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.

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.

Before the Word for World was Forest

...though to be perfectly honest, I've never read The Word for World is Forest, I just thought that it'd supply a catchy name for this post.


The environment of the Devonian Rhynie Chert, as illustrated by Zdenek Burian (via Palaeos.com.

If you want to find out about the evolution of terrestrial life for vertebrates, there are countless sources out there for you to turn to. But if you want to find out about the evolution of terrestrial life for plants, then your options are probably much thinner. Which is just one more example of how screwed up our priorities as humans are, because there's no doubt which is the greater achievement. When the first terrestrial vertebrates emerged, they found a world already made lush by a covering of vegetation. But the first terrestrial plants would have found nothing waiting for them but bare, hostile rock*. It's amazing that they ever managed at all.

*To be honest, I lie slightly. In places where there was available moisture, I'm sure that a film of bacteria would have grown. Ditto for unicellular algae and other such organisms. If lichen-type associations were around at the time (and a cyanobacteria-zygomycete association is preserved in the Rhynie Chert - Selosse & Le Tacon, 1998), the world would have been their mollusc. Sadly, with little potential for their fossilisation and discovery, we may never really know about the contributions of these first unicellular pioneers.


Reconstruction of the trimerophyte Psilophyton, from here.

But manage they did, and by the early Devonian the world was home to a small but respectable diversity of land plants. Most of the vascular plants of the time have been divided between the rhyniophytes, lycophytes, trimerophytes and cladoxylopsids (doubtless there were also moss- and liverwort-like plants around too, if not actual mosses and liverworts, but the spotty fossil record of bryophyte-grade plants doesn't quite reach that far back). Almost all of them, admittedly, would have been fairly similar to the non-expert eye - small, shrubby affairs with simple branching systems and no true leaves or roots. Examination of their fine structure (particularly of their vascular systems) is necessary to recognise their true affinities - rhyniophytes in the stem lineage for all vascular plants; lycophytes including the ancestors of modern Lycopodium, Selaginella and Isoetes; trimerophytes on the stem leading to modern ferns and seed plants; and cladoxylopsids on the stem of modern ferns*. Each of these groups quite possibly represents a grade rather than a clade, but in most cases it is not possible to actually demonstrate this one way or another.

*It is worth noting (especially in relation to a question asked in the comments to a previous post) that the vascular cells of rhyniophytes, lycophytes and trimerophytes each have distinct morphologies from each other** (Friedman & Cook, 2000), and this has led some authors to suggest that the vascular system may have developed independently in each of the three lineages. For now, though, it seems more parsimonious to assume a common origin followed by evolutionary divergence.

**It is also worth noting that when Friedman & Cook (2000) wrote their review, we actually knew more about the structure of the vascular cells in Devonian lycophytes and trimerophytes than in living lycophytes and ferns. Previous studies of vascular cell structure in living plants had almost exclusively looked at seed plants alone.

Trimerophytes differed from the more basal rhyniophytes in their mode of branching - whereas the basalmost land plants had branched dichotomously (dividing into two branches with each branch growing equivalently), trimerophytes branched anisotomously (one branch growing more than the other), effectively giving the trimerophytes some degree of a central stem (this process is called overtopping). Secondary branches from the central stem still branched dichotomously. Sporangia were borne on the tips of the branches, and at least some trimerophytes grew elongate sporangia in pairs that twisted around each other (Gerrienne, 1997).

One particular trimerophyte, Psilophyton princeps, holds a particular significance for palaeobotany as the first Devonian plant to be reconstructed, by William Dawson in 1859 (Taylor & Krings, 2008), with a large creeping rhizome extending successive upright shoots. But perhaps even more significant was the size reached by some trimerophytes. While most Devonian vascular plants would have been struggling to reach half a metre in height, the trimerophyte Pertica dalhousii has been estimated to have reached up to three metres (Mauseth, 2008) - about the height of the ceiling of an average house (the related but smaller species Pertica quadrifaria is shown to the left, in a reconstruction from the Maine Geological Survey). Together with the similarly-sized cladoxylopsid Pseudosporochnus, these were effectively the first trees - not much compared to their modern successors, perhaps, but very impressive compared to anything that came before them (with the exception, of course, of the primordial oddity Prototaxites). It is interesting to imagine what the environment of these early "forests" would have been like. How did they handle the weather, for a start? In the absence of a strong root system to anchor them down, were they prone to collapsing in the wind? If this was so, did they grow rapidly to compensate for their short lives, or did the rhizome readily send up new shoots to replace lost ones? (Remember, with no leaves either, the entire stem would have probably been photosynthetic.) How did this affect life for the early terrestrial animals taking advantage of their presence? There may have been the beginnings of a forest, but a world recognisably our own was still a long way off.

