as far as I can tell, pseudoparaphyllia grow on the stem around the primordium of a new branch and remain on the stem, while proximal branch leaves may start growing around the primordium but end up being transferred to the new branch).

REFERENCES

Buck, W. R., C. J. Cox, A. J. Shaw & B. Goffinet. 2004. Ordinal relationships of pleurocarpous mosses, with special emphasis on the Hookeriales. Systematics and Biodiversity 2 (2): 121-145.

Buck, W. R., & B. C. Tan. 2008. A review of Elmeriobryum (Hypnaceae). Telopea 12 (2): 251-256.

De Luna, E., W. R. Buck, H. Akiyama, T. Arikawa, H. Tsubota, D. González, A. E. Newton & A. J. Shaw. 2000. Ordinal phylogeny within the hypnobryalean pleurocarpous mosses inferred from cladistic analyses of three chloroplast DNA sequence data sets: trnL-F, rps4, and rbcL. Bryologist 103 (2): 242-256.

Ignatov, M. S., & L. Hedenäs. 2007. Homologies of stem structures in pleurocarpous mosses, especially of pseudoparaphyllia and similar structures. In Pleurocarpous Mosses: systematics and evolution (A. E. Newton & R. Tangney, eds) pp. 227-245. The Systematics Association Special Volume Series 71. Taylor& Francis / CRC Press: Boca Raton.

Ireland, R. R. 1992. Studies of the genus Plagiothecium in Australasia. Bryologist 95 (2): 221-224.

Shaw, J., & K. Renzaglia. 2004. Phylogeny and diversification of bryophytes. American Journal of Botany 91 (10): 1557-1581.

It's Not What You Think

A little less than a year ago, I mentioned the strange and extremely cool phenomenon of independent gametophytes in ferns - cases where the tiny haploid gametophyte generation of a fern is able to reproduce asexually and hang around as a plant that, to the untrained eye, wouldn't look much like a fern at all. In that post, I said that independent gametophytes were known for "a single species of Grammitidaceae, two Vittariaceae and nine Hymenophyllaceae". A paper just out in Plant Systematics and Evolution (Li et al., 2009) identifies another independent gametophyte - and this is the most mind-blowing of all. Not only does it come from a family for which independent gametophytes have not previously been recorded, but it turns out to have been hiding in very plain view.


This is it! (Photo from here.)

Süßwassertang (or "suesswassertang") is a plant that people in Europe and North America have been growing in their aquaria for a few years now (the name is German for "freshwater seaweed"). Specimens are propagated vegetatively by simply breaking them apart. I haven't been able to find out exactly where it originally came from - internet fora refer to a probable source from a German botanic garden, but it seems that specimens have mostly been passed around by private individuals (see this discussion, for instance). The original assumption seems to have been that it was some sort of liverwort, like a similar-looking aquarium plant known as Monosolenium tenerum or Pellia* (in fact, Süßwassertang has also been referred to as "round pellia", in reference to its different growth habit from true pellia). However, rarely produced gametangia (reproductive organs) suggested that it may be a fern gametophyte instead, and this has been confirmed by Li et al. through molecular analysis.

*It originally appeared on the market as Pellia, but has since been re-designated Monosolenium tenerum (see here). The Wikipedia page on Monosolenium suggests that this may also be wrong, but doesn't give any sources for this claim. Liverworts are far from easy to identify, so it's not outside the realms of possibility.

Süßwassertang turns out to be very closely related to Lomariopsis lineata in the Lomariopsidaceae, which looks like this (photo by Julie Barcelona):



Lomariopsis lineata is an Asian species of the pantropical epiphytic fern genus Lomariopsis, members of which can climb up trees on long running stems to heights of ten metres (Rouhan et al., 2007). That an arboreal fern could produce an independent gametophyte is surprising - that such a gametophyte should be aquatic is incredible. A number of websites have already started referring to Süßwassertang as Lomariopsis lineata, but this is jumping the gun a little. To date, no Süßwassertang specimens have been successfully induced to produce sporophytes, despite their occassional production of gametangia (normally in ferns, gametophytes produce male and female gametangia, the gametes from which fertilise each other and grow into sporophytes). Even when Süßwassertang were transplanted into terrestrial conditions, no sporophytes were produced though gametangia production increased (on the other hand, their growth was much reduced). Süßwassertang has so far only been demonstrated to be extremely close to L. lineata, not necessarily identical with it.

As alluded to in the previous post, independent gametophytes may be able to survive in conditions which their relevant sporophytes would find intolerable. The Süßwassertang would seem to be one of the ultimate examples.

REFERENCES

Li, F.-W., B. C. Tan, V. Buchbender, R. C. Moran, G. Rouhan, C.-N. Wang & D. Quandt. 2009. Identifying a mysterious aquatic fern gametophyte. Plant Systematics and Evolution 281 (1): 77-86.

Rouhan, G., J. G. Hanks, D. McClelland & R. C. Moran. 2007. Preliminary phylogenetic analysis of the fern genus Lomariopsis (Lomariopsidaceae). Brittonia 59 (2): 115-128.