Malpighiales: A Glorious Mess of Flowering Plants

Ixonanthes reticulata, from here.

There is no denying that the advent of molecular analysis revolutionised the world of plant phylogeny. Previously an uncertain landscape of shifting sands, beset by the eroding forces of convergent evolution and morphological plasticity, the higher relationships of flowering plants have begun to resolve into a much clearer view than before. But some of the revealed vistas have been unexpected, and have led to quagmires of their own.

The Malpighiales are one clade that has become generally recognised as a result of molecular analyses, but remain almost impossible to characterise morphologically. Part of that difficulty is a consequence of sheer diversity: the clade includes about 16,000 species worldwide. The bulk of these species are tropical; it has been estimated that 40% of the world's tropical rain-forest understory is composed of Malpighiales (Xi et al. 2012). Only a relative minority of Malpighiales are found in more temperate parts of the world, though that minority still includes such familiar plants as violets, willows and spurges. The ranks of Malpighiales include some of the most bizarrely modified of all flowering plants: the endoparasitic Rafflesiaceae and the aquatic Podostemaceae.

Fruit of the jellyfish tree Medusagyne oppositifolia, photographed by Christopher Kaiser-Bunbury. The jellyfish tree is restricted to the Seychelles and critically endangered; the few surviving trees occupy marginal habitat where seedling germination seemingly cannot occur.

Though molecular analyses have been fairly consistent in supporting the Malpighiales as a whole, relationships within the Malpighiales long proved more recalcitrant. As a result, its species have been placed in up to 42 different families, these families varying wildly in diversity. At one end of the scale, the Euphorbiaceae has been home to over 5700 species, even in its modern restricted sense (earlier botanists recognised a Euphorbiaceae that was considerably larger). At the other end, the Malesian vine Lophopyxis maingayi and the jellyfish tree Medusagyne oppositifolia of the Seychelles have each been considered distinctive enough and of uncertain enough affinities to be placed in their own monotypic families. Many of these families could only be placed within the Malpighiales as part of a great polytomy, an unresolved mess of relationships at the base of the clade.

Herbarium specimen of Centroplacus glaucinus, from here. This species has a restricted range in West Africa; its closest relatives belong to the genus Bhesa in south-east Asia.

A major advance in our understanding of malpighialean phylogeny was made just recently by Xi et al. (2012), who were able to obtain a more resolved phylogenetic tree than previous studies through the use of data from a large number of genes (they also ignored the Rafflesiaceae; those guys just cause trouble). Their results suggested a division of the Malpighiales between three basal clades. The smallest of these includes relatives of the families Malpighiaceae and Chrysobalanaceae. Few members of this clade are familiar outside the tropics. Some are known for their edible fruit, such as the coco plum Chrysobalanus icaco, the nance Byrsonima crassifolia, the Barbados cherry Malpighia emarginata and the butter-nut Caryocar nuciferum. In contrast, the southern African gifblaar Dichapetalum cymosum contains toxic sodium monofluoroacetate and is regarded as a serious threat to livestock.

Small individual of the mangrove Kandelia candel, photographed by Dans.

The next clade includes families relatied to the Clusiaceae, Ochnaceae and Erythroxylaceae. The latter family is closely related to (and sometimes synonymised with) the Rhizophoraceae, a small but significant family that dominates among the tropical mangroves. The Erythroxylaceae is itself most notorious for including the coca plant Erythroxylum coca, the source of the drug cocaine*. The clusioid families include the Clusiaceae, Hypericaceae and Calophyllaceae, treated in older sources as a single family Guttiferae but currently treated as separate families owing to the paraphyly of such a grouping to the families Bonnetiaceae and Podostemaceae. The name 'Guttiferae' refers to the production of resin by many clusioids. In some species, these resins are produced in the flowers in lieu of nectar and are collected for nest-building by visiting bees. Economically significant clusioids include the mangosteen Garcinia mangostana and the St John's wort Hypericum perforatum, which has been grown commercially in some parts of the world for its supposed medicinal properties but is regarded in other parts of the world as a highly undesirable weed.

*Not raisins.

Flower of Rhizanthes infanticida, a smaller relative of Rafflesia, growing from host roots on the forest floor in Thailand, from here. Further buds are visible as reddish balls closer to the tree.

