Oily and Salty Trees

The Annonaceae is another one of those plant families like Acanthaceae that, despite containing a high diversity of speceis, tend to be overlooked because that diversity is mostly tropical. A number of species in the type genus Annona produce commercially significant fruits: custard apples, cherimoyas, soursops and the like. However, these are just a few of the 2400+ species of trees and lianes assigned to this family.

Ylang-ylang flowers Cananga odorata, from here.

Taxonomically, the Annonaceae is well established as distinct, readily recognised by a number of distinctive features. Among these is a characteristic 'cobweb' appearance to the wood structure when seen in cross-section, resulting from prominent rays of xylem connected by narrow cross-bands of parenchyma (Chatrou et al. 2012). Relationships within the family have been much harder to work out, not becoming well established until the advent of the molecular era. Recently, Chatrou et al. (2012) have recognised four subfamilies within the Annonaceae. The majority of species are placed in the subfamilies Annonoideae and Malmeoideae (which together form a clade), but a handful of species are placed in two basal subfamilies: one for the single genus Anaxagorea, and the Ambavioideae. Anaxagorea and the ambavioids differ from the annonoid-malmeoid clade in the structure of their seeds. Seeds of Annonaceae have what is called ruminate endosperm: that is, the surface of the endosperm is not smooth, but divided by wrinkles and grooves (the term 'ruminate' literally means 'chewed'). In Annonoideae and Malmeoideae, the ruminations of the endosperm are shaped like spines or lamellae. In Anaxagorea and the Ambavioideae, the ruminations are irregular in appearance. Molecular analyses place Anaxagorea as the sister taxon to all other Annonaceae.

View into the canopy of a salt-and-oil tree Cleistopholis patens, copyright Marco Schmidt.>

The Ambavioideae, despite not being very diverse, are widespread, with species found in the tropics of Africa, Asia and the Americas. Perhaps the best known ambavioid is the ylang-ylang tree Cananga odorata, native to south-east Asia, whose flowers are used as a source of perfume. Other south-east Asian ambavioids belong to the genera Cyathocalyx, Drepananthus and Mezzettia. The type genus, Ambavia, is native to Madagascar; other ambavioids in the genera Meiocarpidium, Cleistopholis and Lettowianthus are found in continental Africa. Finally, a single genus Tetrameranthus is found in South America. Most species of ambavioid are not systematically economically exploited but a number are locally used as sources of wood. The wood is light and not suitable for structural uses, but can be shaped and finished for utensils and other small items. The West African species Cleistopholis patens, whose Ghanaian name has been translated as 'salt and oil tree' (in reference to the taste of the bark when chewed), provides a fibrous bark that is readily stripped from the tree and is used for such purposes as matting and carrying straps (see here).

REFERENCES

Chatrou, L W., M. D. Pirie, R. H. J. Erkens, T. L. P. Couvreur, K. M. Neubig, J. R. Abbott, J. B. Mols, J. W. Maas, R. M. K. Saunders & M. W. Chase. 2012. A new subfamilial and tribal classification of the pantropical flowering plant family Annonaceae informed by molecular phylogenetics. Botanical Journal of the Linnean Society 169: 5–40.

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.

Dighloti

Just a brief one today. The above picture, from Assam Plants.com, shows leaves of the dighloti, Litsea salicifolia, a tree of the laurel family Lauraceae found in sparse valley forests of southern Asia from India to Vietnam (Li et al. 2008). Litsea salicifolia is fairly variable in appearance, but general characters include long elliptic, alternate, leathery and evergreen leaves, glabrous branchlets and petioles, 4-6-flowered umbels and small oblong fruit.

Dighloti is cultivated in Assam, with two main uses. It is supposed to be a mosquito repellent, and this has been corroborated by laboratory studies (Phukan & Kalita 2005). It is also used as a secondary food source for the muga silkworm Antheraea assamensis (Bindroo et al. 2006). Muga silk, one of the so-called 'wild silks' produced from caterpillars other than the domesticated silkworm Bombyx mori, is raised primarily on two other Lauraceae species, the som Persea bombycina and the soalu Litsea polyantha. However, dighloti bushes are also grown in som plantations as a supplementary food for young or under-developed silkworms. Muga silk has a naturally golden-brown coloration (photo below from here).

