Cliff Ferns

Historically, the higher classification of ferns has tended to be a bit wobbly. Compared to flowering plants, ferns often offer fewer readily observable features that may offer clues to relationships. As a result, the position of many fern taxa has long been uncertain. One such group is the cliff ferns of the genus Woodsia.

Woodsia scopulina, copyright Jim Morefield.

Cliff ferns, as their name suggests, are commonly found growing on rocks. There are a few dozen species, mostly found in cooler regions of the Northern Hemisphere. A single species, Woodsia montevidensis, extends into South America and southern Africa (Rothfels et al. 2012). They have short creeping rhizomes with a covering of scales and leaves bearing a mixture of scales and hairs. The most distinctive feature of the cliff ferns can only be seen on fertile fronds: the sori (spore packets) are covered by an indusium that is attached to the leaf basally relative to the sori. These indusia are commonly composed of an array of scales or filamentous sections, in contrast to the solid indusia of other ferns.

Underside of pinnule of Woodsia plummerae, showing the filamentous indusia, from here.

Historically, Woodsia has been placed in a family Woodsia with a number of superficially similar fern genera such as the bladder ferns of the genus Cystopteris. However, molecular phylogenetic analyses have disputed the monophyly of such a group. Rothfels et al. (2012) divided the 'woodsioid' ferns between no less than six different families with Woodsiaceae in the strict sense limited to the cliff ferns alone. Though some authors have divided the cliff ferns between multiple genera, an analysis of the group by Shao et al. (2015) found it difficult to reliably distinguish such subgroups and recommended recognition of only a single genus. They did, however, recognise three major clades within Woodsia identified by molecular phylogenetic analysis as distinct subgenera. The type subgenus Woodsia is distinctive among ferns in possessing articulated stems; species of this subgenus are widespread in the Palaearctic region. The subgenus Physematium is mostly found in the Americas and is characterised by bicolored scales on the rhizome. The third subgenus, Cheilanthopsis, is found in eastern Asia with the centre of diversity in the Himalayan region. The rhizome scales are concolorous, and the indusia are solid and globose rather than being composed of individual segments. In some cases in this subgenus, the sori are covered by 'false indusia', indusium-like structures that are formed from inrolled leaf margins rather than being independent membranes.

REFERENCES

Rothfels, C. J., M. A. Sundue, L.-Y. Kuo, A. Larsson, M. Kato, E. Schuettpelz & K. M. Pryer. 2012. A revised family-level classification for eupolypod II ferns (Polypodiidae: Polypodiales). Taxon 61 (3): 515–533.

Shao, Y., R. Wei, X. Zhang & Q. Xiang. 2015. Molecular phylogeny of the cliff ferns (Woodsiaceae: Polypodiales) with a proposed infrageneric classification. PLoS One 10 (9): e0136318.

Matoniaceae: Ferns with a Heritage

Ferns are one of those groups of organisms, like sharks and cockroaches, that are not really as ancient as most people imagine. For all that ferns are indelibly associated in the public conscience with antediluvian imagery of steamy coal swamps and great lumbering reptiles, the dominant fern groups that can be seen today did not arise until the Cretaceous and diversified as part of a flora that would have been largely modern in appearance (Schneider et al. 2004). Nevertheless, there are some fern lineages around today that might be said to have a genuine claim to a more venerable pedigree. One such group is the Matoniaceae.

Matonia pectinata, copyright Ahmad Fuad Morad.

In the modern flora, the Matoniaceae are a small family, including only three or four species in two genera, Matonia and Phanerosorus, found in south-east Asia (Lindsay et al. 2003). The two genera are distinct in appearance and habits. Matonia is found on more or less exposed montane summits and ridges and has pedate fronds with pectinate pinnae radiating from an erect central stipe that may grow well over a metre in height. Phanerosorus is found on vertical limestone walls and has pendulous, branching fronds whose pinnae are simple or more weakly pectinate (Kato & Setoguchi 1999). Both genera have the fronds arising from a long, hairy, creeping rhizome. Lateral veins in the pinnules show one or more bifurcations and in Matonia these branching forks may anastomose with each other to form a reticulate vein pattern. The genera also share features of the reproductive anatomy such as massive, deciduous sporangia.