REFERENCES

Friedman, W. E., & M. E. Cook. 2000. The origin and early evolution of tracheids in vascular plants: integration of palaeobotanical and neobotanical data. Philosophical Transactions of the Royal Society of London Series B 355: 857-868.

Gerrienne, P. 1997. The fossil plants from the Lower Devonian of Marchin (northern margin of Dinant Synclinorium, Belgium): V. Psilophyton genseliae sp. nov., with hypotheses on the origin of Trimerophytina. Review of Palaeobotany and Palynology 98: 303-324.

Mauseth, J. D. 2008. Botany, 4th ed. Jones & Bartlett Publishers.

Selosse, M.-A., & F. Le Tacon. 1998. The land flora: a phototroph-fungus partnership? Trends in Ecology and Evolution 13 (1): 15-20.

Taylor, E. L., & M. Krings. 2008. Paleobotany, 2nd ed. Academic Press.

Southern Moss (Taxon of the Week: Ptychomitrium muelleri)

There don't seem to be any images of Ptychomitrium muelleri available online, so here's another Ptychomitrium species, P. gardneri from China. Photo by Li Zhang.

Mosses are often treated as the poor relation in plant diversity. Popular presentations of plant evolution often tend to have even more of a Scala Natura-esque slant to them than presentations of animal evolution, and so mosses and other non-vascular plants get glossed over as mere stepping stones to their more upright "descendants", if they even warrant a mention at all. This is, of course, complete rubbish - mosses have a very respectable diversity of species (about 10,000, according to Tree of Life). I've met a few moss researchers over the years, and a more devoted following a taxon could not hope for.

Ptychomitrium muelleri is a haplolepidous moss of the family Ptychomitriaceae (I'll explain what that means in a minute). It grows to a maximum height of one and a half centimetres, and if the type specimens are any indication, prefers to grow on rocks. Ptychomitrium mosses seem to be found more or less worldwide, but Ptychomitrium muelleri itself is found in south-eastern Australia, New Caledonia, southern South America and southernmost Africa. What is interesting about this species' distriution is that it was thought to be endemic to Australia until very recently when Cao et al. (2001) established that species described from each of the other localities were conspecific with P. muelleri. As a result, P. muelleri has what might be described as a classic "Gondwanan" distribution, but I rather doubt that Gondwana had anything to do with it. After all, moss spores are very light and extremely easily dispersed, and surely it is no coincidence that all the localities where P. muelleri can be found lie roughly along the same wind belt.



The diagram of a moss life cycle above has been stole from Palaeos.com. For the nonce, the important details are these - mosses, like other plants, are multicellular at both the haploid and diploid stages of the life cycle, but unlike vascular plants, the larger, dominant stage of the life cycle is the haploid gametophyte. When a female gametophyte is fertilised, the diploid sporophyte remains attached to the gametophyte and grows a spore-filled capsule that eventually breaks open (after the loss of the protective calyptra) to release the spores. Around the mouth of the capsule is a ring of "teeth", the peristome. In basal mosses, the peristome is made up of entire cells, but in the class Bryopsida, the arthrodontous mosses (which includes the larger part of the mosses), the teeth are reduced to cell wall remnants. Most of the bryopsid lineages have two rows of teeth in the peristome, an outer and an inner, but Ptychomitrium belongs to a group called the Haplolepideae or Dicranidae which have only the inner row of teeth. The haplolepidous mosses form a monophyletic clade within the Bryopsida.


Ptychomitrium polyphyllum from Scotland, showing the calyptra on the left capsule and the exposed peristome on the right. Photo from here.