REFERENCES

Bindroo, B. B., N. T. Singh, A. K. Sahu & R. Chakravorty. 2006. Muga silkworm host plants. Indian Silk, April 2006: 13-17.

Li X., Li J., Huang P., Wei F., Cui H. & H. van der Werff. 2008. Lauraceae. In: Flora of China Editorial Committee (eds) Flora of China vol. 7. Menispermaceae through Capparaceae. Science Press: Beijing, and Missouri Botanical Garden Press: St. Louis.

Phukan, S., & M. C. Kalita. 2005. Phytopesticidal and repellent efficacy of Litsea salicifolia (Lauraceae) against Aedes aegypti and Culex quinquefasciatus. Indian Journal of Experimental Biology 43: 472-474.

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.

Reference Review: The Monocot Tree

Dracaena draco, from Flora Canaria

Davis, J. I., D. W. Stevenson, G. Petersen, O. Seberg, L. M. Campbell, J. V. Freudenstein, D. H. Goldman, C. R. Hardy, F. A. Michelangeli, M. P. Simmons, C. D. Specht, F. Vergara-Silva & M. Gandolfo. 2004. A phylogeny of the monocots, as inferred from rbcL and atpA sequence variation, and a comparison of methods for calculating jackknife and bootstrap values. Systematic Botany 29 (3): 467-510.

Abstract: "A phylogenetic analysis of the monocots was conducted on the basis of nucleotide sequence variation in two genes (atpA, encoded in the mitochondrial genome, and rbcL, encoded in the plastid genome). The taxon sample of 218 angiosperm terminals included 177 monocots and 41 dicots. Among the major results of the analysis are the resolution of a clade comprising four magnoliid lineages (Canellales, Piperales, Magnoliales, and Laurales) as sister of the monocots, with the deepest branch within the monocots between a clade consisting of Araceae, Tofieldiaceae, Acorus, and Alismatales, and a clade that includes all other monocots. Nartheciaceae are placed as the sister of Pandanales, and Corsiaceae as the sister of Liliales. The Triuridaceae, represented by three genera, including Lacandonia, are resolved as monophyletic and placed in a range of positions, generally within Pandanales. Dasypogonaceae and Arecaceae diverge sequentially from a clade that includes all other commelinid taxa, and within the latter group Poales s. lat. are sister of a clade in which Zingiberales and Commelinales are sisters. Within Poales s. lat., Trithuria (Hydatellaceae) and Mayaca appear to be closely related to some or all elements of Xyridaceae. A comparison was conducted of jackknife and bootstrap values, as computed using strict-consensus (SC) and frequency-within-replicates (FWR) approaches. Jackknife values tend to be higher than bootstrap values, and for each of these methods support values obtained with the FWR approach tend to exceed those obtained with the SC approach."

A pleasing degree of consensus has developed in recent years in regards to many higher-level relationships among angiosperms (though one can't help wondering how much of this consensus is related to the fact that higher-level plant systematics has become an almost entirely molecular affair, and what would happen were a few sophisticated morphological datasets thrown into the mix. Anywho...) While relationships within the basal "magnoliids" are still a bit iffy, we have become reasonably certain about what are the major clades or grades within the flowering plants.

Many of you will have learnt in school about the differences between dicotyledons and monocotyledons, the supposed two major divisions of flowering plants, and I am sure that most basic biology textbooks still use this division. Technically, this is wrong. The characters that are ascribed to dicotyledons (two seed leaves, netted veins, stem with central xylem and external phloem, etc.) are actually the ancestral characters for flowering plants, and the dicots are paraphyletic with regard to the monocots (though a well-supported clade, the eudicots, does include all the traditional dicots except for the "magnoliids"). At least two "dicot" groups, the Nymphaeales and Aristolochiaceae, have some characters that are more traditionally associated with monocots.

The monocots, on the other hand, are a well-supported clade, both molecularly and morphologically. The Cronquist system of angiosperm classification recognised five subclasses within the monocots, the Alismatidae (aquatic and semi-aquatic forms), Arecidae (palms [Arecales], screw pines [Pandanales] and aroids [Arales]), Liliidae (lily-type plants), Commelinidae (grasses, rushes and allies) and Zingiberidae (gingers and bromeliads). Of these, the Arecidae and Zingiberidae are both currently regarded as polyphyletic, though Cronquist's "zingiberids" are all included in the commelinids*. It is the other three that I'll mainly be referring to here.