Phanerosorus major, copyright Wally Suarez.

The fossil record of Matoniaceae indicates that they were far more widespread in the past; indeed, Matonia was illustrated from preserved compression fossils before it was described as a living genus (Klavins et al. 2004). Leaf fossils of Matoniaceae go back to the Late Triassic, and the Middle Triassic stem taxon Soloropteris rupex has been more tentatively assigned to the family (van Konijnenburg-van Cittert 1993). Fossil forms are more similar to Matonia in overall appearance and this is presumed to be the plesiomorphic morphology for the family. A certain resemblance exists between Phanerosorus and younger fronds of Matonia and it seems likely that the former genus evolved from Matonia-like forms by a process of paedomorphosis (Kato & Setoguchi 1998). The family was most widespread during the Jurassic and Early Cretaceous but became extinct in temperate regions of the Northern Hemisphere during the Late Cretaceous. It persisted longer in the Southern Hemisphere, with the stem taxon Heweria kempii known from the Early Tertiary of Australia, but at some point following that it became restricted to its modern localised range.

REFERENCES

Kato, M., & H. Setoguchi. 1999. An rbcL-based phylogeny and heteroblastic leaf morphology of Matoniaceae. Systematic Botany 23 (4): 391–400.

Klavins, S. D., T. N. Taylor & E. L. Taylor. 2004. Matoniaceous ferns (Gleicheniales) from the Middle Triassic of Antactica. Journal of Paleontology 78 (1): 211-217.

Konijnenburg-van Cittert, J. H. A. van. 1993. A review of the Matoniaceae based on in situ spores. Review of Palaeobotany and Palynology 78: 235–267.

Lindsay, S., S. Suddee, D. J. Middleton & R. Pooma. 2003. Matoniaceae (Pteridophyta)—a new family record for Thailand. Thai Forestry Bulletin 31: 47–52.

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.

The Dicranophyllales: An Early Branch of the Conifers?

Reconstruction of Dicranophyllum hallei, from here.

Popular works on the fossil record tend to give us a very uniform picture of the Carboniferous period. A watery swamp can be seen covering the landscape, from which large amphibians emerge onto sodden banks. Giant insects hover in the air. The vegetation is dominated by scaly-trunked lepidodendrons and enormous horsetails. The entire scene is primoeval, presenting us with the representatives of a generation of life long gone, whose like we shall never see again. But of course, not all of the Carboniferous world was given over to coal swamps. While the lepidodendrons and horsetails were indeed around, there were also the early representatives of more familiar plant lineages, though some of them may have been a bit difficult to recognise as such.

The Dicranophyllales may have been one such lineage. Though they survived for a long time, throughout the Carboniferous and Permian, and have been found in many parts of the world, they are generally uncommon in fossil deposits. In life, they would have been small trees or bushes, sparsely and irregularly branched (many reconstructions show them hardly branching at all). The branches bore long, needle-like leaves, not dissimilar to pine needles, in a helical arrangement. The longest of these leaves were over 20 cm in length. A single vein ran down the midline of the leaf, but because this was deeply imbedded it is often not visible in fossils. More prominent, and one of the characteristic features of the group, was a pair of deep grooves running the length of the leaf, one on each side close to the margin, containing the stomata (the openings through which planty leafs exchange gases with the surrounding atmosphere). The leaves were commonly branched towards the tips, at least once and sometimes more. The needle-like leaves, protected stomata, and uncommon preservation all suggest that the Dicranophyllales were mostly plants of drier environments (Wagner 2005). In many species, the leaves left a regular-shaped scar when they fell off, giving the trunk and branches an overall scaly appearance.