The third clade, and the largest by a considerable margin, includes such families as the Euphorbiaceae, Violaceae and Salicaceae. Noteworthy examples of this clade also include the passion fruit Passiflora edulis, and the flax plant Linum usitatissimum. The Euphorbiaceae, as alluded to above, were previously considered to include taxa more recently treated as the separate families Putranjivaceae, Phyllanthaceae, Picodendraceae and Peraceae. The Putranjivaceae were placed by Xi et al. (2012) in the Malpighiaceae-Chrysobalanaceae clade, and so are not close relatives of the Euphorbiaceae sensu stricto. The remaining families are closer, but modern authors would prefer to keep them separate as the demands of monophyly would then require the Euphorbiaceae be further enlarged to include the Linaceae and Rafflesiaceae. Nobody wants a Rafflesia in their family.

REFERENCE

Xi, Z., B. R. Ruhfel, H. Schaefer, A. M. Amorim, M. Sugumarane, K. J. Wurdack, P. K. Endress, M. L. Matthews, P. F. Stevens, S. Mathews & C. C. Davis. 2012. Phylogenomics and a posteriori data partitioning resolve the Cretaceous angiosperm radiation Malpighiales. Proceedings of the National Academy of Science of the USA 109 (43): 17519-17524.

Of New Zoos and Old Libraries

In May 2009, a small fossil mammal was announced to the world as Darwinius masillae. Despite looking (let's be honest) like some sort of road-killed rat, Darwinius attracted a lot of interest due to its being a well-preserved early primate. Around the globe, news reports, blog posts, and strongly-worded letters to the Times were composed on the subject of wee Darwinius. You can get some idea of this attention from the links provided here. But with a publicity machine as large as the one surrounding Darwinius, one should always expect there to be spanners nearby.

As reported at The Loom, it was soon pointed out that there were problems with the name 'Darwinius massilae'. Darwinius had been published in an online-only venue, the web-journal PLoS One. At the time, the International Code of Zoological Nomenclature still did not allow for online-only publications, and a lively debate was going on as to whether provisions for such things should be made (eventually, they were). It looked like the name 'Darwinius' might have to suffer the fate of Akhenaten, erased from the public record and forbidden to be spoken aloud. In the end, a paper edition of the description of Darwinius was deposited in a number of institute libraries, which was believe to satisfy the letter of the ICZN. Peace was restored to the empire, and Darwinius was confirmed as an acceptable name.

For many who had been clinging to the fence on the acceptability of online-only publication, Darwinius massilae represented a bit of a water-shed moment. Online-only publication was here, it was happening, and it couldn't be ignored. Resistance was rapidly becoming futile. Or at least, that was the conclusion I personally felt compelled to draw from the event. The problem wasn't just the sideshow that had arisen around the christening of Darwinius. For me, the real poster-child for this mess was Aerosteon riocoloradensis, a theropod dinosaur that PLoS One had announced some eight months earlier than Darwinius. Like Darwinius, Aerosteon was subject to a fair whack of media coverage, despite the fact that, like Darwinius, its name wasn't acceptable in the eyes of the ICZN. The difference between Darwinius and Aerosteon, though, was that until the problem with Darwinius was realised, no-one had even noticed any issue with Aerosteon.

This, for me, was the very heart of the problem. In the days before electronic documents, the question of whether a given work was 'published' was largely an academic one. For most printed works, the evidence that it was 'published' was simply that it existed. Works that were regarded as 'unpublished', such as hand-written manuscripts and doctoral theses, probably only existed as one or two copies. The chance of your seeing them, except as an archivist, was fairly minute. Online publication changed all that. By the time it was realised that the name 'Aerosteon' might not be valid, its original description had been viewed by hundreds, if not thousands, of people (at the time of writing, PLoS One claims 22,417 views for this paper). The idea that all these readers should be commanded never to speak of what they saw, because they had not seen it in the required medium, seemed frankly ludicrous.

In this light, the amendment of the ICZN to allow for online-only publication (under certain conditions) was something I welcomed. As I noted at the time, it was possible (certain, in fact) that the rules would have to be further manipulated as we saw how they worked out in practice. Recently, a review in Zootaxa by Dubois et al. has purported to look at some of the issues that have arisen as a result of electronic publication. This review has itself received a brief, but snarky, commentary in the editorial section of this week's Nature. The Nature reviewer accuses Dubois et al. of having 'axes to grind'. This is probably true, but the reviewer may be sharpening an axe of their own: among the practices castigated by Dubois et al. are some, such as the publication of important taxonomic information in 'online supplements', that Nature has often been guilty of itself.