*Though the current Angiosperm Phylogeny Group classifications do still recognise higher clades based on the older subclasses, they prefer to use informal names such as "commelinid" or "rosid" rather than recognising them as formal subclasses such as Commelinidae or Rosidae.


Davis et al. (2004) came up with results for their analyses of monocot phylogeny that were fairly similar to what had and has been found elsewhere - basal alismatids (including Arales), then the liliids (including Pandanales) as a grade, then the monophyletic commelinids (including Arecales). Interestingly, Davis et al. in their combined analysis found alismatids as monophyletic - most other analyses have found them to be paraphyletic, with Acorus as the sister group to all other monocots, then a clade of most alismatids. Acorus (shown above in a photo from here) is a Holarctic semi-aquatic plant previously included in the Arales. When Davis et al. ran their analysis using rbcL data only, Acorus returned to its position outside the remaining monocots.



One other result of Davis et al. that definitely caught my eye is that Trithuria (Hydatellaceae) appears snugly nestled within the commelinids (albeit via a long-string of poorly-supported branches). One of the most interesting developments in plant systematics of the past year has been the publication of Saarela et al. (2007), which convincingly showed that the Hydatellaceae, a group of incredibly insignificant aquatic plants previously regarded as monocots (the picture above from Science Daily shows well how minute they are), are in fact part of the ANITA grade at the base of the angiosperms, sister to the Nymphaeales (waterlilies). While Saarela et al. didn't include as many taxa in their analysis as Davis et al., they did use considerably more loci (23 as opposed to only two) and showed that the relationship was also supported (albeit weakly) by morphological data, so I'm inlined to believe Saarela et al. over the earlier analysis. The really big question, then, is how did Davis et al. manage to get Hydatellaceae so deep within the monocots in the first place? What drew the previously used rbcL sequences towards the monocots? Were the sequences even Hydatellaceae at all, or had some sort of mix-up occurred? Regrettably, Saarela et al. gave no suggestions for how the previous analyses could have been so wrong**, and I'm completely stumped.

**Perhaps yet another case of the constrictions of the Nature format dooming us to a far-too-brief article. Humph.

The two papers also differ on the sister group of monocots. Davis et al. joined the monocots to the "core magnoliid" group, while Saarela et al. favoured the eudicots + Ceratophyllum***. While bootstrap support was better for Saarela et al., in neither case was it that great, so the question remains up in the air.

***Ceratophyllum is yet another unassuming aquatic taxon that seemingly exists only to give plant systematists splitting headaches****. For a while it seemed a strong contender for the position of basalmost living flowering plant, but was eventually booted from this position of power by the ANITA group. Since then, it has exacted its revenge for such a rude demotion by refusing to sit in the same place twice between analyses.

****If you're wondering what exactly is so evil about aquatic plants, their shift from a terrestrial to an aquatic habitat is generally associated with an accelerated evolutionary rate, giving them significant long branches. They also tend to develop simplified morphologies relative to their terrestrial relatives.

One thing I find particularly interesting about the state of monocot phylogenetics is the basal position of alismatids, especially if Acorus renders them paraphyletic (if you were wondering, Saarela et al. recovered the Acorus-as-basalmost-monocot topology). This makes me wonder whether monocots as a whole are derived from a semi-aquatic ancestor, which would make the "liliid" + commelinid clade secondarily terrestrial. Could this partially explain how monocots developed their highly derived morphology relative to other angiosperms? Interestingly, the aquatic Nymphaeales + Hydatellaceae clade, though indicated by molecular data to be quite distant from the monocots, shares a number of convergent features with monocots such as loss of the cambium.

One final point of interest about Davis et al. (2004) is their comparison of bootstrap supports calculated using different algorithms. While the differences were not huge, they were certainly there. For me, this definitely came in the "I did not know that" category, and will certainly have to be something I keep in mind in the future.

REFERENCES

Saarela, J. M., H. S. Rai, J. A. Doyle, P. K. Endress, S. Mathews, A. D. Marchant, B. G. Briggs & S. W. Graham. 2007. Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446: 312-315.

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.