Reconstruction of a branch of Polyspermophyllum sergii, from Archangelsky & Cúneo (1990). Note the coiled fertile trusses at the ends of some leaves.

The majority of fossils of Dicranophyllales are of vegetative material (branches and leaves) only, and as a result they have mostly been assigned to the single genus Dicranophyllum, possessing the characters described above. Other genera of Dicranophyllales known from the Upper Permian of Russia include Mostotchkia, which differed in that the leaves were generally not branched, and Slivkovia, which had small scale-like leaves appressed to the branch surface in addition to the long needle-like leaves. Slivkovia and the Lower Permian Entsovia also differed from other Dicranophyllales in having a higher number of stomatiferous furrows on each leaf (Meyen & Smoller 1986). Reproductive structures are definitely recognised for only two species, the European Dicranophyllum gallicum, and Polyspermophyllum sergii from the early Permian of Argentina (Archangelsky & Cúneo 1990). Though Polyspermophyllum resembles Dicranophyllum vegetatively, it is distinct reproductively. In both species, the reproductive organs are broadly similar in appearance to the leaves, and occupy positions in the growth trajectory that would otherwise be occupied by leaves. Seeds are borne separately from each other on the female organs, which have been dubbed polysperms. In Dicranophyllum gallicum, the polysperms end in a bifurcation similar to that of a normal leaf, and the seeds are borne attached to the side. Unfortunately, the compressed fossils do not allow us to determine whether they were arranged helically or pinnately. The male organs were similar in organisation to the polysperms (Wagner 2005). In Polyspermophyllum, the polysperms are divided into multiple branches, and the seeds are borne in trusses at the ends of the branches.

Reconstruction of a section of Dicranophyllum gallicum bearing polysperms, from Seward (1919).

The affinities of the Dicranophyllales have been subject to debate. Some authors, such as Archangelsky & Cúneo (1990), have recognised two families in the Dicranophyllales: the Dicranophyllaceae containing all the taxa referred to above, and a second family including the Permian genus Trichopitys. Trichopitys is vegetatively similar to Dicranophyllales, but its leaves are arranged pinnately rather than helically, and its reproductive organs are borne axillary to the leaves rather than replacing the leaves in the growth sequence. As a result, other authors such as Meyen & Smoller (1986) have regarded the similarities between the two families as convergent. It has also been suggested that the Dicranophyllales might be early members of the lineage including the modern maidenhair tree Ginkgo biloba: under this model, the fan-shaped leaves of the ginkgo may be derived from branched leaves like those of Dicranophyllales by fusion of adjoining branches. However, Meyen & Smoller (1986) pointed out that the structure of Dicranophyllales leaves is less like those of a ginkgo that it is like those of early members of the conifer lineage. Some of the Cordaitanthales, a Palaeozoic group of plants related to the conifers, had furrows on their leaves similar to those found in Dicranophyllales. The leaves of Dicranophyllales also bear resemblances to those of early members of the conifers proper. And this is where the question of seed arrangement on the polysperms of Dicranophyllum becomes interesting: if they were helically arranged, then it becomes possible to the Dicranophyllum polysperm as a distant fore-runner of the modern pine cone.

REFERENCES

Archangelsky, S., & R. Cúneo. 1990. Polyspermophyllum, a new Permian gymnosperm from Argentina, with considerations about the Dicranophyllales. Review of Palaeobotany and Palynology 63: 117-135.

Meyen, S. V., & H. G. Smoller. 1986. The genus Mostotchkia Chachlov (Upper Palaeozoic of Angaraland) and its bearing on the characteristics of the order Dicranophyllales (Pinopsida). Review of Palaeobotany and Palynology 47: 205-223.

Seward, A. C. 1919. Fossil Plants: A text-book for students of botany and geology vol. 4. Ginkgoales, Coniferales, Gnetales. Cambridge University Press.