That said, I can't help but feel sympathy for the Nature reviewer's comments. I have become increasingly disenchanted over the years with any nomenclatural argument that strays too far towards the purely legalistic. For instance, Dubois et al. argue that the validation of Darwinius by the deposition in libraries of paper copies was itself invalid under current rules, as these prohibit validation through the production of 'facsimiles or reproductions as paper-printed copies of unavailable electronic publications' of the original online publication. They were also invalid under the rules current at the time, which required that a published work 'must be obtainable, when first issued'. Because the paper issues were only deposited in libraries, and were not obtainable by anyone from that first print-run, they didn't count. If PLoS One offered to print out a copy for anyone who demanded a paper issue, that didn't count either because the rules exclude 'print-on-demand' documents. If PLoS One pointed out that the paper was freely available at any time simply by going to their website and downloading a copy, that didn't count because electronic documents were not acceptable! In the meantime, their supposed 'unavailability' has been no barrier to use: Google Scholar returns 56 results on a search for 'Aerosteon', and 258 results on a search for 'Darwinius'! Dubois et al. complain that nomenclature doesn't get no respect, and call stridently for higher standards, stating positions such as that, "Publishers who since 2000 have published works containing nomenclatural novelties that do not comply with the Rules of the Code for publication availability...have betrayed the confidence of the authors who had entrusted their works to them for publication". I would counter that it is exactly this sort of legalistic bun-fighting and contrarianism that has caused many researchers (including many taxonomists) to lose respect for the nomenclatural process in the first place. We are not and we should not be here for the purpose of chanting shibboleths!

Dubois et al. complain that, "the recent decision [of the ICZN] to allow the publication of nomenclatural novelties in electronic form, was strongly influenced, if not “imposed”, by pressure from both the international biological community of non-taxonomists, and of non-scientists, e.g. Internet and Google “candid users”. Well, yes, this is exactly the point that I was making above. The users of taxonomy are not just taxonomists. They are researchers in other fields, they are policy-makers, they are farmers, they are fishermen, in fact they are absolutely everyone who has any interest, whether professional or amateur, in the world's biodiversity. The needs of these end-users cannot be simply ignored. And first and foremost among those needs is the need to not have to spend inordinate amounts of time contemplating nomenclatural angels on the heads of systematic pins before they know whether a name is usable. In the past we could be reasonably confident that if we were reading a publication, it was available. That is the ideal that we should be striving towards again.

The Elaenia Elaenias

Yellow-bellied elaenia Elaenia flavogaster, photographed by Félix Uribe.

We are all aware that there are some truly stunning birds out there: majestic eagles and vultures, vibrant parrots and hummingbirds, eye-catching cranes and pelicans. But those of us who spend a lot of time contemplating the nature of bird diversity, whether as bird-watchers or ornithologists, will soon admit that the greater proportion of this diversity is composed of what are affectionately or not-so-affectionately referred to as Little Brown Jobs. In particular, the tyrant flycatchers or Tyrannidae of the Americas are one family of birds that is notorious for including some of the littlest, the brownest, and the jobbiest.

Elaenia is a genus of about twenty or so species of tyrannid found in Central and South America (Sibley & Monroe, 1990, listed eighteen, but phylogenetic studies suggest that some of these should be divided into more than one species—Rheindt et al. 2009). The name 'elaenia' does double service for these guys as both genus and vernacular name, though the members of some related genera are also labelled in the vernacular as 'elaenias'. As a result, Ridgely & Tudor (2009), without a trace of apparent irony, referred to the species of this genus as 'Elaenia elaenias'.

Mottled-backed elaenia Elaenia gigas, showing its distinctive divided crest, photographed by Nick Athanas.