Most of the features separating moss taxa are microscopic and relate to such things as cell arrangement (which is my weaselly method of saying that I don't understand a word of them), but Ptychomitrium is distinguished by having a mitrate calyptra (and those unsure what "mitrate" means might want to look at the Taxon of the Week post of two weeks ago) with characteristic lobes around the lower edge (Hernández-Maqueda et al., 2008, compare it to a Hawaiian skirt). Ptychomitrium muelleri has (amongst other features) lingulate (tongue-shaped, I'm guessing) leaves with smooth margins, and ovoid capsules.

REFERENCES

Cao, T., S. Guo & Y. Zhang. 2001. Distribution of Ptychomitrium muelleri (Bryopsida), with its synonyms. The Bryologist 104 (4): 522-526.

Hernández-Maqueda, R., D. Quandt, O. Werner & J. Muñoz. 2008. Phylogeny and classification of the Grimmiaceae/Ptychomitriaceae complex (Bryophyta) inferred from cpDNA. Molecular Phylogenetics and Evolution 46 (3): 863-877.

Focus on a Fern (Taxon of the Week: Polystichum vestitum)

The New Zealand fern Polystichum vestitum. Photograph by Alan Liefting.

For only the second time, the Taxon of the Week is going to be a single species. But while my earlier attempt at writing a Taxon of the Week post was hampered somewhat by a shortage of information about the species concerned, I'm happy to say that's not so much of a problem this time. And I'm also happy to say that for this post, I'm going home.

Polystichum vestitum (Forst.) Presl 1836, the prickly shield fern, is one of New Zealand's most abundant fern species. It's found in almost every corner of the country, including the Chatham and subantarctic islands, and even reaches as far south as Macquarie Island*. It is, however, restricted to the New Zealand biogeographic region - references in early sources to its presence in South America seem to represent confusion with Polystichum chilense (Looser, 1948). Polystichum vestitum is able to handle a greater deal of direct sun than other forest ferns, and is able to persist in cleared areas (Olsen, 2007). Mature specimens are about a metre in height and have a semi-tree fern growth habit, with a short trunk formed by the upright rhizome. Polystichum species are known as "shield ferns" because the stipes of the leaves are covered with glossy scales.

*Macquarie Island represents a obscure but interesting piece of the Great Trans-Tasman Rivalry. A small, windswept island halfway to Antarctica, almost untroubled by humans since the declines of sealing and whaling removed pretty much every reason why anyone would ever want to go there, Macquarie is biogeographically related to other subantarctic islands belonging to New Zealand, but is itself owned by Australia (in fact, it's technically part of the state of Tasmania, making Tasmania the third-longest Australian state north to south after Western Australian and Queensland). As a result, it's often covered in natural history works (such as bird field guides) for both countries. Despite having no trees, Macquarie Island is also notable for having been home to the world's southern-most parrot species, the parakeet Cyanoramphus erythrotis, until the effects of introduced animals caused their sudden decline and extinction in the late 1800s (according to Taylor, 1979, they survived dogs, they survived cats, but they were eventually undone by the rabbits**).

**The arrival of rabbits meant that the island was able to support higher populations of cats and also-introduced weka than it had previously, increasing the amount of predation by those species on parakeets beyond what the parakeet population could handle.


Another shot of Polystichum vestitum from NZ Plant Pics.

The scales of Polystichum vestitum are quite variable, and some authors have suggested that more than one species might be concealed under this name. Specimens found on the main islands of New Zealand have teardrop-shaped scales with broad bases and smooth edges, and with a glossy dark brown central region surrounded by a light brown margin. In many specimens from the Chatham and subantarctic islands, the scales become much longer, with a long trailing tip to the teardrop, and the dark brown centre disappears to leave an entirely light brown scale. In many Chatham Island specimens, the scales also develop notable marginal projections. However, these divergent morphologies are not universal in the outlying populations - instead, the populations vary from specimens with fully divergent morphologies to ones almost indistinguishable from mainland individuals. Analysis of the variation within Polystichum vestitum by Perrie et al. (2003b) failed to find clear divisions between the variants. When the variants were analysed using AFLP*** data, the fully divergent specimens from the Chatham Islands did cluster together, but with only low support, while the remaining specimens (including less divergent Chatham Island specimens) did not. Perrie et al. therefore recommended against recognising the divergent specimens as a distinct species or variety. However, it is remarkable that the level of variation in the small area of the Chatham Islands should be greater than that seen through mainland New Zealand. Perhaps an early population of P. vestitum became established on the Chathams and was partway into evolving into a new species but a second wave of colonisation from the mainland slowed things down? Multiple colonisations of the Chathams from the mainland have been demonstrated for another fern species, Asplenium hookerianum (Shepherd et al., 2009).