Wagner, R. H. 2005. Dicranophyllum glabrum (Dawson) Stopes, an unusual element of lower Westphalian floras in Atlantic Canada. Revista Española de Paleontología 20 (1): 7-13.

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.

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.

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.

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.

When Ferns Don't Look Like Ferns

I suspect that I would hardly need to explain to anyone what a fern looks like - their cool, green, graceful appearance makes them a favourite of holders of foliage fetishes everywhere. What you possibly may not be aware with is that the classic fern is actually only part of the story. Odds are that the parent of the fern you next see growing in a pot or in a damp grove looked nothing like that fern, and if you took the spores of that fern and grew them, you may not recognise the product. Welcome to the world of alternating generations.



Alternation of generations is actually something that all land plants indulge in. A diploid sporophyte asexually produces haploid spores that grow into haploid gametophytes whose haploid gametes fuse to form the zygotes that grows into new sporophytes, as shown in the diagram above by Jeffrey Finkelstein. In seed plants, the gametophyte has been severely reduced and does not grow outside its parent - the female gametophyte remains contained within the parent flower or cone as the ovule, while the male gametophyte is only a few cells in size and forms the pollen grain. In ferns, the gametophyte grows as a separate (albeit really small - perhaps only about a centimetre across) individual with an undifferentiated thallus. Each gametophyte produces both male and female gametes at different places on the thallus, and male gametes require a layer of moisture across the surface to swim across to the female gametes and fertilise them. Cross-fertilisation occurs when multiple gametophytes grow in close proximity and joined by a common covering of moisture. The sporophyte then grows directly out of the parent gametophyte.

In the majority of fern species, the gametophyte is a small heart-shaped structure like in the diagram above. The meristem, the growing part of the plant, is restricted to the recessed point of the heart. In three fern families, though, the gametophyte is ribbon-like or filamentous with multiple marginal meristems and grows indeterminately. While gametophytes of other fern families tend to be short-lived affairs, the gametophytes of Hymenophyllaceae, Vittariaceae and Grammitidaceae can be much longer-lived. Dassler and Farrar (1997) recorded an individual gametophyte of the Hymenophyllaceae species Callistopteris baueriana still growing seven years after germination. What is more, some inderminately-growing gametophytes are able to reproduce asexually as well as sexually through the production of gemmae, side-buds that can detach and grow into new individuals (anyone who has owned a hen-and-chickens fern or a mother-of-millions plants may have seen gemmae growing along the edge of their leaves). For a very few species, this capacity for sexual reproduction has allowed them to bypass the sporophyte phase of the life-cycle entirely.


The gametophyte-only fern species Vittaria appalachiana. Photo by Bob Klips.

Currently, independent gametophytes (i.e. those that are able to establish populations without forming sporophytes) are known from a single species of Grammitidaceae, two Vittariaceae and nine Hymenophyllaceae (Lindsay, 2003). Most of these species also produce sporophytes over part of the distribution, but the gametophytes are able to survive in areas that are seemingly not conducive to sporophyte production. Vittaria graminifolia, for instance, is known in Louisiana only as gametophytes, with the nearest sporophytes of the species over a thousand kilometres away in Mexico (Lindsay, 2003). As yet, only three species are known that seemingly never produce sporophytes - Vittaria appalachiana, Hymenophyllum tayloriae and Trichomanes intricatum (Raine et al., 1991; Farrar, 1992). Nevertheless, there are good reasons to suspect that the diversity of unrecognised independent gametophytes out there might be much higher. Fern gametophytes have been studied much less than sporophytes - not only are they small and difficult to find, but they have generally been regarded as decidedly low on taxonomically useful characters. Vittaria appalachiana, the first-known gametophyte-only species, was actually discovered sixty years before it was confirmed to be identifiably distinct from sporophyte-producing species of Vittaria. It does not escape notice that all three known gametophyte-only species come from the eastern United States, even though the families involved are found in tropical and subtropical habitats throughout the world. Things become particularly suspicious when you realise that a single person, Donald Farrar of Iowa State University, has been privy to the description of all three. More than likely, the apparent absence of gametophyte-only species from other parts of the world does not suggest that there is something unusual about the eastern United States, but simply that no-one has really looked anywhere else.