The various species of Elaenia elaenias are notoriously difficult to distinguish, and none are particularly eye-catching. They are mostly greenish, though the slaty elaenia Elaenia strepera is dark grey, and the brownish elaenia E. pelzelni is (surprisingly) brown. Underparts may be white, or they may be yellow. One species in particular is labelled as the yellow-bellied elaenia E. flavogaster, but in this case it is not any more strikingly yellow than a number of other species, leading one to suspect whether its vernacular name is any sort of moral judgement. A number of species have some degree of white streak on the crown, and some have a small crest of feathers (the mottle-backed elaenia E. gigas has a well-developed, bifurcated crest). Elaenias are best distinguished by their calls, but that of course requires the bird in question to be calling.

Great elaenia Elaenia dayi, photographed by Thiago Orsi.

Though members of the tyrant flycatcher family in both affinities and appearance, elaenias consume a fair proportion of fruit as well as insects. In at least some species, fruit make up by far the greater part of the diet (Marini & Cavalcanti 1998). Different species often have different preferred habitats, and the relationship between habitat and phylogeny was examined by Rheindt et al. (2008). Two savannah-dwelling species, the plain-crested elaenia Elaenia cristata and the rufous-crowned elaenia E. ruficeps, appear to be the sister clade to the remaining species that mostly inhabit riparian habitats or montane and temperate forests (Elaenia species are largely absent from lowland tropical forest). The forest species fall into two clades nested among the riparian species. The great elaenia E. dayi, which happens to be the largest Elaenia species by a noticeable margin, inhabits the stunted montane forests of the south Venezuelan tepuis (if you've seen the film Up, this is the habitat in which that film is mostly set). Migratory habits, on the other hand, are less correlated with phylogeny than habitat preferences. A number of Elaenia species migrate between temperate breeding grounds and tropical wintering grounds, but migratory species may be closely related to sedentary species that inhabit the tropics all year round. Indeed, some species are mostly sedentary but have somewhat migratory populations in more temperate parts of their range.

REFERENCES

Marini, M. Â., & R. B. Cavalcanti. 1998. Frugivory by Elaenia flycatchers. Hornero 15: 47-50.

Rheindt, F. E., L. Christidis & J. A. Norman. 2008. Habitat shifts in the evolutionary history of a Neotropical flycatcher lineage from forest and open landscapes. BMC Evolutionary Biology 8: 1193.

Rheindt, F. E., L. Christidis & J. A. Norman. 2009. Genetic introgression, incomplete lineage sorting and faulty taxonomy create multiple cases of polyphyly in a montane clade of tyrant-flycatchers (Elaenia, Tyrannidae). Zoologica Scripta 38: 143-153.

Ridgely, R. S., & G. Tudor. 2009. Field Guide to the Songbirds of South America: The Passerines. University of Texas Press.

Sibley, C. G., & B. L. Monroe Jr. 1990. Distribution and Taxonomy of Birds of the World. Yale University Press.

Dream-fish, Coelacanths and Super-Predators: The Sarcopterygians

For the subject of today's post, I drew the Sarcopterygii, the 'lobe-finned fishes'. Though something of a poor relation to their considerably more diverse sister-group, the ray-finned fishes of the Actinopterygii, this is a group most of my readers will have probably encountered in some capacity. As their names both formal and vernacular indicate, the Sarcopterygii were originally characterised by the development of the fins as fleshy lobes, with at least some fins possessing an internal skeleton of serial bones. Living sarcopterygians belong to three major groups, the coelacanths, lungfishes and tetrapods (in which, of course, the ancestral fins have been modified into walking limbs). The majority of recent studies have placed the coelacanths as the most divergent of these groups, with lungfishes and tetrapods as sister taxa. As the tetrapods are a particularly tedious group of organisms, with little to interest the casual observer, I'll put them aside for this post (you can go to Tetrapod Zoology if you must). The lungfishes, too, warrant a more detailed look at another time.

The oldest known sarcopterygian (and, indeed, the oldest known crown-group bony fish) is the Guiyu oneiros (shown above in a reconstruction by Brian Choo for Zhu et al. 2009), whose species name suggests the vernacular name of 'dream fish'. The dream-fish is known from the late Silurian of China, with a number of other stem-sarcopterygians such as Psarolepis and Meemannia known from the early Devonian of the same region. These taxa retained a number of ancestral features such as heavy ganoid scales (a type of scale also found in basal actinopterygians), and strong spines in front of the fins. However, crown-group sarcopterygians had also evolved and diverged by the early Devonian, as shown by the presence of the stem-lungfish Youngolepis.