***Amplified Fragment Length Polymorphism - a method of observing variation in the sizes of the fragments that extracted DNA is chopped into by restriction enzymes. AFLP data is arguably a much rougher means of molecular analysis than full sequence comparison, but it has the distinct advantages of being much quicker and having a fraction of the cost, and hence also allowing comparison of a greater number of genes/alleles and individuals than would often be feasible with full sequencing.


The underside of a Polystichum vestitum leaf, showing the bicoloured scales. Photo by Larry Jensen.

In fact, the whole question of fern dispersal is an interesting one - as in, how much of it goes on? Ferns, of course, reproduce by means of spores which, being very small and light, could easily be carried long distances - perhaps even across oceans. It has therefore been suggested that distance has not been a major barrier in fern evolution. Brownsey (2001) suggested that most New Zealand ferns were derived from recent and common dispersals between Australia and New Zealand. In contrast, an AFLP analysis of Polystichum by Perrie et al. (2003a) found that the New Zealand species clustered in a clade, suggesting that they could possibly be derived from a single dispersal event. Interestingly, the closest relatives of the New Zealand clade were species from Lord Howe Island, which is positioned between Australia and New Zealand. Perrie et al. (2003a) also found specimens of another New Zealand species, Polystichum silvaticum, clustered together but were nested within specimens of Polystichum vestitum. This is in contrast to the results of Perrie et al. (2003b), which found a large distance between data from P. vestitum and P. silvaticum (but without data from other Polystichum species to provide a root). P. silvaticum shares the character of bicoloured scales with P. vestitum, but differs from it (and other Polystichum species) in lacking an indusium, a membrane that covers and protects young developing spores. Is it possible that P. silvaticum represents a derivative of P. vestitum?

And as a final aside, let me return to those subantarctic populations of Polystichum vestitum. On the Snares Islands, clumps of P. vestitum are apparently the preferred cover for nests of the Snares Island snipe, Coenocorypha huegeli (Miskelly, 1999). Why, you may ask, do snipes prefer to nest under ferns? As it turns out, birds on the Snares that nest higher up apparently lose a lot of eggs or chicks to petrels. Petrels don't eat the other birds, but they also nest under cover in the area - and petrels are notoriously bad at making landings. Touchdown for a petrel seems to basically involve throwing itself at the ground and hoping that there is enough vegetation to cushion its descent. Any nest in the way of a plummeting petrel is turned into kindling. In this situation, a nice sturdy fern is a ground-nesting birds friend, catching the petrels before they scramble your eggs.

REFERENCES

Brownsey, P. J. 2001. New Zealand's pteridophyte flora — plants of ancient lineage but recent arrival? Brittonia 53 (2): 284-303.

Looser, G. 1948. The ferns of southern Chile (conclusion). American Fern Journal 38 (3): 71-87.

Miskelly, C. M. 1999. Breeding ecology of Snares Island Snipe (Coenocorypha aucklandica huegeli) and Chatham Island Snipe (C. pusilla). Notornis 46: 207-221.

Olsen, S. 2007. Encyclopedia of Garden Ferns. Timber Press.

Perrie, L. R., P. J. Brownsey, P. J. Lockhart, E. A. Brown & M. F. Large. 2003a. Biogeography of temperate Australasian Polystichum ferns as inferred from chloroplast sequence and AFLP. Journal of Biogeography 30 (11): 1729-1736.

Perrie, L. R., P. J. Brownsey, P. J. Lockhart & M. F. Large. 2003b. Morphological and genetic diversity in the New Zealand fern Polystichum vestitum (Dryopteridaceae), with special reference to the Chatham Islands. New Zealand Journal of Botany 41: 581-602.

Shepherd, L. D., P. J. de Lange & L. R. Perrie (in press, 2009). Multiple colonizations of a remote oceanic archipelago by one species: how common is long-distance dispersal? Journal of Biogeography.

Taylor, R. H. 1979. How the Macquarie Island parakeet became extinct. New Zealand Journal of Ecology 2: 42-45.