Like the relationship between asexually- and sexually-reproducing fungi, the taxonomic and ecological implications of the independent gametophyte may be significant. Rumsey et al. (1999) demonstrated that the Killarney fern (Trichomanes speciosum), previously regarded as extremely rare in the British Isles based on the distribution of the sporophyte, was actually fairly widespread and common as the gametophyte. The wide distribution of the eastern North American Trichomanes intricatum, including areas previously subject to glaciation and despite the apparent low dispersal potential of gametophytes reproducing by gemmae only, led Farrar (1992) to suggest that the "extinction" of the sporophyte form may have happened only recently. Has this species really forever lost the ability to produce sporophytes, or might a change of climate lead to the unfurling of a long-forgotten frond deep within the forests of New England?

REFERENCES

Dassler, C. L., & D. R. Farrar. 1997. Significance of form in fern gametophytes: Clonal, gemmiferous gametophytes of Callistopteris baueriana (Hymenophyllaceae). International Journal of Plant Sciences 158 (5): 622-639.

Farrar, D. R. 1992. Trichomanes intricatum: the independent Trichomanes gametophyte in the eastern United States. American Fern Journal 82 (2): 68-74.

Lindsay, S. 2003. Considerations for a revision of the fern family Vittariaceae for Flora Malesiana. Telopea 10 (1): 99-112.

Raine, C. A., D. R. Farrar & E. Sheffield. 1991. A new Hymenophyllum species in the Appalachians represented by independent gametophyte colonies. American Fern Journal 81 (4): 109-118.

Rumsey, F. J., J. C. Vogel, S. J. Russell, J. A. Barrett & M. Gibby. 1999. Population structure and conservation biology of the endangered fern Trichomanes speciosum Willd. (Hymenophyllaceae) at its northern distributional limit. Biological Journal of the Linnean Society 66 (3): 333-344.

The Origins of Flowers

Reconstruction of the bennettitalean Williamsonia, a potential stem-angiosperm. Image from Turbo Squid.

I'm going to break one of the supposed blogging rules - I'm going to feed a troll. In the comments thread to the bird evolution post I wrote recently, one commenter brought up the supposedly intractable evolutionary problem of the "sudden" appearance of flowering plants. I briefly responded to this comment at the time, but I thought the question is an interesting enough one to deserve further investigation. So here is my presentation on why the "sudden" appearance of flowers was not so sudden.

The origin of the angiosperms (flowering plants) has long been considered one of the great unsolved questions of biology, and I must confess to having occassionally slipped into the hyperbole myself. However, we actually have some much better ground to stand on than the hyperbole might suggest.

First off, we need to ask what exactly makes flowering plants so distinct? What do they have that no other plant has? I bet some of you are fighting the urge to reply with, "They have flowers. Duh." To which I have to reply - wrong! After all, you could debate to what extent the reproductive structures of many flowering plants can really be called 'flowers'. Many flowering plants lack the petals and/or sepals of more classic flowers. They may have bracts (coloured leaves) instead, like poinsettias or bougainvilleas, while many wind-pollinated angiosperms simply do without ornamentation entirely. And if we argue that petals are not necessary to count as a flower - if those plants that surround their reproductive structures with bracts also count as having flowers - then flowers are not actually unique to angiosperms (as I'll explain in a minute). No, the really significant feature of angiosperms is the carpel, the protective covering of two integuments that encloses the ovule of angiosperms. In other living seed plants, the gymnosperms, the ovules generally have only one integument and are produced exposed on the ends of short branches, often surrounded by a protective whorl of leaves or leaf-derived structures to form a structure called a strobilus (in many conifer groups, these protective leaves have become hard and woody to form the scales of a cone with an ovule at the base of each scale). Morphological and molecular phylogenetic analyses disagree significantly about the relationships between angiosperms and living gymnosperms (Friedman & Floyd, 2001). Morphological analyses place angiosperms nested within gymnosperms, forming a clade with the Gnetales, while molecular analyses place the angiosperms as sister to all living gymnosperms, not closely related to Gnetales.