Congregation of West Indian Ocean coelacanths Latimeria chalumnae, photographed by Hans Fricke.

The coelacanths are, of course, best known to most people for the discovery of the living Latimeria chalumnae in 1938 in South Africa, after the lineage had been thought to have become extinct in the Cretaceous. The subsequent media frenzy must have been interesting to fishermen in the area who had long known the coelacanth primarily as an infernal nuisance. Though only captured occasionally as bycatch, a landed coelacanth represents two metres or more of snap-jawed bad temper, while the oily flesh is inedible. More recently, a second species of living coelacanth, Latimeria menadoensis has been described from near Sulawesi in Indonesia.

Because of the circumstances of its discovery, Latimeria became a textbook example of a 'living fossil'. However, all fossil coelacanths were not mere duplicates of Latimeria. To begin with, Latimeria is quite a bit larger than the majority of its fossil relatives (Casane & Laurenti 2013). These included such distinctive forms as the fork-tailed speedster Rebellatrix and the eel-like Holopterygius. And then there was Allenypterus montanus, a Carboniferous taxon that... well, just look at the thing (photo from here):

Though Latimeria may lord it over its immediate relatives, it is far from the largest sarcopterygian (even excluding the tetrapods). The tetrapod stem-group also included a number of large predators, including the famous Eusthenopteron (how many other fossil fish have been referred to by name in an episode of Doraemon?). Particularly dramatic were the Rhizodontida, freshwater ambush predators of the Devonian and Carboniferous. Though probably very low on the tetrapod stem (and hence not directly related to limbed tetrapods), rhizodontids developed enlarged pectoral fins that articulated with the body in a not dissimilar manner to tetrapod forelegs. Like tetrapods, rhizodontids probably used their pectoral fins to push against the substrate and provide explosive propulsion (Davis et al. 2004). The jaw of rhizodontids contained enlarged tusks interspersed among smaller teeth that would have hooked into struggling prey. The largest rhizodontids have been estimated to be about seven metres in length, and were the sort of predator that the term 'apex' was invented for.

Reconstruction of Rhizodus by Mike Coates.

REFERENCES

Casane, D., & P. Laurenti. 2013. Why coelacanths are not 'living fossils'. BioEssays 35: 332-338.

Davis, M. C., N. Shubin & E. B. Daeschler. 2004. A new specimen of Sauripterus taylori (Sarcopterygii, Osteichthyes) from the Famennian Catskill Formation of North America. Journal of Vertebrate Paleontology 24 (1): 26-40.

Zhu, M., W. Zhao, L. Jia, J. Lu, T. Qiao & Q. Qu. 2009. The oldest articulated osteichthyan reveals mosaic gnathostome characters. Nature 458: 469-474.

The Perils of Lamellorthoceras in the Land of Taphonomy

Exfoliated specimen of Lamellorthoceras gracile, from Sweet (1964). The outer shell has been lost.

The title of today's post, offhand, is a hideously contrived allusion to something that I suspect many (most?) of you will not recognise. Those of you that do recognise it, possibly wish that you didn't. Nevertheless, I'll leave it to each of you to decide for yourself whether or not this post would have been improved by the inclusion of kabuki-inspired haute couture, or chariots pulled by topless busty Amazons in lieu of horses.

Lamellorthoceras, to introduce the star of today's post, is a genus of straight-shelled cephalopods from the Lower and Middle Devonian of northern Africa. It was not a large cephalopod. Like most straight-shelled Palaeozoic cephalopods, fossils of Lamellorthoceras represent pieces of the original shell rather than the entire thing (making judging its size when alive a bit tricky), but even with a generous estimate I don't think we're talking about anything more than a few centimetres long. Lamellorthoceras forms the core of a small, mostly Devonian family, the Lamellorthoceratidae, distinguished by a very interesting feature. Like other cephalopods, the shell of lamellorthoceratids was divided into a series of chambers, with a fleshy siphuncle presumably running the length of the shell. In most other cephalopods, the chambers around the siphuncle were more or less hollow, filled with gas to give the shell buoyancy. In fossils of lamellorthoceratids, however, the chambers are filled with thin lamellae arranged in a radial pattern between the shell and the siphuncle. This is so unusual compared to other cephalopods that the lamellorthoceratid Arthrophyllum was initially described as a type of coral! Genera of lamellorthoceratids have been distinguished based on the overall shape of the shell, and by the structure of the lamellae. Arthrophyllum, for instance, has simple straight lamellae in transverse section, while the lamellae of Lamellorthoceras are wavy and/or bifurcating.