Taxon of the Week: Spices of Gondwana

The Canellales are a small order of flowering trees and shrubs, most of which are found in the southern continents though some species reach as far north as Florida and Indonesia. Two families are included in Canellales, the Canellaceae and Winteraceae. Canellaceae is found in the Ethiopian and Neotropical biozones, while Winteraceae is Australasian, Malesian and Neotropical (the image at left is of Drimys winteri [Winteraceae], and comes from Flora Chilena).

Canellales are members of the "magnoliids" - the paraphyletic assemblage of basal flowering plants that aren't eudicotyledons, aren't monocotyledons, and are still proving difficult to place phylogenetically. Recent analyses have all agreed that the so-called "ANITA grade" includes the basalmost flowering plants yet in existence (the name ANITA derives from the taxa included in this group: Amborella-Nymphaeales-Illiciaceae-Trimeniaceae-Austrobaileya). After that, it all goes a bit custard-shaped. As well as the well-established clades of eudicots and monocots, we have Chloranthaceae, Magnoliales, Laurales, Piperales, Aristolochiales, Canellales and Ceratophyllum (some authors, such as Thorne [2000], have included some or all of these orders in an expanded Magnoliales), with almost every combination imaginable of these nine clades turning up somewhere. Nevertheless, there is a reasonable amount of molecular support for a true "magnoliid" clade including everything listed above from Magnoliales to Canellales, with Canellales probably sister to Piperales (including Aristolochiales - Zanis et al., 2002; Angiosperm Phylogeny Group, 2003). Though an association between Canellaceae and Winteraceae was first recognised on molecular grounds only, morphological characters have since been identified in support of the Canellales.


Flowers of Drimys winteri - image from Plant of the Week

Previously, Winteraceae had been regarded as very primitive flowering plants because of their lack of vessels, specialised xylem cells for the transport of water that are characteristic of flowering plants (xylem is the central part of the plant stem that transports most of the plants water through no-longer-living cells). In vessels, the axial ends of the deceased xylem cells has become perforated or open, so instead of separate cells the plant has continuous tubes allowing for much easier water transport. The only other angiosperms to lack vessels are Amborella (possibly the basalmost of all living flowering plants) and the small eudicot order Trochodendrales.

However, the modern position for Winteraceae implies that its vessel-less condition is not primitive but derived from vesselled ancestors. What could have led the ancestors of the Winteraceae to abandon the seeming advantages of a vessel system? Field et al. (2002) compared the effectiveness of water transport in the vessel-less Winteraceae and the vessel-bearing Canellaceae. While Canellaceae had much more efficient water transport than Winteraceae, freezing and thawing had a much greater impact on water transport in Canellaceae than Winteraceae, leading Field et al. to suggest that the lack of vessels in Winteraceae might have been an adaptation to survive freezing cycles in temperate Gondwana. This seems to be the most likely explanation yet available, but as always with science, a whole host of other questions arise - if vessels are so problematic for cold-climate taxa, why have so few other angiosperms lost them? Field et al. do suggest that greater differences between vessels and standard xylem cells in more derived taxa may have put greater constraints on their loss, but I feel this is still very much an open question.

One feature that Canellaceae and Winteraceae share in common is the notable production of aromatic oils by members of both families. Canella alba (shown here in an illustration from Wikipedia) was transported from South America to Europe as "white cinnamon", and its bark is used in much the same way as cinnamon. The leaves of horopito (Pseudowintera colorata), a small tree found in New Zealand, were used as a condiment, as are those of Tasmanian pepper (Tasmannia lanceolata). I can personally vouch for the edibility of horopito - it has a strong peppery taste, similar to nasturtium but far stronger.

REFERENCES

Angiosperm Phylogeny Group. 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141: 399-436.

Field, T. S., T. Brodribb & N. M. Holbrook. 2002. Hardly a relict: freezing and the evolution of vesselless wood in Winteraceae. Evolution 56 (3): 464-478.

Thorne, R. F. 2000. The classification and geography of the flowering plants: Dicotyledons of the class Angiospermae (subclasses Magnoliidae, Ranunculidae, Caryophyllidae, Dilleniidae, Rosidae, Asteridae and Lamiidae). Botanical Review 66: 441-647.

Zanis, M., D. E. Soltis, P. S. Soltis, S. Mathews & M. J. Donoghue. 2002. The root of the angiosperms revisited. Proceedings of the National Academy of Sciences of the USA 99: 6848-6853.