While there is a significant divide between the carpel-enclosed ovules of angiosperms and the exposed ovules of gymnosperms in living taxa, this divide (unsurprisingly) actually dwindles when we consider fossil taxa. Debate still rages about which fossil taxa are the closest relatives of angiosperms, but two taxa that pop up on a regular basis are the Bennettitales and Caytonia. These taxa are often closely related to angiosperms and the Gnetales in morphological analyses (Doyle, 1998), while if morphological analyses are constrained to match the molecular trees the angiosperms form a clade with Bennettitales, Caytonia and glossopterids (Doyle, 2006). The Bennettitales and Caytonia both put in an appearance during the Triassic and survived until the end of the Cretaceous, while angiosperms are first known from the early Cretaceous (Doyle, 1998). Caytonia is generally described as a "seed fern", which were usually trees, but articulated fossils are fairly rare. It produced multiple single-integument ovules reflexed and contained within a protective structure called a cupule. It does not take a significant leap to imagine the reduction to a single ovule per cupule and the cupule developing into the outer integument of the angiosperm carpel.


(From Frohlich & Chase, 2007) Reproductive structures of fossil stem-angiosperm candidates. a, Glossopteris showing cupules borne on stalk above a leaf. b, Caytonia male (above) and female (below) reproductive units. c, Caytonia cupule. d, Corystosperm (Umkomasia) cupule containing one ovule. Cupule wall almost surrounds ovule, except for a slit facing the stalk. e, Bennettitales (Williamsoniella) bisexual reproductive unit; each oval pollen sac consists of several fused microsporangia. Ovules are borne among scales on the central stalk; in Vardekloftia each is enclosed by a cupule wall. Green, cupule wall; red, ovule; yellow, pollen organ.

Bennettitales were plants fairly similar in appearance to modern cycads that lacked any such carpel-like arrangement and had ovules born along scales in the strobilus. What Bennettitales did have, however, were flowers (of a sort). The leaves of the strobilus were expanded into flower-like bracts that were quite large (and possibly quite colourful) in a number of taxa. Certain features of the bennettitalean bracts suggest that they had a role in attracting insect pollinators, just as modern flowers do today (Gottsberger, 1988). The largest bennettitalean "flowers" were found in Cycadeoidea, which had the bracts recurved to enclose a central chamber containing the reproductive organs. This is of great significance because similar arrangements are found in modern beetle-pollinated flowers, which are believed to be among the more basal flower forms. Also significant is the presence in bennettitalean fossils of the chemical oleanane, derived from a secondary metabolite that is only produced by angiosperms among living taxa, further supporting their relationship (Taylor et al., 2006).

The earliest major pollinators of flowers were probably beetles and flies (Kevan & Baker, 1983). Beetles in particular are the major pollinators of members of basal angiosperm orders such as Magnoliales and Nymphaeales. The two insect groups most commonly associated with pollination in most peoples minds, butterflies and bees, were unlikely to have been significant players in the origin of flowers for the simple reason that neither had come into existence yet - Lepidoptera as a whole only started making an appearance during the Cretaceous, while bees were not to appear until the Tertiary. As already noted, many of the basal angiosperm groups show adaptations towards beetle pollination (this is why magnolias, for instance, produce such a powerful perfume and white flowers - nocturnal beetles use smell more in finding food, while white stands out more at night than colour would). Many beetle-pollinated flowers have some sort of enclosed chamber, or close during the day, providing their pollinators with a safe haven from predators as well as providing food in the form of nectar or pollen (it is quite alright if the pollinator eats some of the pollen so long as the flower produces far more than the pollinator can eat - indeed, if the pollinator is actually going for the pollen then it will almost certainly be rooting around in it and getting covered with it), and this may have been the approach Cyacadeoidea was going for. On the other hand, another basal angiosperm family, the Winteraceae, have open and unspecialised flowers that attract a wide range of pollinators such as beetles, moths, flies and thrips.