Cross-section of Lamellorthoceras vermiculare, from Sweet (1964), showing the radiating lamellae.

In a previous post on this site, I discussed some of the implications of such structures, called cameral deposits, for the soft anatomy of fossil cephalopods. If we were to assume that all fossil cephalopods had much the same anatomy as our only real living model, the pearly nautiluses of the Nautilidae, then cameral deposits present us with a real problem. In Nautilus, the siphuncle is sealed away from each chamber by a structure called the connecting ring, and the walls of the chambers are devoid of living tissue. The siphuncle serves to control the buoyancy of the shell by controlling the ratio of fluid to gas in the chambers, but this fluid is only secreted or absorbed via pores in the connecting rings. The only part of the nautilus shell where mineral deposits are being actively laid down is in the anterior body chamber where the living animal is housed. For fossil cephalopods to have been laying down mineral deposits within the chambers behind the body chamber, there would have had to have been outgrowths of the mantle still present in the chambers. The siphuncle could not have been an isolated unit the way it is in Nautilus. Unfortunately, the connecting rings of nautilids are delicate structures that do not preserve easily as fossils, so seeing whether they were present in lamellorthoceratids is not as simple as just looking for them. Nevertheless, Kolebaba (1999) claimed after close examination of the Upper Silurian Nucleoceras that the connecting rings of lamellorthoceratids were at least open dorsally.

However, some researchers (e.g. Mutvei 2002) hold a quite different interpretation of what the cameral deposits meant for the living animal: absolutely nothing. Perhaps they were not a feature of the living cephalopod at all, but represent sediment build-up in empty shells after the animal's death. This would have interesting implications for the lamellorthoceratids, if their primary claim to fame was a taphonomic illusion! Evidence for the inorganic origin of the cameral deposits cited by Mutvei (2002) include their different chemical make-up from the main shell, often more similar to the surrounding matrix, and specimens preserved flattened in shales with no sign of cameral deposits. However, cameral deposits are not laid down haphazardly within a shell as one might expect if they were post-mortem artefacts, but more or less consistently between specimens. Deposits growing out from opposing chamber walls and septa do not merge seemlessly, but remain separated by breaks in the deposits ('pseudosepta') that may represent tissue membranes. Flattened shale specimens may indicate an original absence of cameral deposits, or they may represent preferential dissolution of the cameral deposits under those preservation conditions. It is also possible that cameral deposits present during life may have provided nuclei for further sediment deposition after death.

Reconstruction of a sectioned chamber of the lamellorthoceratid Esopoceras sinuosum, showing the internal arrangement of lamellae, from Stanley & Teichert (1976). Esopoceras had more strongly sinuous lamellae than Lamellorthoceras.

Needless to say, our views on the presence in life of cameral deposits could also have strong implications for our understanding of these animal's lifestyles. If the intra-cameral lamellae of Lamellorthoceras were present in life, the shell would have held little, if any, space for buoyant gas. As such, it probably would not have had the swimming abilities of modern cephalopods; instead, it may have had a more benthic lifestyle.

REFERENCES

Kolebaba, I. 1999. Sipho-cameral structures in some silurian cephalopods from the Barrandian area (Bohemia). Acta Musei Nationalis Pragae, Series B, Historia Naturalis 55 (1-2): 1-16.

Mutvei, H. 2002. Connecting ring structure and its significance for classification of the orthoceratid cephalopods. Acta Palaeontologica Polonica 47 (1): 157–168.

Stanley, G. D., Jr & C. Teichert. 1976. Lamellorthoceratids (Cephalopoda, Orthoceratoidea) from the Lower Devonian of New York. The University of Kansas Paleontological Contributions 86: 1-14, 2 pls.

Sweet, W. C. 1964. Nautiloidea – Orthocerida. In Treatise on Invertebrate Paleontology pt. K. Mollusca 3. Cephalopoda – General Features – Endoceratoidea – Actinoceratoidea – Nautiloidea – Bactritoidea (R. C. Moore, ed.) pp. K216-K261. The Geological Society of America and the University of Kansas Press.