Arabidopsis with induced mutation causing leaves to be partially converted into petals. Photo from University of California, San Diego.

Insect-attracting strobili such as found in Bennettitales could have quite easily given rise to the first flowers. Developmental genetics has confirmed the theory put forward many years previously that petals and sepals represent modified leaves, and by affecting the expression of the genes involved it has proved possible to make leaves grow instead of petals, and petals grow instead of leaves (Goto et al., 2001). So while we have still not entirely solved what Darwin so overquotedly referred to as the "abominable mystery", the answer has drawn tantalisingly close.

REFERENCES

Doyle, J. A. 1998. Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. Molecular Phylogenetics and Evolution 9 (3): 448-462.

Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society 133 (1): 169-209.

Friedman, W. E., & S. K. Floyd. 2001. Perspective: The origin of flowering plants and their reproductive biology - a tale of two phylogenies. Evolution 55(2): 217-231.

Frohlich, M. W., & M. W. Chase. 2007. After a dozen years of progress the origin of angiosperms is still a great mystery. Nature 450: 1184-1189.

Goto, K., J. Kyozuka & J. L. Bowman. 2001. Turning floral organs into leaves, leaves into floral organs. Current Opinion in Genetics and Development 11 (4): 449-456.

Gottsberger, G. 1988. The reproductive biology of primitive angiosperms. Taxon 37 (3): 630-643.

Kevan, P. G., & H. G. Baker. 1983. Insects as flower visitors and pollinators. Annual Review of Entomology 28: 407-453.

Taylor, D. W., H. Li, J. Dahl, F. J. Fago, D. Zinniker & J. M. Moldowan. 2003. Biogeochemical evidence for the presence of the angiosperm molecular fossil oleanane in Paleozoic and Mesozoic non-angiospermous fossils. Paleobiology 32: 179-190.

Of Serpentine Soils

Cape Reinga projects from the north-western end of the Aopouri Peninsula at the very top end of New Zealand. A lone lighthouse stands at the summit of the cape (image at left from Wikimedia), and a venerable pohutukawa tree hanging over the cliffs is pointed out as the very tree from which, in Maori tradition, the spirits of the dead clambered down to the ocean on their way back to Hawaiiki, the mysterious land that was the ancestral point of origin of the Maori to which they returned after their death*. Cape Reinga is a popular tourist spot as the northernmost point in New Zealand. It isn't. If you look carefully at the map at the top of this post (from the Far North District Council), you'll note that at the north-eastern corner of the country, there's a rounded prominence sticking further north. This is the North Cape, and that rounded prominence is the Surville Cliffs.

*There is an unfortunate tendency to refer to 'Maori tradition' as a single unit, when prior to European settlement the different Maori tribes each had their own collection of traditions, agreeing in some points and differing in others. While the concept of a return to Hawaiiki was, I believe, universal among Maori, I haven't been able to find out if this tradition was associated particularly with Cape Reinga for all Maori, or if tribes in other parts of the country identified their own departure points. Apparently more than one Christian missionary, including the memorable William Colenso, tried to have the Cape Reinga pohutukawa chopped down, but these attempts were always rebuffed by local Maori.

So why aren't the tourists all headed for the true northern tip of the country? The Surville Cliffs are part of a conservation reserve (the North Cape Scientific Reserve) that remains closed to the general public. The local Department of Conservation attempts to ruthlessly exclude and/or eradicate introduced taxa from the area, and the primary focus of this protection is a small area of about 120 hectares on the Surville Cliffs and the adjacent plateau that is home to a whole range of plant species found nowhere else on the planet, including Hebe brevifolia (Cheeseman) de Lange 1997, Carex ophiolitica de Lange & Heenan 1997 and Uncinia perplexa Heenan & de Lange, 2001.

Pittosporum serpentinum, an endangered species endemic to the Surville Cliffs area. Seedlings of this species have never yet been observed (photo by Gillian Crowcroft, from New Zealand Plant Conservation Network).

The range of plant species growing in any location is strongly dependent on the soil type. The effect of a change in soil type can be dramatic - sometimes you can practically see a line where one soil abruptly gives way to another. In the case of the Surville Cliffs, the presence of a distinct soil type not found elsewhere in New Zealand is to blame for the unique flora.

The soil at the Surville is serpentine, derived from the exposure of the Tangihua or Northland Ophiolite. Ophiolite forms when part of the sea-floor crust becomes uplifted and integrated into the continental crust. Major ophiolite belts are found in the Alps and the Himalayas where pieces of the oceanic floor between two colliding continental masses have been ripped up and wedged between the fusing continents. In the case of the Tangihua Ophiolite, the rocks that eventually became the ophiolite probably formed in the South Fiji Basin to the north-east of New Zealand (Whattam et al., 2004). They would have then become emplaced onto the New Zealand continental mass with the formation of a subduction zone along the north-east of New Zealand, probably due to the collision of the underwater Hikurangi Plateau with the New Zealand continental shelf further south.



Sketch map showing the disposition of tectonic elements adjacent to Northland. A, Immediately prior to the emplacement of the Northland Ophiolite. B, Immediately after emplacement and as subduction began. SFB, South Fiji Basin; VMFZ, Vening Meinesz Fracture Zone; HP, Hikurangi Plateau. From Whattam et al., 2004.

Ophiolite is very ultramafic rock, meaning it is high in heavy metals such as nickel, iron and magnesium. Soils formed from such rocks are toxic to the majority of plants, which is why they become the preserve of ultramafic specialists. In contrast, most ultramafic specialists do not do well when grown away from their toxic homes (de Lange, 1997; Heenan & de Lange, 2001), which is why the Surville Cliffs flora is so restricted in distribution. The greatest threat to the Surville Cliffs flora is probably invasion by introduced taxa such as Hakea and Cortaderia (pampas grass), though eradication programmes are currently underway to try and reduce the risk from these invaders. Some members of the Surville Cliffs fauna, such as Hebe brevifolia, are present in large numbers and are probably not under immediate threat despite their highly restricted distribution. Others, such as Uncinia perplexa, appear to have always existed in very low numbers, and are seriously endangered.

REFERENCES

de Lange, P. J. 1997. Hebe brevifolia (Scrophulariaceae) - an ultramafic endemic of the Surville Cliffs, North Cape, New Zealand. New Zealand Journal of Botany 35: 1-8.

de Lange, P. J., & P. B. Heenan. 1997. Carex ophiolithica (Cyperaceae): a new ultramafic endemic from the Surville Cliffs, North Cape, New Zealand. New Zealand Journal of Botany 35: 429-436.

Heenan, P. B., & P. J. de Lange. 2001. A new, dodecaploid species of Uncinia (Cyperaceae) from ultramafic rocks, Surville Cliffs, Northland, New Zealand. New Zealand Journal of Botany 39: 373-380.

Whattam, S. A., J. G. Malpas, J. R. Ali, I. E. M. Smith & C.-H. Lo. 2004. Origin of the Northland Ophiolite, northern New Zealand: discussion of new data and reassessment of the model. New Zealand Journal of Geology and Geophysics 47: 383-389.